Becker · Petrić · Zgomba

Norbert Becker
Dušan Petrić
Marija Zgomba
Clive Boase
Minoo Madon
1 Christine Dahl
and Achim Kaiser
Mosquitoes

Mosquitoes
and Their Control
Second Edition

dition 123
Mosquitoes and Their Control
Norbert Becker
Dušan Petrić · Marija Zgomba
Clive Boase · Christine Dahl
Minoo Madon · Achim Kaiser

Mosquitoes
and Their Control

Second Edition
Norbert Becker Dušan Petrić
German Mosquito Control University of Novi Sad
Association (KABS) Department for Phytomedicine
Ludwigstr. 99 and Environment Protection
67165 Waldsee Trg Dositeja Obradovica 8
Germany 21000 Novi Sad
[email protected] Serbia
[email protected] [email protected]

Marija Zgomba Clive Boase

University of Novi Sad The Pest Management
Department for Phytomedicine Consultancy
and Environment Protection Cowslip Pightle, Hazel Stub
Trg Dositeja Obradovica 8 Haverhill, Suffolk
21000 Novi Sad CB9 9AF
Serbia United Kingdom
[email protected] [email protected]

Minoo Madon Christine Dahl

430 Mavis Drive Thomandeers väg 2b
Los Angeles, California 90065-5054 224 65 Lund
USA Sweden
[email protected] [email protected]

Achim Kaiser
German Mosquito Control
Association (KABS)
Ludwigstr. 99
67165 Waldsee
Germany
[email protected]

ISBN 978-3-540-92873-7 e-ISBN 978-3-540-92874-4

DOI 10.1007/978-3-540-92874-4
Springer Heidelberg Dordrecht London New York

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Foreword to the Second Edition

The magnitude of the role played by mosquitoes in the scheme of human life is
undisputed. It is some 100 years since mosquitoes came to be recognised and incrim-
inated as playing a highly significant part in the affairs of humans. Mankind has been
plagued by mosquito nuisance and mosquito-borne diseases since the dawn of human
history, resulting in immeasurable suffering and economic losses. Mosquitoes trans-
mit some of the deadliest diseases known to man, such as malaria, yellow fever,
dengue, encephalitis, filariasis, and a hundred or so other infections, claiming many
millions of lives. Despite much research, and decades of mosquito control work around
the world, mosquitoes remain a major global public health problem. In many develop-
ing countries, the eradication of classic mosquito-borne diseases still seems a long way
off in the future. Some developed countries have experienced the introduction and
establishment of exotic mosquito species, and of mosquito-borne diseases formerly
unknown in these regions. Increased global travel has contributed to the current trends
in re-emerging mosquito-borne infectious diseases, exemplified by increasing num-
bers of imported malaria cases, and recent outbreaks of West Nile and Chikungunya
fever have given rise to growing public concern. Seasonal outbreaks of nuisance mos-
quito populations, which plague ecologically sensitive tourist and urban areas, cause
significant economic damage and constitute major problems globally.
The second edition of “Mosquitoes and Their Control” has been thoroughly
updated since the first edition was published in 2003. This has been achieved through
a review of the very extensive and rapidly-growing global literature on mosquitoes.
The objective of this revised and expanded text is to provide a broad and balanced
description of the biology of mosquitoes, their significance as disease vectors, and the
techniques available for their management. The authors present this in a clear, con-
cise, readable fashion throughout with a variety of specially prepared line illustra-
tions and photographs. As a result, this book is appropriate for students, scientists,
mosquito professionals and the lay reader alike. The text provides a summary of this
important group of insects, of which over 3500 species have been recorded world-
wide, across five continents. Significant sections have been added on mosquito-borne
diseases, such as malaria, arboviruses, and filariases, and their vectors worldwide.
Among others, the most important Sub-Saharan malaria vectors are discussed in
detail, including seven species of the Anopheles Gambiae Complex.
The content is conveniently divided into separate sections and chapters on specific
topics. The book opens with sections on systematics, morphology, and the biology of
mosquitoes, followed by an extensive review of their medical significance. The chap-
ter on mosquito research reviews a wide range of practical techniques that are used
by those involved in mosquito research and surveillance, in both the laboratory and

v
vi Foreword to the Second Edition

the field. Additional sections contain keys to the identification of larval and adult
mosquito genera and species present in Europe, and genera and species of important
vector/nuisance female mosquitoes in Africa, Asia, Australia, and the Americas.
This is followed by a detailed and instructive account of the morphology, ecology,
and distribution of all the discussed species belonging to 13 genera including:
Anopheles, Aedes, Armigeres, Haemagogus, Ochlerotatus, Psorophora, Verrallina,
Culex, Culiseta, Coquillettidia, Mansonia, Orthopodomyia, and Uranotaenia.
Accurate species identification is central to any successful mosquito control or mos-
quito-borne disease surveillance programme.
The final section is dedicated to the control of mosquitoes, and covers biological,
chemical, and physical techniques, as well as genetic control, environmental manage-
ment and personal protection. The section on biological control contains important
information on mosquito predators, parasites, and pathogens and is of special signifi-
cance in the light of the increasing interest in finding alternatives to conventional
pesticides. The section on mosquito control concludes with a review of integrated
mosquito management, showing how these various approaches may be used collec-
tively to improve effectiveness, while ensuring the safety of humans and the
environment.
The authors’ very extensive knowledge and experience in their respective topics,
together with the information so generously contributed by others working in this
field, have been combined to produce this comprehensive and unique treatise.
This text book will serve as a valuable resource for vector ecologists, medical ento-
mologists, and professionals involved in the biology, ecology, systematics and the con-
trol of mosquitoes world-wide. We hope that the primary beneficiaries will be the
students, scientists, and professionals dealing on a day-to-day basis with mosquitoes
and their control. However, society as a whole stands to gain enormously from more
effective and environmentally responsible mosquito management programmes designed
on the basis of a more comprehensive understanding of mosquitoes and the issues
around their control, as presented in this enlightening book.

Yoel Margalith, Ph.D.

Tyler Prize Laureate
Center for Biological Control
Ben-Gurion University of the Negev, Israel
Foreword to the First Edition

Mankind has been plagued by mosquitoes as nuisances and as vectors of mosquito-

borne diseases for centuries, resulting in inestimable economic losses and indeter-
minable human suffering. Mosquitoes transmit some of the deadliest diseases
known to man malaria and yellow fever—as well as dengue, encephalitis, filariasis
and a hundred or so other maladies. In spite of decades of mosquito control efforts
throughout affected regions worldwide, this scourge has not left us and our present-
day overpopulated, jet-linked world remains on the edge of resurgence and out-
breaks of old and new mosquito-borne disease epidemics.
Ninety-two mosquito species of more than 3200 recorded worldwide, traverse the
European continent. In Europe malaria was eradicated ca. 50 years ago. Current trends
in re-emerging mosquito-borne infectious diseases, exemplified by increasing numbers
of imported malaria cases and recent outbreaks of West Nile fever (WNF) virus, how-
ever, have given rise to growing public concern. Seasonal outbreaks of nuisance mos-
quito populations, which plague ecologically sensitive tourist and urban areas cause
significant economic damage and constitute the major problem in Europe.
This book is the product of a monumental task of collecting, processing and
organising vital information on the mosquito populations of Europe. It presents a
multitude of information on the bionomics, systematics, ecology and control of
both pestiferous (nuisance) and disease vectors in an easily readable style provid-
ing practical guidance and important information to both professional and layman
alike. It is conveniently divided into four parts containing sixteen chapters. Part one
deals with general information on systematics, morphology and biology of mosqui-
toes, their medical significance and a very useful subchapter on mosquito research
that includes important techniques and technologies utilised in mosquito surveys
for sampling eggs, larvae and adult mosquito populations. Part two contains keys to
identification of larval and adult mosquito genera. Part three gives a very detailed
and instructive account of the morphology, ecology and distribution of all 92
European species included in eight genera: Anopheles, Aedes, Ochlerotatus, Culex,
Culiseta, Coquillettidia, Orthopodomyia and Uranotaenia. This part is extremely
important for species identification in any successful mosquito control or mosquito-
borne disease surveillance programme.
Part four dealing with control of mosquitoes is well ordered in seven sections:
biological, chemical and physical control as well as personal protection, integrated
pest management, implementation of survey methodologies and management. This
information is particularly necessary for a comprehensive approach to both study-
ing and controlling mosquitoes. This part distinctly demonstrates the tremendous
experience that the authors possess over decades in mosquito biology and control.

vii
viii Foreword to the First Edition

The section on biological control contains important information on predators,

parasites and pathogens is of special significance in light of the increasing inter-
est in replacing detrimental chemical pesticides with environ­mentally friendly inte-
grated biological control technologies.
The authors of this book collectively possess a vast amount of knowledge and
experience in the relevant topics and they have meticulously gathered and incorpo-
rated the experience and knowledge of others to compose the first and only compre-
hensive treatise on the subject of European mosquitoes.
This book is a valuable tool for vector ecologists, entomologists, and all those
involved with mosquito control, biology, ecology and systematics in Europe. It’s
primary beneficiaries will be the students, scientists and professionals dealing on a
day-to-day basis with mosquitoes and their control. Society as a whole stands to
gain from improved, environmentally responsible mosquito management pro-
grammes designed on the basis of the broader understanding of mosquitoes and
their control provided in this enlightening book.

Yoel Margalith, Ph.D

Tyler Prize Laureate
Center for Biological Control
Ben Gurion University of the Negev, Israel
Preface to the Second Edition

The first edition of this book (Becker et al. 2003) included comprehensive and glob-
ally relevant chapters on Mosquito Systematics, Biology, Morphology, Medical
Importance, Research Techniques, and Control. However, the identification keys
and descriptions were limited to European mosquito species. Nonetheless, the
reviews (Olejniček and Gelbič 2004) and the rapid sale of the first edition, indicated
that the book was widely appreciated and accepted by both scientists and
professionals.
Having had time to reflect on the first edition, the authors realised the need for a
second edition and agreed that the scope required widening to include an overview of
selected important vector and nuisance mosquito species world-wide. This 2nd edition
is intended to be useful not only to readers in Europe, but to readers around the
world.
The additional list of mosquito species we chose to include, was compiled using
our own knowledge and experience, and that of our colleagues in various regions,
and of course utilising the very extensive literature.
Despite the natural division of the mosquito fauna of the world into zoo-geograph-
ical regions, in our work we have adopted a continental approach. This allows us to
present a simpler overview of the current situation, and to provide an understanding
of the global distribution of important nuisance and disease vector mosquitoes, irre-
spective of the science of zoo-geography.
Given that the tribe Aedini is the largest and most polyphyletic group of mosqui-
toes, we therefore agree with the work of Reinert (2000c) and Reinert et al. (2004,
2006, 2008), in revising it and establishing monophyletic genera. We believe that
progress should be made towards establishing genera as “monophyletic” or natural
groups of species; that is to say groups including an ancestor and all of its
descendants.
However, several groups of mosquito taxonomists and editors of major profes-
sional journals have not accepted the latest nomenclature proposed by Reinert et al.
(2004, 2006, 2008), and have even returned Ochlerotatus (Reinert 2000c) to the sub-
generic rank after several years of extensive usage.
As a compromise, the placement of genera within the tribe Aedini in this edition,
is based on “traditional” generic and sub-generic affiliations recognised prior to and
including the separation of Aedes and Ochlerotatus by Reinert (2000c). In this text,
the “latest” placement of genera proposed by Reinert et al. (2004, 2006, 2008) is
indicated in square brackets following the “traditional” generic names. Those who
would prefer to follow the nomenclature before Reinert (2000c) can treat the name

ix
x Preface to the Second Edition

Ochlerotatus as equivalent to Aedes. Finally, for those species whose status did not
change after Reinert (2000c), we have not provided additional information.
We have restructured and broadened chapters such as “Mosquito Research
Techniques” and “Medical Importance”, to make this text more useful to our col-
leagues working outside Europe.
In general, we sincerely hope that we have produced a text that will be useful and
interesting to entomologists in general, and particularly to professionals in public
health battling the scourges of mosquito nuisance and mosquito-borne diseases.

The authors
Preface to First Edition

Throughout the world, mosquitoes interact with man in many different ways. However,
despite the very extensive research on these interactions, there remains much that has
not yet been fully understood. The attempt by the authors of this volume is to highlight
the importance of a basic knowledge of mosquito biology as a basis for successful con-
trol operations.
Compared to Curculionidae, the largest family in the animal kingdom, with 35,000
known species, Culicidae, numbering more than 3,200 species, could be ranked as a
family of only a small-to-moderate size. Even though yield losses caused by weevils
could be estimated in billions of dollars, mosquitoes are able to carry many lethal
diseases in their bodies. By the time you have read this Preface (5 min), ten human
lives would have been lost because of plasmodian infections. Apart from being the
well-known vectors of life-threatening diseases, in some parts of the world, mosqui-
toes may also occur in enormous numbers thus causing a significant reduction in
human life quality and serious economic damage, for instance, in livestock.
Ramsdale and Snow (1999) published a list of currently recognised European
mosquito taxa with synonyms. They included 98 species in 7 genera and 17 subgen-
era. The authors of this volume, in deciding upon the species that should be covered,
have come to the conclusion that the pertinent species are those that were recorded on
more than one occasion at least, where type specimens have been deposited, identifi-
cation material has been available and where the position regarding the validity of the
species is satisfactory. In addition to these requirements, information about the geo-
graphical distribution with substantiating references was considered. According to
this, 92 species and subspecies belonging to 8 genera and 18 subgenera are described
and included in the keys.
The following species or subspecies previously reported in Europe are not included in
the list: Oc. gilcolladoi (Villa, Rodrigez and Llera 1985) [Dahliana gilcolladoi] was named
after a form from central Spain differing in certain features of larval chaetotaxy from both
Oc. echinus and Oc. geniculatus. The position regarding the validity of this species is
unsatisfactory. Type specimens were not deposited, and material is not available for exami-
nation (Ramsdale and Snow, 1999). Oc. thibaulti (Dyar and Knab, 1909) is a Nearctic
species in Europe, recorded from the river Dnieper, Ukraine (Gutsevitch and Goritskaya,
1970), but no longer found there according to Gutsevitch and Dubitsky (1987). Oc. atro-
palpus (Coquillett, 1902) is not considered here because it was reported only once from
Italy and it is not considered as a permanent species in the European area.
For the species Oc. krymmontanus Alekseev 1989, Oc. coluzzii Rioux, Guilvard
and Pasteur 1998, Oc. duplex Martini 1926 and Cx. deserticola, short notes are given
in the description of the species.

xi
xii Preface to First Edition

The principal objective of the taxonomy and morphology chapters is to provide an

identification key to both adult females and males as well as to fourth instar larvae,
which incorporate all the 92 species. At the beginning of Chaps. 6–8, keys for the
identification of genera are given. Recently, Reinert (2000c) divided the composite
genus Aedes Meigen into two genera, Ochlerotatus Lynch Arribalzaga and Aedes.
Adults of these genera are distinguished primarily on the basis of genitalic characters
that require dissection. For this reason, the species belonging to these genera are
treated in a single key. The illustrated keys are followed by a detailed description of
the morphology, biology and distribution of each species. The morphological terms
engaged in this volume are somewhat changed from those used by Harbach and
Knight (1980, 1981), taking into consideration homology, phylogeny and their gen-
eral use among the dipterous insects.
When a specimen has been keyed out, it should be compared with the description
of that species to use the additional information as a cross-check. The description of
the species is given according to the examination of the Peus collection, as well as a
considerable number of species sampled in different European regions and various
literature sources.
Characters of fourth instar larvae are often clearer than those of the adults, and
many taxonomists prefer to identify mosquitoes in this stage. Since there is a certain
degree of variation among the larvae of a species, it is best to identify, if possible,
from a series of specimens. Rare exceptions to key characters can almost always be
found. More important variations and their relative frequency are indicated in the
systematic section of the species.
In the keys, the larval chaetotaxy of the thorax and abdomen is not used to such an
extent as by other authors. This seems to be a little bit “old fashioned”, but on the other
hand, quite often setae may be broken off, lying in a misleading or barely visible posi-
tion in slide preparations or in the worst case, are totally missing. If the latter occurs,
an experienced eye is needed to see the alveola or tubercle of the missing seta.
Although eggs, early instar larvae and pupae of most European species are known,
they are more difficult to identify than adults and fourth instar larvae. Rearing eggs to
fourth instar larvae and pupae to adults is easier and less time consuming than to
identify them in the early stages.
The authors suggest that the user should study the sections on general morphology
before starting to identify specimens. The user should also be familiar with the proper
sampling and mounting techniques of adults and larvae, because the presence of a full
set of scales, setae and other features is essential for identification. Updated mosquito
distribution throughout Europe, together with the bioecological conditions to be met
for each species, should also help in the species identification. The territory of Europe,
despite not being a distinct zoogeographical region, is chosen in an attempt to provide
for the first time a unique key for the whole European region.
The authors’ intention is to encourage and give support to every person who
intends to start, or already has some experience in, mosquito control. The concept of
the book is also based on several fields of knowledge that are important for everyone
who deals with mosquitoes. Overviews on mosquito taxonomy, morphology, biology,
biological and chemical control measures are given, to complete the information
needed for a comprehensive approach to both studying and controlling mosquitoes.
Mosquito control measures are dependent on many complex and interacting fac-
tors ranging from biological (species-dependent), abiotic and physical factors influ-
encing the phenology and abundance of mosquitoes (terrain features, climate, types
Preface to First Edition xiii

of breeding sites etc.) to administrative, organisational and most certainly economical

conditions. A decision to use one or another mosquito control measure is highly
dependent on a basic knowledge of all aspects of the target species, and the impact of
a chosen control method on the target and non-target organisms, as well as on the
environment. A professional control programme should combine cost effectiveness,
acceptable level of mosquito population suppression, and an environmentally sensi-
tive approach. In some situations, it is possible to rely on inexpensive and simple
methods such as applying fragments of copper wire into flower pots for the control of
Ae. albopictus larvae (Bellini, pers. comm.), while in others only pure biological,
highly selective control measures are allowed, such as in the Upper Rhine Valley,
where almost the entire mosquito control programme in the river floodplains has
relied solely on B. thuringiensis israelensis larviciding for several decades. Sections
on different approaches in mosquito control (chemical, biological, integrated or per-
sonal protection) provide basic information about different methods of using pro­
ducts with different formulation and toxicological features, effectiveness on target
species and their impact on non-target organisms. Information from this part of the
volume attempts to serve as a basis for an appropriate mosquito control operation,
allowing the user to live in relative security from some vector-borne diseases, to alle-
viate the effects of abundant nuisance populations, to re-establish wetlands and to
share and enjoy nature by conserving the biodiversity, by using environmentally
friendly control tools.
Up to now, a comprehensive book in which the taxonomy, biology and dispersal of
all currently known European mosquito species are described, as well as the options for
their control, has been missing. This volume should fill the gap and be a valuable help
to scientists and indeed all those interested in, or working in any of the fields related to,
Culicidae. It should provide guidance to field workers concerned with mosquito control
and those who wish, for example, to learn more about the behaviour of the species in
their region, about mosquito breeding sites, or about the mosquito control techniques
and options that may be suitable for each specific environment. Since there is still much
information that for some, despite greatly increased access to the Internet, may be dif-
ficult to acquire, we have tried to include and summarise all the available information,
so that entomologists can apply it to their own situations.

The authors
Acknowledgments

We are most indebted to Paul Schädler, President of the German Mosquito Control
Association (KABS, Waldsee, Germany) and the members of the KABS-Scientific
board, Volker Storch (University of Heidelberg, Germany), Herbert W. Ludwig†
(University of Heidelberg), Wolfgang Schnetter† (University of Heidelberg), Hartwig
Rihm (Mayor of Au), Gisbert Dieter† (Mayor A.D. of Lampertheim, Germany), Paul
Glaser (GFS, Germany), Herrmann Magin† (GFS, Germany), and Hans Wirnshofer
(Mayor A.D. Ketsch, Germany, Administrative Director of KABS), for their support
in all aspects of mosquito control in Germany and in preparing this text.
We are grateful for the substantial help in the preparation of the manuscript to
Thin Thin Oo (KABS, Germany), Richard Russell (University of Sydney, Australia),
Major Dhillon (Northwest MVCD, Corona, USA), Mir Mulla (University of
California, Riverside, USA), Ute Timmermann (KABS, Germany), Andreas Arnold
(KABS, Germany), Klaus Hoffmann (KABS, Germany), Thomas Weitzel (KABS,
Germany), Christian Weisser (KABS, Germany), Antje Lohmann (KABS, Germany),
Ernst-Jan Scholte (National Institute for Public Health and the Environment, Centre
for Infectious Disease Control, Bilthoven, The Netherlands), Thania Guaycurus
(Oswaldo Cruz Institute, Rio de Janeiro, Brazil), and Wanderli Tadei (INPA, Manaus,
Brazil).
During the preparation of the manuscript, authors received valuable information
provided by our colleagues and friends worldwide. We thank the following contribu-
tors, who supplied a variety of important and useful information: Carlos Aranda
(Consell Comarcal del Baix Llobregat, Spain), Romeo Bellini (Centro Agricoltura
Ambiente, Italy), Roger Eritja (SCM, Consell Comarcal del Baix Llobregat, Spain),
Raul Escosa (CODE, Ebro Delta, Spain), Remi Foussadier (E.I.D., Rhone-Alpes,
France), Jose Carlos Galvez (SCM, Huelva County Council, Spain), Aleksandra
Gliniewicz (National Institute of Hygiene, Poland), Raymond Gruffaz (E.I.D., Rhone-
Alpes, France), Karch Said (SIIAP Paris, France), Bart Knols (K&S Consulting,
Netherlands), Beata Kubica-Biernat (University of Gdynia, Poland), Christophe
Lagneau (E.I.D. Mediterranee, France), Peter Lüthy (University of Zürich,
Switzerland), Jan Lundström (University of Uppsala, Sweden), Eduard Marques i
Mora (SCM, Roses Bay and Lower Ter, Spain), Jean-Pierre Mas (E.I.D. Atlantique,
France), Elzbieta Lonc (University of Wroclaw, Poland), Enrih Merdic (University of
Osijek, Croatia), Spiros Mourelatos (Environment, Public Health and Ecodevelopment,
Greece), Odile Moussiegt (E.I.D. Mediterranee, France), Francoise Pfirsch (Mosquito
Control Organization, Bas-Rhin, France), Dirk Reichle (KABS, Germany), Frantisek
Rettich (National Institute of Public Health, Czech Republic), Katarzyna Rydzanicz
(University of Wroclaw, Poland), Martina Schäfer (University of Uppsala, Sweden),

xv
xvi Acknowledgments

Francis Schaffner (ETH, Zürich, Switzerland), and Asghar Talbalaghi (Alessandria

Abatement District, Italy).
The authors express appreciation for the skillful and diligent preparation of the
illustrations to Miguel Neri (University of San Carlos, Cebu, Philippines), Michael
Gottwald (University of Heidelberg, Germany), Tara Petrić (Novi Sad, Serbia), Vlada
Vojnić-Hajduk (Novi Sad, Serbia), and Kyaw Kyaw (Ludwigshafen, Germany).
We are grateful to numerous individuals and organizations who assisted in various
ways toward the final form of this book, especially to Matthias Beck (KABS, Germany),
Geoffrey L. Brown (Heidelberg, Germany), Djamal Chakhmaliev (Heidelberg,
Germany), Jeff Charles (Institute Pasteur, Paris, France), Culinex GmbH (Ludwigshafen,
Germany), Ernest Dankwa and Peter DeChant (Valent BioSciences, USA), Jessica
Fussell (Pioneer, USA), Elisabeth and Albert Gasparich (Eppelheim, Germany),
Annette Hinsky-Billhard, Stefanie Keller, Ingrid Lützel (Gesellschaft zur Förderung
der Stechmückenbekampfung-GFS, Waldsee, Germany), Thomas Heeger (Böhl-
Iggelheim, Germany), Mikael Henriksson (Borga, Finland), Icybac GmbH (Speyer,
Germany), Thomas Imhof (Heidelberg, Germany), Michael Kinzig (Heidelberg,
Germany), Olaf Becker (Ludwigshafen, Germany), Daniela Aedes Lanzalaco
(Heidelberg, Germany), Steven Krause (Valent BioSciences, USA), Roland Kuhn
(Mainz, Germany), Charles Myers (Glendora, USA), Beate Ruch-Heeger (Böhl-
Iggelheim, Germany), Willem Takken (University of Wageningen, The Netherlands)
and Srećko and Esther Zgomba (Toronto, Canada).
Contents

Part I General Aspects

1 Systematics..................................................................................................... 3

2 Biology of Mosquitoes................................................................................... 9
2.1 Oviposition............................................................................................. 10
2.2 Embryonic Development....................................................................... 13
2.3 Hatching................................................................................................. 13
2.4 Larvae..................................................................................................... 16
2.5 Pupae...................................................................................................... 19
2.6 Adults..................................................................................................... 19
2.6.1 Emergence.................................................................................. 19
2.6.2 Mating........................................................................................ 20
2.6.3 Dispersal and Host-Seeking Behaviour..................................... 21
2.6.4 Feeding....................................................................................... 22
2.7 Survival During Dry Seasons and Hibernation...................................... 24
2.7.1 Egg Stage................................................................................... 24
2.7.2 Larval Stage............................................................................... 24
2.7.3 Adult Stage................................................................................ 24

3 Medical Importance of Mosquitoes............................................................. 25

3.1 Malaria................................................................................................... 25
3.2 Arboviruses............................................................................................ 30
3.2.1 Togaviridae (Alphavirus)........................................................... 31
3.2.2 Flaviviridae (Flavivirus)............................................................ 34
3.2.3 Bunyaviridae (Bunyavirus)........................................................ 37
3.3 Filariasis................................................................................................. 39
3.4 Future Perspectives and Conclusions..................................................... 40

4 Mosquito Research Techniques................................................................... 43

4.1 Sampling Mosquito Eggs....................................................................... 43
4.1.1 Anopheles Eggs.......................................................................... 43
4.1.2 Egg Rafts.................................................................................... 43
4.1.3 Aedes/Ochlerotatus Eggs........................................................... 44
4.1.4 Eggs in Artificial Oviposition Sites........................................... 45
4.2 Sampling Mosquito Larvae and Pupae.................................................. 46

xvii
xviii Contents

4.3 Sampling Adult Mosquitoes in the Field............................................... 47

4.3.1 Sampling Flying Mosquitoes..................................................... 47
4.3.2 Adult Mosquito–Outdoor Resting Catches................................ 47
4.3.3 Adult Mosquito–Indoor Catches................................................ 47
4.3.4 Bait Catches............................................................................... 48
4.3.5 Adult Mosquito Traps................................................................ 49
4.3.6 Mark-Release-Recapture Techniques........................................ 51
4.4 Laboratory Based Research Techniques................................................ 51
4.4.1 Rearing Mosquitoes................................................................... 51
4.4.2 Preserving Mosquitoes............................................................... 53
4.4.3 Mosquito Blood Meal Identification.......................................... 55
4.4.4 Methods for Measuring the Physiological Stage....................... 55
4.4.5 Morphological and Taxonomic Techniques............................... 56
4.5 Assessing the Activity of Insecticides and Repellents
on Mosquitoes........................................................................................ 58
4.5.1 Insecticide Susceptibility Testing.............................................. 58
4.5.2 Assays of Insecticide Deposits on Surfaces
(e.g. Walls or Nets).................................................................... 60
4.5.3 Assays of Efficacy of ULV Insecticide
Treatments in the Field.............................................................. 60
4.5.4 Assays of Efficacy of Mosquito Repellents............................... 60
4.6 Conclusion............................................................................................. 61

5 Morphology of Mosquitoes........................................................................... 63
5.1 Adults..................................................................................................... 63
5.1.1 Head........................................................................................... 63
5.1.2 Thorax........................................................................................ 67
5.1.3 Abdomen.................................................................................... 72
5.2 Larvae..................................................................................................... 76
5.2.1 Head........................................................................................... 78
5.2.2 Thorax........................................................................................ 80
5.2.3 Abdomen.................................................................................... 80
5.3 Pupae...................................................................................................... 84

Part II I dentification Keys; Morphology; Ecology and Distribution

of European Species

6 Key to Female Mosquitoes........................................................................... 91

Genera............................................................................................................. 91
6.1 Genus Anopheles.................................................................................... 92
6.2 Genera Aedes and Ochlerotatus............................................................. 95
6.3 Genus Culex........................................................................................... 106
6.4 Genus Culiseta....................................................................................... 108
6.5 Genus Coquillettidia.............................................................................. 111

7 Key to Male Mosquitoes............................................................................... 113

Genera............................................................................................................. 113
7.1 Genus Anopheles.................................................................................... 115
7.2 Genera Aedes and Ochlerotatus............................................................. 118
Contents xix

7.3 Genus Culex....................................................................................... 128

7.4 Genus Culiseta................................................................................... 132
7.5 Genus Coquillettidia.......................................................................... 134

8 Key to Mosquito Fourth Instar Larvae..................................................... 135

Genera........................................................................................................... 135
8.1 Genus Anopheles................................................................................ 137
8.2 Genera Aedes and Ochlerotatus......................................................... 141
8.3 Genus Culex....................................................................................... 154
8.4 Genus Culiseta................................................................................... 159
8.5 Genus Coquillettidia.......................................................................... 162

9 Subfamily Anophelinae.............................................................................. 163

9.1 Genus Anopheles (Meigen)................................................................ 164
  9.1.1 Subgenus Anopheles (Meigen)............................................ 165
Anopheles algeriensis (Theobald 1903)............................... 165
Anopheles Claviger Complex.............................................. 166
Anopheles claviger s.s. (Meigen 1804)............................ 166
Anopheles petragnani (Del Vecchio 1939)...................... 168
Anopheles hyrcanus (Pallas 1771)....................................... 169
Anopheles Maculipennis Complex...................................... 170
Anopheles atroparvus (Van Thiel 1927).......................... 173
Anopheles beklemishevi (Stegnii and Kabanova 1976).... 173
Anopheles labranchiae (Falleroni 1926).......................... 174
Anopheles maculipennis s.s. (Meigen 1818).................... 174
Anopheles melanoon (Hackett 1934)............................... 175
Anopheles messeae (Falleroni 1926)................................ 175
Anopheles sacharovi (Favre 1903)................................... 175
Anopheles subalpinus (Hackett and Lewis 1935)............ 176
Anopheles marteri (Senevet and Prunelle 1927).................. 177
Anopheles plumbeus (Stephens 1828).................................. 178
  9.1.2 Subgenus Cellia (Theobald 1902)....................................... 180
Anopheles cinereus (Theobald 1901)................................... 180
Anopheles cinereus hispaniola (Theobald 1903)................. 181
Anopheles multicolor (Cambouliu 1902)............................. 182
Anopheles sergentii (Theobald 1907).................................. 183
Anopheles superpictus (Grassi 1899)................................... 185

10 Subfamily Culicinae.................................................................................... 187

10.1 Genus Aedes (Meigen)....................................................................... 187
10.1.1 Subgenus Aedes (Meigen).................................................... 188
Aedes cinereus (Meigen 1818)............................................. 189
Aedes geminus (Peus 1970).................................................. 191
Aedes rossicus (Dolbeskin, Gorickaja
and Mitrofanova 1930)............................................................ 192
10.1.2 Subgenus Aedimorphus (Theobald)..................................... 193
Aedes vexans (Meigen 1830)............................................... 194
10.1.3 Subgenus Fredwardsius (Reinert)........................................ 196
Aedes vittatus (Bigot 1861).................................................. 196
xx Contents

10.1.4
Subgenus Stegomyia (Theobald).......................................... 198
Aedes aegypti (Linnaeus 1762)............................................ 198
Aedes albopictus (Skuse 1895)............................................ 201
Aedes cretinus (Edwards 1921)............................................ 203
10.2 Genus Ochlerotatus (Lynch Arribalzaga).......................................... 204
10.2.1 Subgenus Finlaya (Theobald)............................................... 205
Ochlerotatus echinus (Edwards 1920)................................. 205
Ochlerotatus geniculatus (Olivier 1791).............................. 206
10.2.2 Subgenus Ochlerotatus Lynch Arribalzaga.......................... 208
Ochlerotatus annulipes (Meigen 1830)................................ 209
Ochlerotatus behningi (Martini 1926)................................. 211
Ochlerotatus berlandi (Seguy 1921).................................... 212
Ochlerotatus cantans (Meigen 1818)................................... 214
Ochlerotatus Caspius Complex............................................ 216
Ochlerotatus caspius (Pallas 1771).................................. 216
Ochlerotatus cataphylla (Dyar 1916)................................... 218
Ochlerotatus Communis Complex....................................... 219
Ochlerotatus communis (De Geer 1776).......................... 220
Ochlerotatus cyprius (Ludlow 1920)................................... 221
Ochlerotatus Detritus Complex............................................ 222
Ochlerotatus detritus (Haliday 1833)............................... 223
Ochlerotatus diantaeus (Howard, Dyar and Knab 1913)..... 224
Ochlerotatus dorsalis (Meigen 1830).................................. 226
Ochlerotatus Excrucians Complex....................................... 228
Ochlerotatus euedes (Howard, Dyar and Knab 1913)..... 228
Ochlerotatus excrucians (Walker 1856)........................... 229
Ochlerotatus surcoufi (Theobald 1912)............................ 231
Ochlerotatus flavescens (Müller 1764)................................ 231
Ochlerotatus hexodontus (Dyar 1916)................................. 233
Ochlerotatus hungaricus (Mihalyi 1955)............................. 234
Ochlerotatus impiger (Walker 1848).................................... 236
Ochlerotatus intrudens (Dyar 1919).................................... 237
Ochlerotatus leucomelas (Meigen 1804)............................. 238
Ochlerotatus Mariae Complex............................................. 240
Ochlerotatus mariae (Sergent and Sergent 1903)............ 240
Ochlerotatus zammitii (Theobald 1903)........................... 242
Ochlerotatus mercurator (Dyar 1920)................................. 242
Ochlerotatus nigrinus (Eckstein 1918)................................ 243
Ochlerotatus nigripes (Zetterstedt 1838)............................. 245
Ochlerotatus pionips (Dyar 1919)........................................ 246
Ochlerotatus pulcritarsis (Rondani 1872)........................... 248
Ochlerotatus pullatus (Coquillett 1904).............................. 249
Ochlerotatus punctodes (Dyar 1922)................................... 250
Ochlerotatus punctor (Kirby 1837)...................................... 251
Ochlerotatus riparius (Dyar and Knab 1907)...................... 253
Ochlerotatus sticticus (Meigen 1838).................................. 255
10.2.3 Subgenus Rusticoidus (Shevchenko and Prudkina).............. 256
Ochlerotatus lepidonotus (Edwards 1920)........................... 257
Ochlerotatus quasirusticus (Torres Canamares 1951)......... 258
Contents xxi

Ochlerotatus refiki (Medschid 1928).................................... 259

Ochlerotatus rusticus (Rossi 1790)...................................... 261
Ochlerotatus subdiversus (Martini 1926)............................. 263
10.3 Genus Culex Linnaeus........................................................................ 264
10.3.1 Subgenus Barraudius (Edwards).......................................... 265
Culex modestus (Ficalbi 1889)............................................. 265
Culex pusillus (Macquart 1850)........................................... 267
10.3.2 Subgenus Culex (Linnaeus).................................................. 268
Culex brumpti (Galliard 1931)............................................. 269
Culex laticinctus (Edwards 1913)........................................ 270
Culex mimeticus (Noe 1899)................................................ 271
Culex perexiguus (Theobald 1903)...................................... 273
Culex Pipiens Complex........................................................ 275
Culex pipiens pipiens (Linnaeus 1758)............................ 275
Culex pipiens pipiens biotype molestus (Forskal 1775)... 277
Culex pipiens quinquefasciatus (Say 1832)..................... 278
Culex torrentium (Martini 1925)...................................... 279
Culex theileri (Theobald 1903)............................................ 280
10.3.3 Subgenus Maillotia (Theobald)............................................ 282
Culex hortensis (Ficalbi 1889)............................................. 282
10.3.4 Subgenus Neoculex (Dyar)................................................... 283
Culex impudicus (Ficalbi 1890)........................................... 284
Culex martinii (Medschid 1930).......................................... 285
Culex territans (Walker 1856).............................................. 286
10.4 Genus Culiseta Felt............................................................................ 288
10.4.1 Subgenus Allotheobaldia (Broelemann)............................... 289
Culiseta longiareolata (Marcquart 1838)............................ 289
10.4.2 Subgenus Culicella (Felt)..................................................... 290
Culiseta fumipennis (Stephens 1825)................................... 291
Culiseta litorea (Shute 1928)............................................... 292
Culiseta morsitans (Theobald 1901).................................... 294
Culiseta ochroptera (Peus 1935).......................................... 296
10.4.3 Subgenus Culiseta (Felt)...................................................... 297
Culiseta alaskaensis (Ludlow 1906).................................... 298
Culiseta annulata (Schrank 1776)....................................... 299
Culiseta bergrothi (Edwards 1921)...................................... 301
Culiseta glaphyroptera (Schiner 1864)................................ 303
Culiseta subochrea (Edwards 1921).................................... 305
10.5 Genus Coquillettidia (Dyar)............................................................... 306
10.5.1 Subgenus Coquillettidia (Dyar)............................................ 307
Coquillettidia buxtoni (Edwards 1923)................................ 307
Coquillettidia richiardii (Ficalbi 1889)................................ 308
10.6 Genus Orthopodomyia (Theobald).................................................... 310
Orthopodomyia pulcripalpis (Rondani 1872)...................... 310
10.7 Genus Uranotaenia (Lynch Arribalzaga)........................................... 312
10.7.1 Subgenus Pseudoficalbia (Theobald)................................... 312
Uranotaenia unguiculata (Edwards 1913)........................... 312
xxii Contents

Part III Identification Keys, Morphology, Ecology, and Distribution

of Important Vector and Nuisance Species – World-Wide

11 Africa............................................................................................................ 317
11.1 Key to African Female Mosquitoes................................................... 318
11.2 Species Description............................................................................ 322
Anopheles (Cellia) funestus (Giles 1900).......................................... 322
Anopheles Gambiae Complex............................................................ 323
Anopheles (Cellia) gambiae s.s. (Giles 1902).......................... 324
Anopheles (Cellia) arabiensis (Patton 1905)............................ 325
Anopheles (Cellia) quadriannulatus s.l. (Theobald 1911)........ 325
Anopheles (Cellia) bwambae (White 1985).............................. 326
Anopheles (Cellia) melas (Theobald 1903).............................. 326
Anopheles (Cellia) merus (Dönitz 1902).................................. 326
Anopheles (Cellia) pharoensis (Theobald 1901)............................... 326
Culex (Culex) antennatus (Becker 1903)........................................... 328
Culex (Culex) univittatus (Theobald 1901)........................................ 329
Mansonia (Mansonioides) africana (Theobald 1901)....................... 330
Mansonia (Mansonioides) uniformis (Theobald 1901)..................... 330

12 Asia............................................................................................................... 333
12.1 Key to Asian Female Mosquitoes...................................................... 334
12.2 Species Description............................................................................ 339
Anopheles (Anopheles) lesteri (Baisas and Hu 1936)........................ 339
Anopheles (Anopheles) sinensis (Wiedemann 1828)......................... 340
Anopheles (Cellia) culicifacies (Giles 1901)..................................... 341
Anopheles (Cellia) dirus (Peyton and Harrison 1979)....................... 342
Anopheles (Cellia) flavirostris (Ludlow 1914).................................. 343
Anopheles (Cellia) fluviatilis (James 1902)....................................... 344
Anopheles (Cellia) maculatus (Theobald 1901)................................ 345
Anopheles (Cellia) minimus (Theobald 1901)................................... 346
Anopheles (Cellia) stephensi (Liston 1901)....................................... 347
Anopheles (Cellia) sundaicus (Rodenwaldt 1925)............................ 348
Culex (Culex) tritaeniorhynchus (Giles 1901)................................... 349

13 Australia....................................................................................................... 351
13.1 Key to Australian Female Mosquitoes............................................... 351
13.2 Species Description............................................................................ 356
Anopheles (Cellia) farauti s.l. (Laveran 1902).................................. 356
Ochlerotatus (Mucidus) alternans (Westwood 1835)........................ 357
Ochlerotatus (Finlaya) notoscriptus (Skuse 1889)............................ 358
Ochlerotatus (Ochlerotatus) camptorhynchus (Thompson 1868)..... 360
Ochlerotatus (Ochlerotatus) normanensis (Taylor 1915).................. 360
Ochlerotatus (Ochlerotatus) sagax (Skuse 1889).............................. 362
Ochlerotatus (Ochlerotatus) theobaldi (Taylor 1914)....................... 363
Ochlerotatus (Ochlerotatus) vigilax (Skuse 1889)............................ 364
Culex (Culex) annulirostris (Skuse 1889).......................................... 365
Culex (Culex) sitiens (Wiedemann 1828).......................................... 366
Coquillettidia (Coquillettidia) xanthogaster (Edwards 1924)........... 367
Contents xxiii

14 Central and South America....................................................................... 369

14.1 Key to Central and South American Female Mosquitoes.................. 369
14.2 Species Description............................................................................ 374
Anopheles (Anopheles) calderoni (Wilkerson 1991)......................... 374
Anopheles (Anopheles) pseudopunctipennis (Theobald 1901)........... 374
Anopheles (Anopheles) punctimacula (Dyar and Knab 1906)........... 375
Anopheles (Nyssorhynchus) albimanus (Wiedemann 1820).............. 376
Anopheles (Nyssorhynchus) aquasalis (Curry 1932)......................... 377
Anopheles (Nyssorhynchus) darlingi (Root 1926)............................. 378
Anopheles (Nyssorhynchus) nuneztovari (Gabaldon 1940)............... 380
Haemagogus (Haemagogus) janthinomys (Dyar 1921)..................... 381
Ochlerotatus (Ochlerotatus) albifasciatus (Macquart 1838)............. 382
Ochlerotatus (Ochlerotatus) scapularis (Rondani 1848)................... 383
Culex (Culex) nigripalpus (Theobald 1901)...................................... 384
Mansonia (Mansonia) titillans (Walker 1848)................................... 385

15 North America............................................................................................. 387

15.1 Key to North American Female Mosquitoes..................................... 387
15.2 Species Description............................................................................ 391
Ochlerotatus (Ochlerotatus) sollicitans (Walker 1856)..................... 391
Ochlerotatus (Ochlerotatus) taeniorhynchus (Wiedemann 1821)..... 393
Psorophora (Grabhamia) columbiae (Dyar and Knab 1906)............ 394
Psorophora (Janthinosoma) ferox (von Humboldt 1819).................. 395
Culex (Culex) restuans (Theobald 1901)........................................... 396
Culex (Culex) salinarius (Coquillett 1904)........................................ 397
Culex (Culex) tarsalis (Coquillett 1896)............................................ 398
Coquillettidia (Coquillettidia) perturbans (Walker 1856)................. 400

Part IV Control of Mosquitoes

16 Biological Control....................................................................................... 405

16.1 Introduction........................................................................................ 405
16.2 Predators............................................................................................ 406
16.2.1 Vertebrate Predators............................................................. 406
16.2.2 Invertebrate Predators.......................................................... 410
16.3 Parasites............................................................................................. 415
16.3.1 Nematodes........................................................................... 415
16.4 Pathogens........................................................................................... 416
16.4.1 Fungi.................................................................................... 416
16.4.2 Protozoa............................................................................... 418
16.4.3 Bacteria................................................................................ 419
16.4.4 Viruses................................................................................. 431

17 Environmental Management of Mosquitoes............................................. 433

17.1 Introduction........................................................................................ 433
17.2 Environmental Management of Mosquitoes in Urban Areas............. 434
17.2.1 Denying Mosquito Access to Urban Areas,
and into Homes.................................................................... 434
17.2.2 Construction Sites................................................................ 434
xxiv Contents

17.2.3 Water Storage Containers.................................................... 434

17.2.4 Drainage Systems................................................................ 435
17.2.5 Sewage and Waste-Water Processing................................... 435
17.2.6 Cemeteries........................................................................... 436
17.2.7 Urban Sanitation.................................................................. 436
17.3 Environmental Management of Mosquitoes in Rural Areas.............. 436
17.3.1 Agriculture........................................................................... 436
17.3.2 Natural Wetlands.................................................................. 437
17.4 Environmental Management of Mosquitoes
and Human Issues.............................................................................. 438
17.4.1 Community Participation..................................................... 438
17.4.2 Regulations for Environmental Management
of Mosquitoes...................................................................... 439

18 Chemical Control........................................................................................ 441

18.1 History................................................................................................ 441
18.2 Insecticide.......................................................................................... 442
18.2.1 Classification of Insecticides............................................... 443
18.2.2 Insecticide Formulations...................................................... 446
18.2.3 Insecticide Application Techniques..................................... 448
18.3 Chemical Groups of Insecticides....................................................... 449
18.3.1 Chlorinated Hydrocarbons................................................... 449
18.3.2 Organophosphates................................................................ 452
18.3.3 Carbamates........................................................................... 458
18.3.4 Pyrethroids........................................................................... 459
18.3.5 Insect Growth Regulators (IGRs)........................................ 466
18.3.6 Novel Insecticide Classes.................................................... 470
18.4 Management and Monitoring of Insecticide Resistance.................... 471
18.4.1 Resistance Mechanisms....................................................... 472
18.4.2 Resistance Surveillance....................................................... 472
18.4.3 Resistance Management...................................................... 474

19 Physical Control.......................................................................................... 477

19.1 Introduction........................................................................................ 477
19.2 Physical Control of Immature Mosquitoes........................................ 477
19.2.1 Oil........................................................................................ 477
19.2.2 Surface Films and Polystyrene Beads.................................. 478
19.3 Physical Control of Adult Mosquitoes............................................... 481
19.3.1 Other Technology: A Novel Technology or New Tool........ 481
19.4 Conclusions........................................................................................ 481

20 Genetic Control of Mosquitoes.................................................................. 483

20.1 Introduction........................................................................................ 483
20.2 Population Elimination Via the Sterile
Insect Technique (SIT)....................................................................... 484
20.2.1 Introduction.......................................................................... 484
20.2.2 Rearing and Sexing.............................................................. 484
20.2.3 Male Sterilization................................................................. 485
20.2.4 SIT in Practice..................................................................... 485
Contents xxv

20.3 Population Replacement.................................................................... 486

20.3.1 The principle of Population Replacement.......................... 486
20.3.2 Refractoriness to Pathogens............................................... 486
20.3.3 Genetic Drivers.................................................................. 487
20.4 Ethical, Legal and Social Implications of the Use
of Genetic Techniques for Mosquito Control.................................... 488
20.4.1 Absence of Community Participation................................ 489
20.4.2 International Committee for Genetic Control Work.......... 489

21 Personal Protection..................................................................................... 491

21.1 Introduction........................................................................................ 491
21.2 Impregnated Bednets......................................................................... 491
21.3 Repellents Against Mosquitoes.......................................................... 493
21.3.1 Repellents on Skin or Clothing.......................................... 493
21.3.2 Mosquito Coils................................................................... 494
21.3.3 Vapourizing Mats............................................................... 496
21.3.4 Liquid Vapourizers............................................................. 496

22 Implementation and Integration of Mosquito Control

Measures...................................................................................................... 499
22.1 Introduction........................................................................................ 499
22.2 Prerequisites for the Successful Implementation
of the IVM programme...................................................................... 501
22.2.1 Entomological Research (Monitoring).............................. 501
22.2.2 Mapping of the Breeding Sites.......................................... 503
22.2.3 Selection of Appropriate Tools.......................................... 504
22.2.4 Effective Dosage Assessment............................................ 505
22.2.5 Design of the Control Strategy.......................................... 505
22.2.6 Training of Field Staff........................................................ 506
22.2.7 Governmental Application Requirements.......................... 506
22.2.8 Community Participation................................................... 506
22.2.9 Registration of Insecticides................................................ 507
22.2.10 Routine Treatments............................................................ 508
22.2.11 Public Information Systems............................................... 509

References............................................................................................................ 511

Subject Index....................................................................................................... 553

Taxonomic Index................................................................................................. 565

Introduction

The mosquitoes (family Culicidae) are at the centre of worldwide entomological

research because of their importance as vectors of a wide range of debilitating viral
and parasitic diseases affecting both humans and animals.
More than half of the world’s population lives under the risk of becoming infected
by mosquitoes that carry the causative agents of diseases such as malaria, dengue,
Chikungunya, West Nile fever, Japanese encephalitis or lymphatic filariasis.
Estimates made by the World Health Organisation (WHO) show that 247 million
people became ill in 2006 and about one million people died (WHO 2008) from
mosquito-borne diseases. Although approximately three quarters of all mosquito
species occur in the humid tropics and subtropics, mosquitoes are a problem not
only in these regions. They also cause a considerable nuisance or can occasionally
transmit pathogens to humans in temperate latitudes, for example, the West Nile
virus epidemic in the USA, or the outbreak of Chikungunya fever, in Italy in 2007
(Depoortere et al. 2008).
The floodwater mosquitoes, such as Aedes vexans, are common nuisance species
along rivers world-wide. The snow-melt mosquitoes, e.g. Ochlerotatus communis,
Oc. punctor and Oc. hexodontus, occur in swampy woodlands and tundra areas. The
halophilous species, Oc. caspius and Oc. detritus, breed particularly in the shallow
lagoons along the coasts of southern Europe, Asia Minor and North Africa, and the
rock-pool mosquito Oc. mariae along parts of the Mediterranean rocky coasts. Mass
outbreaks of all those species can cause a major nuisance. Culex pipiens pipiens
biotype molestus, which is commonly known as the “house mosquito” because of its
presence within close proximity to human settlements, can be a nuisance in temper-
ate zones, as can the closely related Cx. p. quinquefasciatus in the tropics. Mosquitoes
are extremely successful organisms due to their ability to adapt to a wide range of
habitats. They are found throughout the world, except in permanently frozen areas.
Mosquito larvae colonise a wide range of water bodies, temporary and permanent,
highly polluted as well as clean, large or small, stagnant or flowing, and even the
smallest accumulations such as water-filled buckets, flower vases, old tyres, brome-
liads, hoof prints or leaf axils. Adult mosquitoes vary greatly in their bionomics, e.g.
in terms of the host-seeking, biting and dispersal behaviour, and strategy for repro-
duction. Their significant medical importance and their troublesome behaviour have
historically attracted the interest of scientists. Their importance as vectors of malaria
and yellow fever was suspected by Joseph Nott in 1848. In 1878 Sir Patrick Manson
showed that the roundworm Wuchereria bancrofti is transmitted by Cx. p. quinque-
fasciatus. Only 3 years later, Carlos Finley postulated that yellow fever was trans-

xxvii
xxviii Introduction

mitted by mosquitoes, which was later proved by Walter Reed and his co-­workers in
1901. Sir Ronald Ross made a further pioneering discovery in Hyderabad, India in
1897, when he recognised the importance of the anophelines as vectors of malaria.
The discovery of the transmission cycles of most vector-borne diseases led to the
recognition that mosquitoes represented a major scourge to humans, which in turn
triggered the development of mosquito control. The foundations for mosquito con-
trol were established at the beginning of the 20th Century. William C. Gorgas, a
member of the Army Medical Corps, USA, dedicated most of his professional life to
the control of yellow fever, with special focus on control of the vector mosquito Ae.
aegypti [Stegomyia aegypti]. By the turn of the 20th Century, he succeeded in sup-
pressing yellow fever in Panama, and set the basis for the construction of the Panama
Canal. Gorgas was the first to recognise that only by the implementation of an inte-
grated control programme, could the severe burden of vector-borne diseases be
reduced. His approach comprised draining the breeding sites, vegetation cutting to
reduce preferred resting sites of adult mosquitoes, treatment of water ­bodies with oil
derivates to suppress immature mosquito stages, screening and quarantine of infected
people to interrupt the transmission, as well as killing the adult mosquitoes to reduce
the vector-density and vector-human contact (Le Prince 1910; Le Prince and
Orenstein 1916).
The development and use of DDT as a residual insecticide, initially achieved phe-
nomenal success in the control of mosquitoes. In the 1950s, it was believed that
malaria would be eradicated by the use of DDT and chloroquine, but disillusionment
quickly followed, because mosquitoes became resistant to the insecticide in many
areas. In addition, the control efforts against the vectors were not entirely beneficial,
as the widespread use of non-specific and highly persistent insecticides caused a
number of toxicological and eco-toxicological problems. Despite considerable efforts
by national and international organisations such as the WHO, it could be argued that
the main outcome to date is simply the prevention of a more dramatic increase in
vector-borne diseases. The Roll Back Malaria partnership (RBM) – an international
alliance of over 90 organisations – such as WHO, UNICEF, World Bank, USAID, the
Global Fund for AIDS, Tuberculosis and Malaria (GFATM) and many non-govern-
mental organisations (NGOs) was set up in 1998 to highlight the existence of low-
cost and effective interventions for malaria control. RBM is the main instrument
through which African leaders were hoping to achieve the goals of the Abuja
Declaration of 2000, where 53 African heads of state pledged to reduce malaria mor-
tality by 50% by the year 2010. The RBM Programme is mainly based on insecticide-
treated bed nets (long-lasting nets), indoor residual spraying and effective diagnosis
and treatment of malaria cases.
But since its inception, it seems that the 2010 target to halve malaria-related deaths
will not be achieved. This attempt demonstrates that other choices for vector control
strategy have to be implemented. It is imperative to recognize that integrated vector
management (IVM), as a basic sound approach, should be incorporated into mos-
quito-borne disease control programmes. Larviciding, breeding site reduction,
improvements in housing facilities and effective public education efforts should be,
together with health care measures, a key part of any further internationally adopted
strategies in vector-borne disease control.
The risk of becoming infected with a vector-borne disease has increased again
not only in the tropics but also in Europe and USA, as shown by the outbreak of
Introduction xxix

Chikungunya fever in Italy in 2007 (Angelini et al. 2007) and West Nile virus in the
USA. Italy’s outbreak of Chikungunya is the first known disease transmission by the
invasive vector, the Asian tiger mosquito (Ae. albopictus [St. albopicta]) in Europe, and
triggered action by both experts and public in the EU community. Overall, the greater
mobility of people to and from endemic areas, the intensified international trade, as well
as the changing climate, will further encourage the spread and establishment of exotic
diseases and invasive species in formerly safe areas. The Asian tiger mosquito origi-
nates from Southeast Asia, where its developmental stages occur in water-filled
tree-holes, coconut shells, bamboo stumps and similar water collections. Over time,
this species has adapted to breeding in artificial containers such as water barrels, car
tyres or other places where small pools of water may collect. This mosquito has under-
gone an astonishing expansion of its range within the last few decades. Since 1979, Ae.
albopictus has been found in Africa, the Americas and Europe, and more recently also
in the Pacific region. It is expected to spread to tropical and subtropical regions, and
occasionally to regions with moderate climates. Like Ae. albopictus, the “Asian bush”
or “Asian rock pool” mosquito Oc. japonicus japonicus [Hulecoeteomyia japonica] is
also an invasive species that has been established outside of its native range (Japan,
Korea, China and Russia) for more than a decade. It was first recorded in North America
in 1998 and in Europe (France) in 2000 (Schaffner et al. 2003, 2009; Williges et al.
2008). Since Oc. j. japonicus is generally found in more northern climates within its
native range (whereas Ae. albopictus was originally a more tropical species), this spe-
cies is able to establish itself more successfully in moderate climate zones like Central
Europe (e.g. Switzerland, Belgium, Germany). Both species are able to colonise a wide
range of natural and artificial breeding sites (discarded tyres, flower vases, catch basins,
bird baths, tree-holes, rock pools, etc.). Due to the resistance of their eggs to desicca-
tion, cold (diapausing larvae in eggs), and the relative lack of preference concerning
their host type (e.g. humans, mammals and birds), these two invasive species have rap-
idly built up populations in newly colonised geographic regions (Pluskota et al. 2008).
The international trade in used tyres and ornamental flowers has facilitated their spread
over large distances and between continents.
The essential foundation for successful action against the mosquitoes requires not
only an integrated mosquito management (IMM) concept, in which all appropriate
methods for control are used, but also knowledge of the biology and ecology of the
target organisms. The importance of a vector or nuisance species is determined above
all by its physiological characteristics, such as reproduction, migration, host-seeking
and biting behaviour. Accurate identification is a basic pre-requisite to a study of the
autecology of a species as well as its biocoenotic relationship in the ecosystem. All
these efforts should result in an improvement of the quality of life for humans by reduc-
ing the mosquito abundance by enhancing control measures based on IVM principles.
All approaches should favour effective methods with low toxicological profile and
minor environmental impact to contribute to the preservation of wetland biodiversity.
Exchange of information and knowledge in the broadest sense should support sound
mosquito control programmes worldwide.
Exciting achievements in molecular biology such as the sequencing of the genomes
of the malaria parasite Plasmodium falciparum and the mosquito vector Anopheles
gambiae give hope for the development of new drugs, vaccines, genetic engineering
of malaria-resistant mosquitoes, and the release of insects carrying dominant lethal
genes (RIDL). However, these new tools should not lead to the neglect of already
developed and efficient strategies for IVM.
xxx Introduction

It is only by implementing IMM/IVM with inputs from remote sensing and GIS
t­echnology, climatology, geology, biology, ecology, medicine, social sciences and
animal and human behaviour, to genetics and molecular biology, that we will be able
to provide innovative tools for solving the most pressing problems in the control of
nuisance/vector mosquitoes and vector-borne diseases.
 Part I
General Aspects
Chapter 1
Systematics

Hennig’s (1966) concept of hierarchies of monophyletic added Brachycera as the eighth suborder/infraorder
taxons based on common ancestors (with plesiomor- for the rest of the Diptera. The monophyly of most of
phies or retained primitive, ancestral characters) and these suborders is now accepted. However in Fly Tree
shared synapomorphies (homologous shared characters (Yeats et al. 2006, http://www.inhs.uiuc.edu), the term
inferred to have been present in the nearest common Nematocera is still used for infra-orders Ptychoptero­
ancestor but not in earlier ancestors nor in the taxa morpha, Culicomorpha, Blephariceromorpha, Bibiono­
outside this group), has provided the theoretical basis morpha, Psychodomorpha, but superfamily Tipuloidea
for taxa formation. During the first decades following is now a sistergroup to Brachycera.
its proposal, it resulted in the establishment of cladistic Cameron et al. (2007) in a molecular pilot study on
trees where recency of common ancestry is the sole Insecta, mainly Diptera, using several genes including
criterion for grouping of the taxa. The problem of mitochondrial ones, and several methods for tree build-
ranking taxa and tree formation in a Darwinian evolu- ing, reached consensus results for some already
tionary context was the next scientific step (Eldridge accepted suborders/infraorders in Diptera. However,
and Cracraft 1980). Opinions about what different the discussion of the relationships of families within
nodes represent, how to deal with branch lengths, and monophyletic infraorders in Lower Diptera is still
how to rank monophyletic entities, have become part going on.
of a scientific field of its own (Britton et al. 2007). The infraorder Culicomorpha including the
Applying both morphologic and genetic taxonomic Culicidae, Chaoboridae, Dixidae and the Chironomidae
methods, and working with different groups of charac- was already regarded as a monophyletic group by
ters to reveal evolutionary relationships between insect Hennig (1973). This has been accepted in the first
orders or families as monophyletic groups, is now catalogue of Culicidae by Knight and Stone (1977).
becoming standard. In the new millennium this work In a more recent analysis of Culicomorpha, the
has resulted in several new hypotheses of phylogenetic Corethrellidae, Simuliidae and Ceratopogonidae were
trees of Insecta. Wheeler et al. (2001) established the also included, and the Thaumaleidae and the
relationship between Diptera and Strepsiptera. Nymphomyiidae were regarded as a sistergroup (Becker
Grimaldi and Engel (2005) in their comprehensive et al. 2003, Fig. 1.1). A consensus about the monophyly
work on extinct and extant Insecta, summarized differ- of Culicomorpha is given by Grimaldi and Engel
ent hypotheses for Diptera. They accepted five subor- (2005), with the Culicidae, Chaoboridae, Corethrellidae,
ders of Lower Diptera (Nematocera): Tipulomorpha, Dixidae, Ceratopogonidae, Chironomidae, and
Psychodomorpha, Culicomorpha, Blephariceromorpha Simuliidae included. The position of Thaumaleidae and
and Bibionomorpha. They placed Anisopodidae as a Nymphomyiidae as a sistergroup, is still under discus-
sistergroup to Brachycera (all higher Diptera) and dis- sion (Fig. 1.1).
carded Nematocera as a paraphyletic group (including At the family level, the monophyly (sharing a single
a most recent common ancestor and some, but not all, ancestral form) of the family Culicidae with three sub-
of it descendants). This view has been strongly advo- families Anophelinae, Culicinae and Toxorhynchitinae,
cated by Amorim et al. (2006). They recognised seven was established by Edwards (1932), and subsequently
suborders/infraorders instead of Nematocera and accepted by Belkin (1962a) and Knight and Stone

N. Becker et al., Mosquitoes and Their Control, 3

DOI 10.1007/978-3-540-92874-4_1, © Springer-Verlag Berlin Heidelberg 2010
4 1 Systematics

regarded the “phenetic clustering” method (based on

general or overall similarity) of Kumar et al. (2007) as
irrelevant to the conclusions drawn from the cladistic
analyses of Reinert et al. (2004, 2006).
At the level of genera, the “new” genus Ochlerotatus
sensu Reinert, Harbach and Kitching (RHK) now con-
tains some 264 species most of which are unassigned
to the 14 genera currently recognised by authors. For
those involved in practical research, and in writing and
publishing, these changes have caused confusion and
have resulted in a rebuttal of the “new” nomenclature
by many scientists, editors of international journals,
and also by mosquito control managers. Russel (2006)
made a useful analysis of “pros” and “cons” for the
Fig. 1.1 The phylogeny of the monophyletic infraorder proposed changes. For this edition, the same nomen-
Culicomorpha after Saether (2000) from a strict consensus and
majority rule cladogram clature as in the first edition, with minor changes, is
used. On a practical level this will keep the identifica-
tion of species consistent. Until a more precise analy-
(1977). The first attempt to elucidate higher phylogeny sis of evolutionary pathways of characters within and
within subfamilies by creating tribes, was made by between the different RHK genera, and a new analysis
Belkin (1962a). He discussed the general assumption using accepted scientific phylogenetic methods, are
that the Anophelinae were closer to the stem of the carried out on the material, the scientific use of all pro-
superfamily, but did not press it further because of lack posed generic changes by RHK will be contentious on
of evidence. A cladistic phylogenetic study of the fam- scientific grounds.
ily by Harbach and Kitching (1998) has now confirmed Up until Knight and Stone (1977), 2,960 valid spe-
the basal position of the Anophelinae as a subfamily cies in 34 genera and 120 subgenera were recognised
within the family Culicidae. They also partly affirmed worldwide. Since then more species, genera, and sub-
the currently used higher ranks within the family and genera have been described, synonymized, or resur-
regarded Anophelinae and Culicinae as valid mono- rected. With the results of Reinert et al. (2004, 2006,
phyletic subfamilies, but lowered the Toxorhynchitinae 2008, 2009) added, the numbers have risen to 111
to tribal rank within the Culicinae (Fig. 1.2). Their genera and 137 subgenera (Reinert 2009) containing
phylogeny of ten tribes broadly corresponds to the 3,517 species (http://mosquito-taxonomic-inventory.
classic divisions. They discussed the relationship info). More revisions of genera or subgenera, espe-
between lower categories as genera and brought the cially on tropical material, will become available.
tribes Aedini and Mansoniini into one sister group, and These revisions will contribute to the understanding
the tribes Culicini and Sabethini into another. of the characters and evolutionary processes which
Relationships within the Aedini were not fully resolved. have made the Culicidae such a successful group
Reinert (2000c) raised the subgenus Ochlerotatus which, as shown by the fossil record, has existed in
Lynch Arribalzaga of the genus Aedes Meigen to its current shape since the Mesozoic (Grimaldi and
generic rank, placed other former subgenera of Aedes Engel 2005).
in the new genus, and divided it into two sections of All very closely related taxonomic entities such as
species based on larval and pupal characters subspecies, species complexes, and genetically, behav-
(Fig. 1.3a,b). We now have the results of four further iourally, or physiologically different strains or popula-
analyses by Reinert et al. (2004, 2006, 2008, 2009). tions are important in the analyses of vector capacity
These are presented in Fig. 1.3a,b. Until an indepen- and therefore in any approach to vector control. The
dent analysis with other phylogenetic methods and an example of the Anopheles Gambiae Complex shows
evolutionary molecular analysis of the additional this. The introduction of new biochemical and recently
material are available, the scientific discussion of the developed molecular methods has opened up a new
phylogeny of Aedini will go on. Reinert et al. (2008) field of research. However, such studies should be
1 Systematics 5

Subfamily Anophelinae
Genus Anopheles (An.)
Subgenera Anopheles, Baimaia, Cellia, Kerteszia, Lophopodomyia, Nyssorhynchus, Stethomyia
Genus Bironella (Bi.)
Subgenera Bironella, Brugella, Neobironella
Genus Chagasia (Ch.)

Subfamily Culicinae
Tribus Aedeomyiini
Genus Aedeomyia (Ad.)
Subgenera: Aedeomyia, Lepiothauma
Tribus Aedini (given separately in Fig. 1.3a,b)
Tribus Culicini
Genus Culex (Cx.)
Subgenera Acalleomyia, Acallyntrum, Aedinus, Afroculex, Allimanta, Anoedioporpa, Barraudius, Belkinomyia,
Carrollia, Culex, Culiciomyia, Eumelanomyia, Kitzmilleria, Lasiosiphon, Lophoceraomyia, Maillotia,
Melanoconion, Micraedes, Microculex, Neoculex, Nicaromyia, Oculeomyia, Phenacomyia, Phytotelmatomyia,
Sirivanakarnius, Tinolestes
Genus Deinocerites (De.)
Genus Galindomyia (Ga.)
Genus Lutzia (Lt.)
Subgenera Insulalutzia, Lutzia, Metalutzia
Tribus Culisetini
Genus Culiseta (Cs.)
Subgenera Allotheobaldia, Austrotheobaldia, Climacura, Culicella, Culiseta, Neotheobaldia, Theomyia
Tribus Ficalbiini
Genus Ficalbia (Fi.)
Genus Mimomyia (Mi.)
Subgenera Etorleptiomyia, Ingramia, Mimomyia
Tribus Hodgesiini
Genus Hodgesia (Ho.)
Tribus Mansoniini
Genus Coquillettidia (Cq.)
Subgenera Austromansonia, Coquillettidia, Rhynchotaenia
Genus Mansonia (Ma.)
Subgenera Mansonia, Mansonioides
Tribus Orthopodomyiini
Genus Orthopodomyia (Or.)
Tribus Sabethini
Genus Isostomyia (Is.)
Genus Johnbelkinia (Jb.)
Genus Kimia (Km.)
Genus Limatus (Li.)
Genus Malaya (Ml.)
Genus Maorigoeldia (Mg.)
Genus Onirion (On.)
Genus Runchomyia (Ru.)
Subgenera Ctenogoeldia, Runchomyia
Genus Sabethes (Sa.)
Subgenera Davismyia, Peytonulus, Sabethes, Sabethinus, Sabethoides
Genus Shannoniana (Sh.)
Genus Topomyia (To.)
Subgenera Suaymyia, Topomyia
Genus Trichoprosopon (Tr.)
Genus Tripteroides (Tp.)
Subgenera Polylepidomyia, Rachionotomyia, Rachisoura, Tricholeptomyia, Tripteroides
Genus Wyeomyia (Wy.)
Subgenera Antunesmyia, Caenomyiella, Cruzmyia, Decamyia, Dendromyia, Dodecamyia, Exallomyia,
Hystatamyia, Menolepis, Nunezia, Phoniomyia, Prosopolepis, Spilonympha, Wyeomyia, Zinzala
Tribus Toxorhynchitini
Genus Toxorhynchites (Tx.)
Subgenera Afrorhynchus, Ankylorhynchus, Lynchiella, Toxorhynchites
Tribus Uranotaeniini
Genus Uranotaenia (Ur.)
Subgenera Pseudoficalbia, Uranotaenia

Fig. 1.2 Classification of Culicidae (subfamily/ subgenus) after Becker et al. (2003) and WRBU 2009
(http://www.wrbu.org) and abbreviations after Reinert (2009)
6 1 Systematics

Fig. 1.3a Classification of Aedini (genus/subgenus) and abbreviations after Reinert (2009)
1 Systematics 7

Fig. 1.3b Classification of Aedini (genus/subgenus) and abbreviations after Reinert (2009)

complemented by renewed high resolution studies of tematics has been followed by many new studies,
the external morphology of all life-stages to find spe- which have established genetic relationships between
cies differences. Use of a combination of different species and within species complexes. Results from
methods will improve the chances of identifying vec- several authors up to the end of 2006 were discussed
tor species within a sibling species group. Therefore by Reinert et al. (2008) in relation to positive genus
more studies of inter- and intraspecific variability of congruence with their ranking of Aedes, Ochlerotatus
the different morphological life-stages are also much and Stegomyia. The analysis by Shepard et al. (2006)
needed. Cross mating studies also improve understand- is a good example of molecular phylogeny based on
ing of relationships. The difficulties in separating subunits of ribosomal DNA sequences from 37 north-
species on morphological characters alone are shown ern Nearctic and Holarctic species. In Simuliidae,
by the numerous synonyms available for worldwide Moulton (2001) obtained results that corresponded
species such as Culex pipiens s.s. This indicates the with classic phylogeny, by combining ribosomal and
amount of variability in external morphological phe- mitochondrial subunit sequences with phylogenetic
notypic characters such as body size, colour, amount analysis.
and colour of scaling and number and positions of Molecular analysis is of particular interest for the
setae in different life-stages, within one species in dif- study of difficult culicid vector species complexes,
ferent geographic areas. Field studies of behaviour and such as the Neotropical Anopheles Albitarsis Complex
physiology of adults and larvae will also add much to containing four species and possibly a fifth molecular
our knowledge and recognition of species. Such studies species (Wilkerson et al. 2005), and the Australian
are important not only for taxonomic clarity but also for Anopheles Annulipes Complex (Foley et al. 2007).
practical vector recognition and vector control. The latter has been found to have 17 members of two
Molecular research advances have created a separate geographically distinct clades. Harrison (2007) showed
branch of molecular research on Insecta, which also how ongoing molecular research on the South USA
has bearings on systematics (Gilbert et al. 2005). Now Anopheles Crucians Complex, can raise practical vec-
it is possible to retrieve DNA from very small sources, tor problems as well as create serious taxonomical
and also from museum material. This step will be of difficulties. He found that the Crucians Complex,
the utmost importance in highlighting phylogenetic which was formerly considered to include three spe-
problems in species groups, as well as enabling the cies, in fact contained two more sibling species with
analysis of difficult species complexes. Munsterman’s inseparable females. His discussion of which species in
(1995) summary of advances in molecular culicid sys- reality may be present at a site, if no reared material
8 1 Systematics

from larvae are available to help identify a species of a analysis, using a combination of all available methods.
complex, is a useful illumination of the problems facing The basis for such studies are comprehensive field
practical control work. Therefore for both scientific sampling, the careful curating of collections of hatched
taxonomy and practical vector control reasons, sibling material, and the ongoing support of taxonomic knowledge
species or species complexes are important targets for throughout long-term investigations.
Chapter 2
Biology of Mosquitoes

Regarding their special adaptational mechanisms, as rain-water drums, tyres, cemetery vases, small clay
mosquitoes are capable of thriving in a variety of envi- pots, etc.
ronments. There is hardly any aquatic habitat anywhere Furthermore, their capacity to adapt to various
in the world that does not lend itself as a breeding site climatic factors or changing environmental conditions
for mosquitoes. They colonise the temporary and per- is fascinating. For instance, Ae. albopictus, the Asian
manent, highly polluted as well as clean, large and tiger mosquito is originally a tropical species. In the
small water bodies; even the smallest accumulations course of a climate-related evolutionary adaption it
such as water-filled buckets, flower vases, tyres, hoof developed a photoperiodic sensitivity. When days are
prints and leaf axes are potential sources. shorter, the photoperiodically sensitive female inhabit-
In temporarily flooded areas, along rivers or lakes ing a temperate climate, lays eggs that are different
with water fluctuations, floodwater mosquitoes such as from the eggs that she lays when days are longer. Eggs
Aedes vexans or Ochlerotatus sticticus develop in large laid during shorter days, are dormant and do not hatch
numbers and with a flight range of several miles, until the following season, ensuring the species’ sur-
become a tremendous nuisance even in places located vival through the winter.
far away from their breeding sites (Mohrig 1969; This ability to adapt to moderate climatic condi-
Becker and Ludwig 1981; Schäfer et al. 1997). tions and the fact that the eggs are resistant to desic-
In swampy woodlands, snow-melt mosquitoes such cation and survive for more than a year, including the
as Oc. cantans, Oc. communis, Oc. punctor, Oc. hexo­ capability of adaptation to artificial breeding sites
dontus, and Oc. cataphylla, encounter ideal conditions such as tyres and flower pots, make Ae. albopictus
for development in pools that are formed after the or Oc. j. japonicus successful species. This has con-
snow melts or after heavy rainfall. tributed to its spread globally via international trade
In floodplains along coastal areas, the halophilous in plants like Dracaena spp. (“lucky bamboo”) and
species (preferring brackish or salt water habitats) such tyres. Within hours or days they can be transported
as Oc. taeniorhynchus, Oc. sollicitans, Oc. vigilax, Oc. from one country or continent to another by cars, air-
caspius, Oc. detritus, develop in huge numbers. Larvae crafts or trans-oceanic containers (Madon et al.
of the Anopheles can be found in association with other 2002).
mosquito species in fresh- or salt-water marshes, man- These are but a few examples, which illustrate the
grove swamps, rice fields, grassy ditches, edges of tremendous ecological flexibility of mosquitoes suc-
streams as well as in small temporary water collec- cessfully adapted to.
tions. Many species prefer habitats either with or with- Like all Diptera, mosquitoes exhibit complete meta-
out vegetation. morphosis. All mosquitoes need aquatic habitats for
Tree-holes are the habitat of arboreal species such their development, although Aedes/Ochlerotatus spp.
as Oc. geniculatus, Ae. cretinus, Anopheles plumbeus can lay their eggs in moist soil. After hatching they pass
and Orthopodomyia pulcripalpis. through four larval instars and a pupal stage when the
Species like Cx. p. pipiens, Ae. aegypti [St. aegypti] transformation into an adult takes place. Most species
Ae. albopictus [St. albopicta] or Oc. j. japonicus can are unautogenous: following copulation, the females have
even breed in a variety of small water containers such to take a blood-meal to complete the egg development.

N. Becker et al., Mosquitoes and Their Control, 9

DOI 10.1007/978-3-540-92874-4_2, © Springer-Verlag Berlin Heidelberg 2010
10 2 Biology of Mosquitoes

Only a few species have populations that are autoge- keep the egg-raft in position and when rafts drift to
nous. They first develop egg batches without a blood- their aquatic boundaries they tend to remain there.
meal (e.g. Cx. p. pipiens biotype molestus). Immediately following oviposition, the eggs are soft
and white, but they sclerotize and darken within
1–2 h.
Anophelines lay single eggs while standing on the
2.1 Oviposition water surface or hovering above it. The eggs of this
subfamily are adapted for floating and can easily be
Female mosquitoes lay between 50 and 500 eggs, 2–4 damaged by desiccation.
days (or longer in cool temperate climates) after the The embryos of the first group do not enter dormancy
blood-meal. In general, the mosquitoes can be divided or diapause and hatch when the embryonic development
into two groups depending on their egg-laying behav- is completed. Species producing nondormant eggs usu-
iour (Barr 1958) and whether or not the embryos ally have several generations each year. Their develop-
enter into a period of dormancy (externally triggered ing stages are found for the most part in more permanent
resting period) or diapause (genetically determined waters where one generation succeeds another during
resting period). the breeding season. The number of generations depends
In the first group, females deposit their eggs onto the on the length of the breeding season, as well as the
water surface either singly (Anopheles) or in batches abiotic and biotic conditions, and most importantly, it
(e.g. Culex, Uranotaenia, Coquillettidia, Orthopo­ is the temperature which influences the speed of
domyia and subgenus Culiseta, Fig. 2.1). development.
The Culex females lay their eggs in rafts comprising The parameters that determine the choice of a
several hundred eggs locked together in a boat-shaped breeding site by the females laying their eggs onto the
structure. During oviposition, the females stand on the water surface are still unknown for many species.
water surface with the hind-legs in a V-shaped posi- Factors such as water quality, incidence of light, existing
tion. The eggs are released through the genital opening eggs, available food, and local vegetation are decisive
and grouped together between the hind-legs, forming a factors in selecting a favourable breeding site.
raft where the eggs stand vertically on their anterior For Cx. p. pipiens, it is known that the content of
poles attached together by chorionic protrusions organic material in the water plays an important role in
(Clements 1992). The anterior pole of each egg has a attracting the females about to lay eggs. Apparently,
cup-shaped corolla with a hydrophilic inner surface, gaseous substances such as ammonia, methane, or carbon
which lies on the water surface, the outer surface is dioxide, which are released when organic material
hydrophobic. The resulting surface tension helps to decomposes, create an effect of attracting the females
of Cx. p. pipiens (Becker 1989b). They recognise that
such a site has adequate food and that favourable con-
ditions prevail for the development of their brood.
A few other examples illustrate that the egg-laying
behaviour reflects the ecological conditions in the breed-
ing site. The submerged larvae and pupae of Coquillettidia
obtain the oxygen they need by inserting their siphon
into the aerenchyma (air filled tissue) of certain plants
under water. Therefore, in order to ensure the develop-
ment of the larvae, the females must recognise the appro-
priate aquatic plants at the time they lay their eggs in
order to ensure the development of the larvae.
The second group lays eggs which do not hatch
immediately after oviposition (Fig. 2.2). The egg-laying
behaviour of the floodwater mosquitoes (e.g. Ae. vexans),
Fig. 2.1 Egg raft of Culiseta annulata (size approx. 5 mm) and the subgenus Culicella of genus Culiseta, which lay
2.1 Oviposition 11

Fig. 2.2 Eggs of Ae. vexans (a: SEM-photo, 50X; b: light microscopical photo 8X, Oc. cantans (c, SEM, 50X), Oc. rusticus
(d, SEM, 50X)

their eggs singly, not on the water surface but into the The ability of a floodwater mosquito female to find
moist soil, which is subsequently flooded when water appropriate places for egg-laying which guarantees
levels rise, is most interesting. The eggs are laid into maximum breeding success is not yet fully understood.
small depressions or between particles of moss with a However, respect is due to these tiny insects which have
high degree of soil moisture which protect the sensitive adapted their behaviour to overcome the hostile condi-
eggs from drying-out during the embryogenesis (Barr tions in their breeding sites. If the females chose to lay
and Azawi 1958; Horsfall et al. 1973). For Ae. vexans their eggs in low-lying areas with almost permanent
and Oc. caspius, which breed in flooded areas where the water-flow, they would encounter crucial disadvan-
levels fluctuate frequently, the appropriate egg-laying tages: low-lying areas are flooded for long periods of
behaviour is crucial to ensure successful development of time and have, therefore, a very unfavourable alternating
the immature stages. A suitable egg-laying site for flood- sequence of dry and flooding spells, therefore, allowing
water species must meet the following prerequisites: only very small populations of floodwater mosquitoes
to develop. Areas with almost permanent water-flow
(a) The substrate must be wet enough at the time the generally have a high concentration of natural enemies,
eggs are laid in order to ensure that the freshly laid such as fish, so that the risk of being preyed upon would
eggs which are very sensitive to any water loss, do not be very high for the mosquito larvae.
desiccate before their impermeable endochorion has However, flooded areas with a very short period of
been tanned and the wax layer of the serosal cuticle is water-flow are also unfavourable egg-laying sites,
formed (Horsfall et al. 1973; Clements 1992); because they entail the risk of premature drying-out.
(b) There must be a subsequent and sufficient flood- This kind of terrain becomes flooded for a short period
ing of the soil where the eggs have been laid, so of time and only in the years when water is abundant,
that the complete process can take place from thus the wet and dry sequences are not favourable for
hatching all the way to the imago emergence; the development of several consecutive generations.
(c) The water body for subsequent breeding should These areas dry very rapidly following a flood so that
have as few mosquito predators as possible, to the Aedes or Ochlerotatus eggs run the risks of desic-
ensure that the larvae are not preyed upon by natural cation since the developing embryos are very sensitive
enemies when they hatch. to water loss.
12 2 Biology of Mosquitoes

Figure 2.3, shows the preferred egg-laying sites of appropriate egg-laying substrate and are attracted to it.
the floodwater mosquitoes (e.g. Ae. vexans). Usually, However, these criteria alone are not enough, given
these areas consist of dense vegetation and silty soil, that during rainy periods there would be many other
with the reed (e.g. Phragmites australis) being highly places which would apparently appear adequate due to
attractive to ovipositing female mosquitoes. their high moisture content.
Usually, the reed zone precisely demarcates the It is likely that the floodwater mosquitoes are able
mid-water level in riparian systems, since reeds need a to differentiate between various soil types. The soil in
good amount of water. most floodplains consists of a high percentage of clay
The fluctuating curve of the Rhine river, for ­example, and low percentage of humus or organic materials, in
makes it quite clear how important this egg-laying contrast to many other soils (Ikeshoji and Mulla 1970;
behaviour is for the development of the floodwater Strickman 1980a,b; Becker 1989b).
mosquitoes (Fig. 2.4). In a zone of between 4 and 5 m, It is also possible that flooded areas along the river-
there is the ideal timing of dry and wet periods, with banks produce pheromone-like odours, which may be
optimum water-flow to guarantee the development of a recognised by the female mosquitoes and which induce
large number of individuals in a population. Further­ them to lay their eggs. These odours could come from
more, predators, especially fish are usually low in eggs, which have already been laid in the soil, or from
numbers or absent. particular associations of plants which are indicators of
But how do these female floodwater species find a specific moisture level in the soil, and the occurrence
the optimum oviposition site? Gravid females obvi- of regular floods. As a whole, the ovipositional behav-
ously recognise the wet, silty, riparian clay soil as an iour of the floodwater mosquitoes shows an astonishing

water level
preferred oviposition site

Rhine
dike
8m
6m
level of ground water 4m
2m
0m
Scirpus-
plain elm trees etc. willow trees etc. zone of reed Typha- Rorippa submerse zone
zone

Fig. 2.3 Transsection through the Upper Rhine Valley with zones of vegetation and preferred oviposition sites of floodwater
mosquitoes (e.g. Ae. vexans)

River water level

7m

6m

5m

4m

3m

2m

1m
Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct

Fig. 2.4 River water levels in Central Europe favor the development of the eggs of floodwater mosquitoes
2.3 Hatching 13

degree of adaptation to their habitat, an adaptation instance, larvae of Ae. vexans are ready to hatch in
which has developed through the course of evolution. 4–8 days after oviposition, when the eggs are kept at
25 and 20°C, respectively (Horsfall et al. 1973; Becker
1989b). Hatching experiments with freshly laid Ae.
vexans eggs kept at 20°C have shown that 8 days after
2.2 Embryonic Development the eggs had been laid, almost 50% were ready to
hatch. This means that the embryonic development of
Mosquito embryogenesis has been described in detail Cx. p. pipiens usually takes only half as long as that of
by Clements (1992). The embryonic development Ae. vexans, which assures a quick generation renewal
starts almost immediately after the eggs have been of the former. The relatively slow embryonic develop-
laid. Depending on the temperature, it takes about 2–7 ment of floodwater Aedes/Ochlerotatus species can be
days or more until the embryos are fully developed. explained by the fact that these mosquitoes lay their
The course of embryonic development also reflects eggs in flooded areas where there are few ecological
a special adaptation to various abiotic conditions in the factors requiring rapid embryonic development. It usu-
larval habitat (Becker 1989b). The nondormant eggs of ally takes more than one week until the next flooding
the Culex, Coquillettidia, Uranotaenia, Orthopodomyia occurs. Therefore, there is little ecological advantage
and the subgenus Culiseta, usually hatch after a short in the fast sequence of generations that would result
time when the embryonic development is completed. from rapid development of the embryos.
The length of time required is dependent almost
entirely on temperature. At a temperature of 30°C, the
Cx. p. pipiens larvae hatch 1 day after the eggs have
been laid, at 20°C and 10°C it takes 3 and 10 days 2.3 Hatching
respectively, and at 4°C, the embryonic development
of the Cx. p. pipiens cannot be completed (Fig. 2.5). Aedes and Ochlerotatus mosquitoes have developed a
The embryonic development of the Aedes/Ochle­ highly sophisticated mechanism which regulates the
rotatus species usually takes significantly longer, for hatching process, as a direct adaptation to the greatly fluc-
tuating abiotic conditions existing in the temporary waters
where these mosquitoes breed (Gillett 1955; Telford
hours 1963; Horsfall et al. 1973; Beach 1978; Becker 1989b).
320 The timing of larval hatching to coincide with the pres-
300 ence of ideal developmental conditions, is a prerequisite
280 for successful development in temporary water bodies.
260 + The difference in hatching behaviour between the
240 snow-melt mosquitoes (e.g. Oc. cantans, Oc. commu­
220 nis, and Oc. rusticus) and the floodwater mosquitoes
200 (e.g. Ae. vexans) clearly illustrates the extent to which
180 the hatching behaviour of each Aedes/Ochlerotatus
160
species is adapted to the abiotic conditions in their
140
respective breeding sites.
120
+ The breeding waters of snow-melt mosquitoes, for
100
example depressions and ditches in marshy regions
80
60
+ covered frequently with alder trees in central Europe,
40
t0 = 6.78°C are usually flooded for long periods of time with rela-
20
+ + tively cold water.
In Fig. 2.6, the phases of development and diapause
4 10 15 20 25 30 °C of the univoltine (monocyclic, one generation/year)
snow-melt mosquitoes, are shown as a function of the
Fig. 2.5 Duration of the embryonic development of Cx. p.
pipiens at various temperatures (to = no development possible water level variation of a pool in the swampy wood-
according to Tischler 1984) lands in central Europe.
14 2 Biology of Mosquitoes

Fig. 2.6 Phases of development and diapause of univoltine snow-melt mosquitoes in a pond in Central Europe

The breeding sites of the snow-melt mosquitoes are development and diapause of Ae. vexans are shown as
usually flooded in the late fall and after the snow has a function of the water level variation (for e.g. the
melted. The water level usually reaches its peak in Rhine river).
early spring. Under normal conditions it eventually Unlike the semipermanent status of the water in the
recedes slowly but steadily throughout the summer breeding sites of snow-melt mosquitoes, the breeding
until the pools are dry again. sites of the floodwater mosquitoes are characterized by
Snow-melt mosquitoes have adapted perfectly to temporary water-flow caused by rapid, substantial
these conditions in their breeding sites, by their dia- fluctuations in the water level of the rivers following
pause patterns and appropriate reaction to the hatching heavy rains in early and mid-summer. By contrast, late
stimuli. After the eggs have been laid usually in early summer and winter are usually marked by extensive
summer, the embryos of the majority of the snow-melt periods of low water levels. As a consequence of this,
mosquitoes automatically enter diapause. They are the best developmental conditions for larvae of flood-
unable to hatch during the summer months, thus water mosquitoes occur between April and September,
avoiding the risk of premature emergence during the therefore, these mosquitoes diapause during autumn,
dry spells of summer. winter, and early spring (Telford 1963). Due to the
In central Europe, some species, e.g. the snow-melt extremely variable nature of the water-flow, floodwater
mosquito Oc. rusticus and Cs. morsitans, are ready to mosquitoes have to hatch during summer when high
hatch at the beginning of winter after sensing the con- water temperatures enable rapid development to take
tinuous temperature decrease during autumn. The dia- place. Moreover, their being multivoltine (polycyclic,
pause of most snow-melt mosquitoes (e.g. Oc. cantans several generations/year), makes sense from an eco-
and Oc. communis) is interrupted when the tempera- logical viewpoint, since they can go through several
ture has dropped in autumn and the cold winter period generations coinciding with the fluctuations in the
has set-in. Consequently, these mosquitoes are ready water level. This factor is mainly responsible for the
to hatch during the snow-melt in the next spring and huge reproduction rate of these species, often creating
shortly afterwards. This factor, along with their ability a tremendous nuisance.
to hatch in very cold and oxygen-rich waters, enables If the hatching behaviour of the floodwater mos-
these mosquitoes to be ready to hatch at a time when
quito is analyzed in detail, a well-adjusted control
favourable water level conditions are present. After
mechanism can be seen, which is mainly influenced by
hatching, the semipermanent water in forest pools pro-
the following factors:
vides ideal conditions for slow development. In central
Europe, this usually takes place between the end of (a) Dissolved oxygen is present during periods of high
April and the beginning of May. water levels, most of the flooded areas along rivers
Even more sophisticated, is the hatching behaviour are covered with flowing and oxygen-rich water.
of the floodwater mosquitoes. In Fig. 2.7, the phases of Hatching at that time would create the risk of the
2.3 Hatching 15

Fig. 2.7 Phases of development and diapause of the floodwater mosquito Ae. vexans in Central Europe

larvae being swept away. Moreover, fish usually water is warm enough to permit rapid development.
invade deep flooded areas in search for food. In This ensures that the brood will not dry out due to
order to avoid these dangers, the floodwater mos- rapid changes in the water levels. For instance, in the
quitoes have developed a specific hatching behav- Upper Rhine Valley, the Ae. vexans larvae hatch in
iour. The decline in dissolved oxygen when water springtime when the water temperature reaches 10°C
is stagnant, usually triggers hatching of the larvae or more. An interesting phenomenon is the seasonal-
of the floodwater mosquitoes (Hearle 1926; Gjullin related hatching process. Following the cold winter
et al. 1941; Borg and Horsfall 1953; Travis 1953; phase and after the subsequent increase in tempera-
Judson 1960; Horsfall et al. 1958, 1973; Burgess ture, a small percentage of the Ae. vexans larvae are
1959; Becker 1989b). They hatch only when the ready to hatch even at 4°C. The adaptation of the
flooded pools become stagnant and the oxygen temperature-dependent hatching behaviour to the cli-
content starts to decrease very rapidly (due to bac- matic conditions and water-flow in an area in central
terial degradation processes). The decreasing level Europe can be demonstrated with the example of the
of oxygen in the water signals the unhatched hatching response to water of 15°C. In springtime,
­larvae that the water will remain stagnant at the the hatching rate reaches its peak at 15°C. In the
time of their hatching, thus ensuring that the risk of months of March and April, apart from the gradually
being washed away, has diminished. Moreover, the increasing water temperatures during springtime, the
bacterial action causing decomposition of organic water level usually rises due to rainfall. This creates
material ensures that the larvae will have an ade- favourable conditions for the development of the
quate food supply. In addition, the shallow, stag- floodwater mosquitoes. On the other hand, water of
nant waters are not a suitable environment for the the same temperature induces a reduced hatching
larvae’s main predator, the fish. response during late summer and autumn. Larvae
would not be able to complete their development if
(b) Water temperature plays a fundamental role in the
they were to hatch at a temperature of 15°C in October
hatching process of the floodwater mosquito.
or November, since at this time of year the falling
Premature hatching during cold weather would
temperatures prolong the larval development, while
greatly delay the development of the larvae, since
the water level is receding.
the process is very temperature dependent.
It is remarkable that there are also differences in the
Since floodwater mosquitoes usually diapause from hatching behaviour of the Ae. vexans populations in
autumn until springtime, the temperature-dependent different river systems. It appears that the Aedes/
hatching behaviour of Ae. vexans also ensures that Ochlerotatus species are adapted to the hydrological
the larvae will not hatch before the temperature of the characteristics of each river system. In river systems
16 2 Biology of Mosquitoes

with a lower discharge of water, the periods of inunda- at the egg-laying site) determine whether a larva will
tion are usually shorter, which means that the develop- hatch under certain conditions or not. Thus, the larvae
ment of the mosquito has to be rapid. Therefore, the hatch “in installments” (Wilson and Horsfall 1970;
Aedes and Ochlerotatus mosquitoes breeding in these Becker 1989b). For instance, soil samples containing
areas have an extended diapause until summer, to allow the eggs of Ae. vexans and kept at 25°C, were flooded
a faster development at higher temperatures. several times, with dry phases of 4 weeks between
Let us have a closer look at the diapause of the each flooding step. After the first flooding, 57% of the
ready-to-hatch larvae inside the eggs of the floodwater total number of larvae hatched, 10% after the second,
mosquito Ae. vexans, especially concerning the change 25% after the third, and 8% hatched the fourth time
from a state of hatching inhibition to one of hatching (Becker 1989). This behaviour pattern assures long-
readiness. This process is called “conditioning”, whereas, term survival for mosquito species that develop in tem-
the onset of hatching inhibition is called “deconditioning” porary bodies of water. If, for example, all of the larvae
(Horsfall 1956b; Horsfall and Fowler 1961; Clements were to hatch at the same time under ideal hatching
1963; Horsfall et al. 1973). conditions and if, as a consequence of a sudden dry
The factors that are most likely to have an influence spell, all of the breeding sites were to dry-out before
on diapause, or on hatching inhibition and readiness, the brood could complete its developmental cycle. One
are temperature fluctuations, varying degrees of mois- single natural event could virtually wipe out the entire
ture in the air and soil as well as changes in the day- mosquito population. By “hatching in installments”,
length (Brust and Costello 1969). Larvae of Ae. vexans the floodwater mosquito population can survive such
are able to hatch to some extent during a flood in the potentially catastrophic events. There still remains a
same year as that in which the embryogenesis was large contingent of unhatched larvae in the breeding
completed, providing that the temperature remains area. At the time of the next flooding, these larvae will
above 20°C. Decreasing temperatures below 15°C lead still have an opportunity to successfully produce a new
to a hatching inhibition in autumn. After a cold (winter) generation without new eggs having to be laid. Inci­
phase, temperatures of 10°C and above have a condi- dentally, this also happens after a larvicidal treatment.
tioning effect, and interrupt the diapause in the next It is remarkable that the unhatched larvae are able to
spring. However, it is worth mentioning that after a cold persist for at least 4 years without losing their ability to
spell, the readiness to hatch is positively correlated with hatch (Horsfall et al. 1973).
the rise in temperature. The higher the temperature dur- After the content of oxygen decreases in the breeding
ing egg laying and the lower the temperature in winter, site, the larva initiates the shell rupture by pressing
the higher is the hatching response in the following the so-called “egg tooth”, an egg burster located poste-
summer. The complex diapause behaviour allows the rio-dorsally on the head capsule of the larva, onto the
larvae of Ae. vexans to distinguish between favourable egg shell. As a result, the shell splits along a particular
developmental conditions in springtime, and unfavour- line at the anterior end of the egg. A cap (anterior part
able conditions in late summer. It is remarkable that in of the egg shell) breaks away and the larva escapes by
winter even extreme temperatures well below the freez- swallowing water into the gut which forces the body
ing point, will not kill the diapausing larvae. from the shell (Clements 1992). The whole process of
Another behaviour that represents a sophisticated hatching takes only a few minutes.
adaptation to the very variable water-flow in the breed-
ing sites is what is referred to as “hatching in install-
ments”. Even within a batch of eggs laid by one female 2.4 Larvae
subjected to the same microclimatical conditions, not
all of the larvae hatch uniformly. Without a cold phase, The legless (apodous) larval body is divided into three
only a few individuals from a freshly laid egg batch of distinct parts: (a) the head with mouth-parts, eyes and
one female are ready to hatch, whereas, after a cold antennae; (b) the broader thorax and (c) the abdomen
phase, the readiness to hatch is far greater. Apart from which is composed of seven almost identical segments
their inherited variability, the conditions that each egg and three modified posterior segments. These posterior
had experienced (for instance, the location of the egg segments bear four anal papillae to regulate the electro-
in the ovariole during maturation, the timing of the lyte levels. At the abdominal segment VIII, a siphon in
oviposition, as well as differing microclimatic factors culicines, or only spiracular lobes in anophelines, are
2.4 Larvae 17

Fig. 2.8 (a) Larvae of Aedes vexans

Fig. 2.8 (b) Larva of An. plumbeus

tension forces. A gland adjacent to the larval spiracles,

secretes hydrophobic substances to avoid the influx of
water into the respiratory system.
The larvae of the Coquillettidia and Mansonia live
submerged. They therefore possess a siphon which is
modified for piercing submerged parts of aquatic plants
to obtain oxygen from the aerenchyma. The spiracular
apparatus at the distal end of the siphon contains hooks
and a saw-like blade with teeth to pierce the plant tissues.
These larvae have a more sessile habit, hanging head
downwards whilst attached to the plant tissues and filter-
ing the water column for food (Fig. 2.8c). They are there-
fore not easily recognised by predators such as fish.
The larval food consists of microorganisms, algae,
protozoa, invertebrates and detritus. On the basis of their
feeding behaviour they may be classified into filter or
suspension feeders, browsers or predators. The filter
feeders collect food particles suspended in the water col-
umn (especially larvae of the Culex, Coquillettidia, the
subgenus Culiseta or to some extent the Aedes/
Ochlerotatus larvae). The larvae of the filter feeders,
Fig. 2.8 (c) Larva of Coquillettidia richiardii attached to plant
tissue (photo, Hollatz)
typically hang on the water surface filtering the water
column beneath the surface by beating their head brushes
developed where the tracheal trunks open at spiracles (lateral palatal brushes) towards the preoral cavity. This
for the intake of oxygen. Usually the culicine larvae hang generates water currents which carry food particles
head downwards from the water surface (Fig. 2.8a). towards the mouth (Dahl et al. 1988). Mosquito larvae
Anopheline larvae lie horizontally at the water surface. are usually not discriminatory in what they ingest.
Their body is held horizontally by specialized setae (pal- However, the size of the particles are usually less than
mate setae), the notched organ located at the anterior mar- 50 mm. Larvae can also move slowly in the water column
gin of the prothorax and the spiracular lobes which are while filter feeding. The browsers (e.g. most Aedes and
flush with the dorsal surface of the larval body and have Ochlerotatus species) collect food by re-suspension,
direct contact with the air (Fig. 2.8b). scraping or shredding particles, microorganisms, algae,
When the larvae leave the water surface, the lobes and protozoa from the surface of submerged substrates
are retracted, the spiracles are closed and reach the or the microbial film at the air–water interface (the
water surface, the flaplike four or five spiracular lobes Anopheles larvae). Even small portions of dead inverte-
are pulled into their extended position by the surface brates and plants can be bitten-off with the mouth parts.
18 2 Biology of Mosquitoes

The anopheline larva hangs horizontally under the water The development of larvae is temperature dependent.
surface with its dorsal side uppermost and the mouthparts There are great differences in the optimum tempera-
directed downwards. When feeding, the larva rotates its ture for the development of different mosquito species
head 180° and creates a water-current by beating its head (Figs. 2.9a–c). For instance, the snow-melt mosquitoes
brushes to collect the food organisms on the surface film. can complete their development at temperatures as low
Predacious larvae of the genera Toxorhynchites,
Aedes, Psorophora and Culex can feed upon insects b
(often other mosquito larvae). days
Disturbances of the water surface cause the larvae 30
to dive for short periods of time. They dive by flexing 28
the abdomen and moving backwards. When the larvae 26
return to the water surface, they swim backwards until 24 21-23 days
22
their abdomens come into contact with the surface.
20
Larvae moult four times at intervals, before reach-
18

no development t0 = 8.49°C
ing the pupal stage. At each moult, the head capsule is 16
increased to the full size characteristic of the next 14 11-13 days
instar, whereas the body grows continuously. Thus the 12
7-10 days
size of the head capsule is a fairly good morphometric 10
indicator for the larval instar. Each moult is coordi- 8 6-7 days
nated by the relative concentrations and interactions of 6
juvenile hormone and ecdysone, a molting hormone. 4
2

a 4°C 10 °C 15 °C 20 °C 25 °C 30 °C T
days = Duration from the first to the last adult
44
37-42 days Fig. 2.9 (b) Larval and pupal development of Ae. vexans in
42 relation to water temperature
40
38
36 c
days
34
32 64
30 60 48-58 days

28 56
26 52
21-24 days
24 48
22 44
20 40
t0 = 3.98°C

13-17 days
18 36
16 32
t0 = 7.2°C

14 28
11-12 days 21-23 days
12 24
10 20
no development

no development

8 16 11-14 days
6 12
7-8 days
4 8 6-7 days
2 4

4°C 10 °C 15 °C 20 °C 25 °C 30 °C T 4 °C 10 °C 15 °C 20 °C 25 °C 30 °C T
= Duration from the first to the last adult = Duration from the first to the last adult

Fig. 2.9 (a) Larval and pupal development of Oc. cantans in Fig. 2.9 (c) Larval and pupal development of Cx. pipiens in
relation to water temperature relation to water temperature
2.6 Adults 19

as 10°C, whereas they are incapable of developing the cephalothorax makes the pupa positively buoyant.
successfully at temperatures above 25°C (Fig. 2.9a). Mosquito pupae are quite mobile (unlike the pupae of
Usually they hatch in southern and central Europe dur- most other insects). When the pupa is disturbed, it dives
ing February, or later in the northern parts, and the adults by straightening the abdomen and spreading the paddles
emerge 2–3 months later. Larvae of those species which rapidly flexing the abdomen which has retained the lar-
overwinter in the larval stage such as the Oc. rusticus or val musculature. In contrast to larvae which have to swim
Cs. morsitans, will survive in water close to freezing, or actively to the water surface, the pupa floats passively
even in waters which become regularly coated with ice. back to the surface after diving. Pupae of most mosqui-
In contrast, the floodwater mosquitoes (e.g. Ae. toes are relatively tolerant of desiccation and adults can
vexans), develop successfully at higher temperatures emerge successfully even if pupae have been stranded,
within a short period of time, usually 6–7 days from or when the breeding sites have almost dried out. Unlike
hatching to emerging at 30°C (Fig. 2.9b). Larvae of Cx. larvae, pupae do not feed.
p. pipiens can successfully develop in a wide range In Mansonia and Coquillettidia, the trumpets are
(10–30°C) of temperatures (Fig. 2.9c). The develop- modified for penetrating plant tissues. The pupae, like
ment of the aquatic stages also represents an adaptation the larvae, take the oxygen from the aerenchyma of the
to the ecological environment in breeding waters. submerged parts of the plants.
Mosquito larvae (e.g. Ae. vexans) sometimes
aggregate in particular places at the breeding sites.
This crowding effect may be a mechanism to reduce 2.6 Adults
the chance of predation of any single larva.

2.6.1 Emergence

2.5 Pupae The final stage of metamorphosis is completed when

gas is forced between the pupal and the pharate adult
The pupae are also aquatic, the pupal stages usually cuticle, and into its midgut. The pupa straightens the
lasting about 2 days, however, this period may be abdomen into a horizontal position, and by swallowing
reduced or extended, at higher or lower temperatures air it further increases the internal pressure. The cepha-
respectively. During the pupal stage, the process of lothoracic cuticle of the pupa then splits along the
metamorphosis takes place. Some larval organs are ecdysial line and the adult slowly emerges from the
histolysed, whilst the body of the adult is formed pupal skin (Fig. 2.10). The emerging adult moves cau-
through the development of imaginal disks (cells or tiously to avoid falling onto the water surface, whilst
groups of cells that remained quiescent in the larval its appendages still remain partly in the exuvia. In this
body until the pupal stage). In particular, the fat body phase, the emerging individual is highly susceptible to
of the larva is transferred to the adult stage and used as
a source of vitellogenines for autogenous egg forma-
tion or as a reserve for hibernation.
Characteristically, the head and thorax of the pupae
are fused into a prominent cephalothorax which carries
anterolaterally two respiratory trumpets (see Chap. 5,
Fig. 5.18), which are connected to the mesothoracic spir-
acles of the developing adults to provide oxygen. The
abdomen terminates with two paddles and is kept flexed
under the cephalothorax. When at rest, the pupae float
motionless at the water surface, with the tip of the trum-
pets and the palmate setae of the first abdominal segment
in contact with the water surface. The hydrophobic rims
of the trumpets protrude through the water surface for
respiration. An air bubble between the appendages of Fig. 2.10 Emerging adult mosquito
20 2 Biology of Mosquitoes

strong winds and predators such as water striders and The plumose antennae of the males are especially
spiders. receptive to the sound generated by the female. The
The pupae of the genus Coquillettidia are fixed to the flagellum of the antenna starts to vibrate and stimulate
plant tissues in the water body. At the end of the pupal the Johnston’s organ which is located in the swollen
development they have to float to the water surface. second segment (pedicel) of the antenna (Clements
Therefore, the tips of the pupal trumpets break to release 1963; McIver 1982). Contact pheromones may also be
the pupa from the plant before emergence (Mohrig 1969). involved in the mating behaviour.
After emergence, the adult increases the haemo- When a female enters a swarm it will be seized
lymph pressure which causes the legs and wings to immediately by a male. Usually the male and female
stretch. It then immediately ejects droplets of fluid to copulate face to face when flying outside the swarm
empty the gut, while air is dispelled from the gut some (Fig. 2.11). The copulation requires a complex merging
hours later. Within a few minutes it is able to fly when of the male and female reproductive structures. Usually
the soft cuticle has sclerotized. However, 1–1.5 days it takes less than half a minute for the male to deposit
more are required for males and females respectively the spermatozoa in the bursa copulatrix of the female
to adjust their metabolism (Gillett 1983). (Clements 1963), the sperm then moves to the sper-
There is also a difference between male and female mathecae. The male accessory gland secretions contain
sexual maturity at the time of emergence. Male mosqui- a substance known as matronae, which after copulation
toes are not sexually mature at emergence as they have to makes the female unreceptive for the rest of her life.
rotate their hypopygium through 180° before they are The females store sufficient sperm in their spermathe-
ready to mate, which takes about 1 day. Therefore, the cae to fertilize several egg batches without further cop-
males in the population usually emerge 1–2 days before ulation. In contrast to females, male mosquitoes may
the females in order to achieve sexual maturity at the mate many times. The time and preferred location of
same time as the emerging females. Since the pupal stage swarming is species-specific. Swarming (eurygamy) is
of the two sexes appears to be about the same length, the not necessary for all species, and some species may
shortening in development of males takes place primarily mate without it (stenogamy). Usually, mating takes
in the larval stage. Consequently, the male pupae and place soon after emergence, since biting females are
adults of a population are smaller in size than the corre- almost invariably inseminated. After insemination the
sponding females. search for a host to obtain a blood-meal is the next
Following emergence, the adults are ready to begin important phase in the reproductive life of the female.
their life cycle again of mating, feeding and oviposition.

2.6.2 Mating

Mating of most mosquitoes in the palaearctic region

takes place when females enter swarms of flying males.
Such a swarm can consist of only a few or up to several
thousands of male mosquitoes. Usually, males form
swarms over a marker at low light intensities especially
in the evening and morning. Markers are projecting
objects which contrast with the surroundings such as
bushes. When swarming, males face into the wind and
fly forward and backwards, up and down over the
marker. This oscillating flight pattern is often called
“dancing flight”. The sound produced by the male wing
beat has a frequency of ~600 cs–l. The frequency of the
wing beat of the females is lower than that of the males Fig. 2.11 Mating mosquitoes (Photo courtesy of Roland
at 500–550 cs–1 and even lesser when engorged. Kuhn, University of Mainz, Germany)
2.6 Adults 21

2.6.3 D
 ispersal and Host-Seeking wind (passive migration) and an active dispersal
Behaviour (appetitive flight).
During passive migration, the mosquitoes ascend in
swarms and use the wind to drift long distances and
In most mosquito species, oogenesis can only be may occur suddenly in large numbers far away from
completed when the females take a blood-meal. their breeding sites. This non-oriented flight activity is
Therefore, they have developed a complex host-seek- especially influenced by the speed and direction of the
ing behaviour to locate a potential host. Primarily, the wind and guiding landmarks. The passive migration in
location of the host is based on olfactory, visual and swarms occurs only a short time after emergence
thermal stimuli. Females possess numerous antennal (Bidlingmayer 1985).
receptors which respond to host odours. The main During the appetitive flight, female mosquitoes
olfactory stimuli are carbon dioxide, lactic acid, usually disperse actively at least 24 h after emergence.
octenol, acetone, butanone and phenolic compounds. They fly upwind when the wind velocities are below
The host-seeking process may differ within species mosquito flight speed (1 m/s) (Bidlingmayer and
depending on the season and the availability of cer- Evans 1987). The flight against the wind increases the
tain hosts. However, it can usually be divided into likelihood of encountering stimuli deriving from a
three phases (Sutcliffe 1987): host. However, strong winds prevent active dispersal.
(a) Non-oriented dispersal behaviour which enhances This behaviour is species-specific and depends on vari-
the likelihood of the female coming into contact ous features of the terrain and meteorological factors.
with stimuli derived from a potential host. The microclimate influenced by the vegetation type,
(b) Oriented host location behaviour resulting from con- which causes increased humidity and reduced wind,
tact with host stimuli. The strengths of the stimuli are strongly affects the dispersal behaviour. Therefore,
increased as the mosquito and host come closer females usually fly close to the ground or slightly
together; above the top of the vegetation. According to the pre-
(c) Attraction to a suitable candidate host, once the ferred microclimate requirements, some species occur
female has identified it in her immediate vicinity. in greatest numbers in open areas (mostly strong flyers),
others in woodlands (woodland species are moderate
The extent of the non-oriented dispersal behaviour dif- flyers), a third group prefers edges of fields and forests
fers from species to species. In general, it can be sepa- and finally the fourth group comprises the urban
rated into (a) species which usually breed and rest close domestic species, which are usually weak flyers (Gillies
to the habitat of their hosts and therefore do not fly long 1972; Bidlingmayer 1975). Experiments show that Ae.
distances (most container breeders, e.g. Cx. p. pipiens); vexans migrate approximately 1 km/night during warm
(b) species which disperse moderate distances from their and humid weather periods at moderate wind speed.
breeding or resting places to the host’s habitats (some Increasing numbers of Ae. vexans females have been
species of snow-melt mosquitoes, e.g. Oc. rusticus); (c) caught in CDC-traps at a distance of about 5 km from
species, which migrate considerably long distances to their breeding place 8 days after emergence, and
invade new habitats for biting, and/or egg-laying when within 2 weeks at a distance of 10 km or more. Clarke
suitable habitat is available (some floodwater mosquitoes, (1943a,b) recorded migration distances of marked
e.g. Ae. vexans). Ae. vexans females of 22 km and Gjullin and Stage
The flight behaviour is influenced by temperature, (1950) and Mohrig (1969) up to 48 km.
humidity, illumination levels, wind velocity and the In contrast, snow-melt mosquito species stay near
physiological stage of a female. For instance, most their breeding sites and do not regularly migrate long
Aedes/Ochlerotatus species migrate during the twilight distances (Schäfer et al. 1997). In mark-release-recap-
when the temperature is dropping and the humidity is ture experiments Joslyn and Fish (1986) collected
increasing. They are usually more active on moonlit Oc. communis females at distances up to 1,600 m from
nights (Bidlingmayer 1964). their breeding sites. Nielsen (1957) reported a maxi-
Species with a tendency for extensive flight mum flight range of about 1,600 m for Oc. communis
activities usually show two different non-oriented dis- and Ae. cinereus with an average dispersal range of
persal behaviours (Provost 1953), a drift with the less than half this distance.
22 2 Biology of Mosquitoes

In Germany, Oc. rusticus females have been found on mosquito palpi show responses to changes as small
resting in the forest during daytime and flying to the as 0.01% (Kellogg 1970). There are many other com-
forest edge and the adjoining fields with approaching ponents of host breath and odour which stimulate the
dusk. Females preferred to disperse along rows of trees antenna1 receptors of female mosquitoes when mixed
in open areas. It can be assumed that in the absence of with carbon dioxide. For instance, lactic acid is an acti-
other attractants or adverse meteorological conditions, vating and orientating stimulus for mosquitoes, but
the flight of these mosquitoes was guided by the only if carbon dioxide is also present in the air stream
reduced level of illumination beneath the forest can- (Smith et al. 1970; Price et al. 1979). Interaction or
opy, the contrast in illumination with the adjoining for- synergism of the components of the host odour in
est edge as well as the visual image of the rows of the attracting a given species is a very complex process
trees. The mosquitoes obviously follow their hosts, which developed in the course of evolution between
mostly red deer, when these animals browse in the the insect and the target organisms. The components of
meadows near the forest. The flight distance observed the host odour only stimulate the mosquito female
was only a few hundred meters (Schäfer et al. 1997). when they occur in a distinctive mixture typical of the
Dispersal serves mostly to bring these blood suck- host. This enables it to distinguish between different
ing insects into contact with a suitable signal from a hosts and to trace the plume as a series of packets,
potential host animal. It is likely therefore, that species lamellae and filaments of odour mixed and dispersed
which breed in areas where few hosts are available by wind (Murlis 1986). The female mosquito flies
develop a stronger tendency for migration than those upwind in a zigzag pattern which holds the mosquito
which breed in the vicinity of their hosts. For instance, within the plume and brings it closer to the odour
Cx. p. pipiens which breeds in human settlements source. In the final stages of orientation, mosquitoes
migrates usually less than 500 m. It is likely that especially those which bite during daytime or at twilight,
host-seeking females will find stimuli from a suitable use visual contact to locate the host. The compound
host within a few hundred meters. eyes serve to discriminate between form, movement,
In field studies, it was shown that both a horizontal light intensity, contrast and colour. Mosquitoes respond
and a vertical dispersal behaviour assists the host- particularly to blue, black and red colours, whereas least
seeking process. Females of Aedes spp. (Ae. vexans, attraction is caused by white and yellow (Lehane 1991).
Ae. rossicus, and Ae. cinereus) and Ochlerotatus spp. It is unlikely that the utilization of colour information is
(Oc. sticticus), were most frequently captured in traps well developed in mosquitoes active at night, but they
at ground level up to a height of 4 m whereas, at a may be particularly sensitive to intensity contrast between
height of 10 m, Cx. p. pipiens was by far the most the background and the target. When the mosquito is in
abundant (99.2%) species. There is an interaction close proximity of the host, it may also distinguish
between the availability of suitable hosts and the distri- between three-dimensional targets and infrared radiation
bution of mosquito species. For blood-seeking females may also be involved in host location.
of ornithophilic species (Cx. p. pipiens and Cs. morsi­ In the immediate vicinity of the host, odour is
tans), it is an advantage to search for birds in the can- important once again as well as body heat. Mosquitoes
opy. In contrast, the Aedes and Ochlerotatus species can easily detect temperature differences of 0.2°C.
prefer mammals as hosts, which explain the dominance Water vapour in short-range orientation-attraction may
of these species at ground level. also play a role (Lehane 1991).
After encountering the host stimuli, the female
mosquito changes its behaviour from the non-oriented
flight pattern to an oriented host location. Initially, the
mosquito is responsive to the host odour and then it 2.6.4 Feeding
uses this odour to track the host from a distance of
> 20 m. It is the release of carbon dioxide by the host, Mosquitoes have well-developed piercing/sucking
and the change in concentration of carbon dioxide in mouthparts. Males feed on plant juices as a source of
combination with other stimuli, which elicits behav- carbohydrates, the female mouthparts are developed
ioural responses. Mosquitoes are sensitive to very to pierce the skin of the host to obtain blood for
small changes in carbon dioxide levels. The receptors egg maturation (Magnarelli 1979; Clements 1992).
2.6 Adults 23

The mouthparts are extended into a proboscis which

consists of the stylet bundle (fascicle) enclosed by the
labium when the mosquito is not feeding. The stylet
bundle is formed of six long, thin stylets: the labro­
epipharynx, hypopharynx, and two of both maxillae
and mandibles. These stylets are held tightly together
by the labium. The mandibles are sharply pointed and
used to rupture the skin for passage of the other stylets.
The maxillae have a pointed tip and recurved teeth at
their distal ends. They are the main penetrative ele-
ments of the mouthparts, which are thrust alternately
by using the teeth to anchor themselves in the tissues.
Thus the labroepipharynx (food channel) and hypo-
pharynx (salivary channel) are penetrated together into
the tissue (Robinson 1939). The penetration of the sty- Fig. 2.12 Anopheles female ingesting blood (Photo courtesy
of Roger Eritja, Barcelona, Spain)
lets into the tissue is caused by an alternating rotary
movement of the head. Four muscles are associated
with each maxilla, to protract and retract the maxillary and ATP) function as phagostimulants, and the mosquito
stylets (Clements 1992). starts to take-in blood through the food channel.
After the females land on the host, they may probe The female mosquito can ingest more than three
the skin a few times with their labellae while they are times its mean body weight (Nayar and Sauerman
searching for a capillary for the intake of blood. 1975). Larger species such as Oc. cantans can ingest
Thickness and temperature of the skin are probably more than 6 µl and smaller species such as Ae.
important probing stimuli for mosquitoes, since the cinereus only 3.7 µl. The blood and especially its pro-
surface temperature of the skin is related to the num- tein ingredients are essential for egg-production by the
ber of blood vessels in the skin (Davis and Sokolove anautogenous females. Only a few autogenous species
1975). Sensilla on the ventral side of the pair of label- such as Cx. p. pipiens biotype molestus are able to pro-
lae and on the distal part of the labium contain recep- duce their first egg-batch without a bloodmeal (Weitzel
tors for stimuli that may indicate a suitable site for et al. 2009). When they originate from the eutrophic
piercing the skin. breeding sites (e.g. septic tanks) where the larvae can
Having successfully punctured the skin, the female develop a prominent fat body due to the high level of
starts ingesting blood. When feeding, only the stylet bun- nutrition, the fecundity is quite high, but still lower
dle penetrates the skin, while the labium becomes pro- than after a blood-meal by the female. The fat body is
gressively bent backwards as the mosquito probes deeper obviously enough to complete ovarial development
into the tissue. Two pumps, the cibarial pump below the without a further blood-meal. The blood is used more
clypeus and the pharyngeal pump, are the sucking organs for egg production and less as a source of energy. Both
which pump the blood or plant juices into the gut. sexes of mosquitoes require plant juices as an energy
It is important for the female mosquito that the source, mostly for flight. Plant sugars such as floral
blood remains in a liquid form to enable the mosquito nectar, damaged fruits and honeydew are the main
to complete the blood-meal. To prevent coagulation, the energy source during the adult life of both sexes
mosquito injects saliva into the wound which usually (Briegel and Kaiser 1973).
contains anticoagulants similar to hirudin produced by Mosquitoes differ in their feeding and resting
blood-sucking leeches (Parker and Mant 1979). The behaviour. Species which preferably feed indoors are
introduction of saliva into the host tissue usually stimu- called endophagic (endophagy), and those which feed
lates an immune response which can cause an inflamma- mainly outdoors, are called exophagic (exophagy). The
tory reaction of the host at the site of the wound. These females which rest outdoors after feeding or during the
wounds often cause irritation and the scratching by the day outdoors are called exophilic (exophily), and those
host can cause bacterial infection. When the stylets reach which rest indoors are called endophilic (endophily).
a blood vessel, blood-associated components (e.g. ADP Ornithophily is expressed when females prefer to feed
24 2 Biology of Mosquitoes

on birds (ornithophilic species), zoophily when they sites with a frozen surface. During the cold season,
feed on other animals (zoophilic species) and the term their metabolism is reduced and the larval develop-
anthropophily is used when they prefer to feed on ment is delayed. For instance, larvae of Oc. rusticus
humans (anthropophilic species). and Cs. morsitans, which hatched in autumn, hibernate
in the second and third larval instar. The high content
of dissolved oxygen in cold water or bubbles of oxy-
gen under the ice enable the larvae to cover their
2.7 S
 urvival During Dry Seasons
demand of oxygen for survival. However, during a
and Hibernation severe winter, the mortality rate can be very high.
Some anopheline species such as Anopheles claviger
In tropical areas, the dry season survival mechanisms and An. plumbeus hibernate as larvae in pools or tree-
of mosquitoes, such as Anopheles gambiae, is one of holes, respectively. Usually, hibernation takes place in
the most vexing deficiencies in the understanding of the third or fourth larval stage in water bodies that do
the biology of major malaria vectors. Two survival not entirely freeze or only for a short time. This is also
strategies could be observed: continuous reproduction true for the hibernating larvae of Or. pulcripalpis. In
throughout the year and embryo dormancy in moist contrast to the above-mentioned species, the larvae of
soil for at least several days (Minakawa et al. 2001). Coquillettidia richiardii, which usually hibernate in
Mosquitoes in temperate zones have developed effi- the third or fourth-instar are not sensitive to long frost
cient overwintering mechanisms in the egg, larval or periods, because they live submerged in permanent
adult stages. Some species such as Oc. rusticus and Cs. water bodies.
morsitans can overwinter in more than one stage, e.g. in Larvae of Cx. p. pipiens can frequently be found
the larval as well as the egg stage. Several factors, espe- during winter. Whereas the females of anautogenous,
cially the latitude (cold) and hydrological conditions ornithophilic, eurygamous Cx. p. pipiens are over-
(droughts) determine the duration of hibernation and wintering in diapause, its biotype molestus repro-
can differ within one species according to the latitude. duces during the winter. Therefore, all developing
stages of this biotype can be found in the breeding
habitat (usually underground breeding sites) within
2.7.1 Egg Stage the temperate zones during winter.

Hibernation in the egg-stage is practiced by most of

the Aedes/Ochlerotatus species in the temperate zone. 2.7.3 Adult Stage
Their diapause is induced in such a way that they do
not hatch when unsuitable climatic and hydrological
Most mosquito species (Culex, Culiseta, Uranotaenia
conditions prohibit successful development to the adult
and Anopheles) overwinter as adult females. They
stage (Sect. 2.3). The occurrence of larvae of these
seek hibernating shelters (locations free of frost such
species overwintering in the egg stage can vary greatly
as caves, stables, cellars, canals and earth burrows)
within the species of Aedes and Ochlerotatus. Within
during autumn and leave these sites in spring when
some species, the hatching time is closely related to
the temperatures increase. Usually, females of these
snow-melt, others hatch in late spring or summer.
species use the remaining larval fat body and feed
intensively on plant juices during autumn to synthe-
size huge lipid reserves for diapausing. Females of
2.7.2 Larval Stage some species within the Anopheles Maculipennis
Complex can take occasional blood-meals during
Some mosquitoes are known to overwinter in the lar- winter to withstand the long periods of starvation
val stage and can even survive for days in breeding (Clements 1992).
Chapter 3
Medical Importance of Mosquitoes

Mosquitoes are responsible for the transmission of 3.1 Malaria

many medically important pathogens and parasites
such as viruses, bacteria, protozoans, and nematodes, Human malaria caused by protozoans (Plasmodium spp.)
which cause serious diseases such as malaria, den- continues to be the most important vector-borne disease.
gue, yellow and Chikungunya fever, encephalitis or It affects more than 100 tropical countries, placing 3.3
filariasis (Kettle 1995; Beaty and Marquardt 1996; billion people (more than 40% of the world population)
Lehane 1991; Eldridge and Edman 2000). Transmission at risk as of 2006. The disease is responsible for no less
can be mechanical (e.g. Myxoma virus causing myxo- than 300 million infections and more than one million
matosis in rabbits) or biological. The latter is more deaths annually, mainly among children below the age of
complex because it involves an obligatory period of five, with more than 90% of them living in tropical Africa
replication and/or development of the pathogen or (WHO 1997b,c; 2008). The enormous loss of lives and
parasite in the vector insect. Due to their blood-sucking days of labour, the costs for treatment of patients, and the
behaviour, mosquitoes are able to acquire the pathogens negative impact of the disease on development, makes
or parasites from one vertebrate host and pass them to malaria a major socio–economic burden. The annual
another, if the mosquito’s ecology and physiology is costs of malaria in Africa alone were estimated to be
appropriate for transmission. Highly efficient vectors almost two billion US$ (WHO 1993, 2008).
have to be closely associated with the hosts and their At least four species of the genus Plasmodium
longevity has to be sufficient enough to enable the (P. falciparum, P. vivax, P. ovale and P. malariae) cause
pathogens/parasites to proliferate and/or to develop to human malaria and are transmitted solely by the anoph-
the infective stages in the vector. For successful trans- eline mosquitoes. There are more than 400 species of
mission, multiple blood-meals are necessary. Anopheles world-wide and of these about 40 species
In terms of morbidity and mortality caused by vec- are important vectors of human malaria. The most
tor-borne diseases, mosquitoes are the most danger- important vectors in Sub-Saharan Africa and the most
ous animals confronting mankind. They threaten more efficient malaria vectors world-wide belong to the
than three billion people, in the tropical and subtropi- Anopheles Gambiae Complex. Of the seven species of
cal regions and have also substantially influenced the this complex, An. gambiae s.s. and An. arabiensis
development of mankind, not only socio–economi- (species A and B) are the most serious vectors of
cally but also politically. Undoubtedly, insect-trans- P. falciparum (the most serious malarial pathogen) in
mitted pathogens leading to epidemics and pandemics Africa. Due to their anthropophilic behaviour and
have been instrumental in the development, decline, physiological feasibilities, they possess a higher vector
and fall of empires, for, e.g. Greece and Rome. Malaria capacity than other closely related sibling species with
was the dominant health problem in the latter days of no or low vector capacity. Apparently, pathogen/para-
the Roman Empire (Bruce-Chwatt and de Zulueta site and vector (mosquito) either adapted to each other
1980). The Roman marshes were notorious for “mala during the course of evolution, resulting in coexistence,
aria” (bad air). or the pathogen/parasite was repelled. This phenotypic

N. Becker et al., Mosquitoes and Their Control, 25

DOI 10.1007/978-3-540-92874-4_3, © Springer-Verlag Berlin Heidelberg 2010
26 3 Medical Importance of Mosquitoes

and genotypic plasticity exacerbates the difficulties in infected vertebrates containing sexual forms of the
the identification of vector populations and the imple- parasite, the gametes fuse in the mosquito gut to form
mentation of effective surveillance and control/man- a zygote which elongates and develops into a motile
agement strategies. However, new tools such as the ookinete (Fig. 3.2a). It penetrates to the outside of the
PCR-technique, enables scientists to use specific midgut epithelium, settles there and forms an oocyst
genetic markers to distinguish between sibling species (Fig. 3.2b). Meiotic and subsequent mitotic divisions
and in the investigations of defined populations. (sporogony) within the oocyst result in the formation
About 20 Plasmodium species occur in other pri- of many haploid, spindle-shaped sporozoites which
mates, a similar number in other mammals, and about burst the wall of the oocyst and migrate through the
40 each in birds and reptiles (Garnham 1980, 1988). haemocele and accumulate in the salivary glands
The Plasmodium species have a complex replica- (Fig. 3.2c–f). The infected mosquito is now able to
tion and transmission cycle with the sexual replication inject the sporozoites with saliva into the next host.
in mosquitoes and the asexual replication in vertebrates Once inside a vertebrate, the sporozoites infect the
(Fig. 3.1). Shortly after the ingestion of blood from parenchyma of the liver where they immediately

Fig. 3.1 Life cycle of malaria parasites in Anopheles and the human host
3.1 Malaria 27

Fig. 3.2 (a)–(d) (from a scanning electron microscope): (a) (arrow) and the other opened showing tens of sporozoites ready
Plasmodium ookinete (arrow) attached to the mosquito midgut to escape. (e, f) (from a transmission electron microscope): (e)
microvillar epithelium (Mv). The anterior part of the parasite is Initial phase of salivary gland invasion by sporozoites (10 days
already invading between the microvilli. (b) View of an infected after infection). The whole cytoplasm of the secretory cell is full
midgut (6 days after the infective bloodmeal). Several immature of sporozoites(s). (f) Late phase of salivary gland invasion (15
oocysts (arrows) are attached to the outer midgut wall. (c) Mature days after infection). All sporozoites are inside the secretory
oocyst releasing the sporozoites to the haemocele (10 days after cavities (sc) forming longitudinal arrangements (*). Some para-
infection). (d) Two broken oocysts in different phases (12 days of sites are in the salivary duct (N = nucleus). (Micrographs courtesy
infection). One oocyst at the beginning of sporozoite release of Paulo Pimenta, Fundacao Oswaldo Cruz, Brazil)

undergo a cycle of exoerythrocytic schizogony, or released into the circulating blood (end of the prepatent
develop to latent hypnozoites which sometimes later period), where they invade the erythrocytes to com-
undergo schizogony to cause relapse. In each large mence the erythrocytic schizogony. In the infected eryth-
schizont, several thousand merozoites are formed and rocyte, the merozoite becomes a feeding trophozoite
28 3 Medical Importance of Mosquitoes

and then, when a fully grown schizont, produces a nificantly enhance the protection afforded by existing
small number of new merozoites (Garnham 1966). The vector management strategies and consequent malaria
merozoites burst the erythrocytes, are released and reduction (Killeen et al. 2000a,b; Fillinger and Lindsay
then invade other erythrocytes to repeat the schizogonic 2006; Dongus et al. 2007; Walker and Lynch 2007;
cycle. Each release of the merozoites from the erythro- Worrall 2007).
cytes causes an attack of malaria with fever and other In Europe, malaria threatened human life until the
clinical signs. The length of the schizogonic cycle first half of the twentieth century. Although the impact
determines the interval between the fever attacks. of the disease was more severe in Southern Europe, it
P. falciparum causes malignant tertian, and P. vivax is well documented that even in Northern Europe,
and P. ovale benign tertian malaria recurring at 48 h malaria was a well-known hazard of life (Marchant
intervals (fever attack at the third day); and P. malariae et al. 1998). It is known that for instance, Napoleon
quartan malaria recurring at 72 h intervals (Kettle lost large numbers of soldiers due to malaria when he
1995). After several cycles of schizogony, some tro- invaded the Upper Rhine Valley in Germany. The two
phozoites do not produce merozoites but become main Plasmodium species found in Europe were P.
gametocytes which have to be ingested by anopheline vivax and P. falciparum. While the former occurred
mosquitoes to conclude the cycle of development. throughout the continent, the latter was restricted to
In humans, malignant malaria caused by P. falci­ Southern Europe (Jetten and Takken 1994). In Northern
parum, is the most severe form resulting in life-threat- Europe, the parasite must have been P. vivax because
ening complications such as anemia and cerebral of its adaptation to the moderate climate. Furthermore,
malaria. This is a frequent cause of mortality in chil- it is likely that the parasite could survive as hypnozo-
dren and can kill up to 25% of non-immune adults within ites in the human liver during phases too cold for mos-
2 weeks. This form of malaria is called Malaria tropica quito transmission (Marchant et al. 1998). Nowadays,
and occurs mostly in tropical and subtropical areas, P. vivax seldom causes a lethal disease, which suggests
being limited by a summer isotherm of 20°C which is that P. vivax has evolved into a reduced virulence over
necessary to complete the sporogony of the parasite in the the last century (Kettle 1995).
mosquito. In contrast, P. vivax can complete the sporog- Before World War II, endemic malaria was spread
ony and gametogony in mosquitoes in areas with a sum- throughout Europe (Bruce-Chwatt and de Zulueta
mer isotherm of 16°C (Wernsdorfer 1980). 1980). The most endemic malaria areas were found in
In the long battle against malaria, resource shortages, the south, where a continuous transmission occurred
absence of proper infrastructure, and lack of know­ledge from spring to autumn. Greece was considered to be the
and training as well as resistance to chloroquine, other country with the highest incidence of malaria. In the
antimalarial drugs, environmental constraints and use early 1930s, the number of people in Greece infected
of pesticides, have collectively impeded pro­gress in with malaria annually, ranged from one to two million.
malaria prevention and control especially in Africa for Other severe epidemics were reported from the
many years (WHO 2000, 2008; Etang et al. 2004; Dalmatian coast in Croatia, in coastal areas in Southern
Mukabana et al. 2006). The global campaigns against Spain, in the south of Italy and the island of Sardinia. In
malaria such as the Roll Back Malaria (RBM) pro- Central Europe, the malaria incidence was much lower
gramme led by major international organizations, aim than in the south (Jetten and Takken 1994). In Northern
to mitigate these long-standing shortcomings. Extending and Western Europe, the transmission of the disease was
facilities for rapid case detection and treatment, pro- discontinuous with annual maxima. Malaria epidemics
phylactics, personal protection based on the use of were mainly restricted to coastal areas in Southern
long-lasting insecticide-treated bednets (LLINs) against Sweden, Southern Finland, Denmark, the Netherlands,
adult vector-mosquitoes, indoor residual spraying Belgium, Germany and northern France. In the eastern
(IRS) and epidemic preparedness are cornerstones of parts of Europe, malaria was mainly recorded from
these current strategies in malaria vector control in Southern Ukraine and along the lower Volga River.
Africa and worldwide (Makundi et al. 2007; Mboera After World War II, malaria slowly disappeared from
et al. 2007; Protopopoff et al. 2007a,b; RBM 2005). the continent. This was mainly due to the reduction in
Control of vector-mosquito populations in their aquatic natural breeding habitats through improved agricultural
larval habitats offers an additional opportunity to sig- techniques, improved socio-economic conditions and
3.1 Malaria 29

better sanitation practices. An important role was also parts of Europe. An increase in temperature accelerates
played by the malaria eradication campaigns with the not only the development of mosquitoes in their breeding
application of residual insecticides and the availability sites, but also other phases of their life cycle, such as the
of new drugs. The last reported focus of indigenous frequency of blood meals, the duration of the gonotrophic
malaria in continental Europe disappeared in Greek cycle (time from a blood meal to the final development of
Macedonia in 1975 (Bruce-Chwatt et al. 1975). eggs) and their longevity. A reduction in the duration of
There are indications that malaria was mainly trans- the gonotrophic cycle increases the frequency of blood
mitted in Europe by the species of the Anopheles meals and, therefore, also the probability of transmitting
Maculipennis Complex, which are widely distributed in disease agents such as Plasmodium spp. (Dhiman et al.
the Palaearctic region. However, the distribution of 2008; Snow 1999; Becker 2008).
Anopheles maculipennis s.1., was not directly related to Increase in international travel has added to the
the distribution of malaria (Jetten and Takken 1994). complexity of this problem, not only infected people
What was the reason for the “Anophelism without import the parasite, infected anophelines can also be
malaria”? Following intensive research, it was estab- transported by aircraft from one continent to another.
lished that the former described species, An. maculipennis, These insects can become a threat for people working
is not a single species but a species complex consisting in or living close to international airports. Since 1963,
of more than a dozen separate species, of which eight more than 60 cases of “airport malaria” have been
occur in Europe (White 1978). The knowledge of reported in Europe. In 1994, in the vicinity of the
species complexes containing species that are morpho- Charles de Gaulle airport in Paris alone, seven people
logically very similar but differ greatly in their vector were infected by P. falciparum although they had never
competence, has generated interest in the control of visited the tropics. Similar cases have been reported
malaria by genetic manipulation (Crampton et al. 1990; from Gatwick Airport in London and Frankfurt
Crampton 1992; Crampton and Eggleston 1992; Kidwell International Airport in Germany.
and Ribeiro 1992; Carlson 1995; Rai 1995). In North America malaria was widespread, except
In addition to the species of the Anopheles in central areas up until the early twentieth century,
Maculipennis Complex, some other European anophelines with an estimated 600,000 cases occurring in 1914.
are known to be potential malaria vectors, such as The principal vectors were Anopheles freeborni
An. claviger; An. sergentii, An. cinereus hispaniola, (mainly in the Western USA) and An. quadrimaculatus
An. algeriensis, An. superpictus and An. plumbeus. The (mainly in eastern, central and southern areas). Both
latter is increasingly becoming interesting to malariolo- species are still widespread. P. vivax was the main
gists because in recent decades, it has pro­liferated in pathogen. Organised malaria control ­programmes were
huge numbers as a result of its adaptation from natural established in 1914 by the US Public Health Service,
(tree-holes) to artificial breeding sites (underground and then continued to be supported and organised by a
water catch basins and septic tanks contaminated with succession of other regional or national organizations
organic waste). In recent studies it has been demon- including the Tennessee Valley Authority, the National
strated that in contrast to An. atroparvus which is more Malaria Eradication Programme and Centers for
or less refractory to P. falciparum, An. plumbeus, is Disease Control and Prevention (CDC). Following
able to develop oocysts of P. falciparum when fed with intensive house-spraying with DDT in the post World
blood containing gametocytes (Marchant et al. 1998). War II years, indigenous malaria was eventually con-
Although An. plumbeus lives in close proximity to man, sidered eradicated in the USA in 1951.
the risk of malaria epidemics is very low due to good Since the 1970s, there has been an overall upward
malaria notification and the absence of cases of indig- trend in the number of malaria cases in the USA, with
enous transmission. However, the effect of global ~1,000–1,500 cases per year being reported in recent
warming which favours the completion of the sporogonic years. The majority are imported, i.e. the victim
cycle of Plasmodium in anophelines, and the hundreds acquired the disease whilst overseas. However, in addi-
of malaria cases mostly caused by P. falciparum tion, there have been 63 cases of locally transmitted
acquired in the tropics and imported to Europe, could malaria reported between 1957 and 2003, probably
increase the risk of some indigenous malaria ­transmission, arising from infection of indigenous mosquitoes by
even though malaria epidemics can be excluded in most imported malaria cases.
30 3 Medical Importance of Mosquitoes

In Central and South America, malaria has been a continent. The main vectors are An. gambiae s.s., An.
major problem despite recent advances, and still arabiensis and Anopheles funestus, with Anopheles
remains a significant threat. Across the region, a num- pharoensis also important in some areas. The Anopheles
ber of anopheline species are involved in transmission. Gambiae Complex contains some of the most efficient
An. albimanus is very widespread, occurring from the malaria vectors (anthropophilic and endophilic) and
southern states of the USA in the north, to Northern occur in both rural and urban areas.
Peru in the south, including the Caribbean region. It is P. falciparum remains the most important parasite,
a tropical lowland species, occurring most commonly with P. malariae and P. ovale also occurring. P. vivax
on coastal plains and along waterways. An. darlingi is is found in East and Southern Africa, but appears to be
also an important vector, found most commonly in for- absent from West Africa.
ested areas, and occurring from Mexico to Argentina, Asia spans a very wide range of regions, with great
and from the Atlantic to the Pacific coasts. Other spe- diversity of climate, habitat, and socio-economic status.
cies of importance include An. aquasalis, An. albitar­ Vector importance and parasite prevalence is similarly
sis, and An. pseudopunctipennis. varied. Important vectors in Western and Central Asia
P. vivax is the most common parasite in the Americas, include An. sacharovi, An. stephensi, An. culicifacies,
constituting around 75% of cases. Most of the rest is An. fluviatilis, and An. superpictus. In the tropical Far
caused by P. falciparum, with P. malariae also occur- East, a wide range of important species occur, includ-
ring in limited areas. Malaria control has faced a vari- ing An. dirus, An. sundaicus, An. minimus, An. farauti,
ety of challenges including insecticide resistance, and An. sinensis. This range occupies a broad range of
budgetary issues, the emergence of urban malaria, and habitats, from streams, rice fields, polluted urban water
human migration. Nonetheless, there has been a down- bodies, to rain forests.
ward trend in malaria cases from 1.1 million in 2,000, P. falciparum, P. malariae and P. vivax, all occur
to ~770,000 in 2007 (PAHO). in this continent, with the proportion of P. falciparum
In Australia, malaria formerly occurred sporadi- increasing in South East Asia (WHO 2000). The total
cally in the northern areas. A sudden outbreak of number of malaria cases in the South-East Asian
malaria caused by P. falciparum at Fitzroy Crossing region is ~2.5 million annually, with the majority
(Western Australia) in 1934 resulted in 165 deaths, but occurring in India, with ~4% of the world malaria
by 1981 the disease was declared eradicated. The mortality occurring in this region. The trend since
­vectors originally responsible for transmission are not 1996 has been a gradual decrease, although this may
known with certainty, but An. farauti was likely to not include fluctuations on a local scale. As in other
have been an important vector, with other species such parts of the world, military conflicts and human
as An. amictus, An. bancroftii and An. hilli also play- migration exacerbate malaria problems.
ing a role. The exact detail of the species responsible is
complicated by several of these species existing as
complexes. Currently, about 700–800 malaria cases
are imported annually, and a very few cases of locally
transmitted malaria also occur. 3.2 Arboviruses
Sub-Saharan Africa remains the most complex
and challenging malarious region. Political instabil- Arboviruses (arthropod-borne-viruses) are defined as
ity, military activity, uprooted human populations, viruses that replicate in arthropods and are transmitted
poverty and urbanization, collectively complicate by arthropods to vertebrates. The arthropod becomes
the situation. In some former malaria-free upland infected by feeding on blood from an infected verte-
areas in East Africa, cases are now being reported, brate during viraemia (virus circulation in the peripheral
which has been suggested as indicating a climate- blood vessels), and after proliferation in the vector, the
change effect. virus can be transmitted to another vertebrate-host
Across the African continent, 93% of the ­population (horizontal transmission). Arboviruses can also be
lives in areas with endemic malaria or in areas at risk of passed from one arthropod generation to another by
epidemics. There are about 270 million clinical cases transovarial transmission (vertical transmission).
annually, with 95% of the global malaria deaths in this Thus, some of these viruses are known to be capable of
3.2 Arboviruses 31

overwintering in the egg stage of the vector (e.g. a few comes from Swaheli, meaning “that which bends up”,
Aedini species). referring to the severe joint pain). The fever usually
More than 300 arboviruses are listed by Francki subsides after 2–3 days. Other symptoms like joint
et al. (1991) and more than 500 by Karabatsos (1985). pain can last for about a week. However, some severe
Approximately 100 viruses infect humans and 40 cases can require months of recovery, especially when
infect livestock (Monath 1988). The most important older people are infected. Although unusual, people
viruses transmitted by mosquitoes to humans or other above the age of 60 can die due to Chikungunya viral
vertebrates are found in three families: the Togaviridae infection induced complications.
with the genus Alphavirus (e.g. Chikungunya, Sindbis, Chikungunya virus is distributed in Africa and Asia
Equine Encephalitis and Ross River viruses), Flavi­ and in 2007, a few cases occurred in Europe (Italy)
viridae with the genus Flavivirus (e.g. Yellow fever for the first time. During epidemics, the African tiger
virus, Dengue 1–4 viruses, West Nile virus, Japanese mosquito Aedes aegypti [Stegomyia aegypti] and/or
and St. Louis encephalitis viruses) and the Bunyaviridae the Asian tiger mosquito Aedes albopictus [Stegomyia
with the genera Bunyavirus (e.g. the California group), albopicta] are the main vectors transmitting the dis-
and Phlebovirus (Rift Valley virus) (Murphy et al. ease from human to human. In Africa, nonhuman
1995; Eldrige and Edman 2000). Human arboviral primates (monkeys) are thought to serve as reservoir
diseases are classified by the major clinical symptoms hosts from which the virus can spread to humans.
they cause such as encephalitis, febrile illness accom- Mosquito species other than Aedes (Stegomyia) spp.
panied by rash and arthritis as well as haemorrhagic can be involved in the enzootic transmission.
fever. Infections can cause a wide range of mild or severe Chikungunya virus epidemics have recently drawn
symptoms with significant morbidity and mortality, a great amount of attention after there were sudden
especially in tropical countries. outbreaks in 2005 in Réunion (a French island), when
more than 300,000 people were infected, and again in
2006/2007 in India, when more than two million peo-
ple were infected with the Chikungunya virus. In
3.2.1 Togaviridae (Alphavirus) July–October 2007, the first epidemic of this tropical
disease broke out in Italy. One person travelling from
Within this family, only the members of the genus Kerala, India, to Italy developed symptoms of
Alphavirus are arthropod-borne. They replicate in the Chikungunya fever at the end of June. Subsequently,
cytoplasm of host cells. The genome is a single strand there were approximately 280 cases of Chikungunya
of positive sense RNA with 11–12 kb. After ­replication, fever in the Ravenna Province. The disease symp-
the nucleocapsids are released from the host cell form- toms include high fever, limb/muscle and joint pain.
ing an envelope when they push through the host cell Most of the time, the disease is relatively harmless,
membrane (Eldridge and Edman 2000). The viruses of and haemorrhaging ­seldom occurs. However, older
a size of 70 nm are most enzootic and infect mostly people are more prone to dying from this viral infec-
small mammals and birds. Humans are usually dead- tion. In the Ravenna region, an 83-year old man died
end hosts (exceptions Chikungunya and Ross River of this disease. As a result, it is now required to report
viruses) because they do not circulate enough viruses cases when haemorrhagy occurs. In addition, the lab-
to infect vector mosquitoes. Transovarial transmission oratories have to report these cases according to the
from one mosquito generation to the next can be European “Prevention of Infection Regulations”
possible. (ECDC 2008).
Chikungunya virus was detected in Ae. albopictus
females, indicating that the newly introduced exotic
3.2.1.1 Chikungunya Virus pathogens which led to this epidemic, were transmit-
ted by the Asian tiger mosquito which was introduced
Chikungunya viral infections in humans result after an in Italy in 1990. The degree to which indigenous
incubation time of 2–4 days with a sudden onset of ill- mosquitoes (other than the newcomer, Asian tiger
ness, fever, chills, headache, photophobia, arthralgia mosquito) can act as vectors for the Chikungunya
and arthritis affecting multiple joints (“Chikungunya” virus, and whether the viruses can be passed on by
32 3 Medical Importance of Mosquitoes

transovarial transmission during egg development, is to mammalian populations including humans (Morris
now being examined. 1988).
In horses, symptoms occur 1–3 weeks after infection
and begin with high fever which usually lasts for 1–2
3.2.1.2 Ross River Virus days. During the fever period, nervous signs such as sen-
sitivity to sound and restlessness and periods of excite-
Ross River virus is endemic in Australia, Papua New ment and restlessness appear. Brain lesions appear
Guinea and neighbouring islands. Although not fatal, causing drowsiness, drooping ears, circling and abnor-
infections are debilitating, causing fever, rash and poly- mal gait. The horse usually suffers complete paralysis
arthritis. Joint pain can last for weeks or even years and death 2–4 days after symptoms appear. Mortality
thus reducing productivity of people and harming the rates among horses with the eastern strain range from 70
economy (Mckenzie and Smith 1996). The virus was to 90% and 50–90% among infected humans.
first isolated from Ae. vigilax, but a wide range of mos-
quito species including Ae. aegypti [St. aegypti], Ae.
polynesiensis [St. polynesiensis], and Ma. uniformis
show a high degree of vector competence (Kay and 3.2.1.4 W
 estern Equine Encephalomyelitis
Aaskov 1988). Thus a further spread of the virus is not (WEE) Virus
unlikely.
The virus was first isolated from passerine birds, WEE occurs in North, Central and South America, but
but mammals like kangaroos and wallabies are consid- most cases have been reported from the plains of the
ered as major reservoir hosts for enzootic transmission. western and central United States. In the complex life
Stegomyia species may transmit the virus from human cycle, mainly birds, small mammals are also involved.
to human (Eldridge and Edman 2000). Important vectors are Cx. tarsalis (western half of North
America), but Oc. dorsalis or Oc. albifasciatus
(Argentina) may also be involved. In 1930 and 1958, the
3.2.1.3 E
 astern Equine Encephalomyelitis largest outbreaks occurred in California when 6,000
(EEE) Virus horses and almost 1,000 human cases were involved
(Reeves 1990). Clinical cases of horses are often fatal,
EEE virus is present in North, Central and South but compared to EEE virus infections the mortality rate
America and the Caribbean. EEE was first recognised is low (3–15%). The WEE virus is comprised of six sero-
in Massachusetts, USA in 1831, when 75 horses died of types which vary in their virulence. In humans, infec-
encephalitic illness. Epizootics in horses have contin- tions can cause a range of illness from no symptoms to
ued to occur regularly in the United States. The virus headache and fever, to aseptic ­meningitis to encephalitis.
was first isolated from infected horse brains in 1933 People with more severe disease can have sudden high
(Giltner and Shahan 1933). In 1938, the first confirmed fever, headache, drowsiness, ­irritability, nausea, and
human cases were identified when 30 children died vomiting, followed by confusion, weakness, and coma.
of encephalitis in northeastern USA. These cases Infants often suffer seizures. Symptoms usually appear
coincided with outbreaks in horses in the same regions. in 5–10 days after the bite of an infected mosquito.
The fatality rate in humans was 35% and there is
currently no cure for human infections (Scott and
Weaver 1989). 3.2.1.5 V
 enezuelan Equine Encephalomyelitis
EEE virus is capable of infecting a wide range of (VEE) Virus
vertebrates including mammals, birds, reptiles and
amphibians. The virus is maintained in nature through VEE affects equine species such as horses, donkeys
a bird-mosquito cycle. The ornithophilic mosquitoes, and zebras, which are also the amplifying vertebrate
Culiseta melanura and Cs. morsitans are primarily host for epizootic virus transmission. However, small
involved as vectors. Several species, Cq. perturbans, rodents and in some locations birds may be involved in
Ae. vexans, Oc. sollicitans and Oc. canadensis are the transmission cycles. After infection, equines may
bridge vectors which transmit the viruses from avian suddenly die or show progressive central nervous
3.2 Arboviruses 33

system disorders. Healthy human adults who become Antibodies of Sindbis virus have been detected in birds
infected by the virus may experience influenza-like of several orders, e.g. Passeriformes, Galliformes,
symptoms. However, people with weakened immune Anseriformes and Ciconiiformes and also in domestic
systems, children or older people in rare cases, become and wild mammals, e.g. in bovids, in several European
severely ill or die. The incubation period from the countries (Lundström 1999). Additionally, Sindbis
inoculation of the virus until the febrile response gen- viruses were isolated from hamsters and frogs as well
erally is 0.5–5 days. as from sentinel chickens and rabbits (Gresikova et al.
In 1936, VEE was first recognised as a disease of 1973; Kozuch et al. 1978; Aspöck 1996).
concern in Venezuela following a major outbreak of In humans, Sindbis virus infections have resulted in
equine encephalomyelitis. From 1936 to 1968, equines hundreds of clinical cases in Northern Europe, espe-
in several South American countries, suffered devas- cially in Sweden, Finland, Russia and Norway
tating outbreaks. In the following years, the disease (Lundström et al. 1991). The disease results in a rash,
moved north throughout Central America reaching as well as pain in muscles and joints with joint swell-
Mexico and Texas in 1971. Outbreaks are usually ing and fever (Espmark and Niklasson 1984).
related to an increase in mosquito populations. Several In Europe, Sindbis virus was isolated for the first
mosquito species are involved in the transmission time in Sweden in 1984 from Culiseta spp. (Niklasson
cycle including the species of Aedes, Ochlerotatus et al. 1984) and later from Cx. p. pipiens and/or Cx.
(e.g. Oc. taeniorhynchus), Anopheles, Culex, Deino­ torrentium, Cs. morsitans and Ae. cinereus (Francy et al.
cerites, Mansonia, and Psorophora. 1989) as well as from mosquitoes in Russia, Norway
and Germany (Lvov et al. 1984; Norder et al. 1996;
Jöst et al. 2010). The virus circulates in bird populations
during the summer and is transmitted by the ornitho-
3.2.1.6 O’Nyong-Nyong (ONN) Virus philic mosquitoes Cx. p. pipiens and/or Cx. torrentium
(Lundström 1994). In contrast to these Culex species,
ONN virus occurs only in Africa and is closely related Aedes/Ochlerotatus species such as Ae. cinereus, are
to the Chikungunya virus. The name is derived from a less specific concerning host choice. They bite birds as
Ugandan dialect and refers to joints being weak. The well as humans and are thus able to transmit the virus
symptoms are similar to those of Chikungunya infec- infection into the human population (Aspöck 1996;
tions. An. funestus and An. gambiae s.s. are the most Lundström 1999). In Europe, outbreaks of Sindbis dis-
important vectors. ONN virus infection in vertebrates eases occur usually in July and August and disappear at
other than humans has not been reported (Eldridge and the end of autumn. The initiation of Sindbis virus trans-
Edman 2000). mission in summer is not fully understood, the virus
may either overwinter in the mosquito vectors or in the
bird hosts. Reinfections can be caused each year by
3.2.1.7 The Sindbis Virus Complex infected birds migrating from Africa.

In 1952, the Sindbis virus was first isolated from

Culex mosquitoes in the Egyptian village called 3.2.1.8 Viruses of the Semliki Forest Complex
Sindbis, near Cairo. It is known from Europe, Africa,
Asia and Australia. The first human case occurred in Semliki Forest virus was first isolated from Uganda in
Uganda 1961. 1944. Nine viruses of this complex occur in the Old
Four viruses of the Sindbis complex (Sindbis/sub- World (Strauss and Strauss 1994). In Western Europe,
types Ockelbo, Whataroa, Babanki, and Kyzylagach the only record of human disease possibly caused by a
viruses) are widely spread in the Old World (Strauss virus of the Semliki Forest complex is from Albania
and Strauss 1994). In terms of the nucleotide sequences, (Eltari et al. 1987; Lundström 1999). The viruses could
European strains are more or less identical with the possibly occur in humans and other mammals (e.g.
strains in Africa and it can be assumed that they were bovids and ovids) at low frequencies. Clinical cases
transported by birds migrating between the two conti- have not been reported from Western Europe. Although
nents (Shirako et al. 1991; Norder et al. 1996). antibodies have been detected in a number of birds
34 3 Medical Importance of Mosquitoes

(e.g. Ardea cinerea, Acrocephalus spp., Remiz pendu­ Asia, most probably due to the immunologic cross-
linus) and viruses have been isolated from Ochlerotatus protection by the exposure of humans to other related
euedes in central Russia (Mitchell et al. 1993), these viruses or reduced vector efficiency (Eldridge and
viruses may be considered as minor epidemiological Edman 2000).
importance in Europe. After the bite of an infected mosquito, the virus first
replicates locally and then spreads to the rest of the
body via the lymphatic system and establishes itself
throughout organ systems, including the heart, kid-
3.2.2 Flaviviridae (Flavivirus) neys, adrenal glands and the parenchyma of the liver;
high viral loads are also present in the blood. The incu-
The Flaviviridae gets its name from the Yellow fever bation period in humans ranges from 3 to 5 days until
virus (flavus in Latin means “yellow”). The Flaviviridae the victims develop malaise, nausea, fever, chills,
contain some of the most dangerous arboviruses in the vomiting, constipation, rapid heartbeat, back pain, and
world such as Yellow fever virus, Dengue virus, West prostration. Due to liver malfunction, jaundice usually
Nile virus, Japanese encephalitis virus, St. Louis appears on day 2 or 3 after the first signs of the disease.
encephalitis virus, Murray Valley encephalitis virus Patients develop haemorrhagic symptoms, liver and
and Rocio virus. All belong to the genus Flavivirus renal failure and lapse into delirium and coma, fre-
and are transmitted by mosquitoes. quently followed by death. The fatality rate is higher
The enveloped spherical Flaviviridae with a diam- than 50% in patients developing jaundice (Eldridge
eter of 40–60 nm contain a single-stranded positive and Edman 2000).
sense RNA. Numerous vertebrates, especially primates are sus-
ceptible to the virus which enables the virus to persist
in enzootic cycles. Two distinct transmission cycles
3.2.2.1 Yellow Fever Virus can be distinguished:

Yellow fever is historically the most important and (a) The jungle or sylvan cycle in tropical America
dangerous mosquito-borne disease and still an impor- and Africa. Mostly monkeys are the principle
tant cause of haemorrhagic illness in many African verte­brate hosts infected mainly by Haemagogus
and South American countries despite the existence of mosquitoes in the forest canopy in tropical
an effective vaccine. The attribute “yellow” refers to America or by Ae. africanus in Africa. In gallery
the jaundice symptoms that affect some patients. forests or savannahs in Africa, vectors of the yellow
Devastating epidemics of yellow fever broke out in the fever can be Ae. (Stegomyia) bromeliae (East and
1700s in England, France and Spain. In the nineteenth Central Africa) or Ae. vittatus in West Africa.
century, more than 300,000 people are believed to have Humans entering the forests for searching for food
died in Spain. Until the early part of the twentieth cen- or harvesting wood are infected by mosquito bites
tury, in regions of North and Central America, Caribbean and carry the virus to human settlements.
and Europe, the spread of Ae. aegypti [St. aegypti] (b) The urban cycle which begins when infected humans
caused severe yellow fever epidemics. In 1900, the returning to their villages or cities where Ae. aegypti
research of Carlos Finlay, Walter Reed and colleagues carries the virus from human to human and eventu-
proved the role of Ae. aegypti in the transmission ally result in epidemics.
cycle of Yellow fever virus which initiated preventive Mass vaccination and vector control programmes in
efforts against the vector and spread of the disease. In human settlements can reduce the burden of yellow
1927, the Yellow fever virus was isolated by Adrian fever (Norrby 2007).
Strokes in West-Africa (Sosa 1989; Staples and Monath
2008). However, despite all efforts, the disease still
remains as a threat to humans in Africa and Central/
South America. As of 2001, the World Health 3.2.2.2 Dengue Virus
Organization (WHO) estimates that yellow fever
causes 200,000 illnesses and 30,000 deaths every year Dengue is a mosquito-borne disease caused by four
in unvaccinated populations. Yellow fever is absent in serotypes of the Dengue virus (DEN-1, DEN-2, DEN-3
3.2 Arboviruses 35

and DEN-4). The illness usually begins 5–7 days after and subtropical regions around the world, predomi-
the infective bite (intrinsic incubation period). The nantly in urban and semiurban areas. The global inci-
clinical features of dengue include fever with rash, dence of dengue and DHF has grown dramatically in
severe headache, pain behind the eyes, muscle and joint recent decades especially with the dramatic increase in
pains (myalgias and arthralgias – severe pain gives it international travel. Some 2.5 billion people (40%) of
the name “break-bone fever”). The dengue rash usually the world’s population – in more than 100 countries in
appears first on the lower limbs and the chest; in some Africa, Asia, the Western Pacific region, the Caribbean,
patients, it spreads over most of the body. There may as well as Central and South America and the Eastern
also be gastritis with a combination of associated Mediterranean, live under the risk of Dengue virus
abdominal pain, nausea, vomiting, or diarrhoea. infection (Halstead 1980, 1982, 1992; Becker et al.
Recovery from infection by one serotype provides 1991; Gratz 1999; WHO 2008). In 2007 alone, there
lifelong immunity against that virus but confers only were more than 890,000 reported cases of dengue in
partial and transient protection against subsequent infec- the Americas, of which 26,000 cases were DHF. WHO
tion by the other three serotypes. There is good evidence currently estimates that annually there may be 50 mil-
that sequential infection with different serotypes lion dengue infections worldwide. An estimated
increases the risk of developing dengue haemorrhagic 500,000 people with DHF require hospitalization each
fever (DHF). The infection with one serotype initiates year, a high proportion being children. The case fatal-
the production of different antibodies neutralizing the ity rate is about 2.5%.
viruses of this serotype and antibodies which are not In Europe, one of the most recent outbreaks of den-
able to neutralize viruses of another serotype acquired gue occurred in Athens during 1927 and 1928, when
by a second infective bite. The virus of that serotype can the dengue viruses caused a devastating epidemic of
proliferate in the epithelial cells of blood vessels and fever and polyarthritis. Approximately one million
make them permeable for blood serum which enters the people (80% of the inhabitants at that time) were
body tissue and cause haemorrhagic manifestations. infected with more than 1,500 fatalities (Papaevangelou
The blood pressure of the patient sinks dramatically. and Halstead 1977). Dengue cases also occurred in
DHF is a potentially deadly complication that is Spain, Italy, Austria (Vienna had a large epidemic in
characterized by high fever and haemorrhagic mani- 1941) and the former Yugoslavia. In Europe, especially
festations, often with enlargement of the liver and in in countries bordering the Mediterranean Sea, people
severe cases, circulatory failure. The illness begins may still suffer from this disease.
with a sudden rise in temperature accompanied by Ae. aegypti (primary vector in urban areas) and
facial flush, other flu-like symptoms and sometimes Ae. albopictus (secondary vector in suburban/rural
convulsions. The high fever usually continues for 2–7 areas) are the vectors of dengue. The mosquitoes
days. After a few days of high fever the patient’s con- acquire the dengue virus while feeding on an infected
dition can suddenly deteriorate, the temperature drops, person. After virus incubation for 8–10 days (extrinsic
followed by the circulatory failure and the patient can incubation period), the infected mosquito is capable of
rapidly go into a critical state of shock and die within transmitting the virus during a blood meal for the rest
12–24 h, or may quickly recover following appropriate of its life. Infected female mosquitoes may also transmit
medical treatment. the virus to their offspring by transovarial transmis-
The first reported epidemics of dengue fever sion, but the role of this in sustaining transmission of
occurred in 1779–1780 in Asia, Africa and North the virus to humans has not yet been defined.
America. It indicates that these viruses and their mos- Infected humans are the main amplifiers of the
quito vectors have had a worldwide distribution in the virus, serving as a source of the virus for uninfected
tropics for more than 200 years. During most of this mosquitoes. The virus circulates in the blood of the
time, dengue fever was a mild, nonfatal disease until the infected human during the fever period for 2–7 days.
1950s when DHF cases first occurred during dengue Aedes (Stegomyia) females acquire the virus when they
epidemics in the Philippines and Thailand. Today DHF feed on an individual during this period.
has become a leading cause of hospitalization and death The spread of dengue is not only attributed to the
among children in regions with dengue epidemics. expanding geographic distribution of the four Dengue
Dengue and DHF have become a major interna- viruses, but also to their mosquito vectors. Ae. aegypti
tional public health concern and is found in tropical populations increase especially in areas that are
36 3 Medical Importance of Mosquitoes

favourable for mosquito breeding, e.g. where house- an outbreak in Israel in 1957. Equine disease was
hold water storage in containers is common and first noted in Egypt and France in the early 1960s
where solid waste disposal services are inadequate. (Kunz 1969; Aspöck 1979; Filipe 1990; Vesenjak
Increased global travel by airplane provides the ideal et al. 1991).
mechanisms for infected humans transporting Dengue West Nile virus circulates usually in birds with
viruses between regions, countries or even continents, Cx. p. pipiens being the most likely enzootic vector
resulting in a frequent exchange of Dengue viruses (Mouchet et al. 1970). In Europe, virus isolates
and other pathogens. The exposure to various sero- are known from Cx, p. pipiens in the city of
types of the Dengue virus is usually followed by DHF Bucharest, Culex modestus in southern France
outbreaks. (Hannoun et al. 1964), from An. maculipennis s.1.
There is no specific treatment for dengue (no vaccine in Portugal (Filipe 1972) and from Oc. cantans in
is available currently), but appropriate medical care fre- former Czechoslovakia (Labuda et al. 1974).
quently saves the lives of patients with the more serious Obviously virus amplification can occur in a wide
dengue haemorrhagic fever. The best preventive mea- range of birds (e.g. Passeriformes, chickens, ducks,
sures include intensive public education emphasizing geese and pigeons). There is strong evidence that
the elimination/reduction of the breeding sites of Ae. the West Nile virus may have been sporadically
aegypti improved water supply systems (e.g. potable introduced from Africa to Europe by migrating
water supply), overhead tanks/cisterns should be mos- birds. The virus is transmitted in a bird–mosquito
quito-proofed, containers should be covered with tight- cycle in endemic areas in Europe.
fitting lids or screens to avoid egg laying by mosquitoes. Humans and other mammals are infected when
The use of larvicides or predators such as copepods suitable mosquito bridge vectors (mosquitoes biting
can also reduce the vector population. birds and humans like Cx. p. pipiens biotype molestus
and Culex p. quinquefasciatus) are abundant. However,
the possibility of transovarial transmission, with the
3.2.2.3 West Nile Virus virus surviving the winter in hibernating Culex females
in Europe cannot be excluded, as transovarial trans-
West Nile virus was first isolated from a human in the mission has been demonstrated in the laboratory by
West Nile district of Uganda in 1937 and later from Baqar et al. (1993).
many other vertebrate hosts including horses, dogs, Following infection, it takes 3–6 days until the
rodents and bats (Eldridge and Edman 2000). West symptoms of the disease occur, e.g. malaise with fever,
Nile virus is widely distributed and the virus has been headache and muscle pain, sore throat, rash and swol-
described in Africa, Europe, the Middle East, West and len lymph nodes (Lundström 1999). The disease usu-
Central Asia, Oceania, and most recently, North ally lasts for about 1 week. In most endemic areas it is
America. The ecology was characterized in Egypt in a childhood disease, as adults have acquired immunity
the 1950s. Work et al. (1953), isolated WNV from (Manson-Bahr and Bell 1987; Tesh 1990). However,
Hooded Crows and Rock Pigeons in the Nile Delta. severe cases of meningoencephalitis, myocarditis,
Later, in 1955, Work et al. postulated that the indige- acute pancreatitis and hepatitis are reported, which can
nous wild birds are potential reservoirs of WNV in the be fatal. In 1935, 1942 and the early 1960s outbreaks
Nile Delta. Outbreaks of WNV encephalitis in humans occurred in the Camargue (Southern France) with
have occurred in Algeria in 1994, Romania in 1996– benign to fatal encephalitis symptoms (Panthier et al.
1997, the Czech Republic in 1997, the Democratic 1968). More recently, West Nile fever epidemics were
Republic of the Congo in 1998, Russia in 1999, the reported from southeastern Romania (the Danube
United States from 1999 and Israel in 2000. Epizootics plains and the city of Bucharest) with 393 acute human
of disease in horses occurred in Morocco in 1996, Italy cases and a case fatality rate of 4.3% in 1996 (17
in 1998, in the United States from 1999 until the pres- deaths). In 1997, 14 cases with two deaths occurred
ent, and France in 2000 and in birds in Israel in 1997– between July and the end of September (Ceianu, pers.
2001 (Zgomba and Petric 2008). comm.). In Europe virus isolates are known from
The virus became recognised as a cause of severe France, Portugal, former Czechoslovakia and Romania.
human meningitis or encephalitis (inflammation of Serological surveys have revealed antibodies in human
the spinal cord and brain) in elderly patients during sera from Albania, Austria, Germany, Greece, Italy,
3.2 Arboviruses 37

Poland, Spain and former Yugoslavia (Hubalek and encephalitis, Inkoo, La Crosse encephalitis, Tahyna,
Halouzka 1999; Lundström 1999; Hrnjakovic- Snowshoe hare, Trivittatus and Jamestown Canyon
Cvjetkovic et al. 2006). In addition to humans, West viruses, the Bunyamwera complex including the
Nile virus has also been isolated from horses with Bunyamwera, Batai and Cache Valley viruses, and the
encephalomyelitis in France, Italy and Portugal Turlock group including the Lednice virus only in
(Jourbert et al. 1970; Filipe 1972; Cantile et al. 2000). Europe (Lundström 1999; Eldridge and Edman
Antibodies have been detected in other domestic mam- 2000).
mals, e.g. bovids as well as in wild mammals, e.g.
mice, bats and even in the water snake, Natrix natrix
(Aspöck 1996). 3.2.3.1 The California Serogroup
The outbreak of West Nile fever in North America
is remarkable. West Nile fever first appeared on this Viruses of the California group need mammals as
continent in New York in the summer of 1999 when 62 amplification hosts (Lundström 1994, 1999; Aspöck
cases and seven fatalities were recorded. During the 1996). Antibodies have been detected in wild and
next 5 years, it spread across the country. In 2003, domestic mammals such as hares, rabbits, bovids,
9,862 cases and 264 fatalities were recorded in 46 cervids (reindeer), and in carnivores as well as in
States. Since that time West Nile fever occurred regu- hedgehogs (Erinaceus europaeus). Humans are also
larly in more than 40 States with thousands of infected susceptible, infection of this serogroup in humans
people and fatality rates of 2.7–4.1% (CDC 2008). include mild infections to severe CNS diseases such as
In the USA West Nile virus has dramatically reduced encephalitis or involvement of the respiratory system.
populations of several common bird species, including From the public health point of view, the La Crosse (in
robins (Turdus migratorius), chickadees (Parus atri­ North America) and the Tahyna virus (in Europe) are
capillus) and especially crows (Corvus brachyrhyn­ the most important viruses (Calisher and Karabatsos
chos) which have declined in some regions by 50%. 1988; Lundström 1999, Eldridge and Edman 2000).
Sixty two mosquito species belonging to a wide range
of genera have been found positive for West Nile virus
in the United States since 1999 (Reisen et al. 2004). California Encephalitis Virus
Besides mosquitoes, West Nile virus has also been iso-
lated from ticks. The role of ticks in the transmission This virus was first detected from Ae. melanimon
cycle of the virus is not understood so far (Eldridge mosquitoes from the Central Valley in California and
and Edman 2000). later from Oc. dorsalis from Utah (Reeves 1990; Smart
et al. 1972). Antibodies of the virus have been isolated
from many mammals such as raccoons, skunks, oppos-
sums and woodrats. Infected humans may develop
3.2.3 Bunyaviridae (Bunyavirus) encephalitis.

Bunyaviridae are vector-borne viruses with the excep-

tion of Hantaviruses, which are transmitted through Inkoo Virus
aerosol contact with mice feces. There are five genera
currently recognised in the family. In addition to top- The Inkoo virus is circulating widely in Northern
soviruses, which mainly infect plants, Bunyavirus, Europe. Although discovered 40 years ago little is
Hantavirus, Nairovirus and Phlebovirus, infect ani- known about the disease associations and immune
mals. Only the genus Bunyavirus includes the viruses response in humans (Putkuri et al. 2007).
which are transmitted by mosquitoes to humans
(exception Rift Valley fever, a Phlebovirus, which
can also be transmitted by mosquitoes). The genome La Crosse Encephalitis Virus
consists of a negative-stranded RNA with three
segments. La Crosse virus is another important arbovirus in
Three groups of bunyaviruses have been recorded, North America (following West Nile and St. Louis
namely the California group including the California virus). It causes febrile illnesses accompanied by fever,
38 3 Medical Importance of Mosquitoes

h­ eadache, vomiting, nausea, lethargy and coma. The have been from snowpool mosquitoes. The virus can
virus is perpetuated in an enzootic cycle involving mos- be transmitted transovarially and may also persist in
quitoes such as the tree-hole mosquito Oc. triseriatus cold weather. Disease in humans takes the form of
and small mammals such as squirrels. The virus can be infection and inflammation of the brain such as menin-
transmitted transovarially by mosquitoes (Watts gitis and encephalitis (Fauvel et al. 1980). Some cases
et al. 1973). Approximately 70 cases are reported each of clinical illness due to SSH virus probably go unrec-
year. ognised. However, it appears that infection is much
more common than the disease itself.

Tahyna Virus
Trivittatus Virus
The Tahyna virus is widespread in Europe and Asia
and also detected in Africa (Traavik et al. 1978; Aspöck This virus occurs in North America and can cause
1979; Pilaski and Mackenstein 1985; Danielova 1992; disease with CNS symptoms. Antibodies have been
Lundström 1994; Eldridge and Edman 2000). Infected found in rabbits, squirrels, opossums and raccoons.
people develop influenza-like symptoms which can The vectors are Oc. trivittatus and Oc. infirmatus, other
lead to morbidity. It has frequently been isolated from species belonging to the genera Culex and Anopheles
Ae. vexans, but also from other species such as Ae. may be involved (Pinger et al. 1975).
cinereus, Oc. sticticus, Oc. cantans, Oc. flavescens,
Oc. caspius, Cs. annulata, Cx. modestus, Cq. richiar­
dii (Lundström 1994; Aspöck 1996) and even in biting Jamestown Canyon Virus
midges Culicoides spp. (Ceratopogonidae) (Halouzka
et al. 1991). Danielova and Ryba (1979) proved in This virus has been involved in a few cases of human
experiments that the virus can be transmitted trans­ disease including encephalitis. Besides humans, large
ovarially in Ae. vexans. Therefore, it can be assumed mammals such as deer and other cervids and domestic
that the virus overwinters within the eggs and with the livestock can be infected. Snowpool mosquitoes such
mass development of Ae. vexans after spring floods, the as Oc. tahoensis and Oc. punctor are the primary vec-
virus circulation starts again. Virus overwintering in tors (Eldridge and Edman 2000).
females of Culiseta spp. and Culex spp. seems to be of
minor importance (Chippaux et al. 1970). Antibodies have
been detected in many mammals, such as rabbits, wild
3.2.3.2 The Bunyamwera Complex
boars, deer, cattle, swine and foxes. They serve as reser-
voirs for the virus and do not develop signs of illness.
Bunyamwera Virus

This virus occurs in Africa where it was first isolated

Snowshoe Hare Virus in mosquitoes from Uganda. Infected humans develop
a febrile illness, including headache and anthralgia.
Snowshoe hare (SSH) virus has been reported from the Besides humans, the virus has been found in a wide
northwestern USA, Alaska and Canada. As the name variety of mammals, including goats, sheep and rats
suggests, the Snowshoe Hare (Lepus americanus) is (Eldridge and Edman 2000).
thought to be an important host, but evidence of infec-
tion has been found in many wild species such as
rodents, carnivores, ungulates as well as in domestic Batai Virus
species – chickens, dogs, horses and cattle. Many dif-
ferent species of mosquitoes can become infected and The Batai virus (strain: Calovo virus) is mainly trans-
transmit the virus. These include many species of the mitted by An. maculipennis s.1. (Bardos and Cupkova
genera Ochlerotatus and Aedes as well as the species 1962). However, some isolates have also been obtained
of Culiseta and of Culex. Most isolations of this virus from An. claviger, Cq. richiardii and Oc. communis
3.3 Filariasis 39

(Francy et al. 1989; Traavik et al. 1985). It can be 905 million people are directly exposed to the infection
assumed that the virus overwinters in hibernating transmitted by various genera of mosquitoes, the most
anopheline females. Following infection, humans can important being Cx. p. quinquefasciatus and Mansonia
develop febrile disease with bronchopneumonia, spp. (Eldridge and Edman 2000). One-third of the peo-
catarrh and gastritis (Sluka 1969). However in Europe, ple infected with the disease live in India, one third are
Batai virus antibodies are usually found in less than in Africa and most of the remainder are in South Asia,
1% of the human population (Lundström 1999). Bovids the Pacific and the Americas. In tropical and subtropical
are often infected with Batai virus. Antibodies have areas where lymphatic filariasis is well-established, the
also been detected in pigs and deer; birds are not prevalence of infection is continuing to increase. A pri-
important for the virus circulation. This virus has been mary cause of this increase is the rapid and unplanned
reported from several European countries, e.g. Finland, growth of cities which result in break-down in environ-
Sweden, Germany, Austria, former Czechoslovakia mental sanitation which usually creates numerous breed-
and Yugoslavia (Lundström 1999). ing sites for the mosquitoes that transmit the disease.
Lymphatic filariasis is thought to have affected
humans for approximately 4,000 years. Artifacts from
Cache Valley Virus ancient Egypt (2,000 B.C.) and the Nok civilization in
West Africa (500 B.C.) show possible “elephantiasis”
Cache Valley virus may be responsible for defects in symptoms. The first clear reference to the disease
human and animal foetuses as well as for a human case appears in ancient Greek literature, where scholars dif-
of haemorrhagic disease in the USA. The virus has ferentiated the often similar symptoms of lymphatic
been isolated in many mosquito species belonging to filariasis from those of leprosy.
the genera Culiseta, Aedes, Ochlerotatus, Psorophora Human filarial nematode worms have a complicated
and Anopheles. life cycle, which primarily consists of five stages.
Following mating, the female worm produces millions
of microfilariae measuring 244–296 µm by about 10 µm.
3.2.3.3 The Turlock Group They are sheathed and have usually nocturnal periodic-
ity which is an adaptation to the biting habit of the vec-
Lednice Virus tor. The microfilariae migrate into lymph and enter the
blood stream reaching the peripheral blood. A mos-
The Lednice virus has been isolated from Cx. modes­ quito ingests the microfilariae during a blood meal.
tus. It is likely that the virus is transmitted vertically in After ingestion, the microfilariae lose their sheaths and
the Culex population. Only rarely are vertebrates, penetrate through the wall of the proventriculus and
mainly birds, infected (Aspöck 1996; Lundström cardiac portion of the midgut to reach the thoracic mus-
1999). Antibodies have never been found in humans cles of the mosquito. There, the microfilariae develop
or wild mammals, except in two hares (Wojta and into second-stage larvae and subsequently into third-
Aspöck 1982), so the Lednice virus seems to be of no stage larvae. This usually takes 7–21 days. The third-
epidemiological importance. stage larvae migrate through the haemocoel to the
proboscis of the mosquito, ready to enter the punctured
skin following the mosquito bite (Fig. 3.3). During the
next months, up to a year, the larvae moult through two
3.3 Filariasis more stages, maturing into to the adult worm that com-
monly reside in the lymphatic system of humans. They
In the tropics, lymphatic filarial diseases affect an esti- live for 4–6 years, producing millions of immature
mated 120 million people in 80 countries throughout the microfilariae that circulate in the blood.
tropics and subtropics of Asia, Africa, the Western Most of the symptoms of filariasis are caused as a
Pacific, and parts of the Caribbean and South America. consequence of the adult worms living in the lymph
Most of the infections, about 90%, are caused by system in the network of nodes and vessels that main-
Wuchereria bancrofti. In Asia, the disease can also be tain the delicate fluid balance between the tissues and
caused by Brugia malayi and B. timori. An estimated blood and are an essential component for the body’s
40 3 Medical Importance of Mosquitoes

In Europe, filariasis is of no medical importance.

The dog heartworm, Dirofilaria immitis (Oncho­
cercidae) causes canine cardiovascular dirofilariasis in
dogs and other canids, but rarely cats (Boreham and
Atwell 1988). Infection in humans is asymptomatic
because the worm does not mature in humans. The adult
worms are 12–31 cm in length. Usually they are found
in the heart (hence heartworm) and the pulmonary artery
of the host. Infected animals can suffer from cardiac
insufficiency and heart failure. Mature female worms
release microfilariae into the blood. They exhibit a noc-
turnal periodicity and circulate in the peripheral blood
vessels, an adaptation to the biting habit of the potential
mosquito vectors. Lok (1988) listed 26 species of mos-
quitoes, incriminated on the basis of field or laboratory
Fig. 3.3 Worm larvae penetrating into the host skin
studies, as vectors of D. immitis. Most vectors are found
in the genera Aedes/Ochlerotatus, Anopheles and Culex
(Eldridge and Edman 2000). When ingested by a mos-
immune defence system. Tissue damage caused by quito, the microfilariae penetrate the gut epithelium and
the worms restricts the normal flow of lymph fluid. enter the Malpighian tubes where a certain percentage
The disease usually is not life threatening, but it can grow and moult to the infective third larval stage within
permanently damage the lymph system and kidneys. about 2 weeks, under favourable temperate climatic
Because the lymph system does not function cor- conditions. The infective larvae migrate to the mosquito
rectly, fluid collects and causes swelling in arms, mouthparts and enter the labium from which they
breasts, legs, and in the genital area of males. The penetrate into the host skin when the mosquito is biting
name for this swelling is lymphedema. The entire leg, (Fig. 3.3). The development to the adult worms in the
arm, or genital area may swell several times its nor- heart and pulmonary artery of the vertebrate host takes
mal size (hence the name “elephantiasis”). Also, the several months, and after more than 6 months microfi-
swelling and the decreased function of the lymph sys- lariae are produced again. In addition, other dog-
tem make it difficult for the body of the victim to infecting filarioids are Dipetalonema spp. or Mansonella
fight germs and infections. This causes hardening and spp. which have a similar biology as D. immitis (Aranda
thickening of the skin referred to as “elephantiasis”. et al. 1998).
Some of the symptoms are caused by the body’s D. repens, the causative agent of the canine cutane-
immune response to the parasite, but most are the ous dirofilariosis is endemic in large parts of Southern
result of bacterial infection of the skin where normal and Eastern Europe, however, increasing numbers of
defences have been partially lost due to underlying autochthonous cases in dogs have been reported in
lymphatic damage. Careful cleaning can be extremely recent years from northern countries including Germany
helpful in healing the infected surface areas in both (Pantchev et al. 2009).
slowing and even more remarkably, reversing much
of the overt damage that has occurred already. The
symptoms usually appear 5–18 months after the
3.4 F
 uture Perspectives
infectious mosquito bite.
The psychological and social stigma associated and Conclusions
with the aspects of this disease, are immense. Because
of its prevalence often in remote rural areas, on the one In conclusion, the family Culicidae has had, and con-
hand, and in disfavoured periurban and urban areas, on tinues to have, a more negative impact on human well-
the other, lymphatic filariasis is primarily a disease of being, health and socio-economic development, than
the poor. any other group of animals.
3.4 Future Perspectives and Conclusions 41

There are many examples from history, where many individual countries, the urban population now
endemic or epidemic insect-borne disease have affected exceeds 80%. Where the rate of urbanization exceeds the
the pattern of human settlement, changed the outcome of rate at which services and infrastructure can be estab-
military campaigns, or simply acted as a drain on the rate lished, there is the risk of allowing pest species, partic-
of development. Even in the early years of the twenty- ularly mosquitoes, to become established. Improper
first century, as shown in this chapter, despite at least water storage and disposal, whether in residential areas
a century of determined scientific and technological or on construction sites, and the operation of small
advance, the impact of mosquito-borne disease continues. farms within urban areas tend to create opportunities
Approximately 30% of the world’s human population for mosquitoes. Mosquito control in urban areas brings
still lives with the threat of insect-borne disease. very different challenges from those encountered in rural
In some areas, the numbers of people at risk of communities.
disease has actually increased, as a result of the vec- Overall, the outlook for mosquito-borne disease
tor and/or pathogen expanding or consolidating its is not positive. In recent decades, there appears to
range. Such changes may take place as a result of have been more bad news than good. The need for
trade or movement of people, or in changes to the good medical entomologists is as strong as it ever
environment itself. was. Changing environmental conditions creates the
In some cases, the movement of pathogens from one danger of novel host–virus interactions that may lead
geographical region to another has resulted in the spread to potentially disastrous results in the future. To con-
of diseases. The introduction of West Nile virus into the clude, it can be stated that the risk for the reintroduc-
USA for the first time, in 1999, possibly on an infected tion and transmission of mosquito-borne diseases
pet bird, allowed indigenous mosquitoes and birds to has and will increase rapidly, due to the increased
become infected. This enabled the disease to spread populations, lack of proper housing, poverty and
rapidly (within 5 years from the East Coast to the West mobility of humans, the international trade and the
Coast) across the continent, placing another 0.5 billion changing climate.
people at risk (Reisen et al. 2004). The very recent intro- The trade with used tyres and possibly “lucky bam-
duction of Chikun­gunya virus into Northern Italy, prob- boo” (Dracaena spp.) is responsible for the introduc-
ably on a single infected person, brought the virus and tion of Ae. albopictus into most parts of Europe. The
previously introduced vector, Ae. albopictus, into con- introduction of Ae. albopictus and Oc. j. japonicus,
tact, resulting in the first known European outbreak of into the United States under similar circumstances, is
this disease. another well established fact. Ae. albopictus was
Alternatively, increases in the incidence of insect- found for the first time in the continental United
borne disease may take place as a result of a decline of States in used tyres and retrograde cargo returning
the effectiveness of control programmes, perhaps through from Asian ports (Pratt et al. 1946; Eads 1972). The
insecticide resistance or through political changes. first record of establishment of this species in the
Military conflict, through its displacement of human continental US was reported by Sprenger and
populations, and its damage to infrastructure and abject Wuithiranyagool (1986), when a large population
poverty often results in outbreaks of mosquito-borne dis- was discovered breeding in used tyres (shipped from
eases. Those living in refugee camps are particularly at Japan) in Houston, Texas. Within a short period
risk. Changes in political structures, such as the disman- (1985–1999), widespread infestations of Ae. albopic­
tling of the Soviet Union in the 1990s, can also create tus were reported from 28 states east of the Mississippi
opportunities for mosquito populations to develop in the River (Moore 1999). More recently, this species was
absence of monitoring or control programmes, resulting introduced for the first time on the west coast of
in a resurgence of malaria in some territories. the United States, into California in June 2001.
For rural communities, the city has often appeared as Developmental stages and adult specimens were dis-
place of opportunity. The human drift into towns and covered in shipments of Dracaena sp. plants pack-
cities has been taking place for millennia, and it is aged in standing water, arriving in refrigerated
now estimated that for the first time, the proportion of maritime containers at the Los Angeles and Long
the human population living in cities exceeded 50%. In Beach Harbours. Ae. albopictus as a container breeder
42 3 Medical Importance of Mosquitoes

has adapted very well to breeding in such manmade These are just a few examples of mosquito
containers (Madon et al. 2002). vectors and their capability of readily adapting to
Oc. j. japonicus is another exotic species which was different environmental and climatic conditions.
recently introduced into the United States and in Europe Increase in international travel and global commodi-
(Schaffner and Chouin 2003; Eritja et al. 2005; Peyton ties, increased urbanization, change of climate with
et al. 1999). The most likely mode of introduction of Oc. increasing temperatures and unusual heavy rainfalls
j. japonicus may have been via used tyres exported to the may lead to an extension of the range of mosquito
United States. This subspecies prefers to breed in a vari- vectors and mosquito-borne diseases and contribute
ety of natural as well as artificial containers. It is a day- to the complexity of occurrences in world-wide
time biter and is known to readily bite humans. vector-borne disease.
Chapter 4
Mosquito Research Techniques

Basic knowledge about the distribution, abundance, ing techniques to be employed, depending on the
seasonality, and ecology of different mosquito species species and habitat.
is essential for a successful control campaign against
these insects. For example, knowledge of the popula-
tion dynamics and migration behaviour of the target
organisms are crucial to the design of a control strategy. 4.1.1 Anopheles Eggs
In parasitological and epidemiological studies, the
interaction between the parasite or pathogen, and the
vector and host, must be evaluated in order to suppress Anopheles females lay their eggs on the water surface
mosquito-borne diseases successfully. In the initial where they float due to air-filled chambers formed
phases of all mosquito control campaigns, detailed from the outer layer of the egg, the exochorion. Often,
entomological studies are likely to be carried out. In the eggs group themselves into net-like structures until
this chapter, the most important methods of mosquito the larvae hatch. Less than 2 mm in size, the eggs are
research are presented. A complete review of mosquito hardly recognizable with the naked eye. Eggs can be
sampling techniques and the analysis of collected data sampled from the water surface using a light-coloured
is given by Silver (2008). dipper. However, a dipper whose bottom surface has
been cut out and replaced with a fine wire mesh is pre-
ferred. This modification allows the dipper to be pulled
through the water, skimming the surface and thus col-
4.1 Sampling Mosquito Eggs lecting the eggs from the surface. The mesh is then
washed with water into a light-coloured plastic dish,
where the eggs can be collected with a pipette. In the
Mosquitoes lay their eggs singly or in egg rafts in many
absence of a dipper, a metal ring (10 cm diameter) with
different habitats, such as swamps, marshes or pools,
a nylon mesh stretched across the surface can be also
as well as in a great variety of small, natural, and arti-
used. A wooden handle may be attached for easier use
ficial water collections, such as tree-holes, rock pools
(WHO 1975).
or man-made containers. Some females lay their eggs
on the water surface, whereas others lay them onto the
moist soil at the breeding site, on the edge of the water
or on the wall of natural or artificial containers. The
determination of egg densities in natural habitats pro- 4.1.2 Egg Rafts
vides not only a better understanding of the egg-laying
behaviour of the various mosquito species, but can also Species of the genera Culex, Uranotaenia, Coquil­
aid in predicting future larval populations and possible lettidia, and subgenus Culiseta of the genus Culiseta
control areas. lay their eggs in rafts on the water surface. With a size
The range of egg-laying behaviour and of the physi- of several millimeters, the egg rafts can be easily seen
cal characteristics of the eggs require various collect- and sampled by fine forceps, pipettes, or small nets.

N. Becker et al., Mosquitoes and Their Control, 43

DOI 10.1007/978-3-540-92874-4_4, © Springer-Verlag Berlin Heidelberg 2010
44 4 Mosquito Research Techniques

4.1.3 Aedes/Ochlerotatus Eggs at a temperature which aids the hatching of the larvae
(~20°C). It is recommended to use water with an ini-
Aedes and Ochlerotatus females lay their tiny eggs into tially high oxygen content. The decrease in oxygen
the moist substrate of the breeding sites. It is extremely caused by the metabolism of the microbes in the soil
difficult to recognise the eggs in situ even with the help stimulates the hatching of the larvae. Ascorbic acid, or
of a magnifying lens, therefore, soil samples from the yeast and sugar, can be added for further reduction of
breeding sites have to be taken. For the determination oxygen to increase the hatching stimulus. The hatched
of the egg density the so-called “flooding method” or larvae can be collected a day or two after flooding,
the “saltwater method” can be employed. For the esti- counted, and identified after being reared to the fourth
mation of the number of eggs per surface unit, it is larval instar or adult stage. Because of sequential
important to standardize the soil samples (Becker hatching (batches of larvae hatch during consecutive
1989b; Silver 2008). For this purpose, a metal frame of flooding), samples with high egg densities should be
angle iron (20 × 20 × 2.5 cm) is suitable. The frame can repeatedly flooded. The standing water must be
be driven into the ground with a hammer until the decanted so that the soil can dry out until the next
angled side is flush with the ground surface. Using a flooding procedure takes place. The alternate flooding
trowel, the soil along the bottom of the frame can be and drying raises the hatching stimulus of the eggs that
cut horizontally to a depth of 2.5 cm. The soil sample remain in the soil. Even after several floodings, larvae
can then be carefully transferred to a plastic bag, and will still continue to hatch.
labeled with the location and date of sampling. In this As the Aedes/Ochlerotatus larvae may be in diapause
manner, the Aedes/Ochlerotatus eggs should remain in and therefore unable to hatch even when suitable hatch-
their natural state. ing conditions are provided, it is important to interrupt
Females prefer particular sites for egg deposition. It the diapause and so condition the larvae for hatching,
is known that the moisture and quality of the soil, or before the samples are treated. For instance, when eggs
the plant associations, which indicate a special flood- of Aedes vexans are sampled during winter, the samples
ing sequence or degree of soil moisture, are important must be stored for at least 2 weeks at temperatures above
factors in determining where the female mosquito lays 20°C, so that larvae are able to hatch. The higher the dif-
her eggs. This usually results in a heterogeneous distri- ference between the low and high temperature, the
bution of eggs. In order to secure the necessary data higher is the response to the hatching stimulus.
from the different zones, it is therefore recommended In contrast to the flooding method, the “saltwater
to take the samples in transects, to determine the varia- method”, described by Horsfall (1956b), is less time
tion in egg densities in a potential breeding site. Along consuming and ensures close to 90% recovery rate of
the bank of a breeding site, samples should be taken at the eggs. The principle behind this method is that the
equal distances beginning at the deepest point, and density of an aqueous solution is increased by adding
continuing to the upper margin of the breeding site. salt, thereby causing the eggs with a density lower than
This ensures that the areas with the highest densities of the saline solution, to float to the surface.
Aedes/Ochlerotatus eggs will be recorded. Often the If the soil samples are taken from the field during
highest numbers of eggs are laid in bands around pools summer, the samples should be stored at 5°C for at
subject to fluctuations in water level. The bands indi- least 2 weeks to prevent the larvae (e.g. Ae. vexans)
cate the zones above the water edge with a high con- from hatching. To wash the eggs out of the soil, the
tent of moisture during the time of mass oviposition by sample should be placed in a tub and flooded with cold
the gravid females. Until processing, the soil samples water (below 10°C). The cold water further reduces
should be stored out of the sun to avoid drying of the the hatching stimulus. The flooded sample should be
soil and damage to the eggs. If the samples are kept for carefully and uniformly mixed, and lighter particles
several days or weeks, the soil should be regularly (leaves, wood) can be removed from the surface of the
moistened. water (Butterworth 1979). The water and the finer, sus-
When the “flooding method” is applied to calculate pended particles in the water have to be carefully
the relative egg density of a certain breeding site, the decanted. This procedure should be repeated several
standardized soil samples should be flooded with water times. Then salt (sodium chloride) is added to the
4.1 Sampling Mosquito Eggs 45

water, until a 100% saturated salt solution has been hole in the plastic jar above the water line prevents water
achieved and the salt crystals no longer dissolve. This overflow during heavy rainfall. Usually the females of
solution has a higher density than the eggs. By Ae. albopictus and Ae. aegypti lay their eggs just above
thoroughly mixing the sample, the eggs rise to the sur- the water line on the rough side of the strip. At regular
face, where they can be collected by means of a pipette intervals (once a week) the strips are changed and the
or with a filter paper and counted. The eggs can be water replaced. The number of eggs can be counted on
determined either by rearing the larvae, or in some the strips using a dissecting microscope.
species the specific pattern of the egg shell (chorion) Plastic buckets, wash tubes or other receptacles con-
can also be used for species determination. taining several liters of infusion of hay, brewer’s yeast,
Another method for collecting the eggs is the use of dog biscuit, alfalfa or sewage water can be used as ovipo-
a sequence of meshes with a decreasing mesh-size to sition traps for Culex p. pipiens and Cx.
separate the eggs from the soil. p. quinquefasciatus (Yasuno et al. 1973; Sharma et al.
Due to the similar egg-laying behaviour and physical 1976; Leiser and Beier 1982; Reiter 1983, 1986; O’Meara
properties of the eggs of the subgenus Culicella within et al. 1989; Becker 1989b). The Culex mosquitoes are
the genus Culiseta, the same methods can be employed. apparently attracted by gaseous compounds such as
ammonia, methane, or carbon dioxide, which are released
when organic material decomposes in the water. Fatty
acids and n-capric acid are also oviposition attractants
4.1.4 Eggs in Artificial Oviposition Sites for females of Cx. p. pipiens. In order to study the egg-
laying behaviour, or the population density of the Culex
Mosquito species have preferred breeding habitats, mosquitoes, egg rafts can be sampled at regular intervals.
which can differ greatly in abiotic and biotic factors, It can be assumed that in human settlements with limited
such as water quality, light intensity, available food or numbers of natural breeding sites, the Culex population
vegetation. The knowledge of the critical factors in the may be effectively reduced by destroying the egg rafts
choice of a breeding site by a certain mosquito species sampled in oviposition traps at regular intervals. In addi-
allows the construction of artificial oviposition sites or tion to attractants, an insect growth regulator (IGR) may
traps. Oviposition traps (ovitraps) can be useful tools be added to the water in the oviposition traps to prevent
in surveillance programmes for certain mosquito spe- the development of adult mosquitoes, or to sterilize them.
cies, such as mosquitoes breeding in artificial contain- Gravid female mosquitoes in search of oviposition
ers, tree-holes or rock-pools. sites may be sampled using a gravid trap first devel-
In survey programmes Aedes albopictus [St. albopicta] oped by Reiter (1983). The attractive component of a
and Aedes aegypti [St. aegypti] are monitored mainly by gravid trap consists of an open-topped container of a
means of ovitraps (Fay and Eliason 1966; Pratt and water-based infusion (Fig. 4.1). Situated just above
Jakob 1967; Jakob and Brevier 1969a,b; Evans and
Brevier 1969; Thaggard and Eliason 1969; Chadee and
Corbet 1987, 1990; Freier and Francy 1991; Service
1993; Bellini et al. 1996; Reiter and Nathan 2001).
Population levels of both species can be determined
by using a sufficient number of ovitraps in a certain area
(Mogi et al. 1990; Bellini et al. 1996). Commonly used
ovitraps consist of a dark plastic or glass jar which is
painted black on the outside, about 8 cm in diameter at
the top and 5 cm at the bottom, with a height of 12.5 cm.
When the ovitraps are placed in the field, a strip of hard-
board or masonite (2 × 12 cm) with a smooth and a rough
surface is attached vertically with a paper clip to the
inside of the jar so that the rough side is facing towards
the center of the jar (Service 1993).Then, approximately
200 ml of dechlorinated tap water is poured in. A small Fig. 4.1 Gravid trap
46 4 Mosquito Research Techniques

the surface of the water is an updraft collection port,

leading into a collection container, connected to an
extract fan. Gravid females active on the infusion sur-
face are sucked up the port and held in the collection
container. The infusion used is typically prepared by
soaking hay in water for several days, but the attrac-
tiveness of other types of infusions has been deter-
mined (Burkett-Cadena and Mullen 2008; Jackson
et al. 2005). Gravid traps are typically used to monitor
Culex mosquitoes (Tsai et al. 1989), but may also be
successfully used to monitor Oc. j. japonicus (Scott et
al. 2001). In terms of their trapping efficiency com-
pared to light traps, gravid traps appear particularly Fig. 4.2 Assessment of larval densities by using a standard
useful against Culex quinquefasciatus (DiMenna pint dipper
et al. 2006).

ber of various larval instars and pupae per dip

should be separately recorded. By calculating the
4.2 S
 ampling Mosquito Larvae
volume of water inhabited by larvae, a rough esti-
and Pupae mation of the aquatic mosquito population can be
made (Papierok et al. 1975; Croset et al. 1976;
Many sampling techniques are used to assess the Mogi 1978). Silver (2008) suggests more precise
population of the aquatic stages of mosquitoes. methods for population estimates based on data
They are especially employed to study the popula- evaluation by regression statistics. In large habitats,
tion dynamics of mosquitoes, or to estimate popula- a plankton net attached to a handle can be used to
tion densities pre- and post-larvicidal application. catch a relatively large number of larvae within a
Although mosquito larvae occur in a wide range of short time. The net should be drawn through the
habitats, some simple techniques can be employed water in a figure-eight pattern to sample the larvae.
for the assessment of the larval population. The In small collections of water such as tree-holes,
most commonly used tool is the dipper, which may sampling can be difficult. Larvae can be pipetted
vary in size and shape. Soup ladles, white plastic or directly from the surface or can be collected by
enamel bowls or photographic trays with a capacity siphoning out the water.
of a few hundred milliliters to 1 liter are inexpen- A sufficient number of larvae/pupae have to be
sive and easily used tools for collecting larvae. For transported to the laboratory alive for species determi-
comparative purposes it is recommended to use nation, or alternatively fourth-instar larvae can be pre-
standardized dippers. In most programmes the served in 70% ethanol in the field. In the larval stage
“standard pint dipper” is used, consisting of a white only fourth-instar larvae are suitable for species deter-
plastic container measuring 11 cm in diameter and mination. Earlier instars have to be reared to the fourth-
with a capacity of 350 ml (Dixon and Brust 1972; instar or adult stage. For transportation to the laboratory,
Lemenager et al. 1986). The white background aids a glass or plastic container with a close-fitting cap
accurate counting of larvae. A wooden handle is should be 3/4 filled with water from the site. The lar-
attached to the dipper to reach water bodies from a vae can be pipetted into the container, or the contents
distance, and to avoid disturbing the water, which of a dipper or net catches can be released into the con-
causes larvae to dive during sampling (Fig. 4.2). tainer. The containers must be marked carefully record-
According to the size of the surface of the larval ing the date and location of sampling.
habitat, a sufficient number of dips have to be taken In the laboratory, larvae can be killed by hot water
to estimate the number of developmental stages. In (60°C) and transferred into preserving media for fur-
larger ponds (>20 m2) 10–20 samples along the ther handling. Alternatively the larvae can be identi-
edges and in the center should be taken. The num- fied at the fourth-instar, or reared to the adult stage in a
4.3 Sampling Adult Mosquitoes in the Field 47

mosquito breeder for confirmation of the larval identi- a vehicle, with the large open end pointing forwards.
fication (see rearing of mosquitoes). The funnel leads into a small collecting container. The
In Ae. aegypti control programmes, whether vehicle is driven through the area to be sampled, ideally
intended for the control of yellow fever, dengue or on a fixed route and at a steady speed, and at intervals
DHF, several standardized larval assessment ­indices the vehicle is stopped and the insects removed from the
have been established. The House Index is the per- collecting container (Tsai et al. 1989). This trap is also
centage of houses in which larvae or pupae are suited to establishing mosquito flight times.
found, while the Container Index is the percentage
of water-holding containers, that contain active
immature stages (Connor and Monroe 1923). 4.3.1.2 Electrocution Traps
Subsequently the Breteau Index was established
and used, defined as the number of positive con- Gilles et al. (1978) developed an electrified wire grid
tainers per 100 houses (Breteau 1954). However, that killed and collected mosquitoes that blundered
none of these indices takes account of the numbers into it from various directions. The grid was placed
of insects in each container. More recently, Focks between breeding sites and the villages in which the
and Chadee (1997) proposed that counts of pupae, mosquitoes obtained blood meals, and the catches of
and calculations of pupae/person were more mean- mosquitoes moving to and from these locations, were
ingful figures in terms of assessing the risk of dis- related to meteorological conditions. More recently
ease transmission. electrified nets have also been used to catch mosqui-
toes attracted to various host odours (Torr et al. 2008).

4.3 S
 ampling Adult Mosquitoes
in the Field 4.3.2 A
 dult Mosquito–Outdoor Resting
Catches
A very wide variety of sampling techniques for adult
mosquitoes are available, such as direct human bait Many mosquito species rest outdoors, either in vege­
catches (HBC), netting, collecting with aspirators, suc- tation or in natural openings or crevices. Those
tion or attractant traps, e.g. containing carbon dioxide resting in holes may be sampled by the construction
(CO2 traps). Several factors such as the weather condi- of pit shelters. These typically consist of a ca. 1.5 m
tions, activity pattern, host-seeking and resting behaviour, square hole dug into the ground (water-table permit-
as well as the physiological stages of the mosquito, will ting), and a smaller horizontal hole then dug into
determine the composition of the catch in terms of the each vertical face of the pit. At intervals the collec-
species and the sexes. Here, only the more commonly tor enters the pit (beware of wildlife, e.g. snakes)
used techniques will be discussed. Silver (2008) pro- and with the aid of a torch and aspirator, collects the
vides more detailed information. mosquitoes resting in the horizontal holes (Bhatt
et al. 1989).
Adult mosquitoes resting in vegetation may be sam-
4.3.1 Sampling Flying Mosquitoes pled with a sweep net (Holck and Meek 1991), or
directly with an aspirator.
Traps that sample mosquitoes, without relying on the
mosquito to actively orientate towards a potential host
4.3.3 Adult Mosquito–Indoor Catches
or other attractant, are relatively few.

The natural host seeking, movement, and resting

4.3.1.1 Truck Traps behaviour of mosquitoes in and around buildings, may
be assessed by a range of techniques. In addition, these
Truck traps are used to sample mosquitoes in flight. techniques may also be used to assess the changes
They consist of a funnel-shaped net fixed to the roof of resulting from insecticide treatment.
48 4 Mosquito Research Techniques

Mosquitoes resting inside buildings may be collected et al. 1977; McIver 1982; Takken and Kline 1989;
by use of a torch and aspirator. Typically such assess- Takken 1991; Lehane 1991; Becker et al. 1995b, Petric
ments are carried out in the morning, as there may be a et al. 1995). A traditional method of assessing the adult
progressive departure of mosquitoes over the day, or population is to count females landing on a human, and
predation by ants or geckos. Alternatively, the indoor to express the number of females per unit of time. The
resting mosquitoes may be collected by spreading a catch can be performed in hourly or bi-hourly intervals
white sheet on the floor of the selected room, and then over a 24-h period to assess the activity pattern of the
treating the room with a non-residual pyrethrin spray. female mosquitoes in relation to abiotic factors such as
The dead and knocked-down mosquitoes may then be temperature, relative humidity, light intensity or wind
collected from the sheet a few minutes later (Magbity speed. For instance, the biting activity of many mosqui-
et al. 1997). However, frequent use of pyrethrins in a toes is often highest during sunset, when the tempera-
particular room may result in changes in mosquito rest- ture is still high and the humidity is increasing.
ing behaviour in that room. Depending on the number of mosquitoes, the col-
Entry and exit of mosquitoes from buildings may be lector might expose only a part of the body (leg or arm)
assessed using traps fitted over existing window open- or the whole body, to collect the mosquitoes with an
ings. Depending on the orientation of the trap, these aspirator. Widely used aspirators consist of a clear
collect mosquitoes either entering or leaving the build- plastic tube, which can be fitted with a two-hole ­stopper
ing. Typically, these consist of a net-covered funnel to hold the intake and exhaust tubes, made from flexi-
fitted over the window, leading into a holding cage. ble clear plastic (Fig. 4.3b). The top of the intake tube
Depending on the study, the mosquitoes may be should hold a small funnel to aid the sampling of land-
removed in the morning and/or evening. Siting traps ing mosquitoes, and the exhaust tube should be pro-
over windows with overhanging roof eaves, may pro- tected with a fine-mesh nylon net to limit inhalation of
vide protection from direct sunlight, or rain (Magbity undesirable material. The plastic tubes can be removed
et al. 1997). and capped by snap-on caps. Mosquitoes can be killed
Instead of using existing buildings, to which the by placing a small piece of cotton wool absorbed with
behaviour of mosquitoes will differ, due to differences a very small quantity of a killing agent (e.g. ethyl ace-
in design, location and use of the buildings, standard- tate), into the tube (ensure that the tube material is
ized experimental huts may be built and used instead unaffected by the killing agent). If plugs of cotton wool
(WHO 2006). These typically consist of a small one- or paper strips are added to the tube, movement of the
room building, which may be occupied by people or dead, fragile mosquitoes and loss of scales can be
animals, and which may be fitted with window and avoided.
verandah traps. The hut may be built on a raised plinth, A simple aspirator can be easily constructed by
incorporating an ant barrier, to reduce predation of joining two flexible plastic tubes with slight differ-
mosquitoes. Indoor resting collection, and pyrethrin ences in diameters, so that they fit snugly within each
spray collections may also be carried out, depending other. A nylon net fixed between the joined tubes
on the programme.

4.3.4 Bait Catches

The bait or host for a blood-meal (e.g. humans or ani-

mals) emit olfactory stimuli or kairomones, which are
attractants for the host-seeking mosquitoes. Female
mosquitoes respond to compounds such as carbon
dioxide from the exhaled breath, host odour (e.g. lactic
acid) emanating from sweat, water vapour, body heat and Fig. 4.3 Simple (a) and chamber aspirator (b) for collecting
vision aided by the movement of the host (Bar-Zeev adult mosquitoes
4.3 Sampling Adult Mosquitoes in the Field 49

prevents the inhalation of mosquitoes by the collector collecting resting mosquitoes from inside an animal
(Fig. 4.3a). The catch can then be blown into a separate shelter (Kanojia et al. 2003).
killing chamber.
The use of a drop-net is advisable when the number
of mosquitoes is excessive (Fig. 4.4). The trap consists 4.3.5 Adult Mosquito Traps
of a bell-shaped net with three metal hoops which can
be fixed on a branch of a tree just above the collector.
It is known that mosquito species respond differently to
The two lower hoops have a diameter of 1 m with cords
various kairomones and to individual attractiveness of
fixed on the hoops which the collector can pull the
the collectors, resulting in variations in catch sizes and
lower hoop up for exposure to mosquitoes. After an
species composition. To allow a more standardized
exposure time, ranging from 2 to 10 min or longer, the
monitoring of adult mosquito populations in large areas
net is dropped. The collector then samples all mosqui-
without the need for additional collectors, many types
toes inside the drop-net, with an aspirator.
of mosquito traps have been developed to attract differ-
ent target species. In particular, a wide range of mos-
quito light traps have been developed and tested. Some
4.3.4.1 Animal Bait Catches rely solely on a conventional incandescent filament
light bulb as the main source of attraction, others use an
Many important vector species for human disease ultra-violet light source, while others supplement the
transmission may also feed on animals. Catches on a light source with carbon dioxide or another chemical
variety of animal baits, such as cattle, goats, pigs, attractant (Petric et al. 1999). Traps may also incorpo-
rodents and various birds may therefore be carried rate a photosensitive switch which turns the light and
out to determine the role and extent of zoophily motor off during daylight hours, and closes a valve to
(Amerasinghe et al. 1999; Russell 1987). Catches may prevent the mosquitoes from escaping. A variety of
involve removing mosquitoes directly from the teth- models are now commercially available, and for a full
ered animal host with an aspirator or, less directly, by review of light traps, see Silver (2008). The EVS model

Fig. 4.4 Collecting mosquitoes with a drop-net

50 4 Mosquito Research Techniques

has been successfully used for many years and is

described in detail below.

4.3.5.1 Carbon Dioxide-Baited Light Trap

The CO2-baited CDC mosquito trap (also referred to as

Encephalitis virus surveillance trap) was first devel-
oped in the mid 1950s (Nelson and Chamberlain
1955). Further improvements were published by Sudia
and Chamberlain (1962). Since then, many additional
modifications have been made (Newhouse et al. 1966;
Smith and Downs 1970; Johnson et al. 1973; Rohe
1974; Smith et al. 1979; Williams et al. 2009). The top
part consists of a 3.5 l plastic dry ice container. The
walls and snap-on polyethylene lid are insulated with
polyethylene foam to prevent rapid sublimation of the
dry ice that is placed in the container during use. In the
lower part of the container, two to four holes of 0.5 cm
in diameter allow the sublimated CO2, which is the pri-
mary attractant, to escape and flow downwards over
the lower part of the trap. The middle part of the trap
consists of a plastic tube with holders for three 1.5 V
dry cell batteries, which provide power for a fan and a
subminiature 1.5 V, 70 mA lamp, which can be oper-
ated by an off/on switch. Female mosquitoes, attracted Fig. 4.5 Carbon dioxide baited trap
mainly by the carbon dioxide, enter through an open-
ing and are sucked downward by airflow created by the
plastic fan attached to a small motor into a 30-cm long Male mosquitoes are not attracted by CO2 traps,
nylon netting catch bag (Fig. 4.5). In routine monitor- but can respond to light traps. They are best collected
ing programmes the trap is baited with approximately in the field when they are swarming close to their
1 kg dry ice, which is enough to catch mosquitoes during breeding sites. The males of most species usually
one night. swarm above prominent landmarks where they can be
A carrying handle is provided, along with a metal caught by a long-handled insect net.
chain to facilitate hanging from a tree branch or other
object. The traps are set up in the late afternoon and
removed the next morning. The catch, including the 4.3.5.2 Recently Introduced Mosquito Traps
net, can be transferred into a container with dry ice or
other killing agents to kill the mosquitoes. In the labo- In addition to the range of conventional mosquito light
ratory the species composition is determined. Catches traps used by mosquito control organizations for many
at regular intervals (e.g. each fortnight) yield valuable years, a number of novel mosquito trapping or monitor-
information about the seasonality and population size ing devices have been introduced over the last decade.
of the adult mosquitoes. Furthermore, the comparison Some incorporate novel lures, other have alternative air-
of the catches in controlled and uncontrolled areas flow systems, while other use novel technology to power
allows an estimation of the reduction of the mosquito the fan.
population by control operations. Under favourable The Mosquito MagnetTM, was one of the first of the
conditions in areas with mass breeding sites, more than new generation of traps (Fig. 4.6). This is a free-stand-
15,000 female Ae. vexans can be caught in one EVS- ing machine, that was originally intended more for its
trap per night. use as a local mosquito control device, than for moni-
4.4 Laboratory Based Research Techniques 51

Semi-field tests with the BGS trap in Tanzania showed

that it caught more Anopheles gambiae than the
Mosquito magnet (Schmeid et al. 2008).

4.3.6 M
 ark-Release-Recapture
Techniques

Mark-release-recapture techniques may be used in the

field to follow the behaviour and dispersion of marked
mosquitoes, to determine survivorship of mosquitoes,
or as a tool to estimate population size.
These approaches require a marking technique that
lasts for a useful period of time, but which has little
effect on the insects’ behaviour. Fluorescent pigments
applied to adults are most commonly used, and these
may be applied directly to batches of ­laboratory-reared
or field caught insects, or self-marking devices have
been used in which the ­mosquitoes become marked
with pigment when leaving the natural breeding site
(Niebylski and Meek 1989). However, other marking
Fig. 4.6 The Mosquito MagnetTM techniques have also been used, including staining of
the larvae, which then produce stained adults (Paing
and Naing 1988). In general, recapture rates are low,
toring and survey work. It uses a container of propane hence relatively large numbers of mosquitoes need to
gas as an internal energy source. The propane is con- be marked and released. Tietze et al. (2003) released
verted into carbon dioxide by a platinum catalyst, and 43,000 mosquitoes over 3 days, trapping the mosqui-
the heat produced by the reaction is used to generate toes using carbon dioxide baited traps positioned up
enough electricity to drive a small fan generating an to 2.8 km from the release point, and found a recap-
updraft. The device incorporates a replaceable lure that ture rate of about 0.5%. In this study, the population
releases 1-octen-3-o1 into the carbon dioxide plume. size was estimated, using the Lincoln Index, as 3.8–
The machine will run continuously for up to 21 days, 9.4 million adult mosquitoes.
after which time the propane gas cylinder and the
octenol lure need replacement. Mosquitoes and other
biting insects such as phlebotomine sandflies, are
attracted by the plume of carbon dioxide and 1-octen- 4.4 L
 aboratory Based Research
3-o1 emitted by the machine, and are then sucked into Techniques
a net cage by the fan. Kline (2002) evaluated several
propane powered traps and found them highly effective
for collecting mosquitoes. Dennett et al. (2004) con- 4.4.1 Rearing Mosquitoes
ducted field trials at an old tyre dump and found that the
Mosquito Magnet caught more individuals and more It is often necessary to breed mosquitoes to the adult
species than other traps tested. stage in order to identify them. Frequently, the fourth
Other updraft traps, and also counter flow traps, larval instar, its exuviae, or the exuviae of the pupae or
have now been introduced. The Biogents Sentinel trap the adult are needed before identification confirmation
(BGS) incorporates a proprietary odour lure, which can be made. The breeding of mosquitoes is also essen-
improves the number and diversity of mosquitoes tial for assessing insecticide ­efficacy, and the study of
caught compared to the EVS trap (Irish et al. 2008). the bionomy of the species. A wide range of different
52 4 Mosquito Research Techniques

techniques have been developed for rearing various Only a few species can be successfully reared in
mosquito species in the laboratory (Gerberg 1970). the laboratory for several generations, due to the fact
Larvae should be kept in water obtained from the that only a few species mate readily in artificial small
breeding sites, to assist successful development to the cages. However, artificial techniques of mating are
adult stage. If the immature stages of the mosquitoes sometimes used. Males are glued on the edges of
have to be transferred into clean water, either distilled glass Petri-dishes and decapitated with small scis-
or rainwater should be used. If water from the origi- sors. Then the tip of the abdomen of the anesthetized
nal breeding site is used it is not usually necessary to female is moved towards the tip of the abdomen of
add food. However, if distilled water is used, or when the male at an angle of 45o for grasping and copula-
large numbers of larvae are reared, then food in the tion. Afterwards, the female is transferred to a cage
form of powdered fish food, dried yeast or liver pow- and fed with blood (Cosgrove et al. 1994). Some
der should be added. Only small quantities of food researchers feed the mosquitoes on themselves, or on
should be added to avoid fouling of the rearing small mammals such as mice or chickens. A license
medium. A regular change of water or supply of oxy- may be required for such use of laboratory animals. A
gen is necessary if excess food is accumulating, to few species are able to mate in small cages and to lay
avoid anaerobic conditions and scum formation. eggs without a blood-meal, such as the Cx. p. pipiens
Before emergence of the adults, fourth-instar larvae biotype molestus. This mosquito is therefore very
or pupae are transferred into a “mosquito breeder”. often kept in cultures where containers with water for
The mosquito breeder consists of two clear polysty- laying the egg rafts, and a sugar solution or raisins as
rene containers. The water sample with larvae is food, are provided.
placed into the bottom portion. A screw-on lid Females can also be collected in the field from a host
between the two sections contains a funnel through when they take their blood-meal. A glass tube which is
which the emerging adults can fly into the upper part. covered with cotton wool at the bottom is carefully
Refrigerating the apparatus enables removal of the placed onto the female when it starts to suck blood.
adults. Alternatively, they can be reared to adults in When the blood-meal is completed (about 2 min) the
an improvised container, such as a jam jar. As pupae glass container with the blood-fed mosquito is covered
develop, the jar should be covered with fine netting with a nylon mesh and kept for several days at about
held by a rubber band, or alternatively a larger glass 20°C. Raisins can be placed on the nylon mesh as addi-
container may be put upside-down over the jar, so tional food. The cotton wool is kept wet to keep the
that the emerging mosquitoes cannot escape. humidity high, and when Aedes/Ochlerotatus species
When larger numbers of larvae are reared they are captured the wet cotton could also serve for egg lay-
should be placed inside a mesh cage. These can be ing. Females of Culex and Anopheles need a small
constructed by making a cuboidal frame with a side of water body for egg laying. The time from the blood-
about 30 cm, covered with nylon netting. On one side, meal until the deposition of the eggs can be measured.
a circular opening of about 10 cm should be left to The number of eggs can be counted, the morphology of
allow access into the cage, e.g. to remove containers or the eggs can be described, or hatching experiments can
mosquitoes using an aspirator. A sleeve should be be conducted with defined egg batches.
sewn in the opening to prevent the escape of mosqui- The structure and colouration of the chorion of
toes. It can be knotted when access is not required. Anopheles eggs is of crucial importance in distinguish-
A density of not more than 1,000 larvae per liter of ing certain species, e.g. within the Anopheles
water should be kept in shallow containers to avoid Maculipennis Complex. To enable the females to lay
overcrowding. On a daily basis, pupae can be removed eggs, they need to be handled gently both during sam-
with pipettes and transferred into separate containers pling and in the laboratory. The engorged females of
with clean water, also kept in the mesh cage. the complex can be easily obtained within animal shel-
The rearing temperature should be adapted to the ters in any part of a year, depending on the overwinter-
species requirements. For snow-melt mosquitoes it ing behaviour of the species. Test tubes (diameter
should be about 20°C, and for summer species, about 15 mm, length 75 or 150 mm) lined with wet 10 mm
25°C. Adult mosquitoes can be fed with a sugar solu- wide strips of filter paper can be used for direct
tion soaked into cotton wool or with wet raisins. sampling of single females within shelters. After the
4.4 Laboratory Based Research Techniques 53

specimen has been captured, the tube is closed with a

cotton wool ball and transferred to the laboratory. For
successful egg laying, the filter paper needs to be kept
damp until the end of the gonotrophic cycle.

Fig. 4.7 Arrangement of culicine larvae on a slide

4.4.2 Preserving Mosquitoes

4.4.2.1 Larvae widely used material. The fluids must be carefully

pipetted off and then replaced with the next fluid by
The best method for rapidly killing larvae is to drop means of a Pasteur pipette to avoid damaging the
them into hot water (60°C), which leaves the speci- delicate setae, which are important taxonomic char-
mens in a nicely distended condition. After a few acteristics. Finally, a large drop of viscous mountant
minutes they are transferred to a preserving fluid, is to be put on a slide before the larva is transferred
which can be MacGregor’s solution (10 ml 5% borax, by featherweight forceps.
80 ml distilled water, 10 ml formaldehyde and When culicine larvae are mounted, it is necessary to
0.25 ml glycerin) or 70% alcohol, with 1% glycerin cut off the last abdominal segments and to arrange this
added if specimens are to be prevented from drying part alongside the rest of the body. Using two micro-
out when in long-term storage. The specimens can needles the specimen should be worked to the slide
be examined by means of a dissecting microscope in surface, dorsal side upwards, with the head and the end
the preserving fluid, or stored in small glass contain- of abdomen (lateral side up) toward the long-side and
ers with rubber-lined screw caps to avoid fast evapou- across the slide (Fig. 4.7). Then, a coverslip is gently
ration. For quick reference, the glass containers must placed onto the specimen, starting from the abdominal
be clearly labelled. Labels in pencil on a strip of end of the larva rather than the head, which will help
paper can be put into the bottle; those in waterproof keep the larva in position. If needed, more fluid moun-
ink can be stuck to the outside of the bottle. The label tant should be added from the side to apply the
should contain at least the location of collection, coverslip.
type of breeding site, date of sampling and name of A label with data for the specimen, including infor-
the collector. mation on the location of sampling and breeding site
For permanent preparations, larvae are mounted as well as date of sampling and name of the collector,
in Caedax, Canada balsam, Eukit, Euparal or should be placed to the right of the specimen. The label
Histomount. For this purpose, the larvae should first with the name of the specimen and instar stage should
be transferred with some fluid into a solid, small be placed on the left, with the specimen between the
glass vessel. When very late fourth-instar larvae are two labels. The same procedure can be used to pre-
mounted it may be necessary to macerate the larvae serve larval skins.
before dehydration. It is recommended to leave the
larvae in a 5% solution of potassium or sodium
hydroxide overnight, or as an alternative, to heat 4.4.2.2 Pupae
them below the boiling point in the same fluid for
about 10 min. The caustic solution should be removed Slide mounts of pupae and pupal skins can be made in
and 5% acetic acid added for several minutes to neu- the same way as described above. When adults are
tralize the liquid. Then the larvae should be dehy- reared from larvae and pupae it is useful to keep the
drated in graded ethyl alcohols (50, 70, 80, and 96%), adults, the fourth-instar larval and the pupal skins
iso-propanol and xylene, with each step lasting at together in the collection.
least 30 min. The larvae should be kept for 10 min in To mount the pupal skin, the cephalothorax should
a 1:1 mixture of xylene and mounting media when be cut from the abdomen and cut open ventrally to
Caedax or Canada balsam is used. Xylene is not lay flat on the slide alongside with the abdomen
needed when mounted in Euparal, which is the most (dorsal side up).
54 4 Mosquito Research Techniques

4.4.2.3 Adults Stage materials can be strips of cardboard, cork,

polystyrene board, polyporous or expanded polyethyl-
Adult mosquitoes are preferably killed with ether or ene foam. The narrow strips should be equal in size,
ethyl acetate vapour. This is done by placing a small piece usually 13 mm long and a few millimeters in width.
of cotton, which has absorbed several drops of the killing First, the minuten pin for the mosquito is put through
agent, into a glass vessel containing the mosquitoes. the stage about 2 mm from one end. Then, the mos-
Some field workers also use cigarette smoke in the quito is placed upside down on a sheet of polystyrene;
absence of other killing agents, or a killing bottle with a the prepared stage holding the minuten pin is picked up
layer of Plaster of Paris containing cyanide on the bot- with entomological pinning forceps; and the end of the
tom. The dead mosquitoes are pinned and kept dry. The minuten pin is inserted from the ventral side into the
mosquitoes should be pinned soon after killing because thorax of the specimen between the legs, pushing
the soft bodies can be more easily handled than fragile, through until the point of the pin reaches the scutum.
dry insects, which tend to disintegrate. For this reason, The head of the mosquito should face away from the
dry specimens should be relaxed in a humidity chamber end of the stage, and the abdomen and legs along the
prior to pinning. The dried mosquitoes should be sepa- stage. It is ­recommended to pull the minuten pin through
rated from one another on a filter paper in a Petri-dish the stage so that the abdomen of the mosquito remains
and kept for 12–24 h in a desiccator containing water to horizontal to the stage, but avoid arranging the legs, as
soften the specimens. Care should be taken to avoid they could be damaged. A gentle puff of air from
drops of condensation falling on the specimens. behind the mounted specimen will spread wings into a
The mosquito should then be removed by fine- position so that they do not cover the abdomen. The
pointed forceps and pinned using the double-mounted stage should be carefully held between the fingertips
method. In this method, a large stainless steel pin about of one hand by the end in which the large pin will be
38 mm long, no. 2 in thickness, holds the stage where inserted. About 1 mm from the end of the stage, the
the mosquito is mounted. The mosquito is attached with large pin should be pushed through until the upper
a small (about 12 mm) stainless steel point (minuten pin), third of the pin remains above the stage. This allows
and usually two labels with all necessary data similar to room for holding the mounted specimen and for put-
those for permanent preparations of larvae (Fig. 4.8). ting the two labels below the stage. Labels should be of
good quality card and written in India ink, using a fine
pen of uniform size and always attached to the pin in
the same position. On the label pushed next to the
stage, the locality of sampling, date and collector’s ini-
tials are recorded. The label with the identity of the
specimen should be placed below this. A pinning block
is useful for a uniform and neatly presented collection
of specimens (Snow 1990).
A simpler and widely used method, described
below, also provides good protection to the mosquito
and provides easy handling of the mounted mosquito
(Bohart and Washino 1978). The freshly killed, frozen
or newly relaxed mosquito is attached in a horizontal
position by the left pleuron to a drop of clear fingernail
varnish on the tip of a triangular cardboard or cork
strip, of at least 7 mm in length, which is located at the
top of a 38 mm pin. The scutum should face away, and
the legs towards the pin. Then, the cardboard or cork
strip is pulled down to about two-thirds of the pin’s
length, to leave enough room for the two labels.
After drying for about 1–2 days (if possible in a
Fig. 4.8 Mounted adult mosquito refrigerator) the insects should be transferred into a
4.4 Laboratory Based Research Techniques 55

wooden cork-lined storage box with a fumigant (e.g. become more widely used. Burkot et al. (1981) ini-
crystals of naphthalene) to avoid pest damage. tially described an indirect micro titration technique
The external genitalia of males are sometimes in which blood meals taken by Ae. triseriatus could
essential for identification. After the mosquito is killed be identified to species within rodents and canines.
the tip of the abdomen is cut between segment VII and The period between feeding and analysis was criti-
VIII with optical scissors or fine forceps. The end of cal, with 100% of the blood samples being immuno-
the abdomen is placed in a solution of warm sodium positive within 8 h of feeding, but by 16 h after
or potassium hydroxide for about 15 min for macera- feeding, only 40% of samples were immuno-posi-
tion. Then, the genitalia are transferred to glacial ace- tive. Gomes et al. (2001) compared precipitin and
tic acid in order to neutralize the maceration fluid and ELISA techniques and found that the precipitin
to dissolve any remaining fat droplets. They are dehy- showed greater specificity, while the ELISA test
drated and mounted as described for larvae (see showed greater sensitivity.
Sect. 4.4.2.1). To obtain the best view of the genitalia, Most recently, a number of DNA techniques have
they should be placed with the ventral surface facing been used for blood-meal identification, including
upwards before the cover slip is placed in position. DNA profiling. Using DNA profiling of four poly-
The balsam should be viscous enough and in suffi- morphic human loci, Benedictis et al. (2003) estab-
cient quantity to ensure that the specimen is not flat- lished profiles for the residents in a community, and
tened. The remainder of the male is pinned, and both then allocated blood meals taken by wild Ae. aegypti
the slide preparation and the pinned male are labelled mosquitoes to individual residents. Cytochrome b
to indicate their relationship. has also proved useful in establishing the identity of
mosquito blood meals. Lee et al. (2002) used a poly-
merase chain reaction heteroduplex assay to separate
blood meals taken by wild caught Cx. tarsalis from a
4.4.3 Mosquito Blood Meal Identification large numbers of bird species. Results showed that it
was possible to determine avian hosts for up to 7
Identification of host preferences of mosquitoes is cen- days postfeeding, while blood from mammalian
tral to understanding their potential to act as vectors of hosts with non-nucleated erythrocytes had to be
human diseases. Although animal and human landing assayed sooner.
rate catches, or use of baited traps, will give useful
information on this behaviour, analysis of the source of
the blood meal in captured mosquitoes is widely used
4.4.4 M
 ethods for Measuring
to understand the natural feeding preferences of
mosquitoes. the Physiological Stage
Precipitin testing was introduced by Bull and
King (1923) and became the standard technique The vector capacity of a mosquito species depends to
used over many years. The technique typically a great extent on the ability of the females to have
involved the addition of the unknown blood meal to several blood-meals, which in turn enables the vec-
a narrow tube (a capillary is used by some research- tor mosquito to transmit pathogens or parasites from
ers) in which a layer of antiserum has already been a previous infection. In this respect, the knowledge of
placed at the bottom of the tube. The formation of a the physiological stage of a mosquito is of epidemio-
ring at the interface of the two reagents indicates a logical importance. It can be determined by the
positive reaction, i.e. the blood meal is from the assessment of the number of gonotrophic cycles
same species as the antiserum. Other serological through which a mosquito female has passed. The
techniques that have been reported, but less widely gonotrophic cycle for species that require a single
used, include the fluorescent antibody technique blood-meal for each batch of eggs, is defined as the
(Gentry et al. 1967), and the latex agglutination test time period needed from the blood-meal until the ovi-
(Boorman et al. 1977). position of the eggs. After a blood-meal, the basal
Since the 1980s however, techniques based on oocytes within the ovarian tubes (ovarioles) in the
enzyme linked immuno-sorbent assay (ELISA) have ovaries develop into mature eggs. As a result, the
56 4 Mosquito Research Techniques

epithelium surrounding a single ovariole is stretched 4.4.5 M

 orphological and Taxonomic
by the expanding oocyte. When the egg is deposited, Techniques
the epithelial sheet that surrounded the egg during its
development shrinks, leaving a residual lump or a
knot-like dilatation. Following the next blood-meal 4.4.5.1 Morphological Studies
the next sequence of oocytes located more distally in
the direction of the germarium of the ovariole, con- Although the morphological characteristics of most of
tinue their development. After the deposition of the the mosquito species are described, there is still need
next batch of mature eggs a second series of dilata- for further studies on character variation within indi-
tions remains in the ovarioles. Therefore, the number viduals and populations of a species. Not only the
of dilatations corresponds to the number of previous number and size of scales and setae can vary but also
ovipositions. This allows an estimation of the lon- the colouration, size or other features. In particular, the
gevity of the individual mosquito, and its importance comparison of species from different areas can reveal
as a vector. The more the number of blood-meals, the new results on variation. However, in some cases the
greater is the possibility for the mosquito to acquire morphological features are not sufficient for species
and transmit pathogens. identification, and therefore other techniques have to
Furthermore, the age or the physiological stage of a be employed.
mosquito can also be determined by examining the
changes in the ovarian structure. During the first
gonotrophic cycle the coiled ends of the tracheoles are 4.4.5.2 C
 ytodiagnostic Methods for the
unwound by the swelling of the ovaries. These uncoiled Identification of Sibling Species
tracheoles indicate parity (eggs developed) whereas
nulliparity (no eggs developed) is indicated by still The morphological similarity of the members of mos-
coiled tracheoles. quito species complexes (so-called sibling species) in
For the examination of the ovaries, the mosquito the larval and/or adult stages, required the development
must be dissected. After the female mosquito is of tools for species identification which were not based
killed, it is placed in a drop of water on a micro- on external morphological characters. Genetic mapping
scope slide. The mosquito is held with a fine is of great importance to distinguish between species,
mounted needle on the thorax, and with a second subspecies or ecotypes, and for investigations of popu-
needle the intersegmental membrane, between lation genetics. Various types of maps can be constructed
abdominal segments VII and VIII, is cut. The gut (Hillis 1996):
and the ovaries can then be pulled out with forceps. (a) Preparations of polytene chromosomes made from
The gut is cut and the ovaries are inspected. For the larval salivary glands or ovarian nurse cells, pro-
examination of the dilatations of the ovarioles, the vide the basis for physical maps, where the specific
ovarian sheet has to be removed and the ovarioles banding patterns of polytene chromosomes are
have to be separated with a needle. For examina- illustrated in photomicrographs or drawings. For
tion using a microscope, the ovaries are covered several decades polytene chromosomes have been
with a coverslip. particularly useful in chromosomal studies, due to
The appearance of the abdomen can also be used to their specific properties.
determine whether a mosquito has engorged blood, or (b) Genetic or linkage maps are maps where the rela-
to assess the stage of egg development. When the tive position of genes and the distances between
abdomen of the mosquito is thin it is unfed, or has them are plotted.
passed through a gonotrophic cycle. In freshly fed (c) Restriction maps and
females the abdomen (midgut) is filled with red blood, (d) Whole genome or molecular maps.
which gradually becomes dark red. As the eggs
develop, the ovaries increase in size, and the red colour The typical karyotype of culicines consists of three
disappears. In the gravid females, in most cases a trace pairs of homomorphic chromosomes. Typical for the
of dark blood is left and ovaries occupy almost the karyotype of anophelines is one pair of heteromorphic
whole abdomen. sex chromosomes, as well as two pairs of autosomes.
4.4 Laboratory Based Research Techniques 57

In certain mosquito tissues the chromosomes replicate (1962), Green (1972), Hunt (1973), Green and Hunt
repeatedly without mitosis-like events, so that hun- (1980) and Graziosi et al. (1990).
dreds of sister chromatids remain synapsed. This mul-
tiple DNA duplication is accompanied by alignment
and condensation of the DNA strands, thus forming 4.4.5.3 B
 iochemical and Molecular Methods in
specific patterns of bands and interbands. These Studies on Systematics
banded polytene chromosomes occur in larval and
adult tissues, such as the salivary glands and midgut Taxonomy utilizes homologous morphological charac-
epithelium, the malpighian tube cells, as well as in the ters for the identification of species and evaluation of
ovarian nurse cells of adult females. Banding relationships among the taxa. The phenotype depends
sequences can change by rearrangements within or both on the genotype and environmental conditions, so
between chromosome arms, e.g. by inversions or that even characters depending on a monomorphic
translocations. Chromosome aberrations are typical of gene locus, may vary between individuals or popula-
certain mosquito populations. Banding patterns can tions of a distinct species. Consequently, separation of
therefore be used as markers for distinguishing among closely related species may be difficult using variable,
species and ecotypes. Differences in banding, e.g. due quantitative characters.
to inversions, have proved to be a useful tool in distin- Molecular methods for analyzing variation in DNA,
guishing members of sibling species complexes, and and biochemical investigation of gene products, are
for resolving interrelationships between species. widely used in support of taxonomic studies. Generally,
The polytene or so-called giant chromosomes are investigations that incorporate both morphological and
easily seen using a microscope at high magnification molecular approaches will provide the most substanti-
(view at × 1,000 with oil immersion lens and phase ated descriptions and interpretations of diversity within
contrast). In the culicine mosquito Cx. p. pipiens and and between the taxa.
the anopheline mosquitoes, high quality squashes of In taxonomy and evolutionary research, protein-
polytene chromosomes can be obtained from the sali- electrophoresis is a widely used and highly efficient
vary glands of the fourth-instar larvae. The specimen technique. For this, homogenates of animals or
is placed in 5% Carnoy’s fixative (mixture of one part organ samples are applied to a gel (polyacrylamide,
of glacial acetic acid and three parts of 95% ethanol) agarose or starch) and exposed to an electrical field
on a glass slide. The abdomen is cut off and the tho- under ionic buffer conditions. The migration of dis-
rax is slit open dorsally along the mid-line. By pull- solved proteins is determined by their charge, size
ing on the head, the glands attached to the head are and shape. Depending on these factors, the proteins
pulled out of the thorax. Then the salivary glands are segregate to bands in the gel and then are visualized
cut free and transferred to a slide in a droplet of by unspecific or, in the case of enzymes, by the sub-
Carnoy’s fixative, stained for about 5 min by adding strate transformation coupled staining. Differential
two droplets of a mixture of acetic and lactic acids migration of the same protein is the result of a
with orcein (2% by weight of orcein powder is dis- change of its amino acid sequence. Proteins are pri-
solved in 1 part 85% lactic acid and 1 part glacial mary gene products, so changes in their amino acid
acetic acid, and this concentrated stain is then again sequence are caused by changes in the underlying
diluted 1:3 with 45% acetic acid). The tissue is care- DNA sequence, i.e. there are different alleles on
fully squashed by placing a coverslip on top of the their gene locus. When various species possess dif-
preparation and pressing it with a finger. Thus the ferent alleles exclusively, these fixed alleles may be
cells are broken and the chromosomes are spread. used as genetic markers and enhance the identifica-
Species, sex and karyotype composition of larvae tion of species by morphological traits. By investi-
from various habitats can be determined by the exam- gation of several proteins, the resulting data are
ination of the chromosome preparations with a micro- suitable for the quantification of genetic variation
scope. This technique can be successfully employed within populations (e.g. degree of polymorphism
for population studies on the Anopheles Maculipennis and heterozygosity), detection of species boundar-
Complex. Methods for making polytene chromosome ies, phylogenetic relationships and evolutionary
preparations have been described by French et al. processes (Harris and Hopkinson 1976).
58 4 Mosquito Research Techniques

Investigation of DNA has been driven particularly WHO to assist with centralized monitoring of insec-
by the development of the polymerase chain reaction ticide resistance status (WHO 2001a).
(PCR) that allows the amplification of small amounts
of DNA million-fold, and makes DNA accessible for
4.5.1.1 A
 ssessing the Susceptibility of Adult
many purposes. There are several methods of DNA
Mosquitoes
analysis: DNA–DNA-hybridization estimates the
amount of sequence divergence between genomes,
The adult mosquito susceptibility kit consists of two
but provides no information on the structural back-
interconnected plastic tubes, separated by a gate
ground of differences. Fragment and restriction anal-
mechanism. One tube is lined with clean paper, and
ysis such as variation in fragment size (e.g. VNTR),
the other lined with paper treated with a discrimi-
restriction site variation (RFLPs, RAPDs, DNA fin-
nating dose of the chosen insecticide. Typically,
gerprinting) and others, provide some information
adult mosquitoes will be collected from the area
about genome organization, and are suitable for
under study, or reared from immature stages. A
detection of individual and species relationships. By
batch of mosquitoes is introduced into the clean
DNA sequencing, exact information about the geno-
tube, and then moved through the gate onto the
type is obtained that allows solid conclusions to be
insecticide treated paper in the other tube. After a
drawn about molecular evolution and phylogeny
fixed exposure period (ranging from 0.5 to 4 h,
(Murphy et al. 1996).
depending on mosquito species and insecticide) on
All these techniques provide important and useful
the insecticide, the mosquitoes are then moved back
information about biodiversity and evolution, but the
through the gate onto the clean paper. Mortality is
techniques used in any particular study should always
then assessed after a fixed period, typically 24 h
be selected according to the overall aim and resources
after exposure. Control mosquitoes are exposed to
of the investigation.
untreated paper, but otherwise handled identically.
Where mortality is in the range 98–100%, the mos-
quitoes are considered susceptible. Mortality in the
4.5 A
 ssessing the Activity range 80–97% suggests the possibility of resistance
of Insecticides and Repellents that needs confirmation, while mortality of < 80%
suggests resistance (WHO 1998b).
on Mosquitoes
The technique may be used to determine the sus-
ceptibility status of mosquitoes prior to the start of
4.5.1 Insecticide Susceptibility Testing treatment programmes, and should be used at intervals
to detect any changes in the susceptibility status of the
insects over the course of the programme, and as part
The WHO has developed test kits for the assessment
of the investigation of any local control failures.
of insecticide susceptibility of adult and larval mos-
quitoes. The kits typically consist of containers and
tubes for holding and manipulating the insects,
together with various insecticide treated substrates 4.5.1.2 A
 ssessing Susceptibility of Larval
which are commercially available. Insecticides from Mosquitoes
the main insecticide classes, including organochlo-
rines, organophosphates, carbamates, and pyrethroids Laboratory efficacy tests to establish the activity of
are available. Discriminating doses, i.e. those con- different larvicides against a particular species, or
centrations that kill susceptible individuals, but to assess the efficacy of a given insecticide against
allow survival of resistant individuals, have been different strains, may be relatively easily carried
established for the most important species, and are out in the laboratory. The larvicide is prepared as a
available. WHO typically sets the discriminating stock solution (typically 10 g insecticide/l concen-
dose as double the LC99 obtained by extrapolation of tration), and then diluted to give a range of rela-
the log-probit line. Standardized data recording tively widely spaced serial dilutions, spanning the
forms are available, and these may be returned to likely active concentration. Replicate disposable
4.5 Assessing the Activity of Insecticides and Repellents on Mosquitoes 59

cups or other containers are filled with about Twenty-five early fourth-instar larvae of Ae. aegypti
100 ml of each larvicide concentration. For con- (when B. thuringiensis israelensis is to be tested)
ventional and bacterial larvicides, batches of 25 or 25 early fourth-instar larvae of Cx. pipiens (when
third or fourth-instar larvae are introduced to each B. sphaericus is to be tested). Each batch of larvae in
container, and mortality assessed 1 or 2 days later. 2 ml water is put into each cup using a Pasteur pipette.
For insect growth regulators (IGRs), the test will The use of early fourth-instars is very important, and
run longer to allow for pupation and adult emer- should be strictly adhered to. A small amount of food
gence, and the larvae will need feeding. Efficacy of (ground mouse diet) is added to each cup in order to
IGRs is typically expressed not as mortality, but as avoid excessive mortality caused by starvation when
% inhibition of adult emergence (WHO 2005b). the bioassay is run longer than 24 h.
A comparable initial suspension and series of dilutions
are prepared in the same way with the test preparations, but
4.5.1.2.1 Assessing the Potency of Microbial with a range of dilutions exceeding that of the standard, to
Larvicides ensure that a reliable regression line can be obtained.
The results of an initial range-finding bioassay
Standardized methods have been developed to deter- using only two widely spaced concentrations of the
mine the LC50 values for microbial larvicides using test material, can be used to select the concentrations
standard formulations (e.g. IPS 82 for Bacillus thur­ used in the full assay more accurately, and as a partial
ingiensis israelensis tests and SPH 88 for B. sphaericus replicate of the full bioassay.
tests) as reference products. The activity of IPS 82 has Each series of bioassays will involve at least 500 lar-
been assigned the value of 15,000 ITU/mg and of SPH vae exposed to the standard treatment; 100 larvae as
88 the value of 1,700 ITU/mg). controls, and 500–1,000 larvae exposed to the test prep-
arations. All tests should be conducted at 25°C (± 1°C).
The mortality data are recorded after 24 and 48 h by
Bioassay Procedure
counting both dead and living larvae. The second reading
The following procedure for bioassays is recom- is useful in routine work to confirm the previous data, and
mended in order to allow an accurate and standardized to check for the possible intervention of factors other than
measurement of the potency of the B. thuringiensis microbial toxins. If some pupae emerge, they should be
israelensis and B. sphaericus products: taken out and not included in the mortality count.
Fifty mg of the standard microbial agent powder When control mortalities exceed 5%, the percent-
is weighed and poured into a 20 ml penicillin flask, ages observed in the treated containers should be cor-
to which 10 ml of deionized water and 15 glass rected using Abbott’s formula (Abbott 1925). Test
balls (6 mm diameter) are added. This suspension is series with control mortalities greater than 10% should
vigorously homogenized on a flask shaker for be discarded. Mortality concentration regression lines
10 min at 700 strokes/min. Only one stock dilution should be drawn on logarithmic paper. Then the LC50
is made in a test tube of 22 mm diameter: 0.2 ml of of the series treated with the standard and with the test
the initial suspension are added to 19.8 ml of deion- preparations are read and the potency (titre) of the test
ized water. The test tube is agitated for a few sec- material determined by the following formula:
onds on an agitator at maximum speed.
From this dilution (50 mg of product/l), subsequent activity of the standard (ITU) × LC50 of standard
dilutions are immediately made in plastic cups which LC50 of test preparation
have been already filled with 148 ml of deionized water;
using precision pipettes or micropipettes. Aliquots of The potency or titre of the product is expressed in
120, 90, 60, 30 and 15 µl are added to the cups in order ITUs (International Toxic Units). For improved preci-
to obtain final concentrations of 0.04; 0.03; 0.02; 0.01 sion such bioassays should be repeated on at least three
mg and 0.005 mg/l respectively of IPS 82 different days, and the standard deviation calculated.
(B. thuringiensis israelensis) or SPH 88 (B. sphaericus). A very wide range of literature exists on the use of
Four replicate cups are used for each concentration larvicides and assessments, and WHO (2005b) pro-
and for the control. vides a useful overview.
60 4 Mosquito Research Techniques

4.5.2 A
 ssays of Insecticide Deposits mally be transferred to the laboratory, supplied with
on Surfaces (e.g. Walls or Nets) sugar solution on a cotton pad, and mortality recorded
at 24 h after exposure. Control mosquitoes may be
located outdoors in an untreated area for a similar time
The WHO has also established standardized kits and to the treated mosquitoes, before being returned to the
procedures for the measurement of the efficacy of laboratory for holding and assessment.
deposits of insecticides applied to walls and bed nets
(WHO 2006). The test kit consists of a transparent
plastic cone, with a hole at the apex. The cone is fixed
to a surface, such as an insecticide-treated wall, using
4.5.4 A
 ssays of Efficacy of Mosquito
adhesive, nails, rubber bands, etc. A strip of plastic
foam may be fixed to the base of the cone to ensure a Repellents
tight fit against an uneven wall surface. Adult mosqui-
toes are then introduced into the cone through the Personal protection is an important component of any
hole at the apex, which is then plugged with cotton programme intended to reduce nuisance biting or the
wool. After a fixed exposure period, typically 1 h, transmission of mosquito disease. A very wide range
the mosquitoes are removed with an aspirator, trans- of compounds have been proposed and evaluated as
ferred to a clean holding container such as a net-cov- mosquito repellents, with botanical extracts in particu-
ered paper cup, and mortality assessed after 24 h. lar having been widely evaluated.
Control mosquitoes are exposed to an untreated wall, A number of standardized evaluation techniques
but are otherwise handled in the same manner as the have been established, but in addition, a number of
treated mosquitoes. Procedures for assaying treated alternative approaches have been developed by indi-
bed nets are essentially similar (WHO 2005a). vidual researchers.
Such tests enable the quality of treatments to be In broad outline, the standardized techniques typi-
assessed, and allow the longevity of the insecticide cally involve application of a known dosage of the test
deposit to be determined (WHO 2006). repellent to a human volunteer’s arm (research involv-
ing human volunteers will in many countries be cov-
ered by legislation and will require ethics approval),
and then exposing the treated skin to unfed mosqui-
4.5.3 A
 ssays of Efficacy of ULV Insecticide
toes (ASTM 2006a; US EPA 1999; WHO 1996b). The
Treatments in the Field time of first bite, or the number of bites over a fixed
time, are recorded. Depending on the objectives of the
The efficacy of ULV adulticide treatments is typically test, a range of doses are evaluated in order to deter-
assessed using caged mosquitoes positioned in the mine the minimum effective dose, or a given dose is
treated area. Cages may be cuboidal, cylindrical or be evaluated repeatedly over time in order to determine
comprised of modified WHO adult mosquito suscepti- the duration of effectiveness. Initial tests will be car-
bility test kits, but all will have the maximum possible ried out in a laboratory, but field tests will be required
area of open mesh, to allow penetration of air-borne to show the efficacy under realistic conditions (ASTM
droplets. Cages may be left in the open, or positioned 2006b). Tests should be very carefully designed to
under vegetation or within buildings (Perich et al. eliminate or compensate for factors which may affect
1990). There are concerns that the mesh of the cage results, including variation in the human subject due
may prevent insecticide droplets reaching the mosqui- to, e.g. washing, activity, perspiration or underlying
toes inside, while there are also concerns that insecti- human to human variation, and variation in the mos-
cide droplets deposited on the cage mesh may then be quitoes due to age, parity, previous sugar feeding or
available to the insects by tarsal contact. To avoid the larval diet, and other factors including cage size and
risk of artificial contamination, some researchers trans- light intensity (Barnard 2005).
fer the mosquitoes from the exposure cage to a holding Alternative techniques for the evaluation of repel-
cage shortly after treatment (Bunner et al. 1989). After lents include the use of wind tunnels with human
exposure in the field, treated mosquitoes would nor- breath as an attractant (Sharpington et al. 2000), or the
4.6 Conclusion 61

use of a membrane feeding technique as opposed to a interesting and specialized biology, but also because of
human arm (Cockcroft et al. 1998). their major impact on human health. In practice, research
and operational programmes will use a selection of these
techniques to build up a better understanding of the insect,
the way in which it relates to its environment, and the
4.6 Conclusion impact of control techniques. Despite the extensive litera-
ture on research methodology, new techniques are regu-
The above-mentioned techniques represent those that are larly developed, as new questions are asked, or new
used more commonly in mosquito research. Mosquitoes technology becomes available. Researchers are encour-
are a group of insects that have attracted considerable aged to review the literature, both historical and current,
research attention not only because of their intrinsically before finalizing their planned research programme.
Chapter 5
Morphology of Mosquitoes

5.1 Adults (Fig. 5.1) giving some mosquitoes a physicochemical or physical

colouration. The shiny, metallic blue, green and purple
Mosquitoes differ from all other members of the appearance is mostly found within tropical species
Nematocera by having a long scaled proboscis (labium (e.g. Haemagogus spp., Sabethes spp.). In most other
and stylets), always longer than the thorax, which pro­ species the colour of the scales may vary from white to
jects forward together with the maxillary palps almost black but is usually referred to as pale or dark
(Fig. 5.1). The latter are as long as or longer than the in the description of the species. Pale and dark scales
proboscis in males of most species and females of the can be intermixed wherever they occur. They may also
genus Anopheles. The head, thorax, and abdomen are be grouped together, forming the specific contrasting
covered with scales and setae; the extent of coverage is patterns, which will be referred to as rings on all legs,
genus specific. The legs, wing margins, and wing veins stripes on the scutum, and bands on the abdominal
are typically clothed with scales. The closest resem­ terga. Scale colouration can change in different light
blance of the body shape is found within the families sources and after long-term storage. The overall body
of slender, long-legged crane flies (Tipulidae) and non­ colour can be influenced by the colour of the integu­
biting midges (Chironomidae), the latter often being ment which may shine through the scales. The abdom­
mistaken for mosquitoes, especially around artificial inal terga and sterna are densely covered by scales in
lights at night. However, none of these families have the subfamily Culicinae, while the sterna, and usually
mouthparts for piercing and sucking. The short man­ also the terga, are wholly or largely devoid of scales in
dibulate mouthparts of the Tipulidae are of the biting the subfamily Anophelinae. Like all other Diptera, the
and chewing type, and articulated on the tip of a pro­ mosquito head, thorax, and abdomen are covered with
longed, beak-like gnathocephalon. The Chironomidae setae of different length, shape, and colouration
usually have a reduced gnathocephalon and biting which can have significant genus and species-specific
mouthparts. In addition, the Chironomidae possess a taxonomic importance.
conspicuously humped thorax, and often particularly
long, forward-facing fore legs.
The males of most mosquito species clearly differ
from the females by having plumose antennae and 5.1.1 Head (Figs. 5.2 and 5.3)
long, hairy maxillary palps (Fig. 5.2a,b). The first 12
flagellomeres of a male antenna bear dense, long Mosquitoes, like all Pterygota (winged insects) and
setae, which are at least as long as the head capsule. Thysanura, have annulated antennae. Their basal seg­
The setae on the last flagellomere are shorter than the ment (scape) is collar shaped and hidden behind an
head capsule, and of similar length to those on the enlarged, spherical second segment, the pedicel
female antenna. (Fig. 5.2a). In the Chironomidae and Culicidae the pedicel
Unusually for Diptera, the integument of mosqui­ is specially enlarged to accommodate a highly developed
toes is quite extensively covered with scales. Essentially, mechano- and sound-receptor, the Johnston’s organ. The
scales are flattened setae containing pigment and often remaining 13 divisions of the antenna together constitute
have a striate surface, which produces optical effects, the flagellum and are entirely without intrinsic muscles.

N. Becker et al., Mosquitoes and Their Control, 63

DOI 10.1007/978-3-540-92874-4_5, © Springer-Verlag Berlin Heidelberg 2010
64 5 Morphology of Mosquitoes

Fig. 5.1 General outline of a female culicine mosquito (after Marshall 1938)

Consequently, those divisions are named annuli or amalgamated to form the head capsule (Figs. 5.2
flagellomeres instead of segments, the latter term being and 5.3). Compound eyes occupy a substantial portion
used only for the partitions of the insect body having of the head, and if they meet in the middorsal line,
intrinsic musculature. The antennae are usually sub­ this condition is then called holoptic. The epicranial
equal to the proboscis but could be distinctly longer suture is quite indistinct. Its median part is called
in the genera Deinocerites and Galindomyia. The the coronal suture and the two branches above the
exterior of the head is composed of several sclerites scape are called the frontal sutures. The region of
5.1 Adults 65

Fig. 5.2 Head of (a) male; (b) female culicine mosquito (after Wood et al. 1979)

the head below the frontal sutures is the frons, above The gnathocephalon is composed of the anteclypeus
them lies the vertex, though the precise limits of the and postclypeus dorsally, of the genae laterally, and of
former areas are not easily defined. A narrow strip of the hypostomal bridge ventrally.
the vertex between the compound eyes is called the The proboscis, which is articulated with the gna­
interocular space. At the back of the head, between the thocephalon, is almost straight and cylindrical in many
vertex and the cervix, or neck, the occiput and the nar­ genera, but is laterally compressed with the apical third
row ring-like postocciput are located. The vertex and evenly curved downwards (Armigeres spp.) or strongly
occiput may be covered with truncated or forked recurved and tapering towards the apex (Toxorhynchites
erect scales and narrow, curved, or broad decumbent spp.). In Malaya spp. the tip of the proboscis is inflated,
scales. The nearest structure, found immediately turned upwards and setose. It is made of six slender
anterior to the frons, is the bulge of the gnathocepha­ stylets (Fig. 5.3), the labroepipharynx or labro-palatum
lon, called the rostrum in some other orders of insects. (a more or less fused structure made of an outer wall,
66 5 Morphology of Mosquitoes

Fig. 5.3 Head regions and mouthparts (after Clements 1992)

the labrum, and an inner wall, the epipharynx), the for the stylets, is looped backwards during feeding and
paired mandibles, the hypopharynx and the paired does not penetrate the host tissue. The labium of
maxillae. These are lodged in the groove of the elon­ Toxorhynchites spp. females is rigid.
gated labium (prementum) which ends with a distally In males, both mandibles and maxillary laciniae are
articulated pair of labella, thought to represent the reduced or altogether lacking and cannot be used for
modified labial palps (Figs. 5.1 and 5.2). Between the piercing. Nectar and other sugary juices are simply
labella, the ligula, a short pointed lobe is situated, and imbibed through the tubular labroepipharynx.
in its shallow groove lies the tip of the stylet fascicle. The well developed maxillary palps are articulated
The mandibles and the maxillary laciniae are modified below the clypeus, dorsolaterally to the proboscis
into long piercing stylets. The latter, being stronger (Figs. 5.1 and 5.2). Palps are divided into five divisions
and serrated apically, are the main piercing organs which are clearly visible in both sexes of Anopheles
used to perforate the skin of the host. The labroepiphar­ and in the males of almost all the other genera. The
ynx, which bears three pairs of sensillae on its tip, and females of other genera frequently have an atrophied
the other stylets form a fascicle which probes until it basal segment and apical annuli, therefore, their palps
enters a blood capillary of a host. The saliva which acts appear to have fewer segments. The three basal divi­
as an anticoagulant, is injected through the hypophar­ sions are true segments, having intrinsic muscles
ynx. The blood is taken via a channel made mostly of (Clements 1992). Although the two apical divisions
the labroepipharynx. The mandibular and maxillary are not true segments they will be referred to as seg­
stylets are reduced or absent in females of ments or all five as palpomeres, for the convenience in
Toxorhynchites spp. and Malaya spp. which feed on species description. The palps of most female mosqui­
nectar. They have a functional labro­epipharynx and toes are less than half the length of the proboscis
hypopharynx. The labium, being only a protective sheath (except in some Armigeres spp. and Mucidus spp.).
5.1 Adults 67

Only in anopheline females (except Bironella spp.) are lateral pleurae. These regions are differentiated into
the palps of similar length to the proboscis. In almost separate sclerites which are termed as tergites, sterni­
all male mosquitoes the maxillary palps are as long tes and pleurites respectively. The sclerites of the tho­
as, or longer than the proboscis. Exceptions can be rax, according to the segments to which they belong,
found in males of genus Uratonotaenia and subgenus are denoted by the prefixes pro, mes(o) and met(a).
Aedes, where the palps are of similar length as in The pronotum is seemingly absent medially but
females. well developed laterally. It is separated into an anterior
lobe like division, the antepronotum, and a flattened
posterior division, the postpronotum which appears to
be part of the mesopleuron (Fig. 5.5). The lobes of the
5.1.2 Thorax (Figs. 5.4–5.8) antepronotum are very large, protruding and closely
approaching at the midline of the scutum in the genera
The three thoracic segments are known as the protho­ Haemagogus, Sabethes and Wyeomyia. The mesono­
rax, mesothorax and metathorax. In mosquitoes and all tum of Diptera is clearly subdivided into prescutum,
other Diptera, where only the fore wings are used for scutum and scutellum, the fourth tergite, the postno­
flight, the mesothorax is the best developed segment. tum, being generally hidden beneath the scutellum.
The prothorax and metathorax are reduced to little The prefix meso is usually omitted for dipterous insects
more than leg bearing collars fore and aft. The hind because those subdivisions do not occur in the weakly
(metathoracic) wings are modified into gyroscopic developed metanotum, and the pronotum is usually
organs, called the halteres. Each of the thoracic seg­ simple or bipartite. In mosquitoes (Figs. 5.4 and 5.5),
ments is divisible into four main regions, the dorsal the transverse suture separating the prescutum and
tergum or notum, the ventral sternum and the two scutum is not fully developed, hence the term scutum

Fig. 5.4 Dorsal view of thorax

68 5 Morphology of Mosquitoes

Fig. 5.5 Lateral view of thorax – pleurites

Fig. 5.6 Lateral view of thorax – setation

is used for both mesotergites. The scutum is the principal The lateral scutal margin above the mesothoracic
dorsal area of the thorax and is sometimes incorrectly spiracle bears a tubercle named the scutal angle from
referred to as the mesonotum in the mosquito literature. which the transverse suture extends. The scutal fossa is
5.1 Adults 69

Fig. 5.7 Lateral view of thorax – scale patches

a slightly depressed area anterior to the scutal angle, pairs of, more or less dispersed, longitudinal rows
which lies between the scutal margin and the dorsocen­ (Fig. 5.4). The setae of the acrostichal rows are articu­
tral row of setae. A small elongated sclerite of mesono­ lated close to each other and to the median line. The
tal origin, the paratergite, is situated anterior to the second pair of dorsocentral rows of setae is more dis­
wing root and in some species it is not apparent from persed towards the end of the scutum. Finally two
above. The scutum is followed by the scutellum rows of scattered supraalar setae occupy the posterior
(Figs. 5.4 and 5.5). Its posterior margin may be evenly parts of the lateral margins of the scutum. The scutel­
convex (genera Anopheles and Toxo­rhynchites) or lum in species of the genus Anopheles bears a uniform
three lobed (most genera of Culicinae and genus row of backwardly directed setae along its evenly
Chagasia). An additional, well developed sclerite of rounded posterior margin. In the other genera that
intersegmental origin, the postnotum, bears the have a trilobed scutellum, the setae are arranged in
phragma to which the dorsal longitudinal flight mus­ three sets, a median and two groups of lateral scutellar
cles are attached. The metanotum is reduced to a nar­ setae. The postnotum is usually bare.
row, weakly sclerotized transverse band (Figs. 5.4 and Narrow or broad scales may cover the whole scutum
5.5). The metapostnotum is usually not visible. or only some of its areas, the amount of scaling varies
The postpronotum usually bears a vertical row of between different genera. The scales may be entirely
setae close to its posterior margin, the postpronotal of the same colour on the whole scutal surface, or dif­
setae (Fig. 5.6). Sometimes they may cover the meso­ ferently coloured producing usually linear, longitudi­
thoracic spiracle and can easily be mistaken for the nal and patch-like scale patterns which are usually
prespiracular setae (an important diagnostic character species specific and consequently important for identi­
for the genera Culiseta and Psorophora). It is there­ fication. Therefore it is important to catch, handle and
fore advisable to carefully focus on the point where mount specimens with special care to prevent scales of
the setae are inserted. Setae may be concentrated in the central scutal area from being rubbed off, or to col­
several areas of the scutum or scattered over most of lect larvae/pupae and let adults emerge in the labora­
its surface. As far as the identification of the mosqui­ tory. It seems that, although a variety of colour patterns
toes is concerned, the main setae are inserted in three occur, most of them are based on a common template.
70 5 Morphology of Mosquitoes

The nomenclature devised here for the principal part between the propleuron, mesepisternum and
elements of these patterns, is derived from Berlin procoxa, named the postprocoxal membrane.
(1969) who regarded the general distribution of the The mesopleural suture divides the mesopleuron
setae mentioned above (Fig. 5.4). The acrostichal transversely into a large anterior mesepisternum and a
stripe is always a very narrow row of scales confined to smaller posterior mesepimeron. The mesepisternum is
the median line of the scutum. It may be absent, or further subdivided into two pleurites, an upper
often it is reduced to an anterior or anteacrostichal mesanepisternum and a lower mesokatepisternum. The
patch and a usually larger posterior or postacrostichal former pleurite bears the mesothoracic spiracle. It is
patch of scales. If present, the acrostichal stripe divides small, displaced towards the postpronotum and often
the much broader median stripe which is located divided into four areas (Fig. 5.5). The prespiracular
between the dorsocentral rows of setae. The paired area is very narrow, confined between the postprono­
dorsocentral stripes lie in the dorsocentral areas. They tum and the anterior margin of the spiracle. A small
can be subdivided into inner and outer dorsocentral area immediately below the spiracle is called the
stripes. For convenience, if only one of them is present hypostigmal area. The smooth subspiracular area lies
it will be simply named the dorsocentral stripe. The below it and is usually connected to the sclerotized
lateral stripes border the scutum to varying degrees postspiracular area. Because the names of the four
from the anterior border to the wing base, and may be mentioned areas are so widely accepted and used
broken into several prescutal or supraalar fragments. in mosquito morphology, there is no practical
Between the dorsocentral and lateral stripes are the reason to use the designation mesanepisternum for
moderately broad, lanceolate or crescent shaped sub­ the description of the whole pleurite. Consequently, the
median stripes. The stripes are usually subdivided into mesokatepisternum is referred to as the mesepister­
anterior and posterior portions. Lateral to the pre­ num. The membranous anepisternal cleft lies above
scutellar area lie the prescutellar dorsocentral stripes, the mesepisternum, which is particularly well deve­
which can be fused with the dorsocentral stripes loped towards the ventral side. There it frequently
and/or the postacrostichal patch of scales above unites with the opposite mesepisternum separating the
(Fig. 5.4). The prescutellar area is often bare. fore and mid coxae from one another, thus concealing
The pleuron in advanced insects has become an the mesosternum. The very narrow upper portion of
enlarged, flattened and sclerotized part of the thoracic the mesepisternum or preala, bears the lobe-like pre­
wall, which it rigidly supports (Fig. 5.5). It is in ­general alar knob. The mesepimeron, which lies behind the
transversely divided into two main pleurites, the ante­ mesopleural suture, is also divided into a large upper
rior episternum and the posterior epimeron. These are mesanepimeron and a very narrow, bare, inconspicu­
separated by the pleural suture, and may be further ous mesokatepimeron. The latter is not mentioned in
divided into upper and lower pleurites which are the description of the species and consequently, the
denoted by the prefixes an- and kat-, thus anepister­ mesanepimeron will be referred to as the mesepimeron
num refers to the upper pleurite of episternum and (Fig. 5.5). Below the mesopleural suture lies the small
katepimeron to the lower pleurite of epimeron. A small triangular mesotrochantin. Slightly above and imme­
pleurite, the trochantin, is often present near the lower diately behind the mesocoxa and just below the
margin of the episternum. Another small pleurite, the mesokatepimeron, is the small triangular mesomeron
meron (meso- and meta-) was originally the posterior located.
part of the basicoxite which has become completely The metapleuron, like all other sclerites of the
separated from the coxa and forms a part of the tho­ metathorax, is greatly reduced. It is divided by the
racic wall. In a wing-bearing segment the pleuron metapleural suture in an anterior triangular or trape­
develops a dorsal (alar) articular process for the wing. zoid metepisternum, which bears the metathoracic
In mosquitoes the elongated, lobe shaped propleu­ spiracle and the haltere, and the posterior stripe-like
ron is located between the antepronotum and the pro­ metepimeron (Fig. 5.5). The small metameron lies
coxa (Fig. 5.5). The membrane which articulates the above the metacoxa.
procoxa with the prothorax is arbitrarily separated into Propleural setae are grouped above the lower
an anterior part lying between the prosternum and pro­ border of the propleuron (Fig. 5.6). The prespiracular
coxa, the anteprocoxal membrane, and the posterior area bears the taxonomically important prespiracular
5.1 Adults 71

setae, present in the genus Culiseta among European the mesepisterna, which are fused ventrally, and is
mosquitoes and some other genera worldwide (e.g. restricted to the region between the mesocoxae, having
Psorophora), except Aedes, Ochlerotatus, Coquille­t­ a strong median suture. The metasternum is reduced to
tidia, and Culex. a narrow crescent shaped sclerite.
The subspiracular area rarely supports setae, whereas Adult mosquitoes have three pairs of legs, one pair
the postspiracular area may bear the taxonomically sig­ on each of the thoracic segments (Fig. 5.1). They are
nificant postspiracular setae. Three groups of setae are referred to as fore legs, mid legs and hind legs. Each leg
typical for the mesepisternum. Displaced towards the consists typically of six segments, the coxa, trochanter,
wing base, inserted in the prealar knob, is the group of femur, tibia, tarsus and pretarsus, the first five being
prealar setae. The upper mesepisternal setae are grouped almost entirely covered with scales. The tarsus is subdi­
at the level where the mesepisternum narrows into the vided into five tarsomeres. These are, similarly to the
preala, and the lower mesepisternal setae are located flagellomeres, differentiated from true segments by
along the posterior margin, anterior to the mesotro­ the absence of intrinsic muscles. The basal tarsomere
chantin. The mesepimeron bears two groups of setae, I articulates with the distal end of the tibia. Between the
the lower mesepimeral setae located at the anterior tarsomeres there is no articulation; they are connected
lower corner, behind the upper mesepisternal setae, and by a flexible membrane so that they are freely movable
the upper mesepimeral setae at the posterior upper cor­ (Chapman 1982). The distal tarsomere V bears the pre­
ner, anterior to the metathoracic spiracle (Fig. 5.6). tarsus which consists of a pair of claws, or ungues, a
The postpronotum is usually covered with scales of ventral unguitractor plate where the tendon of the flexor
various size. Sometimes the patch is divided into an muscle of the claws is inserted, the paired pad-like or
upper and lower portion, called the upper postpronotal setose pulvilli, if present, one under each claw, and a
patch and lower postpronotal patch (Fig. 5.7). Both median spine-like empodium. The hind tarsus bears
anteprocoxal and postprocoxal membranes may be only one claw in females of the genus Limatus (Smith
covered with scales in some species, the patches are 1973). The tarsal claw may be simple or have a subbasal
named anteprocoxal and postprocoxal patch respec­ tooth. In females of most of the genera, except some of
tively. A group of scales on the hypostigmal area is, if Aedes, Ochlerotatus and Psorophora, all tarsal claws
present, consequently named the hypostigmal patch. are simple and of quite similar shape on all three pairs of
The subspiracular area may bear scales, the subspi­ legs. The shape of the tarsal claws of the fore legs can be
racular patch. The postspiracular patch of scales can used as a diagnostic character, especially in the genus
extend posteriorly onto the anepisternal cleft. The Ochlerotatus. In males, the outer claws of the fore and
scales of the mesepisternum are usually grouped into mid legs are much bigger than the inner claws, modified
two patches, the prealar one below the prealar knob, for grasping the females. The two claws of the hind legs
and the mesepisternal one blended to varying degrees are similar and may be simple or denticulated.
with the upper and lower mesepisternal setae. The The scaling of the coxa and trochanter is not usually
mesepisternal patch may be subdivided into an upper used as a character for species identification. However,
and lower portion (Fig. 5.7). The upper half of the pale scales can form specific patterns on a usually dark
mesepimeron is usually covered with scales, the mes­ background of the femur, tibia and tarsus, generally in
epimeral patch. It can extend downwards towards the the shape of longitudinal stripes and/or rings. The sur­
lower margin of the mesepimeron to a varying degree. faces of the segments are described as if the leg is held
The sternum in advanced insects is often greatly stretched straight out, forming a right angle with the
reduced in width and partly enfolded between the legs, longitudinal body axis. Thus, it can be referred to as an
while the two sternal apophyses are often united on a anterior and posterior, dorsal and ventral, as well as an
common base to form a Y-shaped furca. The proster­ anterodorsal surface, etc. (Wood et al. 1979). The
num in Culicidae is the region lying anteriorly between femur, when characteristically coloured, has basally
the procoxae, connected dorsolaterally with the more pale scales than apically.
propleuron. It bears a distinct median suture and some­ In all Diptera the mesothoracic wings are used for
times setae or scales. The scaling of the prosternum flight; the metathoracic are modified to form small
is of taxonomic significance in some Aedes and vibrating organs known as halteres, which control the
Ochlerotatus species. The mesosternum is obscured by equilibrium during flight. The wings consist of upper
72 5 Morphology of Mosquitoes

and lower epidermal layers, not fused along certain and are conspicuously broad and asymmetrical in
strengthening tubes, the wing veins. The complete sys­ Mansonia spp. The cross veins are usually without scales,
tem of wing veins is called the venation. Beginning except, e.g. in the genera Anopheles and Culiseta. The
from the anterior margin of the mosquito wing (Fig. 5.8), wing margin, from the apex of the costa until the level of
the first unbranched vein is the costa (C), which passes the base of the anal vein, is fringed with a row of scales.
around the apex of the wing and forms its anterior mar­ The veins and the wing margin are usually covered with
gin. The subcosta (Sc) is located closely behind the dark scales, which can aggregate to form distinct spots
costa and is also undivided. The radius (R) forks into an (e.g. some species of Anopheles, Culiseta and
anterior branch R1 and a posterior branch, or radial sec­ Ochlerotatus). Pale scales may be scattered or grouped
tor Rs, which branches again into R2+3 and R4+5. Vein into alternating patches along the veins in a pattern of
R2+3 divides once more into R2 and R3, while R4+5 considerable taxonomic value (Fig. 5.8c). In males, the
remains unbranched. The fourth vein, or media (M), scales are less dense and more easily rubbed off, even
bifurcates apically into M1+2 and M3+4. Likewise, the though of similar colouration and distribution as in the
fifth vein, or cubitus (Cu), divides into Cul and Cu2. females. The same is true for the scaling pattern of other
Finally, there is one anal vein (A) present. All veins are body parts. As a consequence the scaling pattern of
relatively straight but in Bironella spp. Cu1 and M are the males will not be discussed in detail in the species
wavy at their distal parts. The longitudinal veins may description nor used in the keys.
be connected by six different cross veins. Two of them
are situated close to the wing base, the humeral vein (h)
stretches from C to Sc and the arculus (Ar) from R to M
and Cu. The other four cross veins are displaced towards 5.1.3 Abdomen (Fig. 5.1, 5.9–5.12)
the wing apex. They are the subcostal-radial vein (sc-r)
extending from Sc to R, the sectorial vein rl–rs from R1 Basically the insect abdomen consists of eleven seg­
to Rs (apparent in Anophelinae, Fig. 5.8b), the radio- ments (only present in some primitive orders) and the
medial vein (r-m) from R4+5 to M and the medio-cubital nonsegmental telson (absent in most insects). An
vein (m-cu) from M to Cu. The veins divide the wing abdominal segment consists of a sclerotized tergum and
area into cells, the name for each cell is derived from sternum joined by membranous pleural regions. If a ter­
that of the vein forming its anterior margin. Where two gum or sternum is further subdivided each sclerite is
veins have fused or make one part of the anterior bor­ named tergite or sternite, respectively. Numerous reduc­
der, the cell is named after the posterior component. tions and amalgamations of segments can occur in the
Thus, when veins R4 and R5 coalesce, as in mosquitoes, abdomen, especially in the last abdominal segments
the area behind it is called cell R5 (Davies 1992). with the functions of mating, egg laying and disposal of
Almost all wing veins are both dorsally and ventrally feces. In both sexes, segments X and XI are generally
covered with scales. The scales may be narrow or broad represented by a dorsal lobe, or epiproct, and two

Fig. 5.8 Wing of (a) Culicinae; (b) Anophelinae (c) nomenclature of wing spots in certain Anopheles spp.
5.1 Adults 73

lateroventral lobes, or paraprocts. In mosquitoes the suggested to represent the divided gonapophyses of
first segment of the abdomen is somewhat reduced. The abdominal segment IX (Davies 1992). For mosquitoes,
median part of tergum I is often not visible from above. Horsfall and Ronquillo (1970) showed the development
In such cases only lateroterga are apparent (Fig. 5.4). of the aedeagal complex from the genital primordia of
The rest of the pregenital segments, II–VIII in males and segment IX. Some authors claim that claspers of mos­
II–VII in females, are well developed. The posterior part quitoes are parameres and not homologous with the
of each segment overlaps the anterior part of the next claspers of Ephemeroptera (Snodgrass 1935; Seguy
segment; the segments are joined by an intersegmental 1967). Thus parameres and claspers should not be con­
membrane. The pleural membranes of segments I–VII fused, as the latter most probably are derivates of
bear a pair of spiracles anterolaterally (Knight and segment IX as in other nematocera (Dahl 1980).
Laffoon 1971). In males, the segment IX supports the In the present work the widely accepted nomenclature
reproductive opening and is highly modified into a well of gonocoxite and gonostylus is applied for practical
developed copulatory apparatus, the hypopygium. The reasons and without implications of the true origin.
postgenital segments X and XI are reduced, fused and The uncertainty of origin of the various structures
partly telescoped into segment IX, forming the procti­ and consequently the variation in terminology are fur­
ger. In males, both the proctiger and, in some species of ther complicated by the fact that a few hours after emer­
Culiseta, the abdominal segment VIII may be of taxo­ gence of the males, the abdominal segments VIII and IX
nomic value. In females, the genital segment VIII is rotate through 180°. This inverts the terga, sterna and
well developed but shorter than segment VII. The open­ genitalia into an upside-down position. Thus, the aedea­
ing of the internal reproductive organs lies posterior to gus lies above the anus instead of being under it and the
the border of segment VIII. Segment IX is reduced to hindgut is twisted over the reproductive duct. However,
less than a third of the size of the preceding segment and it is unanimously accepted for all the structures to be
bears the rest of the postgenital segments, the proctiger referred to as though they were in their correct, prerota­
(epiproct and paraprocts), and the cerci, which support tional, morphological position. All drawings of the gen­
oviposition. Most of these structures are partly tele­ italia are consequently of dorsal, prerotational view
scoped into segment VIII. The terga and sterna of the (Figs. 5.10–5.12). The synonyms most frequently used
eight easily distinguishable segments (except sternum I) for the genital structures are given in brackets.
may be entirely clothed with decumbent scales or cov­ The tergum, sternum and pleurae of segment IX are
ered with setae only. usually fused into a complete ring (Fig. 5.9). The ter­
Insect genitalia in both sexes are said to be derived gum IX is often bilobed, each lobe bearing a various
from modified abdominal appendages, present in other number of strong setae. These are not always shown in
arthropods and used for mating and egg laying. the drawings of the hypopygia, except in cases of taxo­
Basically, each genital appendage, the gonopod, has nomic importance. The largest unit of the male genita­
been regarded as consisting of a limb base, the gono­ lia is the gonocoxite (basimere, basistyle, coxite,
coxite, which shoulders an apical appendage, the gono­ sidepiece or paramere according to some authors)
stylus, and a median process, the gonapophysis, arising which articulates with sternum IX (Fig. 5.9). The
from its basal region. Some or all of these parts may be gonocoxite may be a sclerotized, truncate cone or may
reduced, obliterated or fused, therefore the homologies have the dorsal and ventral surfaces mesally separated
of the various structures are not known with certainty by a median membrane. It may lack lobes, as in most
for all orders of advanced insects (Davies 1992). Anopheles and some Aedes and Ochlerotatus species,
The male genitalia are said to be derived from or be variously lobed. These lobes are named with the
appendages of the genital segment (IX). In some appropriate combination of position adjectives (e.g.
insects such as the Ephemeroptera these consist of a pair basal lobe, apical lobe, subapical lobe) without intent
of lateral claspers, the gonocoxite with the gonostylus. to imply homologies (Knight and Laffoon 1971). The
They grip the female in copulation, together with a gonocoxite and its lobes are covered with sparse or
pair of parameres, which guide the median intromit­ dense setae of different length, width and shape, some­
tent organ, the aedeagus. Parameres of many orders are times with scattered scales. The movable, elongated
most probably not homologous throughout the class of appendage, the gonostylus (clasper, distimere or disti­
insects. But together with paired rudiments, the meso­ style) is articulated with the gonocoxite at or close to its
meres, from which the aedeagal structures develop, are apex. The gonostylus usually bears one or more setae,
74 5 Morphology of Mosquitoes

the apical spines of gonostylus (Wood et al. 1979), parameres and parameral apodemes, while in this pub­
which are often short, spine or peg-like and situated lication these structures will be referred to separately as
apically or near the apex of the gonostylus. Dorsomesally in Harbach and Knight (1980).
to the gonocoxite and laterally to the aedeagus, a paired The aedeagus (mesosome, phallosome), is the
sclerite, the paramere, is articulated with the gonocoxal median structure of the genitalia. It may be quite vari­
and parameral apodemes, thus supporting the aedeagus able in shape but is often bulb or flask shaped (Figs. 5.10
(Fig. 5.9). Some authors apply the term phallosome to and 5.11). It lies medially, above the ventral surfaces
the complex of structures made up of the aedeagus, of the gonocoxites and below the proctiger (the posi­

Fig. 5.9 End of abdomen of Aedes/Ochlerotatus sp. – male, lateral view

Fig. 5.10 Hypopygium of Anopheles sp.

5.1 Adults 75

Fig. 5.11 Hypopygium of Aedes/Ochlerotatus sp.

tion is switched after rotation). The lateral borders of era and related species often differ considerably in
the aedeagus are usually sclerotized and form two detail and are therefore of great taxonomic value.
darkly coloured plates, the lateral aedeagal plates. In most Anophelinae, one or more strong, spine-
Dorsal to the aedeagus lies the proctiger (anal seg­ like setae (parabasal setae), are sunk into a cuticular
ment, anal cone, tenth segment), a complex formed by socket or elevated on a tubercle, both located dorsoba­
segment X, the cercal sclerite and the paraprocts sally on the gonocoxite (Fig. 5.10). Additionally, a
(Figs. 5.9–5.11). The proctiger bears the anus and is strong spine-like seta, the internal seta (mesal seta), is
largely membranous. Usually the sclerotized parts of mesally attached to the gonocoxite of many species.
the proctiger are tergum X, a portion of the cercal One or more pairs of spine-like or leaf-like setae, the
sclerite and the paraprocts (tenth sternite) (Figs. 5.11 leaflets of aedeagus (aedeagal setae), are often attached
and 5.12). Tergum X is often developed as a pair of to the apex of the aedeagus. The proctiger is usually
dorsally directed arm-like tergites, arising lateroba­ greatly reduced or membranous (cone shaped). It is
sally on the proctiger and sometimes confluent with hardly visible, especially after decolouration with
the basal part of the paraproct. The paraproct is paired, KOH during slide preparation, so it is not shown in any
usually a well sclerotized sclerite, situated laterally on drawing of anopheline hypopygia. Only some ano­
the proctiger. Its strongly sclerotized apex can be den­ phelines (subgenus Nyssorhynchus) have well sclero­
ticulated or covered with numerous short spine-like tized paraprocts. The claspettes of Anopheles may be
setae (in Culex). divided longitudinally into two or three lobes, the
Largely membranous projections of the gonocoxites inner, median and outer lobe. All of these can bear
support variably shaped ventromesal lobes, the clas­ spine-like or flattened spatula-like setae.
pettes (harpes, harpagones), which are well devel­ In the genera Aedes and Ochlerotatus, the typical
oped in Anopheles, Aedes, Ochlerotatus and claspette is divided into a proximal, more or less cylin­
Psorophora but absent in Culex and other genera drical portion, the claspette stem, and a single leaf
(Figs. 5.9–5.12). The male genitalia of different gen­ shaped division, the claspette filament (Fig. 5.11).
76 5 Morphology of Mosquitoes

Fig. 5.12 Hypopygium of Culex sp.

In the subgenus Aedes, the apex of the claspette is most species of the genera Aedes, Ochlerotatus and
bifurcate (claspetoid) with the two branches bearing a Psorophora while in other genera the cerci are short
few setae, while in Aedimorphus and Stegomyia it is of and incons­picuous.
variable shape, covered with numerous setae or bare.
In Culex (Fig. 5.12), the apex of the paraproct is
called the paraproct crown. It may bear a group of
dense, short setae, be denticulate or with a combina­ 5.2 Larvae
tion of both. The lateral aedeagal plates are particu­
larly well developed and subdivided into a lateral The body of the mosquito larva is divided into three
portion, the outer division, and a mesal portion, the principal parts, the completely sclerotized head cap­
inner division. The outer division is often further dif­ sule, the flattened thorax composed of three fused seg­
ferentiated into lateral arms or teeth, the inner division ments which is distinctly broader than the two other
of some species is further divided into a dorsal and a parts in fully grown instars, and the abdomen which
ventral arm. Laterobasally from the paraproct origi­ consists of ten segments. Mosquito larvae are distin­
nates a ventrally pointed process, the ventral arm of guished from all other dipterous larvae by the combina­
the paraproct (basal arm of tenth sternite, basal arm of tion of the following characters: the presence of distinct
anal segment). labral brushes (lateral palatal brushes), exceptions are
Mosquito females do not possess a true appendicular found in carnivorous larvae, e.g. Toxorhynchites spp.,
ovipositor. The posterior segments of the abdomen the expanded thorax and the tubular or cylindrical
form a short apparatus modified for egg laying breathing tube, the siphon. The siphon is located on the
which acts as a functional ovipositor. The structures dorsal surface of abdominal segment VIII in all genera,
of the postgenital segments are greatly reduced. The except Anopheles, Bironella and Chagasia. In the lar­
best developed are the postgenital plate and cerci. vae of Dixidae, which possess labral brushes but lack a
The cerci (Fig. 5.1) are long and readily visible in siphon, the thoracic segments are not fused or broad­
5.2 Larvae 77

Fig. 5.13 Types of larval setae: (a) simple; (b) aciculate; (c) pinnate or plumose; (d) lateral branched; (e) fan like; (f, g)
branched; (h) stellate; (i, j) dendriform; (k) palmate (after Marshall 1938)

ened. In the larvae of the Chaoboridae, especially of rearing of earlier instars until the fully grown fourth-
Mochlonyx spp. which have a siphon, the mouthparts instar is reached. The following description of the larval
are converted for a predacious life and not used for fil­ morphology is mainly confined to those characters which
ter feeding. They have long, ventrally curved prehen­ are of taxonomic importance and used in the keys.
sile antennae, adapted to capture aquatic prey. In Although the larvae of the anopheline and culicine
addition, the chaoborid larvae possess conspicuous subfamilies differ from one another in many respects,
hydrostatic organs, one pair in the thorax, the other in they are structurally similar. Therefore, they are des­
abdominal segment VII, which allow the larvae to float cribed together, directing attention to those characters
in a horizontal position in the water. which are exhibited by one or the other subfamily.
Mosquito larvae pass through four larval instars. The larval body is ornamented with 222 pairs of
During their development various diagnostic characters setae (Forattini 1996). Their arrangement (called
change, e.g. the size of the head capsule, the number of chaetotaxy) and structure, are important taxonomic
pecten teeth or the number of branching of certain features. The setae may be simple or variously branched
setae may increase. For this reasons most larval identi­ (Fig. 5.13). A simple seta is undivided and usually
fication is based on the fourth-instar. This may require cylindrical and apically attenuated. An aciculate seta
78 5 Morphology of Mosquitoes

consists of a main stem with lateral secondary branches d­ ifferent species. Sometimes the leaflets are narrowed
which are short and delicate. The branching may be or shouldered more or less abruptly at or beyond the
sparse or dense. A branched seta consists of a long or middle, and thus divided into a wider proximal part, or
short stem split into two or a few more divisions usu­ blade, and a narrower distal part, called the filament.
ally approximately equal in length, none of them can Palmate setae support the larval body at the water sur­
be recognised as the continuation of the main stem. face film while feeding. When the anopheline larvae
A branched seta, which has no apparent stem and is lie just beneath the water surface, the setae are held in
divided practically at the base into several more or less an open position and the leaflets are spread to at least
equal divisions, is called a tuft. A stellate seta has a 180°. When the larvae dive, the leaflets become folded
very short stem, is basally branched, the stiff branches and hold an air bubble inside which is used to break the
radiating from the stem at various angles. A pinnate or surface film at the next rise to the surface.
plumose seta consists of a main stem with regularly
arranged, long lateral branches, which usually shorten
towards the apex. A lateral branched seta has a main
stem with lateral branches, irregularly arranged and 5.2.1 Head (Fig. 5.14)
often irregular in length. A fan-like seta, which can be
found in the ventral brush of the larva, consists of a Although the heads of culicine and anopheline larvae
very stout stem, usually apically widened, and many resemble each other in structural and other features,
branches. A dendriform seta has various stems with they are noticeably different in shape. In most species
branches that are divided and subdivided so that they of culicine larvae, the head is significantly broader
resemble the branches of a tree. Specialized setae, the than it is long, whereas the head of anopheline larvae
so called palmate setae, characteristic of the genera is normally longer than broad, but the ratio of the
Anopheles, Bironella and Chagasia, can be found on length to the width may vary in different species.
several abdominal segments. A palmate seta consists The head capsule is formed by four sclerotized
of a short stem from which leaf shaped, flattened plates, the frontoclypeus (dorsal apodeme), a large
branches, called the leaflets, extend. They may have sclerite forming the dorsal aspect of the head, and two
smooth or serrated margins. The number of the leaf­ epicranial plates (lateralia), covering the lateral sur­
lets, their shape and marginal serration can vary in faces as well as the ventral surface and the fused

Fig. 5.14 Head of larva – dorsal view (a) Anophelinae; (b) Culicinae
5.2 Larvae 79

c­ ollar-shaped occiput and postocciput. The first three The antennal shaft is usually covered with small ante­
plates meet dorsally in the epicranial suture. In some riorly projecting spines or spicules, only in the subge­
species, the frontoclypeus has areas of darker coloura­ nus Finlaya and in Oc. pulcritarsis is the surface of the
tion which gives rise to a specific pattern, sometimes shaft smooth.
of diagnostic value (e.g. in An. algeriensis). To evalu­ Two pairs of eyes are situated medio-laterally at the
ate this character correctly, the larval head must be epicranial plates. The dark crescent shaped anterior
examined under low magnification. The crescent patches are the primordial compound eyes of the future
shaped labrum is located anterior to the frontoclypeus. adult showing through the larval skin. The smaller
Its well developed ventral surface or palatum carries simple larval eyes (stemmata) are located just behind
the conspicuous lateral palatal brushes. Each lateral them. Posterior to the frontoclypeus and the epicranial
palatal brush is composed of numerous long, some­ plates lies the occipital foramen, the opening of the
times sigmoid setae. The brushes can be moved rapidly cranium to which the cervix (neck) is attached.
and synchronously to produce currents in the surround­ The head bears up to 18 symmetrically paired setae,
ing water and thereby attract floating food particles. which are numbered 0-C to 17-C.The letter “C” is used
The presence or absence of serrations on the setae of to indicate that the setae are located on the head or
the lateral palatal brushes may distinguish those larvae caput. Two more setae, affiliated with the letter “C”,
that brush food particles from those that sweep the C-18 and C-19, are articulated to the cervical sclerite.
water as filter feeders. In predatory larvae, the brushes The setae which are of diagnostic importance and used
have only a few, stout, prehensile setae. The median for identification in the keys, arise from the fronto­
part of the palatum bears a brush, the anteromedian clypeus and are numbered 2-C to 7-C (Fig. 5.14). They
palatal brush, which is much less developed than the provide their diagnostic indication not only by their
lateral palatal brushes. The larval mouthparts are rarely relative position but also by their length, degree of
used for taxonomic purposes and they will not be dis­ branching and other characteristics. One additional
cussed in detail here. Besides the labrum, they consist seta, 8-C also arises from the frontoclypeus. Seta 1-C
of two pairs of flattened sclerites, the mandibles and is prominent, forwardly directed, arising on the labrum.
maxillae and the mentum (labium). The maxillary The inner and outer clypeal setae 2-C and 3-C are
palps arise close to the base of each maxilla. They are located close to the anterior margin of the fronto­
much more developed in anophelines than in culicines. clypeus. In culicines they are either greatly reduced in
For particular descriptions of the mouthparts see size or invisible, or absent. In anophelines they are
Clements (1992) and Pucat (1965) and of the lateral among the most conspicuous setae, and their position
palatal brushes Dahl (2000), Dahl et al. (1988), and in relation to one another is used to separate several
Harbach and Knight (1980). subgenera within Anopheles. The postclypeal seta 4-C
The antennae, which arise at the anterolateral cor­ is located at some distance behind the clypeal seta in
ners of the head, are slender and slightly tapering sen­ anophelines and it is more weakly developed. In most
sory appendages but could be enlarged, broad and culicine species the postclypeal setae 4-C are very
flattened in the genus Aedeomyia or divided with a short, usually multiple branched and situated closer to
freely articulated distal portion in the genus Mimomyia. the midline than the frontal setae. The frontal setae
They may be shorter than the head and either straight consist of three pairs, the inner (5-C), median (6-C)
or slightly curved (e.g. genera Aedes and Ochlerotatus, and outer (7-C) frontals. In Anopheles larvae the fron­
except Oc. diantaeus, and subgenus Culiseta) or as tal setae arise more or less side by side, forming a
long as or longer than the head and evenly curved (e.g. transverse row. Usually they are plumose, except e.g.
genera Culex and Mansonia and subgenus Culicella). in An. plumbeus, which has very short and simple
Each antenna bears six setae, which are numbered 1-A setae. In the other genera, except a few Aedes species,
to 6-A. The antennal seta 1-A projects from the shaft setae 6-C are displaced forward, sometimes even in
of the antenna; it can be simple and inconspicuous front of 4-C, forming a triangle with its two compan­
(e.g. Oc. geniculatus) or mostly has multiple branches ions 5-C and 7-C. The frontal setae are mostly well
of large size (e.g. Cs. morsitans). Its position on the developed and branched. The outer frontal setae 7-C
antennal shaft is often of diagnostic importance. Setae arise near the edge of the frontoclypeus close to the
2-A to 6-A are minute and located at the antennal apex. antennal bases. They are often more densely branched
80 5 Morphology of Mosquitoes

Fig. 5.15 Thorax and abdomen – dorsal setation (a) Culicinae; (b) Anophelinae

than the inner or median frontal setae. In larvae of ends with the one nearest the midventral line, the only
Ur. unguiculata setae 5-C and 6-C are unique, they are exception being seta 0-P which is articulated lateral to
long and stout. Setae 9-C and 10-C are located at the 1-P and displaced towards the mesothorax. Many of
epicranium, below the primordial compound eyes, the the 42 pairs of thoracic setae may be useful for identi­
latter being displaced more laterally. All other setae fication, but only setae 1-P to 3-P are used in the larval
arise on the ventral side of the head. keys, because there exist other convenient characters
for identification, especially on the head and the last
abdominal segments. Setae 1-P to 3-P usually arise
very close to each other in a line and may, at a first
5.2.2 Thorax (Fig. 5.15) glance, be mistaken for branches of a single seta. They
are often situated on a sclerotized tubercle.
The thorax is the most conspicuous part of the larvae.
Its cuticle is mainly or entirely membranous, and during
the growth of the instars it becomes increasingly larger, 5.2.3 Abdomen (Figs. 5.15– 5.17)
relative to the head. Just before pupation of the fourth-
instar larvae, it is much broader than the head. As in The larval abdomen consists of ten segments, the first
the adult, the thorax consists of three segments, the seven segments closely resemble each other. Abdominal
pro-, meso-, and metathorax. The segments are com­ segment I bears 13 pairs of setae and each of segments
pletely fused, their borders can only be determined by II–VII has 15 pairs. When referring to a seta, its num­
the arrangement of the setae in three distinct sets. The ber is followed by the segment number, for example
symmetrically paired setae are numbered 0-P to 14-P 3-VI refers to seta 3 on abdominal segment VI. The
on the prothorax, 1-M to 14-M on the mesothorax and numbering of the setae follows the same principle as
1-T to 13-T on the metathorax. The numbering starts described for the thorax. Of all pairs of abdominal
with the pair of setae closest to the middorsal line and setae available on segments I–VII, only a few are used
5.2 Larvae 81

Fig. 5.16 Lateral view of larval abdomen – Culicinae

anterolateral spiracular lobe

7-S
stigmal opening posterolateral spiracular lobe
6-S
anterior spiracular lobe upper anal seta (2-X)
12-S
tracheal trunk 9-S
8-S 1-S
tergal plate 2-S

0-VIII saddle
1-VIII lower anal seta (3-X)

pecten plate 2-VIII

3-VIII
4-VIII anal papillae
5-VIII
14-VIII
saddle seta (1-X)

abdominal segment VIII

cratal seta (4-X)

abdominal segment X

Fig. 5.17 Lateral view of larval abdomen – Anophelinae

82 5 Morphology of Mosquitoes

for identification in the keys. In anophelines, seta 1 is pis, the comb scales are much more elongated than in
of palmate type in some or all abdominal segments the other genera and form two regular rows. In fourth-
(Fig. 5.15b). The number of segments with fully devel­ instar larvae of anophelines there is no structure which
oped palmate setae, and the shape of the branches, var­ corresponds to the culicine comb (Fig. 5.17).
ies between species. To distinguish between the two In culicines, five out of the seven pairs of setae on
species so far known in the Anopheles Claviger the lateral sides of segment VIII are located posterior
Complex, the branching of the antepalmate setae 2-IV to the comb scales. They cannot be homologized with
and 2-V is a useful characteristic. These setae are the setae on the first seven segments, except the ventral
located anterior to the palmate setae and closer to the most one which is consequently named 14-VIII instead
dorsomedian line, than the setae 3–5 of the segments. of 6-VIII. All setae are numbered, successively from
The most laterally placed seta 6 is the longest and most dorsal to ventral, 0-VIII to 14-VIII. Only 1-VIII to
conspicuous on segments I–VI. In European culicines, 5-VIII are distinct (Fig. 5.16) and in the fourth instar
no palmate setae are present (Fig. 5.15a). In the genus larvae the setae 1-VIII, 3-VIII and 5-VIII are usually
Culex, setae 1 on segments III–V show a diagnostic strongly branched, whereas the intermediate ones,
number of branches useful in separating species of 2-VIII and 4-VIII, are shorter and nearly always sim­
Cx. p. pipiens and Cx. torrentium. In anophelines, each ple, except in Coquillettidia. Both 0-VIII and 14-VIII
of the abdominal segments I–VII bears a sclerotized are minute and of no taxonomic importance.
tergal plate anteriorly, and may also have one or more At the base of the siphon, two small lateral projec­
smaller plates posterior to it near the centre of each tions arise close to its ventral margin, each called acus.
segment. Usually, these plates do not occur in culicine They are the points of muscle attachment which enable
larvae, except Or. pulcripalpis which in the fourth- the siphon to be bent posteriorly. In all species of the
instar larva has sclerotized plates of different sizes dor­ subgenus Stegomyia, the acus is absent and in Ae. vit­
sally on segments VI–VIII. tatus it is very indistinct. The siphon of the culicines is
Segment VIII is entirely different from the preced­ one of the most useful structures for identification. Its
ing segments. It bears the only functional external shape and proportions vary considerably. Very often
openings of the metapneustic respiratory system, the the siphonal index is used for identification, its value is
spiracles, which are located posteriorly on the dorsal expressed as the ratio of the length of the siphon to its
surface of the segment. In culicines, the spiracles are basal width. Harbach and Knight (1980) and Belkin
situated at the tip of a long, tubular and cylindrical (1962) suggested measuring the width of the siphon at
organ called the siphon (Fig. 5.16). In anophelines, the its middle. In many cases such measurement is diffi­
siphon is almost completely reduced to the spiracular cult and quite subjective. For this reason it is suggested
plate and often is said to be absent (Fig. 5.17). to measure the width of the siphon at its base (Gutsevich
On each side of segment VIII a number of decum­ et al. 1974; Forattini 1996). The index may vary from
bent scales can be found. The whole structure is called less than 2.0 in some species, such as Oc. mariae, to
the comb (Fig. 5.16). Each comb scale is directed pos­ over 7.0 in others, like Cx. hortensis. In some Culiseta
teriorly and fringed with small spines. All spines may species the ratio of the siphonal length to the width of
be of the same length or the median, or terminal spine its apex is diagnostic. The siphon also carries a pair of
can be exceptionally distinct and longer than the oth­ ventrolateral rows of stout, sclerotized spines, the
ers. The shape of the spines can only be studied ade­ pecten teeth. Each row is known as the pecten. A single
quately under sufficient magnification, therefore this pecten tooth usually has 1–4 lateral denticles on its
character is used in the keys only to separate a few spe­ ventral margin. In culicines the pecten teeth commonly
cies within the genera Aedes, Ochlerotatus and Culex. increase uniformly in size toward the apex. All teeth
The number of comb scales varies greatly with the spe­ may be evenly spaced, but in some species the distal
cies, from 5 to 7 to more than 100 and they may be pecten teeth may be more widely and irregularly
arranged in a single row, a double row or in an irregu­ spaced than the others. In the keys they are referred to
lar pattern. The total number of comb scales, with its as being detached apically. The proportion of the
range of variability, is of diagnostic value. In Ur. siphon to which the pecten extends from the base, is of
unguiculata, the comb scales arise from the posterior taxonomic importance. It may be short, with a few
margin of a sclerotized lateral plate. In Or. pulcripal­ teeth which do not exceed the middle of the siphon, or
5.2 Larvae 83

it may extend almost to the apex of the siphon, as in lated behind the pecten plate (Fig. 5.17). Seta 2-S is
Oc. cataphylla. In Cs. longiareolata the pecten con­ located dorsoapically, closely to the spiracular appara­
sists of a row of teeth which are widely spaced along tus in culicines and on the pecten plate in anophelines.
the entire siphon. In Cs. fumipennis the stout teeth con­ The spiracles are surrounded by the spiracular plate. It
tinue on in an irregularly row of large spines. In the is a five-lobed valve which closes the openings during
subgenus Culiseta typical pecten teeth are found only submersion of the larva. These lobes are the anterior
at the base of the siphon. They are then followed by a spiracular lobe and two pairs of anterolateral and pos­
row of thin, hair-like setae. Among the European culi­ terolateral spiracular lobes. They bear several setae,
cine species, the pecten is absent in the species of 3-S to 13-S, of which only 9-S, the second one below
the genus Coquillettidia and in Or. pulcripalpis, and the apices of the posterolateral, largest valves, are used
elsewhere in the genera Armigeres, Mansonia, in the keys. It is elongated, thickened and hook-shaped
Orthopodomyia and Toxorhynchites. in some Ochlerotatus species. In the genus Coqui­
In anophelines which lack an elongated siphon, the l­lettidia the spiracular plate is highly modified, bearing
pecten is situated immediately below the spiracles and inner and outer spiracular teeth at the apex and a row
consists of a row of alternate long and short teeth aris­ of teeth on the anterior surface known as the saw, for
ing from the posterior side of a triangular sclerite, the piercing and penetrating submerged parts of plants in
pecten plate (Fig. 5.17). The two plates on each side of order to obtain oxygen. Similar modifications are not
segment VIII are connected by a U-shaped band. The found in any other European genus, but may be charac­
setae 0-VIII to 14-VIII are located ventrally to the teristic of larvae of all Mansonia, some Culex (subgenus
pecten and are less conspicuous than in culicines. Lutzia), Mimomyia and Hodgesia species occurring
The siphon and spiracular plate bear 13 pairs of elsewhere.
setae designated 1-S to 13-S. In culicine larvae, the Segment IX is reduced, its remnant is visible as a
siphon is adorned with one or more pairs of tufts or small ring at the base of the anus bearing segment X in
simple setae on its ventral and/or lateral surface, the many species, but in some others, like in Ur. unguicu­
siphonal setae 1-S (Fig. 5.16). If there is more than one lata, this rudiment disappears entirely. It does not exist
pair of setae 1-S present, the basalmost is named la-S, as a separate morphological unit and is of no taxo­
the next one towards the apex of the siphon lb-S and so nomic importance.
on, proceeding distally (Darsie and Ward 1981). Larvae The most posterior, or anal segment X is narrower
of the genus Culex have several pairs of tufts, they may than the others, forms an angle to the ventral side of
be arranged symmetrically and sometimes the penulti­ segment VIII and bears four pairs of setae, 1-X to 4-X.
mate tuft is found to be situated dorsally out of line It possesses a curved, sclerotized plate called the saddle.
with the others, or they may arise in a more or less zig- Although in many species the plate is saddle-shaped
zag row. The total number of siphonal tufts, their length and extends down the lateral sides of the segment to
compared to the width of the siphon at the point of various degrees, e.g. almost reaching to the midventral
articulation of each 1-S, and their position on the line in Oc. punctodes, it completely encircles the anal
siphon, is often characteristic. A single paired siphonal segment in others. The shape of the saddle is of diag­
tuft is usually present, either at the base, as in Culiseta, nostic value in many species. It bears a lateral saddle
which is the principal diagnostic feature of this genus, seta, 1-X. In the fourth-instar larva the saddle seta
or between the mid length and the apex of the siphon, arises well within the saddle, closer to its posterior
as in other culicines. The position of 1-S with respect margin than to its ventral margin. Its length compared
to the pecten is used to separate some species of to the length of the saddle is frequently used for iden­
Ochlerotatus. Usually 1-S is attached distally to the tification. The posterior margin of the saddle may bear
pecten, but sometimes it is attached basally to the dis­ denticles or spines of varying shape. Dorsally at the
tal pecten teeth, and is then described as being attached distal end, the anal segment bears two long, paired
within the pecten. The number and length of the setae, the upper anal seta 2-X and the lower anal seta
branches of 1-S may vary and are used for species 3-X. In anophelines both pairs are composed of mul­
identification. Occasionally additional setae can be tiple branched setae, which are often hooked and sup­
found on the dorsal surface of the siphon (subgenus port the larvae while in horizontal position (Fig. 5.17).
Rusticoidus). In anopheline larvae, seta 1-S is articu­ In most culicines, seta 2-X is multiple branched and
84 5 Morphology of Mosquitoes

3-X is a long stout seta which is usually either simple regulation. The length of the anal papillae varies
or only slightly branched (Fig. 5.16). Along the mid­ remarkably in different species. In salt marsh species
ventral line of the anal segment, close to its apex, arise and others which are associated with brackish or alka­
a number of long setae 4-X, which make up the ventral line water, the anal papillae are extremely short. In
brush or fin. The number of 4-X can vary from two, a some species the length of the papillae depends upon
few (e.g. Malaya, Sabethes, Wyeomyia) to many more the physico-chemical conditions of the water in which
(e.g. Ochlerotatus). All setae of the ventral brush are the larvae develop, as it is well known for Oc. caspius.
fan-like and they act as a rudder during swimming. Usually the two pairs are of the same length, but
Some or all of these setae are attached to a heavily occasionally one pair may be longer than the other.
sclerotized network of bars which resembles a ladder The length and shape of the anal papillae are regularly
or grid for greater basal support. In anophelines, all used for identification but often they are broken off or
setae arise from the grid, while in culicines, the setae hardly visible, especially in mounted specimens.
may be situated partly on and partly proximal to the
grid. Those setae attached to the grid are called the
cratal setae and those attached to the segment anterior
to the grid are called the precratal setae (Fig. 5.16). 5.3 Pupae (Fig. 5.18–5.21)
The number of precratal setae is an important feature
to separate various Ochlerotatus species. Sometimes it The mosquito pupae provide less distinct characters for
is not easy to differentiate between the cratals and pre­ identification than the larvae or adults. Although there
cratals, especially when they are close together. In this are differences in the external morphology and chaeto­
case, attention should be focused on the proximal end taxy of the pupae in different genera and even at the
of the grid and the first tuft which is attached to it. species level, no attempt is made here to include the
Then the number of tufts anterior to it should be pupae in the keys. It is easier to rear pupae, which are
counted. The anal segment terminates with two pairs collected in the field to the adult stage and then identify
of flexible, papilliform structures, the anal papillae them. However, occasionally there may be difficulties
which surround the anus and are involved in osmo­ in separating certain closely related species in the adult

Fig. 5.18 Pupa – lateral aspect of the body

5.3 Pupae 85

or larval stage, e.g. Cs. annulata and Cs. subochrea, or cephalothorax, are located posterior to the respiratory
An. claviger s.s. and An. petragnani. In these cases trumpets. Between the sheaths of the wings and mouth­
some pupal characters are needed for proper identifica­ parts, the sheaths of the legs are visible, the tarsi being
tion. Thus, a brief overview of the external morphology curled up under the wing apex.
and chaetotaxy of mosquito pupae is provided. The abdomen of the pupa is flattened dorsoven­
The body of the pupa consists of a large globular trally and consists of nine segments, the last of which
anterior portion, the cephalothorax, and a narrower articu­ is very small and carries the terminal paddles
lated abdomen, which is kept flexed under the cephalo­ (Figs. 5.18 and 5.19). The segments are sclerotized,
thorax and used to propel the individual while swimming connected with intersegmental membranes and freely
(Fig. 5.18). Mosquito pupae, unlike the pupae of most movable on each other in flexion and tension, but
other insects, are quite mobile and can rapidly dive with little or no lateral movement. The first abdomi­
from the water surface when disturbed. Usually they nal segment bears a pair of conspicuous palmate
remain at the water surface most of the time, with the setae (1-I), which resemble those of the Anopheles
paired respiratory trumpets in contact with the air. larvae and have the same function in supporting the
The general appearance of the mosquito pupa with pupal body at the water surface in the upright posi­
its division into only two obvious parts is mainly due to tion. Again the genera Coquillettidia and Mansonia
the morphology of the pupal case. The head with the are exceptions. Due to the permanently submerged
sheaths of the mouthparts together with the thorax with life of the pupae, the seta 1-I is not of the palmate
the sheaths of the wings and legs appear to form one type, but short and simple. Both ventrally and later­
structure, the cephalothorax. The flattened head with the ally, the first abdominal segment is largely membra­
mouthparts is located at the front of the cephalothorax. nous. Abdominal segments II to VII are more or less
The mouthparts are bent beneath it along the ventral sur­ the same size. They consist of completely sclerotized
face to its posterior part, like a keel. The pupal cuticle is rings without pleural membranes between the terga
transparent and the compound eyes of the adult are vis­ and sterna. Segment VIII is smaller than the preced­
ible at the sides of the head and behind these, the stem­ ing segments and bears on its dorsal side a median
mata of the former larva. The antennae arise in front of caudal lobe of tergum IX. The lateral lobes of the
the compound eyes in the upper part, and are directed tergum IX are developed into the paddles, and the
backwards in a curved line over the sides of the thorax. sternum IX is an indistinct transverse band. The pad­
The broad convex scutum of the mesothorax extends on dles are irregularly oval in shape with a narrow base,
the anterior dorsal surface of the cephalothorax. Along and overlap by about half of their width. They are
its median dorsal line a crest-like ridge or median keel is the main organs of movement of the pupae. They are
visible. This ridge forms the line of weakness, the ecdy­ provided with a median longitudinal strengthening
sial line, along which the cuticle splits before the emer­ or midrib. Close to the end of the midrib arises an
gence of the adult. The respiratory trumpets project apical seta (1-P). In pupae of Anopheles a small
from the sides of the scutum. In pupae of culicine mos­ accessory seta (2-P) is present above the apical seta
quitoes the respiratory trumpets are long and cylindri­ on the ventral side (Fig. 5.19a), while in Culex the
cal. An exception, as with the siphon of the larvae, can accessory seta arises dorsally side by side with 1-P
be found in the genera Coquillettidia and Mansonia. In (Fig. 5.19b). In the genera Coquillettidia and
this case, the trumpets taper apically and have a strong Mansonia, both the apical and accessory setae are
sclerotized hook, adapted for piercing submerged parts absent. In many species the margin of the paddle is
of aquatic plants. In pupae of anopheline mosquitoes, fringed with spicules or small spines which are of
the respiratory trumpets are shorter and broad, with a taxonomic significance.
flap-like appearance. The base of the trumpet is very Caudal and ventral to the median caudal lobe lies
flexible allowing it to be easily moved into position medially a small rudiment of segments X and XI, the
when brought to the water surface. A tracheal trunk, anal lobe or proctiger. In female mosquitoes it is wid­
which leads from the base of the trumpet to the develop­ ened and carries a more or less distinct pair of cercal
ing mesothoracic spiracle of the imago, is visible lobes. Between the bases of the paddles, caudal and
through the cuticle. The wing bases from which the ventral to the anal lobe, arises a sheath, enclosing the
pupal wing sheaths pass downwards on the sides of the developing genitalia of the adult, the genital lobe. In
86 5 Morphology of Mosquitoes

genital lobe in relation to the size of the paddles, and

the extent of the median fissure.
Another separation technique may also be used in
the laboratory. If larvae are reared in aerated water and
overfed, the female pupae are distinctly larger than
those of the males and the abdomen is almost of the
same width as the cephalothorax, while in male pupae
the abdomen is distinctly narrower than the cephalo­
thorax. Bearing in mind that the development of male
larvae into pupae is usually faster than that of females,
sexing according to the size and general appearance
of the pupae can be used with quite high accuracy.
Both separation techniques can be applied to living
individuals and are useful in a number of laboratory
experiments, e.g. for single pair rearing without the
necessity of handling the adults.
The abdominal segments bear paired dorsal and
ventral setae. Except for segments I and VIII, they
resemble those of the larvae. Together with the form of
the respiratory trumpets and the characteristics of the
paddles, the chaetotaxy of the pupal abdomen is mainly
used for description and identification of species. The
nomenclature used in this work follows that of Harbach
and Knight (1980) and is given in Fig. 5.19. Characteristic
of the pupae of the subfamily Anophelinae are setae 9
Fig. 5.19 Abdominal setation of pupa – dorsal view,
of the abdominal segments III to VII. They are located
(a) Anophelinae; (b) Culicinae at the lateral posterior corner of the segments and have
the form of stout spines (Fig. 5.19a). In pupae of the
males the lobe is relatively large, conical and clearly Culicinae, the setae do not arise quite at the corner but
divided, almost completely separated by a deep median a little anterior to it and they are usually small and sim­
fissure which extends closely to its base (Fig. 5.20a). ple, rarely branched (Fig. 5.19b). Within the Culicinae,
In females the lobe is smaller and of similar size to the the genera Coquillettidia and Mansonia again show an
cercal lobes, with a more or less blunt end, and the exception in the chaetotaxy by having scarcely devel­
median fissure is short and does not divide the lobe oped abdominal setae.
completely (Fig. 5.20b). The sex of the pupae can be The shape and structure of the terminal appendages
readily determined by the shape and the size of the or paddles may be used to separate mosquito pupae

Fig. 5.20 Abdomen of pupa, (a) male; (b) female

5.3 Pupae 87

a b c d

Fig. 5.21 Abdomen of pupa, (a) Chaoboridae; (b) Chironomidae; (c) Culicidae; (d) Dixidae (after Cranston et al. 1987)

from those of the closely related families of Chao­ toes, but they are stiffened by three veins or ribs. Despite
boridae, Chironomidae and Dixidae. As mentioned great variations within the family, the paddles of chiro­
above, the paddles of culicid pupae are provided with a nomid pupae lack a midrib and they are never com­
median longitudinal strengthening or midrib. Chaoborid pletely separated. In Dixidae the pupal abdomen ends
pupae have paddles quite similar to those of mosqui­ with sharply tapered caudal lobes (Fig. 5.21).
 Part II
Identification Keys; Morphology;
Ecology and Distribution of European Species
Chapter 6
Key to Female Mosquitoes

Genera

1 Palps as long as proboscis. Scutellum evenly rounded and uniformly setose (Fig. 6.1a). ..Anopheles (p 164)
Palps distinctly shorter than proboscis. Scutellum trilobed, setae arranged in three sets (Fig. 6.1b).
Abdominal terga and sterna densely covered with scales. . ........................................................................ 2
2 (1) Anal vein (A) sharply bent apically, ending slightly before or at the same level as furcation of cubitus (Cu)
(Fig. 6.2a).................................................................................................Uranotaenia unguiculata (p 312)
Anal vein (A) evenly curved, ending distinctly beyond fork of cubitus (Cu) (Fig. 6.2b). . ........................ 3

a
a

b b

Fig. 6.1 Scutellum of: (a) Anopheles sp.; (b) Aedes sp. Fig. 6.2 Wing of: (a) Ur. unguiculata; (b) Ae. vexans

3 (2) Prespiracular setae present (Fig. 6.3a).................................................................................Culiseta (p 288)

Prespiracular setae absent (Fig. 6.3b). ........................................................................................................ 4

a b

Fig. 6.3 Lateral view of thorax of: (a) Cs. annulata; (b) Oc. geniculatus

N. Becker et al., Mosquitoes and Their Control, 91

DOI 10.1007/978-3-540-92874-4_6, © Springer-Verlag Berlin Heidelberg 2010
92 6 Key to Female Mosquitoes

4 (3) Tarsomere I of fore legs longer than tarsomeres II to V together. Tarsomere IV of fore legs reduced, not
longer than broad (Fig. 6.4a). ............................................................ Orthopodomyia pulcripalpis (p 310)
Tarsomere I of fore legs usually shorter than tarsomeres II to V together. Tarsomere IV of fore legs not
reduced, distinctly longer than broad (Fig. 6.4b). . ..................................................................................... 5

Fig. 6.5 Dorsal view of abdomen of:

Fig. 6.4 Fore tarsus of: (a) Or. pulcripalpis; (b) Aedes sp. (a) Aedes sp.; (b) Culex sp.

5 (4) Postspiracular setae present. Claws usually with subbasal tooth. Abdomen tapering apically, cerci long,
easy visible (Fig. 6.5a). ......................................................................Aedes and Ochlerotatus (p 187, 204)
Postspiracular setae absent. Claws simple, without subbasal tooth. Abdomen rounded apically, cerci short,
hardly visible (Fig. 6.5b). ...............................................................................................................................6
6 (5) Pulvilli present. Wing scales narrow (Fig. 6.6a). . ..................................................................Culex (p 264)
Pulvilli absent. Wing scales usually broad and conspicuous (Fig. 6.6b). ................. Coquillettidia (p 306)

a b

Fig. 6.6 Wing scales of: (a) Culex sp.; (b) Coquillettidia sp.

6.1 Genus Anopheles

1 Wing veins entirely dark scaled (Fig. 6.7a). ............................................................................................... 2

Wing veins covered with dark and pale scales, forming contrasting spots at least on costa (C), radius (R)
and R1 (Fig. 6.7b). . ..................................................................................................................................... 7
2 (1) Dark scales on wing veins more dense in some areas forming spots, mainly on cross veins and furca­
tions. Furcation of R2+3 and M situated at the same distance from base of wing (Fig. 6.8a). ................ 3
Dark scales evenly distributed, not aggregated into spots. Furcation of R2+3 usually situated slightly closer
to base of wing than furcation of M (Fig. 6.8b). . ....................................................................................... 4
6.1 Genus Anopheles 93

Fig. 6.7 Wing of: (a) An. marteri; (b) An. hispaniola Fig. 6.8 Wing of: (a) An. maculipennis s.l.; (b) An. marteri

3 (2) Scutum more or less pale brown, without a pale longitudinal stripe, dark spots on wing usually inconspicuous,
scales of wing fringe unicolourous dark, without a pale patch at the apex (Fig. 6.9a). ................................
....................................................................................................................................An. sacharovi (p 175)
Scutum dark brown with a broad pale longitudinal stripe, dark spots on wing conspicuous, scales of wing
fringe with a pale patch at the apex (Fig. 6.9b). . .............................................................................................
................................................................ all other members of Anopheles Maculipennis Complex (p 170)
4 (2) All erect scales on vertex dark brown. Scutum unicolourous brown, without a median stripe of pale scales
(Fig. 6.10a). . ............................................................................................................An. algeriensis (p 165)
Erect scales on median part of vertex white or cream coloured, lateral parts dark. Scutum with median
stripe of pale scales (Fig. 6.10b). ................................................................................................................ 5

Fig. 6.9 Wing of: (a) An. sacharovi; (b) An. maculipennis s.l. Fig. 6.10 Scutum of: (a) An. algeriensis; (b) An. plumbeus

5 (4) Apex of proboscis pale scaled (Fig. 6.11a). . ................................................................ An. marteri (p 177)
Apex of proboscis dark scaled (Fig. 6.11b). ............................................................................................... 6

Fig. 6.12 Scutum of: (a) An. plumbeus; (b) An. claviger s.l.
Fig. 6.11 Head of: (a) An. marteri; (b) An. plumbeus
94 6 Key to Female Mosquitoes

6 (5) Body blackish grey with a leaden tinge. Anteacrostichal patch well developed, distinct, snow white
(Fig. 6.12a). . ..............................................................................................................An. plumbeus (p 178)
Body yellowish brown or brown. Anteacrostichal patch weakly developed, yellowish (Fig. 6.12b). . ........
........................................................................................An. claviger s.s. and An. petragnani (p 166, 168)
7 (1) Costal margin of wing with 2 pale spots situated in the apical half. Base of fore femur distinctly swollen
(Fig. 6.13a, b). . ........................................................................................................................................... 8
Costal margin of wing with more than 3 pale spots along its entire length. Base of fore femur not swollen
(Fig. 6.13c, d). . ........................................................................................................................................... 9

Fig. 6.13 Wing and fore leg of: (a, b) An. hyrcanus; (c, d) An. superpictus

8 (7) Tarsomere IV of hind leg mostly dark, pale only at apex (Fig. 6.14a). . ................. An. hyrcanus (p 169)
Tarsomere IV of hind leg entirely pale scaled (Fig. 6.14b). ...... An. hyrcanus var. pseudopictus (p 170)
9 (7) Palps pale at apex (Fig. 6.15a). . ............................................................................................................. 10
Palps dark at apex, rarely with a small white spot (Fig. 6.15b). ............................................................ 11
10 (9) Dark scales predominate on wing veins RS to Cu. Vein R4+5 almost entirely dark scaled. Pale spot at
the apex of wing fringe small (Fig. 6.16a). .............................................................. An. sergentii (p 183)
Pale scales predominate on wing veins RS to Cu. Vein R4+5 almost entirely pale scaled. Pale spot at the
apex of wing fringe large (Fig. 6.16b). . ...............................................................An. superpictus (p 185)

Fig. 6.14 Hind tarsus of:

(a) An. hyrcanus; (b) An. hyrcanus var. pseudopictus Fig. 6.15 Head of: (a) An. sergentii; (b) An. multicolor
6.2 Genera Aedes and Ochlerotatus 95

Fig. 6.16 Wing of: (a) An. sergentii; (b) An. superpictus Fig. 6.17 Wing of: (a) An. multicolor; (b) An. cinereus hispaniola

11 (9) Pleurites with a few pale scales. Submedian and lateral areas of scutum with scattered pale scales. Base
of costa pale scaled (Fig. 6.17a). ........................................................................... An. multicolor (p 182)
Pleurites without scales. Submedian and lateral areas of scutum without scales, sometimes a few hair-
like pale scales present, but confined to the extreme anterior margin of scutum. Base of costa dark scaled
(Fig. 6.17b). ............................................................................................ An. cinereus hispaniola (p 181)

6.2 Genera Aedes and Ochlerotatus

1 Tarsomeres with pale rings, usually more distinct on hind legs, rings sometimes very narrow (pale rings
better visible against a dark background and with a blue light filter) (Fig. 6.18a). . ................................ 2
Tarsomeres without pale rings (Fig. 6.18b). . ......................................................................................... 20

Fig. 6.18 Hind tarsus of: (a) Oc. cantans; (b) Ae. rossicus Fig. 6.19 Hind tarsus of: (a) Oc. caspius; (b) Ae. vexans

2 (1) Each pale ring embraces two tarsomeres, the apex of one and the base of the following tarsomere
(Fig. 6.19a)................................................................................................................................................ 3
Pale rings present only at base of tarsomeres (Fig. 6.19b). ...................................................................... 6
3 (2) Wing veins uniformly dark scaled (in Oc. berlandi isolated pale scales sometimes present on wing veins
and legs). Tarsomere V of all legs entirely pale scaled (Fig. 6.20a). .........................................................
...........................................................................................Oc. berlandi and Oc. pulcritarsis (p 212, 248)
Wing veins with pale and dark scales. Only tarsomere V of hind legs entirely pale scaled (Fig. 6.20b). ...........4
96 6 Key to Female Mosquitoes

Fig. 6.20 Fore, mid and hind tarsi of: Fig. 6.21 Dorsal view of abdomen of:
(a) Oc. berlandi; (b) Oc. dorsalis (a) Oc. caspius; (b–d) Oc. mariae s.l.

4 (3) Terga with a median longitudinal pale band (in Oc. caspius rarely restricted to tergum II). The last terga
sometimes almost completely covered with pale scales (Fig. 6.21a). ........................................................ 5
Terga without a median longitudinal pale band. Pale scales form narrow basal transverse bands of varying
pattern (Fig. 6.21b–d). ..................................................................Oc. mariae and Oc. zamitii (p 240, 242)
5 (4) Scutum fawn coloured, with two narrow dorsocentral white stripes, reaching to the posterior margin of
scutum. Wing veins with dark and pale scales more or less evenly mixed (Fig. 6.22a,b). . .........................
........................................................................................................................................Oc. caspius (p 216)
Scutum with a dark brown median stripe, reaching to the prescutellar dorsocentral area. Median stripe
posteriorly ornamented with a pair of narrow white lines. Posterior submedian area usually dark
brown scaled. Lateral parts of scutum greyish-white. Base of C, Sc, and R predominantly pale scaled
(Fig. 6.22c, d). . .............................................................................................................Oc. dorsalis (p 226)

Fig. 6.22 Scutum and wing of: (a, b) Oc. caspius; (c, d) Oc. dorsalis
6.2 Genera Aedes and Ochlerotatus 97

6 (2) Proboscis as long as fore femur or slightly shorter. Scutellum with broad, white scales (Fig. 6.23a). ...... 7
Proboscis distinctly longer than fore femur. Scutellum with narrow, yellowish or pale and curved scales
(Fig. 6.23b)................................................................................................................................................. 10

Fig. 6.23 Scutellum of: (a) Ae. aegypti; (b) Ae. vexans Fig. 6.24 Scutum of: (a) Ae. vittatus; (b) Ae. aegypti

7 (6) Scutum with 2 to 3 pairs of small white spots, distributed along the dorsocental area (Fig. 6.24a). Tibiae of
hind legs with white rings in the middle. ......................................................................... Ae. vittatus (p 196)
Scutum with one or more longitudinal white stripes (Fig. 6.24b). Tibiae of hind legs entirely dark scaled
. .............................................................................................................................................................................. 8
8 (7) Scutum without acrostichal stripe on anterior part, but with two narrow white dorsocentral stripes separa­
ted from anterior margin. Lateral white stripes broad, continuing over transverse suture to the end of
scutum, lyre shaped (Fig. 6.25a). . ................................................................................. Ae. aegypti (p 198)
Scutum with a white acrostichal stripe extending from the anterior margin to the beginning of the prescu­
tellar area, where it forks to end at the anterior margin of scutellum. If lateral stripes are present, they are
narrow and do not continue over transverse suture, never lyre shaped (Fig. 6.25b). ....................................9

Fig. 6.25 Scutum of: (a) Ae. aegypti; (b) Ae. albopictus Fig. 6.26 Scutum of: (a) Ae. albopictus; (b) Ae. cretinus

9 (8) Acrostichal stripe broad. Posterior dorsocentral white stripes narrow, short, not reaching to middle of scu­
tum (Fig. 6.26a). ........................................................................................................Ae. albopictus (p 201)
Acrostichal stripe narrow. Posterior dorsocentral white stripes narrow, long, reaching to middle of scutum
slightly posterior to the level of scutal angle (Fig. 6.26b)............................................. Ae. cretinus (p 203)
98 6 Key to Female Mosquitoes

10 (6) Pale rings on tarsi very narrow, usually not exceeding more than 1/4 the length of the tarsomeres. Terga
with white transverse basal bands constricted in the middle giving them a bilobed pattern (Fig. 6.27a, b).
...................................................................................................................................... Ae. vexans (p 194)
Pale rings on tarsi broad. Tarsomere III of hind legs with the pale ring embracing at least 1/3 of its length
(Fig. 6.27c).............................................................................................................................................. 11

b
a

Fig. 6.27 Tarsus (a) and abdomen (b) of Ae. vexans and tarsus (c) of Oc. flavescens

11 (10) Dorsal surface of terga with pale scales, sometimes mixed with isolated dark scales (Fig. 6.28a). . ... 12
Dorsal surface of terga with scattered dark scales (not isolated). Sometimes dark scales predominate
(Fig. 6.28b). .......................................................................................................................................... 13

Fig. 6.28 Dorsal view of abdomen of: Fig. 6.29 Lateral view of thorax of:
(a) Oc. flavescens; (b) Oc. cantans (a) Oc. flavescens; (b) Oc. cyprius

12 (11) Scutum covered with copper or golden brown scales. Scales on terga straw coloured, distinctly paler
than scutal scales. Pleural scales also paler compared to scutal scales. Lower mesepimeral setae absent
(Fig. 6.29a). . ......................................................................................................... Oc. flavescens (p 231)
Scutum covered with golden yellowish scales. Scales on terga usually ochre yellowish, not distinctly
differing in colour from the scales of the scutum. Pleurites with cream coloured scales, colouration
similar to scutum. Lower mesepimeral setae present (Fig. 6.29b). ...........................Oc. cyprius (p 221)
6.2 Genera Aedes and Ochlerotatus 99

13 (11) Palps, proboscis and wing veins uniformly dark scaled, occasionally isolated pale scales may be pre­sent
at tip of palps or at base of costa (C) (Fig. 6.30a). . ............................................ Oc. mercurator (p 242)
Palps, proboscis and wing veins, or at least one of them, with scattered or grouped pale scales
(Fig. 6.30b). .......................................................................................................................................... 14

Fig. 6.30 Head of: (a) Oc. mercurator; (b) Oc. excrucians
Fig. 6.31 Dorsal view of abdomen of:
(a) Oc. behningi; (b) Oc. excrucians

14 (13) Terga almost completely covered with dark scales dorsally, without pale transverse bands. Pale scales
usually forming diffuse patches in the midline of the terga (Fig. 6.31a). Scutum usually uniformly
coloured with small, bronze or rust coloured scales. .............................................. Oc. behningi (p 211)
Terga with scattered pale scales not forming patches or with more or less distinct pale transverse bands
dorsally (Fig. 6.31b). Scutum with a dark median stripe or with diffuse pale patches.......................... 15
15 (14) Claw strongly and abruptly bent beyond the base of subbasal tooth. Subbasal tooth nearly parallel
enclosing an angle of less than 25°. Claw more or less sinuous beyond bend (Fig. 6.32a).
..............................................................................................................................Oc. excrucians (p 229)
Claw evenly curved. Subbasal tooth clearly diverging, enclosing an angle of at least 30°. Apex of claw
not sinuous (Fig. 6.32b). ....................................................................................................................... 16

Fig. 6.32 Claws of: (a) Oc. excrucians; (b) Oc. riparius

16 (15) Scutum with a more or less well defined median stripe formed by brown scales (Fig. 6.33a). ........... 17
Scutum without a well defined median dark brown stripe (Fig. 6.33b). . ............................................. 18
100 6 Key to Female Mosquitoes

Fig. 6.33 Scutum of: (a) Oc. riparius; (b) Oc. euedes Fig. 6.34 Dorsal view of abdomen of:
(a) Oc. riparius; (b) Oc. annulipes

17 (16) Median stripe of scutum dark brown or bronze. Integument reddish brown. Terga with distinct white or
pale basal transverse bands, sometimes interrupted in the middle on terga II–V forming indistinct pale
triangular patches laterally. Apical bands of pale scales present at least on segments VI–VIII (Fig. 6.34a).
Lower postpronotal patch with sickle-shaped pale scales. .......................................Oc. riparius (p 253)
Median stripe of scutum chocolate brown, golden brown or fawn coloured (sometimes not so distinct).
Integument brownish, mesepimeral sclerite honey coloured. Terga with distinct yellowish basal trans-
verse bands, scattered light scales might be present at the apex (Fig. 6.34b). Lower postpronotal patch
with broad white scales. . .......................................................................................Oc. annulipes (p 209)
Note: To separate annulipes from cantans, the hind supraalar setae may be considered. They are straw coloured in the
former and dark coloured in the latter. General body colouration should also be considered, see species description.

18 (16) Scutum covered with dark brown or bronze brown scales. Usually a pair of white submedian
patches present just beyond scutal angle (Fig. 6.35a). White basal transverse bands on terga
of variable width, sometimes indistinct. More or less numerous white scales scattered among
the dark distal part of the terga. ................................................................................Oc. cantans (p 214)
Scutum covered with reddish brown, golden or bronze scales. Submedian pale patches absent
(Fig. 6.35b). At least anterior terga with narrow basal transverse bands. Numerous scattered white
scales apically, sometimes forming narrow transverse apical bands..................................................... 19

Fig. 6.35 Scutum of: (a) Oc. cantans; (b) Oc. euedes
6.2 Genera Aedes and Ochlerotatus 101

19 (18) Dorsocentral stripes of pale scales start at some distance from anterior margin of scutum, extending to
level of transverse suture, white lateral stripes continuing over transverse suture and reaching the end of
dorsocentral stripes......................................................................................................Oc. euedes (p 228)
Dorsocentral stripes of pale scales usually start at about the level of transverse suture reaching close to
the posterior margin of scutum. White lateral stripes sometimes indistinct, transverse suture with well
visible stripes of white scales. ................................................................................. Oc. surcoufi (p 231)
20 (1) Proboscis not longer than fore femur (Fig. 6.36a). ............................................................................... 21
Proboscis distinctly longer than fore femur (Fig. 6.36b). ..................................................................... 22

Fig. 6.36 Head and thorax of: (a) Ae. cinereus; (b) Ae. vexans

21 (20) Scales of scutum fawn brown, scales of terga dark brown, colouration distinctly different. Scales of
pleurites yellowish white, scales of sterna yellowish. ..........Ae. cinereus and Ae. geminus (p 189, 191)
Scales of scutum and terga unicolourous, dark brown. Scales of pleurites and sterna greyish white.
..................................................................................................................................Ae. rossicus (p 192)
22 (20) Cerci short, blunt (Fig. 6.37a). Pale patches on terga silvery, with metallic sheen............................... 23
Cerci long, tapering (Fig. 6.37b). Pale scales on terga, if present, without silvery sheen..................... 24

Fig. 6.37 Abdominal end of: Fig. 6.38 Dorsal view of abdomen of:
(a) Oc. geniculatus; (b) Oc. rusticus (a) Oc. detritus; (b) Oc. cataphylla
102 6 Key to Female Mosquitoes

23 (22) Scutellum with narrow yellowish scales. ............................................................Oc. geniculatus (p 206)

Scutellum with broad whitish scales. . ...................................................................... Oc. echinus (p 205)
24 (22) Pale scales present or predominating in apical half of terga (Fig. 6.38a). ............................................ 25
Apical half of terga with dark scales, pale scales forming basal bands or lateral spots (Fig. 6.38b).
.............................................................................................................................................................. 30
25 (24) Upper scales of postpronotum broad, straight and black (Fig. 6.39a). Scutum with a dark median stripe,
which can be divided into two stripes by a narrow acrostichal stripe of paler scales. . ........................ 26
Upper scales of postpronotum often narrow, curved (Fig. 6.39b). If broad and straight, the colour is
yellowish or light brown, not black. Scutum usually without dark median stripe, if present, the colour
of the stripe is bronze or yellowish. ...................................................................................................... 28
26 (25) Basal transverse bands on terga distinct, usually widened middorsally. Often at least the apical 2-3 terga
with a continuous median longitudinal band (Fig. 6.40a). ................................................................... 27
Basal transverse bands on terga present, sometimes not well defined and not widened in the middle. Pale
scales scattered on apical part of terga (sometimes predominating) and occasionally forming narrow
apical bands (Fig. 6.40b). ............................................................................................. Oc. refiki (p 259)

a b

Fig. 6.39 Lateral view of thorax of: Fig. 6.40 Dorsal view of abdomen of:
(a) Oc. refiki; (b) Oc. detritus (a) Oc. rusticus; (b) Oc. refiki

27 (26) Subcosta with scattered pale scales, most numerous at its apex. . ............................Oc. rusticus (p 261)
Subcosta without pale scales. ..........................................................................Oc. quasirusticus (p 258)
28 (25) Terga with transverse bands of pale scales. Scattered pale scales usually present in apical part of terga
(Fig. 6.38a). . ............................................................................................................. Oc. detritus (p 223)
Pale transverse bands absent. Terga completely covered with pale scales or with scattered dark scales
sometimes forming diffuse spots. ......................................................................................................... 29
29 (28) Postnotum with a group of scales........................................................................Oc. lepidonotus (p 257)
Postnotum without a group of scales...................................................................Oc. subdiversus (p 263)
30 (24) Scutum with dense, long and black setae. Postpronotal setae scattered on entire postpronotum
(Fig. 6.41a). . ......................................................................................................................................... 31
Setae of scutum not that long and fewer, often brown or golden. Postpronotal setae only
present along posterior margin, sometimes with a few setae confined to dorsal margin of pospronotum
(Fig. 6.41b). .......................................................................................................................................... 32
6.2 Genera Aedes and Ochlerotatus 103

Fig. 6.41 Lateral view of thorax of: (a) Oc. impiger; (b) Oc. cataphylla

31 (30) Tarsal claws sharply bent in the middle. Apical part of claw nearly parallel to long subbasal tooth (most
distinct on fore legs). Postspiracular area with 10 or less setae (Fig. 6.42a, b). ....... Oc. impiger (p 236)
Tarsal claw evenly curved. Apical part of claw not parallel to short subbasal tooth (enclosing an angle
of more than 45°). Postspiracular area with 14 or more setae (Fig. 6.42c, d).......... Oc. nigripes (p 245)

Fig. 6.42 Claw and lateral view of thorax of: (a, b) Oc. impiger; (c, d) Oc. nigripes

32 (30) Wing veins with pale and dark scales intermixed, especially on C and R1. . ........................................ 33
Wing veins without pale scales, if present, pale scales restricted to basal part of veins. ..................... 34
33 (32) Proboscis uniformly dark scaled. . ........................................................................Oc. cataphylla (p 218)
Proboscis speckled with more or less numerous pale scales, especially in the middle..................................
.................................................................................................................................... Oc. leucomelas (p 238)
34 (32) Hypostigmal patch of scales present, postprocoxal patch of scales absent (Fig. 6.43a). ..................... 35
Hypostigmal patch of scales absent, postprocoxal patch of scales present or absent (Fig. 6.43b). . .... 36

Fig. 6.43 Lateral view of thorax of: (a) Oc. pullatus; (b) Oc. punctor
104 6 Key to Female Mosquitoes

35 (34) Mesepimeral patch of white scales reaching lower margin of mesepimeron. Lower mesepimeral setae
present (Fig. 6.44a)................................................................................................... Oc. pullatus (p 249)
Mesepimeral patch of white scales not reaching lower margin of mesepimeron. Lower mesepimeral
setae usually absent (Fig. 6.44b). . ......................................................................... Oc. intrudens (p 237)

Fig. 6.44 Lateral view of thorax of: (a) Oc. pullatus; (b) Oc. intrudens

36 (34) Upper mesepisternal patch of scales not reaching anterior angle of mesepisternum, or the lower edge
ending above the level of anterior angle (Fig. 6.45a). .......................................................................... 37
Upper mesepisternal patch of scales reaching anterior angle of mesepisternum or at least a few scales
situated close to it or below the level of anterior angle (Fig. 6.45b). ................................................... 38

Fig. 6.45 Lateral view of thorax of: (a) Oc. diantaeus; (b) Oc. communis

37 (36) Upper mesepisternal patch of scales large, not divided into two portions (Fig. 6.45a). Abdominal terga
with triangular patches of pale scales, patches usually connected by a basal transverse band on the last
segments..................................................................................................................Oc. diantaeus (p 224)
Upper mesepisternal patch of scales small, divided into two or more portions (Fig. 6.44b). All abdo­
minal terga with pale transverse basal bands.......................................................... Oc. intrudens (p 237)
38 (36) Mesepimeral patch of scales reaches lower margin of mesepimeron (Fig. 6.46a)................................ 39
Mesepimeral patch of scales ends distinctly above lower margin of mesepimeron (Fig. 6.46b).......... 42
6.2 Genera Aedes and Ochlerotatus 105

Fig. 6.46 Lateral view of thorax of: (a) Oc. communis; (b) Oc. sticticus

39 (38) Postprocoxal scales present (Fig. 6.47a). . ............................................................................................ 40

Postprocoxal scales absent (Fig. 6.47b). . .............................................................Oc. communis (p 220)

Fig. 6.47 Lateral view of thorax of: (a) Oc. punctor; (b) Oc. communis

40 (39) Pale bands of terga II–V distinctly confined in the middle (Fig. 6.48a). ..................................................
............................................................................................Oc. punctor and Oc. punctodes (p 251, 250)
Pale bands of terga II–V of uniform width or only slightly confined in the middle (Fig. 6.48b). ........ 41

Fig. 6.48 Dorsal view of abdomen of: Fig. 6.49 Scutum of: (a) Oc. pionips; (b) Oc. hexodontus
(a) Oc. punctor; (b) Oc. hexodontus
106 6 Key to Female Mosquitoes

41 (40) Scutum with dark brown median stripe, occasionally divided into two dorsocentral stripes by an acro­
stichal row of yellowish scales (Fig. 6.49a). Base of costa covered with dark scales, rarely a few pale
scales present. . ...........................................................................................................Oc. pionips (p 246)
Scutum more or less uniformly covered with yellowish brown scales (Fig. 6.49b). Base of costa with
numerous pale scales often forming large patch..................................................Oc. hexodontus (p 233)
42 (38) Hind tibia generally covered with light scales on anterior surface........................................................ 43
Hind tibia with dark scales on anterior surface. ..................................................Oc. hungaricus (p 234)
43 (42) Wing veins usually entirely dark scaled. Terga II–IV with pale basal bands distinctly constricted in
the middle, on following terga basal bands interrupted in the middle forming triangular pale patches
at lateral sides (Fig. 6.50a). First flagellomere yellowish at the base, second and third not distinctly
shortened. ............................................................................................................ Oc. sticticus (p 255)
Wing veins with scattered pale scales at base of C, entire Sc and M proximal to the cross veins. Terga
with broad pale basal bands, slightly, if at all, constricted in the middle (Fig. 6.50b). First flagellomere
entirely black, second and third distinctly shortened.���������������������������������������������� Oc. nigrinus (p 243)

Fig. 6.50 Dorsal view of abdomen of:

(a) Oc. sticticus; (b) Oc. nigrinus

6.3 Genus Culex

1 Tarsomere I of hind legs distinctly shorter than hind tibia (Fig. 6.51a).................................................... 2
Tarsomere I of hind legs as long as or slightly longer than hind tibia (Fig. 6.51b). ................................. 3

Fig. 6.51 Hind leg of: (a) Cx. modestus; (b) Cx. p. pipiens Fig. 6.52 Wing of: (a) Cx. mimeticus; (b) Cx. p. pipiens
6.3 Genus Culex 107

2 (1) Terga with continuous lateral longitudinal bands of pale scales. Pale scales sometimes form more
or less developed, triangular patches, which are usually connected. ...................... Cx. modestus (p 265)
Terga without continuous lateral longitudinal bands. More or less developed patches of pale scales at the
lateral basal margins of terga present. ........................................................................Cx. pusillus (p 267)
3 (1) Tarsi with pale rings, which are sometimes narrow. Wings with large, prominent spots of pale scales,
especially on C (Fig. 6.52a). . .................................................................................Cx. mimeticus (p 271)
Tarsi without pale rings. Wing veins mainly covered with dark scales (in theileri a few pale scales may
be present on C) (Fig. 6.52b). . ................................................................................................................. 4
4 (3) Terga uniformly covered with reddish brown scales, without pale transverse bands. .Cx. martinii (p 285)
Terga with more or less developed transverse bands formed by white or yellowish scales. .................... 5
5 (4) Terga with pale basal bands, sometimes reduced to lateral triangular patches......................................... 6
Terga with pale apical bands, sometimes reduced to lateral spots or completely absent. ...................... 10
6 (5) Femora and tibiae of fore and mid legs with a distinct anterior pale longitudinal stripe, rarely only the
fore femur with a pale stripe (Fig. 6.53a). Pale basal bands on abdominal terga usually triangularly
extended posteriorly. . .................................................................................................. Cx. theileri (p 280)
Femora and tibiae of fore and mid legs without anterior pale longitudinal stripe (Fig. 6.53b). ............... 7

Fig. 6.53 Fore femur and tibia of: Fig. 6.54 Dorsal view of abdomen of:
(a) Cx. theileri; (b) Cx. p. pipiens (a) Cx. laticinctus; (b) Cx. p. pipiens

7 (6) Proboscis with an indistinct pale median ring...........................................................Cx. brumpti (p 269)

Proboscis dark scaled. ............................................................................................................................. 8
8 (7) Basal bands on abdominal terga broad and white, covering 1/2 to 2/3 of each tergum (Fig. 6.54a). Tibia
of hind leg with a prominent apical pale spot. ....................................................... Cx. laticintus (p 270)
Basal bands on abdominal terga narrow, usually covering less than 1/2 of each tergum (Fig. 6.54b).
Tibia of hind leg without apical pale spot. .............................................................................................. 9
9 (8) Basal bands on terga formed by white scales. Hind tibia with more or less distinct longitudinal anterior
pale stripe (Fig. 6.55a). . .......................................................................................Cx. perexiguus (p 273)
Basal bands on terga formed by yellowish scales. The bands are sometimes reduced or pale scales form
patches at the sides of the terga. Hind tibia without longitudinal pale stripe (Fig. 6.55b). . .....................
.......................................Cx. p. pipiens, Cx. p. quinquefasciatus and Cx. torrentium (p 275, 278, 279)
10 (5) Apical bands narrowed or interrupted in the middle on some terga......................Cx. impudicus (p 284)
Apical bands well developed, not interrupted in the middle. ............................................................... 11
108 6 Key to Female Mosquitoes

11 (10) Palps with dark and pale scales. End of Sc nearly aligned with furcations of R2+3 and M (Fig. 6.56a).
Pale apical bands on terga relatively broad, distinctly widened in the middle of some segments. Apex of
hind tibia with a pale spot........................................................................................Cx. hortensis (p 282)
Palps with dark scales. End of Sc distinctly displaced towards the wing base compared to furcations of
R2+3 and M (Fig. 6.56b). Pale apical bands on terga relatively narrow, without widening in the middle.
Apex of hind tibia without a pale spot. Abdomen usually greenish ventrally. ........Cx. territans (p 286)

Fig. 6.55 Hind tibia of: Fig. 6.56 Wing of: (a) Cx. hortensis; (b) Cx. territans
(a) Cx. perexiguus; (b) Cx. p. pipiens and Cx. torrentium

6.4 Genus Culiseta

1 Scutum with distinct longitudinal pale stripes (resemble a lyre in shape). Femora and tibiae with well
defined pale spots and stripes. Costa mainly covered with pale scales. .......... Cs. longiareolata (p 289)
Scutum without distinct longitudinal stripes. Femora and tibiae without pale stripes, uniformly dark
scaled or with scattered light scales. Costa completely or mainly dark scaled. ..................................... 2
2 (1) Cross veins r-m and m-cu well separated. The distance between them usually at least the length of m-cu
(Fig. 6.57a). Wings usually without dark spots, otherwise with an indistinct dark spot at the base
of R4+5....................................................................................................................................................... 3
Cross veins r-m and m-cu aligned or slightly separated. If separated, the distance between them is usu-
ally not longer than m-cu (Fig. 6.57b). Wings weakly or distinctly spotted (spots sometimes absent in
Cs. glaphyroptera)................................................................................................................................... 6

Fig. 6.57 Wing of: (a) Culicella; (b) Culiseta

6.4 Genus Culiseta 109

3 (2) Proboscis with scattered pale scales, mainly in its middle part. Sterna usually with dark scales arranged
in a pattern of an inverted “V” (Fig. 6.58a, b)......................................................................................... 4
Proboscis uniformly dark scaled, rarely with a few pale scales in the middle (in Cs. morsitans), or pale
scales predominating (in Cs. ochroptera). Sterna without a pattern of an inverted “V”, pale and dark
scales diffused (Fig. 6.58c, d). ................................................................................................................ 5

Fig. 6.58 Proboscis and sternum of: (a, b) Cs. fumipennis; (c, d) Cs. morsitans

4 (3) On fore legs pale rings include apical and basal parts between tarsomeres III–IV and IV–V (Fig. 6.59a).......
........................................................................................................................................ Cs. fumipennis (p 291)
On fore legs apical parts of tarsomeres III and IV entirely dark scaled (Fig. 6.59b). .....Cs. litorea (p 292)

a
a

b
b

Fig. 6.59 Fore tarsus of: (a) Cs. fumipennis; (b) Cs. litorea Fig. 6.60 Hind tarsus of: (a) Cs. glaphyroptera; (b) Cs. annulata

5 (3) Terga with narrow basal pale bands. Scales on wing veins evenly distributed, not forming spots. Tibia of
fore leg mainly dark brown scaled. . .......................................................................... Cs. morsitans (p 294)
Terga with narrow indistinct basal and apical pale bands, sometimes absent. Tergum VIII completely covered
with pale scales. Indistinct dark spot at the base of R4+5 may be present. Tibia of fore leg mainly yellowish
scaled. ............................................................................................................................. Cs. ochroptera (p 296)
6 (2) Tarsi dark (Fig. 6.60a). . .............................................................................................................................. 7
Tarsi with white rings (Fig. 6.60b). ............................................................................................................ 8
7 (6) Palps dark with scattered pale scales, eyes distinctly bordered with light scales. Spots on wing veins
always present, sometimes indistinct. Usually not more than 15 prespiracular setae and not more than 10
lower mesepisternal setae present (Fig. 6.61a). ..........................................................Cs. bergrothi (p 301)
110 6 Key to Female Mosquitoes

Palps entirely dark scaled, eyes not bordered with light scales. Spots on wing veins absent or indistinct.
Number of prespiracular setae 16-22 and of lower mesepisternal setae 12-18 (Fig. 6.61b)................................
. ..................................................................................................................................... Cs. glaphyroptera (p 303)

a b

Fig. 6.61 Lateral view of thorax of: (a) Cs. bergrothi; (b) Cs. glaphyroptera

8 (6) Femora with subapical pale rings. Tarsomere I of hind legs with a median white ring (Fig. 6.62a). . ........... 9
Femora without subapical pale rings. Tarsomere I of hind legs without a median white ring (Fig. 6.62b). . ........
.............................................................................................................................................. Cs. alaskaensis (p 298)

Fig. 6.62 Hind tarsus of: (a) Cs. annulata; (b) Cs. alaskaensis Fig. 6.63 Wing of: (a) Cs. annulata; (b) Cs. subochrea

9 (8) Costa (C) usually completely dark scaled or isolated pale scales could be present on C, Sc and R. Cu entirely
dark scaled. Dark spots on wings distinct. Terga with distinct white basal bands, pale scales absent in apical
half of terga. Cross veins r-m and m-cu aligned (Fig. 6.63a)........................................... Cs. annulata (p 299)
Costa, Sc and R with scattered pale scales. Cu with more or less numerous pale scales. Dark spots on
wings indistinct. Terga with indistinct pale basal bands formed by yellowish scales (not white), pale scales
are also present among the dark scales in the apical half of the terga. Cross veins r-m and m-cu slightly
separated (Fig. 6.63b). .............................................................................................. Cs. subochrea (p 305)
6.5 Genus Coquillettidia 111

6.5 Genus Coquillettidia

1 Tarsomeres with pale rings. Proboscis and palps with numerous pale scales. Wing veins with broad dark
and pale scales intermixed. ........................................................................................ Cq. richiardii (p 308)
Tarsomeres without pale rings. Proboscis and palps uniformly blackish brown. Wing veins uniformly dark
scaled. ........................................................................................................................... Cq. buxtoni (p 307)
Chapter 7
Key to Male Mosquitoes

Genera

1 Gonocoxite without lobes. Gonostylus about as long as gonocoxite. Sclerotized paraproct absent. Proctiger,
if present, membranous, cone-shaped and hardly visible (Fig. 7.1a).............................. Anopheles (p 164)
Gonocoxite with 1 or 2 lobes. Lobes sometimes rudimentary or absent (subgenus Finlaya). Gonostylus
shorter than gonocoxite. Proctiger different, sclerotized paraproct present (Fig. 7.1b). ............................. 2

Fig. 7.1 Hypopygium of: (a) An maculipennis s.l.; (b) Oc. mercurator

2 (1) Gonocoxite with only one subapically located lobe covered with spines and setae. Apex of paraproct with
abundant spines or rows of numerous denticles (paraproct crown) (Fig. 7.2a).......................Culex (p 264)
Gonocoxite with 2 lobes (basal and apical), if only one lobe is present, it is situated at the base of the
gonocoxite, lobes absent in subgenus Finlaya. Apex of paraproct without spines or rows of numerous
denticles (Fig. 7.2b)..................................................................................................................................... 3
3 (2) Apical spine of gonostylus longer than the maximum width of gonostylus (Fig. 7.3a). If the spine is shorter
than the maximum width of the gonostylus, it is articulated subapically (Fig. 7.3b). If the spine is absent,
the gonostylus is divided at its base (Fig. 7.3c)................................. Aedes and Ochlerotatus (p 187, 204)
Apical spine of gonostylus shorter than or equal to the maximum width of the gonostylus (Fig. 7.3d)......... 4

N. Becker et al., Mosquitoes and Their Control, 113

DOI 10.1007/978-3-540-92874-4_7, © Springer-Verlag Berlin Heidelberg 2010
114 7 Key to Male Mosquitoes

Fig. 7.2 Hypopygium of: (a) Cx. modestus; (b) Oc. annulipes

Fig. 7.3 Gonostylus of: (a) Oc. riparius; (b) Ae. vittatus; (c) Ae. rossicus; (d) Cs. morsitans

4 (3) Basal lobe of gonocoxite with one strongly sclerotized rod like spine (Fig. 7.4a)..... Coquillettidia (p 306)
Basal lobe of gonocoxite with at least 2 spines or strong setae (Fig. 7.4b)................................................. 5

Fig. 7.4 Basal lobe of gonocoxite of: (a) Cq. richiardii; (b) Cs. fumipennis

5 (4) Gonocoxite broad and short, plumpy in appearance with a small, flattened basal lobe. Gonostylus broad, flat-
tened dorsoventrally. Proctiger lobe shaped, membranous (Fig. 7.5a)........Uranotaenia unguiculata (p 312)
Gonocoxite more elongated, with a distinct basal lobe. Gonostylus narrow, not flattened dorsoventrally
(Fig. 7.5b)..................................................................................................................................................... 6
7.1 Genus Anopheles 115

Fig. 7.5 Hypopygium of: (a) Ur. unguiculata; (b) Or. pulcripalpis

6 (5) Apical spine of gonostylus fingered at the apex. Spine as long as the maximum width of the gonostylus
(Fig. 7.6a)............................................................................................ Orthopodomyia pulcripalpis (p 310)
Apical spine of gonostylus not fingered (there may be 2 spines at the apex of the gonostylus in Cs. longia-
reolata, Fig. 7.6b). Spine distinctly shorter than the maximum width of the gonostylus (except in Cs.
glaphyroptera, Fig. 7.6c). ...................................................................................................Culiseta (p 288)

a b c

Fig. 7.6 Gonostylus of: (a) Or. pulcripalpis; (b) Cs. longiareolata; (c) Cs. glaphyroptera

7.1 Genus Anopheles

1 Base of gonocoxite with 1-3, usually 2, parabasal setae. At least one of them originated from a tubercle
(tubercles weakly developed in An. plumbeus). Internal seta present (subgenus Anopheles, Fig. 7.7a)..... 2
Base of gonocoxite with 4-7, usually 6, parabasal setae. None of them elevated on a tubercle. Internal seta
absent (subgenus Cellia, Fig. 7.7b). ........................................................................................................... 7
2 (1) Base of gonocoxite with 1 parabasal seta (Fig. 7.8a).............................................. An. algeriensis (p 165)
Base of gonocoxite with 2-3 parabasal setae (Fig. 7.8b)............................................................................. 3
116 7 Key to Male Mosquitoes

Fig. 7.7 Gonocoxite of: (a) An. marteri; (b) An. superpictus Fig. 7.8 Base of gonocoxite of:
(a) An. algeriensis; (b) An. maculipennis s.l.

3 (2) Base of gonocoxite with 3 parabasal setae, inner 1 simple, the 2 outer setae apically branched (Fig. 7.9a).
........................................................................................An. claviger s.s. and An. petragnani (p 166, 168)
Base of gonocoxite with 2 simple parabasal setae (Fig. 7.9b). ................................................................... 4

Fig. 7.9 Base of gonocoxite of: Fig. 7.10 Aedeagus and parabasal setae of:
(a) An. claviger s.l.; (b) An. hyrcanus (a) An. maculipennis s.l.; (b) An. plumbeus

4 (3) Aedeagus with leaflets. Parabasal setae of different length, outer seta longer than inner seta
(Fig. 7.10a)................................................................................................................................................... 5
Aedeagus without leaflets. Parabasal setae of approximately the same length, tubercles weakly sclerotized
(Fig. 7.10b)..................................................................................................................An. plumbeus (p 178)
5 (4) Parabasal setae arising from a strongly sclerotized base (Fig. 7.7a). Outer and inner claspette lobes bear
flattened spatula-like or longer sabre-like setae (Fig. 7.11a)......................................... An. marteri (p 177)
Parabasal setae arising from a weakly or not sclerotized base (Fig. 7.8b). At least the inner claspette lobe
bears spine like setae (Fig. 7.11b)................................................................................................................ 6
6 (5) Claspette lobes not well defined, bearing only spine like setae of variable length and shape
(Fig. 7.12a).......................................................................... Anopheles Maculipennis Complex (p 170)
Claspette lobes well defined. Setae of outer lobe fused into broad, spatula like processes, inner lobe with
2 spine-like setae (Fig. 7.12b)..................................................................................... An. hyrcanus (p 169)
7.1 Genus Anopheles 117

Fig. 7.11 Claspette of: (a) An. marteri; (b) An. hyrcanus Fig. 7.12 Claspette of:
(a) An. maculipennis s.l.; (b) An. hyrcanus

7 (1) Leaflets of aedeagus present (Fig. 7.13a)..................................................................................................... 8

Leaflets of aedeagus absent (Fig. 7.13b)................................................................... An. multicolor (p 182)
8 (7) Leaflets of aedeagus short, distinctly shorter than half the length of the aedeagus (Fig. 7.14a)...................
.................................................................................................................................An. superpictus (p 185)
Leaflets of aedeagus well developed, longest leaflet almost half as long as the aedeagus (Fig. 7.14b)...... 9
9 (8) Longest spine-like seta of claspette distinctly longer than spatula-like seta. The longest leaflet of aedeagus
is less than 1/3 longer than the second longest. Leaflets weakly serrated (Fig. 7.15a)..................................
.................................................................................................................... An. cinereus hispanola (p 181)
Longest spine-like seta of claspette of similar length as spatula-like seta. The longest leaflet of aedeagus is
distinctly longer than the second longest. Leaflets strongly serrated (Fig. 7.15b)........... An. sergentii (p 183)

Fig. 7.13 Aedeagus of: Fig. 7.14 Aedeagus of:

(a) An. superpictus; (b) An. multicolor (a) An. superpictus; (b) An. cinereus hispaniola

Fig. 7.15 Claspette and aedeagus of: (a) An. cinereus hispaniola; (b) An. sergentii
118 7 Key to Male Mosquitoes

7.2 Genera Aedes and Ochlerotatus

1 Apex of gonocoxite exceeding articulation point of gonostylus, which is divided into two branches
(Fig. 7.16a). Palps several times shorter than the proboscis, as in females................................................. 2
Gonostylus arising at the apex of gonocoxite, simple, not divided into 2 branches (Fig. 7.16b). Palps about
as long as the proboscis................................................................................................................................ 4
2 (1) Longer branch of gonostylus forked into 2 prongs at the apex (Fig. 7.17a)................................................ 3
Longer branch of gonostylus not forked at the apex, denticulated at outer apical margin
(Fig. 7.17b).....................................................................................................................Ae. rossicus (p 192)

Fig. 7.16 Apex of gonocoxite and gonostylus of: Fig. 7.17 Gonostylus of: (a) Ae. cinereus; (b) Ae. rossicus
(a) Ae. cinereus; (b) Oc. communis

3 (2) Outer prong of the fork usually longer than or equal to the inner one (Fig. 7.18a,b)... Ae. geminus (p 191)
Inner prong of the fork usually longer than the outer one (Fig. 7.18c,d)...................... Ae. cinereus (p 189)
Note: Transitional forms present, specific status of geminus uncertain.
4 (1) Typical claspettes (divided into stem and filament) present (Fig. 7.19a).................................................... 9
Typical claspettes absent (Fig. 7.19b).......................................................................................................... 5

Fig. 7.18 Gonostylus of:

(a, b) Ae. geminus; (c, d) Ae. cinereus Fig. 7.19 Claspette of: (a) Oc. nigripes; (b) Ae. vexans
7.2 Genera Aedes and Ochlerotatus 119

5 (4) Gonostylus distinctly expanded apically (Fig. 7.20a). Claspettes of different shape, elongated, well sepa-
rated from basal part of gonocoxite. ........................................................................................................... 6
Gonostylus slightly expanded apically or evenly tapering (Fig. 7.20b,c). Claspettes lobe like, seem to be
inner basal part of gonocoxite and covered with dense setae, some of them may be enlarged, spine
like................................................................................................................................................................ 7

Fig. 7.20 Gonostylus of: Fig. 7.21 Gonostylus of: (a) Ae. vexans; (b) Ae. vittatus
(a) Ae. vexans; (b) Ae. albopictus; (c) Ae. aegypti

6 (5) Gonostylus gradually expanded to apex. Spine of gonostylus articulated subapically, straight
(Fig. 7.21a).......................................................................................................................Ae. vexans (p 194)
Gonostylus abruptly expanded apically, flask shaped. Spine of gonostylus articulated subapically, strongly
curved (Fig. 7.21b).......................................................................................................... Ae. vittatus (p 196)
7 (5) Apical part of gonostylus slightly broader than median part. Spine of gonostylus articulated subapically
(Fig. 7.22a)................................................................................................................................................... 8
Apical part of gonostylus distinctly narrower than median part, tapering. Spine of gonostylus articulated
at the apex (Fig. 7.22b)................................................................................................... Ae. aegypti (p 198)

Fig. 7.22 Gonostylus of: (a) Ae. cretinus; (b) Ae. aegypti Fig. 7.23 Claspette lobes and tergum IX of:
(a) Ae. cretinus; (b) Ae. albopictus

8 (7) Setae below subapical spine of gonostylus usually scattered (Fig. 7.22a). Claspette lobes covered with
short setae. Median part of tergum IX evenly rounded (Fig. 7.23a)..............................Ae. cretinus (p 203)
Setae below subapical spine of gonostylus usually forming a row (Fig. 7.20b). Claspette lobes covered
with long setae, several of them stronger, spine like, curved at the apex. Median part of tergum IX pointed
(Fig. 7.23b)................................................................................................................. Ae. albopictus (p 201)
120 7 Key to Male Mosquitoes

9 (4) Gonocoxite without lobes. Several tubercles bearing thin setae may be present at the inner base of gono-
coxite (Fig. 7.24a).................................................................................................................................... 10
Gonocoxite with more or less distinct basal and apical lobes, or at least basal lobe present
(Fig. 7.24b).............................................................................................................................................. 11

Fig. 7.24 Gonocoxite of: (a) Oc. geniculatus; (b) Oc. nigripes Fig. 7.25 Hypopygium of: (a) Oc. echinus; (b) Oc. geniculatus

10 (9) Setae of gonocoxite very long and dense (Fig. 7.25a)................................................. Oc. echinus (p 205)
Setae of gonocoxite short and less dense (Fig. 7.25b)..........................................Oc. geniculatus (p 206)
Note: Males of the two species are difficult to separate.
11 (9) Basal lobe of gonocoxite usually divided, one lobe with several long, lanceolate, flattened setae which
may be slightly or strongly curved (Fig. 7.26a)...................................................................................... 12
Basal lobe of gonocoxite usually undivided, without a row of several lanceolate, flattened setae, but 1 or
2 could be present (Fig. 7.26b)................................................................................................................ 16

Fig. 7.26 Basal lobe of gonocoxite of: Fig. 7.27 Apex of gonostylus of: (a) Oc. rusticus; (b) Oc. refiki
(a) Oc. rusticus; (b) Oc. intrudens

12 (11) Apical spine of gonostylus distinctly S-shaped (Fig. 7.27a).....................................Oc. rusticus (p 261)
Apical spine of gonostylus straight or slightly curved (Fig. 7.27b)...................................................... 13
7.2 Genera Aedes and Ochlerotatus 121

13 (12) Division of basal lobe which bears lanceolate setae elongated, at least in basal part. Claspette filament
distinctly transversely striated (Fig. 7.28a)............................................................................................ 14
Division of basal lobe which bears lanceolate setae arising gradually from gonocoxite, more or less
conical. Claspette filament not distinctly striated (Fig. 7.29a).............................................................. 15
14 (13) Claspette stem broader at the apex than at the base. Number of slightly curved lanceolate setae on basal
lobe 15–16, arranged in several rows (Fig. 7.28a)......................................................... Oc. refiki (p 259)
Apex and base of claspette stem have more or less equal width. Number of strongly curved lanceolate
setae on basal lobe 6-8, located at the distal margin (Fig. 7.28b).....................Oc. quasirusticus (p 258)
15 (13) Base of gonocoxite with one lobe, bearing a group of lanceolate, flattened setae (Fig. 7.29a).................
.............................................................................................................................Oc. lepidonotus (p 257)
Base of gonocoxite with two or more lobes. Only one lobe bears lanceolate, flattened setae, the others
with hair like setae (Fig. 7.29b)...........................................................................Oc. subdiversus (p 263)

Fig. 7.28 Claspette and basal lobe of gonocoxite of: Fig. 7.29 Base of gonocoxite of:
(a) Oc. refiki; (b) Oc. quasirusticus (a) Oc. lepidonotus; (b) Oc. subdiversus

16 (11) Basal lobe of gonocoxite with 3 setae distinctly larger than the others (Fig. 7.30a)........................... 17
Basal lobe of gonocoxite with 0-2 setae which are larger than the others (Fig. 7.30b)......................... 19

Fig. 7.30 Basal lobe of gonocoxite of: Fig. 7.31 Basal lobe of gonocoxite and claspette of:
(a) Oc. intrudens; (b) Oc. caspius (a) Oc. diantaeus; (b) Oc. pullatus

17 (16) Basal lobe of gonocoxite with all 3 large setae spine like. Claspette stem with a thorn shaped process
beyond the middle (Fig. 7.31a).............................................................................................................. 18
Basal lobe of gonocoxite with 1 or 2 of the larger setae flattened and lanceolate. Claspette stem without
a thorn shaped process, bent and swollen in the middle (Fig. 7.31b)....................... Oc. pullatus (p 249)
122 7 Key to Male Mosquitoes

18 (17) Apical half of gonocoxite with very dense setae directed more inwardly (Fig. 7.32a). ...........................
................................................................................................................................Oc. diantaeus (p 224)
Only small subapical zone with dense setae directed more distally (Fig. 7.32b)...... Oc. intrudens (p 237)

Fig. 7.32 Hypopygium of: (a) Oc. diantaeus; (b) Oc. intrudens

19 (16) Basal lobe of gonocoxite with 2 spine like setae (Fig. 7.33a)............................................................... 20
Basal lobe of gonocoxite with 0-1 spine like setae (Fig. 7.33b)............................................................ 22

Fig. 7.33 Basal lobe of gonocoxite of: Fig. 7.34 Basal lobe of gonocoxite of:
(a) Oc. caspius; (b) Oc. impiger (a) Oc.dorsalis; (b) Oc. hungaricus

20 (19) Larger spine of basal lobe hook shaped (Fig. 7.34a)............................................................................. 21

Larger spine of basal lobe not hook shaped, slightly curved in the middle (Fig. 7.34b)
.............................................................................................................................Oc. hungaricus (p 234)
21 (20) Basal lobe gradually arising from gonocoxite, spines situated close together, larger spine strongly
curved apically (usually tip extending backwards to almost the middle of the spine) (Fig. 7.35a)
....................................................................................................................................Oc. caspius (p 216)
Basal lobe of gonocoxite slightly constricted at base, spines widely separated, larger spine
slightly curved apically (usually tip extending backwards to not more than one third of the spine)
(Fig. 7.35b).................................................................................................................Oc. dorsalis (p 226)
Note: The structure of the hypopygium of the two species is very similar and difficult to distinguish, intermediate forms
are common.
22 (19) Apical lobe of gonocoxite small, weakly developed or absent (Fig. 7.36a).......................................... 23
Apical lobe of gonocoxite well developed (Fig. 7.36b)......................................................................... 26
7.2 Genera Aedes and Ochlerotatus 123

Fig. 7.35 Basal lobe of gonocoxite of: Fig. 7.36 Apical lobe of gonocoxite of:
(a) Oc. caspius; (b) Oc. dorsalis (a) Oc. pulcritarsis; (b) Oc. cataphylla

23 (22) Basal lobe of gonocoxite indistinct, weakly developed (Fig. 7.37a)..................................................... 24

Basal lobe well developed (Fig. 7.37b).................................................................................................. 25

Fig. 7.37 Basal lobe of gonocoxite of: Fig. 7.38 Basal lobe of gonocoxite of:
(a) Oc. mariae s.l.; (b) Oc. impiger (a) Oc. mariae s.l.; (b) Oc. berlandi

24 (23) Longer setae on basal lobe thin, of equal length and thickness. Strong spine like setae absent
(Fig. 7.38a)...............................................................................Oc. mariae and Oc. zammitii (p 240, 242)
Longer setae on basal lobe distinctly differ in length and thickness, 1 strong spine like seta present
(Fig. 7.38b)........................................................................Oc. pulcritarsis and Oc. berlandi (p 248, 212)
25 (23) Gonocoxite with long setae predominating on inner side. Basal lobe with setae of more or less equal
thickness (Fig. 7.39a)................................................................................................ Oc. nigripes (p 245)
Gonocoxite with short setae predominating on inner side. Basal lobe with one seta distinctly stronger
than the others (Fig. 7.39b)........................................................................................ Oc. impiger (p 236)
26 (22) Basal lobe of gonocoxite with one spine or with at least one enlarged seta among thinner setae
(Fig. 7.40a)............................................................................................................................................. 27
Basal lobe without a spine or enlarged seta. All setae on basal lobe with more or less the same length
and width (Fig. 7.40b)............................................................................................................................ 40
124 7 Key to Male Mosquitoes

Fig. 7.39 Gonocoxite of: (a) Oc. nigripes; (b) Oc. impiger Fig. 7.40 Basal lobe of gonocoxite of:
(a) Oc. cataphylla; (b) Oc. behningi

27 (26) Claspette filament evenly sclerotized, without transparent wings (Fig. 7.41a)..................................... 28
Claspette filament differentiated into a well sclerotized ridge and 1 or 2 weakly sclerotized, transparent
wings (Fig. 7.41b).................................................................................................................................. 29

Fig. 7.41 Claspette filament of:

(a) Oc. punctor; (b) Oc. communis Fig. 7.42 Claspette of: (a) Oc. hexodontus; (b) Oc. punctodes

28 (27) Claspette filament relatively short, shorter than the stem, strongly sclerotized (Fig. 7.42a).....................
......................................................................................... Oc. hexodontus and Oc. punctor (p 233, 251)
Claspette filament relatively long, of almost the same length as the stem, weakly sclerotized
(Fig. 7.42b)............................................................................................................. Oc. punctodes (p 250)
29 (27) Wing narrow, of more or less similar width along the whole claspette filament (Fig. 7.43a)............... 30
Wing broad, distinctly widening the claspette filament at any section between its base and apex
(Fig. 7.43b)............................................................................................................................................. 32

Fig. 7.43 Claspette filament of: (a) Oc. leucomelas; (b) Oc. cataphylla
7.2 Genera Aedes and Ochlerotatus 125

30 (29) Upper part of basal lobe with a row of apically strongly curved, sometimes. hooked setae
(Fig. 7.44a).............................................................................................................Oc. communis (p 220)
Upper part of basal lobe with straight or slightly curved setae, never hooked (Fig. 7.44b).................. 31

Fig. 7.44 Basal lobe of gonocoxite of: Fig. 7.45 Claspette of: (a) Oc. pionips; (b) Oc. leucomelas
(a) Oc. communis; (b) Oc. pionips

31 (30) Claspette stem straight or slightly curved (Fig. 7.45a)...............................................Oc. pionips (p 246)
Claspette stem strongly curved (Fig. 7.45b)........................................................ Oc. leucomelas (p 238)
32 (29) Setae above basal lobe of gonocoxite long, usually overlapping in the middle. Claspette stem strongly
curved in the middle (Fig. 7.46a,b)........................................................................Oc. cataphylla (p 218)
At least several setae immediately above basal lobe of gonocoxite short, not overlapping in the middle,
or if all setae are long, claspette stem more or less straight or slightly curved in the apical part (Oc.
detritus) (Fig. 7.46c,d)........................................................................................................................... 33

Fig. 7.46 Gonocoxite and claspette of: (a, b) Oc. cataphylla; (c) Oc. sticticus; (d) Oc. detritus
126 7 Key to Male Mosquitoes

33 (32) Basal lobe of gonocoxite constricted at its base (Fig. 7.47a)................................................................. 34

Basal lobe gradually arising from gonocoxite (Fig. 7.47b)................................................................... 35

Fig. 7.47 Basal lobe of gonocoxite of: Fig. 7.48 Basal lobe of gonocoxite of:
(a) Oc. sticticus; (b) Oc. mercurator (a) Oc. sticticus; (b) Oc. nigrinus

34 (33) Basal lobe of gonocoxite more or less crescent shaped, its upper part slender (Fig. 7.48a)
.................................................................................................................................. Oc. sticticus (p 255)
Upper part of basal lobe of gonocoxite broad and rounded (Fig. 7.48b)..................Oc. nigrinus (p 243)
35 (33) Basal lobe of gonocoxite longer than broad at its base (Fig. 7.49a)...................................................... 36
Basal lobe distinct but not longer than broad at its base (Fig. 7.49b).................................................... 37

Fig. 7.49 Basal lobe of gonocoxite of: Fig. 7.50 Basal lobe of gonocoxite and claspette of:
(a) Oc. cantans; (b) Oc. cyprius (a) Oc. cantans; (b) Oc. riparius

36 (35) Basal lobe of gonocoxite narrow and markedly elongated. Claspette filament extremely broad, at least
half as wide as long (Fig. 7.50a)................................................................................Oc. cantans (p 214)
Basal lobe of gonocoxite slightly longer than broad at its base. Claspette filament moderately broad, less
than 1/4 of its length (Fig. 7.50b)..............................................................................Oc. riparius (p 253)
7.2 Genera Aedes and Ochlerotatus 127

37 (35) Basal lobe of gonocoxite more or less conical, with 1 spine and long setae (Fig. 7.51a)..................... 38
Basal lobe of gonocoxite more flattened, with 1 spine and short, dense setae (Fig. 7.51b)......................
............................................................................................................................... Oc. flavescens (p 231)

Fig. 7.51 Basal lobe of gonocoxite of: Fig. 7.52 Claspette filament of:
(a) Oc. detritus; (b) Oc. flavescens (a) Oc. mercurator; (b) Oc. cyprius

38 (37) Claspette filament with long stalk, widened from about or beyond the middle (Fig. 7.52a)................. 39
Claspette filament without stalk, widened from its base (Fig. 7.52b).........................Oc. cyprius (p 221)
39 (38) Claspette filament evenly widened into a wing from about its middle. Lobe of tergum IX with 3-8 spine-
like setae (Fig. 7.53a,b).............................................................................................. Oc. detritus (p 223)
Claspette filament abruptly widened into a wing beyond the middle. Lobe of tergum IX with 6–12 spine
like setae (Fig. 7.53c,d)........................................................................................ Oc. mercurator (p 242)

Fig. 7.53 Claspette filament and lobe of tergum IX of: (a, b) Oc. detritus; (c, d) Oc. mercurator

40 (26) Basal lobe of gonocoxite conical, more or less as long as broad at the base (Fig. 7.54a).
.................................................................................................................................................Oc. behningi (p 211)
Basal lobe of gonocoxite flattened, indistinct or absent (Fig. 7.54b).................................................... 41
41 (40) Claspette stem stout, slightly swollen at the apex. Claspette filament slightly swollen beyond the middle
(Fig. 7.55a)..............................................................................................................Oc. annulipes (p 209)
Claspette stem slender, tapering apically. Claspette filament tapering gradually towards the apex
(Fig. 7.55b)............................................................................................................................................. 42
128 7 Key to Male Mosquitoes

Fig. 7.54 Basal lobe of gonocoxite of: Fig. 7.55 Claspette of: (a) Oc. annulipes; (b) Oc. excrucians
(a) Oc. behningi; (b) Oc. annulipes

42 (41) Apical lobe small, not reaching the level of gonostylus articulation (Fig. 7.56a).....................................
..........................................................................................Oc. excrucians and Oc. surcoufi (p 229, 231)
Apical lobe prominent, protruding above the level of gonostylus articulation (Fig. 7.56b)......................
.....................................................................................................................................Oc. euedes (p 228)

Fig. 7.56 Apical lobe of gonocoxite of: (a) Oc. excrucians s.l.; (b) Oc. euedes

7.3 Genus Culex

1 Gonocoxite with a broad, flattened, sclerotized process at the apex, extending distinctly beyond the base
of the gonostylus (Fig. 7.57a)......................................................................................Cx. hortensis (p 282)
Gonocoxite without a process at the apex (Fig. 7.57b)................................................................................ 2
2 (1) Gonocoxite with small scales on the outer surface. Lobe of gonocoxite located slightly beyond the middle
(Fig. 7.58a)................................................................................................................................................... 3
Gonocoxite without scales on the outer surface. Lobe of gonocoxite located well beyond the middle
(Fig. 7.58b)................................................................................................................................................... 4
7.3 Genus Culex 129

Fig. 7.57 Apex of gonocoxite of: Fig. 7.58 Gonocoxite of: (a) Cx. modestus; (b) Cx. brumpti
(a) Cx. hortensis; (b) Cx. martinii

3 (2) Gonostylus relatively long, more or less half as long as gonocoxite. Ventral arm of aedeagus short, its apex
not extending beyond the apex of paraproct (Fig. 7.59a)........................................... Cx. modestus (p 265)
Gonostylus short, distinctly shorter than half the length of gonocoxite. Ventral arm of aedeagus long, its
apex extending beyond apex of paraproct (Fig. 7.59b)..................................................Cx. pusillus (p 267)

Fig. 7.59 Hypopygium of: (a) Cx. modestus; (b) Cx. pusillus

4 (2) Lobe of gonocoxite with one or several transparent, broad, oval or lanceolate scale like setae. Apex of
paraproct with several rows of spines (Fig. 7.60a)...................................................................................... 5
Lobe of gonocoxite with distinctly sclerotized broad and narrow setae. Transparent scale like setae absent.
Apex of paraproct with a row of large denticles, sometimes in addition to the denticles several rows of
short spines could be present (Fig. 7.60b)................................................................................................. 12
5 (4) Gonostylus expanded beyond the middle (Fig. 7.61a)................................................................................. 6
Gonostylus not expanded beyond the middle, tapering apically (Fig. 7.61b)............................................. 7
130 7 Key to Male Mosquitoes

Fig. 7.60 Gonocoxite and paraproct of: Fig. 7.61 Gonostylus of: (a) Cx. perexiguus; (b) Cx. mimeticus
(a) Cx. perexiguus; (b) Cx. territans

6 (5) Ventral arm of aedeagus slender, extended apically into a fan shaped process which bears 5 spines.
The spines do not exceed the upper border of the fan (Fig. 7.62a)................................Cx. brumpti (p 269)
Ventral arm of aedeagus stout, with a concave apex not bearing any spines (Fig. 7.62b)...Cx. perexiguus (p 273)

Fig. 7.62 Aedeagus of: (a) Cx. brumpti; (b) Cx. perexiguus Fig. 7.63 Gonostylus of: (a) Cx. laticinctus; (b) Cx. theileri

7 (5) Gonostylus sharply bent (Fig. 7.63a).........................................................................Cx. laticinctus (p 270)

Gonostylus gradually curved (Fig. 7.63b). ................................................................................................. 8
8 (7) Ventral arm or both, dorsal and ventral arms of aedeagus with denticles or teeth (Fig. 7.64a)................... 9
Dorsal and ventral arms of aedeagus without denticles or teeth (Fig. 7.64b)............................................ 10

Fig. 7.64 Aedeagus of: (a) Cx. theileri; (b) Cx. p. pipiens Fig. 7.65 Aedeagus of: (a) Cx. mimeticus; (b) Cx. theileri

9 (8) Ventral arm of aedeagus with 1-2 denticles, dorsal arm usually with 3 finger-like processes
(Fig. 7.65a).................................................................................................................Cx. mimeticus (p 271)
Ventral arm of aedeagus with 2-4 strong lateral teeth, dorsal arm simple, slender, pointed
(Fig. 7.65b)...................................................................................................................... Cx. theileri (p 280)
7.3 Genus Culex 131

10 (8) Dorsal arm of aedeagus tube like, truncate apically or straight and pointed, never twisted. Ventral arm of
paraproct usually weakly developed, transparent (slightly sclerotized) (Fig. 7.66a,c).......................... 11
Dorsal arm of aedeagus twisted and pointed apically. Ventral arm of paraproct well developed, strongly
sclerotized (Fig. 7.66b)......................................................................................... Cx. torrentium (p 279)
11 (10) Ventral arm of aedeagus slender, sickle shaped (Fig. 7.66a).................................. Cx. p. pipiens (p 275)
Ventral arm of aedeagus broad, leaf like (Fig. 7.66c).............................Cx. p. quinquefasciatus (p 278)

Fig. 7.66 Aedeagus and paraproct of: (a) Cx. p. pipiens; (b) Cx. torrentium; (c) Cx. p. quinquefasciatus

12 (4) Gonocoxite with many long and conspicuous setae on its outer surface. Gonostylus constricted subapically,
then expanding into a “T”-shaped apical part (Fig. 7.67a)....................................Cx. impudicus (p 284)
Gonocoxite with less conspicuous setae on its outer surface. Apex of gonostylus not “T”-shaped, gradu-
ally tapering from the middle (Fig. 7.67b)............................................................................................. 13

Fig. 7.67 Gonocoxite of: (a) Cx. impudicus; (b) Cx. territans Fig. 7.68 Gonocoxite and paraproct of:
(a) Cx. martinii; (b) Cx. territans

13 (12) Gonostylus short, markedly widened beyond the middle. Apex of paraproct widened with a convex row
of denticles (Fig. 7.68a)............................................................................................ Cx. martinii (p 285)
Gonostylus elongated, usually evenly tapering from base to apex. Apex of paraproct not widened, with
an inwardly curved row of denticles (Fig. 7.68b).....................................................Cx. territans (p 286)
132 7 Key to Male Mosquitoes

7.4 Genus Culiseta

1 Tergum IX laterally expanded into two long and slender, sclerotized lobes bearing tiny spine like
setae at the apex. Gonostylus broadened apically, blunt, with 2 short, pointed apical spines
(Fig. 7.69a,b)..................................................................................................... Cs. longiareolata (p 289)
Lobe of tergum IX small or indistinct, bearing long setae. Gonostylus tapering apically, apical spine
single (Fig. 7.69c,d)................................................................................................................................. 2

a b c d

Fig. 7.69 Tergum IX and gonostylus of: (a, b) Cs. longiareolata; (c, d) Cs. morsitans

2 (1) Aedeagus usually oval, slightly sclerotized (Fig. 7.70a) (in Cs. bergrothi the oval shaped aedeagus is
slightly sclerotized at least in the lateral parts). . .................................................................................... 3
Aedeagus usually elongated, conical. Lateral plates strongly sclerotized, pointed and well separated at
the apex (Fig. 7.70b)................................................................................................................................ 7

Fig. 7.70 Aedeagus of: (a) Cs. litorea; (b) Cs. alaskaensis Fig. 7.71 Basal lobes and tergum VIII of:
(a) Cs. litorea; (b) Cs. bergrothi

3 (2) Basal lobe of gonocoxite well developed, elongated. Median lobe of tergum VIII with a row of less than
10 strong spine like setae (Fig. 7.71a)...................................................................................................... 4
Basal lobe of gonocoxite weakly developed. Median lobe of tergum VIII with a row of usually more
than 10 (4–18) strong spine like setae (Fig. 7.71b)..................................................Cs. bergrothi (p 301)
7.4 Genus Culiseta 133

4 (3) Gonocoxite plump in appearance, more or less twice as long as its basal width. Basal lobe of gonocoxite
with 2 stout setae, longer seta reaching apex of gonocoxite (Fig. 7.72a).........................Cs. litorea (p 292)
Gonocoxite elongated, at least 2.5 times as long as its basal width. Basal lobe of gonocoxite with 2 or more
(usually 3-8) stout setae, no seta reaching apex of gonocoxite (Fig. 7.72b)................................................ 5

Fig. 7.72 Gonocoxite of: (a) Cs. litorea; (b) Cs. fumipennis Fig. 7.73 Basal lobe of gonocoxite of:
(a) Cs. ochroptera; (b) Cs. morsitans

5 (4) Basal lobe of gonocoxite with 5-8 strong setae (Fig. 7.73a).................................... Cs. ochroptera (p 296)
Basal lobe of gonocoxite with 2-4 strong setae (Fig. 7.73b)....................................................................... 6
6 (5) Gonostylus long and slender, abruptly constricted shortly beyond the base (Fig. 7.74a)
..................................................................................................................................Cs. fumipennis (p 291)
Gonostylus more stout, without abrupt constriction (Fig. 7.74b)............................... Cs. morsitans (p 294)

Fig. 7.74 Gonostylus of: (a) Cs. fumipennis; (b) Cs. morsitans Fig. 7.75 Apical lobe of gonocoxite of:
(a) Cs. glaphyroptera; (b) Cs. alaskaensis

7 (2) Apical lobe of gonocoxite with several long lanceolate setae (Fig. 7.75a)......... Cs. glaphyroptera (p 303)
Apical lobe of gonocoxite with thin short setae or absent (Fig. 7.75b)....................................................... 8
134 7 Key to Male Mosquitoes

8 (7) Apical lobe of gonocoxite well developed and slightly convex, densely covered with short setae
(Fig. 7.76a)............................................................................................................... Cs. alaskaensis (p 298)
Apical lobe of gonocoxite indistinct or absent (Fig. 7.76b)........................................................................ 9

Fig. 7.76 Apical lobe of gonocoxite of: Fig. 7.77 Basal lobe of gonocoxite of:
(a) Cs. alaskaensis; (b) Cs. annulata (a) Cs. annulata; (b) Cs. subochrea

9 (8) Basal lobe of gonocoxite with 2 (rarely 3) setae distinctly stouter than the others (Fig. 7.77a). Median lobe
of tergum VIII usually without stout setae, rarely a few present (1–4)....................... Cs. annulata (p 299)
Basal lobe of gonocoxite with 3-5 setae distinctly stouter than the others (Fig. 7.77b). Median lobe of
tergum VIII with several stout setae (usually 4)........................................................ Cs. subochrea (p 305)

7.5 Genus Coquillettidia

1 Base of gonostylus slightly constricted below expanded portion, and then sharply narrowed in the middle
part (Fig. 7.78a)........................................................................................................... Cq. richiardii (p 308)
Base of gonostylus broad, continuation stem like, expanded apically into a bulbous structure
(Fig. 7.78b)..................................................................................................................... Cq. buxtoni (p 307)

Fig. 7.78 Gonostylus of: (a) Cq. richiardii; (b) Cq. buxtoni
Chapter 8
Key to Mosquito Fourth Instar Larvae

Genera

1 Abdominal segment VIII without elongate siphon (Fig. 8.1a)........................................ Anopheles (p 164)
Abdominal segment VIII with elongate siphon (Fig. 8.1b)......................................................................... 2
2 (1) Siphon short, apex strongly sclerotized and pointed, with saw-like apparatus for cutting
and piercing plant tissues (Fig. 8.2a).......................................................................... Coquillettidia (p 306)
Siphon longer, apex not pointed, without such an adaptation (Fig. 8.2b). .................................................. 3

Fig. 8.1 Abdominal segment VIII of: (a) Anopheles sp.; (b) Aedes sp.

Fig. 8.2 Siphon of: (a) Cq. richiardii; (b) Cx. p. pipiens

N. Becker et al., Mosquitoes and Their Control, 135

DOI 10.1007/978-3-540-92874-4_8, © Springer-Verlag Berlin Heidelberg 2010
136 8 Key to Mosquito Fourth Instar Larvae

3 (2) Siphon with several pairs of siphonal tufts (1-S) (Fig. 8.3a)...................................................Culex (p 264)
Siphon with one pair of siphonal tufts (Fig. 8.3b)....................................................................................... 4
4 (3) Pecten absent. Abdominal segments VI–VIII with more or less developed sclerotized plates dorsally
(Fig. 8.4a). .......................................................................................... Orthopodomyia pulcripalpis (p 310)
Pecten present. Abdominal segments VI–VIII without sclerotized plates dorsally (Fig. 8.4b). ................. 5

Fig. 8.3 Siphon of: (a) Cx. hortensis; (b) Ae. vexans

Fig. 8.4 End of abdomen of: (a) Or. pulcripalpis; (b) Oc. detritus

5 (4) Siphonal tuft (1-S) inserted at the base of the siphon (Fig. 8.5a)........................................Culiseta (p 288)
Siphonal tuft inserted close to the middle or near the apex of the siphon (Fig. 8.5b)................................. 6
6 (5) Abdominal segment VIII with sclerotized plates laterally, comb scales arising from the posterior margin
of the plates (Fig. 8.6a)............................................................................Uranotaenia unguiculata (p 312)
Abdominal segment VIII without sclerotized plates laterally. Only comb scales are present
and they never arise from sclerotized plates (Fig. 8.6b).....................Aedes and Ochlerotatus (p 187, 204)
8.1 Genus Anopheles 137

Fig. 8.5 Siphon of: (a) Cs. annulata; (b) Oc. caspius

Fig. 8.6 Abdominal segment VIII of: (a) Ur. unguiculata; (b) Ae. cinereus

8.1 Genus Anopheles

1 Frontal setae (5-C to 7-C) long, pinnate. Antenna covered with spicules, at least on its inner surface
(Fig. 8.7a)..................................................................................................................................................... 2
Frontal setae short, single. Antenna not covered with spicules (Fig. 8.7b)................An. plumbeus (p 178)

a b

Fig. 8.7 Head of: (a) An. algeriensis; (b) An. plumbeus
138 8 Key to Mosquito Fourth Instar Larvae

2 (1) Inner clypeal setae (2-C) situated close together, closer to each other than to outer clypeal setae (3-C)
(Fig. 8.8a). ................................................................................................................................................... 3
Inner clypeal setae widely separated, closer to outer clypeal setae than to each other (Fig. 8.8b). ............ 8

a b

Fig. 8.8 Head of: (a) An. claviger s.s.; (b) An. superpictus

3 (2) Outer clypeal seta (3-C) simple or aciculate (Fig. 8.9a) (2-3 apical branches in An. claviger s.l.)............. 4
Outer clypeal seta dendriform (Fig. 8.9b). .................................................................................................. 7

a b

Fig. 8.9 Head of: (a) An. marteri; (b) An. maculipennis s.l.

4 (3) Frontoclypeus with 3 dark transverse bands. Clypeal setae (2-C and 3-C) aciculate (Fig. 8.10a)................
..................................................................................................................................An. algeriensis (p 165)
Frontoclypeus spotted but not banded. Clypeal setae simple or with 2-3 apical branches (Fig. 8.10b). .... 5

a b

Fig. 8.10 Head of: (a) An. algeriensis; (b) An. claviger s.s.
8.1 Genus Anopheles 139

5 (4) Postclypeal seta (4-C) single, sometimes with 2 branches (Fig. 8.11a). Antepalmate setae on abdominal
segments IV and V (2-IV and 2-V) with 1-3 branches.............................................................................. 6
Postclypeal seta with 2-5 branches (Fig. 8.11b). Antepalmate setae on abdominal segments IV and V
with 3-5 branches. Palmate setae on abdominal segment II (1-II) with 10–15 leaflets...............................
.............................................................................................................................. An. claviger s.s. (p 166)

a b

Fig. 8.11 Head of: (a) An. marteri; (b) An. claviger s.s.

6 (5) Leaflets of palmate setae terminating in a long filament which is 1/3 as long as the blade (Fig. 8.12a). Antepalmate
setae on abdominal segments IV and V (2-IV and 2-V) with 1 or rarely 2 branches.............An. marteri (p 177)
Leaflets of palmate setae with slightly elongated apex but without terminal filaments. (Fig. 8.12b).
Antepalmate setae on abdominal segments IV and V with 2-3 branches. Palmate setae on abdominal
segment II (1-II) with more than 15 leaflets........................................................... An. petragnani (p 168)
7 (3) Inner clypeal seta (2-C) with short apical branches. Antennal seta (1-A) inserted in the middle
or slightly below the middle of antenna (Fig. 8.13a). .............................................. An. hyrcanus (p 169)
Inner clypeal seta with long apical branches. Antennal seta inserted in basal 1/4 to 1/3 of antenna
(Fig. 8.13b)............................................................................Anopheles Maculipennis Complex (p 170)

a b

Fig. 8.12 Leaflet of palmate seta of: Fig. 8.13 Head of: (a) An. hyrcanus; (b) An. maculipennis s.l.
(a) An. marteri; (b) An. petragnani
140 8 Key to Mosquito Fourth Instar Larvae

8 (2) Inner frontal setae (5-C) slightly longer than median frontal setae (6-C) (Fig. 8.14a)............................. 9
Inner frontal setae distinctly longer than median frontal setae (Fig. 8.14b)............................................ 10

a b

Fig. 8.14 Head of: (a) An. sergentii; (b) An. multicolor

9 (8) Sclerotized tergal plate on abdominal segment VII broad, broader than distance between palmate
setae (1-VII). Filament of abdominal palmate setae long, more than half as long as the blade (Fig. 8.15a,
b)................................................................................................................................. An. sergentii (p 183)
Sclerotized tergal plate on abdominal segment VII relatively small, smaller than distance
between palmate setae. Filament of abdominal palmate setae short, about half as long as the blade
(Fig. 8.15c, d)...........................................................................................An. cinereus hispaniola (p 181)

a b c d

Fig. 8.15 Abdominal segment VII and leaflet of palmate seta of: (a, b) An. sergentii; (c, d) An. cinereus hispaniola

10 (8) Inner clypeal setae (2-C) simple (Fig. 8.16a). Typical palmate setae on metathorax (1-T) absent.............
................................................................................................................................. An. multicolor (p 182)
Inner clypeal setae with short branches (aciculate) (Fig. 8.16b). Typical palmate setae on metathorax
present.................................................................................................................... An. superpictus (p 185)
a b

Fig. 8.16 Head of: (a) An. multicolor; (b) An. superpictus
8.2 Genera Aedes and Ochlerotatus 141

8.2 Genera Aedes and Ochlerotatus

1 (2) Antenna distinctly longer than the head (Fig. 8.17a) . ............................................... Oc. diantaeus (p 224)
Antenna as long as or shorter than the head (Fig. 8.17b)............................................................................ 2

a b

Fig. 8.17 Head of: (a) Oc. diantaeus; (b) Oc. riparius Fig. 8.18 Siphon of: (a) Oc. berlandi; (b) Oc. euedes

2 (1) Siphon extremely long and slender, siphonal index at least 5.5 (Fig. 8.18a) ...............Oc. berlandi (p 212)
Siphon otherwise, siphonal index never exceeds 5.5 (Fig. 8.18b)............................................................... 3
3 (2) Entire body surface covered with dense rows of spicules (Fig. 8.19a).......................... Oc. cyprius (p 221)
Body surface without spicules. Some indistinct spicules may be present on the last abdominal segments
(Fig. 8.19b)................................................................................................................................................... 4

Fig. 8.19 Fragment of integument of: Fig. 8.20 Siphon of: (a) Ae. vexans; (b) Oc. hexodontus
(a) Oc. cyprius; (b) Ae. vexans

4 (3) Siphonal tuft (1-S) short, about half as long as the width of the siphon at the point of its origin, or shorter.
Tuft inserted well beyond the middle of siphon (Fig. 8.20a)....................................................................... 5
Siphonal tuft long, at least 2/3 as long as the width of the siphon at the point of its origin, or longer. Tuft
may be inserted before or beyond the middle of siphon (Fig. 8.20b).......................................................... 7
5 (4) Frontal setae (5-C to 7-C) arranged in an triangular pattern (Fig. 8.21a). Median setae of labral brush ser-
rated apically.................................................................................................................... Ae. vexans (p 194)
Frontal setae arranged in an arc-like row (Fig. 8.21b). All setae of labral brush simple............................. 6
142 8 Key to Mosquito Fourth Instar Larvae

Fig. 8.22 Head and prothorax of:

Fig. 8.21 Head of: (a) Ae. vexans; (b) Ae. cinereus (a) Ae. rossicus; (b) Ae. cinereus

6 (5) Antennal seta (1-A) inserted in the middle of antenna. Prothoracic seta 4-P with 4 branches, 7-P
with 5-6 branches (Fig. 8.22a)................................................................................... Ae. rossicus (p 192)
Antennal seta inserted slightly before the middle, at 2/5 of the length of antenna. Prothoracic
setae 4-P with 2 branches, 7-P with 3 branches (Fig. 8.22b).Ae. cinereus and Ae. geminus (p 189, 191)
7 (4) Base of siphon with acus (Fig. 8.23a). .................................................................................................... 8
Base of siphon without acus. (indistinct in Ae. vittatus) (Fig. 8.23b).................................................... 45

Fig. 8.23 Siphon of: (a) Oc. punctor; (b) Ae. aegypti Fig. 8.24 Antenna of: (a) Oc. rusticus; (b) Oc. geniculatus

8 (7) Antennae covered with more or less numerous spicules (Fig. 8.24a). .................................................... 9
Antennae without spicules (Fig. 8.24b)................................................................................................. 43
9 (8) Dorsal surface of siphon with several pairs of additional setae (Fig. 8.25a)......................................... 10
Dorsal surface of siphon without additional setae (Fig. 8.25b)............................................................. 14
10 (9) Siphonal tuft (1-S) attached within the distal pecten teeth (Fig. 8.26a)................................................ 11
Siphonal tuft attached beyond the distalmost pecten tooth (Fig. 8.26b). .............................................. 13

Fig. 8.25 Siphon of: (a) Oc. rusticus; (b) Oc. punctor Fig. 8.26 Siphon of: (a) Oc. rusticus; (b) Oc. refiki
8.2 Genera Aedes and Ochlerotatus 143

11 (10) Siphonal seta (1-S) simple. 3-4 distal pecten teeth atypical, spine-like, widely spaced, almost reaching
apex (Fig. 8.27a)................................................................................................. Oc. subdiversus (p 263)
Siphonal seta with 5-8 branches. 1-3 distal pecten teeth widely spaced, but not reaching to apical 1/3 of
siphon (Fig. 8.27b)................................................................................................................................. 12
12 (11) Prothoracic seta 1-P simple. Seta 9-S small (Fig. 8.26a). ........................................ Oc. rusticus (p 261)
Prothoracic seta 1-P with 3 branches. Seta 9-S large, hook shaped (Fig. 8.27b). .Oc. quasirusticus (p 258)

Fig. 8.27 Siphon of: (a) Oc. subdiversus; (b) Oc. quasirusticus Fig. 8.28 Siphon of: (a) Oc. refiki; (b) Oc. lepidonotus

13 (10) Dorsal surface of siphon with 3 pairs of additional setae (Fig. 8.28a)...........................Oc. refiki (p 259)
Dorsal surface of siphon with 2 pairs of additional setae (Fig. 8.28b)................ Oc. lepidonotus (p 257)
14 (9) Saddle completely surrounding anal segment or ventral margins of the saddle are separated by a very
narrow gap (Fig. 8.29a).......................................................................................................................... 15
Saddle extending to the lateral parts of the anal segment to various degrees, but leaving the ventral part
of segment uncovered (Fig. 8.29b)........................................................................................................ 18
15 (14) Distal pecten teeth (one to three) detached (Fig. 8.30a)............................................ Oc. nigripes (p 245)
Pecten teeth evenly spaced, close together (Fig. 8.30b)........................................................................ 16

Fig. 8.29 Anal segment of: (a) Oc. punctor; (b) Oc. cataphylla Fig. 8.30 Siphon of: (a) Oc. nigripes; (b) Oc. punctodes
144 8 Key to Mosquito Fourth Instar Larvae

16 (15) Number of comb scales 6-9. (Fig. 8.31a)............................................................. Oc. hexodontus (p 233)
Number of comb scales 10–30. (Fig. 8.31b).......................................................................................... 17

a b

Fig. 8.31 Abdominal segment VIII of: Fig. 8.32 Head of: (a) Oc. punctor; (b) Oc. punctodes
(a) Oc. hexodontus; (b) Oc. punctor

17 (16) Saddle completely surrounding anal segment. Inner (5-C) and median (6-C) frontal setae with
1-3 branches (Fig. 8.32a)............................................................................................Oc. punctor (p 251)
Lower margins of the saddle are separated by a very narrow gap. Inner and median frontal setae single
(Fig. 8.32b). ............................................................................................................Oc. punctodes (p 250)
18 (14) Anal segment with 1-3 precratal setae (4-X) (Fig. 8.33a)..................................................................... 19
Anal segment with 4-6 precratal setae, sometimes up to 10 (Fig. 8.33b).............................................. 33

Fig. 8.33 Anal segment of: (a) Oc. intrudens; (b) Oc. annulipes Fig. 8.34 Siphon of: (a) Oc. cataphylla; (b) Oc. caspius

19 (18) Distal pecten teeth (1-4) detached (Fig. 8.34a). .................................................................................... 20

Pecten teeth evenly spaced, close together (Fig. 8.34b)........................................................................ 21
20 (19) Inner (5-C) and median (6-C) frontal setae single. All detached pecten teeth (2-4) located beyond the
insertion point of the siphonal tuft (1-S) (Fig. 8.35a,b)........................................ Oc. cataphylla (p 218)
Inner and median frontal setae with 3-5 branches. Detached pecten teeth usually located below insertion
point of the siphonal tuft, the distalmost tooth may be located slightly beyond it (Fig. 8.35c,d)................
....................................................................................................................................Oc. intrudens (p 237)
8.2 Genera Aedes and Ochlerotatus 145

a b c d

Fig. 8.35 Head and siphon of: (a, b) Oc. cataphylla; (c, d) Oc. intrudens

21 (19) Anal papillae usually much shorter than the saddle, rarely as long as or up to 1.3 times longer than the
saddle (Fig. 8.36a).................................................................................................................................. 22
Anal papillae distinctly longer than the saddle, at least 1.3 times longer than the saddle
(Fig. 8.36b)............................................................................................................................................. 25

a b

Fig. 8.36 Anal segment of: (a) Oc. detritus; (b) Oc. communis Fig. 8.37 Comb scales of: (a) Oc. detritus; (b) Oc. caspius

22 (21) Comb with more than 40 scales. Comb scales blunt ended (median spine is not distinctly longer
than the others) (Fig. 8.37a). Inner frontal seta (5-C) with 2-3 branches................... Oc. detritus (p 223)
Comb with less than 35 scales. Comb scales pointed (median spine always distinctly longer than the others, at
least in some scales) (Fig. 8.37b). Inner frontal seta usually single, sometimes with 2 branches.....................23
23 (22) Siphonal tuft (1-S) situated beyond the middle of siphon (Fig. 8.38a) ..................... Oc. caspius (p 216)
Siphonal tuft usually situated below, rarely slightly beyond the middle of siphon (Fig. 8.38b)........... 24
146 8 Key to Mosquito Fourth Instar Larvae

Fig. 8.38 Siphon of: (a) Oc. caspius; (b) Oc. leucomelas Fig. 8.39 Anal segment of: (a) Oc. leucomelas; (b) Oc. dorsalis

24 (23) Anal papillae tapering. Saddle seta (1-X) long, nearly as long as the saddle (Fig. 8.39a). . .....................
.............................................................................................................................. Oc. leucomelas (p 238)
Anal papillae rounded. Saddle seta half as long as the saddle (Fig. 8.39b)................Oc. dorsalis (p 226)
25 (21) Comb with more than 40 scales (Fig. 8.40a)......................................................................................... 26
Comb with less than 40 scales (Fig. 8.40b)........................................................................................... 28

a b

Fig. 8.40 Abdominal segment VIII of: Fig. 8.41 Head of: (a) Oc. communis; (b) Oc. pionips
(a) Oc. communis; (b) Oc. sticticus

26 (25) Inner (5-C) and median (6-C) frontal setae single, rarely one seta with 2 branches
(Fig. 8.41a). .......................................................................................................... Oc. communis (p 220)
Inner and median frontal setae multiple branched, with 3 or more branches (Fig. 8.41b). .................. 27
27 (26) Antennae long, about 2/3 as long as the head or slightly longer. General appearance of comb
scales blunt. Elongated median spine absent, all spines of similar length (Fig. 8.42a,b). .Oc. pionips (p 246)
Antennae shorter, about half as long as the head. General appearance of comb scales pointed. At least some
lateral scales with the median spine distinctly longer than the others (Fig. 8.42c,d). ..........Oc. pullatus (p 249)
8.2 Genera Aedes and Ochlerotatus 147

a b c d

Fig. 8.42 Head and comb scale of: (a, b) Oc. pionips; (c, d) Oc. pullatus

28 (25) Number of comb scales 6–16 (Fig. 8.43a)............................................................................................. 29

Number of comb scales more than 16 (Fig. 8.43b)................................................................................ 30

Fig. 8.43 Abdominal segment VIII of: Fig. 8.44 Anal segment of:
(a) Oc. nigrinus; (b) Oc. hungaricus (a) Oc. nigrinus; (b) Oc. impiger

29 (28) Saddle almost completely covering lateral parts of anal segment (Fig. 8.44a)........ Oc. nigrinus (p 243)
Saddle more plate shaped, extending slightly beyond lateral half of anal segment
(Fig. 8.44b)..................................................................................................................Oc. impiger (p 236)
148 8 Key to Mosquito Fourth Instar Larvae

30 (28) Inner frontal seta (5-C) single. Anal segment with 3 precratal setae (4-X), saddle extending at most to
half of lateral sides (Fig. 8.45a)............................................................................Oc. hungaricus (p 234)
Inner frontal seta with 2 or more branches. If one of the pairs of setae is single, anal segment with
1-2 precratal setae and saddle extending to at least 2/3 of lateral sides (atypical Oc. sticticus)
(Fig. 8.45b)............................................................................................................................................. 31

Fig. 8.45 Anal segment of: Fig. 8.46 Siphon of: (a) Oc. sticticus; (b) Oc. pullatus
(a) Oc. hungaricus; (b) Oc. mercurator

31 (30) Siphonal tuft (1-S) short, never longer than the width of the siphon at its insertion
point (Fig. 8.46a)........................................................................................................ Oc. sticticus (p 255)
Siphonal tuft long, distinctly longer than the width of the siphon at its insertion point
(Fig. 8.46b)............................................................................................................................................. 32
32 (31) Prothoracic setae 2-P and 3-P distinctly shorter and thinner than 1-P (Fig. 8.47a)......................................
................................................................................................................................. Oc. mercurator (p 242)
Prothoracic setae 2-P and 3-P nearly as long and strong as 1-P (Fig. 8.47b)............ Oc. pullatus (p 249)

a b

Fig. 8.47 Prothoracic setae 1-P to 3-P of: Fig. 8.48 Abdominal segment VIII of:
(a) Oc. mercurator; (b) Oc. pullatus (a) Oc. riparius; (b) Oc. mariae s.l.
8.2 Genera Aedes and Ochlerotatus 149

33 (18) Number of comb scales 6–12, rarely 15–17 in Oc. nigrinus (Fig. 8.48a)............................................. 34
Number of comb scales 15–45 (Fig. 8.48b)........................................................................................... 35
34 (33) Inner (5-C) and median (6-C) frontal setae with 2-3 branches. Comb scales arranged
in one row (Fig. 8.49a,b). Siphonal index 3.5–4.0..................................................... Oc. riparius (p 253)
Inner and median frontal setae single (rarely one seta with 2 branches). Comb scales arranged in
2 (rarely 3) rows (Fig. 8.49c,d). Siphonal index never exceeds 3.0, usually 2.0–2.5....Oc. nigrinus (p 243)

a b c d

Fig. 8.49 Head and abdominal segment VIII of: (a, b) Oc. riparius; (c, d) Oc. nigrinus

35 (33) Siphonal index less than 2.0. Anal segment with weakly developed saddle, lateral part triangular.
Anal papillae very short and spherical (Fig. 8.50a).................Oc. mariae and Oc. zammitii (p 240, 242)
Siphonal index more than 2.0. Anal segment with well developed saddle, lateral part more or less rect-
angular. Anal papillae shorter or longer than the saddle, tapering (Fig. 8.50b)..................................... 36

Fig. 8.50 End of abdomen of: (a) Oc. mariae s.l.; (b) Oc. excrucians

36 (35) Number of comb scales less than 20. Siphonal tuft (1-S) short, inserted distinctly beyond the middle of
siphon (Fig. 8.51a)....................................................................................................... Oc. euedes (p 228)
Number of comb scales more than 20. Siphonal tuft usually long, inserted at about the middle
of siphon (Fig. 8.51b)............................................................................................................................. 37
150 8 Key to Mosquito Fourth Instar Larvae

Fig. 8.51 End of abdomen of: (a) Oc. euedes; (b) Oc. excrucians

37 (36) Seta 9-S on posterolateral flap of stigmal plate strong and hooked or curved (Fig. 8.52a)................... 38
Seta 9-S on posterolateral flap of stigmal plate relatively weak, slightly curved (Fig. 8.52b).............. 40

Fig. 8.52 Siphon of: (a) Oc. excrucians; (b) Oc. mercurator

38 (37) Postclypeal seta (4-C) with 6-8 branches. Comb with less than 30 scales (Fig. 8.53a,b)..........................
..................................................................................................................................Oc. behningi (p 211)
Postclypeal seta with 2-3 short, thin branches. Comb with more than 30 scales (Fig. 8.53c,d)............ 39

Fig. 8.53 Head and abdominal segment VIII of: (a, b) Oc. behningi; (c, d) Oc. surcoufi
8.2 Genera Aedes and Ochlerotatus 151

39 (38) Abdominal seta 6 with 2 branches on segments I and II, single on segments III–VI
(Fig. 8.54a)............................................................................................................ Oc. excrucians (p 229)
Abdominal seta 6 with 2 branches on segments I–VI (Fig. 8.54b)............................Oc. surcoufi (p 231)

a b

Fig. 8.54 Abdominal segments I–VI of: (a) Oc. excrucians; (b) Oc. surcoufi

40 (37) Saddle seta (1-X) short, distinctly shorter than the saddle. Siphonal tuft (1-S) distinctly longer
than the width of the siphon at the point of its insertion (Fig. 8.55a)...................Oc. mercurator (p 242)
Saddle seta long, about as long as the saddle. Siphonal tuft (1-S) about as long as the width
of the siphon at the point of its insertion (Fig. 8.55b)............................................................................ 41

Fig. 8.55 End of abdomen of: Fig. 8.56 End of abdomen of:
(a) Oc. mercurator; (b) Oc. flavescens (a) Oc. flavescens; (b) Oc. cantans

41 (40) Anal papillae short, about half as long as the saddle. Siphonal index more than 3.0 (Fig. 8.56a).
................................................................................................................................Oc. flavescens (p 231)
Anal papillae long, about as long as the saddle or longer. Siphonal index usually less than 3.0
(Fig. 8.56b)............................................................................................................................................. 42
42 (41) Ventral brush with 4-6 precratal setae (4-X) and 15–20 cratal setae (4-X) (Fig. 8.57a).................................
.......................................................................................................................................... Oc. cantans (p 214)
Ventral brush with 6-10 precratal setae and 10–15 cratal setae (Fig. 8.57b).......... Oc. annulipes (p 209)
152 8 Key to Mosquito Fourth Instar Larvae

Fig. 8.57 Anal segment of: (a) Oc. cantans; (b) Oc. annulipes

43 (8) Numerous stellate setae on thorax and abdomen. Antennal seta (1-A) single, pecten teeth long
and spine like (Fig. 8.58a,b)................................................................................................................... 44
Stellate setae absent. Antennal seta with 3-4 short branches, pecten teeth short, not spine-like, with a
broad base (Fig. 8.58c,d).......................................................................................Oc. pulcritarsis (p 248)

Fig. 8.58 Antennna and siphon of: (a, b) Oc. echinus; (c, d) Oc. pulcritarsis

44 (43) Branches of stellate setae on abdominal segment I longer than length of the segment. Pecten at least half
as long as the siphon (Fig. 8.59a,b)............................................................................Oc. echinus (p 205)
Branches of stellate setae on abdominal segment I about the same length as the segment. Pecten 1/4-2/5
as long as the siphon (Fig. 8.59c,d)..................................................................... Oc. geniculatus (p 206)
8.2 Genera Aedes and Ochlerotatus 153

a b d

Fig. 8.59 Abdominal segment I and siphon of: (a, b) Oc. echinus; (c, d) Oc. geniculatus

45 (7) Outer frontal seta (7-C) single (Fig. 8.60a)............................................................................................ 46

Outer frontal seta usually with 2 or more branches, rarely single (Fig. 8.60b)..................................... 47

a b

Fig. 8.60 Head of: (a) Ae. aegypti; (b) Ae. vittatus Fig. 8.61 Siphon of: (a) Ae. cretinus; (b) Ae. aegypti

46 (45) In addition to the siphonal tuft (1-S), a single seta is inserted laterally within the apical 1/3 of the siphon
(Fig. 8.61a)................................................................................................................. Ae. cretinus (p 203)
Additional lateral seta absent (Fig. 8.61b)...................................................................Ae. aegypti (p 198)
47 (45) Antennal seta (1-A) with 2-3 branches. Siphonal tuft (1-S) inserted at about 2/3 the length of the siphon
and within the pecten. Distalmost pecten tooth spine like and apically detached (Fig. 8.62a,b)
....................................................................................................................................Ae. vittatus (p 196)
Antennal seta single. Siphonal tuft inserted slightly beyond the middle of the siphon, distal to the pecten
(Fig. 8.62c,d)...........................................................................................................Ae. albopictus (p 201)
154 8 Key to Mosquito Fourth Instar Larvae

a b c d

Fig. 8.62 Antenna and siphon of: (a, b) Ae. vittatus; (c, d) Ae. albopictus

8.3 Genus Culex

1 Siphon long and slender, siphonal index 6.5 or more (Fig. 8.63a).............................................................. 2
Siphon shorter, siphonal index usually less than 6.0 (Fig. 8.63b)............................................................... 7
Note: The siphonal index in specimens of Cx. perexiguus, Cx. brumpti and Cx. territans may vary between the above defined
groups, consequently they are treated under both branches of the key

a b a b

Fig. 8.63 Siphon of: (a) Cx. hortensis; (b) Cx. mimeticus Fig. 8.64 Siphon of: (a) Cx. brumpti; (b) Cx. territans

2 (1) Basal siphonal tuft (1a-S) shorter than the width of siphon at the point of its origin (Fig. 8.64a).............. 3
Basal siphonal tuft equal or longer than the width of siphon at the point of its origin (Fig. 8.64b)............ 4
3 (2) Upper anal seta (2-X) with 2 branches (Fig. 8.65a).................................................. Cx. perexiguus (p 273)
Upper anal seta with 3-4 branches (Fig. 8.65b)............................................................. Cx. brumpti (p 269)
8.3 Genus Culex 155

Fig. 8.65 Anal segment of: (a) Cx. perexiguus; (b) Cx. brumpti

4 (2) Prothoracic seta 3-P nearly as long as 1-P, always longer than the half of 1-P. Basal siphonal tuft (1a-S)
more or less 3 times longer than the width of siphon at the point of its origin. At least one siphonal tuft
clearly inserted within the pecten (Fig. 8.66a,b). ........................................................ Cx. hortensis (p 282)
Prothoracic seta 3-P never exceeding half the length of 1-P. Basal siphonal tuft of variable length,
­usually not more than twice as long as the width of siphon at the point of its origin. Usually no siphonal
tuft inserted within the pecten, rarely one tuft may be inserted close to the last pecten tooth
(Fig. 8.66c,d). ..................................................................................................................................... 5

a b c d

Fig. 8.66 Prothorax and siphon of: (a, b) Cx. hortensis; (c, d) Cx. territans

5 (4) Siphon usually evenly tapering towards the apex. More than 1, usually 2, apical siphonal tufts inserted
laterally. Pecten occupying 1/5 of the siphon length. Anal papillae half as long as the saddle (Fig. 8.67a).
. ...................................................................................................................................... Cx. martinii (p 285)
Siphon distinctly widened at the apex. Only one apical siphonal tuft inserted laterally. Pecten occupying
more than 1/4 of siphon length. Length of anal papillae variable (Fig. 8.67b)............................................. 6
156 8 Key to Mosquito Fourth Instar Larvae

a b

Fig. 8.67 End of abdomen of: Fig. 8.68 Anal segment of:
(a) Cx. martinii; (b) Cx. territans (a) Cx. territans; (b) Cx. impudicus

6 (5) Anal papillae nearly as long as or longer than saddle, pointed (Fig. 8.68a). ............... Cx. territans (p 286)
Anal papillae about half as long as saddle, blunt ended (Fig. 8.68b)........................ Cx. impudicus (p 284)
7 (1) Siphon short, siphonal index at most 3.0. Siphonal tufts (1-S) arranged in a zigzag row on ventral side
(Fig. 8.69a). ....................................................................................................................Cx. pusillus (p 267)
Siphon longer, siphonal index at least 4.0 (Fig. 8.69b). .............................................................................. 8

a b

Fig. 8.69 Siphon of: (a) Cx. pusillus; (b) Cx. p. pipiens Fig. 8.70 Comb scale of: (a) Cx. mimeticus; (b) Cx. territans

8 (7) Comb scales with a distinct median spine longer than the others (Fig. 8.70a). .......................................... 9
Comb scales without a distinct median spine. All spines at the apex of more or less the same length
(Fig. 8.70b). ............................................................................................................................................... 10
9 (8) Subapical setae (2-A, 3-A) inserted at about 2/3 the distance between antennal seta (1-A) and tip of the
antenna. Main tracheal trunks narrow, less than half as wide as the siphon at its apical 1/3 (Fig. 8.71a,b)
....................................................................................................................................Cx. mimeticus (p 271)
Subapical setae inserted close to the tip of antenna. Main tracheal trunks broad, at least half as wide as the
siphon at its apical 1/3 (Fig. 8.71c,d). .............................................................................Cx. theileri (p 280)
8.3 Genus Culex 157

Fig. 8.71 Antenna and siphon of: (a, b) Cx. mimeticus; (c, d) Cx. theileri

10 (8) Several basal siphonal tufts not paired, inserted at the ventral surface forming a zigzag row. If paired,
inserted very close together, near the ventral midline (Fig. 8.72a). ...................................................... 11
All siphonal tufts paired. The pairs more widely separated, inserted ventrolaterally or laterally
(Fig. 8.72b). ........................................................................................................................................... 12

Fig. 8.72 Siphon of: Fig. 8.73 End of abdomen of:

(a) Cx. laticinctus; (b) Cx. territans (a) Cx. modestus; (b) Cx. laticinctus

11 (10) All siphonal tufts (1-S) arranged in a ventral zigzag row. The length of the tufts suddenly drops towards
the apex of the siphon. Usually one tuft inserted within the pecten. Saddle seta (1-X) with
2-3 branches (Fig. 8.73a)......................................................................................... Cx. modestus (p 265)
Not all siphonal tufts arranged in a ventral zigzag row, penultimate tuft arising from the lateral
surface of siphon. The length of the ventral tufts gradually decreases towards the apex of the
siphon. Usually 3 tufts inserted within the pecten. Saddle seta single, sometimes with 2 branches
(Fig. 8.73b). ........................................................................................................... Cx. laticinctus (p 270)
158 8 Key to Mosquito Fourth Instar Larvae

12 (10) All siphonal tufts (1-S) shorter than or equal to the width of the siphon at the point of their insertion
(Fig. 8.74a). ........................................................................................................................................... 13
At least some siphonal tufts distinctly longer than the width of the siphon at the point of their insertion
(Fig. 8.74b). ........................................................................................................................................... 14

Fig. 8.74 Siphon of: (a) Cx. perexiguus; (b) Cx. territans Fig. 8.75 Anal segment of:
(a) Cx. perexiguus; (b) Cx. brumpti

13 (12) Upper anal seta (2-X) with 2 branches (Fig. 8.75a). ............................................ Cx. perexiguus (p 273)
Upper anal seta with 3-4 branches (Fig. 8.75b).........................................................Cx. brumpti (p 269)
14 (12) All siphonal tufts longer than the width of the siphon at the point of their insertion. Basalmost tuft usu-
ally inserted apart from the last pecten tooth (Fig. 8.76a)....................................... Cx. territans (p 286)
Apicalmost siphonal tuft as long as or shorter than the width of the siphon at its point of insertion.
Basalmost tuft usually inserted close to the last pecten tooth (Fig. 8.76b). .......................................... 15

Fig. 8.76 Siphon of: (a) Cx. territans; (b) Cx. p. pipiens

15 (14) Metathoracic seta 1-T longer than half of the length of 2-T. Seta 1 on abdominal segments III–V
(1-III to 1-V) usually with 4-5 branches (sum of the branches on one side usually more than 10).
Saddle seta (1-X) usually with 2 branches. (Fig. 8.77a,b).....................................Cx. torrentium (p 279)
Seta 1-T shorter than half of the length of 2-T. Seta 1 on abdominal segments III–V usually with
1-2 branches (sum of the branches on one side usually 6 or less). Saddle seta usually single.
(Fig. 8.77c,d)..................................................... Cx. p. pipiens and Cx. p. quinquefasciatus (p 275, 278)
8.4 Genus Culiseta 159

Fig. 8.77 Abdominal segments III–V and anal segment of: (a, b) Cx. torrentium; (c, d) Cx. p. pipiens

8.4 Genus Culiseta

1 Antenna shorter than the head, seta 1-A weakly developed. Siphon short, siphonal index less than 4.0
(Fig. 8.78a,b). .......................................................................................................................................... 2
Antenna longer than the head, seta 1-A well developed. Siphon long and slender, siphonal index more
than 5.0 (Fig. 8.78c,d). ............................................................................................................................ 7

Fig. 8.78 Head and siphon of: (a, b) Cs. annulata; (c, d) Cs. morsitans

2 (1) Inner (5-C) and median (6-C) frontal setae single. Siphonal index 2.0 or less. Saddle plate shaped, not
surrounding anal segment (Fig. 8.79a,b)...........................................................Cs. longiareolata (p 289)
Inner and median frontal setae multiple branched. Siphonal index more than 2.0. Saddle completely
surrounding anal segment (Fig. 8.79c,d)................................................................................................. 3

Fig. 8.79 Head and end abdomen of: (a, b) Cs. longiareolata; (c, d) Cs. annulata
160 8 Key to Mosquito Fourth Instar Larvae

3 (2) Antenna less than half as long as the head. Median frontal seta (6-C) with 1-3 branches. (Fig. 8.80a).
Number of comb scales usually less than 50........................................................................................... 4
Antenna at least half as long as the head. Median frontal seta with 4-8 branches. (Fig. 8.80b). Number
of comb scales usually more than 60....................................................................................................... 6

a b

Fig. 8.80 Head of: (a) Cs. alaskaensis; (b) Cs. glaphyroptera Fig. 8.81 Siphon of: (a) Cs. alaskaensis; (b) Cs. annulata

4 (3) Siphonal index less than 3.0, siphon slightly tapering apically (Fig. 8.81a)........ Cs. alaskaensis (p 298)
Siphonal index 3.0–4.0, siphon distinctly tapering apically (Fig. 8.81b)................................................ 5
5 (4) Distance between postclypeal setae (4-C) equal to or longer than distance between inner frontal setae
(5-C) (Fig. 8.82a)...................................................................................................... Cs. annulata (p 299)
Distance between postclypeal setae distinctly shorter than distance between inner frontal setae
(Fig. 8.82b). ............................................................................................................Cs. subochrea (p 305)

a b

Fig. 8.82 Head of: (a) Cs. annulata; (b) Cs. subochrea

6 (3) Antenna 2/3 as long as the head. Pecten spread over 3/4 the length of siphon. Ventral brush with 5 pre-
cratal setae (4-X) (Fig. 8.83a,b)........................................................................Cs. glaphyroptera (p 303)
Antenna half as long as the head. Pecten spread over 2/3 the length of siphon. Ventral brush with
3-4 precratal setae (Fig. 8.83c,d)..............................................................................Cs. bergrothi (p 301)

a b c d

Fig. 8.83 Head and end of abdomen of: (a, b) Cs. glaphyroptera; (c, d) Cs. bergrothi
8.4 Genus Culiseta 161

7 (1) In addition to the typical pecten teeth, the siphon bears spine-like setae irregularly scattered on its ventro-
lateral surface (Fig. 8.84a)........................................................................................Cs. fumipennis (p 291)
Siphon with typical pecten teeth only (distal 1-2 teeth may be detached and atypical, spine like setae in Cs.
ochroptera) (Fig. 8.84b). ............................................................................................................................. 8

Fig. 8.84 Siphon of: (a) Cs. fumipennis; (b) Cs. ochroptera

8 (7) Inner frontal seta (5-C) with 5-9 branches. Anal papillae 1.5–2.0 times longer than the saddle (Fig. 8.85a,b).
. ................................................................................................................. Cs. ochroptera (p 296)
Inner frontal seta with 2-4 branches. Anal papillae shorter than the saddle (Fig. 8.85c,d)......................... 9

a b c d

Fig. 8.85 Head and anal segment of: (a, b) Cs. ochroptera; (c, d) Cs. morsitans

9 (8) Pecten confined to basal 1/4 of siphon. Length of siphonal tuft (1-S) usually 1/3 or less than
length of siphon (Fig. 8.86a). ......................................................................................Cs. morsitans (p 294)
Pecten confined to basal 1/3 of siphon. Length of siphonal tuft usually more than 1/3 length of siphon
(Fig. 8.86b). ...................................................................................................................... Cs. litorea (p 292)
Note: Both species show variation and overlapping in these characters and are difficult to distinguish.
162 8 Key to Mosquito Fourth Instar Larvae

Fig. 8.86 Siphon of: (a) Cs. morsitans; (b) Cs. litorea Fig. 8.87 End of abdomen of:
(a) Cq. richiardii; (b) Cq. buxtoni

8.5 Genus Coquillettidia

1 Seta 1-VIII with 2-4 branches. Saddle completely covered with short and stout, usually single spicules,
rarely 2-3 grouped on a common base (Fig. 8.87a).....................................................Cq. richiardii (p 308)
Seta 1-VIII with 5-7, usually 6 branches. Spicules on saddle grouped in rows of 2-8 (usually 5-6) on a
common base (Fig. 8.87b)..............................................................................................Cq. buxtoni (p 307)
Chapter 9
Subfamily Anophelinae

In adults of this subfamily, at least the first abdominal studies of Sallum et al. (2002) and Harbach and Kitching
segment (tergum I) is devoid of any scales. In general (2005), which suggest that, at the present, Bironella
the development of scaling has not reached the same should be regarded as a subgenus of Anopheles.
level as in the subfamily Culicinae; often the abdomen Adult anophelines (except Chagasia) are usually
is covered with fine setae only. The palps of both sexes recognised at once by their attitude when at rest on walls
are approximately the same length as the proboscis. or other objects. The proboscis is held straight out in
The larvae have no discernible respiratory siphon and line with the body axis, not at an angle as in culicine
seta 1 of most abdominal segments is usually of the mosquitoes, and the body is strongly tilted downwards
palmate type. to the head end. This causes the abdomen to point away
The subfamily comprises only three genera: from the surface and the whole body to form an angle
Anopheles, Bironella and Chagasia. The genus Bironella with the surface. The majority of species form angles of
Theobald includes eight species divided between three 30–45°with the surface on which they rest, but in some
subgenera (Fig. 1.2) that are confined to the Australasian species, such as Anopheles hyrcanus, this angle may
Region. They are easily distinguished from Anopheles even approach 90°. The tip of the labium and the palps
by wing veins Cu1 and M being wavy at their distal parts are usually brought close to the surface, almost being in
and thoracic setae 1-M and 3-T in larvae that are both contact with it. In addition, adult anophelines generally
palmate. The adults are seldom seen in nature and rarely have longer legs than culicines. In females the palps are
bite man. Chagasia Cruz is a small and rare genus; its elongated, about the same length as the proboscis. They
four species are exclusively distributed in the Neotropical are held closely adjacent to the proboscis (except during
region. Adults of this genus are mainly characterized by feeding), so that the palps and the proboscis appear to be
the somewhat trilobed scutellum with a set of setae on a single organ. When the insect is dead and the tissue
each lobe, wings without distinct spots as in most somewhat dried, the elongated palps separate and are
Anopheles and the large claws on the fore and mid legs easily recognised. In males, as in nearly all other mos-
of the males. The larvae of Chagasia have the anterior quitoes, the palps are also elongated. The two apical
flap of the spiracular apparatus produced into a long segments of the palps are swollen and laterally flattened,
spine-like process and the palmate setae on the abdomi- giving them a club like appearance. The larvae of anoph-
nal segments are characteristically shaped. Most of the elines are distinguishable from all other mosquitoes by
species of the subfamily, including all European spe- their feeding behaviour. They usually rest under the
cies, belonging to the genus Anopheles Meigen have a water surface in a horizontal position and feed on parti-
worldwide distribution with more than 450 described cles from the surface film. The head can be rotated
species, species complexes, subspecies and varieties. through 180° toward both sides, so that the ventral side
The genus Bironella of the subfamily, including its three is upward and the mouthparts are in contact with the
subgenera Bironella Theobald, Brugella Edwards and surface. At the sides of the anterior margin of the thorax
Neobironella Tenorio was synonymized with the genus are two lobed, reversible organs (notched organs) which
Anopheles Meigen and redefined as an informal group can be retracted and together with the palmate setae on
within the subgenus Anopheles (Sallum et al. 2000). the abdominal segments, support the body when attach-
However, this synonymy was not supported by later ing into a horizontal position at the surface film.

N. Becker et al., Mosquitoes and Their Control, 163

DOI 10.1007/978-3-540-92874-4_9, © Springer-Verlag Berlin Heidelberg 2010
164 9 Subfamily Anophelinae

9.1 Genus Anopheles Meigen nal segments I–VII is usually of the palmate type, it is
often rudimentary on segments I and II, and well devel-
Members of the genus Anopheles are usually medium oped on segments III–VII. The lateral setae of the first
sized to small mosquitoes with long and slender legs three segments (6-I to 6-III) are long and plumose.
and relatively narrow wings. Their general colouration Each segment has 1 or 2 dorsal sclerotized plates posi-
may be variable from grey, brown or almost black to tioned medially. The spiracular apparatus is situated at
whitish or pale, but without a metallic shine. The the posterior margin of the dorsal side of abdominal
proboscis is straight, long and slender. The palps are segment VIII flush with its surface. On the sides of
usually as long as the proboscis in both sexes, rarely, segment VIII pecten plates are located, each with a
slightly shorter in some tropical females. The palps of posterior row of conspicuous teeth. Both plates are
females consist of five slender palpomeres, except in connected by a narrow sclerotized band, bordering the
An. plumbeus that has a slightly swollen palpomere V. spiracular apparatus posteriorly. The saddle is plate-
The clypeus is usually longer than it is broad, and shaped, and does not encircle the anal segment. The
triangular in shape. The occiput is covered with erect, ventral brush consists of a group of fan-like setae, but
forked scales. The scutum is slightly convex and not without precratal setae. The anal papillae are usually
strongly arched, and clothed with setae of various colours. blunt ended, and about the length of the anal segment.
The scutellum is evenly rounded with a more or less The genus Anopheles is divided into seven subgen-
regular row of long setae. Prespiracular setae are era (Fig. 1.2). Members of the subgenera Kerteszia
usually present. Pulvilli are absent, and tarsal claws of Theobald, Lophopodomyia Antunes, Nyssorhynchus
females are without a subbasal tooth. The wings are Blanchard and Stethomyia Theobald have a mainly
relatively narrow, often with dark or pale scales forming neotropical distribution. Only species of the subgenera
characteristic spots or evenly dark scaled and without Anopheles Meigen and Cellia Theobald are represented
spots; cross veins are usually well separated. The in the Palaearctic region, which includes Europe. A
integument of the terga is usually dark, covered with new subgenus Baimaia Abraham is introduced for the
various coloured setae and usually without scales. The unusual crabhole species, An. kyondawensis Abraham,
abdomen is parallel sided, with a blunt end. The cerci in Southeast Asia (Harbach et al. 2005). The phyloge-
of the females are short, rounded and inconspicuous, netic relationships of Lophopodomyia and Stethomyia
and only one spermatheca is present. with subgenus Anopheles and their sub­generic status
The male hypopygium with a conical gonocoxite, is are uncertain (Sallum et al. 2000, 2002; Harbach and
about twice as long as it is broad, usually without an Kitching 2005).
apical and basal lobe, but with prominent parabasal The eggs of Anopheles are commonly laid singly and
setae of variable number and shape in place of a basal directly on the water surface, where they lie horizontally,
lobe. The gonostylus is approximately as long as the several of them often adhering to one another and form-
gonocoxite, curved, with the apical spine of the gono- ing characteristic configurations of triangles, stars or rib-
stylus short and blunt ended. The claspettes are divided bons due to the surface tension and the shape of the eggs.
into two or more lobes, each lobe bearing long, various The egg of the anopheline is usually boat shaped with
shaped setae at its apex. The aedeagus is tubular, bare pointed ends and has a flattened or slightly concave
or with apical aedeagal leaflets of various shape. upper surface or deck and a more convex lower surface.
The head of the larvae is as long as or longer than it The frill or fringe surrounds the whole, or parts, of the
is broad, and antenna shorter than the head, and rod- upper surface. At the sides of the egg are the floats or air
shaped. Antennal seta (1-A) is small and single or cells, which may interrupt the fringe in the middle. The
more prominent and multiple branched. Two pairs of number of air cells is characteristic for different species.
clypeal setae, the inner (2-C) and outer (3-C), are situ- In species of the Anopheles Maculipennis Complex the
ated at the anterior margin of the head. The frontal ornamentation of the upper surface of the egg and the
setae (5-C to 7-C) are of pinnate or plumose type, form of the intercostal membrane (surface of the air
except in An. plumbeus that has short and single fron- cells) are important diagnostic tools for identification.
tal setae. Most setae of the thorax are usually plumose, Larvae of Anopheles are usually found in natural
varying in length, and arranged in three sets, corre- water bodies and rarely in artificial collections of water.
sponding to the thoracic segments. Seta 1 of abdomi- The preferred breeding places include permanent and
9.1 Genus Anopheles Meigen 165

semi permanent ponds, pools, puddles or ditches with a coloured and may vary from reddish-brown to brown or
growth of emergent aquatic vegetation. They can also dark brown, showing no trace of darkening at the sides
be found in rice fields, swamps or margins of rivers and (Fig. 6.10a). The characteristic median stripe of pale
lakes, where the water flow is reduced through shelters. scales on the scutum, that stretches at least along the
Only a few species show exceptions, like An. plumbeus, anterior half in An. marteri, is also absent. The probos-
which is a typical tree-hole breeder, and An. multicolor, cis and palps are brown to dark brown, the latter nearly
which exhibits a preference for brackish water. as long as the former. The erect head scales are broad,
Although adult females seek their blood meal from and dark brown throughout. The scutum and scutellum
early evening on and then continue to be active through- are brown with blackish setae, and the lobes of the
out the night, they are considered predominantly biters antepronotum are dark brown. The colour of the pleurites
during the crepuscular period after sunset and during is uniformly dark to greyish brown with 2 prespiracular
dawn (Bates 1949). setae, 3 prealar setae, 2 upper mesepisternal setae, and
10 upper mesepimeral setae. The lower mesepisternal
setae and lower mesepimeral setae are absent. The legs
are uniformly dark, very rarely the hind tarsi show indis-
9.1.1 Subgenus Anopheles Meigen tinct pale ringing. The wing veins are covered with dark
scales that are uniformly distributed. The abdominal
The wing is often entirely without pale spots; if pale terga are mainly dark brown without transverse bands.
spots are present (An. hyrcanus), the costal margin is Male (Figs. 7.8a and 9.1): The genitalia are character-
covered with one or two of them in its apical half. The ized by the gonocoxite with only one apically curved
cross veins and bifurcations of R2+3 and M are dark parabasal spine-like seta situated on a distinct lobe. Above
scaled. In the male genitalia, 1-3, usually 2, parabasal it, another prominent pointed seta, the internal seta, arises
setae are situated at the base of the gonocoxite with at from the inner side of the gonocoxite near the apex. The
least one of them arising from a more or less distinct claspettes are 3-lobed, the outer lobe with 2-3 spine-like
tubercle. Internal setae are present. The larvae of the pointed setae located close together, the middle lobe with
subgenus Anopheles, except those of An. plumbeus, are 2 flattened setae inwardly curved at the apex and the inner
characterized by the branched antennal seta (1-A) which lobe with 3 long, thin and pointed setae. The aedeagus
arises from the inner surface of the antennal shaft, and has 2-3 pairs of long narrow leaflets.
the inner clypeal setae (2-C) arising close together, their Larva: The antenna is slightly curved, dark and
bases often nearly touching. In An. plumbeus, seta 1-A spiculate throughout its inner surface. The antennal
is single and the pair of setae 2-C is more widely sepa- seta (1-A) is short with 5-6 branches arising close to
rated, the distance between them is nearly the same as the base of the antenna. The inner clypeal seta (2-C) is
the distance between 2-C and the outer clypeal setae long, with a few minute branchlets along the apical
(3-C). In all species of the subgenus, the leaflets of the half of the shaft. The outer clypeal seta (3-C) is about
palmate setae are lanceolate, not abruptly narrowed or half as long as the inner clypeals (2-C), with 2-3
shouldered, and have a more or less developed terminal
filament. The subgenus Anopheles is widely distributed
and occurs with appro­ximately 150 other species in all
zoogeographical regions. In Europe, 15 species of the
subgenus (including An. daciae) are recorded with a
distribution range throughout the whole region.

Anopheles (Anopheles) algeriensis Theobald 1903

Female: An. algeriensis differs from all other European

species of the subgenus Anopheles which have unspot-
ted wings by the absence of white or cream coloured
scales on the vertex, and by the scutum which is uni- Fig. 9.1 Hypopygium of An. algeriensis
166 9 Subfamily Anophelinae

branches near the apex. The postclypeal seta (4-C) is Medical importance: Although the vectorial capac-
single, rarely with 2 branches at the apex. One of the ity of An. algeriensis is high (e.g. it can easily be infected
most suitable features to separate larvae of An. alge- with P. falciparum in the laboratory), it is considered as
riensis from those of the closely resembling An. clavi- a secondary vector due to its exophily. An. algeriensis is
ger s.l. is the pattern of dark markings on the head. In rarely encountered in villages and an abundance of its
An. algeriensis, at least three transverse dark bands run population, even in the open field, is rarely high.
across the frontoclypeus (Fig. 8.10a). The most ante-
rior band is located behind the postclypeal setae, the
median band behind the frontal setae, and the posterior Anopheles Claviger Complex
band is situated close to the base of the frontoclypeus.
In An. claviger s.l. the frontoclypeus is dark spotted, It has been shown by Coluzzi (1960, 1962) and Coluzzi
but never banded. The palmate setae on abdominal et al. (1965) that An. claviger is a species complex
segments III–VII (1-III to 1-VII) each consist of 16–18 with at least two distinct members, An. claviger s.s.
leaflets with a weakly developed terminal filament and (Meigen) and An. petragnani Del Vecchio. These two
a conspicuous sawed margin. The sclerotized tergal sibling species are distributed in the western
plate on segment VIII is as broad as, or broader than Mediterranean subregion and differ distinctly in their
the distance between the palmate setae on segment VII larval and pupal morphology and larval and adult
(1-VII). The saddle seta (1-X) arises well within the behaviour. The question remains unsolved if other
margin of the saddle. described forms, e.g. missiroli Del Vecchio from Italy
Biology: The larvae are found in natural or artificial, and pollutus Torres Canamares from Spain, so far
well shaded, and more or less fresh, water bodies, such treated as synonyms of An. claviger, are also distinct
as ditches, canals or flooded pools with a rich over- species or varieties of the nominative form.
growth of vegetation (Phragmites sp.). They often
occur in shaded permanent pools among thick sedge or
in swamps and marshes. Owing to their tolerance of Anopheles (Anopheles) claviger s.s. (Meigen 1804)
slight salinity, they are occasionally found in high num-
bers in brackish water. They are associated with larvae Female: An. claviger s.s. is distinguished from An.
of An. maculipennis s.l. and Ur. unguiculata, but rarely marteri by its entirely dark palps without pale scales at
with An. claviger s.l., Cx. hortensis or Cx. theileri. In the tip and from the similar An. plumbeus by its decid-
central Europe, adults of An. algeriensis first occur in edly larger size and its general brownish colouration.
early summer and the species usually hibernates in the The pleurites and lateral parts of the scutum are fawn
larval stage, but in its southern range in northern Africa, brown or light brown, whereas An. plumbeus is a small
both adults and larvae can be found during the winter mosquito with dark brown or bluish pleurites with the
months. In this area the larvae can be found in clear, lateral parts of the scutum forming a distinct contrast
cool, mountain streams or in wells and cisterns (Senevet to the pale scales of the median scutal area. In An.
and Andarelli 1956). An. algeriensis is considered to be claviger s.s. the median pale stripe is always visible,
an exophilic mosquito; the adults rest outside in dense but it is not so distinctly contrasted. In old and dried-
grassy vegetation and readily attack their hosts, humans up specimens with an indistinct colouration, the differ-
and animal, in the open preferably at dusk and dawn. ent length of the palpomeres may be of more help in
They rarely enter houses or stables. the separation of the two species. In An claviger s.s.
Distribution: An. algeriensis is widely distributed the last segment of the palps is less than half as long
throughout the Mediterranean region and northern as the penultimate segment, whereas in An. plumbeus
Africa. In central Europe, it is recorded in England, it exceeds half the length of the penultimate segment.
Germany, northern France, Hungary and Bulgaria. In An. claviger s.s. has a uniformly dark brown proboscis
the eastern part of Europe there is one record from the and palps. The antennae are brown, the vertex has a
west coast of Estonia (Gutsevich et al. 1974). The east- tuft of whitish and cream coloured scales and the setae
ward extension of An. algeriensis includes the coastal are anteriorly directed. The occiput has narrow pale
plain area of Turkey to the northern slopes of the scales. The integument of the scutum is brown, with
Caucasus and through Middle Asia. narrow to moderately broad pale scales forming the
9.1 Genus Anopheles Meigen 167

median stripe, which is broad and covers more than (Fig. 8.11b). The frontal setae (5-C to 7-C) are strongly
half of the scutum. The anteacrostichal patch of pale branched. Dark markings on the frontoclypeus are
scales is faintly developed (Fig. 6.12b). The scutellum restricted to spots on the posterior part of it, and not
is brown, darker in the middle with dark setae on its banded as in An. algeriensis. The palmate setae on the
posterior margin. The pleurites of the thorax are brown, abdominal segment II (1-II) have 10–15 leaflets. The
and the legs are brown or dark brown with a few pale palmate setae on abdominal segments III–VII (1-III to
scales at the articulations. The scales on the wing veins 1-VII) have lanceolate leaflets with an elongated apex
are dark, evenly distributed and do not form dark spots. but without a long filament. The antepalmate setae on
The abdomen is brown, with indistinct pale apical segments IV and V (2-IV and 2-V) have 4-5 branches;
bands and long, pale brown setae. on the rare occasions when they have 3 branches, all
Male (Fig. 9.2): The gonocoxite has 3 parabasal branches are of the same length. The sclerotized, tergal
setae: the inner one, a single seta tapering and arising plate on abdominal segment VIII is not as broad as that
on a distinct lobe, the two outer setae located close of the palmate setae on segment VII (1-VII). The sad-
together and apically branched. The internal seta is dle seta (1-X) arises just outside the margin of the
inserted on the inner side of the gonocoxite near the saddle.
apex, and the gonostylus is relatively thick with a short Biology: The larvae are found in a wide variety of
apical spine. The claspettes are made up of three habitats, but show a preference for clean water and for
distinct lobes, the outer lobe carries 2-3 lanceolate bodies of water with a more or less permanent charac-
blades, the middle one 2, and the inner one, 2-3 pointed ter. They are found in cool water in the shade, e.g.
spines. The aedeagus has 2-3 pairs of leaflets at its weedy pools sheltered by trees or among growth
apex. of reeds at the edges of ponds or lakes, where they
Larva: The antenna is about half as long as the are often associated with the larvae of An. atroparvus,
head with small spicules on the inner surface, decreas- Cs. annulata, Cx. impudicus and Cx. theileri. The lar-
ing in size towards the tip, and rarely absent from the vae are also common in ditches overgrown with weed,
distal third. The antennal seta (1-A) is short, with 4-7 in the Mediterranean region they are frequently found
branches, and located near the base of the antenna. The in wells and water containers. In mountainous areas
inner clypeal seta (2-C) is long, nearly as long as the the larvae breed among the aquatic vegetation on the
antenna; the setae are situated close together and are margins of small well shaded mountain streams. In the
single or sometimes with 2-3 branches at the apex. The northern range of its distribution, the larvae are often
outer clypeal seta (3-C) is rarely single, more often found together with Cs. morsitans and Oc. punctor.
with 2-3 apical branches, and the postclypeal seta The larvae hibernate, and the adults appear in early
(4-C) is short and thin, with 2-4, rarely 5 branches spring. They can be found during the summer months
until late autumn. In southern England, maximum bit-
ing activity of adult females was observed in May and
September showing that An. claviger is bivoltine in
this area (Service 1973b). The females deposit their
eggs not directly on the water surface, like other
Anopheles species, but above the water level into the
wet soil. The females die off before the end of the year.
Hibernation takes place in the 3rd or 4th larval stage in
water bodies that do not entirely freeze. In the southern
range of its distribution, the larval development is not
interrupted in winter, but is merely very slow at that
time. The larvae are very sensitive to disturbance
and promptly descend to the bottom of the breeding
sites after sensing the slightest movement of the water.
An. claviger s.s. is a more exophilic species; the adult
females do not readily enter houses or stables, but bite
Fig. 9.2 Hypopygium of An. claviger in the open, outside villages (exophagy). An. claviger
168 9 Subfamily Anophelinae

s.s. is a zoophillic species, and its preferred hosts are V (2-IV and 2-V) have 2 or 3 branches, and if
large domestic animals. Sampling carried out in 3-branched, the median one is shorter than the outer
human dwellings and stables revealed that more branches. In An. claviger s.s., the postclypeal setae
females of An. claviger s.s. fed on humans (3.3%) than (4-C) are short and thin, with 2-4, rarely 5 branches.
was the case for An. maculipennis s.l. (2.3%) (Tovornik The palmate setae on abdominal segment II (1-II) have
1974). Autogenous populations are reported from Italy 10–15 leaflets. The antepalmate setae on segments IV
(Rioux et al. 1975). and V (2-IV and 2-V) have 4-5 branches, rarely
Distribution: The species is widely distributed in 3-branched and if so, they are all of the same length.
the Palaearctic region. Its northern range runs through Pupa: A reliable morphological character, which
central Scandinavia, Estonia and the St. Petersburg facilitates the separation of the two species, is found in
area. It is found throughout nearly all of Europe from the length of seta 9 on abdominal segments IV and V
central Sweden and Norway to northern Africa and in (9-IV and 9-V). In all anophelines, seta 9 on abdomi-
the Caucasus and Crimea area. In the mountains of nal segments III–VII is developed into a short, stout,
Central Asia, it is found at an altitude of up to 2,000 m dark spine arising from the extreme posterior corner
and its range stretches to Iraq, Iran and Pakistan. In the of the segment. According to Coluzzi (1960), in An.
western Mediterranean area it is sympatric with An. claviger s.s. the spine of abdominal segment IV (9-IV)
petragnani, but not as common (Ramos et al. 1978). is less than half as long as the spine of abdominal
Medical importance: An. claviger s.s. is a poten- segment V (9-V), whereas 9-IV is more than half as
tial vector of malaria. Although its epidemiological long as 9-V in An. petragnani.
importance is not significant due to its small popula- Biology: The larvae of An. petragnani are able to
tions, it is well known as a principal malaria vector in the tolerate slightly higher water temperatures than An.
eastern Mediterranean region (Postiglione et al. 1973) claviger s.s. In Sardinia they are found from February
Note on systematics: An. claviger was first through July and from October to December in fresh-
described by Meigen in 1804 as Culex bifurcatus. After water rockholes, ditches, drainage canals, and the
the generic change, the name An. bifurcatus was used edges of streams and rivers preferably in shady situa-
for a long time, but this usage was inadmissible because tions (Marchi and Munstermann 1987). Pires et al.
bifurcatus was a name given earlier by Linnaeus for (1982) reported larvae breeding in southern Portugal
the males of Cx. pipiens. along shaded mountain streams with submerged green
algae at an altitude of 600 m. The water surface was
covered with Lemna sp. and the larvae were associated
Anopheles (Anopheles) petragnani with those of An. atroparvus and Cx. impudicus.
Del Vecchio 1939 Ribeiro et al. (1989) found An. petragnani in Portugal
from about sea level up to an altitude of 1,750 m, and
Female: An. petragnani as a member of the Anopheles in central Portugal, 87% of its recorded findings are
Claviger Complex can only be separated from the above 500 m. They also reported a marked host prefer-
nominative form by larval and pupal characters. Coluzzi ence of the adult females for livestock such as pigs and
(1960) reported that the adult females have a darker cows.
colouration than An. claviger s.s., but this character Distribution: An. petragnani seems to be
is of less value for taxonomic separation and the restricted to the western Mediterranean subregion,
females of the two species are particularly difficult to where it is largely sympatric with An. claviger s.s. It
distinguish. is the prevalent species of the Anopheles Claviger
Male: In the male hypopygium, as in the adult Complex in southern Italy, Sardinia and Corsica, but
females, no distinct differences can be found to distin- has not been recorded from east of the Italian peninsula.
guish An. petragnani from An. claviger s.s. Its whole range of distribution has not yet been fully
Larva: In An. petragnani, the postclypeal setae clarified.
(4-C) are usually single, rarely bifid. The palmate setae Medical importance: An. petragnani seems to be a
of abdominal segment II (1-II) usually have more than strongly zoophilic species, which often appears in
15 leaflets with slightly elongated apices (Fig. 8.12b). small numbers only. It apparently plays no role in
The antepalmate setae on abdominal segments IV and malaria transmission.
9.1 Genus Anopheles Meigen 169

Anopheles (Anopheles) hyrcanus (Pallas 1771)

Female: The proboscis is dark brown. The palps are

nearly as long as the proboscis, and dark brown with a
pale apex and 3 narrow pale rings at the joints of pal-
pomeres II–III, III–IV and IV–V. The clypeus is dark
brown with a large tuft of dark scales positioned later-
ally on each side. The antennae are dark brown, and
the basal 5-7 flagellomeres have a few white scales.
The vertex has a tuft of anteriorly directed white nar-
row scales between the eyes. There are white erect
scales on the dorsal surface of the occiput and blackish
Fig. 9.3 Hypopygium of An. hyrcanus
brown upright scales at its sides. The scutum is brown
with a stripe of greyish narrow scales in the middle.
Often the median stripe is divided by dark longitudinal
stripes into 2 or 4 narrow greyish stripes. In addition, a exceeds that of the tip of the gonocoxite. The outer
few pale scales are present on the anterior margin of lobe of the claspettes has setae fused into a flattened
the scutum. The postnotum is light brown, and the spatula like process, and the inner lobe has 2 single
pleurites are brown. The legs are brown, but lighter on pointed setae. The aedeagus has several pairs of leaf-
the ventral surfaces of the femora and the inner sur- lets at the apex. These leaflets are delicate, and about
faces of the tibiae, and the bases of the front femora are 1/3 the length of the aedeagus.
distinctly enlarged (Fig. 6.13b). The tarsi are dark Larva: The larvae of An. hyrcanus resemble those
brown, and the fore and mid tarsi have white rings at of the Anopheles Maculipennis Complex, but can easily
the apices of tarsomeres I–III. Tarsomere IV of the be distinguished by the characteristics given in the
hind tarsi is also pale at the apex (Fig. 6.14a), and keys. The head is longer than the width. The antennae
entirely pale in var. pseudopictus (Fig. 6.14b). are straight with small spicules located on the inner
Sometimes the white ring extends to parts of the hind aspect and a conspicuous antennal seta (1-A), which is
tarsomere V. The wing veins are covered with dark and multiple-branched (7-8 branches) and at least half as
pale scales, forming contrasting dark and pale spots. long as the antenna. It arises about midway on the
The dark costal margin of the wing is interrupted by 2 antennal shaft or slightly below it. The inner clypeal
pale areas in the apical half; the more proximal spot setae (2-C) are situated close together, with short api-
includes C and R1, and the spot near the apex extends cal branches (Fig. 8.13a). The outer clypeal seta (3-C)
from C to R2 (Fig. 6.13a). White scales particularly is multiple-branched, and dendriform. The frontal setae
dominate on Cu and A, and sometimes these veins are (5-C to 7-C) are long and plumose. The palmate setae
almost entirely white scaled. The fringe scales of the on abdominal segments I and II are rudimentary, but
wing are white at the apex, but otherwise brownish. It well developed on segments III–VII, with 17–24 leaflets
has to be mentioned that An. hyrcanus exhibits a con- ending in indistinct terminal filaments. The sclerotized
siderable amount of intra-specific variation in the wing tergal plates on the abdominal segments are compara-
markings. The dark to white area ratio may vary as tively broader than the length.
well as the discreteness and vividness of the spotting. Biology: The larvae of An. hyrcanus can be usually
The abdomen is dark with long, dense, brown or golden found in reasonably clean, stagnant, sun-exposed water
setae, and sternum VII has a tuft of dark greyish scales bodies, rich in aquatic vegetation. They are found espe-
at its apical half. cially in rice fields and associated irrigation systems, in
Male: Tergum IX has long lateral lobes which are swamps and similar locations in the open, e.g. pools,
enlarged at their apices. The gonocoxite has 2 para- margins of lakes or ditches with grassy edges. Elsewhere,
basal setae, unequal in length, the outer seta being longer the larvae breed at the edges of slowly moving waters
than the inner, and neither is inserted in a sclerotized such as grassy streams and canals or road side ditches.
base (Fig. 9.3). The internal seta is inserted near the They exhibit a tolerance to a slight degree of salinity
middle of the gonocoxite, and its length slightly and can also be found in coastal and inland marshes.
170 9 Subfamily Anophelinae

In rice fields in northern Greece, the larvae are associ- described from different localities as variations or
ated with An. sacharovi and Cx. modestus. From the subspecies of the nominative form. Some of these
coastal plains of Turkey, Postiglione et al. (1973) forms from south-east Asia are now considered as dis-
reported the presence of larvae in association with those tinct species within the An. hyrcanus sibling species
of An. maculipennis s.l., An. superpictus and An. alge- group, e.g. An. sinensis Wiedemann, An. nigerrimus
riensis. At a temperature of about 20°C the larval devel- Giles, An. paeditaeniatus (Leicester) and others (Reid
opment of An. hyrcanus lasts 14–16 days (Senevet and 1953; Harrison 1972). The Palaearctic variations
Andarelli 1956). The adults occur in small numbers in include the form mesopotamiae from western Asia
late April and May but the size of the population with a lighter, diffused colour pattern of the wing
increases towards autumn. An. hyrcanus produces 2-4 caused by more pale scales intermixed on the wing
generations/year. The biting behaviour of the adult veins and a western Palaearctic form pseudopictus
females is predominantly exophilic (outdoors), but the with tarsomere IV of the hind legs entirely white, found
degree of exophily is known to differ between places. mainly in southern and southeastern Europe. Glick
Usually they rest outdoors in bushes and other dense (1992) treated An. pseudopictus as a distinct species
vegetation during the day time. They rarely enter houses, being clearly separated from An. hyrcanus by its
but are common in cattle sheds or shelters, from where sympatric distribution throughout Turkey, Iran and
they return into the open after blood feeding. Livestock, Afghanistan with apparently no evidence of hybrid-
or when these are not available as hosts, humans are ization. However, Gutsevich (1976) reported a wide
readily attacked in the open field at dusk or in the night. variation of An. hyrcanus in the extent of the pale
Occasionally, feeding is observed during the day time in ringing on the hind legs and found intermediate forms.
shaded situations. Autogenous populations have been Because Glick’s judgment was solely based on one
reported from Kirgisia (Rioux et al. 1975). character of female morphology and no investigations
Distribution: In Europe An. hyrcanus is widely on the morphology, of the male genitalia, the develop-
distributed throughout the northern Mediterranean ing stages or cross-mating experiments have been car-
countries, from Spain, southern France, Italy, and ried out since, the opinion not to treat the European
Greece to Turkey. In central Europe it is reported from form pseudopictus as a distinct species nor a subspe-
Hungary (Toth 2003), Slovakia (Halgos and Benkova cies of An. hyrcanus is favored here.
2004) and the Czech Republic (Votypka et al. 2008;
Sebesta et al. 2009). It is distributed in the Ukraine,
southern Russia, southern Kazakhstan, the Caucasus Anopheles Maculipennis Complex
and middle Asia. Together with closely related species
it is common in southeast Asia and its eastern distribu- The mosquitoes of the Anopheles Maculipennis
tion range includes China, Japan and Korea. Complex are the classical example of a “species
Medical importance: Because of its exophilic complex”, comprising various sibling species. Before
behaviour, An. hyrcanus has never been regarded as a 1925, it was reported that malaria was transmitted by
significant vector of malaria in the Mediterranean the malaria mosquito “An. maculipennis”. Further
region. With regard to the probability of changes in research on the distribution and ecology of this mos-
human behaviour (e.g. increased mobility of humans quito uncovered considerable irregularities. It was
or increase in the number of seasonal workers in the found that the distribution of malaria and the distribu-
rice and cotton fields), its role as a potential malaria tion of An. maculipennis were not closely correlated. In
vector should not be ignored. some areas where individuals of An. maculipennis were
Note on systematics: An. hyrcanus is one of the abundant, the incidence of malaria was low or absent.
most widespread and common species of the genus This situation was characterized as anophelism without
Anopheles, and certainly one of the most variable. It malaria (Bates 1940). Furthermore, differences in the
has an enormous distribution range throughout the biology and behaviour of various populations were dis-
Palaearctic from the Atlantic in the west to the Pacific covered. In some regions the larvae were restricted to
in the East and the Oriental region in the south. Due to fresh water, in others, to brackish water; the adult
its variability, a number of different forms have been females preferred to feed on humans in some areas and
9.1 Genus Anopheles Meigen 171

elsewhere they mainly fed on livestock. Exceptional tioned advanced techniques of identification, e.g. An.
differences in the swarming and mating behaviour daciae (Nicolescu et al. 2004).
(stenogamy, eurygamy) between certain populations Once the existence of a complex of sibling species
were also observed. The first evidence for the existence was established, some morphological differences
of a complex of sibling species was brought up by between adults and larvae were also found. The
Falleroni (1926), who described distinct morphological females may be separated by the form and shape of
differences of the chorion pattern of the eggs in popula- scales on certain wing veins, the males differ in the
tions with a different biology. Unfortunately, Falleroni’s form and length of the spines on the outer claspette
observations lay dormant for five years and were not lobe and larvae may be distinguished by the overall
rediscovered until 1931. Research of Martini et al. number of branches of the four antepalmate setae on
(1931), Van Thiel (1933) and Hackett and Missiroli abdominal segments IV and V (2-IV and 2-V, four
(1935) gave more evidence of the presence of a com- setae together). Unfortunately, there exists an intra-
plex and by the end of the 1930s, most of the present specific variation of the characters and overlapping
species of the complex were identified (Bates 1940). between the species is not uncommon. Therefore, it is
Studies using cross-breeding experiments, cytotaxo- necessary to investigate a series of specimens with
nomic methods or enzyme electrophoresis confirmed statistical analysis of the results, which is not appli-
the existence of the different species within the com- cable for individual identification. Thus the morpho-
plex (Stegnii and Kabanova 1976; Bullini and Coluzzi logical identification is still based largely on characters
1978; Suzzoni-Blatger et al. 1990). The complex com- of the egg (markings of the dorsal exochorion, pres-
prises of at least a dozen reproductively isolated but ence of floats and their size, position and texture).
morphologically similar species in the northern hemi- Engorged females can be directly sampled into vials,
sphere (White 1978) and it can be expected that more e.g. from animal shelters, and allowed to lay their
members will be found with the use of the above men- eggs for individual identification.

Identification key for European species of the Anopheles Maculipennis Complex based on characters of the eggs
(after White 1978):
1 Egg without floats (but rudimentary floats may develop at low temperatures), egg surface uniformly pale
(frosty-white) from pole to pole (Fig. 9.4a)................................................................................... sacharovi
Egg with fully developed floats, egg surface dark, barred or mottled........................................................... 2
2 (1) Intercostal membranes of floats (surface of the air cells) smooth................................................................. 3
Intercostal membranes of floats rough (finely corrugated)........................................................................... 5
3 (2) Surface of egg entirely dark (Fig. 9.4b)..........................................................................................melanoon
Surface of egg otherwise, barred or mottled................................................................................................. 4
4 (3) Surface of egg softly patterned with wedge-shaped black marks on a pale background, pale almost at the
tip (Fig. 9.4c) . .............................................................................................................................. atroparvus
Surface of egg with pattern of 2 transverse dark bars near the ends of floats, poles dark and remainder of
the surface irregularly mottled (Fig. 9.4d) ................................................................................... subalpinus
5 (2) Surface of egg richly patterned with wedge-shaped dark marks on frosted pale backround, tip of poles dark
and narrow (Fig. 9.4e) ................................................................................................................ labranchiae
Surface of egg marked with 2 transverse dark bars near the end of the floats, with or without other pattern
(mottled background).................................................................................................................................... 6
6 (5) Transverse dark bars on surface forming part of diffuse mottled pattern (Fig. 9.4f).........................messeae
Transverse dark bars on upper surface sharply contrasted with unmottled pale background colour............ 7
7 (6) Tips of eggs less acutely pointed, chorion of upper egg surface relatively rough, width of egg between
floats about 17% of egg length (Fig. 9.4g)......................................................................... maculipennis s.s.
Tips of eggs more acutely pointed, chorion of upper egg surface relatively smooth, width of egg between
floats about 12% of egg length (Fig. 9.4h)................................................................................ beklemishevi
172 9 Subfamily Anophelinae

Fig. 9.4 Eggs of Anopheles Maculipennis Complex:

(a) sacharovi, (b) melanoon, (c) atroparvus, (d) subalpinus, (e) labranchiae, (f) messeae, (g) maculipennis s.s., (h) beklemishevi

Morphological characters of adults and larvae blackish brown with long, golden brown, narrow
shared between the members of the complex: scales.
Female: Dark or medium brown in colour, although Male (Fig. 9.5): The gonocoxite has 2 single
there is a wide variation in colouration and size. parabasal setae positioned on small, but distinct
Individuals of southern origin are usually lighter and tubercles, and the setae are unequal in length, with
smaller. The characteristic features, which differ from the outer one being longer. The internal seta is
all other European Anopheles species, are the wings inserted near the middle of the gonocoxite. The
with an aggregation of dark scales forming several gonostylus is well developed, and is longer than the
distinct spots (Fig. 6.8a). The proboscis is dark brown, gonocoxite, with a short apical spine. The claspette
and the palps are nearly as long as the proboscis, and lobes are not well defined, and have spine-like setae
of the same colour. The antennae are brown coloured. of variable length and shape situated close together
The vertex has a tuft of long, whitish, anteriorly but not fused. The aedeagus is long and narrow with
directed narrow scales and setae. The occiput has leaflets at the apex.
erect dark brown scales. The scutum has a broad Larva: Very variable in pigmentation and size
greyish median stripe tapering anteriorly and usually according to their different habitats. Larvae from the
2-3 indistinct brownish stripes on its anterior half. northern parts of Europe are usually larger with a
The lateral parts of the scutum are brown anteriorly darker head capsule. The head is longer than the width,
and blackish brown posteriorly (for different coloura- and the antenna is nearly straight, sparsely spiculate,
tion patterns of An. sacharovi see under species and about 2/3 as long as the head. The antennal seta
description). The antechrostichal patch is made of (1-A) is small, with 4-6 branches arising at the basal
pale, long and thin scales. The scutellum is brown
with golden narrow scales, the postnotum is pale
brown, and the pleurites are dark brown. The femora
are dark brown on the dorsal side and pale brown on
the ventral side, the tibiae are brown but slightly paler
at their apices, and the tarsi are dark brown. The
wings have dark scales unevenly distributed forming
several dark spots close to the cross veins, base of Rs
and furcations of R2+3 and M. The furcations of R2+3
and M are situated at about the same distance from
the wing base. The fringe of the wing has a patch of
pale scales at the apex of the wing (Fig. 6.9b). An.
sacharovi has dark spots on the wing veins which are
more indistinct and the fringe of the wing is uni-
formly dark (Fig. 6.9a). The abdomen is brown or Fig. 9.5 Hypopygium of An. maculipennis s.l
9.1 Genus Anopheles Meigen 173

1/3 to 1/4 of the antennal shaft (Fig. 8.13b). The inner and mate almost entirely indoors. Flight ranges of An.
clypeal setae (2-C) are situated close together, with atroparvus females of at least 3 km have been reported
long apical branches. The outer clypeal seta (3-C) is (Cambournac and Hill 1938).
dendriform (Fig. 8.9b). The frontal setae (5-C to 7-C) Distribution: It is a largely a littoral species occur-
are long and plumose. The palmate setae on abdominal ring from southeastern Sweden to Portugal along the coasts
segments I and II are rudimentary, but well developed of the Atlantic, Baltic, and Mediterranean Sea. In
on segments III–VII, with 16–24 leaflets which are southern and southeastern Europe it has a patchy dis-
slightly wider in the middle. The terminal filament is tribution, e.g. from northern Italy and inland areas of
nearly 1/3 as long as the leaflet. central Italy through southwestern parts of Russia
and the coastal area of the Black Sea. In Serbia and
Macedonia it is widespread in the lowlands, but con-
Anopheles (Anopheles) atroparvus Van Thiel 1927 spicuously dominant only in areas with saline/alka-
line soils in the Pannonean Plain (Adamovic 1980).
Biology: The larvae can be found in a variety of stagnant, In Portugal it is the most common, most abundant,
semi-permanent or permanent, clean breeding sites, both and most widely distributed Anopheles species
in saline and fresh water, but they show a slight prefer- throughout the country (Ribeiro et al. 1988). An.
ence for brackish water. They may occur in canals, atroparvus was more common in the past, but has a
ditches, marshes in coastal areas, river margins, pools in diminished distribution today. In the Netherlands,
river beds, rice fields, and are sometimes even found industrial pollution is considered to be one reason for
in septic tanks. The water bodies are usually exposed the decrease of the species abundance (Jetten and
to the sun and carry a considerable amount of filamen- Takken 1994).
tous green algae and other floating and submerged
vegetation. In their southern distribution range, the
larvae are often found together with those of Cx. theileri, Anopheles (Anopheles) beklemishevi
Cx. impudicus, and Cx. p. pipiens (Ramos et al. 1978). Stegnii and Kabanova 1976
An. atroparvus hibernates as the adult female and usually
shows incomplete diapause. After seeking shelter in sta- Biology: The larvae may occur in breeding sites quite
bles or dwellings in autumn, the females remain active typical for An. messeae. Stegnii and Kabanova (1976)
during winter time and may irregularly take blood- reported a finding of larvae in a pond that was heavily
meals without subsequent oviposition. This habit mainly polluted with organic material and aquatic vegetation
contributed to the indoor transmission of winter malaria was absent. The larvae could be found only along the
in Great Britain, Netherlands, and other parts of Europe edges of the pond. They seem to be more tolerant of the
at the beginning of the twentieth century. The problem cold than larvae of An. messeae, and thus show an adap-
disappeared in the late 1940s, due to improved socio- tion to the continental climate. So far little is known
economic conditions. The duration of the diapause about the biology and the biting behaviour of the females.
depends on the length of day and also on temperature Many characteristics of this species seem to be similar to
and thus varies with the latitude of the distribution of An. those of An. maculipennis s.s., e.g. its zoophily (prefer-
atroparvus. It may last from September-April in north- ence for feeding on animals). The adults usually rest
ern Europe or from November-February in southern indoors. In northern Sweden, Jaenson et al. (1986a) col-
Europe. The females are mainly zoophilic and prefer dif- lected females from livestock shelters. An. beklemi-
ferent domestic animals according to their availability in shevi was found resting in cattle sheds, horse stables, and
different areas, but also readily feed on humans. They pigsties without showing a preference for a particular spe-
usually rest indoors, predominantly in stables and man- cies of domestic animal. It is an eurygamous species,
made shelters. Although swarming of the males before e.g. swarming occurs before mating and the species under-
mating has been observed on several occasions, it is con- goes complete winter diapause of a duration that is
sidered to be a vestigial characteristic, playing only a inversely correlated with the photoperiod (White 1978).
minor part in the actual mating behaviour of the sexes Distribution: An. beklemishevi is endemic to the
(Cambournac and Hill 1940). Usually the adults of An. cooler highlands and northern latitudes of Russia and
atroparvus do not swarm before mating (stenogamy) the Baltics (White 1978). It can be found in Siberia,
174 9 Subfamily Anophelinae

northern Sweden and Finland (Korvenkontio et al. coast. In northern Africa, the species occurs in
1979; Jaenson et al. 1986a) and is also recorded in sev- Morocco, Algeria and Tunisia.
eral localities in southern Finland (Utrio 1979).
Note on systematics: An. beklemishevi was the first
mosquito species ever to be named and described pri- Anopheles (Anopheles) maculipennis s.s.
marily from cytogenetic evidence, rather than from a Meigen 1818
morphological description (White 1978).
Biology: The larvae mainly occur in cold clear waters
of upland areas, but they can also be found in plains
and coastal zones (Hackett and Missiroli 1935). Typical
Anopheles (Anopheles) labranchiae Falleroni 1926 breeding sites are sheltered areas in running streams,
river edges, rice fields, or artificial pools. In mountainous
Biology: Larvae can be found in sunlit, stagnant fresh regions in central Europe, the species can be found at
and brackish water containing horizontal vegetation in altitudes of > 1,000 m, and occur there as the only
coastal areas in Europe and in some inland regions member of the complex. Altitudes of 2,190 m-2,300 m
(Jetten and Takken 1994). They may occur in coastal are reported from Bulgaria and Turkey (Bozkov 1966;
marshes, sheltered edges of flowing streams, rice Postiglione et al. 1973). An. maculipennis s.s. shows a
fields, grassy pools and a number of similar breeding better adaptation to breeding in small water bodies
sites. In Europe, larvae of An. labranchiae are usually without vegetation and artificial collections of water
associated with brackish water, where the salinity of with a wide fluctuation of the daily temperature than
the breeding sites can reach up to 10 g/l (Weyer 1939). An. messeae (Mohrig 1969). Therefore, this species
In Sardinia, where other members of the complex are seems to be better suited for survival in cultivated land
virtually absent, the larvae are almost entirely limited that was widely created in Europe in the past decades
to fresh water breeding sites. On the island they can be through water management campaigns and the use of
found in ponds, ground-flooded pools, streams, ditches, extensive agriculture techniques. The larvae can fre-
drainages or canals (Aitken 1954a; Marchi and quently be found in waters with a high content of
Munstermann 1987). An. labranchiae larvae are better organic matter together with those of Cx. p. pipiens.
adapted to warmer waters than those of An. atroparvus. Hibernation of adult females is complete, but it can be
Hibernation takes place in the adult female stage in of relatively short duration in warmer climates (Senevet
dark sheltered situations, e.g. in stables and/or other and Andarelli 1956). The winter months are usually
natural cavities. Diapause may be complete or incom- passed in abandoned buildings without a potential
plete, e.g. occasional blood-feeding is possible during host. The adults normally have little contact with
the winter months. The females principally feed on humans, the females are considered to be strongly zoo-
humans and they persistently try to enter bedrooms at philic, feeding mainly on cattle (Weyer 1939), but also
night (Hackett and Missiroli 1935), but domestic on pigs and chicken (Tovornik 1980). Nonetheless, in
animals may also serve as hosts. An. labranchiae is case of a shortage of livestock, An. maculipennis s.s.
predominantly an endophilic species, indoor resting may feed on humans as well, both outdoors and indoors
sites include human dwellings, stables, animal shelters, (Barber and Rice 1935). It is usually an endophilic
etc. Occasionally they may be found resting outdoors species; the daytime resting sites are stables and dwell-
in various natural shelters, such as tree cavities. ings. The adults are eurygamous, usually swarming
Swarming before mating was reported by Horsfall before mating.
(1955), but in the laboratory adults were found to mate Distribution: An. maculipennis s.s. is widely dis-
in small cages of 50 × 50 × 100 cm (Hackett and Bates tributed throughout Europe. With the exception of the
1938). The flight range of the species is considered to southern parts of the Iberian Peninsula it is recorded in
be 2–5 km (Senevet and Andarelli 1956). nearly every European country. The range extends
Distribution: An. labranchiae has a restricted dis- eastwards to southwest Asia and the Persian Gulf. It is
tribution in southern and southeastern Europe. It has considered to be more of a continental species with
been reported in the south east of Spain, Corsica, demands for humidity considerably lower than those
coastal areas of Italy, Sardinia, Sicily, and the Dalmatian of An. messae and An. atroparvus.
9.1 Genus Anopheles Meigen 175

Anopheles (Anopheles) melanoon Hackett 1934 rare or almost completely absent along the coastlines
and in mountainous regions. Hibernation takes place
Biology: Larvae of An. melanoon are typically found in the adult female stage, the diapause is complete.
in sunlit stagnant water bodies with a large surface The winter months are usually passed in abandoned
area and some vegetation (Jetten and Takken 1994). buildings. The females are essentially zoophilic spe-
They may occur in marshes, edges of rivers and cies feeding almost exclusively on domestic animals;
lakes, ponds, and ground pools. In Sardinia, larvae thus contact with humans is largely suppressed in an
can be found in fresh-water ground pools, streams agricultural area with livestock (Jetten and Takken
and water collections with a sunny exposure in the 1994). Blood meals are taken from humans only
springtime and shadier situations during the sum- when the density of An. messeae is very high and
mer months (Aitken 1954a). Elsewhere, the species there is a shortage of livestock, but they may also
is reported to breed in rice fields (Hackett and attack humans in houses (Barber and Rice 1935;
Missiroli 1935). Hibernation takes place in the adult Dahl 1977). Artemiev (1980) described the species
female stage with complete diapause. The winter as endophilic as it was found resting during the day-
quarters are not well known, but may be the same as time in stables, barns, and cellars as well as in human
in other members of the complex, e.g. An maculi- buildings. The adults are eurygamous.
pennis s.s., An. messeae and An. subalpinus. An. Distribution: An. messeae is the most widespread
melanoon females reveal a zoophilic preference, member of the complex. Its range stretches in the
they mainly feed on cattle and have only occasion- northern Palaearctic region from the Atlantic coast in
ally been recorded as feeding on humans, both the west, through Scandinavia, across northern and
indoors and outdoors. Cattle stables are reported as central Europe and Asia as far as into China. The
daytime resting shelters (Ribeiro et al. 1980), but species is virtually absent in southern Europe, it cannot
others described the species as semi-exophilic be found on the Iberian peninsula, southern Italy, and
(Artemiev 1980). The adults are eurygamous. An. in the eastern Mediterranean region. An. messeae is
melanoon is a rare species with a limited distribu- regarded as being comparatively more susceptible to
tion range. So far, it has never been found in the high temperature and low humidity than An. atroparvus
same numbers as other members of the complex. and this behaviour might limit the southern distribution
Distribution: An. melanoon seems to be confined of the species.
to southwestern and southern Europe. It has been found
in Portugal and Spain (one record each), Corsica,
Sardinia, and Italy. More eastern records probably Anopheles (Anopheles) sacharovi Favre 1903
refer to An. subalpinus.
Adults of this species are most readily distinguished
from the other members of the complex by the lighter
Anopheles (Anopheles) messeae Falleroni 1926 colouration of the mesonotum and some wing charac-
ters. The pale median stripe on the scutum, character-
Biology: The larvae are typically found in cool, istic of the other members of the complex is absent.
fresh, stagnant water bodies with an abundant growth The lateral parts of the scutum are yellowish brown,
of submerged vegetation. They occur at the edges of more or less the same as in the middle part. The scales
rivers and lakes, in swamps, flood plains, ponds and of the wing fringe are uniformly dark, without a pale
ditches. In central Europe, the larvae are restricted to patch at the wing apex (Fig. 6.9a). The dark spots on
inland areas and fresh water habitats and avoid the wings, particularly in males, are less conspicuous
breeding sites with a high content of organic matter. than in the other members of the complex and barely
An. messeae prefers larger water bodies which are distinguishable in old worn out specimens. The eggs of
available mainly in lowlands with poorly regulated An. sacharovi are unique in the lack of the air floats
ground water level (Mohrig 1969). It is the predomi- (Fig. 9.4a), but in the south of its distribution range,
nant species of the Anopheles Maculipennis Complex where development continues throughout the year,
in inundation areas and flood plains of larger rivers, eggs deposited in winter may have rudimentary floats.
e.g. the Danube, Sava, Rhone or Rhine rivers. It is Usually the larvae of An. sacharovi are smaller than
176 9 Subfamily Anophelinae

the larvae of the other members of the complex, and East through middle Asia, Iran, and Afghanistan to
the outer clypeal setae are relatively longer. China. In its continental distribution range, An. sacha-
Biology: Larvae can be generally found in open, sun rovi is a characteristic species for areas with a dry and
exposed shallow water bodies with abundant surface hot climate.
vegetation, both in fresh and saline waters. They are
more tolerant to salinity than other members of the
complex (e.g. An. maculipennis s.s.), and usually occur  nopheles (Anopheles) subalpinus
A
in coastal swamps and marshes, lagoons and nearby Hackett and Lewis 1935
streams, irrigation drains, and roadside ditches, rice
fields, grassy ponds, pools, or seepages. In rice fields, Biology: Larvae can be found in various types of sun-
the larvae are often found together with those of Cx. lit, stagnant water bodies where aquatic vegetation is
modestus. The larvae are not very mobile and rarely present. They occur in swamps, edges of lakes, flooded
leave the water surface, but if they do, they return after rice fields, or ponds and avoid shady places and small
a short time (Gutsevich and Dubitzky 1987). An. sacha- water collections. Regular breeding sites can be found
rovi is the most thermophylic species of the Anopheles up to an altitude of about 1200 m (Postiglione et al.
Maculipennis Complex, and water temperatures of the 1973). Hibernation of adult females is complete, and
breeding sites up to 39°C during daytime are not caves and abandoned buildings are chosen as winter
uncommon. Hibernation takes place in the adult quarters (Senevet and Andarelli 1956). An. subalpinus
female stage, and the individuals preferably seek sta- is regarded as being a strongly zoophilic species, which
bles and other animal shelters for overwintering. When rarely feeds on humans. Females are endophilic and
the temperatures are suitable, they may take blood can be found during the day in large numbers in stables
meals occasionally during winter. Hibernation starts and barns, and very rarely in human dwellings or build-
earlier and lasts longer than in other members of the ings; the adults are eurygamous.
complex (Martini 1931). In spring, adults are not very Distribution: An. subalpinus is a southern European
abundant, the maximum population is usually reached mosquito with a range from the Iberian Peninsula,
between July and August. The females predomi- through the northern Mediterranean countries to the
nantly feed on humans but also on cattle when avail- lowlands around the Caspian Sea.
able. Even during the daytime they may be persistent Note on systematics: According to genetic studies
biters in sheltered situations (Postiglione et al. 1973). and widespread surveys, An. subalpinus was formerly
In some places they become numerous and attack humans regarded as a subspecies of An. melanoon. It should
in large numbers (Gutsevich and Dubitzky 1987). An. merely represent an alternative egg phenotype of An.
sacharovi is usually an endophilic species; adults are melanoon. The two forms of eggs apparently are inter-
frequently found in stables and human dwellings dur- grading conspecific varieties that occur in pure popu-
ing the day, and leave their daytime shelters during the lations in limited geographical areas (Bates 1940;
hours of darkness. Occasionally they can also be found White 1978). Based on material from Portugal, An.
resting outdoors: recorded outdoor shelters include hol- melanoon and An. subalpinus were treated as two dis-
lows and cavities under bridges and earth banks, hol- tinct species on account of the differences of their
low trees or rock cavities (Postiglione et al. 1973). eggs and the apparent area of sympatry of both forms
Saliternik (1957) caught marked mosquitoes at a dis- in southwestern Europe (Ribeiro et al. 1980; Ramos
tance of 3.5 km from the release point. The flight range et al. 1982). Furthermore, evidence was provided of
of An. sacharovi may exceed this distance, if the blood reproductive isolation between sympatric populations
source is far from the breeding places. of the two species (Cianchi et al. 1987). Subsequently,
Distribution: In southern Europe, An. sacharovi is regarding An. subalpinus as a distinct species of the
mainly a coastal species and distributed in the eastern Anopheles Maculipennis Complex was accepted by
Mediterranean sub-region. It can be found in Corsica, others (Ward 1992).
Sardinia, Sicily, in coastal areas of Italy, Greece, for- Medical importance of the species of the
mer Yugoslavia and Albania, south of the Balkan pen- Anopheles Maculipennis Complex: The anthropo-
insula and in the western and southern coastal plains of philic species of the complex, such as An. atroparvus
Turkey. The range extends eastwards from the Near in coastal Europe, An. labranchiae around the west-
9.1 Genus Anopheles Meigen 177

ern Mediterranean region and An. sacharovi around a median stripe, the sublateral and lateral areas are
the eastern Mediterranean region are the three main dark and bare. An anteacrostichal patch of pale scales
malaria vectors in the complex. All three species is present. The lateral scutellar setae are longer than
tend to be most prevalent in relation to saltwater hab- the median ones. The prespiracular setae are brown
itats. An. labranchiae and An. sacharovi are impor- and often absent. The femora, tibiae, and tarsi are
tant vectors throughout their distribution range. The blackish brown with a blue metallic shine. The femora
medical importance of An. atroparvus depends on and tibiae have a pale scaled apex and the tarsi are
local conditions, e.g. presence of the species in large without rings. Tarsomere I of the fore leg is distinctly
numbers, or transmission of winter malaria (avail- longer than tarsomeres II–V combined. The scales on
ability of human hosts in or close to overwintering the wing veins are dense and all dark, and the wings
shelters). The more zoophilic species, e.g. An. macu- are without spots (Fig. 6.7a). The wing fringe is made
lipennis s.s., An. beklemishevi, An. messeae, An. of lanceolate scales of unequal length, with a white
melanoon and An. subalpinus which are usually apical spot.
associated with freshwater habitats, play a minor Male: The palps are as long as or slightly shorter
role in malaria transmission. Nevertheless, at least than the proboscis. The gonocoxite has two strong
An. maculipennis s.s. and An. messeae are responsi- parabasal setae, curved at the end, arising from a
ble for malaria transmission in limited regions of strongly sclerotized base (Fig. 9.6). The outer seta is
Europe where high incidences of the species and a longer and thinner than the inner seta. A crescent
shortage of domestic animals occur. shaped internal seta is inserted at the apical 1/3 of the
Notes on systematics: After the detection of a new gonocoxite, and numerous long thin setae cover the
species within the Anopheles Maculipennis Complex same portion of its dorsal surface. The claspettes have
with cytotaxonomic techniques by Stegnii and two lobes. The outer lobe bears three flattened,
Kabanova (1976) and evidence of the presence of other spatula-like setae and the inner lobe has a single, lon-
hitherto unknown members, White (1978) resurrected ger, sabre-like seta. The aedeagus has 8-10 or more
two members of the complex, previously regarded as long leaflets on each side.
synonyms, to specific rank, namely: An. martinius Larva: The antennae have a dark, spiculate apex.
Shingarev 1926, with an eastern distribution in central The antennal seta (1-A) has 3-4 moderately long
Asia, from synonymy with An. sacharovi, and An. branches inserted in the basal half of the antenna, close
sicaulti Roubaud 1935, found in northern Africa, from to the middle. The frontoclypeus is spotted but not
synonymy with An. labranchiae. Several North banded. The clypeal setae are all single. The inner cly-
American mosquitoes clearly belong to the Anopheles peal setae (2-C) are closer to each other than to the
Maculipennis Complex, e.g. An. aztecus Hoffmann
1935, An. earlei Vargas 1943, An. freeborni Aitken
1939, An. occidentalis Dyar and Knab 1906.

Anopheles (Anopheles) marteri

Senevet and Prunelle 1927

Female: Resembles An. claviger in general appear-

ance, most easily distinguished from it by the whitish
apex of the proboscis and a usually present pale apical
spot on the fringe of the wing. The proboscis is with-
out pale rings, and its apex is distinctly paler than the
brown basal part (Fig. 6.11a). The palps are subequal
to the proboscis, with scattered pale scales at the base.
The terminal segment of the palps is at least half as
long as the penultimate one. The occiput bears a tuft of
whitish scales. The scutum has pale scales which form Fig. 9.6 Hypopygium of An. marteri
178 9 Subfamily Anophelinae

outer (3-C), and more than twice as long as the outer Medical importance: According to its strong
setae. The postclypeal setae (4-C) are of variable preference for animal hosts, An. marteri is most prob-
length, and as long as the outer clypeal setae (3-C) ably of minor importance as a vector of human dis-
which extend beyond the anterior margin of the fronto- eases (Ribeiro et al. 1988).
clypeus (frequent character of larvae from Portugal, Notes on systematics: Since 1927 when Senevet
Greece, Turkey, Iran and Tadzikistan populations), or and Prunelle described An. marteri as a new species,
are short and do not surpass the margin (larvae from the closely related An. sogdianus was described in
Spain, Algeria, Tunisia, Israel and Jordan). The frontal Tadzhikistan (Keshishian 1938) and An. marteri var.
setae (5-C to 7-C) are plumose, with 6-7 pairs of lat- conquensis in Spain (Torres Canamares 1946).
eral branches. The end of the inner frontal seta (5-C) Later, An. sogdianus was given subspecific status
hardly reaches the base of the postclypeal seta (4-C). under An. marteri after Beklemischev (in Boyd
The prothoracal seta 1-P is well developed, with a 1949). Ribeiro et al. (1987) stated that An. marteri is
strong shaft, pinnately branched, similar to 2-P and a polymorphic, monotypic species, and that the
4-P. Seta 3-P is single, rarely 2-branched. Seta 1-T on names sogdianus and conquensis were only the
the metathorax of palmate type, with 10-11 leaflets. morphs that have to be treated as junior synonyms
The abdominal seta 1-I is short and spine-like. The of marteri. The authors hypothesize that the clinical
palmate setae 1-II to 1-VII are well developed, with distributions of the morphs is temperature depen-
15–19 leaflets, sometimes more. The leaflets are nar- dent, with a January isoterm of + 10°C separating
rowed in 2-3 irregular steps beyond the middle, form- marteri/conquensis in the south from sogdianus in
ing a filament that is at least 1/3 as long as the blade the north. The proposed status was accepted by
(Fig. 8.12a). The antepalmate setae on abdominal seg- Ward (1992).
ments IV and V (2-IV and 2-V) are single, rarely with 2
branches. The abdominal setae 6-I to 6-III are pin-
nately branched. Anopheles (Anopheles) plumbeus Stephens 1828
Biology: An. marteri is a polycyclic species often
found in mountainous regions. In Sardinia and Female: An. plumbeus can be distinguished from the
Corsica, the species was collected from sea level up similar An. claviger by its smaller size and its general
to 1,000 m (Aitken 1954a), and in Tadzikistan from darker, leaden colouration. The pleurites of the thorax
900 to 1,600 m (Keshishian 1938). Females hibernate and the lateral parts of the scutum are blackish brown,
in natural shelters. Spring is the preferred season for forming a distinct contrast to the pale or ashy-grey
larval development but a second, autumnal peak has median part of the scutum. Furthermore, the wings are
been registered as well (Logan 1953; Senevet and more densely scaled and darker in appearance than
Andarelli 1956). Larvae have been found from those of An. claviger. The proboscis and palps are
March-September in shaded, clear and cool water in black, with the palps being approximately the same
rock pools and mountain streams and springs, with length as the proboscis with the apical segment more
rocky bottom and scarce vegetation. They usually than half as long as the penultimate one. The pedicel is
breed in acidic water (pH 5.5–6.0) within a tempera- brown, and the flagellum is blackish brown with black
ture range of 15–22°C (Senevet and Andarelli 1956; setae. The vertex has a tuft of narrow, pure white scales,
Ribeiro et al. 1987). The larvae can be found in asso- which is directed anteriorly, and yellowish longer
ciation with those of An. atroparvus, An. claviger setae. The occiput is covered in its median part with
s.s., An. petragnani, Cx. p. pipiens and Cx. territans whitish lanceolate and erect forked scales, laterally
(Gutsevich et al. 1974; Ribeiro et al. 1987). An. mar- with black erect forked scales. Lateral parts of the
teri females are sylvatic, exophagic and markedly scutum are blackish brown, with a median longitudinal
zoophilic. grey stripe which covers at least 1/3 of the width of the
Distribution: It is a southern Palaearctic species, scutum. The anterior margin of the scutum has a well
which is distributed from Portugal and North Morocco developed anteachrostichal tuft of pure white, narrow
to Tadzhikistan. In Europe it is recorded in Albania, scales (Fig. 6.12a). The scutellum is brown with dark
Bulgaria, Corsica, Greece, Portugal, Sardinia, Sicily, setae, its posterior margin is slightly concave at the
and Spain. sides, and the postnotum is dark brown. The pleurites
9.1 Genus Anopheles Meigen 179

are blackish brown with 5-6 prespiracular setae. The branched. The distance between the pair of inner clypeal
legs are black or blackish brown, the coxae and ventral setae (2-C) is smaller or almost the same as the dis-
surfaces of the tibiae are slightly paler. The wings are tance between the inner (2-C) and outer clypeal setae
densely covered with dark brown, lanceolate scales (3-C). The postclypeal setae (4-C) are short and single,
and not spotted; the cross veins are well separated. The and situated wide apart. The distance between them is
abdomen is black, and covered with pale brown or larger than the distance between the outer clypeal setae
dark setae with a golden tinge. (3-C). Seta 1 of abdominal segment I (1-I) is short and
Male (Fig. 9.7): The gonocoxite bears 2 two single. The palmate setae on abdominal segments
strong parabasal setae of approximately the same II–VI (1-II to 1-VI) are conspicuous, but inconspicu-
length. They arise directly from the surface of the ous or rudimentary on segment VII. Each palmate seta
gonocoxite, not from a tubercle. The internal setae are consists of 14–15 lanceolate leaflets with a pointed
inserted near the middle of the gonocoxite. The apical apex, but without a terminal filament, their margin may
spine of the gonostylus is short. The claspettes are be slightly serrated in the apical half. The lateral setae
divided into two lobes, the outer lobe bears three setae, on segments I–VI (6-I to 6-VI) are large and pinnately
which might be slightly flattened and situated close branched. Each abdominal segment ventrally carries
together but are not fused. The inner lobe bears one two pairs of stellate setae. The pecten plate is usually
short hair-like seta and two to three spine-like setae of composed of teeth of more or less the same length. The
variable length, at least one of which is slightly bent at saddle is covered with numerous spicules. The ventral
the apex. The aedeagus is short and broad, without brush has 17–19 fan-like setae arising from a common
spines or leaflets. base. The anal papillae are shorter than the saddle.
Larva: Larvae of An. plumbeus are at once distin- Biology: Larvae of An. plumbeus develop almost
guished from all other European species of the genus exclusively in tree-holes. The breeding water is usually
Anopheles by the frontal setae (5-C to 7-C) which are dark brown owing to the dissolved tannins and pigments
reduced in size and are single (Fig. 8.7b). The head is derived from the wood and has a high concentration of
more or less oval, uniformly dark brown, and the salts in combination with a deficiency of oxygen (Mohrig
primordial compound eyes are weakly developed. 1969). The larvae are ordinarily found in tree-holes in
The antennae are approximately 1/3 of the length of beech (Fagus sylvatica), ash (Fraxinus excelsior), elm
the head, straight and smooth. The antennal seta (1-A) (Ulmus sp.), sycamore (Acer pseudoplatanus), lime
is very short and single, situated close to the base. The (Tilia sp.), oak (Quercus sp.), birch (Betula sp.), horse-
clypeal setae (2-C and 3-C) are thin and sparsely chestnut (Aesculus hippocastanum) and others, often
together with larvae of Oc. geniculatus. Further associ-
ates may be larvae of Or. pulcripalpis, Oc. berlandi, Oc.
Echinus, and Oc. pulcritarsis. The eggs of An. plumbeus
are not laid on the water surface but on the side of the
tree-hole and hatching occurs when the hole is flooded.
Thus, the number of generations per year depends on
the hydrological situation. Hibernation takes place in
the egg or larval stage. The larvae which hatch in autumn
usually grow into the second and third-instar by the end
of the year, but do not pupate until the next spring. They
spend most of the time at the bottom of the hole and can
survive long periods when the water surface is frozen,
but high mortality can be observed when the breeding
water and the mud at the bottom are entirely frozen dur-
ing a long period (Mohrig 1969). In spring, a major pro-
portion of the larvae hatch from hibernated eggs.
Occasionally, especially in periods of drought, larvae of
An. plumbeus may also occur in artificial containers,
Fig. 9.7 Hypopygium of An. plumbeus rock holes, or in ground depressions in shaded situations
180 9 Subfamily Anophelinae

containing a rich infusion of fallen leafs (Aitken 1954a). 9.1.2 Subgenus Cellia Theobald
In central Europe the adults usually occur from late
spring on and are present until the end of September.
Members of this subgenus are characterized as fol-
They can be found from sea level up to an altitude of
lows: In the adults, the costa (C) has four or more
1,200 m (Senevet and Andarelli 1956), and in the south-
pale spots and the cross vein areas and furcations of
ern part of its range the species occurs in forests and in
R2+3 and M are pale scaled. In males the base of the
mountainous areas up to altitudes of 1,600–2,000 m
gonocoxite bears 4-7, usually 6, parabasal setae, sit-
(Gutsevich et al. 1974). Females are persistent biters
uated close together and not arising from distinct
and they are most active during the crepuscular period,
tubercles. The internal seta is absent. The larvae of
feeding principally on mammalian blood, including that
the subgenus Cellia have a single and small antennal
of humans (Service 1971a). Occasionally they have
seta (1-A) which is situated on the outer side of the
been observed to attack humans during the day in shaded
antennal shaft. The inner clypeal setae (2-C) are
situations along forest edges. Some populations have
wide apart, situated closer to the outer clypeal setae
shown a strong anthropophilic preference (Petric 1989).
(3-C) than to each other. The leaflets of the palmate
Because of its preferred larval habitats, An. plumbeus is
setae are not lanceolate, but always abruptly nar-
mainly found in forests and rural areas, but considerable
rowed or shouldered, thus divided into a blade and a
populations may also be found in urban situations,
terminal filament. The subgenus Cellia is mainly
where the larvae develop in tree-holes in gardens or
distributed in the Oriental and Ethiopian regions and
parks. However, it has adapted its breeding habit to
is not found in the Nearctic. In Europe, the distribu-
widely available artificial breeding sites below the
tion range of the subgenus is confined to the
ground, such as catch basins and septic tanks with water
Mediterranean region, where three species and one
contaminated with organic waste. Therefore, in central
subspecies of An. cinereus can be found. Therefore,
Europe An. plumbeus has increased in numbers during
An. cinereus is described here, despite the compli-
the last decades and can be a major nuisance species in
cated situation of its real distribution.
human dwellings especially when unused septic tanks
support mass breeding.
Distribution: An. plumbeus is widely distributed
throughout Europe wherever there are deciduous trees Anopheles (Cellia) cinereus Theobald 1901
in which rot holes can be found. It is also distributed in
the northern Caucasus, in the Middle East south to Iran Female: The proboscis and palps are extraordinarily
and Iraq and in North Africa. A similar species which long and slender. The palps commonly have four pale
is found in India and Pakistan is considered by most rings. The basal three rings are broad, subequal, and
experts to be the species An. barianensis James, but extend to both segments at the articulations of palpom-
Gutsevich et al. (1974) pointed out that there are no eres II–III, III–IV and IV–V. The distalmost ring is
distinct differences between An. plumbeus and An. often very narrow, sometimes indistinct or absent.
barianensis. In North America, An. plumbeus is When present and well developed, it occupies the api-
replaced by an allied species, An. barberi Coquillett, cal third of palpomere V. Palpomeres IV and V are long
which closely resembles it (Marshall 1938). and when combined, distinctly longer than palpomere
Medical importance: Although laboratory studies III. Glick (1992) described the palps of An. cinereus as
have shown that An. plumbeus can successfully be having three rings and a dark apex which is usually true
infected with P. vivax and P. falciparum (Weyer 1939; for ssp. hispaniola. The first flagellomere is speckled
Marchant et al. 1998) and that the species is an effi- with white scales. The occiput has a well developed tuft
cient carrier of malaria, it is considered to be of minor of white scales. The scutum has a median stripe of long,
epidemiological importance at the present time because usually narrow pale scales, and the submedian and lat-
of its ecology. In the past, An. plumbeus played a major eral areas are devoid of scales. The femora and tibia are
role as a vector in forests in Caucasian resorts dark with distinct pale spots on the femorotibial and
(Gutsevich et al. 1974) and probably has been respon- tibiotarsal articulations. The fore and mid tarsi are
sible for two recorded cases of locally transmitted entirely dark or have very narrow pale apical rings, but
malaria in London, UK (Shute 1954). usually only on tarsomere I. The hind tarsi have very
9.1 Genus Anopheles Meigen 181

narrow white apical rings on tarsomeres I–IV. Tarsomere Distribution: Eastern Afrotropical region from
V is entirely dark scaled. The costa has five large dark Sudan and Ethiopia to South Africa, Arabian Peninsula
spots, and its very base is dark scaled. R4+5 are mainly
pale scaled, dark scaling of cubitus (Cu) is quite vari-
able, and the anal vein (A) usually has three dark spots  nopheles (Cellia) cinereus hispaniola
A
with no pale fringe spot at its end. (Theobald 1903)
Male: Palpomeres IV and V are very long; their
combined lengths exceed that of palpomere III. The Female: Similar to the nominative form in all stages,
palps have 3-4 pale rings, the basalmost ring is some- but easily distinguished from the other European
times indistinct, and the apicalmost ring is distinct. members of the subgenus Cellia. It differs from An.
The gonocoxite has 3-6 subequal parabasal setae. The multicolor by having a dark base of costa (C)
claspette lobe is undivided, and the inner seta is nearly (Fig. 6.17b) and a bare submedian scutal area, from
twice as long as the lobe. Two additional outer setae An. sergentii by having a mainly pale scaled R4+5 and
may be present. The aedeagus has 7-10 pairs of long from An. superpictus by having the apex of the palps
leaflets, some of them distinctly broadened and ser- dark and three relatively short dark spots on the anal
rated. The longest leaflet is almost half as long as the vein (A). The palps usually have three pale rings, on
aedeagus. both sides of articulations between palpomeres II–III,
Larva: The frontoclypeus is marked with dark III–IV and IV–V, with a dark apex. Rarely, the very
spots of variable size and shape. The antenna is tip may be white but the middle of palpomere V
sparsely spiculate. The antennal seta (1-A) is single, remains dark scaled. The hind tarsomeres have indis-
and inserted at about 1/3 the length of the shaft, nearly tinct pale apical rings, sometimes reduced to a few
as long as the width of the antenna at the point of its scattered white scales. Other characters are similar to
insertion. The clypeal setae are all single. The inner An. cinereus.
clypeal setae (2-C) are closer to the outer (3-C) than to Male (Fig. 9.8): The gonocoxite has 4-7 (usually 6)
each other, and 1.5–2.0 times as long as the outer short parabasal setae of similar size and length. The
setae. The length of the postclypeal setae (4-C) is vari- inner seta on the claspette lobe is about as long as the
able, often subequal to the outer clypeal setae (3-C). lobe, and one or two shorter median setae may be pres-
The frontal setae (5-C to 7-C) are strong and pinnately ent. Several outer setae are fused to form a conspicu-
branched (3-5 pairs of branches are evenly distributed ous broad spatula-like process, which is distinctly
over the entire main stem). The prothoracal seta 1-P is shorter than the inner seta. The aedeagus has 7-8 pairs
well developed, pinnately branched, and similar to of long, broad weakly serrated leaflets.
2-P and 4-P but distinctly shorter. Seta 3-P is short and
single. The abdominal seta 1-I is short, variable in
shape, and bifurcated or plumose. The palmate setae
on abdominal segment II (1-II) are small, with 6-9
leaflets. The palmate setae on abdominal segments
III–VII (1-III to 1-VII) have 13–15 leaflets abruptly
narrowed in one or several irregular steps forming a
filament which is about half as long as the blade
(Fig. 8.15d). The abdominal setae 6-IV to 6-VI are
pinnately branched.
Biology: An. cinereus is a polycyclic species. The
most preferred breeding sites are edges of swamps,
streams, irrigation ditches, rock pools and marshy
pools. The larvae prefer moderately shaded water bod-
ies with a slightly alkaline pH ranging from 7.7 to 8.3
(Evans 1938). The females are zoophilic and frequently
enter shelters of domestic animals. Occasionally they
can be encountered inside human dwellings. Fig. 9.8 Hypopygium of An. cinereus hispaniola
182 9 Subfamily Anophelinae

Larva: The frontal setae (5-C to 7-C) are poorly Anopheles (Cellia) multicolor Cambouliu 1902
developed, with a few branches arising near the base of
the main stem. The inner frontal seta (5-C) is slightly Female: The proboscis is dark brown, and the palps
longer than the median frontal seta (6-C). The lateral are nearly as long as the proboscis with three pale
abdominal setae 6-I to 6-V are pinnately branched, rings at the joints of palpomeres II–III, III–IV and
weakly pinnated on segments IV and V. IV–V. The proximal ring is very narrow with pale
Biology: A polycyclic, orophilic (preference for scales mainly at the apex of palpomere II and some-
higher altitudes) species, which can be found from sea times with a few scales at the base of palpomere III.
level to 2,334 m (Logan 1953). The larvae breed on The median and distal rings are broader than the
hilly grounds, most numerous from mid summer on in proximal ring. Half of palpomere V is dark. The
the mountains of Sardinia (Aitken 1954a). The pre- clypeus is light brown, the flagellum brown, and the
ferred breeding sites are sandy and gravelly edges of pedicel and the first 3-4 flagellomeres have a few pale
streams in shallow, clear water, but larvae can also be scales. The vertex has long pale scales and setae
found in irrigation ditches and swamps (Senevet and forming a frontal tuft, the occiput in the upper half
Andarelli 1956). According to the same authors, the has pale scales, and dark scaled at the sides. The
larvae were found in waters with salinity ranging from integument of the scutum is brown, the lateral areas
0 to 2.9% and a pH value ranging from 5.0 to 7.0. When somewhat darker than the median. The submedian
disturbed, the larvae may remain below the surface of and lateral areas are covered with narrow creamy
the water for one hour or more (Aitken 1954a). Often scales, and the setae on the scutum are black. The
they breed in association with larvae of An. labran- scutellum is light brown, the pleurites brown with
chiae. The females express zoophily and exophily, but some pale scales, and about 3-5 prespiracular setae.
readily bite humans in the open (Ribeiro et al. 1988). The tibiae are prominently pale apically, the tarsi
Distribution: Mediterranean region, North Africa, minutely pale apically, with pale scales not forming
French Equatorial Africa, Sinai Peninsula and definite pale rings, and the hind tarsi may be com-
Transjordan (Knight and Stone 1977; Ribeiro et al. pletely dark. The wing veins are covered with narrow
1980). In Europe, the species is registered in Portugal, to moderately broad scales, and the cross veins are
Spain, Italy and Greece. well separated. The wing is extensively pale scaled,
Medical importance: The species is a potential and not well ornamented due to the paleness of the
vector of malaria in southern Europe (MacDonald dark scales. The costa (C) is largely pale, with dark
1957). However, owing to its exophilic and exophagic areas reduced in some specimens, and pale at the
behaviour it is regarded as a vector of minor importance extreme base (Fig. 6.17a). The anal vein (A) is mainly
(Jetten and Takken 1994). pale with three small dark spots. There are pale fringe
Notes on systematics: The status of the name his- spots at the ends of all the veins except the anal vein
paniola is still rather undefined. Knight (1978) and (A). The abdomen is brown, entirely devoid of scales,
Knight and Stone (1977) treated both An. cinereus and but with dark setae, and the first abdominal segment
An. hispaniola as valid species of the subgenus Cellia is more densely covered with setae.
Theobald. The status of An. hispaniola was changed to Male (Fig. 9.9): The gonocoxite is slightly longer
synonymy of An. cinereus after Dahl and White (1978) than broad. The base of the gonocoxite has 5 rather
with no further explanation, which was acknowledged slender parabasal setae. The outermost seta is long and
by others (Ward 1984). Finally, the status of hispaniola straight, arising from slightly above the other setae.
was changed from species (former change to synon- The claspette is not clearly divided into distinct lobes,
ymy ignored) to subspecies of An. cinereus (Ward has a long and slender spine-like seta, several smaller
1992) following Ribeiro et al. (1980). The authors setae and a broad, spatula-like seta situated at the outer
stated that owing to a very low degree of morphologi- border. The aedeagus is distinctly shorter than half the
cal differences and absence of information concerning length of the gonocoxite, and leaflets and spines of the
hybridisation between the forms, it is most advisable aedeagus are absent.
to treat hispaniola as a subspecies. Nevertheless, Larva: The larva of An. multicolor closely resem-
Ramsdale (1998) stated that the name hispaniola bles that of An. superpictus. The antenna has numer-
should be regarded as a junior primary synonym of ous spicules along the inner border, and the antennal
cinereus, until further evidence is given. seta (1-A) is usually situated close to the base of the
9.1 Genus Anopheles Meigen 183

able to tolerate a high content of salinity, which may

occasionally reach the point of saturation. In North
Africa, they were found in association with larvae of
Oc. caspius, Cs. longiareolata and An. cinereus his-
paniola (Senevet and Andarelli 1956). The authors
reported larval findings throughout the year with two
peaks, the first between April and July and a second
peak from November to December. Although An. mul-
ticolor has a wide distribution range, very little is
known about the adult behaviour. The females are con-
sidered to feed on humans. In Egypt they readily enter
houses and bite at night (Kirkpatrick 1925). The same
author reported considerable flight ranges; adults have
Fig. 9.9 Hypopygium of An. multicolor
been found up to 13 km from the nearest possible
breeding places.
shaft and is single. The apex of seta 1-A is sometimes Distribution: An. multicolor is mainly a desert spe-
divided into 2 or 3 extremely fine branches. The inner cies distributed in North Africa and much of Southwest
clypeal setae (2-C) have widely separated bases. Both Asia. Its range extends from Cyprus, Egypt, Palestine
inner and outer clypeal setae (2-C and 3-C) are single and Anatolia eastwards to West Pakistan. It has been
(Fig. 8.16a), the outer seta is about 2/3 the length of reported in Spain in the province of Murcia and the
the inner seta. The postclypeal setae (4-C) are single, Canary Islands (Romeo Viamonte 1950).
as long as or longer than the outer clypeals, with their Medical importance: The role of An. multicolor as
distal ends reaching beyond the bases of the clypeal a vector of malaria is still uncertain. Several authors
setae. The frontal setae are pinnately branched, and have considered it to be an important vector on epide-
the inner frontals (5-C) are usually distinctly longer miological grounds, but no naturally infected females
than the median frontals (6-C) (Fig. 8.14b). The pal- have been found. Other authors regard its role as doubt-
mate setae are undeveloped or rudimentary on abdom- ful even in areas of mass breeding (Gillies and de
inal segments I and II (1-I and 1-II), and variably Meillon 1968).
developed on segments III–VII, or sometimes undif-
ferentiated. If fully developed, the leaflets are more or
less uniformly pigmented and narrow. The shoulder is Anopheles (Cellia) sergentii (Theobald 1907)
well marked, with a long filament about 2/3 the length
of the blade, rather broad at the base and sharply Female: Resembling An. superpictus, but differs from
pointed distally. The pecten plate has 7-8 long teeth the latter by its smaller size and the wing ornamenta-
usually alternating with 1-2 short teeth, finely serrated tion. The proboscis is dark brown, long and slender.
on the basal half. The arrangement is sometimes regu- The palps are nearly as long as the proboscis, of uni-
lar, but often irregular. The sclerotized tergal plates form thickness from the apex to the base, and the last
are small, and on abdominal segment V the width of palpomere is very short and entirely pale scaled
the plate is about 1/3 of the distance between the pair (Fig. 6.15a). In addition to the pale tip of the palps, two
of palmate setae (1-V). A small, single accessory plate more narrow, but well marked pale rings are present at
is present near the centre of segment V. The saddle the joints of palpomeres II–III and III–IV. The clypeus
seta (1-X) is long and single, and the anal papillae are is dark brown. The pedicel is dark brown, and without
very short. scales. The flagellum is brown with black setae and
Biology: The larvae are generally to be found in some narrow pale scales on the first and often on the
inland or coastal breeding places in semi-arid regions succeeding flagellomeres. The vertex has pale lanceo-
in brackish and fresh water, but they show a preference late scales, which are directing forwards, and the frontal
for saline desert waters. They occur in salt pans, oases, tuft is not well developed but is distinct. The occiput in
small pools with or without aquatic vegetation, and the upper part has pale forked scales and at the sides
sometimes in unused shallow wells. They are never has dark forked scales and setae. The eyes are bordered
found in rice fields (Christophers 1933). The larvae are with broad scales. The scutum is brown, the lateral
184 9 Subfamily Anophelinae

areas and transverse suture are somewhat darker than ger than the second longest, and all the broad leaflets
the median area, but not distinct and varies between are serrated through most of their length.
the specimens. The scutum is covered with lanceolate Larva: The antenna is covered with spicules along its
hair-like scales and dark setae. The scutellum is brown inner border, and the antennal seta (1-A) is inserted at the
with dark setae. The pleurites are entirely devoid of basal 1/3 of the antennal shaft, and is short and single.
scales, with 2 prespiracular setae, and 8 upper mesepi- The clypeal setae are usually single, rarely do the outer
meral setae. The coxae are without scales, the femora clypeals (3-C) have 2 branches. 3-C is slightly longer
are uniformly dark except for pale markings at the tips than half the length of the inner clypeals (2-C). The bases
of the femora and tibiae of all the legs. The tarsi are of the inner clypeal setae are not that much separated as
entirely dark, without pale rings. The wing has pre- in the other members of the subgenus Cellia, but the dis-
dominating dark scales on veins Rs to Cu, and vein R4+5 tance between them is nearly twice the distance between
is usually almost entirely dark scaled, but may show an the inner and outer clypeals. The postclypeal setae (4-C)
indistinct pale area about the middle. The extreme base are usually single, about the same length as the outer cly-
of the radius (R) is entirely pale. Pale spots are also peals, with their distal ends reaching well beyond the
present at the furcations of R2+3 and M, at the cross bases of 2-C and 3-C. Occasionally 4-C may be divided
veins, at the bases of Cu and A and at the middle of into 2-4 branches. The frontal setae (5-C to 7-C) are pin-
Cu2. The wing fringe is well marked with pale spots at nately branched, and the inner frontals (5-C) are slightly
the ends of all veins except the anal vein (A) longer than the median frontals (6-C) (Fig. 8.14a). The
(Fig. 6.16a). The abdomen has no scales, is blackish typical palmate setae are well developed on abdominal
brown, and covered with light setae. segments III–VII, with 17–18 large leaflets, which are
Male (Fig. 9.10): The gonocoxite is slightly longer more or less uniformly pigmented. The filament is long,
than it is broad. The base of the gonocoxite has 4-5 slender and pointed, and more than half the length of the
parabasal setae of varying length irregularly scattered blade (Fig. 8.15b). The sclerotized tergal plates are broad,
over the surface and sometimes slightly curved at their nearly as broad as the distance between the palmate setae
apices. The claspette is not divided into lobes, and on the first five abdominal segments and broader than the
presents a massive unit, with a spatula-like seta on the distance between the palmate setae on segments VI–VIII
outer border and a stout spine-like seta of similar (Fig. 8.15a). The last tergal plate occupies more than 1/3
length on the inner border. Between them is a second of segment VIII. The pecten plate has 6-8 long and 4-8
spine-like seta of half the length of the others. The short spine-like teeth. The saddle seta is long and single.
aedeagus is long and slender, with 3-5 pairs of more or Biology: The breeding places of An. sergentii are
less broad leaflets. The longest leaflet is distinctly lon- quite variable. Larvae can be found in rice fields, irri-
gation channels, slow moving streams, small pools in
river beds or ponds with a rich aquatic vegetation, and
grassy swamps from overrunning irrigation ditches or
streams. In the Canary Islands, it was found in pools in
ravines, especially in small rock pockets (Christophers
1929). An. sergentii often occurs together with larvae
of An. sacharovi and An. superpictus, and other associ-
ates are An. multicolor, Cx. p. pipiens and Cs. longia-
reolata (Senevet and Andarelli 1956). Adults are rarely
found from spring to early summer and are most prev-
alent in late summer and autumn (Martini 1931).
Hibernation may take place in both the larval and adult
stage. Adult females commonly enter any kind of habi-
tation, including houses, and readily bite humans soon
after dark, with the main activity period being during
the night. They appear to be moderate flyers, and have
been found in large numbers 2.5 km from the nearest
Fig. 9.10 Hypopygium of An. sergentii possible breeding place (Christophers 1933).
9.1 Genus Anopheles Meigen 185

Distribution: An. sergentii has a wide distribution

in the southern Mediterranean region. Its range
stretches from North Africa, through the Middle East
to Pakistan. It is recorded in the Canary Islands (Romeo
Viamonte 1950) and in Europe in Sicily (Coluzzi and
Sabatini 1995). Senevet and Andarelli (1956) reported
a doubtful record in Bulgaria.
Medical importance: Although natural infections
were rarely found, the species is considered as a poten-
tial vector of malaria on epidemiological grounds. In
Palestine it was regarded as the principal malarial vec-
tor (Saliternik 1955).

Anopheles (Cellia) superpictus Grassi 1899

Female: A variable species, especially in the scal- Fig. 9.11 Hypopygium of An. superpictus
ing of the palps, with whitish scales on the wings
and legs. The four white scale patches on the costa
(C) and subcosta (Sc) may be of variable length. half as long as the gonocoxite, and bearing several
The proboscis is dark, palpomeres III and IV have very short leaflets (Fig. 7.13a).
basal and apical white rings, and palpomere V is Larva: The inner clypeal seta (2-C) has short
nearly completely covered with white scales. The branches (Fig. 8.16b), and the outer clypeal seta (3-C)
vertex is dark, and the occiput has light, erect scales is single and about half as long as 2-C. The inner
and an anterior patch of flat white scales. The scutum frontal seta (5-C) is distinctly longer than the median
has a median stripe of pale greyish scales, but is oth- frontal seta (6-C). Typical palmate setae on the
erwise dark, and the scutellum has some white metathorax are present (1-T). The palmate setae on
scales. The pleurites are dark with some greyish abdominal segments II–VII (1-II to 1-VII) have
tinge, pale setae, and no distinct patches of scales. 13–19 leaflets, with well developed, serrated and
The costa (C) and subcosta (Sc) have four white pointed filaments. The pecten plate has 4 long strong
areas, somewhat variable in length. Predominant and 5 smaller teeth.
pale scales are present on veins Rs to Cu, and vein Biology: The larvae are found in slow running,
R4+5 is usually almost entirely pale scaled. The pale warm and not polluted waters, e.g. in pools at the
spot at the apex of the wing fringe is large edges of rivers or in irrigated rice fields. They also
(Fig. 6.16b). Because of the numerous pale scales occur in shallow pools in dry river beds (Gutsevich
the whole wing has a light impression. The legs are et al. 1974). They are able to tolerate some amount
dark, the coxae are without scales, the femora have of salinity but avoid eutrophic and muddy waters.
a lighter ventral surface, the knee spot is indistinct They are found in smaller numbers early in the sum-
or absent and the tarsomeres have some white basal mer (first generation) and can occur in great numbers
scales, sometimes forming indistinct rings. The in autumn (further generations). The larval develop-
abdomen has long yellowish setae. ment may be rapid in high temperatures but usually
Male (Fig. 9.11): The gonocoxite is rounded and takes nearly a month. The females may survive a
short with very few scales and five strong parabasal cold climate, and can remain active throughout the
setae, the two innermost setae are the shortest and the cold season. They bite humans and animals, and bit-
outermost one the longest. The gonostylus is long, bent ing activity reaches its peak at sunset. They are both
at the apex, with a small apical spine. The claspette is endo- and exophilic.
not divided into lobes, but is broad, bearing several Distribution: In Europe the species is distributed in
setae. The outer seta is spatula-like, the inner seta is the Mediterranean region and occurs also in adjacent
long and spine-like. The aedeagus is short, less than areas in Asia Minor and northern Africa. It has a ­southern
186 9 Subfamily Anophelinae

Palaearctic distribution throughout Transcaucasia and Note on systematics: Knight and Stone (1977)
middle Asia and is recorded as far as Pakistan and north- listed seven subspecies, described from Greece,
western India. Taschkent, and Baluchistan. There are two more sub-
Medical importance: The species is reported as species mentioned in the European literature (Martini
being an important vector of malaria in middle Asia 1931; Peus 1967). Thus the variability of the species
(Gutsevich et al. 1974). needs to be further investigated.
Chapter 10
Subfamily Culicinae

Most of the mosquito species of the world belong to more parallel to their resting surface in contrast to
this subfamily, which is subdivided into 11 tribes. most of the females of Anophelinae. Some species
The adults exhibit a high morphological variability have developed autogeny, the ability to lay eggs with-
ranging from species with little scaling to those with out a previous blood meal, usually in extremely cold
explicit patterns of scales of different colours, from regions and also when they inhabit confined spaces.
white to black and even a metallic appearance, as The eggs can be laid either on the water surface for
well as from small to large species. Many species direct development in rafts (Culex, subgenus Culiseta,
have prominent patterns of scales and setae on the Coquillettidia) or into the substrate as single eggs.
scutum. The scutellum is trilobed with setae grouped These may be drought resistant and able to overwinter
on the lobes, except in Toxorhynchitini, which have for up to several years (most Aedes and Ochlerotatus
an evenly rounded scutellum. The short female palps species).
and the trilobed scutellum clearly distinguish the In tropical and subtropical regions, the main portion
Culicinae from the Anophelinae. The legs are often of the mosquito fauna belongs to the tribes of Culicini,
scaled in a characteristic pattern and the claws in Sabethini, Mansoniini and others not occurring in
some tribes have a subbasal tooth which can be spe- Europe. Most of the Aedini species belonging to the
cies specific. The wings are often broader than those genera Ochlerotatus and Aedes are found in the tem-
of Anophelinae and have the cross veins r-m and perate zones, and they dominate in the most extreme
m-cu well expressed. They have usually three sper- northern cold areas of the Holarctic region.
mathecae (receptaculum seminalis). The structure of
the male hypopygium, especially the aedeagal appa-
ratus is often more complex and in some tribes the
gonocoxite may be enriched with well developed 10.1 Genus Aedes Meigen
lobes. The head capsule of the larvae is more or less
squared or rounded, and the antennae are of variable The scaling and setation pattern is extensive and vari-
length. The larval thorax and abdomen are orna- able. The colour of the integument varies from brown-
mented with long but less spiculate setae and lack, in ish to blackish. The proboscis is long, straight, and
the European species, palmate setae. The elongated always entirely scaled. The palps of the female are
siphon with the plate-like, or in Mansoniini piercing, usually very short but in some species can extend to
spiracular apparatus distinguishes the larvae of the half the length of the proboscis. The vertex is scaled,
Culicinae from those of the Anophelinae. The pupae and the occiput has erect scales. The scutum has a
have long trumpets; their openings being less wide more or less species specific pattern of broad and/or
than they are in Anophelinae. The chorionic pattern narrow scales. The lobes of the scutellum are scarcely
of the eggs varies with the mode of egg laying and scaled, but have groups of setae. The prespiracular
can be used for genus, and in some cases, for species area is without setae, but postspiracular setae are
identification. present. The postpronotum and sometimes also the
The culicine females belong to the fiercest biters postprocoxal membrane have pale scale patches. The
especially in the cold temperate regions. They stand mesepisternum, mesepimeron, and mesomeron have

N. Becker et al., Mosquitoes and Their Control, 187

DOI 10.1007/978-3-540-92874-4_10, © Springer-Verlag Berlin Heidelberg 2010
188 10 Subfamily Culicinae

groups of setae and patches of more or less broad The genus Aedes comprises more than 40 subgenera.
scales. The coxae are scaled, and the femora and tib- Some of them are strictly tropical, confined to the
iae have distinct light and dark scaling patterns. Neotropical, Afrotropical, Oriental, and/or Australian
Tarsomere IV is always distinctly longer than tarsom- regions. In the European region, species of the subgen-
ere V. The pulvilli are usually barely developed, and era Aedes, Aedimorphus, Fredwardsius, and Stegomyia
setose. The claws usually have a subbasal tooth; the can be found. Some of the most feared vectors belong
European species of the subgenus Aedes have simple to the genus Aedes. They can transmit diseases such as
claws on all legs. The wing veins are covered with Yellow Fever and Dengue as well as other arboviruses
numerous dark scales, and sometimes scattered pale from several different families causing encephalitis in
scales are present, most frequently on the costa (C), humans and equines and transmit dog heart worm,
subcosta (Sc) and radius (R). The abdomen is covered filariae and bacteria.
with flat and more or less broad scales. The end of the
abdomen differs from other Culicinae by its tapered
last segments, and usually distinct cerci, which are
elongated and rarely rounded. The scaling patterns of 10.1.1 Subgenus Aedes Meigen
males is similar to those of females but often with
less scaling on the pleurites. The palps of males are as Members of the subgenus Aedes are characterized by
long as or longer than the proboscis, and only rarely the palps which are short in both sexes and the pro­
shorter (subgenus Aedes). The antenna has numerous boscis which is usually about as long as the fore femur.
whorls of setae. Tergum IX usually has two lateral The vertex is covered with narrow curved scales, the
lobes bearing a variable number of setae. The gono- occiput with flat broad scales. The patches of scales
coxite has more or less developed basal and apical on the pleurites are weakly developed and the lower
lobes, but the lobes are sometimes absent. The gono- mesepimeral setae are absent. The wings of the adults
stylus is of variable length, and can be simple or are dark scaled. The most characteristic features are
divided. The paraproct is sclerotized, and usually not found in the male genitalia. The gonostylus is subapi-
fused, with a more or less acute tip. The claspettes are cally inserted, unequally bifurcated and does not sup-
present but of variable shape and structure. The aede- port an apical spine. The shorter branch of the
agus is pear shaped, rounded or elongated. The head gonostylus bears several setae on its distal half.
of the larva is oval, usually wider than long, and with Typical claspettes, divided in a more or less slender
a rounded frontal margin. The antenna is about half stem and a flattened appendage or filament, are absent.
as long as the head, occasionally longer than the head, Instead of this, a process which arises from the dorsal
and usually covered with more or less numerous spic- part of the basal lobe is developed. It can be simple or
ules. The antennal seta 1-A is usually multiple- unequally bifurcated. If present, both branches bear
branched, inserted at about the middle of the antennal distinct setae on their apices. The larvae closely
shaft, and the inner frontal seta (5-C) is usually resemble those of the subgenus Aedimorphus and the
inserted in front of the median frontal seta (6-C). genus Ochlerotatus.
Branching of the prothoracic setae 1-P to 7-P is often Knight and Stone (1977) included more than 20
species specific. Abdominal segment VIII has between species in the subgenus, but earlier Reinert (1974)
a few to numerous comb scales arranged in one or transferred nearly half of them, mostly from the Oriental
more irregular rows. The siphon is usually moder- region, into the subgenus Verallina. This transfer was
ately long, and only one siphonal tuft (1-S) is present. acknowledged by Knight (1978). At present, 12 species
It is never located at the base of the siphon, but often are listed under the subgenus Aedes; three from the
inserted distal to the last pecten tooth, at about or Oriental, one from the Australian and eight species
beyond the middle of the siphon. The saddle does not from the Holarctic region, but none are found in the
usually encircle the anal segment, and seta 1-X is Ethiopian or Neotropical regions.
always located on the saddle, and is often single. The General remarks on the systematics: The taxo-
ventral brush has a variable number of precratal and nomic status of the species of the subgenus Aedes
cratal tufts (4-X). The anal papillae are of variable found in the Palaearctic region is still uncertain.
lengths and shapes. Gutsevich et al. (1974) treated Ae. cinereus, Ae. ­rossicus,
10.1 Genus Aedes Meigen 189

and Ae. esoensis as subspecies of the nominative form eral margins and above the wing roots, giving the
Ae. cinereus. This opinion is not shared, because there scutum a fawn brown colouration. The scutellum has
is a large overlap between Ae. cinereus and Ae. rossi- dark setae and pale narrow scales on each lobe. The
cus in Europe; very often the larvae occur in the same integument of the pleurites is light brown with patches
breeding sites and transitional forms are not known. of broad yellowish white or creamy scales on the
There is no doubt that the Palaearctic species can be propleuron, postspiracular area, mesepisternum, and
divided into two groups – first, the cinereus-group with mesepimeron. The scales on the postpronotum are nar-
Ae. cinereus, Ae. geminus, and Ae. sasai described row and hair-like; often the lower portion is paler than
from Japan, second, the esoensis-group with the two the upper one. The prealar area is not scaled, but cov-
eastern species Ae. esoensis and Ae. yamadai and Ae. ered with setae. The mesepimeron is bare on the lower
rossicus from Europe. The members of each group half, and lower mesepimeral setae are absent. The
closely resemble each other. Whether the two other anterior part of the fore coxa has a patch of brown
species of the subgenus, Ae. dahuricus (Danilov 1987) scales. The femora and tibiae are dark scaled, with
and Ae. mubiensis (Luh and Shih 1958), belong to one paler scales on their posterior surfaces. There are small,
of these groups remains unresolved so far. indistinct patches of pale scales on the apices of the
Peus (1972) treated Ae. rossicus as a subspecies of femora, the tarsi are entirely dark brown scaled, and
the eastern Ae. esoensis and this opinion was followed pale rings are absent. The wing veins are covered with
by others (Ward 1984). Although the record of Ae. ros- dark scales. The terga have dark brown scales on the
sicus from Japan by Hara (1958) was based on a mis- dorsal surface, but without pale transverse bands. The
identification (Tanaka et al. 1975) and there is lateral patches of pale scales on each tergum are usu-
apparently no overlap between the two forms, the argu- ally joined, forming longitudinal stripes at the sides of
ments given by Peus are not convincing. There are the abdomen, which are not readily visible in dorsal
clear and distinct differences between the two species view. The sterna have yellowish white scales. The apex
in the shape of the shorter branch of the gonostylus and of the abdomen is pointed, with cerci of short or mod-
the structure of the claspettes. In Ae. rossicus, the erate length.
shorter branch of the gonostylus is nearly as half as Owing to the general colouration, adult females of
long as the main branch and the claspettes are divided Ae. cinereus may, at first glance, be confused with
into a longer and a shorter branch. In Ae. esoensis the Cx. modestus, but the pointed end of the abdomen and
shorter branch of the gonostylus is only one third as cerci, the claw with subbasal tooth, and the lack of pul-
long as the main branch and the claspettes are simple. villi easily identify it as a member of the genus Aedes.
Furthermore the white basal bands on the abdominal Male: The lobes of tergum IX are as long as broad,
terga are always absent in Ae. rossicus and generally widely separated, and each lobe bears several slender
present in Ae. esoensis, at least as patches (Tanaka spine-like setae. The gonocoxite is about twice as long
et al. 1979). Thus until the distribution and status of all as broad, conical, with scales, and long setae on its
the forms involved are clarified, Ae. rossicus should be outer surface (Fig. 10.1). The basal lobe is well devel-
considered as a valid species. oped. The basal lobe as well as the part distal to it is
covered with dense long setae, and the apical lobe is
absent. The gonostylus is inserted well before the apex
Aedes (Aedes) cinereus Meigen 1818 of the gonocoxite and is unequally divided. The inner
and broader branch reaches between 1/3 and 1/2 of the
Female: Medium sized to rather small mosquitoes. length of the main outer branch, tapers towards the
The proboscis is dark brown with lighter scales on its apex, and is rounded at its tip. It bears several setae on
ventral surface, and is about as long as the fore femur the lateral margin. The longer main branch is slightly
(Fig. 6.36a). The palps are entirely dark brown. The curved and bifurcated at the apex giving it a fishtail-
head is mainly covered with flat dark scales, the vertex like appearance. The outer branch of the fork is usually
with golden narrow curved scales and lateral parts of shorter than the inner branch. Their lengths may vary
the occiput with broad yellowish scales. The integu- and often the prongs are nearly the same length, but
ment of the scutum is reddish brown, covered with the outer branch is never longer than the inner branch
golden brown narrow scales which are paler on the lat- (Fig. 7.18c,d). The prongs appear to be flattened
190 10 Subfamily Culicinae

Fig. 10.1 Hypopygium of Ae. cinereus

dorsoventrally and are usually stouter than in Ae.

geminus. The claspettes are unequally bifurcated with
a long and slender branch usually bearing 1–6 long
setae and a shorter branch usually bearing one apical Fig. 10.2 Larva of Ae. cinereus
and 2–3 subapical setae. The paraproct is heavily scle-
rotized, slender and rod shaped with a narrow apex. inserted distal to the pecten and usually consists of 3–6
The lateral plates of the aedeagus are heavily sclero- short branches. The saddle is longer than it is wide and
tized, closed at the base and apex, with the apical half extends to the middle of the lateral sides of abdominal
expanded. segment X or beyond it. The saddle seta (1-X) is dou-
Larva: The head is distinctly broader than long, ble-branched and shorter than the saddle. The ventral
and the antennae, slender and nearly as long as the brush consists of 8–10 tufts of cratal setae (4-X) on the
head. The antennal tuft (1-A) is inserted slightly below common base, and 2–4 shorter tufts of precratal setae.
the middle at about 2/5 of the length of the shaft The anal papillae are long, at least twice as long as the
(Fig. 8.22b). The setae of the labral brush are simple, saddle.
not denticulated. The postclypeal seta (4-C) is inserted Biology: The larvae can be found in various habi-
anterior to the frontal setae, and is small and multiple- tats, but most often they occur at the edges of semi-
branched. The frontal setae (5-C to 7-C) are arranged permanent, partly shaded pools of flood plains, in
in a posteriorly curved row (Fig. 8.21b). The inner sedge marshes or Sphagnum sp. bogs and at the edges
(5-C) and median (6-C) frontal setae have 5 or more of lakes covered by emergent vegetation. The larvae
branches, rarely 3–4, the outer frontal seta (7-C) is also occur in woodland pools, but they require a
long and multiple-branched. The comb of abdominal higher temperature for larval development than the
segment VIII usually has 10–16 scales arranged in a typical snow-melt mosquitoes. Ae. cinereus larvae
double row partly. The individual scale is long with a can be found in these pools when they are subse-
strong apical spine and small lateral spines. The siphon quently reflooded after rainfall. The larvae usually
is slender; the siphonal index 3.0–4.0 (Fig. 10.2). The hatch at a temperature of 12–13°C and the develop-
pecten consists of about 13–21 weakly sclerotized ment starts at 14–15°C, the optimum temperature
teeth reaching beyond the middle of the siphon, and being 24–25°C (Mohrig 1969). Under these condi-
the distal pecten teeth are unevenly and more widely tions the larvae develop very rapidly and finish their
spaced than the basal teeth. The siphonal tuft (1-S) is immature stages within 8–10 days. The adults occur
10.1 Genus Aedes Meigen 191

later than the ­typical snow-melt mosquitoes Oc. rus- Male (Fig. 10.3): In Ae. geminus the basal lobe is
ticus, Oc. communis, Oc. cantans, or Oc. punctor. In less developed than in Ae. cinereus and the covering
central Europe the larvae can be found from April on, with long setae seems not to be as dense as it is in the
in the northern parts of Europe a couple of weeks latter species. Whereas in this case it is recommended
later, and the adults first occur usually in May and to compare individuals of the two species to get a clear
through the summer months until late September. The picture, the immediately visible difference between
findings of larvae in Sphagnum sp. bogs and other the two species is the shape of the apical fork of the
acido-oligotrophic habitats indicate that Ae. cinereus gonostylus. It is bifurcated in both species, but in Ae.
seems to be slightly acidophilic. The females feed geminus the outer branch is longer than the inner one
principally on mammals and bite human hosts readily (Fig. 7.18a, b). In Ae. cinereus the length of the outer
when available. They attack in numbers at dusk and branch never exceeds that of the inner branch. In the
dawn, but do not bite in an exposed sunlit situation. typical form the prongs appear to be thinner and much
During the day they rest in the low vegetation, but slender in Ae. geminus and they are more or less
feed readily after arrival of the prospective host biting rounded, whereas in Ae. cinereus they are often flat-
those parts of the host within the vegetative cover tened. The claspette is divided into two branches, the
(Wesenberg-Lund 1921). The migration range of Ae. shorter branch bearing 2–3 setae, and in Ae. cinereus
cinereus seems to be low, the species is practically this branch bears usually 3–4 setae.
never seen in the open unshaded field. It has at least Larva: No specific differences, neither in the
two generations per year, in its more northern range chaetotaxy nor in other characteristics, can be found in
only one generation per year may occur. The oviposi- the larvae of Ae. geminus and Ae. cinereus. Both show
tion takes place in the summer months in suitable individual variability, e.g. in the number of the small
dried up depressions prone to subsequent flooding, accessory siphonal setae on the dorsal part of the
and hibernation takes place in the egg stage. In many siphon.
localities Ae. cinereus occurs in masses and causes Biology: So far, the information available about the
great annoyance to ­walkers or people seeking recre- biology of Ae. geminus is scanty. There is a large over-
ation in forested areas. lap in the preferred breeding sites with Ae. cinereus,
Distribution: Ae. cinereus is distributed in the north- and very often both species can be found together in
ern Holarctic region and widely spread over Europe. It the same water bodies. Peus (1972) reported Ae. gemi-
can be found from Finland to Italy and from Spain to the nus to have a lower tolerance against acidic habitats,
eastern shores of the Baltic Sea and the North Caucasus.
It is distributed in Middle Asia, Kazakhstan and Siberia,
the Far East and North America.

Aedes (Aedes) geminus Peus 1970

Female: Ae. geminus closely resembles Ae. cinereus

and can be identified with certainty solely through
hypopygial characteristics. Peus (1972) considered
both as sibling species and described the adults of
Ae. geminus in the typical form usually being smaller
than the adults of Ae. cinereus and the females of the
latter usually with a lighter colouration in the typical
form than the females of the former. However, the size
of an adult is closely related to the nutritional situation
during the immature stages and females of Ae. cinereus
show a variation in their colouration, e.g. darker forms
may exist, thus these characteristics are of no value for
identification of the two species. Fig. 10.3 Hypopygium of Ae. geminus
192 10 Subfamily Culicinae

though he could not find the species in mesotrophic occiput are ­covered with broad light coloured whitish
and higher acido-oligotrophic swamps, where Ae. grey scales, producing a distinct contrast to the scales
cinereus was numerous. As Ae. cinereus, Ae. geminus on the vertex. The eyes are bordered with a narrow row
has at least two generations per year and the males of whitish scales. The scutum has narrow brown scales,
form mating swarms of only 10 individuals or less. often with an inconspicuous pale stripe on the lateral
The females are anthropophilic and can cause great margins, which is more distinct on the posterior part.
annoyance, when present in large numbers. The upper part of the postpronotum has narrow dark
Distribution: Because of the close similarity to Ae. scales, and on the lower part the scales are broad, flat,
cinereus it is difficult to assess the whole range of dis- and of a lighter colour. The prealar area has whitish
tribution for Ae. geminus. Records of Ae. cinereus ear- scales and setae, the scales on the mesepisternum do
lier than 1970 or those which are solely based on not reach the anterior angle, and the scales on the
females or larvae are at best questionable. Lvov (1956) mesepimeron do not reach the lower margin. The
worked on the specific status and distribution of Ae. abdomen has dark brown scales on the dorsal surface
esoensis and Ae. cinereus in the eastern Palaearctic (the same colour as on the scutum), without pale trans-
region with findings of transitional forms, but never verse bands. The lateral pale scales on each tergum are
mentioned the characteristic form of the apical fork of fused, forming longitudinal stripes at the sides of the
the gonostylus which is typical for Ae. geminus. It is abdomen, which are hardly visible from above.
most likely that Ae. geminus does not occur in this Male: The general morphology of the hypopygium
region and is distributed mainly in middle and western is very similar to that of Ae. cinereus. A readily visible
Europe (Peus 1972). The species is recorded with cer- difference is the shape of the longer branch of the
tainty from England, northwestern France, Germany, gonostylus, which is never apically bifurcated. It is
Poland, Czech Republic and southern Sweden. It has somewhat flattened distally and rounded at the apex,
also been identified from the southern and eastern and the outer margin has fine spatula shaped serrations
shores of the Baltic Sea (Peus 1972). (Fig. 10.4). The apical part of the gonocoxite, distal to
the point of insertion of gonostylus, tapers more
abruptly and seems to be more slender than in Ae.
Aedes (Aedes) rossicus cinereus. The claspette is divided into two branches,
Dolbeskin, Gorickaja and Mitrofanova 1930

Female: Ae. rossicus is easy to distinguish from the

morphologically similar Ae. cinereus by comparing
the colour of the thorax and the abdomen. In Ae.
cinereus the colour of the scutum is fawn brown with
light brown pleurites, the colour of the abdomen is
dark brown, distinctly different from the colour of the
thorax. In Ae. rossicus, the scutum, the integument of
the pleurites and the abdomen, are more or less of the
same dark brown colour, and the differences in
colouration of the thorax and the abdomen are indis-
tinct. In addition, the scales on the pleurites and the
sterna are pale yellowish or yellowish white in Ae.
cinereus and greyish white in Ae. rossicus, producing a
distinct contrast between the colour of the terga and
sterna in the latter species. The proboscis of Ae. rossi-
cus is dark scaled on its dorsal surface, the ventral sur-
face has mixed pale and dark scales mainly on the
basal half, and the palps are intermixed with pale and
dark scales. The head has narrow pale and broad dark
brown scales on the vertex. The lateral parts of the Fig. 10.4 Hypopygium of Ae. rossicus
10.1 Genus Aedes Meigen 193

the shorter branch is broad with 3–4 setae, two of them waters (Becker and Ludwig 1981). In the inundated
strong and spine-like, and usually stronger than the forests of the Upper Rhine valley, the females are
setae in Ae. cinereus. The longer branch of the clas- severe biters and readily attack humans even during
pette is slender with 1–2 setae. the day. They rarely leave the protected and shaded
Larva (Fig. 10.5): The larva of Ae. rossicus is very areas for host-seeking, their migration range is limited,
similar to that of Ae. cinereus. Both species show sub- thus they are only occasionally found in the open field.
tle differences in certain characteristics, e.g. the point Adults are found during the summer months usually
of origin of the antennal seta (1-A) and the setation of from early May to October. Occasionally single indi-
the prothorax, as indicated in the keys (Fig. 8.22a). viduals can be found in November when other species
Often it is hardly visible and difficult to decide if the of the genera Aedes and Ochlerotatus have already dis-
antennal tuft is located in the middle of the antenna or appeared; apparently they have a higher tolerance
slightly below it, sometimes the prothoracic setae may against the cold. It is assumed that Ae. rossicus pro-
be broken or lost. In these cases one needs to rear the duces several generations per year in the temperate
larvae until the adults are hatched and then differenti- zones, in its more northern distribution range it could
ate between the two species in the adult stage. be less (1 or 2 generations per year). Hibernation takes
Biology: The larvae occur from mid March to early place in the egg stage.
September in small temporary pools, where they can Distribution: The western European range of its
be found together with those of Ae. cinereus and Ae. distribution is not so well known as yet. It is supposed
geminus, but apparently the first generation of Ae. ros- that Ae. rossicus is distributed in the West as far as
sicus occurs earlier in the year than in the two latter the Atlantic Ocean. The species is recorded in
species. Larvae of Ae. rossicus can also be found in Sweden, Norway, France, Germany, Hungary, the
large numbers in the inundation areas of rivers, often Czech Republic, and former Yugoslavia and can be
associated with Ae. vexans and Oc. sticticus. They are found in the Ukraine and north of the Caucasus to the
rarely found in swampy woodlands in acid breeding western slopes of the Ural. In the eastern Palaearctic
it can be found in the northern regions of the Far East.
The record of Ae. rossicus from Japan (Hara 1958)
was based on a misidentification (Tanaka et al.
1975).

10.1.2 Subgenus Aedimorphus Theobald

The females are characterized by the numerous erect

forked scales on the vertex and occiput. The achros-
tichal and dorsocentral setae are well developed and
numerous. The ante- and postpronotum are usually
covered with narrow curved scales, and postspiracular
setae are present. The mesepisternum has several upper
mesepisternal setae, and the mesepimeron has no setae
or scales in its lower part. Sternum VIII has a deep
median V-shaped notch apically, and the cerci are long
and narrow. In males the gonostylus is usually com-
plex with an expanded apical portion, and typical clas-
pettes divided into a stem; and winged filaments are
absent. The antennae of the larvae are moderately pig-
mented and slightly curved distally. The postclypeal
seta (4-C) is very small and usually multiple-branched.
Fig. 10.5 Larva of Ae. rossicus The pecten has 10–23 teeth, distal 2–4 teeth spine-like
194 10 Subfamily Culicinae

and apically detached. The siphonal tuft (1-S) is located erately broad, with scattered scales on the lateral and
well beyond the middle of the siphon. ventral surfaces. The basal and apical lobes are
The structure of the female genitalia and some male absent. The gonostylus gradually expands towards
characteristics resemble the species of the subgenus the apex. The spine of the gonostylus is articulated
Stegomyia; therefore a close relationship between the subapically arising from a small tubercle, and is
two subgenera is assumed. The subgenus Aedimorphus straight (Fig. 10.6). The claspette has a moderately
embraces approximately 110 species and subspecies. broad basal part, and the apex is slightly expanded
The majority of them can be found in the Ethiopian and rounded, with a crown of numerous spine-like
and Oriental regions. Only one species of Aedimorphus, setae, some of them curved apically. The claspette
namely Ae. vexans, occurs in Europe. filament is absent. The paraproct has a pointed apex,
and the aedeagus is strongly sclerotized, with lateral
plates connected at the base.
Aedes (Aedimorphus) vexans (Meigen 1830) Larva: The antenna is less than half as long as the
[Aedimorphus vexans] head, with numerous spicules scattered over the shaft.
The antennal seta (1-A) with 5–10 branches, is inserted
Female: Tarsomeres II and III of the fore legs, tarsom- below the middle of the antenna. The median setae of
eres I–IV of the mid legs, and all the tarsomeres of the the labral brush are serrated apically, a valuable char-
hind legs have narrow basal pale rings which usually do acteristic to distinguish Ae. vexans from the similar
not exceed more than 1/4 of the length of the tarsomeres larvae of Ae. rossicus and Ae. cinereus, both of which
(Fig. 6.27a). Compared to other European Ochlerotatus have simple setae. The frontal setae (5-C to 7-C) are
species with pale rings on the legs, e.g. Oc. annulipes, arranged in a triangular pattern (Fig. 8.21a), the median
Oc. cantans, Oc. flavescens, or Oc. excrucians, the rings frontal seta (6-C) is situated in front of the inner frontal
are much narrower. The proboscis and palps are dark seta (5-C); 5-C has 1–5 branches, 6-C has 1–2 (rarely
scaled, and the palps have some white scales apically. 3) branches, and 7-C has 6–12 (usually 7–9) branches.
The head is covered with narrow curved decumbent pale The comb with 7–13 scales is arranged in 1–2 irregular
and dark scales and numerous dark brown erect forked
scales which extend anteriorly to the interocular space.
The scutal integument is dark brown, and the scutum is
covered with narrow curved dark scales and narrow pale
scales forming indistinct patches on the anterior sub-
median, and prescutellar dorsocentral areas, as well as
on the transverse suture. The acrostichal and dorsocen-
tral setae are well developed. The postspiracular area
has a large patch of narrow curved or moderately broad
pale scales. The upper and lower mesepisternal scale
patches are present. The mesepimeron has a patch of
broad pale scales in the upper part. The tibiae are dark
scaled dorsally and light scaled ventrally. The wing
veins are covered with moderately broad dark scales and
isolated pale scales at the bases of the costa (C) and sub-
costa (Sc). The abdominal terga have white basal bands
with the distal parts dark scaled. The basal bands on
terga III–VI are distinctly narrowed in the middle, form-
ing a bilobed pattern (Fig. 6.27b). Old and worn females,
which have lost most of their scales, can still unequivo-
cally be identified by the distinct V-shaped notch at the
apical margin of sternum VIII.
Male: Tergum IX is strongly bilobed with 6–11
setae on each lobe. The gonocoxite is long and mod- Fig. 10.6 Hypopygium of Ae. vexans
10.1 Genus Aedes Meigen 195

rows (Fig. 10.7). Each comb scale has a long, stout within a few minutes to hours when the flooded water
pointed median spine and small spines at the base. The becomes stagnant and the content of oxygen
siphonal index is usually 2.3–3.0. The pecten has decreases. The hatching behaviour of the larvae is
13–18 teeth, the apical 2–3 teeth are larger than the adjusted to the temporary water conditions. After the
others and detached. The basal teeth are with 1–3 lat- completion of the embryogenesis, which may last
eral denticles. The siphonal tuft (1-S) is situated well 4–8 days (about 1 week at 20°C), not all the larvae
beyond the middle of the siphon, with 3–8 short hatch after flooding, but only a proportion of them
branches, and about half as long as the width of the (“hatching in installments”). If one population of lar-
siphon at the point of origin. The saddle reaches far vae fail to complete the development due to drying
down the sides of the anal segment, and the saddle seta out, a second population can develop during a fol-
(1-X) has 1–2 branches. The ventral brush has pre- lowing flood even if no additional eggs are laid. The
cratal setae (4-X). The anal papillae are distinctly lon- hatching rate is particularly high at high water tem-
ger than the saddle. peratures and after the completion of a diapause,
Biology: Ae. vexans is a polycyclic species pre- which lasts from September to early March of the
dominantly breeding in inundated areas such as following year in temperate zones. If suitable hatch-
floodplains of rivers or lakes with fluctuating water ing conditions fail to exist (e.g. lack of floods during
levels. The preferred breeding sites are temporary summer), the eggs are capable of surviving for a long
water bodies with neutral to alkaline water, which time (at least 5 years).
are present only a few days to weeks after a flood, Ae. vexans as a “summer species” has an optimum
such as flooded meadows, poplar cultures, willow temperature of 30°C for its development. At a water
and reed areas. Usually the larvae hatch in large temperature of 30°C, the development from hatching
numbers if the water temperature exceeds 9°C. In of the first-instars to emergence of the adults lasts 1
central Europe they occur in springtime when the week; at a temperature of 15°C it is 3 weeks. Ae. vex-
typical snow-melt mosquitoes, such as Oc. cantans ans frequently becomes the dominant species during
are already hatched. After ­flooding, the larvae hatch the summer months rich in floods and is often the most
important nuisance mosquito in temperate climate
zones. Often, hundreds of larvae per liter of water can
be encountered, that is frequently > 100 million larvae
per hectare. Owing to the pressure of a large popula-
tion, after mass emergence, the adults frequently
migrate long distances from their breeding sites to find
a host for the blood meal and thus may become a seri-
ous nuisance, not only close to the breeding sites, but
also far away from their breeding waters. A migration
of up to 15 km (according to the circumstances, the
flight capacity is about 1 km/night), occasionally even
a multiple of that, could be proven. The imigration of
females into human settlements, e.g. gardens and
parks, can cause a considerable nuisance. After the
blood meal, the females lay the eggs 5–8 days at the
earliest into damp depressions. A female can lay > 100
eggs after a single blood meal; occasionally after
repeated blood meals, multiple egg batches are laid.
The preferred hosts are mammals. Both females and
males imbibe plant juices in order to cover their energy
requirements. However, no eggs are developed with-
out a blood meal. Under optimum conditions, Ae. vex-
ans needs less than 3 weeks from hatching of one
Fig. 10.7 Larva of Ae. vexans generation to the hatching of the larvae of the next
196 10 Subfamily Culicinae

generation (development in water: approx. 6 days; Aedimorphus, but possessed unique and unusual charac-
­copulation: approx. 2 days; blood meal: approx. 2 days; teristics, that are of subgeneric rank. The combination of
egg development: approx. 5 days and embryogenesis these characteristics distinguishes Fredwardsius from all
about 4 days). It is suspected that only a part of the emi- other subgenera and genera within the tribe Aedini, e.g.
grated population returns to the original breeding sites 2–6 well developed lower mesepimeral setae in the
after the blood meal, while a considerable part of the female, the greatly expanded distal portion of the gonos-
population do not return and lay eggs far away from tylus in the male hypopygium, and the position and
their original breeding sites. Therefore, the migration development of head setae 4-C to 7-C in fourth-instar
leads to a natural regulation of the population densities. larvae. For a more detailed morphological description of
Distribution: Ae. vexans is distributed almost the subgenus, see Reinert (2000a).
worldwide and can be found in nearly every country in
Europe.
Medical importance: Ae. vexans has many attri- Aedes (Fredwardsius) vittatus (Bigot 1861)
butes of an ideal vector species. It is widely distrib- [Fredwardsius vittatus]
uted, can become very abundant, often at the same
time when virus activity is at its peak, it feeds readily Female: The proboscis is as long as the fore femur. Its
on humans and domestic animals, and it has been median part has a band of whitish scales of varying
found naturally infected with various arboviruses width, which is better developed ventrally than on the
(Reinert 1973). Natural infections with western equine dorsal surface. The palps have a few white scales in
encephalomyelitis (WEE) virus, eastern equine ence- the middle and the apex is broadly pale scaled. The
phalomyelitis (EEE) virus and California encephalitis clypeus has lateral patches of white scales. The anten-
(CE) group viruses have been reported from North nae are shorter than the proboscis, and the pedicel and
America (Wallis et al. 1960; McLintock et al. 1970; first flagellomere are white scaled on the median and
Hayes et al. 1971; Sudia et al. 1971). In Europe, Ae. lateral parts. The vertex has decumbent curved black-
vexans is involved in the transmission of Tahyna virus ish brown scales and black, erect forked scales. There
(Aspöck 1965; Mattingly 1969; Gligic and Adamovic are two dorsolateral patches of white decumbent
1976; Lundström 1994). scales behind the eyes. The scutum is mainly covered
Note on systematics: Three subspecies of Ae. vex- with narrow, curved, blackish brown scales. Three
ans, ssp. arabiensis (Patton 1905), ssp. nipponii pairs of prominent silvery whitish spots are present,
(Theobald 1907) and ssp. vexans (Meigen 1830), have located close to the dorsocentral areas (Fig. 6.24a).
been described (Reinert et al. 2009). The anterior two pairs are usually larger than the pos-
terior pair, which is situated close to the wing roots.
All three lobes of the scutellum have broad white
10.1.3 Subgenus Fredwardsius Reinert scales, and a few black scales may be present at the
apex of the middle lobe. Broad white scale patches
The establishment of the monotypic subgenus are present on the ante- and postpronotum, propleuron,
Fredwardsius is based on the type species, Ae. vittatus postprocoxal membrane, and sub- and postspiracular
(Reinert 2000a). The species has long been recognised to areas. The mesepisternum has upper and lower scale
not fully conform to any recognised subgenus of Aedes. patches. The mesepimeral patch is located in the upper
Edwards (1932) included Ae. vittatus in the subgenus part of the mesepimeron. The femora of all the legs
Stegomyia Theobald and placed it in a monotypic group have a white ring close to their apices and white knee
(Group D), apart from other species of the subgenus. spots, and the hind femur is more extensively white
Later on, Huang (1977) transferred Ae. vittatus from scaled at the base. The hind tibia has a distinct median
subgenus Stegomyia Theobald to subgenus Aedimorphus white ring. The tarsi of the fore and mid legs have nar-
Theobald, mainly based on the structure of the male row white basal rings on tarsomeres I–III, and tarsom-
hypopygium. After a comparison of Ae. vittatus with all eres IV and V are entirely dark. The tarsi of the hind
currently recognised subgenera and genera in the tribe legs have broad white basal rings on tarsomeres I–IV,
Aedini, Reinert (2000a) found the species shared some but tarsomere V is entirely white scaled. The wing
characteristics with the subgenera Stegomyia and veins are mainly dark scaled, with a few broad white
10.1 Genus Aedes Meigen 197

scales at the base of the costa (C) and a few scattered of the antennal shaft, usually with 2–3 branches
white scales on the costa (C) and radius (R). The (Fig. 8.62a). The postclypeal seta (4-C) has 2–3
abdominal terga are predominantly covered with black branches, the inner and median frontal setae (5-C and
scales. Tergum I has a median longitudinal white band 6-C) are single, and the outer frontal seta (7-C) has 5–7
extending to near the apical margi, terga II–VII have branches. The comb consists of 6–9 (usually 8) large
narrow white basal bands, and lateral curved white comb scales, each scale with a long, pointed median
markings separated from the basal bands. Sterna I–VI spine and a few thin, short spines close to its base. The
have lateral and central areas of scattered white scales, siphon is sclerotized along its entire length, except for a
and sternum VII is extensively white scaled. Sternum very small area at the extreme base, and the acus is
VIII has a deep notch at the middle, and the cerci have indistinct. The siphon slightly tapers towards its apex
dark scales. (Fig. 10.9). The siphonal index is 2.0 or slightly more.
Male: Tergum IX is narrowed in the middle, with a The pecten usually has 15–25 well sclerotized teeth,
distinct setose lobe on each side. The gonocoxite is occupying about 2/3 of the length of the siphon. The
elongate, and about three times as long as it is wide at distalmost pecten tooth is spine-like, and apically
its base, without distinct basal and apical lobes detached (Fig. 8.62b). The siphonal tuft (1-S) is situ-
(Fig. 10.8). The gonostylus has a very characteristic ated below the distalmost pecten tooth, with 3–6
shape, being greatly expanded apically. The apical branches, which are about as long as the width of the
spine is situated at the base of the expanded apical part, siphon at the point of origin. The saddle seta (1-X) is
and is long and strongly curved. The claspette is large, short and single. The upper anal seta (2-X) has 4–6
with a narrow base, is distinctly swollen from about branches, and the lower anal seta (3-X) is single and
the middle, and is covered with numerous small setae. long. The ventral brush has 5–7 tufts of cratal setae
The aedeagus is small with several well developed (4-X) and 3–4 tufts of precratal setae. The anal papillae
recurved teeth on the lateral and apical parts. are more than twice as long as the saddle, and pointed.
Larva: The antenna is slightly more than half as Biology: Females prefer to lay their eggs above
long as the head, and is covered with very small spic- the water level of rock pools, occasional utensils,
ules, although sometimes the antenna is smooth. The boats, wells, or tree-holes (Mattingly 1965). Boorman
antennal seta (1-A) is situated slightly below the middle (1961) found that deep rock holes usually contained

Fig. 10.8 Hypopygium of Ae. vittatus Fig. 10.9 Larva of Ae. vittatus
198 10 Subfamily Culicinae

larvae of Ae. vittatus, particularly those where the narrow scales on all the veins. The abdominal terga have
water was clear and the bottom covered with a layer white basal bands and often white lateral spots, and the
of mud and a few dead leaves. Ae. vittatus is particu- cerci are relatively short. In the male genitalia, the basal
larly well suited to such an environment, as its eggs and apical lobes of the gonocoxite are absent. The gono-
can tolerate desiccation for many years, and the very stylus is usually simple and elongated, or sometimes it
rapid larval development minimizes the likelihood of is expanded apically or at the base. Typical claspettes,
the immature stages being killed by the pools drying which are divided into a stem and a filament are modi-
out. In Nigeria, larval and pupal development were fied into a structure which is usually lobed, and located
completed within 6 days (Service 1970a). Larvae of at the base of the gonocoxite and covered with numer-
Ae. vittaus were found in rock pools in association ous setae. The aedeagus is divided into two plates and is
with those of Cx. hortensis, Cx. mimeticus, An. clavi- strongly toothed apically. In the larvae, the antennae are
ger, and Cs. longiareolata. In France, Ae. vittatus is without spicules, the antennal seta (1-A) is usually small
mainly a crepuscular species, but its biting activity and single. The postclypeal seta 4-C is well developed
continues during most of the night (Rioux 1958). In and branched, and the median frontal setae (6-C) are
the Mediterranean region, the species is found from situated in front of the inner frontal setae (5-C). The
late spring to early autumn. Its seasonal incidence comb scales are arranged in a single row, and the base of
depends both on local rainfall and on the water level the siphon has no acus. The ventral brush has 8–10
of rivers. There are records of equal biting intensity cratal seate (4-X) on a common base, without any pre-
both indoors and outdoors. Ae. vittatus females some- cratal setae.
times attack humans in large numbers (Gutsevich The subgenus is confined to the Old World and
et al. 1974). mainly occurs in the tropical and subtropical zones
Distribution: Mediterranean subregion, Afro-tropical throughout this region, except Ae. aegypti and Ae.
and Oriental regions. Its northernmost distribution range albopictus which have been introduced through com-
is probably limited by the 10°C isotherm. Even if the merce into the New World. It seems that in Stegomyia
species can survive cold winters in the north, summer there are a few widely distributed species and a num-
temperatures must be sufficiently high to enable the ber of specialized endemic species (Huang 1979). In
completion of at least one gonotrophic cycle. Europe the subgenus is represented (or was partly rep-
resented in the past) by three species which could be
found in the southern countries of the continent. In the
family Culicidae the subgenus Stegomyia is one of the
10.1.4 Subgenus Stegomyia Theobald
most important subgenera in view of the transmission
of pathogens and parasites, it includes several vectors
Members of this subgenus are rather small, rarely of human filiariasis and a number of severe viral
medium sized mosquitoes. According to Gutsevich diseases.
et al. (1974) and Huang (1979) the following combina-
tion of characteristics can be found within species of
Stegomyia. The male palps are more than half the length Aedes (Stegomyia) aegypti (Linnaeus 1762)
of the proboscis, often slightly longer than the probos- [Stegomyia aegypti]
cis, and with 5 palpomeres. The female palps are up to
1/4 the length of the proboscis, 4- or sometimes 5-seg- Female: A medium sized dark species with contrast-
mented and when present, palpomere V is minute. The ing silvery white ornamentation on the head, scutum,
vertex is largely covered with broad and flat decumbent legs, and abdomen. Ae. aegypti is easily recognised
scales, erect forked scales are not numerous and and distinguished from the other members of the sub-
restricted to the occiput. The scutum has a characteristic genus by the white scutal markings which form the
pattern of light scales for each species. The acrostichal typical “lyre-shaped” pattern of the species (Fig. 6.25a).
and spiracular setae are absent, and postspiracular setae The proboscis is dark scaled, the palps 1/5 the length
present. The scutellum has broad scales on all the lobes, of the proboscis with white scales on the apical half,
and the postnotum is bare. The hind tarsus has a basal the clypeus with lateral white scales, and the pedicel
white ring at least on tarsomere I, and the wings have with large patches of white scales at the sides. The
10.1 Genus Aedes Meigen 199

v­ ertex has a median line of broad white scales from the Male: The palps are as long as the proboscis with
interocular space to the back of the occiput, and white white basal rings on palpomeres II–V. The last two
scales also on the sides, separated by patches of dark segments are slender and upturned with only a few
scales. Erect scales are restricted to the occiput, and short setae. The posterior margin of tergum IX is
are all pale. The scutum is predominantly covered with deeply concave in the middle, and the lateral lobes are
narrow dark brown scales, with a distinctive pattern of prominent with 3 apical setae. The gonocoxite is
light scales as follows: a small anteacrostichal patch slightly more than twice as long as wide, with scales
of white scales, a pair of narrow dorsocentral stripes of restricted to the lateral and ventral surfaces (Fig. 10.10).
narrow pale yellowish scales close to the midline The gonostylus markedly narrows apically and is
extending to the anterior 2/3 of the scutum, a short curved, with a pointed apical spine (Fig. 7.20c). The
postacrostichal stripe of white scales just in front of claspettes are large, lobe-like, appressed to and occupy
the prescutellar area where it forks forming prescutel- most of the mesal surface of the gonocoxite, with
lar dorsocentral stripes which end at the margin of the numerous setae and several stronger setae, 3 or 4 of
scutellum, broad lateral presutural stripes which con- which are bent at the tip. The paraproct has an inwardly
tinue over the transverse suture covered with crescent- directed mesal arm, and the aedeagus is strongly
shaped white scales followed by submedian stripes of serrated.
narrow white scales reaching the posterior margin of Larva: The antennae are about half as long as the
the scutum, and a patch of broad white scales on the head and without spicules. The antennal seta (1-A) is
lateral margin just in front of the wing root. The scutel- small and single, and inserted slightly beyond the
lum has broad white scales on all the lobes and a middle of the antennal shaft. The postclypeal (4-C)
few broad dark scales at the apex of the mid lobe and median frontal (6-C) setae are displaced far for-
(Fig. 6.23a). The postpronotum has a patch of broad ward toward the anterior margin of the head. 4-C is
white scales and some dark and pale narrow scales in situated slightly anterior to 6-C, and is well developed
the upper part, and the paratergite has broad white with 4–7 short branches. The frontal setae (5-C to
scales. The postspiracular area is without scales, but 7-C) are long and single (Fig. 8.60a), and the outer
there are patches of broad white scales on the propleu- frontal seta (7-C) very rarely have 2 branches. At the
ron, and subspiracular and hypostigmal areas. base of the meso- and metathoracic setae (9-M to
Mesepisternal and mesepimeral patches are present, 12-M and 9-T to 12-T) there is a long stout spine
divided into an upper and lower portion, but not con- which is pointed and hooked at the tip. The comb con-
nected. The upper mesepisternal scale patch does not sists of a single irregular row of 6–12 scales, each
reach the anterior corner of the mesepisternum. The
mesepimeron has no lower mesepimeral setae. The
coxae have patches of white scales, and all femora
have white knee spots, the fore and mid femora with a
narrow white longitudinal stripe on the anterior sur-
face. All the tibiae are dark anteriorly, the fore and mid
tarsi have a white basal band on tarsomeres I and II,
the hind tarsus has a broad basal white band on tarsom-
eres I–IV, and tarsomere V is all white. The claws of
the fore and mid tarsi have a subbasal tooth, and the
claws of the hind tarsi are simple. The wing veins are
all dark scaled except for a small spot of white scales
at the base of the costa (C). Tergum I has white scales
laterally and a median pale patch, terga II–VI have
basal white bands and basolateral white spots separate
from the bands, and tergum VII has lateral white spots
only. Sterna II–IV are largely pale scaled, V and VI
have predominantly dark scales, and VII is dark except
for a small lateral pale patch. Fig. 10.10 Hypopygium of Ae. aegypti
200 10 Subfamily Culicinae

comb scale has a long median spine and strong smaller collection in harbors and on ships. The breeding water
spines at the base forming a “triffid” appearance. The is mostly clean or has a moderate content of organic
siphon is moderately pigmented, the siphonal index is matter. The larvae spend a long time under water feed-
about 1.8–2.5, and the acus is not developed ing on the bottom of their breeding sites. The eggs are
(Fig. 10.11). The pecten has 8–22 teeth (usually resistant to desiccation and are deposited close to the
10–16), evenly spaced or sometimes the distalmost waterline in the mentioned recipients. At a tempera-
tooth is detached apically, and each tooth has 1–4 lat- ture of 27–30°C the larvae will hatch 2 days after egg
eral denticles. The siphonal tuft (1-S) has 3 or 4 deposition, pupation occurs after 8 days and the adults
branches, usually inserted close to the distal pecten emerge from the pupae 9–10 days after the eggs have
tooth and just beyond the middle of the siphon. The been laid. The females feed predominantly during the
saddle reaches far down the lateral sides of the anal day in shaded places and only occasionally during the
segment, the saddle seta (1-X) usually has 2 short night in lit rooms. Human blood seems to be preferred
branches. The ventral brush has 8–10 tufts of cratal to that of domestic animals (Carpenter and La Casse
setae (4-X), and the precratal setae are absent. The 1955); the blood feeding interval is only about 2–4
anal papillae are about 2.5–3 times the length of the days. The adults are frequently found resting indoors,
saddle, sausage-like, and rounded apically. e.g. in cupboards, closets or behind doors. They do
Biology: In subtropical climates the species is not migrate over long distances, and rarely fly more
found almost always in the close vicinity of human than several hundred meters from their breeding sites.
settlements. The larvae occur in a wide variety of The species is supposed to have had its origin in Africa
small artificial containers and water recipients of all and subsequently spread over vast areas, mainly the
kinds, both inside and outside of human habitations in Tropics.
gardens and within a radius of 500 m around dwell- Ae. aegypti is one of the most suitable mosquitoes
ings, e.g. in earthenware pots and water tanks for stor- for laboratory colonies and has been extensively used
ing water, uncovered cisterns, rainfilled empty cans or as a test organism for laboratory research in many
flower pots, broken bottles or discarded motor vehicle fields. At a constant rearing temperature of 22–28°C
tyres. If vegetation surrounds the settlements, the lar- the species has some outstanding advantages in respect
vae may breed in tree-holes, leaf axils, bamboo of colonization: the adults and larvae are easy to han-
stumps, or coconut shells after heavy rainfall. They dle, rearing is possible in nearly every type of cage and
can also be found in any artificial and natural water breeding container, and mating takes place even in the
smallest space. The females readily feed on a variety
of small mammals offered as a blood source and the
eggs can be stored for months, if necessary, without
losing viability. The available literature about Ae.
aegypti, its biology and medical significance is numer-
ous; a well recognised monograph was published by
Christophers in 1960.
Distribution: This cosmotropical species is distrib-
uted in the tropical, subtropical, and warm temperate
regions of both hemispheres. Its range is mainly lim-
ited by the 10°C cold-month isotherms where breeding
can continue all year round (Christophers 1960).
Certain populations may extend their summer range
considerably north of this line, e.g. in North America
specimens may be found at the 40° northern latitude in
southern Illinois and Indiana, but they are not able to
survive during cold winter months; this prevents the
establishment of permanent populations. In Europe,
prior to 1945, all Mediterranean countries and most
Fig. 10.11 Larva of Ae. aegypti major port cities had reported at least occasional
10.1 Genus Aedes Meigen 201

introductions of Ae. aegypti (Mitchell 1995). It could supraalar white stripe is incomplete, there is a patch of
be found in Portugal, Spain, France, Italy, former broad white scales on the lateral margin just before the
Yugoslavia, Greece and Albania, but has now been level of the wing root and a few narrow white scales
eradicated or has become rare in many countries where over the wing root. The scutellum has broad white
it was previously common. scales over all the lobes with an apical area of dark
Medical importance: As the major vector of yel- scales on the mid lobe. The postpronotum has a large
low fever virus, Ae. aegypti has long been notorious patch of broad white scales and some narrow dark ones
as the “yellow fever mosquito”, but it is also an in the upper part, and the paratergite has broad white
important vector of dengue and several other viral scales. The postspiracular area is without scales, and
infections. the subspiracular area has white scales. The mesepis-
Synonymy: The species in question has appeared ternal patch is divided into large upper and lower
under various other names in the past. The number of patches of white scales. The mesepimeron has con-
names, which are now accepted as synonyms is large nected upper and lower scale patches which form a
and listed in Knight and Stone (1977). Synonyms that V-shaped white scale patch, with the open V directed
are often found in the early literature are Stegomyia backwards. The coxae have patches of white scales,
fasciata of Theobald 1901 (described as Culex fas- the fore and mid femora are dark anteriorly and paler
ciatus by Fabricius 1805), Aedes calopus Meigen posteriorly with apical pale spots. The hind femur has
1818, and Aedes argenteus of Edwards 1921 a broad white longitudinal anterior stripe widening at
(described as Culex argenteus by Poiret 1787). From its base and slightly separated from the apical white
about 1935 on, the earliest name, aegypti given by scale patch. The tibiae are all dark. The fore and mid
Linnaeus in 1762, was accepted and is in general use tarsi have narrow basal white bands on tarsomeres I
until today. and II, the hind tarsus has broad basal white bands on
Note on systematics: A paler variation of the type tarsomeres I–IV, and tarsomere V is all white. The
form, var. queenslandensis (Theobald) exists and a claws are simple without a subbasal tooth. The scales
subspecies formosus (Walker) is characterized through on the wing veins are all dark except for a small spot of
its markedly darker appearance. The latter form is con- white scales at the base of the costa (C). Tergum I has
fined to Africa south of the Sahara and has been white scales laterally, terga II–VII have basolateral
recorded from the forest or bush away from human white spots. In addition, terga III–VI have narrow basal
settlements, breeding in natural places. white bands, which widen laterally and do not connect
with the spots.
Male: The palps are longer than the proboscis with
Aedes (Stegomyia) albopictus (Skuse 1895) white basal rings on palpomeres II–V. The last two
[Stegomyia albopicta] segments are slender and upturned with only a few
short setae. The posterior margin of tergum IX has a
Female: The proboscis is dark scaled, about the same conspicuous horn-like median projection and a small
length as the fore femur, and the palps are 1/5 the setose lobe on each side. The gonocoxite is approxi-
length of the proboscis with white scales on the apical mately twice as long as wide with a patch of setae on
half. The clypeus is bare and entirely dark. The vertex the basomesal area of the dorsal surface (Fig. 10.12).
has broad white scales, and the occiput in the middle is The gonostylus is simple, elongated, distinctly swollen
white scaled with dark scales at the sides; erect scales apically and has a few thin setae. The spine of the
are usually absent. The scutum is mainly covered with gonostylus is inserted subapically and is blunt ended.
narrow dark scales, with a prominent acrostichal stripe The claspettes are large, lobe-like, and occupy most of
of narrow white scales which narrows posteriorly, and the mesal surface of the gonocoxite, with numerous
extends from the anterior margin of the scutum to the long setae and several stronger setae, a few of which
beginning of the prescutellar area where it forks to the are curved apically.
end at the margin of the scutellum (Fig. 6.26a). On Larva: The head is approximately as long as it is
each side a slender posterior dorsocentral white stripe wide. The antennae are about half as long as the head,
does not reach the middle of the scutum, but extends and without spicules. The antennal seta (1-A) is single
about midway to the level of the scutal angle. The and small and situated close to the middle of the antennal
202 10 Subfamily Culicinae

Fig. 10.12 Hypopygium of Ae. albopictus

Fig. 10.13 Larva of Ae. albopictus

shaft (Fig. 8.62c). The postclypeal seta (4-C) is located Biology: The immature stages occur in a variety of
close to the anterior margin of the head. It is well devel- small natural and artifical containers, e.g. in tree-holes,
oped with 6–15 branches and a short stem. The median bamboo stumps, coconut shells, rock holes, plant axils
frontal seta (6-C) is displaced anteriorly, and has 1–2 or palm fronds, and in flower pots, tin cans, water jars,
branches, the inner frontal seta (5-C) is situated poste- metal and wooden buckets or drums, broken glass bot-
rior to 6-C, and is longer and single, and the outer fron- tles, or discarded motor vehicle tyres (Huang 1972).
tal seta (7-C) usually has 2–3 branches. The comb The eggs are resistant to desiccation, which facilitates
consists of 6–13 (usually 8–10) long slender scales in a their transport in used tyre casings, even over long dis-
single row, and each comb scale has a large pointed tances. Continuous breeding throughout the year takes
median spine and fine denticles or fringes at its base. place in tropical and subtropical areas, but in more
The siphon is short and tapers distinctly from the mid- temperate climatic zones, such as Europe, populations
dle, the siphonal index is 1.7–2.5 (Fig. 10.13). The of Ae. albopictus are found which show embryonic
number of pecten teeth is between 8 and 14, they are diapause and overwinter in the egg stage. Several gen-
evenly spaced, and each tooth usually has 2 lateral den- erations per year may occur. Adult females predomi-
ticles. The siphonal tuft (1-S) has 2–4 branches, and is nantly feed on humans, but may also bite other
inserted beyond the distalmost pecten tooth, slightly mammals including rabbits, dogs, cows and squirrels
beyond the middle of the siphon (Fig. 8.62d). The sad- or occasionally avian hosts, e.g. Passeriformes or
dle extends to the ventral margin of the anal segment, Columbiformes. This feeding behaviour indicates that
and the saddle seta (1-X) usually has 2 branches, at Ae. albopictus is well suited for transmission of a vari-
least one of them distinctly longer than the saddle. The ety of arboviruses that use mammals and birds as their
upper anal seta (2-X) has usually 2 branches, which are main hosts (Mitchell 1995). To feed on humans the
rarely single, but the lower anal seta (3-X) is single. females readily enter dwellings during dusk and night,
The ventral brush has 8 tufts of cratal setae (4-X), but but may also be found biting during daytime outside
the precratal setae are absent. The anal papillae are houses in shaded areas. Ae. albopictus is an abundant
sausage-like, and about 8 times the length of the species in East Asia causing great nuisance wherever it
saddle. occurs and, although it was not present before 1990, it
10.1 Genus Aedes Meigen 203

has become a major pest species in some areas of whitish scales dorsally on the apical half and dark
northern Italy. scales ventrally. The clypeus is bare, and the pedicel
Distribution: In the past Ae. albopictus was mainly has white scales anteriorly. The vertex has a broad
distributed in the Oriental Region and Oceania and median stripe of broad white scales, and the occiput
thus it got its popular name, the “Asian Tiger Mosquito”. has a lateral stripe of broad white scales and extensive
In the Palaearctic it occurred in Japan and China. In broad white scaling below, all dark scales are broad
1985 it was discovered for the first time in the New and flat. There are narrow white scales at the eye mar-
World (Houston, Texas) and this was the beginning of gin, and the erect forked scales are dark. The scutum
a rapid spread and discovery of recently introduced has narrow dark scales, and an acrostichal stripe of
populations of Ae. albopictus in many parts of the narrow white scales extends from the anterior margin
world (Mitchell 1995). It is now present in over 25 to the beginning of the prescutellar area, where it forks
states of the USA and in several countries of South and ends just before the margin of the scutellum
America and Africa. Specimens have been found in (Fig. 6.26b). Dorsocentral white stripes are present on
Australia and New Zealand, but breeding populations the posterior part of the scutum extending from just
have not so far become established there. In Europe, posterior to the level of the scutal angle to near the
Ae. albopictus has probably been present in Albania lateral lobes of the scutellum; these stripes are narrow
since at least 1979 (Adhami and Reiter 1998; Adhami and composed of narrow white scales. The scutum is
and Murati 1987). In the early 1990s it was passively bordered with a lateral prescutal stripe of narrow white
introduced in Italy, owing to the international trade of scales which reaches the scutal angle, where after a
used tyres which provide a suitable habitat for the eggs. minute break it continues on with broad white scales
The species was first detected in Genoa in September and terminates with a few narrow white scales just
1990 (Dalla Pozza and Majori 1992) followed by a before the margin of the lateral lobes of the scutellum.
rapid spread into other areas of northern and central The scutellum has broad white scales on all the lobes
Italy (Romi 1995). Since 1999 Ae. albopictus has been and a small apical area of dark scales on the mid lobe.
found in various southern and central European coun- The ante- and postpronotum are largely covered with
tries, including France (Schaffner et al. 2001), Montenegro broad white scales. The pleurites have several patches
(Petric et al. 2001), Belgium (Schaffner et al. 2004), of broad white scales, some of them very densely
Switzerland (Flacio et al. 2004), Greece (Samanidou- scaled. The wing veins are dark scaled except for a
Voyadjoglou et al. 2005), Croatia (Klobucar et al. conspicuous basal spot of pale scales on the costa (C).
2006), Spain (Aranda et al. 2006), the Netherlands The fore femur anteriorly has sparse white scales on
(Scholte et al. 2007), and Germany (Pluskota et al. the basal half and a small white knee spot, posteriorly
2008). Another way in which the eggs and larvae of it is white and the fore tibia is dark. The fore tarsom-
Ae. albopictus spread was through the trade of the eres I and II have basal white rings, and tarsomeres
ornamental plant Dracaena sp. (“lucky bamboo”). III–V are dark. The mid femur is dark anteriorly except
These plants are packaged in standing water during for a few white scales at the base and a conspicuous
shipment and permit an “ideal insectary in transit” white knee spot, the mid tibia is dark, the mid tarsom-
which lead to the introduction of Ae. albopictus from eres I and II with basal white rings, tarsomeres III–V
Asia to California (Madon et al. 2004). dark. The hind femur anteriorly is white almost to its
Medical importance: Ae. albopictus is a vector of apex and has a conspicuous white knee spot, the hind
dengue viruses and a competent transmitter for numer- tibia is dark, and hind tarsomeres I–III have a basal
ous other arboviruses as well as Dirofilaria immitis white ring, and hind tarsomere IV has an extreme tip
(dog heartworm). which is dark, but tarsomere V is white. Abdominal
terga II–IV have narrow white basal bands slightly
constricted in the middle and not connected to the
Aedes (Stegomyia) cretinus Edwards 1921 broad lateral white patches. Sterna II–IV are largely
[Stegomyia cretina] covered with white scales, and sterna V–VII with basal
white bands.
Female: The proboscis is completely dark scaled, the Male: The median part of tergum IX is evenly
palps are about 1/4 the length of the proboscis with rounded, and the small lateral lobes are strongly
204 10 Subfamily Culicinae

Fig. 10.15 Larva of Ae. cretinus

Fig. 10.14 Hypopygium of Ae. cretinus Biology: Little appears to be known about the biol-
ogy of Ae. cretinus (Lane 1982). Gutsevich et al.
(1974) reported that larvae were found in tree-holes
sclerotized with 2–4 fine setae. The gonocoxite is together with those of An. plumbeus, Oc. geniculatus,
oblong, the gonostylus is long and slender, and and Or. pulchripalpis and that adult females were bit-
dilated at the apex where it bears a number of fine ing humans in shaded areas.
setae and a long, slender subapical spine Distribution: Cyprus, Greece, Crete, Georgia and
(Fig. 10.14). This spine is markedly longer and Turkey.
more slender than that of Ae. albopictus (Mattingly
1954). The claspettes narrow apically, and are cov-
ered with setae of varying length, but no special-
 enus Ochlerotatus
10.2 G
ized setae are present.
Larva: The antenna is smooth, and the antennal Lynch Arribalzaga
seta (1-A) is minute and single, located at just beyond
midway from the base. The outer frontal seta (7-C) is This genus was established by the division of the com-
single. The comb has 9–13 scales arranged in one row posite genus Aedes into 2 genera, Aedes and
with exceedingly minute basal denticles. The siphonal Ochlerotatus, and restoration of the former subgenus
index is about 2.0 (Fig. 10.15). The pecten has 10–13 Ochlerotatus of genus Aedes to generic rank. A further
teeth, some with the main denticle longer and more subdivision of Ochlerotatus into two sections is pro-
finely drawn out. The siphonal tuft (1-S) has 3 branches, posed (Reinert 2000c). This classification is primarily
located near the middle of the siphon with a single seta based on female and male genitalic charactristics, e.g.
situated laterally in the apical third (Fig. 8.61a). The the aedeagus in the male hypopygium consisting of
saddle reaches the ventral margin of the anal segment two lateral plates that usually bear teeth laterally and/
and has a smooth distal edge, the saddle seta (1-X) is or apically in Aedes, and the aedeagus being simple
single or 2-branched, the upper anal seta (2-X) has 2–3 and scoop-like, trough-like, or tube-like in Ochlerotatus.
branches, and the lower anal seta (3-X) is single. The Supplemental features supporting the partition of the
anal papillae are longer than the saddle, but at most 2/3 genera include characteristics of the fourth-stage larvae
of the length of the siphon. and pupae. For a detailed morphological description
10.2 Genus Ochlerotatus Lynch Arribalzaga 205

and delimitation of Aedes and Ochlerotatus, see Reinert European species, Oc. echinus and Oc. geniculatus,
(2000c). Of the European mosquito species, members really belong to Finlaya.
of the subgenera Finlaya, Ochlerotatus and Rusticoidus
are included in Ochlerotatus, all of which belong to
Sect. 10.1.
Ochlerotatus (Finlaya) echinus Edwards 1920
[Dahliana echinus]

10.2.1 Subgenus Finlaya Theobald Female: Closely related to Oc. geniculatus with a
­similar morphology in all stages. The female of Oc.
The subgenus comprises medium to large species. echinus differs from that of Oc. geniculatus by the pat-
The length of the palps in the females ranges from terns of scaling on the head, thorax, abdomen and legs.
very short to 2/3 the length of the proboscis. The head The proboscis and palps are dark scaled, the head has
has a mixture of narrow and broad scales, with erect black setae, the scales on the vertex are dark and with
forked scales on the vertex and occiput. The scutum lateral white patches, and there is no white scale bor-
has prominent white and dark scale patterns and vari- der around the eyes. The scutum has two dorsocentral
able setation, the dark scales are black or have a stripes of narrow dark bronze scales divided by a
metallic tinge. The pleurites have patterns of white creamy white acrostichal stripe. The supraalar dark
scales, and are more extensively scaled in females scale patch is nearly fused with the dorsocentral stripes.
than in males. The mesepimeral setae are sometimes The scutellum has broad whitish scales. The postpro-
absent. White knee spots are present, and all tarsom- notal scales are whitish, and the mesepisternum and
eres are dark. The wing veins are covered with dark mesepimeron have patches of creamy scales, distinct
scales. The abdominal terga have more or less dis- against the dark integument. The femora have a white
tinct lateral white patches, sometimes with white ventral stripe and white knee spot. The tibiae and tar-
basal bands, and the cerci are short and blunt. The someres are entirely black scaled. The wings have
length of the male palps varies from half the length of rather narrow blackish scales. The abdominal terga are
the proboscis to much longer than it. Tergum IX has dark scaled with narrow white basal bands, sometimes
well developed lobes and more or less spine-like interrupted in the middle from tergum V on, and on all
setae. The hypopygium has an elongated gonocoxite, segments extended laterally into triangular whitish
without distinct basal or apical lobes but defined patches. Abdominal segment VIII is broad, and the
fields of setation. The gonostylus is long and slender, cerci are short and rounded.
and the claspette is divided into a stem and a filament Male (Fig. 10.16): The general shape of the hypopy-
of different shapes. The paraproct is usually heavily gium is similar to that of Oc. geniculatus except for the
sclerotized, and the aedeagus is pear shaped. The denser setation of the gonocoxite toward the tip. The
head of the larva is rounded, and the antenna is usu- claspette stem has a stout seta near the middle and
ally shorter than the head, with a single antennal seta some thin setae at the base, and the claspette filament
(1-A). The frontal setae (5-C to 7-C) are single or is hook-like.
may have 2 branches. The abdominal segments are Larva: The antenna is more than half as long as the
usually covered with stellate setae. The comb scales head (longer than in Oc. geniculatus), smooth and is
are large and arranged in a single row. The saddle not covered with spicules. The antennal seta (1-A) is
does not encircle the anal segment, and precratal tufts single (Fig. 8.58a). The inner frontal seta (5-C) is sin-
are present. The ventral and dorsal anal papillae are gle, the median frontal seta (6-C) is single or double
of different sizes. and the outer frontal seta (7-C) usually has 2–4
The subgenus with its nearly 200 species is one of branches. Branches of the stellate setae on abdominal
the largest in the genus Ochlerotatus. It is mainly dis- segment I are longer than the length of the segment
tributed in Asia, Australia, and Africa. It is a polymor- (Fig. 8.59a). The number of comb scales is 11–18,
phic subgenus of which a species of North and South arranged in one row. Each scale is elongated with
America has been revised and placed in other ­subgenera ­lateral spines, and a prominent median spine is absent.
(Zavortink 1972). It is doubtful whether the two The siphonal index is 2.5–3.6, and the acus is well
206 10 Subfamily Culicinae

Fig. 10.17 Larva of Oc. echinus

of Oc. geniculatus also apply to Oc. echinus. As the

types of most of the synonymous species of Oc. genicu-
latus are lost, apparent synonymy to Oc. echinus is not
resolved. From Madeira and the Canary Islands another
species within the subgenus Finlaya, Oc. eatoni
Edwards, has been reported (Knight and Stone 1977).
Fig. 10.16 Hypopygium of Oc. echinus

developed (Fig. 10.17). The pecten has 15–27 teeth Ochlerotatus (Finlaya) geniculatus (Olivier 1791)
and occupies at least the basal half of the siphon, each [Dahliana geniculata]
tooth is very long and spine-like. The siphonal tuft
(1-S) is inserted beyond the middle of the siphon, with Female: Dark scales with a violet tinge especially on
2–4 branches. The anal segment is not entirely encir- the abdomen, the white and blackish pattern of the
cled by the saddle, and 1–2 precratal tufts (4-X) are scutum, the conspicuous white knee spots and the
present. The anal papillae are broad and long, and the blunt cerci immediately distinguish the females from
dorsal pair is twice as long as the ventral pair. all other females of the genus Ochlerotatus except the
Biology: Larvae have been found in the same habi- closely related Oc. echinus. The proboscis and palps
tats as Oc. geniculatus. In Anatolia and Bulgaria they are black scaled, and the vertex is dark with a median
may also occur in root holes of olive trees. Not much light stripe and a narrow band of whitish scales around
is known of the biology of the larvae, they are sup- the eyes. The scutum has two dorsocentral black stripes
posed to feed on microorganisms in the tree-holes in which sometimes fuse into one anteriorly, or are other-
the same way as the larvae of Oc. geniculatus do. In wise completely separated by a pale acrostichal stripe.
Portugal, larvae and adults were found in August and The submedian and lateral areas of the scutum have
September (Ribeiro et al. 1988). creamy or silvery grey scales. Dark anterior and poste-
Distribution: In Europe this species is confined to rior submedian stripes are present, and the scutellum
the Mediterranean region and has been reported in has narrow yellowish scales. The pleurites have patches
Portugal, Italy, Greece, and Bulgaria where it has been of broad, whitish scales. The legs are dark, the femora
found in abundance along the Black Sea coast. have a white knee spot, and the tibiae and tarsomeres
Note on systematics: Edwards (1920) originally are entirely black scaled. The fore and mid claws have
placed this species in the subgenus Ochlerotatus and a subbasal tooth. The wing veins are covered with dark
transferred it to Finlaya later (Edwards 1932). The brownish scales. The abdominal terga are black scaled
same considerations regarding the subgenus affiliation with conspicuous white triangular lateral patches on
10.2 Genus Ochlerotatus Lynch Arribalzaga 207

segments II–VII. Sternum VIII is unusually broad, and type. The branches of the stellate setae on abdominal
the cerci are broad and rounded (Fig. 6.37a). segment I are about the same length as the segment
Male: Tergum IX has somewhat elongated lobes (Fig. 8.59c). The number of comb scales is 8–15
and 4–5 spine-like setae on each lobe. The hypopy- arranged in a single row. Each individual scale is
gium superficially resembles that of the species of the elongated with a swollen base, a strong median spine,
Ochlerotatus Excrucians Complex by lacking a basal and small lateral spines at the base. The siphonal
lobe, but is distinguished from it by the absence of an index is 2.3–3.2 (Fig. 10.19). The number of pecten
apical lobe (Fig. 10.18). The long and evenly tapered teeth is 15–19, and each tooth is long, spine-like, with
gonocoxite has two areas of dense setation, a basal one a few indistinct denticles at the base. The pecten usu-
with shorter setae, and an apical one with long setae. ally occupies less than the basal half of the siphon.
The claspette stem is short with several setae, and the The siphonal tuft (1-S) is situated at about the middle
filament is narrow and somewhat shorter than the stem. of the siphon or slightly below it, with 4–5 branches.
The paraproct is heavily sclerotized and bent at the tip, The anal segment X is not completely encircled by
and the aedeagus is pear shaped. the saddle, and the latter has a row of long microtri-
Larva: The larvae are distinguished from those of chiae at the distal part. The ventral brush is made up
all other subgenera of Aedes and Ochlerotatus (except of 7–10 cratal tufts (4-X) and 1–2 precratal tufts. The
Oc. echinus) by the numerous stellate setae on the anal papillae are broad and longer than the saddle,
thorax and abdomen, the broad and unequally long with the ventral pair being shorter.
anal papillae and the single row of large comb scales. Biology: The larvae live in tree-holes at various
The antenna is half as long as the head, smooth, and heights and in open tree stumps of different deciduous
not covered with spicules (Fig. 8.24b). The antennal trees as Quercus sp., Fagus sp., Alnus sp., Betula sp.,
seta (1-A) is usually single. The inner frontal seta and Juglans sp. They also occur in mixed forests in old
(5-C) is usually single, the median frontal seta (6-C) trees and can occasionally be found in ground pools
has 1–2 branches and the outer frontal seta (7-C) has together with Or. pulcripalpis, An. plumbeus, and Oc.
2–4 branches. All setae on the prothorax are pulcritarsis, but very rarely in coniferous forests. The
2-branched, except for 2-P. Most of the setae on the species hibernates in the egg stage in northern areas,
rest of the thorax and abdomen are of the stellate and in the larval stage in more southern regions. The

Fig. 10.18 Hypopygium of Oc. geniculatus Fig. 10.19 Larva of Oc. geniculatus
208 10 Subfamily Culicinae

adults appear during the summer as the development The proboscis of the males is often not longer than
depends on spring and summer rains collected in the the fore femur, and the palps are usually longer than
tree-holes. Females are day and crepuscular biters and the proboscis, but sometimes as long as the proboscis
readily feed on humans. In southeastern Europe they or shorter. The tarsal claws of the front and mid legs
occur in masses, viciously attack humans in the open, have prolonged main and subbasal teeth. Tergum IX
but rarely enter urban areas. always has two more or less expressed lateral lobes
Distribution: Found in the Palaearctic region, which usually bears a group of strong or spine-like
known in most European countries, and its northern- setae. The gonocoxite in most species has basal and
most limit follows that of deciduous or mixed forests. apical lobes, sometimes one or both less expressed,
In the Mediterranean region it is reported in northern indistinct, or absent. The gonostylus is simple with an
Portugal, Sardinia, Italy mainland, Greece, and extends apical spine. The paraproct has pointed tips, some-
east to the Caucasus. Also reported from North Africa times inwardly curved. Typical claspettes are present,
to Asia Minor. divided into a stem and a filament. The aedeagus is
pear shaped, elongated, or rounded.
The antennae of the larvae have a multiple-branched
antennal seta (1-A), usually inserted at about the middle
 ubgenus Ochlerotatus
10.2.2 S
of the antennal shaft. The lateral palatal brushes are
Lynch Arribalzaga well developed for suspension feeding or brushing. The
postclypeal seta (4-C) is inconspicuous, and multiple-
The flagellomeres of the female antennae are prolon- branched. The inner frontal seta (5-C) is often situated
gated distally, the palps are only 1/3 to 1/4 the length of in front of the median frontal seta (6-C), both pairs
the proboscis, the latter being longer than the fore being single to multiple-branched. Prothoracic setae
femur. The scale pattern on the vertex and occiput is 1-P to 7-P are single to 3-branched. The number of
variable, often with numerous erect forked scales on comb scales is variable from a few to many, arranged in
the occiput and mixed narrow and broad scales on the a single or irregular rows. The siphon is well developed,
vertex and along the eye margin. The thorax in most with siphonal seta (1-S) usually inserted at about the
species has a dark grey to dark brown or blackish integ- middle of the siphon. The pecten has more or less
ument. The scutum is covered with scales and with spaced teeth of significant shape. The saddle partly or
rows of acrostichal, dorsocentral and supraalar setae. fully encircles the anal segment, and the saddle seta
The scutellum has three lobes and groups of setae and a (1-X) is usually single. The cratal and precratal tufts
few narrow scales. The pleurites are extensively scaled (4-X) are well developed. The anal papillae are of vari-
with patches of mostly pale to whitish scales. able shape and size.
Prespiracular setae are absent. A postprocoxal patch of Of the nearly 200 species of the subgenus described
whitish scales is present in some species. The legs are worldwide, more than half are distributed in the
mostly covered with dark scales, but pale scales may be Holarctic region and nearly a quarter in each of the
scattered or grouped to form a knee spot or basal or api- Australian and the Neotropical regions. Only a few
cal rings, mainly on the tarsomeres. All the tarsal claws species are found in the Oriental and African regions.
have an additional subbasal tooth, and the pulvilli are In the western Palaearctic and throughout Europe,
setous or inconspicuous. The wings are predominantly Alphavirus, Flavivirus, and three different groups of
dark scaled, both the costa (C) and subcosta (Sc) may Bunyavirus were found in a few isolates from the
have patches of paler scales, and in some species the Ochlerotatus species, such as Oc. cantans, Oc. cas-
wing veins are covered with mixed dark and pale scales. pius, Oc. communis, Oc. flavescens, Oc. hexodontus,
The abdomen has elongated cerci and the usually nar- Oc. punctor, and Oc. sticticus (Traavik et al. 1985;
rowed last segments give the impression of being Lundström 1994; Aspöck 1996). Some other parasites
pointed. The scaling of the abdomen is extensive on have been reported from the Ochlerotatus species in
both the terga and sterna. It can be rather uniform or Europe, such as the bacterium Francisella tularensis.
display various patterns of banding or mixed colours. In North America virus vector capacity is documented
The scale patterns on the thorax, legs, wings, and abdo- for several species of the subgenus (Reeves 1990;
men are often used for species identification. Beaty and Marquardt 1996).
10.2 Genus Ochlerotatus Lynch Arribalzaga 209

Morphological heterogenity in the subgenus is which are unique for this group. The basal lobe of the
great; several species groups show distinct characteris- gonocoxite has 3 setae distinctly larger than the rest.
tics. As long as no worldwide analysis of the subgenus One basal seta is well separated from the two distal
exists, discrepancies of grouping the species within setae. Dense long setae cover the inner surface of the
different regions will prevail. Edwards (1932) first apical half of the gonocoxite to a large extent. The
revised and designed species groups and subgroups of claspette stem has a thorn shaped process or is distinctly
Ochlerotatus on a worldwide base including Holarctic, swollen and bent at about the middle. The species
South American, Oriental, and Australian species. included in this group are: diantaeus, intrudens,
A complete grouping of all European members of the pullatus.
subgenus Ochlerotatus does not exist so far. Based on
the suggestions for the species grouping given for the Punctor Group
Palaearctic region (Martini 1931), the Fennoscandian
The tarsi are entirely dark scaled, but members of
region (Natvig 1948), Germany (Mohrig 1969), and
this group differ from the others by the structure of the
the former USSR (Gutsevich et al. 1974), the follow-
abdominal segment X of the larvae. The saddle
ing classification is given regarding the European spe-
completely or almost completely surrounds the anal
cies which are included in the keys.
segment leaves a very narrow gap ventrally. In the
male hypopygium the claspette filament is evenly
Annulipes Group
sclerotized without a narrow transparent wing. The
Large to medium sized mosquitoes. The tarsi have species included in this group are: hexodontus,
pale basal rings, which are broad at least on some nigripes, punctor, punctodes.
tarsomeres. Identification of the females is sometimes
very difficult and arbitrary. The basal lobe of the
gonocoxite is never constricted at the base. The apical
lobe is well developed. The claspette filament is
Ochlerotatus (Ochlerotatus) annulipes
winged. The larvae usually have 4–6 precratal setae
(Meigen 1830)
(4-X). The species included in this group are: annulipes,
behningi, cantans, cyprius, euedes, excrucians,
Female: The general colouration of the integument
flavescens, mercurator, riparius, surcoufi.
is more brownish and the scaling more yellowish
than in Oc. cantans, but less golden than Oc. ripar-
Caspius Group
ius. The females of these three species resemble each
The tarsi have pale rings embracing two tarsomeres, other superficially, however the scale pattern of the
the apex of one and the base of the following tarsomere. scutum is different. The proboscis of Oc. annulipes
The apical lobe of the gonocoxite is weakly developed or is predominantly creamy white with mixed dark
absent. The species included in this group are: berlandi, scales. The palps have mixed dark and pale scales,
caspius, dorsalis, mariae, pulcritarsis, zamitii. and a sometimes distinct basal light ring. The head
has bronze scales and a lateral patch or stripe of
Communis Group creamy white scales. The scutum has a defined
median stripe of brown or fawn coloured scales, and
Usually medium sized mosquitoes. The tarsi are
the lateral parts are covered with cream coloured or
entirely dark scaled. The claspette filament is differentiated
greyish scales. The antepronotum and propleuron
into a well sclerotized ridge and weakly sclerotized
have whitish scales. The postpronotum in the upper
transparent wings. The species included in this group are:
half has narrow bronze scales, and broad yellowish
cataphylla, coluzzii, communis, detritus, hungaricus,
ones in the lower half. A few postprocoxal scales are
impiger, nigrinus, leucomelas, pionips, sticticus.
usually present. A hypostigmal patch is absent, but
two distinct patches are present on the sub- and post-
Intrudens Group
spiracular areas. The mesepisternum has three dis-
The tarsi are entirely dark scaled, but particular tinct patches and a few scattered scales at its upper
differences can be found in the male hypopygium, edge. The mesepimeron is covered with creamy
210 10 Subfamily Culicinae

white scales in the upper half, and a few scales are the apex. The claspette stem is stout and slightly
present on the lower half and on the mesomeron. The swollen at the apex, the filament is broad and less
coxae have scattered light scales, the femora are than half as long as the stem, and slightly swollen
mostly yellowish scaled, the front leg occasionally beyond the middle.
has a dark spot above the knee, the mid leg is some- Larva: Very similar to that of Oc. cantans but with
what darker on the dorsal side, and all legs have a more tapered distal part of the siphon. The antennae
white knee spots. The tibiae are light scaled, espe- are shorter than the head, and the antennal seta (1-A)
cially the fore tibia, or otherwise speckled with dark has 3–4 branches, inserted at about the middle of the
scales. There are basal rings of whitish scales on tar- antennal shaft. The inner and median frontal setae (5-C
someres I–V, except tarsomere V of the fore legs, and 6-C) have 2–3 branches. The prothoracic for-
which is usually entirely dark scaled. The tarsal rings mula 1-P to 7-P is as follows: 1 (short, single to
are variable in width, but usually wider than in Oc. 2-branched); 2 (moderately long, single); 3 (long, sin-
cantans. The wing veins are covered with intermixed gle); 4 (shorter than 2-P, single); 5 and 6 (single, long);
dark and pale scales, the pale scales are usually more 7 (long, 3–4 branches). The number of comb scales
yellowish than in Oc. cantans. The abdomen has ranges between 30 and 40, and each scale has a long
basal white bands on terga I–VII, the last segments median spine (Fig. 10.21). The siphonal index is usu-
rarely have very narrow apical bands. All the terga ally less than 3.0, and the pecten teeth are similar to
have some light scales mixed among the darker ones that of Oc. cantans. The siphonal tuft (1-S) has 5–7
(Fig. 6.34b). The sterna are usually yellowish scaled, branches, situated at about the middle of the siphon.
with some speckled dark scales. Seta 9-S is prominent, but not stout. The saddle does
Male: Tergum IX has two well developed lateral not encircle the anal segment but covers 2/3 of its lat-
lobes, each with 4–6 strong setae. The basal lobe of eral sides. There are usually six or more precratal tufts
the gonocoxite is indistinct or absent, without strong (4-X) present, which separates the larvae from those of
spine-like setae, but numerous thin setae (Fig. 10.20). Oc. cantans, that usually have less precratals. The anal
The apical lobe is well developed. The gonocoxite papillae are about as long as the saddle or longer.
bears a large amount of long and dense setae at the
distal part of its inner ventral surface. This is a
unique character within the species of the Annulipes
Group. The gonostylus is curved, and tapers towards

Fig. 10.20 Hypopygium of Oc. annulipes Fig. 10.21 Larva of Oc. annulipes
10.2 Genus Ochlerotatus Lynch Arribalzaga 211

Biology: Oc. annulipes is a monocyclic species scales and the propleuron has some whitish scales.
occuring in spring. It is widespread throughout Europe, The postpronotum has narrow scales, more than two
but most abundant in the central parts of the continent, third of them are bronze, the rest are creamy coloured.
where it can be very dominant locally. It overwinters in A postprocoxal scale patch is present. The sub- and
the egg stage and the larvae occur at the same time as postspiracular areas have a continuous whitish scal-
Oc. cantans or slightly later. They breed in open ing. The mesepisternum has three distinct patches, an
meadow pools, at forest edges and inside deciduous upper patch with creamy scales, a prominent median
forests, preferably in semipermanent pools with leaf patch reaching the anterior margin and a small lower
detritus, where they are often found together with lar- patch along the posterior border of the pleurite. One
vae of Oc. cantans. In more open habitats they occur patch covers the upper half of the mesepimeron. The
together with larvae of Oc. flavescens, Oc. riparius coxae have prominent light scale patches. The femora
and Oc. excrucians. The males are found around the have mixed whitish and dark scales, with white knee
breeding sites for several days after emergence. The spots. The tibiae as well as tarsomeres I have a some-
females are day biters with a crepuscular activity in the what darker pattern. Tarsomeres II–IV have broad
areas of high abundance. They are present over several whitish basal bands covering up to half of their length,
weeks to months during late spring and summer and tarsomere V is dark with a few light scales on the
depending on local climate. fore and mid legs. The wing veins have dark scales
Distribution: Oc. annulipes is a western Palaearctic intermixed with a few or many creamy white scales.
species reported from southern Scandinavia to the Some amount of colour variation in scaling might be
Mediterranean region. The separation of larvae and expected in the females. The abdominal terga are pre-
females of Oc. cantans and Oc. annulipes from differ- dominantly covered with brownish scales, with scat-
ent areas may be difficult because of the variation of tered creamy white or yellowish scales. Pale scales
characteristics such as colouration and setation. usually form diffuse median patches, and sometimes
Medical importance: Tahyna virus has been iso- short longitudinal stripes (Fig. 6.31a). Transverse
lated from Oc. cantans/annulipes in Austria (Lundström pale basal or apical bands are absent. The sterna have
1999). dominantly black scales and a few white basal, nar-
row bands or lateral patches. The cerci have a few
white scales among the dark ones.
Ochlerotatus (Ochlerotatus) behningi Male: Tergum IX has a deep notch and the protrud-
(Martini 1926) ing lateral lobes have numerous thin setae. The gono-
coxite is short and stout, with a conical basal lobe
Female: A medium to large species. Oc. behningi has which bears many setae of uniform length and width
a more pronounced blackish integument and setation (Fig. 10.22). The apical lobe is well developed. The
than other members of the Annulipes Group. The gonostylus is curved apically, and is narrow with a
setae on the pleurites rarely have a golden shine. The slender apical spine. A relatively shorter claspette stem
proboscis is dark, with intermixed creamy scales differentiates the species from Oc. cantans, Oc. ripar-
along its whole length, and mostly pale scales in the ius, Oc. flavescens and Oc. excrucians males. The clas-
middle. The palps are dark scaled, mixed with a few pette filament is narrow, and approximately as long as
white scales. The antennae are covered with very the stem.
dark setae, the pedicel with some white scales. The Larva: Similar to that of Oc. excrucians and often
vertex is covered with creamy scales intermixed with it is difficult to distinguish between the species. The
some black ones, forming an indistinct patch, and the antennae are short with many distinct spicules, and
occiput has a mixture of narrow golden and dark erect the antennal seta (1-A) is located below the middle of
scales and a broad midstripe of yellowish flat scales. the antennal shaft. The postclypeal seta (4-C) has 6–8
The scutum is usually entirely covered with small, branches (Fig. 8.53a). The inner frontal seta (5-C) has
narrow golden bronze or rust coloured scales, some- 2–4 branches, and the median frontal seta (6-C) has
times indistinct creamy white posterior submedian 2–3 branches. A report on material from the Don Basin
stripes are present, and the scutellum is covered with referred to both setae as being double. The prothoracic
dark scales. The antepronotum has a few bronze formula 1-P to 7-P is as follows: 1 (double, short, thin);
212 10 Subfamily Culicinae

Fig. 10.22 Hypopygium of Oc. behningi Fig. 10.23 Larva of Oc. behningi

2–4 (single); 5 (double); 6 (single); 7 (triple). The Note on systematics: As no male belongs to the
number of comb scales is 18–28 (usually 20–24) type series (Martini 1931), the missing characteristics
arranged in irregular rows (Fig. 10.23). Individual and the amount of variation need further studies. The
scales have a very protruding median spine and insig- species certainly needs a closer analysis of female,
nificant lateral spines. The siphon is more or less male and larval characteristics and comparisons with
tapered at the apex, and the siphonal index is 3.0–4.0. species of similar colouration.
The pecten teeth are usually evenly spaced, sometimes
the two distalmost teeth may be detached apically.
Each pecten tooth has a few lateral denticles at its base. Ochlerotatus (Ochlerotatus) berlandi
The siphonal tuft (1-S) is inserted beyond the middle (Seguy 1921)
of the siphon, with 5 branches. The saddle does not
encircle the anal segment but covers most of it. Five to Female: The palps are predominantly dark scaled,
6 precratal tufts (4-X) are present, and the anal papillae with scattered pale scales in the middle, and the tip of
are at least as long as the saddle. the palps is white scaled. The vertex is pale to whitish
Biology: The species belongs to the early summer with some diffuse darker scales which are more numer-
species and seems to be monocyclic. Little is known ous at the occiput forming a dark triangular patch. The
about its general biology. Martini (1931) reported mass eye margin is covered with long setae. The scutum is
occurrence of females as fierce day biters in open mainly covered with pale golden scales, with distinct
spaces from the plains along the Volga river in the patches and stripes of dark brown scales. Pale golden
Saratov area. The species occurred later than Ae. vex- scales form a broad median stripe and two lateral
ans. Females were also found in higher mountainous stripes. Dark scales form distinct patches on the ante-
areas, this could indicate that the females may fly long rior and posterior submedian areas. Dark posterior
distances to search for a blood meal. dorsocentral stripes extend from the transverse suture
Distribution: The distribution is not very well to the end of the scutum. Post- and subspiracular scale
known. It has been recorded in Russia, Ukraine, patches are present. The mesepisternum has a prealar
Slovakia and Poland which seem to confine the species scale patch, and the mesepisternal patch is divided into
to a eastern European distribution. It has not been a larger upper portion and a smaller lower portion. The
reported from the East Palaearctic. mesepimeron has two whitish scale patches on its
10.2 Genus Ochlerotatus Lynch Arribalzaga 213

upper half. The femora and tibiae are dark scaled, but tuft (1-A) is inserted beyond the middle of the antennal
scattered pale scales may be present. The tarsi have shaft. The postclypeal seta (4-C) is well developed
white apical and basal rings usually present on tarsom- and multiple branched. The inner frontal seta (5-C) is
eres I and II of the front and mid legs, and on tarsom- the most prominent of all the frontal setae, and usu-
eres I–III of the hind legs. Tarsomere V of all legs is ally has 9 branches. The median frontal seta (6-C) is
entirely pale scaled (Fig. 6.20a). The wing veins are situated almost at the same level as 4-C, is less devel-
dark scaled; rarely a few isolated pale scales may be oped than 5-C, and usually has 8 branches. The outer
present. The abdominal terga have creamy white basal frontal seta (7-C) is well developed, long and usually
bands which are usually slightly widened laterally, and has 10 branches. The comb usually has 16–20 comb
sometimes expanded into triangular patches. The scales arranged in several irregular rows, each scale
sterna are black scaled, with more or less developed with a well developed median spine. The siphon is
pale lateral patches, sometimes almost connected in very long and slender, the siphonal index is 5.5–7.8
the middle. (Fig. 10.25). The pecten consists of 19–29 small and
Male: The hypopygium is very similar to that of blunt teeth. The siphonal tuft (1-S) is long, more than
Oc. pulcritarsis, no constant differences can be found twice the width of the siphon at the point of its ori-
(Fig. 10.24). Oc. berlandi has the lobes of tergum IX gin, and is inserted distinctly below the middle of
well developed and widely separated, and each lobe the siphon, with 3–5 branches. The saddle reaches far
bears 5–8 spine-like setae. The gonoxocite is about beyond the half of the lateral sides of the anal seg-
three times as long as it is broad. The basal lobe is ment. The saddle seta (1-X) is much longer than the
weakly developed with one strong, apically recurved, saddle, and is single. The upper anal seta (2-X) has
spine-like seta (Fig. 7.38b). The other setae on the 4–6 branches, the lower anal seta (3-X) is single, and
basal lobe are thin and of variable length. The apical
lobe is indistinct. The gonostylus is somewhat wid-
ened in the middle, with a slender apical spine. The
claspette filament is slender and longer than the stem.
Larva: The head is broader than long, and the
antennae are almost as long as the head. The antennal

Fig. 10.24 Hypopygium of Oc. berlandi Fig. 10.25 Larva of Oc. berlandi
214 10 Subfamily Culicinae

about as long as the siphon. The ventral brush has 3 are usually present just beyond the scutal angle and
precratal setae (4-X). The anal papillae are elongated, sometimes narrow whitish submedian stripes run from
sausage shaped, and much longer than the saddle, the patches to the posterior margin of the scutum
with the dorsal pair being longer than the ­ventral (Fig. 6.35a). The scutellum has white and brown scales
pair. and light setae. The postpronotum has yellow and nar-
Biology: The species hibernates in the larval or row upper scales, white and somewhat broader lower
pupal stage and usually has two generations per year. scales; and the postprocoxal membrane is bare. The
Larvae can be exclusively found in tree-holes, very white patches of the post- and subspiracular areas are
often in those of Platanus orientalis, Quercus ilex, Q. fused. The mesepisternum has one upper and two dis-
suber and Sophora japonica, preferably in alkaline tinct lower patches of white scales, and the mesepim-
waters rich with organic materials. They can usually eron has a patch of white scales. The coxae have white
be found in association with larvae of Oc. echinus, An. scales, and the femora and tibae have mixed dark and
plumbeus and Or. pulcripalpis (Ramos 1983). Under pale scales. Tarsomere I of all the legs has more or less
laboratory conditions, at a temperature of 24°C, larval mixed scales, tarsomeres II–V have moderately broad
development lasts for 24 days and the pupal stage for white basal rings (Fig. 6.18a), except tarsomere V of
about 7 days. Under natural conditions, the larval the fore legs which is entirely dark scaled. The wings
development lasts for approximately 4 months (Ramos are predominantly dark scaled. Usually a few white
1983). Adult females are mainly zoophilic, but readily scales are scattered on the costa (C) and on some other
bite humans either outside or inside human habitations veins. Abdominal terga I–VIII have white basal bands,
(Ribeiro et al. 1988). sometimes narrow and indistinct. The apical parts of
Distribution: Oc. berlandi is endemic to the the terga have more or less numerous scattered pale
Mediterranean region and has been recorded in Portugal, scales (Fig. 6.28b). Sterna I–VIII are whitish with
Spain, France, Italy, Greece, and in Morocco, Algeria, darker lateral patches, and the cerci are predominantly
and Tunisia. It was the prevalent tree-hole species dark scaled and elongated.
(together with Oc. geniculatus) of Sardinia during a Male: The lobes of tergum IX have numerous
five year survey (Marchi and Munstermann 1987). strong setae. The hypopygium is of a different shape
to that of the other members in the Annulipes Group
(Fig. 10.26). The basal lobe of the gonocoxite is slen-
Ochlerotatus (Ochlerotatus) cantans der, and distinctly elongated with a large spine-like
(Meigen 1818) seta at the base. The apical lobe is present, and cov-
ered with short setae. The gonostylus is long with a
Female: Its greyish integument with dominant dark, curved tip. The paraproct is long and narrow. The
blackish brown scaling and fewer scattered white or claspette filament is shorter than the stem, prominently
yellowish white scales on the body and wings distin-
guishes Oc. cantans from Oc. annulipes, which has a
more yellowish scaling. The white rings on the legs are
not as broad as in Oc. annulipes, Oc. behningi, and Oc.
riparius. The proboscis has no or few white scales.
The palps are dark with a few white scales at the tip.
The clypeus has a dark brown integument. The anten-
nae have dark segments with brownish setae, and the
pedicel has a few white scales. The vertex is white
scaled with a lateral spot of brown scales. The occiput
has brownish scales and two median stripes of white
scales. The colouration of the scutum is very variable.
Typically it is covered with dark brown or bronze
brown scales, the lateral parts with greyish white or
creamy scales, but sometimes these scales are light
brown. A pair of distinct whitish submedian patches Fig. 10.26 Hypopygium of Oc. cantans
10.2 Genus Ochlerotatus Lynch Arribalzaga 215

winged, and at least as long as it is wide. The shape of Biology: The larvae develop rather early in spring
the spine-like seta of the basal lobe and the claspette in Southern and Central Europe, in northern areas
filament seem to be variable characteristics. The aede- they occur somewhat later but also belong to the
agus is elongated and tapered. early species. Larvae are present until late spring or
Larva: The antennae are shorter than the head, early summer in varying numbers, depending on the
and the antennal tuft (1-A) is inserted slightly beyond amount of inundation and insolation of the habitat.
the middle of the antennal shaft. The inner frontal The species is predominantly monocyclic, but capa-
seta (5-C) has 3–5 branches, the median frontal seta ble of a bicyclic occurrence; the further north, the
(6-C) has 2–3 branches and the outer frontal seta more obligate monocyclic it is. Under special cir-
(7-C) has 7–8 branches. The pothoracic formula of cumstances another batch of eggs may hatch in late
setae 1-P to 7-P is as follows: 1 (short, double to tri- summer. It will mostly originate from unhatched
ple); 2 (medium long, single); 3 (very long, single); 4 eggs from the spring generation or even the previous
(short, single); 5 and 6 (long, single); 7 (long, triple). year. Eggs are hibernating, and larval development
The number of comb scales is 28–40 (usually about lasts from 2 months to less than 4 weeks, entirely
35) arranged in an irregular patch. Each scale has a depending on regional temperature regimes. The
moderately long median spine. The siphonal index is larvae occur in open permanent or semipermanent
approximately 3.0 or less (Fig. 10.27). The pecten meadow pools and dominate in deciduous or mixed
teeth are evenly spaced, and each tooth has 3-4 lateral forest pools with scarce aquatic vegetation and a
denticles at the base. The siphonal tuft (1-S) is thick layer of leaves on the bottom of the pools. In
inserted distal to the last pecten tooth about the mid- these habitats they may occur together with larvae
dle of the siphon, with 5–12 branches. The saddle of Oc. annulipes, Oc. communis, Oc. punctor and
does not encircle the anal segment, and covers 3/4 of occasionally with late spring species, such as Ae.
its lateral sides. The saddle seta (1-X) is single, and cinereus or Ae. geminus. The adults emerge shortly
about as long as the saddle. Usually 4–6 precratal after the trees turn green. It has been reported that
tufts (4-X) are present, quite frequently less than in females need a period of rest in vegetation before
Oc. annulipes. The anal papillae are usually as long they search for a blood meal, but local populations
as or longer than the saddle. differ in this behaviour and some attack soon after
emergence. Biting females are encountered most
abundantly in lowland regions from late March to
June in the Mediterranean region and from late May
to early August at the southern borders of the taiga
zone. The wide distribution range of Oc. cantans
over all of Europe comprises plenty of local varia-
tions in time of occurrence and biting habits. The
life span of the females is between 1 and 2 months.
They are frequently found in dense vegetation but
also fly over short distances to open spaces such as
pastures and river lowlands to feed on cattle and
sheep. Their daily biting cycle on humans seems to
be bimodal with peaks during dawn and dusk. No
autogenous forms have been reported.
Distribution: The species has a western Palaearctic
distribution and occurs from the taiga zone in the north
to the Mediterranean region in the south.
Medical importance: Flavivirus and Bunyavirus
isolates have been reported from Slovakia and Austria
(Lundström 1994, 1999). On material from Slovakia it
was shown that the species is susceptible to infection
Fig. 10.27 Larva of Oc. cantans with Tahyna virus.
216 10 Subfamily Culicinae

Ochlerotatus Caspius Complex the same number or the dark scales predominate. The
abdominal terga are dark brown scaled, with yellowish
Two apparently morphologically identical forms of scales dorsally and white scales laterally. The terga
Oc. caspius designated as “species A” and “species B” have basal and apical yellowish bands which are wid-
were detected by electrophoretic analysis of wild pop- est in the middle. A longitudinal middorsal yellowish
ulations from Italy (Cianchi et al. 1980). As no mor- stripe is present, but of varying length (Fig. 6.21a). It is
phological and/or biological differences were attributed usually present on terga II–IV, otherwise only vaguely
to those sibling species, they will be treated together expressed by a median widening of the transverse
under the description of the nominative form. Another bands. In some specimens the median stripe is present
species, described as Aedes duplex, was recorded from on tergum II only (this pattern resembles that of Cs.
the European part of Russia by Martini (1926). The annulata). The lateral sides of the terga are ornamented
two male specimens particularly exhibit differences in with central, triangular, white patches. Tergum VII has
their hypopygium with the basal lobe bearing 4 spine- mixed dark and pale scales.
like setae instead of 2 setae. As no further record of Male (Fig. 10.28): The basal lobe gradually arises
any stage of Ae. duplex has been made since that time, from the gonocoxite, and is not constricted at the base.
it is more probable that the two sampled males are only Two spine-like setae arise from it, one seta is longer
aberrant specimens, thus Ae. duplex should not be and sharply hooked at the apex, the tip of the hook
regarded as a distinct species and member of the extends backwards to almost the middle of the spine,
Ochlerotatus Caspius Complex. and the shorter seta is straight or slightly curved
(Fig. 7.35a). The apical lobe of the gonocoxite is
inconspicuous, almost bare dorsally. The claspette fila-
Ochlerotatus (Ochlerotatus) caspius (Pallas 1771) ment is about as long as the stem, with a narrow unilat-
eral wing.
Female: Oc. caspius is very similar to Oc. dorsalis in Larva: Similar to those of Oc. dorsalis, Oc. detri-
general colouration, but is usually distinguished from tus, Oc. leucomelas and Oc. flavescens. Average val-
the latter by two dorsocentral white stripes which run ues of some quantitative traits can be used to distinguish
over the bright fawn coloured scutum. However, the between larvae of Oc. caspius and Oc. dorsalis, but
colouration of Oc. caspius is subject to considerable only at population levels (Milankov et al. 1998). The
variation. The proboscis and palps are covered with antenna is about half as long as the head, with sparse
brown and white scales (Fig. 6.30b). The vertex has tiny spicules. The antennal seta (1-A) is inserted
white and yellowish brown scales intermixed. The slightly below the middle of the antennal shaft, usually
scutum has two narrow, white dorsocentral stripes run-
ning continuously from its anterior to posterior margin
(Fig. 6.22a). The stripes may also be wide and diffuse,
and if more yellowish, indistinct against the light
brown background, but when the scales are well pre-
served, the distinction from the scutal pattern of Oc.
dorsalis is quite easy. Even in species with the scales
rubbed off from the central part of the scutum, the
anterior and/or posterior parts of the longitudinal
stripes are often well preserved and visible. The scales
on the pleurites are broad and white. Tarsomeres I and
II of the fore and mid legs and tarsomeres I–IV of the
hind legs have white or cream-coloured basal and api-
cal rings (Fig. 6.19a). The light rings are sometimes
indistinct, and hind tarsomere V is entirely white
scaled. The wing veins are covered with mixed dark
and pale scales (Fig. 6.22b). At the basal quarter of the
costa (C), the dark and pale scales are of more or less Fig. 10.28 Hypopygium of Oc. caspius
10.2 Genus Ochlerotatus Lynch Arribalzaga 217

with 9 branches which are half as long as the antenna. produced due to the nature of the breeding site. The
The postclypeal seta (4-C) has 3–5 short, thin branches. species overwinters in the egg stage, the first occur-
The inner frontal seta (5-C) is inserted well below the rence of larvae varies with the latitude, but generally
median frontal seta (6-C), both are single, or less fre- takes place at the beginning of the year, this may be
quently 2-branched, but rarely does one of the setae February–March in southern parts of Europe. It is
have 3 branches. The outer frontal seta (7-C) has 7–10 regarded as a seaside mosquito that readily breeds in
branches. The mesothoracic seta 1-M is single and inland salt marshes and freshwaters with 0.5 g NaCl/l
moderately long. The comb consists of 18–28 (usually (Pires et al. 1982). It is a common species in the
20–25) variegated scales arranged in 2–3 irregular Atlantic and Mediterranean coastal marches and rock-
rows (Fig. 10.29). At least some of the scales have a holes. The breeding sites in the coastal areas of Portugal
distinct median spine (Fig. 8.37b). The siphon slightly are usually restricted to altitudes < 50 m (Ribeiro et al.
tapers in the apical half, and the siphonal index is 1.8– 1989). The larvae develop in open or shaded waters,
2.6. The pecten has 17–26 (usually 20–22) evenly permanent or temporary water bodies formed by the
spaced teeth, the basalmost four teeth are rudimentary. snow melt, river floods or coastal marshes subjected to
The pecten extends slightly beyond the middle of the intermittent flooding and rice fields, usually with little
siphon. The siphonal tuft (1-S) has 5–10 branches vegetation and muddy bottom, often with a high con-
inserted beyond the middle of the siphon. The saddle centration of salt, which may reach values of up to
covers more than half of the lateral sides of the anal 150 g/l (Bozicic-Lothrop 1988). The acidity of the
segment. The saddle seta (1-X) is about half as long as breeding sites recorded in Portugal ranged from pH
the saddle, and is single. The lower anal seta (3-X) is 6.0–7.0 (Pires et al. 1982). The most characteristic
longer than the siphon, and single. The ventral brush is freshwater habitats are river valleys, where larvae can
made up of 12–17 cratal tufts (4-X) and 2–3 precratal breed in large numbers in the floodplains. They can be
tufts. The anal papillae are short, 0.3–0.9 times as long associated with larvae of many mosquito species, such
as the saddle, and lanceolate. The ventral pair is shorter as An. atroparvus, An. maculipennis, Ae. vexans, Ae.
than the dorsal pair. vittatus, Oc. annulipes, Oc. cantans, Oc. detritus, Oc.
Biology: Oc. caspius is a polycyclic, halophylic intrudens, Oc. mariae, Oc. sticticus, Cx. p. pipiens, Cx.
species. Sometimes only one generation per year is theileri, Cx. impudicus, Cs. annulata (Bozkov et al.
1969; Ramos et al. 1978; Pires et al. 1982; Knoz and
Vanhara 1982; Marchi and Munstermann 1987).
Although females are strongly exophagic, they enter
inhabited areas, houses, and cattle sheds if they occur
in masses. The females readily bite humans and ani-
mals both in rural and urban areas (Gutsevich et al.
1974). They often bite during the day and night, but
usually most actively search for a blood meal at dusk.
Females are repelled by the lights of standard CDC
miniature light traps. The species has a high resistance
to heat and drought. Females actively search for blood
at temperatures ranging from 11.5 to 36°C and relative
humidity ranging from 47 to 92% (Petric 1989). They
may migrate for long distances, up to 10 km.
Autogenous development of Oc. caspius was detected
in Uzbekistan (Chinaev 1964).
Distribution: It is a Palaearctic species which is
more common in southern and dry regions than Oc.
dorsalis which is of Holarctic origin. Oc. caspius is
distributed from Europe to Mongolia, north and west
China, north Africa, west and middle Asia. In Europe
Fig. 10.29 Larva of Oc. caspius it can be found from England to the central parts of
218 10 Subfamily Culicinae

Russia, and from the southwest to the Mediterranean pale scales. Postpronotal setae are present along the
basin. The distributions of the sympatric Oc. caspius posterior margin of the postpronotum (Fig. 6.41b). The
and Oc. dorsalis overlap in most of Europe. postprocoxal membrane has a patch of pale scales. The
Medical importance: West Nile virus (WNV), subspiracular area is more or less entirely covered with
Tahyna virus, and the bacterium Francisella tularen- scales, and the hypostigmal and postspiracular patches
sis, the causative agent of tularemia, could be detected are fused. The upper and posterior part of the mesepis-
in natural populations (Detinova and Smelova 1973). ternum are extensively scaled, the scales extending
Oc. caspius may have played a role in the spread of near to the anterior angle. The scales on the mesepim-
tularaemia and transmission of Tahyna and rabbit eron end before its lower margin, and mesepimeral
myxoma viruses in former Czechoslovakia, France, setae are present. The femora anteriorly have pale and
and Portugal (Bardos and Danielova 1959; Joubert dark scales. The tibiae and tarsi are mostly dark scaled,
1975; Pires et al. 1982). but with pale scales especially on the ventral surface,
Note on systematics: Most authors consider Oc. and the tarsi are without white rings. The tarsal claws
caspius and Oc. dorsalis as separate species according are small and evenly curved. The wing veins have pale
to morphologic and genetic differences (Edwards scales on the base of the costa (C) and scattered pale
1921; Natvig 1948; Mohrig 1969; Lambert et al. 1990; scales along the costa, subcosta (Sc) and R1; the
Milankov et al. 1998, 2000). Concerning the morpho- remaining veins are dark scaled. The terga are dark
logical variation within Oc. caspius, Kazantsev (1931) scaled with broad basal bands of white scales
found that the light, “sand-coloured” Oc. caspius devel- (Fig. 6.38b), sometimes the last terga are mainly cov-
oped in water with a high salinity, whereas mosquitoes ered with white scales.
breeding in fresh water had a more contrasting colou- Male: The lateral lobes of tergum IX have 4–13
ration. Specimens with intermediate morphological (usually 6–8) short spine-like setae. The gonocoxite
characteristics are common in Europe (Bozicic- has well developed basal and apical lobes. All the setae
Lothrop 1988) as also in more eastern regions of the located on the inner side of the gonocoxite above the
former USSR (Gutsevich 1977). Three intermediate basal lobe are inwardly directed, and usually overlap-
types of scutal colouration and two intermediate types ping in the middle (Fig. 10.30). The basal lobe is coni-
of male genitalia are described in Europe, but no cor- cal with a group of medially directed long setae, one of
relation between water salinity and scutal pattern or which is strong, spine-like, and apically curved. The
development of the basal lobe of the gonocoxite were
found (Bozicic-Lothrop 1988). All the above men-
tioned differences could suggest the possible presence
of subspecies or more than one species in Europe,
which was documented by Cianchi et al. (1980).

Ochlerotatus (Ochlerotatus) cataphylla

(Dyar 1916)

Female: The proboscis is entirely dark scaled, which

is the main character to distinguish the species from
Oc. leucomelas, which has the proboscis speckled with
numerous pale scales. The palps of Oc. cataphylla are
dark scaled, with numerous scattered white scales. The
scutum is usually covered with reddish brown scales,
with lateral areas of paler scales. Sometimes a broad
median stripe and two posterior submedian stripes of
darker scales are present. The pleurites are extensively
covered with scales. The upper part of the postprono-
tum is mostly brown scaled, and the lower part has Fig. 10.30 Hypopygium of Oc. cataphylla
10.2 Genus Ochlerotatus Lynch Arribalzaga 219

paraproct is sclerotized with inwardly curved tips. The segment, and the saddle seta (1-X) is single and short.
claspette stem is strongly curved, and the claspette fila- The upper anal seta (2-X) has 5–8 branches, and the
ment is half as long as the stem, with a broad unilateral lower anal seta (3-X) is single. The ventral brush has
wing. The aedeagus is more or less conical. 1–2 precratal tufts (4-X). The anal papillae are of vari-
Larva: The antenna is less than half as long as the able length and tapered.
head. The antennal seta (1-A) has 3–5 branches, Biology: Oc. cataphylla is a monocyclic species.
located at about the middle of the antenna. The post- The most common breeding sites are forest pools in
clypeal seta (4-C) has 2–3 short branches. The inner swampy woodlands, e.g. alder forests, with neutral to
and median frontal setae (5-C and 6-C) are single, the alkaline water. The pools are usually devoid of sub-
median frontals are located in front of the inner fron- merged vegetation but frequently covered with dead
tals, and the outer frontal seta (7-C) has 3–6 branches leaves at the bottom. In addition, larval populations are
(Fig. 8.35a). The comb is composed of 10–30 (usually recorded from open areas, e.g. inundated meadows
25) scales arranged in 2–3 irregular rows (Fig. 10.31). (Wesenberg-Lund 1921; Natvig 1948; Monchadskii
Each scale has a long-terminal spine and smaller spines 1951). The larvae hatch immediately after the snow
near the base. The siphonal index is about 3.0. The thaw when meltwaters or heavy rainfall flood the
pecten is made up of 13–25 teeth, occupying about 3/4 depressions. The larvae are usually associated with
of the length of the siphon. The 2–4 distalmost teeth those of Oc. rusticus, Oc. cantans, and Ae. cinereus.
are larger and apically detached, all are located beyond Occasionally the larvae of acidophilic species, e.g.
the siphonal tuft (1-S). 1-S is situated approximately in Oc. punctor and Oc. communis are found in the same
the middle of the siphon, with 3–5 branches. The sad- breeding sites. In central Europe the adults appear usu-
dle extends about 2/3 to 3/4 down the sides of the anal ally in the first half of April, before those of Oc. can-
tans and Oc. rusticus. The copulation swarms of male
mosquitoes can frequently be observed at a height of
about 1 m in shaded areas with bushes. Usually the
females of Oc. cataphylla are a nuisance only in forest
areas, where they can bite even during daytime.
Repeated blood meals and ovipositions are possible
(Carpenter and Nielsen 1965).
Distribution: Holarctic, Eurasia, and North
America, northern to southern Europe. In northern
Europe the species occurs in the tundra, in central
Europe in swampy forests, in southern Europe mainly
in mountainous areas.

Ochlerotatus Communis Complex

Owing to differences in the reproductive physiology,

habitat preferences, swarming behaviour, emergence,
and dispersal patterns, the complex is composed of
two or more sibling species (Chapman and Barr
1964; Ellis and Brust 1973; Schutz and Eldridge
1993). Morphometric and electrophoretic compari-
sons of populations of the Ochlerotatus Communis
Complex in North America revealed 4 sibling spe-
cies, namely Oc. communis, Oc. nevadensis, Oc.
tahoensis, and Oc. churchillensis. The females of the
latter species are found to be autogenous, whereas
Fig. 10.31 Larva of Oc. cataphylla the other three species are anautogenous (Brust and
220 10 Subfamily Culicinae

Munstermann 1992). According to variable morpho-

logical characteristics in European populations, it is
feasible to expect more sibling species of the com-
plex in Europe as well. However, electrophoretical
analysis of populations from northern Sweden and
Germany has not provided evidence of any differ-
ences (Weitzel et al. 1998).

Ochlerotatus (Ochlerotatus) communis

(De Geer 1776)

Female: The proboscis and palps are dark scaled,

the palps rarely have a few white scattered scales.
The scutal scale pattern is rather variable, but typi-
cally the scutum is covered with yellow to golden
scales. A broad median stripe and posterior sub-
median stripes of dark bronze scales are present.
They are separated by narrow stripes of pale scales,
which are sometimes fused. The scutellar and Fig. 10.32 Hypopygium of Oc. communis
supraalar setae are dark brown. A postprocoxal
scale patch is absent (Fig. 6.47b), the hypostigmal
patch is usually absent, or occasionally with only a heavily sclerotized with a narrow unilateral wing.
few pale scales. The upper mesepisternal patch The aedeagus is conical, rounded, and notched at
extends to the level of the anterior angle, and the the apex.
mesepimeral patch extends to the lower margin of Larva: The antenna is nearly half as long as the
the mesepimeron (Figs. 6.45b and 6.46a). Lower head, and the antennal seta (1-A) is situated at about
mesepimeral setae are present. The femora, tibiae, the middle of the antennal shaft, with 6–7 branches.
and tarsomeres I of all legs are mostly dark scaled The median frontal seta (6-C) is situated in front of the
dorsally and with a few whitish scales ventrally, the inner frontal seta (5-C), both setae are single and rarely
remaining tarsomeres are dark scaled. The tarsal one seta has 2 branches. The outer frontal seta (7-C)
claws are curved with a long subbasal tooth. The has 4–8 branches (Fig. 8.41a). The number of comb
wing veins are covered with dark scales, and a few scales varies from 40–70, but the average is 60 scales
pale scales are scattered at the base of the costa (C) (Fig. 10.33). The scales are arranged in an irregular
and radius (R). The terga are dark scaled with broad triangular patch, each individual scale without a pro-
basal bands of white scales. longed terminal spine, thus appearing to be rounded
Male: The lobes of tergum IX are covered with apically. The siphonal index is 2.3–3.2, usually about
8–10 short spine-like setae. The hypopygium is 2.8. The pecten has 17–26 evenly and closely spaced
similar to that of Oc. pionips (Fig. 10.32). The basal teeth which do not extend to the middle of the siphon.
lobe of the gonocoxite is rounded, concave at its The siphonal tuft (1-S) has 5–9 branches which are
lower part, with one long, strong spine-like seta. about as long as the width of the siphon at the point of
Mesal to it, is a row of closely spaced, inwardly insertion. The saddle extends about 3/4 down the sides
directed long setae. The upper part of the basal lobe of the anal segment, and the saddle seta (1-X) is dis-
has a row of long, prominent, widely spaced, api- tinctly shorter than the saddle, and is single. The ven-
cally strongly curved, or sometimes hooked setae. tral brush has 2, rarely 3, precratal setae (4-X). The
The apical lobe of the gonocoxite is well developed anal papillae are distinctly longer than the saddle.
and rounded apically. The paraproct is strongly Biology: Oc. communis is usually a monocyclic
sclerotized apically. The claspette stem is long, and snow-melt mosquito, which is one of the most fre-
the claspette filament is shorter than the stem, and quent mosquitoes of swampy forests. The preferred
10.2 Genus Ochlerotatus Lynch Arribalzaga 221

Ochlerotatus (Ochlerotatus) cyprius

(Ludlow 1920)

Female: A large species with a light integument and

golden to yellowish scaling. Natvig (1948) described
Oc. cyprius as variable in colour, the golden tinge is
sometimes lost and the scales are more or less whitish
or yellowish orange in some specimens. It is similar to
Oc. flavescens, and for separation of the two species,
see the description of the latter. The proboscis is yel-
lowish with a few dark scales at the labellum. The
palps are 1/4 of the length of the proboscis, with mixed
golden and greyish scales. The head is pale scaled,
with some dark scales laterally. The antenna is yellow-
ish at the base, with the distal flagellomeres more
brownish. The integument of the scutum is light brown
with yellowish and golden narrow scales, and some-
times a weak dark median stripe and short dark lateral
stripes are present. The postpronotum has narrow
golden scales and golden setae. A postprocoxal patch
Fig. 10.33 Larva of Oc. communis is present. The mesepisternum has two separate cream
coloured scale patches, the lower patch reaching the
breeding sites are acidic water bodies which are filled anterior margin. The mesepimeral scale patch nearly
with water during the snow-melt or spring rainfall. reaches the lower margin of the mesepimeron, and the
Larvae can mainly be found in depressions and ditches lower mesepimeral setae are present (Fig. 6.29b). The
without vegetation but with a dense layer of dead fore and mid femora have yellowish scales mixed with
leaves at the bottom. Often they are found in strongly dark ones, the hind femur apically has dark scales, and
acidic waters, e.g. with Sphagnum sp., with a pH- yellowish knee spots but these are usually indistinct.
value of little more than 3.0. They appear only rarely The tibiae are predominantly yellowish scaled with
or are absent in waters with neutral reaction, e.g. in scattered black scales, which are more numerous
inundated areas of large rivers. Most of the larvae hatch towards the apical parts of the mid and hind tibiae. The
at temperatures of little more than 0°C, when the tarsomeres have broad, yellowish basal rings and dark
breeding sites are still partly covered with ice. In cen- scaling apically, which is more pronounced at the mid
tral Europe the larvae hatch from February onwards, and hind legs. The wing veins are yellow scaled with
adults emerge usually in April. In the laboratory, the scattered dark scales. The abdomen dorsally and ven-
optimum temperature for larval development is 25°C. trally has ochre yellowish broad scales mixed with iso-
At this temperature the development to the adult stage lated dark scales, and the terga sometimes have more
is completed within 18 days, but above 30°C and below dark scales laterally which never form a continuous
4°C the development is not completed. In central transverse band. The cerci are predominantly dark
Europe, females are troublesome for warmblooded scaled.
creatures in forest areas from April onwards, particu- Male: Tergum IX has 6–11 spine-like setae on each
larly during twilight. Females do not migrate long dis- of the lateral lobes. The gonocoxite is long and slen-
tances from the breeding sites. Usually the population der, and the basal lobe is well developed, with one
decreases from July on, but Scherpner (1960) found spine-like seta and several long setae of different
isolated freshly hatched larvae of Oc. communis in widths (Fig. 10.34). The apical lobe is prominent with
August. rather short setae. The gonostylus is long and slender,
Distribution: Holarctic, North America, and with an elongated apical spine. The paraproct has a
Eurasia. The species is found from northern Europe to sclerotized and recurved tip. The claspette stem is long
the Mediterranean area. and slender, and evenly curved. The claspette filament
222 10 Subfamily Culicinae

Fig. 10.34 Hypopygium of Oc. cyprius

is more than half as long as the stem, slightly triangular, Fig. 10.35 Larva of Oc. cyprius
and unilaterally winged from the base, without a stalk.
The aedeagus is elongated and pear shaped with a and adults were caught resting nearby on a flooded
narrow opening at the apex. meadow surrounded by a deciduous forest (Dahl 1975).
Larva: The entire body is densely covered with The larvae occur together with Oc. flavescens, Oc.
dark spicules (Fig. 8.19a), which identifies the large excrucians, Oc. cantans, and Oc. riparius. Adults
larvae from all other European Aedes and Ochlerotatus appear until July and from more eastern areas the spe-
species. The antennae are shorter than the head, and cies is recorded as being a mid spring species
the antennal seta (1-A) has 1–3 branches. The inner (Gutsevich et al. 1974). The females are aggressive
and median frontal setae (5-C and 6-C) are single or biters, they can attack their hosts in sunlit situations
double. The prothoracic setae according to Peus (1937) (Peus 1937). In Siberia Oc. cyprius is sometimes a
follow the formula: 1 and 2 (single); 3 (2-branched); 4 vicious biter (Gutsevich et al. 1974).
(single, short); 5 (2-branched); 6 (single); 7 Distribution: It is a rare species in western European
(3-branched). The number of comb scales is 9–15 regions, reported in Sweden, Finland, Germany,
arranged in an irregular row (Fig. 10.35). The siphon is Slovakia, and Poland. It can also be found along the
long and slender, and moderately tapering. The pecten eastern shores of the Baltic Sea, the eastern distribu-
usually has 19–21 pecten teeth, with several distal tion range stretches from the Ukrainian steppe to
teeth detached. Each individual pecten tooth has many Central Kazaksthan.
lateral denticles. The siphonal tuft (1-S) is situated
beyond the distalmost pecten tooth, with three to four
branches. The anal segment is not encircled by the Ochlerotatus Detritus Complex
saddle, the saddle seta (1-X) is about as long as the
saddle, the number of precratal tufts (4-X) is 4–5, and Laboratory studies carried out using isoenzyme identi-
the anal papillae are longer than the saddle. fication techniques gave evidence for the existence of
Biology: The species hibernates in the egg stage. sibling species within the complex (Pasteur et al.
Larvae occur in semipermanent pools along inundated 1977). The “species A” and “species B”, as they were
river shores and in snow-melt pools. Peus (1937) found then called, occurred sympatrically in the Carmargue
the larvae always in the middle of the pools with an and showed reproductive isolation. Further ecological
average water depth of 50–80 cm and regarded the spe- and distributional differences between the apparently
cies as preferring cold water for development. In morphologically identical siblings, e.g. frequent auto-
Sweden one larva was found in late May in a cold well genity in “species A” which is an exception in “species
10.2 Genus Ochlerotatus Lynch Arribalzaga 223

B”, have been recorded (Agoulon et al. 1997; Schaffner

1998); “species A” has finally been named coluzzii
(Rioux et al. 1998).

Ochlerotatus (Ochlerotatus) detritus

(Haliday 1833)

Female: The species is easily distinguished from all

other Ochlerotatus members with unringed tarsi by its
abdominal colouration. The apical parts of the terga are
usually covered with dark and pale scales, with dark
scales predominating on the first segments and pale
scales on the last segments. The proboscis and palps
have dark and pale scales intermixed, and the clypeus
is black. The vertex has yellowish white narrow curved
scales and blackish brown erect forked scales. The Fig. 10.36 Hypopygium of Oc. detritus
integument of the scutum is brown, and more or less
uniformly covered with yellowish brown scales, lighter
on the posterior part. Stout black setae are more numer- slightly bent from the end of the stalk on. The convex
ous above the wing bases. The scutellum has patches side of the filament is evenly widened from about its
of yellowish white scales on each lobe. The integu- middle. The aedeagus is small and oval.
ment of the pleurites is dark brown with patches of Larva: The head is broader than long. The antenna
broad, flat yellowish white scales. The mesepimeral is short, about half the length of the head, slightly
scale patch does not reach the lower margin of the curved and moderately spiculate. The antennal seta
mesepimeron, and lower mesepimeral setae are (1-A) is inserted at about the middle of the antennal
­present. The anterior part of the fore and mid femora shaft, with 5–8 branches. The postclypeal seta (4-C)
are conspicuously speckled with pale scales, the tibiae has 2–3 thin and short branches. The inner and median
and tarsi have dark scales and more or less numerous frontal setae (5-C and 6-C) are usually 2–3 branched,
scattered pale scales, pale tarsal rings are absent. The 5-C may rarely have 3–5 branches, but is always situ-
wing veins are covered with broad pale and dark scales, ated behind 6-C. The outer frontal seta (7-C) has
sometimes the pale scaling is reduced. The abdominal 7–12 branches. The comb consists of more than 40
terga have pale transverse basal bands of more or less scales, usually 45–60, arranged in a triangular patch,
uniform width, the apical parts of the terga have dark each individual scale is blunt ended and fringed with
and pale scales intermixed (Fig. 6.38a). The sterna are spines of more or less the same length (Fig. 8.37a).
mostly pale scaled. The siphon slightly tapers from the middle, and the
Male: The lateral lobes of tergum IX have 3–8 siphonal index is 2.2–2.8 (Fig. 10.37). The pecten is
straight, spine-like setae. The gonocoxite is about three composed of about 20 (18–27) evenly spaced teeth,
times as long as it is wide (Fig. 10.36). The basal lobe rarely the distalmost tooth may be slightly detached;
is more or less conical, and covered with fine setae and each pecten tooth has 2–3 ventral denticles. The
arranged in an irregular row and 1 conspicuous strong siphonal tuft (1-S) is inserted at about the middle of
spine-like seta, which is curved apically. The apical the siphon, beyond the distalmost pecten tooth, with
lobe is well developed carrying straight setae of mod- 6–10 (usually 8) branches. The saddle reaches more
erate length. The gonostylus is curved, tapers apically, than half way down the sides of the anal segment.
and the apical spine of the gonostylus is long. The The saddle seta (1-X) is single, and about as long as
paraproct is well sclerotized in the apical part. The the saddle. The upper anal seta (2-X) has 8–11
claspettes have a short stem, the distal third of the stem branches, and the lower anal seta (3-X) is single and
is sometimes constricted. The claspette filament is as longer than the siphon. The ventral brush has 1–3
long as or longer than the stem, with a long stalk, and precratal setae (4-X), but most often only 1 precratal
224 10 Subfamily Culicinae

May until September (Martini 1931; Mohrig 1969).

The females are persistent biters and readily attack
humans, often in large numbers. They may feed during
the day, but are predominantly active at dusk. Rioux
(1958) considered Oc. detritus as a typical exophilic
species which enters buildings only occasionally, but
Cranston et al. (1987) reported frequent entering of
houses to feed (endophagy), although no resting
indoors. Along with Oc. caspius, Oc. detritus is the
most common coastal species in Europe causing con-
siderable annoyance in villages at the seaside and in
their vicinity. Migration distances of about 6 km are
recorded from Britain (Marshall 1938), in southern
France the flight range of Oc. detritus is estimated to
be approximately 20 km (Rioux 1958). The differences
in the biology and behaviour might be attributed to the
presence of sibling species of the complex.
Distribution: Oc. detritus is a Palaearctic species,
Fig. 10.37 Larva of Oc. detritus it occurs along most of the European coast lines, e.g.
Northern and Baltic Sea as well as the Atlantic Ocean
and around the Mediterranean bassin. Furthermore the
seta is present. The anal papillae are very short and species has a scattered distribution in saline inland
rounded. areas in Europe, northern Africa, and southwest Asia.
Biology: Oc. detritus is a polycyclic species which It is possible that the southern range of its distribution
may have up to three generations per year, according is dominated by the sibling species Oc. coluzzii.
to the latitude of its occurrence. Usually the species
hibernates in the egg stage (Gutsevich et al. 1974) and
the first larvae occur some weeks later than the major- Ochlerotatus (Ochlerotatus) diantaeus
ity of the typical snow-melt mosquitoes, when the (Howard, Dyar and Knab 1913)
water temperature of the breeding sites exceeds 10°C
(Martini 1931; Mohrig 1969). Hibernating larvae were Female: The large dark legged female has a dark
reported from England, late hatching larvae developed brown to greyish integument, golden brownish setae
into the fourth-instar during autumn and did not pupate and scales and some blackish brown scaling with a
before March of the next year (Service 1968b). Oc. slight metallic shine. The proboscis and palps are
detritus is a typical halophilic species and the larvae blackish brown. The head has pale golden setae
occur almost exclusively in breeding habitats with an between the eyes and golden, narrow, curved and erect
exceptionally high content of salinity, only occasion- forked scales on the vertex and occiput. The scutum
ally they are found in fresh water. Preferred breeding has narrow pale golden or whitish scales and a broad
sites are brackish waters in estuaries and coastal median or two slightly divided dorsocentral stripes of
marshes. Larvae can be found in semipermanent ponds narrow dark bronze scales and an anterolateral dark
in open Salicornia and Tamarix marshes (depending stripe. The postpronotum has pale yellow or whitish
on fluctuation of the water level), and in stagnant drain- narrow curved scales. The postprocoxal and hypostig-
age channels or lagoons, with little aquatic vegetation. mal scale patches are absent. The upper mesepisternal
They are sometimes found together with larvae of Oc. patch of white broad scales does not reach the anterior
caspius and Oc. dorsalis, but more often, due to the margin of the mesepisternum, and the lower edge of
tolerance of extreme salinity, the species occurs alone the patch ends slightly above the level of the anterior
in its breeding site. Adults can be found from late angle (Fig. 6.45a). The mesepimeral patch does not
March until November in England (Cranston et al. reach the lower margin of the mesepimeron. The pleu-
1987), in central Europe they are recorded from early ral setae are pale golden. The coxae have white broad
10.2 Genus Ochlerotatus Lynch Arribalzaga 225

scales and yellowish setae. The fore and mid femora half of the gonocoxite. The gonostylus is slender and
are dark scaled anteriorly, white scaled posteriorly, curved with a long apical spine, and usually one addi-
sometimes with basal whitish scaling. The hind femur tional seta close to the apex. The paraproct has broad
has more dominant basal white scaling, and a whitish sclerotization. The claspette stem has a thorn-like pro-
knee spot. The tibiae and tarsomeres are entirely dark cess beyond the middle. The claspette filament is broad
scaled. The wing veins are covered with dark scales. and somewhat crescent shaped. The aedeagus is pear
The abdominal terga have dark scales, sparsely inter- shaped.
mixed with white scales and with large white triangu- Larva: The larvae differ from all other European
lar lateral patches. The lateral patches are connected Aedes and Ochlerotatus species by the antennae, which
by distinct white basal bands at least on terga IV–VII, are distinctly longer than the head (Fig. 8.17a). The
and sometimes narrow white basal bands are present head is broad, the antennae have numerous spicules.
also on terga II and III. The sterna have whitish scales, The antennal seta (1-A) has 2–4 long branches. The
with indistinct dark triangular scale patches apically. inner and median frontal setae (5-C and 6-C) have 2–5
Segment VIII and the cerci are entirely black scaled. branches. The thorax has the prothoracic formula 1-P
Male: Tergum IX has 6–8 strong, spine-like setae to 7-P as follows: 1 and 2 (single); 3 (2-branched); 4–6
on each lobe. The hypopygium shows two characteris- (single); 7 (2-branched). The comb has 8–13 scales,
tics which distinguish it from that of the other mem- each individual scale with a long and strong median
bers of the Intrudens Group (Fig. 10.38). The first is spine. The siphon is long and tapering, the siphonal
the group of dense setae on the inner apical surface of index is 3.2–3.7 (Fig. 10.39). The last two pecten teeth
the gonocoxite and the second is the distinct shape of are apically detached, and the siphonal tuft (1-S) is
the claspette filament. The basal lobe of the gonocoxite inserted beyond the distalmost pecten tooth, usually
bears three spine-like setae, two of them located close with 7–8 branches. The anal segment is not completely
together at about the middle of the gonocoxite, and the encircled by the saddle, but the saddle reaches far
third one is widely displaced towards the base of the down the lateral sides. The saddle seta (1-X) is single,
gonocoxite. The apical lobe is well developed. Dense and shorter than the saddle. The lower anal seta (2-X)
long inwardly directed setae are located on the apical is single and usually longer than the siphon. The ventral

Fig. 10.38 Hypopygium of Oc. diantaeus Fig. 10.39 Larva of Oc. diantaeus
226 10 Subfamily Culicinae

brush has 2–3 precratal setae (4-X). The anal papillae to the apical portion of the costa (C), R1, R3 and forked
are very long and slender, and longer than the saddle. portions of media (M) and cubitus (Cu). The basal
Biology: The species hibernates in the egg stage quarter of the costa is exclusively white scaled, a char-
and is monocyclic. Larvae occur early in spring in tem- acter which can be used to distiguish the species from
porary water bodies formed after snow-melt. They Oc. caspius. The abdominal terga have a whitish grey
may be found in boggy localities, in shaded ditches longitudinal stripe which may not be present on all
and pools in mixed forests, or in open water pools in segments. Indistinct, narrow basal and apical light
more northern and taiga areas. Usually the bottom of transverse bands of more or less uniform width are
the breeding sites is covered with abundant leaf debris. present. Blackish brown or black scales are restricted
Wood et al. (1979) suggest that the exceptionally long to two rectangular areas on terga I–V, terga VI and VII
antennae might indicate a peculiar feeding behaviour. are mostly light scaled.
The larvae tolerate acidic conditions and occur together Male: The hypopygium is very similar to that of
with several common species, such as Oc. cantans, Oc. Oc. caspius (Fig. 10.40). The basal lobe of the gono-
cataphylla, Oc. communis, Oc. pionips, Oc. punctor, coxite is constricted at the base with two widely sepa-
and Cs. morsitans. The adults emerge later than those rated spine-like setae. The apex of the longer seta is
of Oc. communis, owing to delayed larval development sometimes not hook shaped, otherwise the tip does not
(Gutsevich et al. 1974). Males can be attracted to mam- extend backwards to more than one third of the spine
mals where females are present and biting (Jaenson (Fig. 7.35b). The shorter spine-like seta is straight. The
1985). Females have been reported to feed on humans apical lobe is inconspicious, and usually covered with
in southeastern Russia. numerous setae. The claspette filament is shorter than
Distribution: A northern Holarctic species, it the stem, and strongly curved.
occurs in central and northern Europe and does extend Larva: The characteristics separating larvae of
into the taiga and the subarctic zone. It can be found in Oc. dorsalis from those of Oc. leucomelas and Oc.
the southeastern parts of Russia and is also recorded caspius are not very obvious. The antenna is about
from Canada and northernmost United States. half as long as the head, with sparse spicules. The
antennal seta (1-A) has 4–7 branches articulated in
the middle of the antennal shaft or slightly below it,
Ochlerotatus (Ochlerotatus) dorsalis and is not more than half as long as the antenna. The
(Meigen 1830) postclypeal seta (4-C) is short, with 2–5 thin branches.
The inner frontal seta (5-C) is situated posterior
Female: Most easily distinguished from the similar
Oc. caspius by its scutal markings and colouration. The
scale pattern on the scutum can be variable, but usually
is found as described below. The acrostichal and dors-
ocentral stripes on the scutum of Oc. dorsalis are fused
to form a dark brown median stripe extending to the
pale prescutellar dorsocentral stripes. Posteriorly the
stripe is ornamented with a pair of narrow, white lines.
There is also a well defined pair of dark posterior sub-
median stripes. The scales on the other areas of the
scutum are ashy white (Fig. 6.22c). Two distinct dors-
ocentral white stripes, which can be found on the
scutum of Oc. caspius, are always absent. The probos-
cis is covered with dark scales, sometimes with scat-
tered pale scales on its middle third. The pleural scales
are narrow, and creamy to straw coloured. The tarsom-
eres have pale rings both basally and apically
(Fig. 6.20b). The wing veins are predominantly covered
with light scales (Fig. 6.22d). Dark scales are restricted Fig. 10.40 Hypopygium of Oc. dorsalis
10.2 Genus Ochlerotatus Lynch Arribalzaga 227

to the median frontals (6-C), and both pairs are sin- times as long as the saddle in fresh water, but not
gle, or more frequently with 2 branches (in Nearctic more than 0.3–0.4 times the length of the saddle in
populations 5-C is usually single, rarely double on saline water (Gutsevich et al. 1974).
one side and 6-C is single). The outer frontal seta Biology: Oc. dorsalis is a polycyclic and halophilic
(7-C) has 4–8 branches (usually 5–6). Seta 1-M has 2 species that hibernates in the egg stage. There are usu-
long branches, which may be used as a characteristic ally 2–4 generations per year in central Europe depend-
to distinguish the species from Oc. caspius. The comb ing on the number of floodings. The larvae occur
has 13–35 (usually 20–25) scales arranged in 2–3 mainly in small, open water bodies and swamps, they
irregular rows (Fig. 10.41). The scales are variable in are found in permanent or temporary water bodies
shape, as in Oc. caspius. The siphonal index is 2.5– formed by melted snow, floods, rainfall or groundwa-
3.0, rarely less. The pecten has 14–23 evenly or ter such as inland pastures, roadside and drainage
slightly irregularly spaced teeth not reaching the mid- ditches. Females preferably oviposit around saline
dle of the siphon. The siphonal tuft (1-S) has 3–8 water bodies but the ground near fresh waters can be
(usually 4–5) branches, and is inserted in the middle chosen as well. The larvae can be found in waters with
of the siphon or slightly below it, usually closer to the a salt content of up to 12% and a pH value which
base than in Oc. caspius. The saddle is reduced to the ranges from 7.0 to 9.3 (Chapman 1960). They are
dorsal half of the anal segment, is strongly pigmented numerous in the Atlantic and Mediterranean coastal
and with a sharply defined lower margin. The saddle marshes but prefer inland saline areas in the Palaearctic
seta (1-X) is half as long as the saddle. The anal papil- region (Bozicic-Lothrop 1988). Adults can be very
lae are rounded, their length greatly varies with the numerous in some localities such as river valleys,
salinity of the breeding water. They are about 1.3 saline ponds, and lakes. The females attack humans
readily inflicting painful bites (Richards 1956). They
are also characteristic of open habitats in mixed forests
and pastures. Blood-searching activity is recorded
from 9 to 30°C and 52 to 92% relative humidity in the
southern part of central Europe (Petric 1989). The peak
of daily biting activity occurs in late afternoon and
early evening, but females can be quite active during
the night also. They can also search for blood during
the day in open areas (Cranston et al. 1987). Females
are exophagic but readily enter houses, tents, and
wards (Waterston 1918). Autogeny is rare, but was
detected in Nevada (Chapman 1962).
Distribution: Oc. dorsalis is a widespread Holarctic
salt marsh species in Europe, central Asia, China,
northern Russia, and North America. In Europe the
distribution range extends north to Scandinavia (Natvig
1948) and south to Greece (Pandazis 1935).
Medical importance: Oc. dorsalis transmits
Western Equine Encephalitis virus (WEE), St. Louis
Encephalitis virus (SLE), California Encephalitis virus
(CE) in the United States (Hammon and Reeves 1945;
Hammon et al. 1952). Japanese Encephalitis virus
(JE), and the bacterium Francisella tularensis, the
causative agent of tularemia, were isolated from natu-
ral populations (Detinova and Smelova 1973).
Note on systematics: Three species closely related
to Oc. dorsalis are the Nearctic Oc. melanimon and
Fig. 10.41 Larva of Oc. dorsalis Oc. campestris as well as the Palaearctic Oc. caspius.
228 10 Subfamily Culicinae

The current status of Oc. dorsalis is discussed under The white lateral stripes are sometimes indistinct, and
the description of Oc. caspius. the transverse suture is covered with clearly visible
stripes of white scales. The abdominal terga of Oc.
euedes have dark scales and narrow basal bands at least
Ochlerotatus Excrucians Complex on the first segments, otherwise median and lateral
patches of white scales and sometimes narrow apical
The complex is composed of the Holartic species Oc. white bands are present. The cerci are dark with scat-
excrucians and Oc. euedes, some other Neartic species, tered light scales.
e.g. Oc. aloponotum, and the Palaearctic, European spe- Male: The hypopygium is similar to those of the
cies Oc. surcoufi. The current status of the sibling spe- other members of the complex (Fig. 10.42). The only
cies within the complex is rather unsatisfactory. There difference may be found in the shape of the apical lobe.
exists a great variation between populations from differ- In Oc. euedes it is well developed, usually protruding
ent geographical areas. Apart from differences in the above the level of the gonostylus articulation, whereas
general body colouration of females of Oc. excrucians, the apical lobe in Oc. excrucians and Oc. surcoufi usu-
the shape of the tarsal claw also varies in populations ally does not reach the articulation of the gonostylus.
within both North America and Europe (Wood et al. Larva: The large larvae are very similar to those of
1979; Dahl 1984). The variation is expressed by the Oc. excrucians (Fig. 10.43). The number of comb scales
angle formed between the main and the subbasal tooth, is 11–19 arranged in 2–3 irregular rows. The siphon is
as well as the degree of bending of the former. The more evenly tapered from the base to the apex, and not as
“wide type” claw described by Wood et al. (1979) as a abruptly narrowed as in Oc. excrucians. The distalmost
southern Canadian variant of Oc. excucians is quite pecten tooth is situated well beyond the middle of the
similar to some specimens from Italy, France and siphon, almost reaching 1-S. The siphonal tuft (1-S) is
Germany, designated as Oc. surcoufi by Arnaud et al. inserted distinctly beyond the middle of the siphon, and
(1976), another “wide type” variant was also found in the branches of 1-S are shorter than in Oc. excrucians.
Sweden (Dahl 1984). Further confusion arises because Biology: The species is monocyclic and hibernates
the European members of the complex, Oc. excrucians, in the egg stage. In Europe, it breeds in the same kind
Oc. surcoufi and Oc. euedes, are not very well studied. of habitats and occurs at the same time as Oc. excru-
However, Arnaud et al. (1976) suggested the substitu- cians, Oc. cantans, and Oc. annulipes.
tion of all earlier Oc. excrucians records in Europe by its
European form Oc. surcoufi. As no worldwide compari-
son of geographic variations and redescriptions of all
stages of the species in question has been carried out,
this suggestion has not been followed.

Ochlerotatus (Ochlerotatus) euedes

(Howard, Dyar and Knab 1913)

Female: For separation from Oc. excrucians refer to

the description of Oc. surcoufi. Oc. euedes is usually
distinguished from the latter species by the scutal scale
pattern. In Oc. euedes the dorsocentral stripes of pale
scales start at some distance from the anterior margin of
the scutum and extend to the transverse suture. The
pale lateral stripes continue over the transverse suture
and reach the end of the dorsocentral stripes (Fig. 6.35b).
In Oc. surcoufi the dorsocentral stripes of pale scales
usually start at about the level of the ­transverse suture
and reach close to the posterior ­margin of the scutum. Fig. 10.42 Hypopygium of Oc. euedes
10.2 Genus Ochlerotatus Lynch Arribalzaga 229

subbasal tooth. The integument colour varies from dark

in northern specimens to brownish in more southern
ones. The colour of scales varies from white to creamy
white, and the dark scales from nearly black to very
dark brown. The body setae are mostly brownish
golden. The proboscis is dark scaled, sometimes with
a white scale patch in the middle. The palps have white
rings at the basal part of palpomeres I and II. The head
has some prominent blackish to bronze erect forked
scales. The vertex and occiput have mixed scaling, and
a more or less expressed white median stripe and a
regular dark spot laterally. The scutum is covered with
narrow, bronze scales, which are usually lighter on the
lateral parts, sometimes with an indistinct broad
median stripe of darker scales. The upper postprono-
tum has bronze, narrow scales and a patch of broad
white ones at the lower part. A postprocoxal patch is
present, and distinct white subspiracular and postspi-
racular patches are usually present. In northern speci-
mens the mesepisternum is covered with three distinct
white patches. The variability in southern populations
Fig. 10.43 Larva of Oc. euedes is expressed by a larger median patch which may be
fused with the lower patch. The mesepimeron has a
Distribution: Reported in the eastern and northern white patch which occupies half of the sclerite, but
states of the United States and Canada (Wood et al. never reaches its lower margins. The femora are thor-
1979; Darsie and Ward 1981). In Europe it has been oughly whitish scaled with a few dark scales and dark,
recorded from southern Scandinavia and, sometimes irregular bands close to the white knee spots. The tib-
under the synonym of Oc. beklemeshevi Denisova iae have mixed scaling, which on the fore and mid leg
1955, from Finland, Poland, Lithuania, and European is somewhat lighter, and the amount of white and dark
Russia (Snow and Ramsdale 1999). Very little scales may vary. Tarsomere I of all the legs has mixed
European material is available. scales and more or less well defined white basal rings,
Medical importance: Alphavirus has been reported tarsomeres II–IV have well defined white rings, except
from Oc. euedes in central Russia (Lundström 1999). for the fore leg, which has an entirely dark scaled tar-
Note on systematics: Oc. euedes Howard, Dyar and somere IV. Tarsomere V of the hind leg has a white
Knab 1913, was resurrected from synonymy of Oc. basal ring. The fore leg has the main tooth of the unguis
excrucians and regarded as a separate species. At the sharply bent, almost parallel to the subbasal tooth.
same time, Oc. beklemishevi Denisova 1955, reported However, in northern parts of Europe a “wider” form
from the former USSR and Poland, was put under syn- exists, which nevertheless has the typical bent charac-
onymy of Oc. euedes (Wood 1977; Knight 1978). teristic of an Oc. excrucians unguis (Fig. 6.32a). The
wing veins are mainly dark scaled, with pale scales
usually present on the costa (C) and subcosta (Sc), and
Ochlerotatus (Ochlerotatus) excrucians the other veins with a variable amount of pale scales.
(Walker 1856) The terga are dark scaled, with narrow pale basal bands
or patches and more or less numerous scattered pale
Female: A large species, similar in size and body scale scales in the apical part (Fig. 6.31b). The irregular yel-
patterns to Oc. euedes and Oc. surcoufi. The best iden- lowish basal bands of the terga, which may extend lat-
tification character for females of Oc. excrucians is the erally on the last segments, may be a distinct feature of
shape of the fore unguis, which is bent in a sharp angle the northernmost populations. The sterna are nearly
with a very narrow space between the unguis and the entirely whitish scaled, with the exception of sterna
230 10 Subfamily Culicinae

II–V which have dark apical edges, and the cerci have abdominal seta 6 of segments I and II (6-I and 6-II)
dark scales. has 2 branches, but is single on the rest of the seg-
Male: The hypopygium of Oc. excrucians is very ments (Fig. 8.54a). The number of comb scales is
similar to those of Oc. euedes and Oc. surcoufi 30–38 arranged in a more or less triangular patch,
(Fig. 10.44). From the latter species it has not been each individual scale with a conspicuous median
separated in much of the European material. The spine. The siphonal index is 3.4–4.5, and the distal
lobes of tergum IX bear 5–7 more or less stout setae. part of the siphon is distinctly tapered (Fig. 10.45).
The basal lobe of the gonocoxite is flat, moderately The pecten has 15–24 pecten teeth, with 1-3 teeth
developed or indistinct, almost absent. It is covered apically detached. The siphonal tuft (1-S) is posi-
with many short setae of similar length and thick- tioned at about the middle of the siphon, beyond the
ness. The apical lobe usually does not reach the distalmost pecten tooth, with 6 long branches. Seta
articulation of the gonostylus. The gonostylus is 9-S is thickened and transformed into a prominent
slender, curved apically, and somewhat flattened hook. The saddle extends beyond the middle of the
with a moderate long apical spine. The claspette lateral part of the anal segment. The ventral brush
stem is slender, tapers apically, and the claspette fila- has 4–6 precratal tufts (4-X). The anal papillae are
ment gradually tapers towards the apex. The aedea- slender, and longer than the saddle.
gus is elongated. Biology: The larvae start to hatch from the over-
Larva: Large in size, the antenna is shorter than wintering eggs in early spring. More often they hatch
the head with well developed spicules. The antennal later in the year and can be found until the middle of
seta (1-A) is inserted at about the middle of the summer in shaded, permanent pools. Only one genera-
antennal shaft. The postclypeal seta (4-C) has 2–3 tion has been recorded from all the different habitats.
short, thin branches. The inner frontal seta (5-C) has They occur in greater numbers in open semipermanent
2–3 branches, the median frontal seta (6-C) has 2 or permanent pools or pits with vegetation like Typha
branches, and the outer frontal seta (7-C) has 6–7 sp. or Carex sp. together with larvae of Oc. cantans
branches. The prothoracic formula 1-P to 7-P is as and Ae. cinereus. They can also be found in less abun-
follows: 1 (double, long); 2 (single, medium long); 3 dance in a variety of other habitats, especially in mixed
(4–5 very thin, short branches); 4 (medium long, forest regions. Larvae have been observed to feed upon
thin); 5 and 6 (long, single); 7 (3-branched). The Euglena sp. and larger protozoans. Larval ­development

Fig. 10.44 Hypopygium of Oc. excrucians Fig. 10.45 Larva of Oc. excrucians
10.2 Genus Ochlerotatus Lynch Arribalzaga 231

can last from a few to many weeks depending on the

water temperature. The females are fierce day biters
(for that reason they got the name excrucians) and can
be found until autumn.
Distribution: Oc. excrucians is a Holarctic species.
Its actual distribution for central and southern Europe
is difficult to state, as some earlier records may contain
a mixture of sibling species.

Ochlerotatus (Ochlerotatus) surcoufi

(Theobald 1912)

Female: Very similar to Oc. excrucians. The most

reliable characteristic to distinguish between
females of these species is found in the tarsal claws
of the fore leg. In Oc. surcoufi the main tooth is
evenly curved, and the subbasal tooth is diverging,
not parallel. The abdominal terga have mixed light
and dark scales. Tergum I has a white patch, the
following terga have both basal and apical yellow-
ish bands. The apical bands are often reduced to a Fig. 10.46 Larva of Oc. surcoufi
narrow line, and the basal bands are sometimes lat-
erally irregular. Tergum VII has light scales
predominating.
Male: The hypopygium is very similar to that
of Oc. excrucians, apparently morphologically
identical. cussion of the Ochlerotatus Excrucians Complex the
Larva: Similar in most characteristics to Oc. excru- authors required biometric and genetic analysis of all
cians. A striking difference is found in setae 6 on sibling species to clarify their status.
abdominal segments I to VI (6-I to 6-VI) all of which
have 2 branches (Fig. 8.54b), whereas in Oc. excru-
cians only setae 6-I and 6-II have 2 branches, and setae Ochlerotatus (Ochlerotatus) flavescens
6-III to 6-VI are single. The siphon is long, and tapered (Müller 1764)
towards the apex, the siphonal index is 2.8–3.1
(Fig. 10.46). Seta 9-S is hooked, and not as strong as in Female: Oc. flavescens can be distinguished from
Oc. excrucians. The ventral brush has 5–6 precratal other Aedes and Ochlerotatus species by the abdomi-
tufts (4-X). nal terga which are almost entirely covered with light
Biology: In the Pyrenees, the species seems to occur scales, with only a few scattered dark scales, a charac-
in the same habitats as Oc. excrucians. The eggs and teristic, which is shared only with Oc. cyprius. The
larvae were found in inundation areas in a Pyrenean scutum of Oc. flavescens is covered with copper or
valley. Females were caught on humans in the same golden brown scales and the terga with straw coloured
habitat (Arnaud et al. 1976). scales, which are distinctly paler than the scutal scales.
Distribution: Oc. surcoufi has so far been reported In contrast, Oc. cyprius has golden yellowish scales on
in France (near Paris and the eastern Pyrenees), and on the scutum and usually ochre yellowish scales on the
material from Germany and Italy according to Arnaud terga, with the scutum and terga being of more or less
et al. (1976). the same colour. The proboscis and palps of Oc. flave-
Note on systematics: The species has been resur- scens have dark and yellowish scales, with the yellow-
rected from synonymy with Oc. excrucians based on ish scales on the proboscis less numerous in the distal
European material by Arnaud et al. (1976). In their dis- half. The vertex and occiput have narrow golden scales
232 10 Subfamily Culicinae

and brown erect forked scales, and broad cream ­coloured

scales laterally. The scutellum has narrow yellowish or
light brown scales and brown setae on the lobes. The
antepronotum has yellow bronze scales. The postpro-
notum has upper narrow, bronze scales, and lower
broader, cream coloured scales. The postprocoxal
membrane usually has a patch of pale scales. The
hypostigmal, subspiracular and postspiracular scale
patches are well developed. The mesepisternum has
pale yellow scales, the upper patch reaching its ante-
rior angle. Pale scales on the mesepimeron end slightly
before its lower margin, and lower mesepimeral setae
are absent (Fig. 6.29a). The femora are brown with
yellowish scales intermixed, pale on the posterior sur-
face. The tibiae are mostly yellow scaled, tarsomeres
II–IV of the mid and hind legs with broad basal rings
of whitish scales (Fig. 6.27c). The wing veins are cov-
ered with narrow yellowish scales and scattered dark
scales. The terga are covered with straw-coloured
scales, sometimes mixed with isolated dark scales
Fig. 10.47 Hypopygium of Oc. flavescens
(Fig. 6.28a). The sterna have pale yellowish scales.
Male: The lobes of tergum IX are short and narrow,
with 5–7 long spine-like setae. The basal lobe of the
gonocoxite is slightly flattened with a strong medially
directed spine and numerous short setae extending to
the middle of the gonocoxite (Fig. 10.47). The apical
lobe is prominent, and rounded apically. The gonosty-
lus is slightly expanded in the middle, and the apical
spine of the gonostylus is long and slender. The parap-
roct is strongly sclerotized, and pointed at the apex. The
claspette stem is short and straight, slightly tapered dis-
tally, with 2–3 long setae on the inner margin near the
base. The claspette filament is about as long as the
stem, with a cylindrical base and a plate shaped widen-
ing on the convex side of the filament, and the apex of
the filament is distinctly curved. The aedeagus is long,
cylindrical, and notched at the apex.
Larva: One of the largest Ochlerotatus larva. The
antennae are less than half as long as the head, and
entirely covered with distinct spicules. The antennal
seta (1-A) is located close to the middle of the antennal
shaft, with 5–8 branches reaching near the tip. The Fig. 10.48 Larva of Oc. flavescens
inner (5-C) and median (6-C) frontal setae have 2–4
branches, and the outer frontal setae (7-C) have 6–9 3.4–4.0. The pecten has 17–28 teeth not reaching to
branches. The number of comb scales is 17–36 (usu- the middle of the siphon, and 1 or 2 distal teeth may or
ally 20–27) arranged in three irregular rows (Fig. 10.48). may not be apically detached. The siphonal tuft (1-S)
Each individual scale has a strong median spine and has 4–7 branches, situated in the middle of the siphon,
several smaller spines at the side, which are about about as long as the width of the siphon at the point of
half as long as the median spine. The siphonal index is its origin. The saddle extends about 3/4 of the way
10.2 Genus Ochlerotatus Lynch Arribalzaga 233

down the sides of the anal segment. The saddle seta submedian stripes (Fig. 6.49b). The supraalar and scutel-
(1-X) is single and approximately as long as the sad- lar setae are yellowish or yellow brown. The prosternum
dle. The upper anal seta (2-X) has > 7 branches, and is scaled with yellow white scales, the upper 3/4 of the
the lower anal seta (3-X) is single and longer than the postpronotum with rust brown scales. The postprocoxal
siphon. The ventral brush has 18–19 tufts of cratal membrane has pale scales. A hypostigmal scale patch is
setae (4-X) and 5–7 precratal setae extending nearly to absent, the subspiracular patch is divided into an upper
the base of the segment. The anal papillae are usually and lower portion, and the postspiracular scale patch is
short, and about half as long as the saddle. well developed. The mesepisternum has a pale upper
Biology: Oc. flavescens usually produces only one patch extending to the anterior angle, narrowly sepa-
generation per year (Mihalyi 1959; Trpis 1962). After rated from the prealar patch, and the lower mesepister-
overwintering in the egg stage the larvae hatch during nal patch is confined to the posterior margin. The
spring time. They occur predominantly in reeded areas mesepimeron has yellowish scales extending to near the
which are not totally shaded. They can frequently be lower margin, and 1–3 mesepimeral setae are present.
found in brackish marshes along coasts (Gjullin et al. The femora are dark scaled, speckled with pale scales,
1961; Mohrig 1969), but also in partly shaded tempo- and pale on the posterior surface. The tibiae and tarsi are
rary fresh water ponds in floodplains (Hearle 1929; dark brown with scattered pale scales especially towards
Rempel 1953). The immature stages of this species are the apices of the tarsomeres, but pale basal rings on the
tolerant to a wide range of salinity. Usually they occur tarsomeres are absent. The wing veins are covered with
in neutral or slightly alkaline water, associated with lar- dark scales, and pale scales are present at the base of the
vae of Oc. cantans, Oc. leucomelas, Ae. rossicus, and costa (C), and subcosta (Sc) often forming a large patch.
Oc. sticticus. However, in saline water they can be The abdominal terga are dark scaled with basal bands of
found together with the larvae of Oc. detritus, Oc. cas- greyish white scales of uniform width, sometimes
pius, or Oc. dorsalis. The adults prefer open areas when slightly constricted in the middle (Fig. 6.48b). The sterna
they are searching for a blood meal. The biting peak of are covered with greyish pale scales.
adults occurs during dusk and dawn. Wesenberg-Lund Male: The colouration and scaling are much like
(1921) observed swarming of males near sunset, above the females except that the prosternum is not scaled.
nettles. Although Oc. flavescens is widely distributed it The hypopygium of Oc. hexodontus (Fig. 10.49) is
usually does not occur in great numbers. similar to that of Oc. punctor; see the description of
Distribution: It is a Holarctic species, reported the latter species.
from Eurasia and North America. In Europe the spe-
cies is widely distributed except for some Mediterranean
countries.

Ochlerotatus (Ochlerotatus) hexodontus

(Dyar 1916)

Female: A medium sized species, similar to that of Oc.

punctor, but can be distinguished from the latter by the
pale bands on abdominal sterna III–VI which are of uni-
form width or only slightly constricted in the middle
and the large patch of pale scales at the base of the costa
(C). The proboscis and palps are dark scaled, the palps
rarely with a few white scales. The head has narrow
dark brownish scales and erect forked scales dorsally.
The pedicel usually has some whitish scales. The scutum
is more or less uniformly covered with rusty brown or
yellowish brown scales, usually without a darker median
pattern, and occasionally with a pair of indistinct dark Fig. 10.49 Hypopygium of Oc. hexodontus
234 10 Subfamily Culicinae

Larva: Very similar to that of Oc. punctor, but may brush has 16–18 cratal setae (4-X) and 2, rarely 1, pre-
be distiguished from the latter by the size and number cratal setae. The anal papillae are lanceolate, and usu-
of comb scales. In Oc. hexodontus the number of comb ally twice as long as the saddle or longer.
scales is usually 6–9, the individual scales are large, Biology: Oc. hexodontus is a monocyclic species
and usually longer than the distalmost pecten tooth. In which is one of the dominant mosquitoes in areas with
Oc. punctor the number of comb scales is > 10, and long severe winters and short summers. The species
individual scales are shorter than the distal three pecten occurs in tundra areas close to the tree border where
teeth. In Nearctic populations there also exist differ- the numerous immature stages develop in oligotrophic
ences in the thoracal setation (Wood et al. 1979), which snow-melt ponds. In high mountain regions, the larvae
is probably also true for European populations. In Oc. can be found in small snow-melt pools with little or no
hexodontus seta 5-P is branched and setae 1-M, 1-T vegetation. The larvae hatch at water temperatures of
and 3-T are usually short and multiple branched. In just above 0°C. The larvae are frequently found associ-
Oc. punctor seta 5-P is usually single, and 1-M, 1-T ated with those of other snow-melt mosquitoes, such
and 3-T are longer and usually single or double. Oc. as Oc. communis, Oc. punctor, Oc. pionips, and Oc.
hexodontus has antennae much shorter than the head, pullatus. The adults of Oc. hexodontus can also occur
and the antennal seta (1-A) is small, and inserted in mountainous regions close to the tree border and
slightly below the middle of the antennal shaft, with furthermore, in larger numbers if the number of the
multiple branches not reaching to the tip. The inner other species has already decreased. The females are
(5-C) and median (6-C) frontal setae are usually single, very aggressive biters and may approach their hosts
rarely with 2 branches, and the outer frontal setae (7-C) even during strong winds.
have 3–6 branches. The siphon is straight, tapers in the Distribution: Oc. hexodontus is a Holarctic spe-
apical half, and the siphonal index is about 3.0 cies found in North America and Eurasia, from north-
(Fig. 10.50). The pecten has 12–22 evenly spaced teeth ern Scandinavia to eastern Siberia, subarctic tundra,
situated in the basal half of the siphon. The siphonal and taiga, and above the tree line in mountainous
tuft (1-S) is located beyond the distalmost pecten tooth, regions.
usually with 4–5 branches. The anal segment is entirely
encircled by the saddle, and the saddle seta (1-X) is
single and about as long as the saddle. The ventral Ochlerotatus (Ochlerotatus) hungaricus
(Mihalyi 1955)

Female: A small species, with blackish brown scaled

proboscis and palps. The occiput has narrow whitish
scales dorsally and broad whitish scales and scattered
dark scales laterally, which may form a small patch.
The scutum is covered with greyish white scales and a
median stripe of dark brown scales, which is divided
into two prescutellar dorsocentral stripes not reaching
the posterior margin of the scutum. The scutellum has
pale narrow scales and light and dark brown setae on
the lobes. The postprocoxal membrane is without
scales, and a hypostigmal scale patch is absent. The
upper mesepisternal scale patch reaches the anterior
angle of the mesepisternum, and the mesepimeral scale
patch does not reach the lower margin of the mesepim-
eron. The femora of the fore legs are predominantly
pale scaled in the basal half, and the tibiae of the hind
legs have dark scales on the anterior surface. The tar-
someres are dark scaled, and pale basal rings are
Fig. 10.50 Larva of Oc. hexodontus absent. The wing veins are covered with dark scales,
10.2 Genus Ochlerotatus Lynch Arribalzaga 235

and a few isolated pale scales may be present at the

base of the costa (C). The abdominal terga have black-
ish brown scales and pale basal bands which are
slightly narrower in the middle and connected with
pale lateral triangular patches. The sterna have whitish
scales and broad apical dark bands.
Male: The gonocoxite is about three times as long
as it is wide at the base, and is covered with scales and
setae of different length (Fig. 10.51). The basal lobe of
the gonocoxite is well developed and conical, with 2
strong spine-like setae of different length and several
short setae. The longer spine is slightly curved in the
middle, the other spine is short and straight (Fig. 7.34b).
The apical lobe is weakly developed and indistinct,
with numerous short setae. The gonostylus gradually
tapers towards the apex, and the apical spine is moder-
ately long and slender. The paraproct is inwardly
curved and pointed. The claspette stem is short and
straight, the claspette filament has a long stalk and a
broad unilateral wing at the convex side. The aedeagus
is tubular shaped.
Larva: The head is very dark, blackish brown. The
antenna is slightly more than half as long as the head.
The antennal seta (1-A) is located distinctly below the Fig. 10.51 Hypopygium of Oc. hungaricus
middle of the antennal shaft, at about 1/3 of the length
from the base, with 5–8 branches. The inner frontal
seta (5-C) is single, the median frontal seta (6-C) has
1–2 branches, and the outer frontal seta (7-C) has 6–8
branches. The prothoracic formula (1-P to 7-P) is as
follows: 1 (long, single); 2 (medium long, single); 3
(short, 2–4 branched); 4 (short, single); 5 and 6 (long,
single); 7 (long, 2-branched). The comb has 16–24
(average 20) scales, arranged in 2 irregular rows
(Fig. 10.52). Each individual scale has a long median
spine and several shorter spines at the sides. The
siphon is cylindrical, only slightly tapering towards
the apex, and the siphonal index is 2.0–2.4. The pecten
has 19–24 evenly spaced teeth, reaching beyond the
middle of the siphon. Each pecten tooth has several
lateral denticles at its ventral margin. The siphonal
tuft (1-S) has 3–6 branches, situated well beyond the
middle of the siphon and well separated from the dis-
talmost pecten tooth. The saddle extends approxi-
mately half way down the sides of the anal segment,
and the saddle seta (1-X) is single and shorter than the
saddle. The upper anal seta (2-X) has 8–11 branches,
the lower anal seta (3-X) is single and longer than the
siphon. The ventral brush has 13–16 cratal setae (4-X)
and 3 precratal setae. The anal papillae are ­lanceolate, Fig. 10.52 Larva of Oc. hungaricus
236 10 Subfamily Culicinae

distinctly longer than the saddle, and the dorsal pair is circumpolar populations. The abdominal terga have
longer than the ventral pair. broad basal white bands.
Biology: Because the distribution range of the spe- Male: The lobes of tergum IX are rounded, with
cies seems to be limited, little is known about its biol- long setae. The gonocoxite has short setae predominat-
ogy. Larvae are typically found in the floodplains of ing on the inner side (Fig. 10.53). The basal lobe of the
larger river systems. Mihalyi (1961) collected the lar- gonocoxite is well developed, and conical, with one
vae in shaded floodwater pools under trees along the spine-like seta. The apical lobe is small and indistinct.
Danube river. The species has been found from April to The gonostylus is slender, and somewhat broadened in
September, thus more than one generation per year is the middle. The paraproct is broadly sclerotized. The
assumed. The females are severe biters and readily feed claspette filament is about as long as the stem, with a
on humans in shaded situations even during the day. unilateral wing, and the aedeagus is elongated.
Distribution: Oc. hungaricus has so far been Larva: The small fourth-instar larva can easily be
reported from Austria, Slovakia, and Hungary (Snow mistaken for earlier instars of Oc. hexodontus or Oc.
and Ramsdale 1999). punctor where the saddle is not fully developed and
does not encircle the anal segment. The antennae are
very short. The inner and median frontal setae (5-C and
Ochlerotatus (Ochlerotatus) impiger 6-C) are always single, and the outer frontal seta (7-C)
(Walker 1848) has 3 branches. The prothoracic formula 1-P to 7-P is
as follows: 1 (single or 2-branched, short); 2 (single,
Female: This small species may sometimes be mis- little longer); 3 (single, long); 4 (single, short); 5 (single
taken for small specimens of Oc. punctor. Its integu- or 2-branched, long); 6 (single, long); 7 (3-branched,
ment is brownish grey with conspicuously long and long). The number of comb scales is 10–14, each scale
black setae on the scutum. The proboscis and palps has a long median spine and several short spines at the
are entirely black scaled. The vertex has a spot of base. The siphonal index is 2.8–3.0. The pecten teeth
dark brown scales. The occiput is covered with erect are evenly spaced, each tooth with one long, lateral
black setae and white scales. The antenna is black, denticle (Fig. 10.54). The siphonal tuft (1-S) is situated
and the pedicel has some scattered white scales. The slightly below the middle of the siphon, with 4–6 long
scutum has a median stripe of bronze narrow scales, branches. The saddle covers approximately half of the
and a lateral stripe of white narrow scales. The scutel- anal segment. The ventral brush has 2 tufts of precratal
lum has white narrow scales. The postpronotum has a
few bronze scales, otherwise broad white scales, and
postpronotal setae are scattered on the entire postpro-
notum (Fig. 6.41a). A postprocoxal patch is present,
the subspiracular and postspiracular scale patches are
present, but a hypostigmal patch is absent. The num-
ber of postspiracular setae is 10 or fewer (Fig. 6.42b).
The mesepisternum has three, more or less, distinct
white scale patches, the middle one not reaching the
anterior margin. The mesepimeron has a large white
patch of scales. All the coxae have white scales, the
femora and tibiae of all the legs are dark with scat-
tered white scales, which are less numerous than in
Oc. nigripes, the tibiae have conspicuous black setae,
and all the tarsomeres are dark scaled. The tarsal
claws are sharply bent in the middle (Fig. 6.42a). The
wing veins are usually entirely dark scaled, a few
pale scales are sometimes present at the base of the
costa (C) and radius (R). The scaling of the legs and
wings seems to vary between Scandinavian and other Fig. 10.53 Hypopygium of Oc. impiger
10.2 Genus Ochlerotatus Lynch Arribalzaga 237

Ochlerotatus (Ochlerotatus) intrudens (Dyar 1919)

Female: A dark greyish species without metallic lustre

in the scales. The presence of a hypostigmal patch of
pale scales distinguishes the females from those of
Oc. communis, Oc. diantaeus, and Oc. nigrinus.
However, the patch is composed of a few scales,
which may often be rubbed off in old specimens. The
proboscis is black scaled, the palps have scattered
white scales, and the head has some pale golden setae
between the eyes and yellowish white narrow scales
on the vertex. The scutum has two dorsocentral stripes
of narrow curved bronze scales, divided by a narrow
pale acrostichal stripe, which is sometimes indistinct.
The anterior submedian and whole lateral areas are
covered with pale scales, and two distinct posterior
submedian dark stripes are present. The scutellum
has pale yellowish scales and setae. The postprono-
tum has yellowish-brown narrow curved scales and
some whitish scales at the posterior corner. The post-
procoxal patch is absent, and a hypostigmal patch is
usually present. The sub- and postspiracular areas
have patches of white scales. The upper mesepister-
nal patch of scales is small, and divided into two or
Fig. 10.54 Larva of Oc. impiger more portions, not reaching the anterior margin of the
mesepisternum. The prealar patch of scales is dis-
setae (4-X), and the anal papillae are longer than the placed apically, and the lower third of the mesepim-
saddle (Dahl 1997). eron is without scales. The lower mesepimeral setae
Biology: The species is monocyclic. The larvae are usually absent (Fig. 6.44b). The coxae have white
appear very early in the year and can be found in ponds scaling, the rest of the legs are almost entirely dark
at the borders of birch-willow shrubs in subarctic scaled, the fore femur sometimes with some scattered
areas. They develop fast in snow-melt ponds, prefera- white scales. The wing veins are almost entirely dark
bly with some rotten plant material on the bottom. The scaled, and the base of the costa (C) and radius (R)
small females are most obnoxious daytime biters in the sometimes have a few white scales. The abdominal
subarctic and arctic areas of Europe. Females bite soon terga are dark scaled, with distinct basal white
after emergence. However, they quickly leave their bands.
hosts and are thus not easy to catch on humans. The Male: The hypopygium is similar to those of Oc.
biology of the species, together with that of Oc. diantaeus and Oc. pullatus, but differs in the shape of
nigripes, has been more thoroughly studied in arctic the claspette stem and the setation on the apical half of
Canada (Wood et al. 1979). the gonocoxite (Fig. 10.55). The lobes of tergum IX
Distribution: Oc. impiger is a circumpolar species are prominent, with a row of 4–7 spine-like setae. The
and in North America it is found, together with Oc. basal lobe of the gonocoxite has 3 large setae which
nigripes, under extreme arctic conditions. It seems to are all spine-like, one of them well separated from the
have a more southern limit than the latter species. In others. The apical lobe of the gonocoxite is well devel-
Europe the distribution of Oc. impiger is restricted to oped, and a small subapical zone of the gonocoxite is
the tundra of Scandinavia, but its whole distribution covered with long dense setae directed more distally.
range is not well known; it has been recorded in south- The gonostylus is curved, and tapers towards the apex.
ern Norway (Natvig 1948) and in the tundra of Russia The claspette stem has a thorn shaped process at about
(Gutsevich et al. 1974). its middle. The claspette filament is strongly bent. The
238 10 Subfamily Culicinae

Fig. 10.55 Hypopygium of Oc. intrudens

aedeagus is pear shaped, relatively short and with a

wide opening.
Larva: The head is broader than long, and the
antenna is shorter than the head, and covered with
Fig. 10.56 Larva of Oc. intrudens
spicules. The antennal seta (1-A) is short and inserted
slightly below the middle of the antennal shaft. The
inner frontal seta (5-C) has 3–5, usually four branches
and the median frontal seta (6-C) has 3–5, usually are often found together with those of Oc. communis,
three branches (Fig. 8.35c). The number of comb Oc. diantaeus, and Oc. punctor, but they emerge
scales is 12–17, each individual scale is elongated and before any of these other species (Barr 1958; Wood
pointed with lateral spines along the basal part. The et al. 1979). The first adults occur from early spring to
siphon is long and slightly tapered (Fig. 10.56). Usually midsummer depending on the latitude. The females
2–3 distalmost pecten teeth are large, spine-like, with- are locally dominant, fierce biters which also enter
out lateral denticles and more widely spaced. The dis- houses.
talmost tooth may be located slightly beyond the point Distribution: It is a Holarctic species, recorded
of 1-S insertion. The siphonal tuft (1-S) is inserted from central to northern, and eastern to southeastern
slightly beyond the middle of the siphon. The anal seg- Europe, it occurs from the steppe in southeastern
ment is not entirely encircled by the saddle, the num- Europe to the taiga in the north. The distribution range
ber of precratal tufts (4-X) is 1–2, and the anal papillae does not seem to extend into western Europe.
are slender and longer than the saddle.
Biology: The species is monocyclic at least in the
northern parts of its distribution range. Whether it can Ochlerotatus (Ochlerotatus) leucomelas
have two generations in southern areas is not known. (Meigen 1804)
Eggs overwinter and larvae are found from early
spring to early summer in many types of temporary Female: Oc. leucomelas is similar to Oc. cataphylla in
pools, which can be located in forests, without sub- sharing the character of intermixed pale and dark
merged vegetation but covered with dead leaves at the scales on the wing veins, but differs from the latter in
bottom, or in more open areas in grassy or snow-melt the proboscis which is speckled with numerous pale
water pools as well as along floodplains. The larvae scales, whereas in Oc. cataphylla the proboscis is
10.2 Genus Ochlerotatus Lynch Arribalzaga 239

u­ niformly dark scaled. The palps are dark brown with ated in front of the inner frontal seta (5-C), and both
scattered pale scales. The vertex and occiput have nar- pairs are single, 5-C rarely with 2 branches, and the
row yellowish white scales and dark erect forked outer frontal seta (7-C) has 3–6 branches. The comb
scales, and pale decumbent scales at the sides. The consists of 18–30 scales (average 24) arranged in 2–3
scutum has golden bronze scales, the lateral and pres- irregular rows (Fig. 10.58). Each individual scale var-
cutellar areas usually have straw coloured scales. The ies in shape, the dorsal scales are without a long median
scutellum is dark brown with narrow yellowish white spine, the ventral scales have a prominent median
scales. The postpronotum has broad white scales, more spine, and both types have several spines at the sides.
yellowish in the upper part, and the scales of the pleu- The siphon tapers in the apical third, and the siphonal
rites and legs are as for Oc. cataphylla. The postpro- index is 2.5–3.1. The pecten has 13–18 (usually 15)
coxal membrane has a patch of pale scales. The
hypostigmal, subspiracular and postspiracular scale
patches are fused. The scales of the mesepisternum do
not extend to its anterior angle and the mesepimeral
scale patch ends slightly before its lower margin of the
sclerite, lower mesepimeral setae are present. The tib-
iae and tarsi are mostly dark scaled, with pale scales
especially on the ventral surface. The tarsi do not have
pale rings. The wings are covered with dark scales and
numerous scattered pale scales on all veins. The terga
have broad basal bands of white scales, the distal parts
are mainly dark scaled, and sometimes the last terga
are predominantly covered with white scales. The
sterna are almost entirely whitish scaled, with some
dark scales at the base.
Male: The lobes of tergum IX usually have > 10
short spine-like setae which are directed slightly out-
wards, in Oc. cataphylla these setae are usually less
numerous and directed distally. The gonocoxite is long
and slender, with numerous long setae on the inner sur-
face, and the basal setae do not overlap in the middle
(Fig. 10.57). The basal lobe is conical with a medially Fig. 10.57 Hypopygium of Oc. leucomelas
directed, apically strongly recurved long spine and
several long setae. The apical lobe of the gonocoxite is
well developed and rounded at the apex. The paraproct
is strongly sclerotized in the lateral parts, with an
inwardly pointed apex. The claspette stem is long and
slender, and strongly curved. The claspette filament is
very long, with a small plate shaped unilateral widen-
ing beginning at the base of the filament and ending
distinctly before the apex. The aedeagus is cylindrical
and notched at the apex.
Larva: The head is broader than long. The antennae
are nearly half as long as the head, with weakly devel-
oped spicules, usually ventrally located in rows. The
antennal seta (1-A) is located in the middle of the
antennal shaft with 3–6 branches which are half as
long as the antenna. The postclypeal seta (4-C) has 4
short branches, the median frontal seta (6-C) is situ- Fig. 10.58 Larva of Oc. leucomelas
240 10 Subfamily Culicinae

more or less evenly spaced teeth located in the basal all species have an apparently identical adaptation to
third of the siphon. The siphonal tuft (1-S) is situated breeding in rock pools along the Mediterranean coasts.
below the middle of the siphon with 3–8 branches. The The distribution range is western Mediterranean for
saddle extends down to 2/3 of the sides of the anal seg- Oc. mariae and eastern Mediterranean for Oc. zam-
ment, and the saddle seta (1-X) is nearly as long as the mitii and Oc. phoeniciae. The latter has been recorded
saddle. The lower anal seta (3-X) is single, the upper from the coasts of Cyprus, southeastern Turkey,
anal seta (2-X) has 4–9 branches, and is half as long as Lebanon and Israel (Coluzzi et al. 1974). No overlap
3-X. The ventral brush has 15–18 tufts of cratal setae between these distributional ranges has been recorded
(4-X) and 1–3 precratal setae. The shape of the cratal so far. According to the updated checklist of European
setae is characteristic, the branching of the tufts starts mosquitoes by Ramsdale and Snow (1999), Oc. mar-
far from the base, thus the stem of each tuft is very iae and Oc. zamitii correspond to the aforementioned
long. The anal papillae are not longer than the saddle geographical “isolation” within the Mediterranean
and are tapered apically, with the ventral pair shorter basin, except for the Greek record of Oc. marie, which
than the dorsal pair. most probably is Oc. zammitii.
Biology: Oc. leucomelas is a monocyclic snow-
melt mosquito. The larvae occur early in the year
after the snow-melt but seldom in extensive numbers. Ochlerotatus (Ochlerotatus) mariae
They are usually found at the edge of forests, in (Sergent and Sergent 1903)
flooded meadows or reeded areas together with larvae [Acartomyia mariae]
of Oc. cantans, Oc. communis, Oc. rusticus, Ae. ros-
sicus, and Oc. sticticus. In shadowed areas the num- Female: The species differs from Oc. caspius in the
ber of larvae usually decreases. They also occur in ornamentation of the scutum, the black scaling of the
slightly saline waters associated with Oc. detritus, legs, and in the absence of a longitudinal light stripe on
e.g. in flooded meadows along coasts, thus the larvae the abdomen. The proboscis is long and slender, with
are obviously tolerant to variations in the salinity of dark brown scales, sometimes mixed with whitish
the breeding sites. The pH can be slightly acidic to scales in the middle, giving the impression of being
alkaline (Natvig 1948). In central Europe the adults ringed. The palps are 1/6 of the length of the proboscis,
usually emerge in May and they decrease in numbers and covered predominantly with dark brown scales,
by early July. with a white tip and some scattered whitish and cream
Distribution: Oc. leucomelas is a European spe- coloured scales. The scutum is largely covered with
cies. It is mainly distributed in northern, central, and rust brown to golden scales, usually with some whitish
eastern Europe and has a limited distribution in the scales, which may sometimes form an indistinct, vari-
southern European countries, where it is solely reported able scutal pattern. The scutal setae are predominantly
in Spain. blackish brown. The scutellum has three groups of
white sickle shaped scales and golden brown or dark
setae. The pleurites have a brown integument and small
Ochlerotatus Mariae Complex patches of white scales. A postprocoxal patch of white
scales is present. The ventral surfaces of the femora are
Three sibling species, Oc. mariae, Oc. zammitii, and white scaled, and the anterior surfaces and tibiae are
Oc. phoeniciae [Acartomyia phoeniciae], have been predominantly dark scaled with speckled white scales.
recognised so far in the complex (Coluzzi and Sabatini The tarsi are conspicuous by their white apical and
1968; Coluzzi and Bullini 1971; Coluzzi et al. 1976; basal rings on some tarsomeres. Tarsomere V of the
Bullini and Coluzzi 1982). Apart from slight morpho- fore and mid legs are whitish with some scattered dark
logical differences between the species, a varying scales, and tarsomere V of the hind leg is completely
degree of hybrid sterility was demonstrated. The steril- white scaled. The wing veins are covered with dark
ity involves both hybrid sexes between Oc. phoeniciae and pale scales, the pale scales more numerous on the
and the other two members of the complex, while only costa (C), subcosta (Sc) and radius (R). The colouration
F1 hybrid males were found to be sterile in the cross of the abdominal segments is variable (Figs. 6.21b–d).
between Oc. mariae and Oc. zammitii. The larvae of The general appearance is dark, the terga have narrow
10.2 Genus Ochlerotatus Lynch Arribalzaga 241

basal bands of pale scales which are usually widened slightly beyond the middle of the siphon, with 6–7
laterally into triangular spots. The sterna are covered branches, which are as long as the width of the siphon
with whitish and cream coloured scales and dark lateral at the point of its origin. The saddle is weakly devel-
spots in the apical half, and the cerci are slightly oped, extending slightly to the sides of the anal seg-
projected. ment. The saddle seta (1-X) is single. The upper anal
Male: The lobes of tergum IX have 4–6 long setae. seta (2-X) has 12–14 branches, the lower anal seta
The basal lobe of the gonocoxite is moderately convex, (3-X) is single, and more than twice as long as the
densely covered with setae, some of which may be siphon. The ventral brush has 11–13 cratal tufts (4-X)
slightly thicker and longer than the others, but strong and 4–5 precratal tufts. The anal papillae are very short
spine-like setae are absent. The apical lobe of the gono- and spherical.
coxite is indistinct (Fig. 10.59). The claspette has a short Biology: The larvae can be found exclusively in
and straight stem, and the filament is nearly as long as rock pools on the sea shore, often in the surf zone. The
the stem, narrow and slightly curved, and without a usual concentration of salt in such pools is 2–4%, but
transparent wing. The aedeagus is more or less tubular. the larvae are able to tolerate a much higher concentra-
Larva: The antenna is shorter than the head, slightly tion, up to 20% (Rioux 1958). In the Mediterranean
curved, with weakly developed spicules. The antennal region Oc. mariae has several generations per year and
seta (1-A) is situated in the middle of the antennal shaft, its larvae are commonly found from March to October.
with 6–9 branches. The postclypeal seta (4-C) is very Full embryonic diapause is observed when eggs are
thin and short, and branched. The inner and median incubated at relatively low temperatures (< 16°C) and
frontal setae (5-C and 6-C) are single, the median fron- a short photoperiod. A photoperiod also induces a
tals are situated in front of the inner frontals, and the remarkable change in oviposition behaviour of Oc.
outer frontal seta (7-C) usually has 7 branches. The mariae females. Coluzzi et al. (1975) demonstrated
comb is composed of 16–25 scales arranged in 2–3 that the adult females readily oviposit when originating
irregular rows, each individual comb scale with a dis-
tinct median spine and a varying number of smaller
spines of different size at the base (Fig. 10.60). The
siphon is short, slightly tapered, and the siphonal index
is 1.4–2.0. The pecten consists of 15 or more thin teeth
which are longer distally, reaching to the middle of the
siphon. Each pecten tooth ­usually has 4 or more lateral
denticles at the base. The siphonal tuft (1-S) is ­situated

Fig.. 10.59 Hypopygium of Oc. mariae Fig. 10.60 Larva of Oc. mariae
242 10 Subfamily Culicinae

from larvae reared at a long day ­photoperiod, whereas sometimes divided by a narrow acrostichal stripe of
they are very reluctant to oviposit in the same situation pale scales. The posterior submedian areas are brown
when reared at a short day photoperiod. This species scaled, and all other areas of the scutum are covered
can frequently cause nuisance in rocky coastal Medi­ with yellowish scales. A postproxocal scale patch is
terranean areas. present, the sub- and postspiracular patches are pres-
Distribution: Oc. mariae which belongs to the so ent, but a hypostigmal patch is absent. The mesepister-
called “Tyrrhenean” type of the complex inhabits num has a prealar patch and upper and lower
western Mediterranean coasts, ranging from the mesepisternal patches of pale scales, the upper patch
Algarve in southern Portugal to the Italian western not reaching the anterior angle of the mesepisternum.
coast, including the western coast of Sicily. It can also Almost all of the mesepimeron is covered with pale
be found in Tunisia, Algeria and the Balearic Islands scales. The femora and tibiae of the fore and mid legs
(Coluzzi et al. 1975; Ribeiro et al. 1988). have mixed white and dark scales on the anterior sur-
Medical importance: According to Ribeiro et al. face, and white scales predominate on the posterior
(1988) Oc. mariae is not known as a vector of any ­disease, surface. The hind femur is light scaled, and the hind
but Gutsevich et al. (1974) reported that the species trans- tibia has a longitudinal light stripe. The tarsi are pre-
mits the parasite of bird malaria, Plasmodium relictum. dominantly dark scaled with pale basal rings.
Tarsomeres I of all the legs have a diffuse basal ring
and scattered pale scales almost reaching to the apex.
Ochlerotatus (Ochlerotatus) zammitii Tarsomeres II and III of all the legs have a more or less
(Theobald 1903) distinct basal ring, which is broadest on hind tarsomere
[Acartomyia zammitii] III, where it embraces about half of the length of the
tarsomere. Tarsomeres IV and V of the fore legs and
Very similar to Oc. mariae in all stages. It seems to be tarsomere V of the mid legs are usually entirely dark
somewhat more robust in appearance with a more dis- scaled. Tarsomere V of the hind legs sometimes has a
tinct colouration pattern. Whereas the scutum of Oc. few white scales at the base. The tarsal claws are rela-
mariae is without special ornamentation, Oc. zammittii tively large, and bent near the middle at some distance
sometimes has a scutum with two light creamy white from the base of the subbasal tooth. The wing veins are
longitudinal stripes. The hypopygium of the male is entirely dark scaled, sometimes some isolated pale
identical to that of Oc. mariae, but the larvae differ from scales are present at the base of the costa (C). The terga
those of the latter species by the more numerous spic- are predominantly dark scaled, terga I and II with basal
ules on the antenna and the pecten teeth usually having white bands reduced to the median part. The rest of the
fewer than 4 lateral denticles at the base (Seguy 1924; terga have fully developed transverse basal white
Darsie and Samanidou-Voyadjoglou 1997). bands, which are widened laterally into triangular
Distribution: Adriatic coasts, eastern coast of Sicily, patches, and are most distinct on terga VI and VII.
the whole Island of Malta, and Ionean and Aegean coasts Narrow apical bands are sometimes present on the last
(Labuda 1969; Regner 1969; Coluzzi et al. 1974). segments. The cerci are long and distinctly projecting.
Male: The lobes of tergum IX have 6–12 spine-like
setae. The gonocoxite is elongated, with well devel-
Ochlerotatus (Ochlerotatus) mercurator oped basal and apical lobes (Fig. 10.61). The inner sur-
(Dyar 1920) face of the gonocoxite is covered with long inwardly
directed setae, and at least several setae located just
Female: The proboscis and palps are dark scaled, and above the basal lobe do not overlap in the middle. The
sometimes the palps have a few pale scales at the tip. basal lobe is conical, and densely covered with thin
The pedicel has mixed pale and dark scales. The vertex setae and one medially directed very long spine-like
is yellowish scaled, and the occiput has a pair of dark seta which is slightly curved at the apex. The gonosty-
lateral spots (Fig. 6.30a). The antepronotum and lower lus is somewhat broadened in the middle, with a slen-
part of the postpronotum are pale scaled, and the upper der apical spine. The claspette filament is longer than
part of the postpronotum has brown scales. The scutum the stem, with a long stalk, abruptly broadened into a
has a broad median stripe of dark reddish brown scales, unilateral wing beyond its middle. The paraproct is
10.2 Genus Ochlerotatus Lynch Arribalzaga 243

Fig. 10.61 Hypopygium of Oc. mercurator Fig. 10.62 Larva of Oc. mercurator

strongly sclerotized in its apical part, and the aedeagus is single, or rarely with 2 branches. The upper anal seta
is elongated. (2-X) has 8–13 branches. The ventral brush has 2–6
Larva: The head is wider than long. The antenna is precratal setae (4-X). The anal papillae are slightly
about half as long as the head, and is covered with pigmented, tapered, and distinctly longer than the
spicules. The antennal seta (1-A) is inserted slightly saddle.
below the middle of the antenal shaft, with 8–13 (usu- Biology: The species may have two generations per
ally 9–10) branches. The inner frontal seta (5-C) has year. The larvae can be found from May onwards in
3–6 branches, usually four or more are present on one semipermanent water bodies, such as ditches and small
side, and the median frontal seta (6-C) has 1–4 ground pools, or less frequently in permanent waters in
branches. The prothoracic formula 1-P to 7-P is as fol- open marshes or in old river arms. Adults were encoun-
lows: 1 (long, single, rarely 2 branches); 2 (short, sin- tered from the end of June until the beginning of
gle); 3 (short, 2–3 branches) (Fig. 8.47a); 4 (short, September. Gutsevich and Dubitsky (1987) stated that
single); 5 (long, 2–3 branches); 6 (long, single); 7 nowhere is the species very numerous.
(long, 3 branches). The comb is composed of 23–36 Distribution: Northern Holarctic region, in Europe
(usually about 30) comb scales arranged in several found in the northern part of European Russia as well
irregular rows (Fig. 10.62). Each scale has indistinct as in the mountains of Crimea and Caucasus.
median and lateral spines which become smaller
towards the base. The siphon tapers towards the apex,
and the siphonal index is 3.3–3.5. The pecten consists Ochlerotatus (Ochlerotatus) nigrinus
of 20–29 (usually 24) closely spaced teeth occupying (Eckstein 1918)
from about 1/3 to slightly less than half of the siphon
length. Each pecten tooth has 2–6 lateral denticles. Female: Closely related to Oc. sticticus and very simi-
The siphonal tuft (1-S) is distinctly longer than the lar to it in all stages. The proboscis and palps are dark
width of the siphon at the point of its origin, with 4–7 scaled. The occiput has dark erect forked scales at the
(usually 5) branches. The saddle covers more than half sides. Flagellomere I of the antennae is entirely dark
of the lateral sides of the abdominal segment. The sad- scaled and slightly swollen, and flagellomeres I–III are
dle seta (1-X) is distinctly shorter than the saddle, and distinctly shorter than the others. The pattern of the
244 10 Subfamily Culicinae

scutum is similar to that of Oc. sticticus, and the hypos- frontal setae which are usually single, very rarely
tigmal and postprocoxal scale patches are absent. The 2-branched (Fig. 8.49c). The antenna is slightly less
upper mesepisternal scale patch extends to the anterior than half as long as the head, and the antennal seta
angle of the mesepisternum, and the pale scales on the (1-A) is situated at about the middle of the antennal
mesepimeron end distinctly above its lower margin. shaft, with 3–5 branches not reaching the tip. The
The wing veins are covered with dark scales, with scat- number of comb scales is usually 10–12, rarely > 20
tered pale scales at the base of the costa (C), the entire (Fig. 10.64). Each scale is more elongated and the
length of the subcosta (Sc) and the media (M), proxi- median spine slightly longer than in Oc. sticticus. The
mal to the cross veins. The abdominal terga are dark siphon is short and straight, and the siphonal index is
scaled, with broad basal pale bands of more or less about 2.5. The pecten teeth are more or less evenly
uniform width (Fig. 6.50b). On some terga the bands spaced, reaching beyond the middle of the siphon. The
may be slightly, if at all, constricted. siphonal tuft (1-S) is situated slightly beyond the dis-
Male (Fig. 10.63): The differences between the talmost pecten tooth, with 4–7 branches. The saddle
hypopygia of Oc. nigrinus and Oc. sticticus are subtle extends far down the sides of the anal segment, and the
but usually obvious when directly compared to each saddle seta (1-X) is single and shorter than the saddle.
other. In Oc. nigrinus the basal lobe of the gonocoxite is The ventral brush usually has 4, rarely 3 precratal setae
not as much constricted at the base as it is in Oc. sticti- (4-X). The anal papillae are longer than the saddle, and
cus and its upper part is broad and rounded, not slender of varying length.
and crescent shaped (Fig. 7.48b). The apical lobe arises Biology: Oc. nigrinus prefers to breed in open ter-
abruptly from the gonocoxite, is widest at its base and rain, preferably flooded meadows in river depressions,
rounded in its middle part, and not apically rounded as mostly associated with Ae. vexans, however, it is not so
in Oc. sticticus. In all other characteristics the male widely distributed and by far not so numerous as Ae.
­genitalia of the two species are nearly identical. vexans (Eckstein 1918, 1920; Peus 1933).
Larva: Similar to that of Oc. sticticus, but can be Distribution: Southern Scandinavia, Finland,
distinguished by the inner (5-C) and median (6-C) Denmark, Germany, France, Poland, Estonia, northern
Urals to western Siberia.

Fig. 10.63 Hypopygium of Oc. nigrinus Fig. 10.64 Larva of Oc. nigrinus
10.2 Genus Ochlerotatus Lynch Arribalzaga 245

Ochlerotatus (Ochlerotatus) nigripes

(Zetterstedt 1838)

Female: A medium to large species, easy to identify

by its dense blackish body setation, especially on the
scutum, its blackish brown integument, and the entirely
white scaling of the pleurites. The proboscis is entirely
dark scaled, and the palps are dark with some scattered
white scales. The head is covered with dark brownish
scales, and the occiput with some golden brown erect
scales, mixed with grey and dark scales. The antenna is
dark greyish, and the pedicel has mixed pale and dark
scales. The scutum and scutellum have prominent and
dense black or very dark brown setae. The scutum is
covered with narrow dark brown scales, occasionally
with spots of light scales laterally and on the prescutel-
lar dorsocentral area. All the light scale patches on the
pleurites are white. The postpronotum has narrow dark
brown scales, and a lower patch either with narrow or
broad white scales, and setae scattered on the entire
postpronotum. A postprocoxal patch is usually present,
but a hypostigmal patch is absent. The subspiracular Fig. 10.65 Hypopygium of Oc. nigripes
and postspiracular areas have white scale patches.
The number of postspiracular setae is 14 or more long as the stem, with a unilateral wing. The aedeagus
(Fig. 6.42d). The mesepisternum has dense upper and is oval shaped with a rather wide opening.
lower patches of narrow white scales. The mesepim- Larva: The antenna is short and less than half as
eron has a broad upper whitish scale patch. The wing long as the head. The antennal seta (1-A) is situated
veins are covered with dark scales, and pale scales are beyond the middle of the antennal shaft, and has 1–3
usually present at the base of the costa (C) and radius short branches. The inner and median frontal setae
(R), sometimes also at the bases of other veins. All the (5-C and 6-C) are usually single, sometimes with 2
coxae have white scale patches and long dark setae. branches. The prothoracic setae are heavily acidu-
The femora, tibiae and tarsomeres I of all legs are dark lated, the formula 1-P to 7-P is as follows: 1 (1–2
scaled with scattered paler brownish scales. Tarsomeres branches, very short); 2 (single, medium long); 3
II–V are dark scaled, with a few pale scales sometimes (3-branched); 4 (1–3 branches, medium long); 5 and
present on tarsomeres IV and V. The abdominal terga 6 (2–3 branches); 7 (multiple-branched). The number
have white basal bands. The sterna are entirely covered of comb scales is 8–19 and each individual scale has
with white scales, and the cerci are covered with dark a long median spine and insignificant small lateral
scales and are very setous. spines. The siphonal index is 2.6–3.1 (Fig. 10.66).
Male: The lateral lobes of tergum IX have numer- The pecten has 1–3 distal teeth apically detached,
ous, heavily sclerotized setae, a characteristic which is with at least one tooth located beyond the siphonal
shared with Oc. impiger. The gonocoxite has long tuft (1-S). Each pecten tooth is elongated with only
setae predominating on its inner side (Fig. 10.65). The one long lateral denticle. The siphonal tuft (1-S) is as
basal lobe of the gonocoxite is well developed, with long as or longer than the width of the siphon at the
numerous setae of different length, but of more or less point of its insertion, with 2–6 branches. The saddle
the same thickness. The apical lobe is small and indis- completely encircles the anal segment, but sometimes
tinct. The gonostylus is broad, and the apical spine of a narrow gap may be present at the ventral surface.
the gonostylus is slender. The paraproct has inwardly The saddle seta (1-X) is short, and less than half as
curved tips. The claspette stem tapers towards the long as the saddle. The anal papillae are at least 1.5
apex, and the claspette filament is more than half as times longer than the saddle.
246 10 Subfamily Culicinae

mals (Wood et al. 1979), facultatively autogeny is

reported by Corbet (1964). The females are not as
aggressive biters as Oc. impiger females.
Distribution: Oc. nigripes is one of the highest arc-
tic, circumpolar species. It mainly occurs north of the
tree line in the entire northern hemisphere. Together
with Oc. impiger its distribution range extends further
to the north than any other mosquito species.

Ochlerotatus (Ochlerotatus) pionips (Dyar 1919)

Female: Similar to Oc. communis but can be disti-

guished from the latter by the presence of the postpro-
coxal scale patch. A medium sized species, usually a
little larger than Oc. communis. The proboscis and
palps are entirely dark scaled. The head has narrow
yellowish brown scales dorsally and broad appressed
yellowish scales laterally and numerous pale erect
forked scales. The scutum is covered with golden
bronze or yellowish grey scales, with a dark brown
median stripe, occasionally divided by a narrow acros-
tichal stripe of yellowish scales, and a posterior sub-
median stripe of dark brown scales (Fig. 6.49a). The
Fig. 10.66 Larva of Oc. nigripes scutellum has narrow curved yellowish scales and light
brown to brown setae on the lobes. The postpronotum
has narrow brown scales dorsally, becoming pale ven-
Biology: It is a monocyclic species. In the Canadian trally. The postprocoxal membrane has a patch of pale
tundra (beyond 80°N) females were observed to ovi- scales. A hypostigmal patch is absent, but the subspi-
posit only in direct sunlight during the warmest part of racular and postspiracular scale patches are well devel-
the day. Eggs were laid several cm above the water oped. The upper and lower mesepisternal scale patches
level at the edges of ponds. Such an oviposition behav- are fused with the prealar patch, reaching the anterior
iour is connected with the search for south facing sites angle of the mesepisternum. The mesepimeron has a
where the snow melts earliest in the next season pale scale patch reaching the lower margin, and 1–4
(Corbet and Danks 1975). In Europe, the larvae have lower mesepimeral setae are usually present. The fem-
been found in high mountains in Dalarna, Sweden, but ora are dark brown scaled with scattered pale scales,
mostly occur in the northernmost tundra in willow and and the posterior surface is pale scaled. The tibiae and
birch shrub marshes in the arctic zone in temporary tarsi have dark scales, but pale basal rings on the tar-
water bodies formed by snow-melt. They are encoun- someres are absent. The wing veins are covered with
tered in deep and less oligotrophic pools, as well as in narrow dark scales, and occassionally a few pale scales
shallow puddles surrounded by Carex sp. at higher may be present at the base of the costa (C) and radius
treeless elevations in the Scandinavian mountains. The (R). The abdominal terga are dark scaled, each with a
larvae are easily disturbed and may spend a long time pale basal band of more or less uniform width or
at the bottom of their breeding sites. The larval devel- slightly widening at the sides. The sterna are covered
opment lasts several weeks, adults emerge a little later with whitish scales, and more or less distinct narrow
than those of Oc. impiger. Copulation takes places dark apical bands are present.
during swarming (Corbet 1965). Females were Male: The hypopygium is very similar to that of
observed attempting to feed on various birds and mam- Oc. communis and sometimes they are difficult to
10.2 Genus Ochlerotatus Lynch Arribalzaga 247

Fig. 10.67 Hypopygium of Oc. pionips

Fig. 10.68 Larva of Oc. pionips

distinguish (Fig. 10.67). The upper part of the basal lobe margin is fringed with short spines, decreasing in size
bears a row of long, prominent setae, which are straight towards the base (Fig. 8.42b). The siphon is straight,
or only slightly curved, but never strongly curved or tapers towards the apex, and the siphonal index is
hooked as in Oc. communis (Fig. 7.44a,b). No other dis- 2.5–3.0. The pecten has 18–24 evenly spaced teeth,
tinct differences exist in the hypopygia of the two spe- confined to the basal half of the siphon. The siphonal
cies. In case the identification by the hypopygium alone tuft (1-S) is located beyond the distalmost pecten
is uncertain and the whole specimen is available, the tooth at about the middle of the siphon, with 4–9
length of the palps and the postprocoxal scale patch branches, which are slightly longer than the width of
should be taken into consideration. In males of Oc. the siphon at the point of its insertion. The saddle
pionips the palps are slightly shorter than the proboscis extends far down the sides of the anal segment, and
and the postprocoxal scale patch is present. In males of the saddle seta (1-X) is single and a little shorter than
Oc. communis the palps are longer than the proboscis the saddle. The upper anal seta (2-X) has 9–13
and the postprocoxal scale patch is absent. branches, the lower anal seta (3-X) is single, and is
Larva: The head is wider than long. The antenna much longer than the siphon. The ventral brush has
is about 2/3 as long as the head, slender and slightly 17–21 tufts of cratal setae (4-X) and 2–3 precratal
curved with spicules. The antennal seta (1-A) is situ- setae. The anal papillae are lanceolate, pointed, and
ated slightly below the middle of the antennal shaft, longer than the saddle.
with 7–13 (usually 9) branches which do not reach Biology: Oc. pionips, like Oc. communis, is a typical
the tip. The postclypeal seta (4-C) is small, with 3–5 monocyclic snow-melt mosquito, whose larvae hatch
short branches. The inner (5-C) and median (6-C) during the snow-melt in early spring. Its breeding sites
frontal setae have 3–5 (rarely 6) branches (Fig. 8.42a), are snow-melt ponds in boggy forests up to an altitude of
and in Oc. communis both pairs are single, rarely with > 1,000 m, where larvae often are associated with those
2 branches. The outer frontal seta (7-C) has 5–9 of Oc. communis, Oc. hexodontus, and Oc. punctor.
branches. The comb consists of more than 60 scales Gjullin et al. (1961) observed that Oc. pionips develops
arranged in an irregular patch (Fig. 10.68). Each indi- slower than the associated Aedes/Ochlerotatus species.
vidual scale is without a ­prolonged median spine, The adults seem to appear later and are often less numer-
thus appears to be rounded apically, and the lateral ous than the other snow-melt mosquitoes.
248 10 Subfamily Culicinae

Distribution: Holarctic species, occurs in North arranged in one row (Fig. 10.70). Each scale is large
America and northern Eurasia. with a well developed median spine, and small spines
on the basal half of the scale. The siphon is dark, almost
black, slightly tapering in the apical half, and the
Ochlerotatus (Ochlerotatus) pulcritarsis siphonal index is 4.0–5.0. The pecten consists of 18–22
(Rondani 1872) evenly spaced teeth. Each individual tooth is blunt
ended with 3–6 heavily sclerotized lateral denticles.
Female: Very similar to the females of Oc. berlandi. A The siphonal tuft (1-S) has 3–4 branches, is about as
slight difference exists in the scutal colouration pattern. long as the width of the siphon at the point of origin,
Whereas the scutum of Oc. berlandi has clearly con- and is situated below the middle of the siphon. The
trasting by dark and pale golden scales, Oc. pulcritar- saddle covers about half of the anal segment. The sad-
sis exhibits a weaker pattern of pale and dark scales on dle seta (1-X) is longer than the saddle and is single.
the scutum, and looks rather uniformly golden brown- The upper anal seta (2-X) has 4–5 branches of variable
ish in colour. However, the median and lateral stripes length. The lower anal seta (3-X) is longer than the
may be somewhat lighter than the submedian spots. siphon, and single. The anal papillae are very long,
Male (Fig. 10.69): The hypopygium is very similar sausage shaped, and several times longer than the
to that of Oc. berlandi. The spine-like seta on the basal saddle.
lobe of the gonocoxite is usually less curved at the Biology: Hibernation takes place in the egg stage,
apex, and rarely hooked. and the species has usually two generations per year,
Larva: The head is square shaped, and somewhat but sometimes only one generation occurs. The larvae
broader than long. The antenna is almost as long as the can be found in tree-holes, stumps and among roots of
head, and the antennal shaft is smooth. The antennal deciduous trees, such as Quercus sp., Platanus sp., and
seta (1-A) has 3–4 branches, inserted at about the mid- Ulmus sp., the latter being preferred, as well as in olive
dle of the antennal shaft (Fig. 8.58c). The postclypeal tree-holes (Shannon and Hadjinicolaou 1937). The
seta (4-C) is small and multiple-branched. The frontal water temperature of the breeding sites never exceeds
setae (5-C to 7-C) are well developed and multiple- 21°C even in southern European climatic conditions.
branched. The comb consist of 6–10 (usually 8) scales Similar observations were made along the Black Sea
shore in Bulgaria (Bozkov et al. 1969). Larval develop­
ment may last up to two months. Adult females are

Fig. 10.69 Hypopygium of Oc. pulcritarsis Fig. 10.70 Larva of Oc. pulcritarsis
10.2 Genus Ochlerotatus Lynch Arribalzaga 249

anthropophilic; they bite outdoors during daytime cially on the ventral surface. The remaining tarsomeres
(Rioux 1958). Adult mosquitoes of both sexes were are entirely dark scaled. The wing veins are covered
found in stables and houses in a village where no trees with narrow dark scales, and with patches of pale scales
were present. This may indicate that the species is fac- at the base of the costa (C), radius (R) and anal vein
ultatively zoophilic and could breed in artificial con- (A). Abdominal tergum I has a broad patch of white
tainers or have a considerable migrating capacity scales, terga II–VII are blackish brown scaled with a
(Shannon and Hadjinicolaou 1937). basal transverse band of white scales which are some-
Distribution: Oc. pulcritarsis is principally a spe- times slightly widened laterally, and the abdominal
cies of the Mediterranean region. Its northern distribu- sterna are mostly white scaled. The cerci are
tion range reaches as far as the Czech Republic. It is ­exceptionally long and conspicuous.
also found in central and southeastern Asia. Male: The lobes of tergum IX have 5–7 short stout
Note on systematics: One subspecies, ssp. asiaticus setae. The gonocoxite is long and slender, about three
Edwards is reported in Uzbekistan, Turkmenia, and times as long as it is wide, with its inner surface densely
Pakistan. covered with long setae (Fig. 10.71). The basal lobe of
the gonocoxite is prominent and has 3 setae which are
distinctly larger than the rest, one long stout apically
Ochlerotatus (Ochlerotatus) pullatus curved spine-like seta inserted dorsally and two sinu-
(Coquillett 1904) ous, flattened and slightly lanceolate setae arising from
the ventral surface of the basal lobe (Fig. 7.31b). The
Female: A medium sized species. The proboscis is apical lobe is well developed, thumb-like, with numer-
dark scaled, and the palps are predominantly dark ous setae at the tip. The gonostylus is about half as
scaled with a few scattered pale scales at the joints of long as the gonocoxite, curved, slightly expanded
the palpomeres. The clypeus is blackish brown, and the before the middle, bearing a few small setae close to
pedicel is dark brown with a few pale scales. The vertex the apex, and the apical spine of the gonostylus is long
and occiput are covered with pale yellowish narrow and slender. The paraproct is heavily sclerotized api-
scales and erect forked scales of the same colour on the cally. The claspette stem is long, swollen, and strongly
dorsal part and usually broad appressed yellowish white bent in the middle, without a thorn shaped process, the
scales laterally. The integument of the scutum is black, basal half is stout, and the distal half is slender. The
and the scutum is covered with yellowish brown narrow
curved scales, disconnected by several bare longitudi-
nal stripes and areas to which they contrast, mainly due
to the exposure of the dark integument. The transverse
suture, prescutellar area, and lateral ends of the scutum
are also devoid of scales. The setae of the scutum are
usually golden brown, sometimes blackish brown, and
are more numerous on the posterior part. The scutellum
has narrow pale scales and yellowish brown setae on
the lobes. The pleurites have patches of broad yellow-
ish white scales, a hypostigmal patch of scales is pres-
ent, and the postprocoxal membrane is bare. The
mesepisternal patch of scales is divided into an upper
and lower portion, and the upper patch does not reach
the anterior margin of the mesepisternum (Fig. 6.43a).
The mesepimeral patch of scales reaches near the lower
margin of the mesepimeron, and 1–5 lower mesepim-
eral setae are present (Fig. 6.44a). The femora have
dark brown and pale scales intermixed, but are darker
apically with a pale knee spot. The tibiae and tarsomere
I are dark brown, and speckled with pale scales, espe- Fig. 10.71 Hypopygium of Oc. pullatus
250 10 Subfamily Culicinae

claspette filament is shorter than the stem, prominently than half way down the side, and the saddle seta (1-X)
winged on the convex side, and the aedeagus longer is single and shorter than the saddle. The upper anal
than wide. seta (2-X) has 6–10 branches, and the lower anal seta
Larva: The head is slightly wider than long. The (3-X) is long and single. The ventral brush has about
antenna is about half as long as the head, slightly 12–15 tufts of cratal setae (4-X) and 1–3 precratal
curved, and covered with spicules. The antennal seta tufts. The anal papillae are about twice as long as the
(1-A) is inserted at the basal third of the antennal shaft, saddle, and pointed.
with about 5 branches, which do not reach to the tip of Biology: Oc. pullatus produces one generation per
the antenna. The postclypeal seta (4-C) is small, with year. The larvae hatch from overwintering eggs from
4–5 branches, the frontal setae are multiple-branched, early spring until late summer, depending on the eleva-
the inner (5-C) and median (6-C) setae have at least 3 tion of their occurrence. They can be found in the tun-
branches (mostly 4–6), and the outer frontal seta (7-C) dra mostly in small clear snow-melt pools and in
has 8–13 branches (Fig. 8.42c). The prothoracic setae mountainous regions in a variety of breeding sites, e.g.
2-P and 3-P are nearly as long and strong as 1-P in puddles and pools, without vegetation, created by
(Fig. 8.47b). The comb consists of 40–60 scales overflow of mountain streams or after heavy rainfall,
arranged in a large triangular patch, the lateral scales small clear lakes with a rocky bottom or boggy holes
are more or less pointed, with a longer median spine, (Kaiser et al. 2001). The larvae may be associated with
and fringed with smaller lateral spines. The pecten has those of other mountainous Aedes/Ochlerotatus spe-
15–25 teeth, which are evenly spaced and situated cies, e.g. Oc. communis and Oc. punctor. Their devel-
close together (Fig. 10.72). The siphon uniformly opment lasts longer than that of their associates and
tapers towards the tip from near the middle, and the consequently the adults occur later, mainly in the sum-
siphonal index is 3.0–3.5. The siphonal tuft (1-S) is mer months. The females readily attack their hosts
situated more or less at the middle of the siphon, during any time of the day in forested areas. Male
beyond the distalmost pecten tooth, with 5–8 branches. swarming takes place after sunset in openings of the
The anal segment has a saddle which extends more forest. The species is usually found in small numbers,
but adults can be abundant in some localities, gener-
ally far remote from human habitations (Carpenter and
La Casse 1955).
Distribution: Oc. pullatus is a northern Holarctic
species with a disjunct distribution range. In central
and southern Europe it is restricted to mountainous
regions, including the Pyrenees, Alps, Dinari Mountains,
Tatras, Carpathians, Balkans, Rhodopi Mountains and
can be found up to very high elevations (2,000 m and
higher). In the northern parts of its distribution range it
occurs in the arctic tundra, lowlands and plains in
Eurasia as well as in North America.

Ochlerotatus (Ochlerotatus) punctodes

(Dyar 1922)

Female: The adult females cannot be distinguished

from those of Oc. punctor. Differences occur mainly
in the larval stage (Knight 1951).
Male (Fig. 10.73): Separable from Oc. punctor by
the shape of the basal lobe of the gonocoxite and the
claspette filament. The basal lobe has an irregular tri-
Fig. 10.72 Larva of Oc. pullatus angular shape, and the basal part of the lobe abruptly
10.2 Genus Ochlerotatus Lynch Arribalzaga 251

Fig. 10.73 Hypopygium of Oc. punctodes

arises from the gonocoxite, whereas in Oc. punctor the

basal part of the lobe arises more gradually from the Fig. 10.74 Larva of Oc. punctodes
gonocoxite. The claspette filament is relatively long
and narrow, and of almost the same length as the stem
and weakly sclerotized, but in Oc. punctor the filament found newly hatched larvae of Oc. punctodes in
is shorter than the stem and strongly sclerotized Alaska at the end of April and a few larvae were still
(Fig. 7.42b). Carpenter and La Casse (1955) stated that present in August.
the spine of the basal lobe is more weakly developed in Distribution: Oc. punctodes is a subarctic species.
Oc. punctodes and sometimes is difficult to separate It is reported from Alaska and in Europe from Norway,
from the long setae at the base of the lobe. In Oc. punc- Sweden, Finland, and European Russia.
tor the spine of the basal lobe is strongly developed
and distinctly different from the long setae at the base
of the lobe. Ochlerotatus (Ochlerotatus) punctor (Kirby 1837)
Larva: The inner (5-C) and median (6-C) frontal
setae are usually single (Fig. 8.32b), whereas in Oc. Female: A medium sized species. The proboscis and
punctor both pairs are usually 2-branched. The saddle palps are dark scaled. The occiput has golden yellow-
does not completely encircle the anal segment, and ish narrow scales and yellow erect forked scales dor-
extends to near the midventral line (Fig. 10.74). The sally, with broad appressed creamy white scales
anal papillae are usually much shorter than in larvae of laterally. The scutum is covered with yellowish brown
Oc. punctor, varying from much shorter to slightly scales, usually with a median stripe of dark brown
longer than the saddle. scales and occassionally divided by an acrostichal
Biology: Oc. punctodes belongs to the typical salt stripe of yellowish scales, and the posterior submedian
marsh fauna in subarctic regions (Frohne 1953). The areas with dark brown scales. The scutellum has
larvae occur predominantly in the more saline waters, ­yellowish brown scales and light brown setae on the
whereas the larvae of the closely related Oc. punctor lobes. The prosternum has no scales on the anterior
prefer fresh water habitats. In these habitats the lar- surface, or occasionally has scattered pale scales, but
vae of Oc. punctodes can be found together with is not as extensively covered with scales as in Oc.
those of Oc. punctor, Oc. communis, Oc. impiger, hexodontus. The postpronotum has narrow yellowish
Oc. excrucians, and Oc. flavescens. Frohne (1953) brown scales anteriorly and broader paler scales at the
252 10 Subfamily Culicinae

posterior margin. The postprocoxal membrane has the apical part is densely covered with short setae.
pale scales (absent in Oc. communis). A hypostigmal The apical lobe is broadly rounded with short curved
patch is absent, the subspiracular patch is divided into setae extending downwards to near the middle of the
an upper and lower portion, and the postspiracular gonocoxite. The gonostylus is slightly expanded in
patch is well developed. The upper and lower mese- the middle with several small setae before the apex,
pisternal scale patches are fused, and extend to the and the apical spine of the gonostylus is slender. The
anterior angle of the mesepisternum, narrowly sepa- paraproct is strongly sclerotized, with the apex
rated from the prealar patch (Fig. 6.47a). The scales inwardly pointed. The claspette stem is short and
on the mesepimeron extend to its lower margin, and slightly curved near the middle. The claspette fila-
1–5 lower mesepimeral setae are present. The femora, ment is shorter than the stem, lanceolate, wide in the
tibiae and tarsomeres are mostly dark scaled. The middle, strongly sclerotized and not transparent, with
claws of the fore legs are elongated, and gradually a curved apex. The aedeagus is cylindrical, and
curving distal to the subbasal tooth. The wing veins notched at the apex.
are usually entirely dark scaled, with a few pale scales Larva: Very similar to that of Oc. hexodontus. For
present occasionally (less than in Oc. hexodontus, Oc. separation of the two species see the description of the
communis, and Oc. pionips) at the base of the costa latter. The antennae are less than half as long as the
(C). The abdominal terga are dark scaled with basal head, and covered with numerous spicules. The anten-
bands of white scales, which are distinctly confined in nal seta (1-A) is situated in the middle of the antennal
the middle or even interrupted on the more anterior shaft or slightly below it, with 4–7 branches not reach-
terga (Fig. 6.48a). The sterna are covered with greyish ing the tip. The postclypeal seta (4-C) has 2–4 short
white scales, and the apices of some of the dark sterna branches. The inner (5-C) and median (6-C) frontal
are scaled medially. setae have 1–3 branches, usually 2-branched, and the
Male: The lobes of tergum IX are sclerotized, each outer frontal seta (7-C) has 2–8 branches (Fig. 8.32a).
bearing several spine-like setae. The gonocoxite is The comb has 10–25 small scales, usually arranged in
about three times as long as it is wide, the basal lobe 2–3 irregular rows or a triangular patch, and each scale
of the gonocoxite is well developed, and more or less has a prominent median spine and several smaller
triangular shaped (Fig. 10.75). The basal part has a spines in the basal part. The siphon tapers in the apical
row of long setae, a long apically recurved spine, and half, and the siphonal index is about 3.0 (Fig. 10.76).
The pecten has 14–26 evenly spaced teeth confined to
the basal half of the siphon. The siphonal tuft (1-S) is
located beyond the distalmost pecten tooth, with 3–9
branches, and is about as long as the width of the
siphon at the point of origin. The saddle completely
encircles the anal segment, and the saddle seta (1-X) is
usually as long as or a little longer than the saddle. The
upper anal seta (2-X) has 5–9 branches, and the lower
anal seta (3-X) is single and long. The ventral brush
has 16–19 tufts of cratal setae (4-X) and 1–2 precratal
setae. The anal papillae taper and are of variable length
but are always distinctly longer than the saddle.
Biology: Oc. punctor is a snow-melt mosquito,
which has a preference for swampy forests with
boggy waters. The larvae hatch during the snow-melt,
when the water temperature is only a little above 0°C.
While Monchadskii (1951) and Horsfall (1955) found
larvae only in springtime, they occur in southern
Germany also in the summer after strong rainfall;
Fig. 10.75 Hypopygium of Oc. punctor sometimes together with the larvae of Ae. cinereus
10.2 Genus Ochlerotatus Lynch Arribalzaga 253

Eurasia. In Europe it is distributed from Scandinavia to

the Mediterranean region.

 chlerotatus (Ochlerotatus) riparius

O
(Dyar and Knab 1907)

Female: The species has a brownish integument. The

proboscis is predominantly white scaled and the palps
are dark scaled with scattered white scales or a nar-
row white band. The vertex and occiput are covered
with bronze golden narrow scales and a small lateral,
white patch. The scutum has narrow, bronze and
golden gleaming scales, and a broad median stripe of
darker scales is usually present. Small pale anterior
submedian patches close to the transverse suture may
be present, and the prescutellar bare space is usually
surrounded by pale scales (Fig. 6.33a). The scutellum
has bronze scales and a diffuse pale patch on the
median lobe. The postpronotum is covered with nar-
row bronze scales in the upper half and with narrow
Fig. 10.76 Larva of Oc. punctor sickle shaped pale scales in the lower half. Small
white scale patches on the antepronotum and propleu-
ron are present, and the postprocoxal membrane has a
and Cs. alaskaensis (Peus 1929; Vogel 1933, 1940; small white patch. A small hypostigmal patch of
Becker and Ludwig 1981). Some larvae may over- scales is sometimes present. The postspiracular area
winter together with those of Oc. rusticus and Cs. and paratergite have pale scale patches. The mesepis-
morsitans. Larvae of this acidophilic species can be ternum has three distinct patches along the posterior
found in great numbers in boggy waters with margin, and the mesepimeral patch of pale scales
Sphagnum sp. growth, where the pH-value can be covers a little more than half of the mesepimeron.
less than 4.0. The optimum temperature for the devel- The coxae have white scale patches, the fore femur
opment of Oc. punctor is 25°C, however the lowest and all the tibiae have mixed scales dorsally, with
mortality rate is found at temperatures of 15°C. At white scales ventrally; and the femora of the mid and
25°C larval and pupal development lasts 10–17 days, hind legs are a little darker. Tarsomeres I of all the
at 20°C 15–22 days, at 15°C 20–26 days and at 10°C legs are predominantly white scaled with a diffuse
33–41 days. At 30°C the larvae die in the first and basal ring (sometimes absent), tarsomeres II–IV have
second larval stages. In early spring the larvae of Oc. a basal white band of a different width, tarsomeres V
punctor occur together with those of Oc. communis, are entirely dark scaled, and the tarsal claws are
and a little earlier than the larvae of Oc. diantaeus evenly curved (Fig. 6.32b). The wing veins are cov-
and Ae. cinereus. In central Europe, the adults occur ered with dark greyish scales, which on the costa (C)
in the second half of April, mostly later than those of and subcosta (Sc) are mixed with white scales. The
Oc. communis, but earlier than Oc. cantans. The abdominal terga have distinct white or pale basal
adults prefer sheltered terrain and seldom migrate out bands, which are sometimes diffused or interrupted
of the forest. Their peak biting activity is during dusk, in the middle forming indistinct triangular patches
on sultry days and in strongly shaded situations they laterally. All terga have scattered white scales api-
can be troublesome even during daytime. cally which usually form apical bands at least on seg-
Distribution: Oc. punctor is a Holarctic species ments VI–VIII (Fig. 6.34a). The sterna are covered
and can commonly be found in North America and with broad white scales.
254 10 Subfamily Culicinae

Fig. 10.77 Hypopygium of Oc. riparius

Fig. 10.78 Larva of Oc. riparius

Male: The lateral lobes of tergum IX have 4–7
setae. The shape of the hypopygium is similar to that
of Oc. cantans. The basal lobe of the gonocoxite is lateral denticles. The siphonal tuft (1-S) is situated
slightly longer than broad at its base, and not that elon- beyond the middle of the siphon and beyond the dis-
gated as in the latter species, with one long apically talmost pecten tooth, with 4–5 long branches. Seta
curved spine-like seta (Fig. 10.77). The apical lobe is 9-S is rather long and curved, but is not transformed
well developed, and covered with short, thin setae. The into a strong hook. The saddle does not encircle the
gonostylus is somewhat broadened in its middle part, anal segment, but covers most of its lateral sides.
with a slender apical spine. The claspette stem is slen- The saddle seta (1-X) is single and shorter than the
der, and the claspette filament is moderately broad, and saddle. The ventral brush has 4–6 precratal tufts
unilaterally winged. The aedeagus is elongated and (4-X). The anal papillae are about as long as the
pear shaped. saddle.
Larva: The antenna is shorter than the head and Biology: The species is uncommon or rare over
covered with numerous spicules. The antennal tuft most of its range (Wood et al. 1979), thus its biology is
(1-A) is situated at about the middle of the antenna, not well known. It hibernates in the egg stage and is
with moderately long branches not reaching the tip. probably monocyclic, although females can be found
The inner and median frontal setae (5-C and 6-C) throughout the season. The larvae and adults occur at
usually have 2 branches (Fig. 8.49a), 5-C is some- the same time as Oc. excrucians and Ae. cinereus.
times 3-branched. The prothoracic formula (1-P to Breeding habitats are pools at mixed forest edges, or
7-P) is as follows: 1 (long, single); 2 and 3 (short, pools in deciduous forests, usually rich in leaf debris
single); 4 (medium, single); 5 and 6 (long, single); 7 on the bottom. Larvae can also be found in peat bogs
(long, 2–3 branches). The number of comb scales is in the open (Gutsevich et al. 1974).
6–12, arranged in one row (Fig. 10.78). Each indi- Distribution: It is a Nearctic and northern
vidual scale is elongated with a long median spine. Palaearctic species, which has mostly been reported
The siphonal index ranges between 3.5 and 4.0. The in northern and central Europe. It is usually rare,
2–3 last pecten teeth are apically slightly detached. sometimes locally abundant, but is rather widespread
Each pecten tooth has one larger and 2–3 smaller in temperate areas.
10.2 Genus Ochlerotatus Lynch Arribalzaga 255

 chlerotatus (Ochlerotatus) sticticus

O
(Meigen 1838)

Female: A medium sized species, with the proboscis

and palps dark scaled. The pedicel has pale scales on
its median part, and flagellomere I is yellowish at the
base. Flagellomeres I–III are of the same length as the
others. The vertex is predominantly covered with pale
yellowish scales, and the occiput with pale erect forked
scales. The scutum has a dark, median longitudinal
stripe sometimes separated by a narrow acrostichal
stripe of pale scales. The lateral parts of the scutum are
pale yellowish scaled, and the posterior submedian
stripe is reddish to dark brown. The upper part of the
postpronotum has dark scales, and the lower third is
mostly pale scaled. The postprocoxal membrane is
without scales, and a hypostigmal patch is absent. The
subspiracular and postspiracular scale patches are well
developed. The mesepisternum has greyish white
scales, and the upper mesepisternal patch extends to
near the anterior angle, narrowly separated from the
prealar patch. The mesepimeral patch of scales ends Fig. 10.79 Hypopygium of Oc. sticticus
distinctly above the lower margin of the mesepimeron,
and the lower mesepimeral setae are absent. The tibiae
and tarsi are dark scaled dorsally and mostly pale about half as long as the stem, with a small bilateral
scaled ventrally, and tarsomeres V of all the legs are wing. The wing abruptly expands close to the base of
mostly dark scaled. The tarsal claws are moderately the filament, and more or less gradually tapers towards
and evenly curved, each with a small subbasal tooth. the apex. The aedeagus is pear shaped.
The wing veins are usually entirely dark scaled, occas- Larva: The antenna is nearly half as long as the
sionally some isolated pale scales may be present at head, covered with less numerous, but prominent,
the base of the costa (C). The abdominal terga are dark coarse spicules. The antennal seta (1-A) is inserted
scaled, terga II–IV with pale basal bands distinctly slightly below the middle of the antennal shaft, with
constricted in the middle, and on the following terga 4–5 branches not reaching the tip. The postclypeal seta
the basal bands are interrupted forming triangular pale (4-C) is small, and situated between the median frontal
patches at the lateral sides (Fig. 6.50a). setae (6-C), with 1–4 short branches. The inner frontal
Male (Fig. 10.79): The basal lobe of the gonocoxite seta (5-C) has 2–4 branches, the median frontal seta
is constricted at its base, the apical part is slender and (6-C) is usually 2-branched, and the outer frontal seta
not attached to the gonocoxite, and is more or less (7-C) usually has 5 branches. The number of comb
crescent shaped (Fig. 7.48a). The lobe is densely cov- scales is 18–27 arranged in 2–3 irregular rows
ered with short setae and a rather large and prominent (Fig. 10.80). Each individual scale has a median spine
spine, which is curved apically and located at the con- 1.5 times the length of the subapical spines. The siphon
stricted base. The apical lobe is well developed, gradu- is straight, gradually tapering towards the apex, and
ally arising from the gonocoxite, apically rounded, and the siphonal index is 2.5–3.0. The pecten teeth are
covered with short setae. The gonostylus is slightly more or less evenly spaced extending beyond the mid-
expanded in the middle, with several small setae close dle of the siphon, and the siphonal tuft (1-S) is inserted
to the apex. The apical spine of the gonostylus is long beyond the pecten, with 4–6 branches not exceeding
and slender. The paraproct is strongly sclerotized, the width of the siphon at the point of insertion. The
inwardly curved and pointed at its apex. The claspette saddle extends far down the sides of the anal segment,
stem is short and straight, and the filament is short, and the saddle seta (1-X) is single and shorter than the
256 10 Subfamily Culicinae

where the females frequently become a nuisance.

The peak of biting activity of females is at twilight;
however, they can also bite during the day in shaded
situations. The females may lay up to 150 eggs in
shady, damp depressions which will become flooded
by rising water levels.
Distribution: The Holarctic species is widespread
in Europe and occurs from northern Europe to the
Mediterranean area and to Siberia in the East. It has
also been reported from North America.

 ubgenus Rusticoidus
10.2.3 S
Shevchenko and Prudkina

The adults are large sized mosquitoes with numerous

erect forked scales on the occiput and lateral parts of
the vertex. The scutum is covered with narrow scales
Fig. 10.80 Larva of Oc. sticticus including most of the prescutellar area, and the scutel-
lum with curved narrow scales and numerous long
saddle. The ventral brush has 1–2 precratal setae (4-X). setae on all lobes. The postpronotum has only broad flat
The anal papillae are long and pointed, and often scales. Both the anteprocoxal and postprocoxal mem-
2.0–2.5 times longer than the saddle. brane have a patch of broad pale scales. The pleurites
Biology: Oc. sticticus is a polycylic species. The are extensively covered with pale scales and numerous
larvae occur mainly in temporary water bodies after setae. The abdominal terga have dark scales but with
floods and are regularly associated with those of Ae. extensive pale scaled areas. In the male genitalia ter-
vexans; it is often the second most frequent mosquito gum IX has narrow lobes on each side with several
after Ae. vexans. The larvae can certainly hatch at short setae. The basal lobe of the gonocoxite bears several
lower water temperatures (<8°C) than the larvae of long lanceolate setae, and the claspette filament is short
Ae. vexans. In central Europe they are associated with and more or less onion or triangular shaped. The fourth-
the hatching of the larvae of Ae. rossicus, Ae. cinereus instar larvae of European Rusticoidus species are easily
and Oc. cantans, after floods during spring time, when distinguished from all other Aedes and Ochlerotatus
Ae. vexans is not ready to hatch in masses. However, species by having several pairs of setae inserted dor-
the peak development occurs during floods in sum- sally at the siphon and a variable branched small seta
mer. In contrast to Ae. vexans, Oc. sticticus has an located laterally, usually close to the distal pecten teeth
unequivocal preference for shaded breeding waters in in addition to the siphonal tuft (1-S).
the flood plains, which are often covered by trees; the The members of the subgenus were previously placed
pH-value of the waters usually ranges from neutral to in the former subgenus Ochlerotatus of Aedes as a sepa-
alkaline. The optimum temperature for the develop- rated globus (Feltianus) or group (rusticus-group)
ment of Oc. sticticus is about 25°C. The development (Martini 1931; Edwards 1932) and this classification
from hatching of first-instar larvae to the emergence was followed by others (Natvig 1948; Mohrig 1969). In
of the adults lasts 6–8 days at 25°C, 10–14 days at 1973, Shevchenko and Prudkina established the new
20°C, 18–19 days at 15°C and 37 days at 10°C. The subgenus Rusticoidus as a monotypic subgenus, based
females can migrate considerable distances when on the structures of the male genitalia and the larval
searching for a blood meal, distances of more than siphon of Oc. refiki, but confusion has existed since then
20 km have been observed (Hearle 1926). Adults of as to which species should be included in the subgenus.
Oc. sticticus stay predominantly in covered terrains, According to Reinert (1999a) the ­following European
e.g. in flood plains of river systems covered with trees species are now included in the subgenus Rusticoidus:
10.2 Genus Ochlerotatus Lynch Arribalzaga 257

Oc. krymmontanus, Oc. lepidonotus, Oc. quasirusticus,

Oc. rusticus, Oc. refiki, and Oc. subdiversus. Additionally,
two North American species, Oc. bicristatus and Oc.
provocans, were transferred from the former subgenus
Ochlerotatus to Rusticoidus (Reinert 2000b).
Oc. krymmontanus was described from the south-
ern slopes of the Crimean Mountains (Alekseev
1989). Owing to the lack of material for examination
and the uncertain specific status, the species is not
included here.

 chlerotatus (Rusticoidus) lepidonotus

O
(Edwards 1920)

Female: Can be distinguished from other Rusticoidus

species by the presence of whitish scales on the post-
notum. The proboscis and palps are black scaled, the
palps with scattered pale scales. The vertex and occiput
have narrow yellowish scales and dark erect forked Fig. 10.81 Hypopygium of Oc. lepidonotus
scales, and the lateral parts of the head have whitish
scales. The pedicel is black with dense white scales,
and the clypeus is blackish brown. The integument of apex. The claspette stem is relatively short and thick,
the scutum is blackish brown, and the scutum is cov- and more or less straight. The claspette filament is short,
ered with narrow yellowish scales. The scutellum has and of an irregular triangular shape. The aedeagus has a
pale yellowish scales and setae on the lobes. The post- broadly rounded apex and small lateral denticles.
notum is dark brown, with a group of narrow whitish Larva: The head is wider than long. The antenna is
scales. The pleurites are extensively covered with pale less than half as long as the head, and is entirely cov-
scales, and the postpronotom with light yellowish or ered with spicules. The antennal seta (1-A) is located
brown scales. The femora and tibiae have light yellow- slightly below the middle of the antennal shaft, with
ish scales, except for black scales at the apices. The 5–6 branches. The postclypeal seta (4-C) is short with
tarsi are dark brown scaled with scattered white scales 2–3 thin branches. The inner frontal seta (5-C) has 3–4
on the entire part of tarsomere I and the basal part of branches, the median frontal seta (6-C) has 1–3
tarsomere II. The wing veins are covered with inter- branches and the outer frontal seta (7-C) has 8–10
mixed yellowish white and dark scales, with dark branches. The number of comb scales is 6–11, arranged
scales predominantly located on the costa (C), radius 1 in an irregular row (Fig. 10.82). Each scale is large
(R1), and anal vein (A). The abdominal terga are with a prominent median spine, and sometimes 1 or 2
entirely covered with greyish white scales, with a more lateral spines of almost the same size as the median
or less prominent median part with black scales on spine. The siphon tapers from the basal third, the siph-
terga II–V. The sterna are entirely whitish scaled. onal index is 2.7–4.1, and the dorsal surface of the
Male (Fig. 10.81): The base of the gonocoxite has siphon has 2 pairs of setae. A single additional seta
one lobe arising gradually from the gonocoxite, more or which is longer than the width of the siphon at the
less conical in shape, with a group of lanceolate, flat- point of its insertion, is located on the lateral side of
tened setae, but additional smaller lobes are absent. The the siphon close to the distalmost pecten tooth. The
apical lobe is less developed than in other members of pecten has 9–21 teeth (average 13–15), sometimes 1–2
Rusticoidus, and is hardly visible. The gonostylus is distalmost teeth are apically detached, and the pecten
strongly curved apically, with several small setae near does not extend beyond the basal half of the siphon.
the apex, and the apical spine of the gonostylus is long The siphonal tuft (1-S) is inserted slightly below the
and straight. The paraproct is inwardly curved at the middle of the siphon, beyond the distalmost pecten
258 10 Subfamily Culicinae

Fig. 10.83 Hypopygium of Oc. quasirusticus

The scutal pattern is less distinct than in Oc. rusticus,

Fig. 10.82 Larva of Oc. lepidonotus
the scutum is covered with narrow yellowish brown
scales, disconnected by several bare longitudinal
tooth, with 8–13 branches. The saddle extends far stripes at the acrostichal, anterior dorsocentral, and
down the sides of the anal ­segment, and the saddle seta posterior submedian areas to which they contrast,
(1-X) has 3–5 branches, and is longer than the saddle. mainly due to the exposure of the dark integument.
The upper anal seta (2-X) has 7–9 branches, the lower The subcosta (Sc) is without pale scales, but there are
anal seta (3-X) is single and much longer than the no other distinct differences.
siphon. The ventral brush has 14–16 tufts of cratal Male: The lobes of tergum IX are situated close
setae (4-X) and 2 precratal setae. The anal papillae are together, with 5–8 short spine-like setae. The gonocox-
lanceolate, usually shorter than the saddle, and the dor- ite is more or less straight, not as rounded as in Oc.
sal pair is longer than the ventral pair. rusticus (Fig. 10.83). The basal lobe of the gonocoxite
Biology: Oc. lepidonotus is a rare species and so far is well elongated, the distal margin has 6–8 strongly
recorded from southeastern Europe only; thus little curved lanceolate setae, and the apical portion of the
information is available about its biology. It is apparen­ basal lobe has 2–3 long and strong setae (Fig. 7.28b).
tly a monocyclic species, which hibernates in the egg The gonostylus is distinctly bent in the apical third,
stage (Medschid 1928). Larvae occur by early spring and the apical spine of the gonostylus is long, slender,
after heavy rainfall or snow-melt. They may be associ- and nearly straight, but never S-shaped as in Oc.
ated with larvae of Oc. detritus when the breeding sites rusticus.
are slightly saline (Gutsevich et al. 1974). Adults are Larva: The antennae have large and strong spic-
predominantly found at the end of April and during ules, more developed than in Oc. rusticus. Prothoracic
May. Martini (1931) reported numerous females biting seta 3-P has 3 branches. 1–2 distalmost pecten teeth
horses at dawn in Asia Minor. are apically detached, and situated beyond the middle
Distribution: Greece and Turkey. of the siphon (Fig. 10.84). The siphonal seta (1-S) is
attached within the pecten. Dorsal additional pairs of
setae are longer than the width of the siphon at its
Ochlerotatus (Rusticoidus) quasirusticus base, as opposed to being shorter than the width of
(Torres Canamares 1951) the siphon at its base in Oc. rusticus. The lateral addi-
tional seta is usually single, about as long as the width
Female: Very similar to Oc. rusticus in all stages, and of the siphon at the point of origin, and longer than in
the females particularly, closely resemble each other. Oc. rusticus. Seta 9-S is strongly developed, large and
10.2 Genus Ochlerotatus Lynch Arribalzaga 259

fied yet. The species is believed to occur also in North

Africa (Encinas Grandes 1982).

Ochlerotatus (Rusticoidus) refiki (Medschid 1928)

Female: Oc. refiki closely resembles Oc. rusticus, but

differs from the latter in the colouration of the terga.
The proboscis and palps are predominantly dark
scaled, with scattered pale scales of varying number,
mainly at the base of the proboscis. The vertex and
occiput have yellowish white narrow scales and erect
forked scales of the same colour. The pedicel is dark
with a row of white scales at the base, and the clypeus
is dark brown. The integument of the scutum is black-
ish brown, and covered with yellowish scales and a
median stripe of dark scales, sometimes divided by a
narrow yellowish acrostichal stripe. The scutellum
has whitish narrow scales on the lobes. The postpro-
coxal membrane has pale scales, and the postprono-
tum has broad flattened scales, dark brown or black in
the upper part and white in the lower part. The hypos-
Fig. 10.84 Larva of Oc. quasirusticus tigmal and spiracular scale patches are fused. White
scales on the mesepisternum extend more or less to
the anterior angle and to the lower margin, and the
hooked. The anal papillae are ­distinctly longer than mesepimeral patch extends to the lower margin of the
the saddle, with the dorsal pair nearly twice as long as mesepimeron. The femora are predominantly pale
the saddle. scaled, the tibiae and tarsomeres I mostly have dark
Biology: Very similar to that of Oc. rusticus. Some scales, and tarsomeres II–V are entirely dark scaled.
larvae hatch in late autumn and hibernate in the larval The wing veins are covered with dark scales, with
stage, others hatch in early spring of the following year scattered pale scales at the base of the costa (C), sub-
(Encinas Grandes 1982). They are predominantly found costa (Sc), and radius (R). The colour of the abdomen
in permanent water bodies in forests or in ditches and varies greatly. The terga are often covered with dark
flooded meadows. Often they are associated with lar- scales and indistinct pale basal bands not wide in the
vae of Oc. refiki, Oc. excrucians, Cx. hortensis, Cs. middle and scattered pale scales at the distal part of
fumipennis, and An. atroparvus (Torres Canamares the terga, sometimes with a narrow band of pale
1951). Adults can be found from May to June and they scales at the apical margin. Sometimes pale scales
are often encountered close to their breeding sites, indi- predominate on all terga, with only a few scattered
cating that their migration ability is limited. The females dark scales (Fig. 6.40b). In contrast to Oc. rusticus
are mainly zoophilic but also feed on humans, predom- the pale scales on the terga never show a tendency to
inantly in shaded situations. form a longitudinal stripe in the middle.
Distribution: Oc. quasirusticus is so far reported Male: The lobe of tergum IX has 5–10 short spine-
only from Spain, where it belongs to one of the most like setae. The basal lobe is situated close to the middle
abundant Ochlerotatus species in certain regions of the gonocoxite, the ventral division with an elon-
(Encinas Grandes 1982). Owing to the great similarity gated basal part is covered with 15–16 slightly curved
to Oc. rusticus it was probably overseen or misidenti- lanceolate setae arranged in several rows (Fig. 10.85).
fied in the mosquito collections of other countries in The dorsal division of the basal lobe is small, and situ-
the past, thus its whole distribution range is not clari- ated apically to the ventral part with 2 long and strong
setae directed towards the apex. The gonostylus is bent
260 10 Subfamily Culicinae

Fig. 10.86 Larva of Oc. refiki

Fig. 10.85 Hypopygium of Oc. refiki

12–21 teeth occupying the basal third of the siphon,
apically and the apical spine of the gonostylus is slen- each tooth has a prominent main spine and 3–4 lateral
der and more or less straight. The paraproct is strongly denticles. Sometimes 1–2 distalmost pecten teeth are
sclerotized, inwardly curved at the apex, and pointed. apically detached. The siphonal tuft (1-S) has 6–9
The claspette stem is long, curved at the basal part, and branches, and is located at about the middle of the
swollen at the apex. The claspette filament is elongated siphon or slightly below it, but always beyond the dis-
and pointed at the apex, and transversely striated. The talmost pecten tooth. The saddle extends down to near
aedeagus is moderately rounded at the apex with small the lower margin of the anal segment, and the saddle
lateral denticles. seta (1-X) has 1–3 branches, and is longer than the
Larva: The head is wider than long. The antenna is saddle. The upper anal seta (2-X) has 7–9 branches,
less than half as long as the head, is slightly curved, and the lower anal seta (3-X) is single and longer than
and covered with spicules. The antennal seta (1-A) is the siphon. The ventral brush has 13–15 tufts of cratal
located at about the middle of the antennal shaft, with setae (4-X) and 2–3 precratal setae. The anal papillae
5–6 short branches. The postclypeal seta (4-C) is thin, are lanceolate and about as long as the saddle.
with thin branches. The median frontal seta (6-C) is Biology: The biology of Oc. refiki is similar to that
usually single, occasionally with 2–3 branches, and is of Oc. rusticus. It is a rare species. The early larval
situated before the inner frontal seta (5-C), which has stages of this monocyclic snow-melt mosquito can be
2–5 (usually 3) branches. The outer frontal seta (7-C) found after heavy rainfall in late autumn. They can
usually has 6–9 branches. The number of comb scales survive even when the breeding sites are covered with
is 6–11 arranged in a row, and each individual scale ice during wintertime. However, the majority of the
has a strong median spine and several shorter spines at population overwinters in the egg stage and hatching
the base (Fig. 10.86). The siphon is straight, gradually takes place during the snow-melt early in the year.
tapers towards the apex, and the siphonal index is 3.0– Typical breeding sites are semipermanent water bodies
4.0. The dorsal surface of the siphon has 3 pairs of in swampy woodlands, e.g. with Alnus glutinosa,
additional setae, and another seta with 2–5 short occasionally larvae can be found in flooded meadows
branches is located on the lateral side of the siphon (Vogel 1933). Larvae of Oc. refiki are often associated
close to the distalmost pecten tooth. The pecten has with those of Oc. rusticus, Oc. cantans, and Oc. cata-
10.2 Genus Ochlerotatus Lynch Arribalzaga 261

phylla. The waters of the breeding sites have usually a (Sc), and are most numerous at the apex of the sub-
neutral to alkaline pH-value. In central Europe the lar- costa. Abdominal tergum I has 2 patches of yellowish
vae pupate in April and the first adults occur at the end white scales and pale setae, the other terga are dark
of April or early May. They prefer shaded areas where scaled with pale basal bands which are usually wid-
they may bite humans and mammals even during day- ened middorsally and show a tendency to form a lon-
time; however, the biting activity is usually highest at gitudinal stripe in the middle, at least on the apical
dusk. The adults do not migrate much and prefer to terga (Fig. 6.40a). Dark parts of the terga often have
stay close to their breeding sites in shaded areas. scattered pale scales. The sterna are predominantly
Distribution: In Scandinavia, Oc. refiki has been whitish scaled.
reported from Sweden (Dahl 1975). It is widely dis- Male: The apical margin of tergum VIII is densely
tributed in the other parts of Europe, e.g. France, covered with long, inwardly curved setae. The lobe
Spain, Italy, Switzerland, Germany, Czech Republic, of tergum IX has 5–7 short spine-like setae. The
former Yugoslavia, Slovakia, Hungary, and Romania. gonocoxite has dense long setation on the entire
Outside Europe the species can be found in Asia inner surface (Fig. 10.87). The basal lobe of the
Minor. gonocoxite has a constricted stem-like base and a
group of lanceolate, flattened setae arranged more or
less in a row. The apical lobe is well developed, pro-
Ochlerotatus (Rusticoidus) rusticus (Rossi 1790) truding beyond the level of the insertion point of the
gonostylus, with numerous short setae. The gonosty-
Female: A large mosquito, with a dark scaled pro- lus is slightly curved at the apex with several small
boscis and palps, and a few scattered pale scales at subapical setae, and the apical spine of the gonosty-
the base of the proboscis. The vertex and occiput have lus is twisted and distinctly S-shaped. The paraproct
narrow yellowish white scales, and the eyes are bor- is strongly sclerotized, and inwardly curved at the
dered with narrow white scales. The pedicel is dark apex. The claspette stem is long, distinctly curved in
brown with a circle of whitish scales, and the clypeus the middle, and slightly swollen at the apex. The
is blackish brown. The integument of the scutum is claspette filament is short, more or less onion-like,
blackish brown, covered with golden bronze scales without a plate shaped widening, and is transversely
and a median stripe of dark scales, usually divided by striated. The aedeagus is moderately rounded at the
a narrow acrostichal stripe, but sometimes there are apex with small lateral denticles.
two more dark stripes in the posterior submedian Larva: The head is wider than long. The antennae
areas. The lateral parts of the scutum have cream are approximately half as long as the head, slightly
coloured scales. The scutellum is dark brown with curved, and adorned with numerous spicules
narrow yellowish white scales and pale setae on the
lobes. The postprocoxal membrane has pale scales.
The pleurites are extensively covered with yellowish
or white scales. The postpronotum has broad flattened
scales, blackish brown in the upper part and whitish
in the lower part. The hypostigmal and spiracular
scale patches are fused. The mesepisternum has
scales extending to the anterior angle and lower mar-
gin, the scales of the mesepimeron extend more or
less to the lower margin, and lower mesepimeral setae
are present. The femora have pale yellowish scales on
the ventral surface and dark scales on the dorsal sur-
face, the tibiae and tarsomeres I have pale and dark
scales intermixed, and tarsomeres II–V are almost
entirely dark scaled. The wing veins are predomi-
nantly covered with dark scales, with scattered pale
scales at the base of the costa (C) and on the subcosta Fig. 10.87 Hypopygium of Oc. rusticus
262 10 Subfamily Culicinae

(Fig. 8.24a). The antennal seta (1-A) is located at The upper anal seta (2-X) has more than 6 branches,
about the middle of the antennal shaft or slightly and is half as long as the lower anal seta (3-X) which
below it, with 5–6 branches. The median frontal seta is single and longer than the siphon. The ventral brush
(6-C) has 2, occasionally 3, branches situated before has 11–16 tufts of cratal setae (4-X) and 3–4 precratal
the inner frontal seta (5-C), which has 3, sometimes setae. The anal papillae are about half as long as the
2, branches, and the outer frontal seta (7-C) usually saddle, and the dorsal pair is longer than the ventral
has 8 branches. The number of comb scales is 10–18, pair.
arranged in two irregular rows, each individual scale Biology: Oc. rusticus is a monocyclic snow-melt
with a strong median spine, 1–2 shorter lateral spines mosquito which predominantly occurs in swampy
and small spines at the base. The siphon is straight, woodlands with a high level of ground water; occas-
tapering in the apical half, and the siphonal index is sionally it can be found in floodplains. Larvae are able
approximately 3.0–3.5 (Fig. 10.88). The dorsal sur- to hatch during heavy rainfall in autumn when the water
face of the siphon has 3, occassionally 4, pairs of level rises. The diapause of these larvae is terminated by
additional setae; another seta with 1–2 thin branches the decreasing temperatures in autumn. Usually the lar-
is located on the lateral side of the siphon beyond the vae which hatch in autumn hibernate in the second and
median pecten teeth. The pecten has 15–25 teeth not third larval instar; they can even survive under a closed
extending to the apical third of the siphon, the basal coverage of ice. The high content of dissolved oxygen
and median teeth have 2–3 lateral denticles, 1–3 dis- in cold water or bubbles of oxygen under the ice which
tal pecten teeth are detached and spine-like. The siph- are produced by assimilating plants enable the larvae to
onal tuft (1-S) is located at about the middle of the cover their demand of oxygen and to survive; they are
siphon within the distal pecten teeth, with 6–8 usually attached to these oxygen bubbles. However,
branches. The saddle extends about 3/4 of the way during a severe winter the mortality rate can be very
down the sides of the anal segment, and the saddle high. For this reason Oc. rusticus usually does not occur
seta (1-X) is single, and nearly as long as the saddle. in areas where the isotherm of January is less than −1°C
(Kirchberg and Petri 1955). Often the larvae of Oc. rus-
ticus are associated with those of Cs. morsitans or with
overwintering larvae of An. claviger. A second larval
population of Oc. rusticus and Cs. morsitans hatches
from hibernating eggs in early spring shortly after the
snow-melt. Thus, first and fourth-instars of these two
species can be found together with numerous first-instar
larvae of Oc. communis and Oc. punctor which usually
hatch in early spring from hibernating eggs. Typical
breeding sites are ditches or deeper depressions with
vegetation, e.g. Carex sp. or Phragmites sp. The larvae
of Oc. rusticus are seldom found in shallow water bod-
ies because of the high risk that the entire water body
may freeze. Larvae are found preferably in breeding
sites with a pH-value of 5.0–8.0; they are rare or absent
in water bodies with pH values less than 5.0. The opti-
mum temperature for the larval development in the
laboratory is 15–20°C. The time of development is
about 66 days at a constant temperature of 10°C, 28–29
days at 15°C and 23–25 days at 20°C. Although the
larvae of Oc. rusticus belong to the first occurring spe-
cies of snow-melt mosquitoes, they pupate and emerge
after the species which hatch in early spring from hiber-
nating eggs such as Oc. communis and Oc. punctor. In
Fig. 10.88 Larva of Oc. rusticus central Europe adults usually emerge at the end of
10.2 Genus Ochlerotatus Lynch Arribalzaga 263

April. Females are vicious biters in shaded situations. paraproct is well sclerotized, and inwardly curved at
The adults prefer to stay in forested areas and do not the apex. The claspette stem is long and slightly curved
migrate long distances, usually not more than 2 km in the basal part. The claspette filament is short, and
(Schäfer et al. 1997). more or less triangular shaped with a pointed apex.
Distribution: Ae rusticus is widely distributed The aedeagus is not as broadly rounded at the apex as
throughout Europe and can also be found in North in Oc. lepidonotus, and has small lateral denticles.
Africa and Asia Minor. Larva: The head is wider than long. The antenna is
about half as long as the head, and densely covered with
spicules. The antennal seta (1-A) is located at about the
 chlerotatus (Rusticoidus) subdiversus
O middle of the antennal shaft, with 3 branches. The post-
(Martini 1926) clypeal seta (4-C) is short, with 2 branches. The inner
frontal seta (5-C) has 2 branches, the median frontal seta
Female: The proboscis and palps are dark scaled, (6-C) has 2–3 branches and the outer frontal seta (7-C)
often with some scattered pale scales. The vertex has has 5 branches. The number of comb scales is usually
whitish narrow scales, and the occiput has pale and 14–15 arranged in two irregular rows, and each scale is
dark scales. The integument of the scutum is blackish large with a prominent median spine and small spines at
brown, the scutum has a median stripe of yellowish the base. The siphon is straight, tapering in the apical
bronze scales, lighter in the median and darker in the third, and the siphonal index is 3.0–3.3 (Fig. 10.90). The
lateral part, but sometimes the stripe is indistinct. The dorsal surface of the siphon has 3–4 pairs of additional
scutellum has narrow whitish scales and pale setae on long setae, and another thin seta with 2 branches is
the lobes. The postnotum is blackish brown without a located on the lateral side of the siphon close to the
group of scales. The pleurites have dense patches of median pecten teeth. The pecten has the 3–4 distalmost
silvery to yellowish scales, and the upper part of the teeth atypical, spine-like, widely spaced, almost reach-
postpronotum has straight or slightly curved bronze ing the apex of the siphon. The siphonal tuft (1-S) is
scales. Postprocoxal and hypostigmal patches are single, and nearly twice as long as the width of the
present. The femora and tibiae have light and dark siphon at the point of its origin. It is attached at about the
scales intermixed, and the tarsi are dark scaled with middle of the siphon within the pecten. The saddle
numerous pale scales on tarsomeres I and the basal extends down 3/4 of the sides of the anal segment, and
part of tarsomeres II. The wing veins are predomi- the saddle seta (1-X) is single and as long as the saddle.
nantly covered with narrow dark scales, and pale The upper anal seta (2-X) usually has 11 branches, and
scales are present mainly at the base and the anterior the lower anal seta (3-X) is single and about as long as
part of the wing. The abdominal terga have greyish the siphon. The ventral brush has 13–15 tufts of cratal
white scales and a varying number of dark scales,
forming indistinct spots, and pale transverse bands
are absent. There is great variation in the colouration
of the species. Gutsevich et al. (1974) described a
light form with numerous pale scales on the abdomi-
nal terga, proboscis, and palps of females. Transitional
forms have also been found.
Male: The apical margin of tergum VIII is densely
covered with long, thin setae. The lobes of tergum IX
are situated close together, with 7–10 short, thick setae.
The base of the gonocoxite has two or more lobes, but
only one lobe bears a group of lanceolate, flattened
setae, the other smaller lobes have long hair-like setae
(Fig. 10.89). The apical lobe is weakly developed with
short, slightly curved setae. The gonostylus is curved,
with several small setae near the apex, and the apical
spine of the gonostylus is more or less straight. The Fig. 10.89 Hypopygium of Oc. subdiversus
264 10 Subfamily Culicinae

ered with numerous setae. The proboscis is usually

dark, sometimes with scattered pale scales, and the
length of the female palps is about 1/3 that of the pro-
boscis, and most often shorter. The eyes meet in the
middorsal line or are slightly separated, the vertex has
numerous erect scales, and the occiput has narrow and
broad scales. The scutum is covered with narrow
scales and a full pattern of setae, but acrostichal setae
are sometimes absent. The scaling on the pleurites is
reduced and variable. The dorsal margin of the
mesomeron is not in line with the hind coxa. Tarsomere
I of the hind legs is as long as or longer than the hind
tibia (except in subgenus Barraudius), pulvilli are
present in most species. The wing has narrow scales
on all veins and a long radial fork. All abdominal seg-
ments are nearly equally broad, usually banded or
with lateral triangular patches of pale scales. The
males are smaller than the females, but scaling and
setation are quite similar. The antenna has numerous
flagellate whorls, and the palps are long with five pal-
pomeres exceeding the length of the proboscis. The
morphology of the Culex hypopygium is very compli-
cated and belongs to one of the most complex struc-
tures in the family of Culicidae. Usually the gonocoxite
Fig. 10.90 Larva of Oc. subdiversus
is devoid of scales (except in subgenus Baraudius)
and bears only one lobe, which is displaced mesally;
setae (4-X) and 6–7 precratal setae. The anal papillae hence, the name subapical lobe. It may be divided and
are lanceolate, shorter than the saddle, and the dorsal ornamented with several setae of different length and
pair is l­onger than the ventral pair. shape. Typical claspettes are absent, and the aedeagal
Biology: Oc. subdiversus is a monocyclic species. apparatus is of a complicated structure with several
Larvae occur in early spring after heavy rainfalls or snow- characteristics of unknown homology. These surround
melt. Adults may be very numerous in some localities the phallosome, which is dorsally covered by the
and massive attacks of biting females on humans and live membranous proctiger and the sclerotized and fused
stock have been observed (Gutsevich et al. 1974). or unfused parts of the paraproct, which distally bear
Distribution: European part of Russia to Kazakhstan a more or less crown-like area of spines or denticles.
and southern Siberia. The head of the larva is broader than long. The antenna
is spiculate in most species and longer than the head
in many species. The antennal tuft (1-A) usually has
multiple branches situated in the distal half of the
10.3 Genus Culex Linnaeus antennal shaft. The mouthparts are adapted to filter
feeding with well developed anteromedian and lateral
Members of this genus are usually small to medium palatal brushes with an exception in the predacious
sized species with sparse pleural scaling. The scutel- larvae of the tropical subgenus Lutzia, which have the
lum is distinctly trilobed, prespiracular setae are labrum and the brushes modified for capturing prey.
absent, all claws are without a subbasal tooth. The The frontal seta 5-C is located distally to 6-C, and all
abdomen is blunt ended with short, oval cerci. The setae are usually multiple-branched. Setae 1-P to 3-P
last three characteristics separate Culex species from are located on a common sclerotized tubercle.
nearly all Aedes and Ochlerotatus species. The antenna Abdominal seta 4-I is plumose, but never palmate, and
is as long as or shorter than the proboscis, and is cov- setae 6-I to 6-VII have a variable number of long
10.3 Genus Culex Linnaeus 265

branches. The number of comb scales is usually antenna is as long as the head or slightly longer and
between 40 and 60, and each individual scale is more spiculate towards the tip, and the antennal seta
­relatively small. The siphonal index is variable, and (1-A) is multiple-branched. The comb scales are
the siphon is usually slender and moderately to numerous, small and elongated. The pecten occupies
extremely long. At least 4–6 siphonal setae (1-S) are about half of the siphon length; each tooth has sev-
inserted along the ventral surface of the siphon, either eral lateral denticles. The siphonal tufts (1-S) are
paired or arranged in a straight or zig-zag row. The arranged in a zig-zag row on the ventral side of the
pecten teeth in some species are widely spaced dis- siphon, and the main tracheal trunks are broad. The
tally. The saddle usually completely encircles the anal saddle entirely surrounds the anal segment, precratal
segment, and the saddle seta (1-X) is often branched. setae (4-X) are absent, and the anal papillae are
The precratal tufts (4-X) are usually reduced in num- short.
ber or absent, and the anal papillae are variable in The small subgenus Barraudius embraces only four
shape and size. species so far, Cx. richeti Brunhes and Venhard is only
The genus Culex with more than 750 described spe- known in Nigeria and Cx. inatomii Kamimura and
cies from 24 subgenera world wide comprises only a Wada reported from Japan. The two other members of
few non tropical species. In Europe, species of the sub- Barraudius, Cx. modestus and Cx. pusillus, are partly
genera Barraudius, Culex, Maillotia and Neoculex can distributed in the European region.
be found and most of them have a Mediterranean and/
or central European distribution.
Several tropical Culex species from Asia and Africa
are well known for transmission of lymphatic filariasis Culex (Barraudius) modestus Ficalbi 1889
and various viral diseases.
Female: The proboscis is dark brown, paler on its ven-
tral surface from the base to the middle, and slightly
swollen at the apex. The palps, clypeus and flagellum
10.3.1 Subgenus Barraudius Edwards of the antenna are dark brown. The vertex has dark
brown setae which are directed anteriorly between the
Members of the subgenus are small brownish spe- eyes. The head is covered with brown or yellowish nar-
cies. The proboscis of the female is shorter than the row scales, with some broader pale scales on each side,
fore femur, the margin of the eyes is usually orna- and the occiput has dark brown erect and forked scales.
mented with narrow scales, and the vertex has erect The integument of the scutum is brown, and covered
and broad light scales. The scutum has uniform with chestnut-brown scales, rather lighter on the scutel-
brownish scales, and the scutellum is usually light lum and in front of it. Fine, blackish setae are scattered
scaled. The hind tarsomere I is distinctly shorter than mainly along the margin of the scutum, along the dors-
the hind tibia. The abdominal terga are dark scaled ocentral stripes and above the wing roots. The setae are
without transverse pale bands, but basolateral pale more conspicuous and longer on the scutellum. The
patches of scales may be present, and the sterna have pleurites are pale brown, with small patches of pale
light scales. The palps of the male are longer than the scales on the mesepisternum and upper mesepimeron,
proboscis, without long setae, but are covered with a 3–6 postpronotal setae, and one lower mesepimeral
few short spines. The gonocoxite is covered with seta is present. The legs are mainly dark brown, the
small scales on the outer surface. The subapical lobe fore and mid femora have pale scales on the posterior
of the gonocoxite arises slightly beyond the middle, surface, and the hind femur is pale except for the dor-
not as far apically situated as in the majority of other sal surface which is brown scaled, and the pale knee
Culex species, with a number of spine-like or hair- spot is distinct. The tibiae are dark brown dorsally,
like setae; any transparent, broad scale-like setae are with pale scales on the ventral surface. All tarsomeres
absent. The gonostylus is slender, the paraproct api- are dark scaled, and the hind tarsomere I is shorter than
cally has a group of small spines forming a paraproct the hind tibia (Fig. 6.51a). The wings are entirely dark
crown, and the aedeagus has dorsal and ventral arms. scaled, and the cross veins are well separated. The
The head of the larva is broader than long, the terga are dark brown scaled, transverse pale bands are
266 10 Subfamily Culicinae

absent, but lateral pale patches usually form a continu- gus is short, only slightly curved or nearly straight at
ous pale border on either side of the abdomen. The the apex and not extending beyond the paraproct
sterna are uniformly covered with pale yellowish crown. The dorsal arm of the aedeagus is conspicu-
scales. The abdomen is blunt ended, which separates ously bent upwards.
the species from the similarly coloured females of Larva: The antenna is moderately spiculate, slightly
Ae. cinereus. longer than the head, curved, darkly pigmented at the
Male: The palps are almost devoid of setae, and are base and distinctly narrowing from the insertion point
longer than the proboscis. The long palps separate the of the antennal seta (1-A) to the apex. Seta 1-A is
males from the similarly coloured males of Ae. cinereus inserted beyond the middle of the antennal shaft, and is
which have palps which are considerably shorter than half as long as the antenna, with 15–25 branches. The
the proboscis. The gonocoxite is approximately twice inner frontal seta (5-C) has 3–5 branches, the median
as long as it is wide with more or less dense scales on frontal seta (6-C) has 3–4 branches and the outer fron-
its outer surface (Fig. 10.91). The lobe of the gono- tal seta (7-C) has 7–8 branches. The comb consists of
coxite is situated slightly beyond the middle of the a patch of 50 or more fringed scales which are more or
gonocoxite and is divided into two distinct tubercles. less rounded apically. The siphon is straight, the main
The proximal one bears 2–3 spines of different size, 1 tracheal trunks are broad, and the siphonal index is
or 2 of them may be curved apically, and the more about 4.0–5.0 (Fig. 10.92). The pecten has about 12
distal tubercle carries 2 strong setae. Broad transpar- relatively widely spaced teeth situated in the basal half
ent scale-like setae are absent. The gonostylus is long of the siphon, and most of the teeth have 4–5 lateral
and slender (longer than in the similar Cx. pusillus), denticles. Setae 1-S has 10–12 tufts arranged in a more
usually more than half as long as the gonocoxite, or less ventral zig-zag row. The basalmost tuft arises
evenly tapering apically and curved in the apical half. proximal to the distalmost pecten tooth, and the distal-
The apex of the paraproct has one row of spines form- most tuft is located close to the apex of the siphon.
ing a paraproct crown. The ventral arm of the aedea- Each tuft is slightly shorter, or occasionally slightly

Fig. 10.91 Hypopygium of Cx. modestus Fig. 10.92 Larva of Cx. modestus
10.3 Genus Culex Linnaeus 267

longer than the width of the siphon at the point of its modestus. The proboscis, palps and clypeus are dark
insertion. The saddle is as long as it is wide or slightly brown, the proboscis is apically swollen and shorter
longer and completely encircles the anal segment. The than the fore femur. The pedicel is dark brown with a
saddle seta (1-X) is small with 2–3 branches. The tuft of brown scales, and the flagellum is dark brown.
upper anal seta (2-X) has 3–4 branches, one branch The occiput is brown with golden narrow scales and
longer than the others, and the lower anal seta (3-X) is dark forked scales, and the sides are scattered with
long and single. The ventral brush has 10–13 cratal whitish scales. All decumbent scales of the vertex are
setae (4-X). The anal papillae are shorter than the sad- narrow and golden, with a few dark setae, directing
dle, slender, and tapering. anteriorly between the eyes. The integument of the
Biology: The larvae show a preference for shal- scutum is brown, and covered with brown narrow
low sunlit habitats and are frequently found on mead- scales and blackish brown setae. The scutellum is
ows, in irrigation channels, inundation areas of brown, occasionally with a pale greenish shine, with
rivers, or rice fields. Other common breeding waters brown coarse setae. The pleurites are brown with large
are ground pools, ponds, swamps, and marshes with patches of pale scales, but prealar scales are absent.
rich vegetation; the water may be fresh or slightly The femora have brown scales, usually slightly paler
saline. In southern Europe they are mainly found in on the ventral surface, with an indistinct knee spot.
salt water marshes (Ribeiro et al. 1988) and rice The tibiae and tarsomeres are dark brown scaled, and
fields. The larvae occur from late spring until late the hind tarsomere I is shorter than the hind tibia. The
autumn and they are often found together with those wings are entirely dark scaled, and the cross veins are
of the Anopheles species. In central Europe the sea- well separated. The abdominal terga are dark brown
sonal maximum of the adult population is recorded with separated basolateral spots of white scales, and
from the beginning of July to late September. Usually the sterna are uniformly covered with whitish grey
the females do not enter buildings, but readily bite scales.
humans outside, often during the day at sun and wind
exposed places. They may cause a considerable nui-
sance in some regions, especially in late summer
when the floodwater Aedes and Ochlerotatus species
have already vanished.
Distribution: Cx. modestus is widely distributed in
the Palaearctic region from England to southern
Siberia. It is recorded from middle and southwest Asia,
northern India, and northern Africa. In Europe it is a
common species in the southern and central countries.
Medical importance: The species has repeatedly
been reported as an arbovirus vector of two different
Bunyaviremia, Tahyna and Lednice (Lundström 1994)
and is also regarded as a potential vector of WNV
(Ribeiro et al. 1988). In addition, it has been found
naturally infected with tularemia (Gutsevich et al.
1974)

Culex (Barraudius) pusillus Macquart 1850

Female: It can be distinguished from the closely

related Cx. modestus by its commonly darker coloura-
tion and the separated basolateral pure white patches
of scales on the abdominal terga, which do not form a
continuous longitudinal stripe usually present in Cx. Fig. 10.93 Hypopygium of Cx. pusillus
268 10 Subfamily Culicinae

Male: The gonocoxite has scales on the outer

surface (Fig. 10.93). The lobe of the gonocoxite is
situated slightly beyond the middle of the gonocoxite,
with numerous setae and 2–3 strong spines of differ-
ent sizes which are recurved apically, one of them
may be more or less flattened. A single strong seta is
situated more distally on a small separated eleva-
tion. The gonostylus is straight or slightly curved,
relatively short, less than half as long as the gono-
coxite, with a broad base and tapering apically. 4–5
small setae are located on the outer surface of the
gonostylus close to its apex. The apex of the parap-
roct is densely covered with small spines forming a
paraproct crown. The ventral arm of the aedeagus is
long and curved at the apex and usually extends
beyond the paraproct crown. To distinguish Cx.
pusillus males from those of the similar Cx modes-
tus, the shape of the gonostylus and the length of the
ventral arm of the aedeagus should be taken into
consideration as indicated in the key. These two
characteristics are usually sufficient for a positive Fig. 10.94 Larva of Cx. pusillus
identification.
Larva: The body is nearly transparent, pale yel-
lowish green, and the head and siphon are slightly saddle seta (1-X) is short with 1–2 branches. The
pigmented. The antennae are weakly spiculate, upper anal seta (2-X) has 2–3 branches, 1 branch is
approximately as long as the head, straight, darkly longer than the others, and the lower anal seta (3-X)
pigmented at the base and distinctly narrowing from is long and single. The ventral brush has about 12
the insertion point of the antennal seta (1-A) to the cratal setae (4-X). The anal papillae are half as long
apex. Seta 1-A is inserted slightly below the middle as the saddle, and the dorsal pair is slightly longer
of the antennal shaft, and is half as long as the antenna than the ventral pair.
or slightly more, with 15–27 branches. The frontal Biology: Cx. pusillus is apparently a halophilic spe-
setae are long, the inner and median frontals (5-C and cies. The larvae are mainly found in coastal breeding
6-C) have 2–3 branches, and the outer frontal seta places, e.g. saline marshes and swamps, lagoons or
(7-C) has 7 branches. The comb consists of a patch of stagnant pools with or without vegetation. Occasionally
50 or more long fringed pointed scales (Fig. 10.94). they occur in saline inland waters such as salt lakes or
The siphon is short, more or less cylindrical, the main oases, but rarely in fresh water. Common associates in
tracheal trunks are broad, and the siphonal index is the breeding waters are larvae of Oc. caspius, An. mul-
about 3.0. The pecten has 11–13 teeth, the distalmost ticolor, and An. pulcherrimus. Cx. pusillus is not a
teeth extending slightly beyond the middle of the very common species, therefore little is known about
siphon, and each individual tooth is long and slender its biology and adult behaviour. They are frequently
with 1–3 lateral denticles. Setae 1-S have 8-10 tufts found between September and November (Martini
arranged in a more or less zig-zag row along the ven- 1931). Females have never been observed entering
tral surface of the siphon. 2–3 basalmost tufts are dwellings or stables and probably do not feed on
situated between the distal pecten teeth. The tufts humans (Senevet and Andarelli 1959).
with about 6 or more branches, are each at least as Distribution: Eastern Mediterranean, Middle East,
long as the width of the siphon at the point of its southwest Asia, and northern Africa. In Europe, Cx.
insertion. The anal segment is slightly shorter than pusillus is solely reported from eastern and southern
the siphon, the saddle is approximately as long as it is Greece (Samanidou-Voyadjoglou and Darsie 1993).
wide, and completely encircles the anal segment. The This may represent its northernmost record.
10.3 Genus Culex Linnaeus 269

10.3.2 Subgenus Culex Linnaeus

The body of the females is small to medium sized,

and the proboscis in some species has a pale ring in
the middle, but otherwise is entirely dark scaled.
The ­vertex has numerous erect scales, and the occiput
mainly has narrow scales with a few broad scales.
The setal and scale patterns of the scutum and pleu-
rites are as for the genus Culex. Lower mesepimeral
setae are usually absent, but in some species 2–3
setae may be found. The coxae have a few scales,
and wing scaling is as for the genus Culex. The
abdominal terga may or may not have basal pale
bands. The sterna are usually scaled and some spe-
cies have laterosternal patches of pale scales. The
proboscis of the males is usually lacking a pale ring.
Fig. 10.95 Hypopygium of Cx. brumpti
The gonocoxite is without scales, and the gonostylus
is flattened and bent, and an apical spine is present.
The structure of the aedeagus is very complex with
Male (Fig. 10.95): The subapical lobe of the gono-
differently shaped plates of outer and inner divisions.
coxite has a group of 3 long spine-like setae, two
The paraproct bears distally a crown-like area com-
broad, transparent scale-like setae and 2 shorter nar-
posed of heavy spines. The antenna of the larva is
row setae, one of them curved at the apex. At the base
spiculate, and is usually not longer than the head.
of the lobe there is an additional long, narrow hair-
Other morphological characteristics and setation are
like seta. The gonostylus is expanded beyond the
as for the genus Culex.
middle and then tapers apically. The apex of the para-
The subgenus Culex comprises the most species of
proct has several rows of stout spines. The dorsal arm
the genus, but the main portion of it is of tropical dis-
of the aedeagus is robust basally and directed out-
tribution. In Europe two species occur in northern
ward at an angle in the form of a sharp tooth, and the
parts, the rest in central and southern Europe. Cx. p.
ventral arm of the aedeagus is slender and curved,
pipiens occurs throughout the continent, whereas the
and extended apically in a fan shaped process
southern and northern limits of Cx. torrentium are not
(Fig. 7.62a).
fully understood. Other species have a more southern
Larva: Relatively large in size, with a curved
distribution or are limited to the Mediterranean and
antenna, abruptly narrowed distal from the insertion
adjacent areas.
point of the antennal seta (1-A). 1-A is situated at 2/3
length of the antennal shaft, with multiple branches.
The inner (5-C) and median (6-C) frontal setae have
Culex (Culex) brumpti Galliard 1931 2–3 branches, the outer frontal seta (7-C) has 6–8
branches. The comb is arranged in a patch of 22–24
Female: According to Galliard (1931) Cx. brumpti is a fringed scales (Fig. 10.96). The siphon is long and
relatively large mosquito. The proboscis is dark with slender, the siphonal index is about 6.0–7.0. The
an indistinct pale median ring, the scutum is covered siphonal setae (1-S) consist of 4–6 pairs of tufts, each
with brownish scales, sometimes slightly paler on its with 2–3 branches. The tufts are very short, much
post­erior part, and the pleurites have 5 patches of pale shorter than the siphon at the point of insertion, and
scales. The legs have pale spots at the femoro-tibial all tufts arise beyond the distalmost pecten tooth. The
and tibio-tarsal joints, and the tarsi are all dark, with- pecten has about 8–11 teeth occupying the basal
out pale rings. The wings are entirely dark scaled. The quarter to a third of the siphon. The main tracheal
abdominal terga have basolateral triangular pale trunks are broad. The anal segment is completely
spots. encircled by the saddle, the upper anal seta (2-X) has
270 10 Subfamily Culicinae

I have a few pale scales. The erect forked scales of

the vertex are light yellowish brown, and the curved
scales are white to pale yellowish. The integument of
the scutum is brown, and the scutal scales are light
yellowish-brown, with paler scales located anteriorly,
laterally, and on the prescutellar area. The scutal setae
are prominent, brown, and darker than the scales. The
scutellum has narrow pale curved scales and darker
setae on all three lobes. The pleural integument is
yellowish-brown, with yellowish to golden-brown
setae and patches of narrow pale scales. Postspiracular
and prealar scales are absent, the prealar area has
7–14 setae, and usually 2–3 lower mesepimeral setae
are present. The fore coxae have pale scales on the
anterior surface, and the mid and hind coxae have a
longitudinal area of pale scales. The fore and mid
femora have dark scales anteriorly and pale scales on
the posterior surface, and inconspicuous pale knee
spots are present. The hind femur is mainly pale
scaled with a dorsal stripe of dark scales widening to
encircle the distal end. The tibiae are dark scaled
anteriorly, whitish posteriorly, and the apex of the
Fig. 10.96 Larva of Cx. brumpti hind tibia has a prominent pale spot. The tarsi are
entirely dark scaled. The wings are dark scaled with a
short line of pale scales on the costa (C) located near
3–4 branches of varying length, and the lower anal the humeral cross vein (h). Tergum I has a median
seta (3-X) is single and nearly as long as the siphon. posterior patch of pale scales, terga II–VII have broad
The ventral brush has about 11 tufts of cratal setae pale basal bands, covering 1/2 to 2/3 of each segment,
(4-X). The anal papillae are pointed and nearly as and tergum VIII has lateral patches of pale scales
long as the saddle. (Fig. 6.54a). Sterna I–VII have cream coloured scales,
Biology: Because of its limited distribution range, and sternum VIII is usually entirely white scaled.
little information is available on the biology of Cx.
brumpti. In Corsica, the larvae were found in pools
with aquatic vegetation, and in river beds (Galliard
1931; Aitken 1954a). Both authors sampled the larvae
in August. Nothing is known about the feeding behav-
iour of adult females.
Distribution: Corsica, Sardinia.

Culex (Culex) laticinctus Edwards 1913

Female: The proboscis is dark, but slightly paler on

the basal half of the ventral surface. The palps are
usually entirely dark scaled, but palpomere III may
have a few apical pale scales. The clypeus and flagel-
lum are dark brown, and the pedicel and flagellomere Fig. 10.97 Hypopygium of Cx. laticinctus
10.3 Genus Culex Linnaeus 271

Male: The tergum IX has small lobes bearing 4–9 5-C and 6-C. The comb consists of > 30 evenly fringed
small setae. The gonocoxite is stout, with dense patches scales (Fig. 10.98). The siphon is straight, evenly
of long and short setae around the apex and near the tapering towards the apex, and the siphonal index
subapical lobe (Fig. 10.97). The lobe is distinctly averages 3.5 (2.8–4.6). The siphonal setae (1-S) con-
divided but not prominent, the proximal portion has 3 sist of about 7 pairs of tufts arranged in a more or less
stout setae, slightly flattened and bent distally, and the ventral zig-zag row, with the penultimate pair of tufts
distal portion has 2 setae similar in shape, and a displaced laterally. Each tuft has 6–9 branches about
crescent shaped, scale-like seta with a pointed apex. as long as the width of the siphon at its points of ori-
The gonostylus is relatively short, sharply bent in the gin, and 2–3 basalmost pairs of tufts arising within the
middle and then tapering towards the apex, with a crest pecten. The lateral and most distal tufts are smaller
of small sharp ridges close to the tip (Fig. 7.63a). The and have fewer branches than the others, and are
apex of the paraproct has several rows of spines, and shorter than the width of the siphon at the point of
the ventral arm of the paraproct is well developed and insertion. The pecten has 10–16 long curved teeth
curved. with 3–4 basal denticles, extending to near the middle
Larva: The head is wider than long, and the of the siphon. The saddle completely encircles the
antenna is about 2/3 the length of the head, curved and anal segment, and is longer than broad, the saddle seta
strongly spiculate, with a darker distal part. The anten- (1-X) is small, usually single, sometimes with 2
nal seta (1-A) has about 25 branches (19–30). Seta branches, the upper anal seta (2-X) has 4–5 branches
1-C is long and rather stout, and the postclypeal seta of varying length, and the lower anal seta (3-X) is
(4-C) is short and single. The inner frontal seta (5-C) single. The ventral brush has about 7 pairs of multi-
usually has 3–5 branches, the median frontal seta ple-branched cratal setae (4-X), and precratal setae
(6-C) usually has 4 branches, both reaching just are absent. The anal papillae are pointed, and about as
beyond the anterior margin of the head, and the outer long as the saddle.
frontal seta (7-C) has about 7 branches, longer than Biology: Cx. laticinctus seems to have been more
common in the past than it is today (Harbach 1988).
It was frequently collected in cisterns and concrete
basins or artificial pools, tanks and barrels in gardens
(Aitken 1954a). Nowadays it is more often found in
stream pools, rock pools, swamps or ditches. The lar-
vae usually occur in fresh water, but are occasionally
found in brackish water. They are often collected with
larvae of other Culex sp., Anopheles sp., Cs. annu-
lata, Cs. longiareolata and Ur. unguiculata. Cx.
laticinctus is mainly to be found in the summer
months, although a few specimens may occur during
the rest of the year. Adult females have never been
observed entering houses (Senevet and Andarelli
1959), and it is not known whether they bite humans
(Harbach 1988). Ribeiro et al. (1988) noted that it is
apparently a zoophilic species with little or no medi-
cal importance.
Distribution: The range of Cx. laticinctus extends
from the Canary Islands eastwards through the coun-
tries around the Mediterranean Sea, Somalia, Ethiopia,
Sudan, the Arabian Peninsula, to the Middle East, and
southwestern Asian countries. In Europe it is reported
in Portugal, Spain, Romania, Italy, Greece (Crete), and
Fig. 10.98 Larva of Cx. laticinctus former Yugoslavia.
272 10 Subfamily Culicinae

Culex (Culex) mimeticus Noe 1899

Female: It is the only European Culex species with

spots of pale scales on the wing veins and pale rings
on the tarsomeres. The head has narrow pale yellow-
ish scales dorsally, brownish laterally. The lateral
patches of broad white scales are quite prominent.
The palpomeres I–III are covered with blackish brown
scales, and the apex of palpomere V is usually white
scaled. The proboscis is predominantly dark scaled,
with a broad median white ring. The scutum is cov-
ered with yellowish to golden scales in the middle,
and greyish or whitish scales laterally. The pleurites
have patches of white scales. The femora and tibiae
of the fore and mid legs are usually entirely blackish
brown scaled anteriorly, sometimes speckled with
some pale scales, and the posterior surface is white
scaled. The anterior surface of the hind tibia usually Fig. 10.99 Hypopygium of Cx. mimeticus
has a distinct longitudinal stripe of pale scales.
Tarsomeres I–IV of all the legs have pale rings extend-
ing to both sides of articulation, and the basal rings
are broader. The wing veins are predominantly cov- gonocoxite has relatively short setae predominant on
ered with blackish brown scales, but numerous pale the inner surface (Fig. 10.99). The subapical lobe has a
scales form a characteristic spotted pattern broad, leaf shaped appendage and usually 4–6 large
(Fig. 6.52a). The anterior margin of the wing has flattened setae. The gonostylus tapers apically. The
three white spots, the first spot at the middle of the ventral arm of the aedeagus has 1–2 denticles, and the
costa (C), envelops (C) and subcosta (Sc), the second dorsal arm usually has three finger-like processes
at half distance toward the apex, envelops C, Sc and (Fig. 7.65a). The apical crown of the paraproct is large,
R1, and the third spot near the apex of the wing, usu- and made up of numerous spines. The ventral arm of
ally envelops C, R1 and R2. Pale scales are also pres- the paraproct is thin, and the apex is slightly curved
ent at the furcations of R2+3 and M, the broad ventrally.
midportion of R4, the midportion of Cu1 and the basal Larva: Similar to the larvae of the subgenus
portion of the anal vein (A). Cu2 is almost entirely Neoculex. The main tracheal trunks are narrow, less
covered with blackish brown scales, only a very short than half as wide as the siphon. The head is relatively
apical part may be pale scaled. The abdominal terga broad, often dark. The antenna is as long as the head,
are dark brown to black with transverse pale basal usually light with a darker apex, with the basal 2/3 cov-
bands (usually 1/3 as wide as the tergum) and large ered with tiny spicules. The antennal seta (1-A) is mul-
lateral pale spots. Terga VI and VII have narrow api- tiple-branched, and inserted just above the spiculate
cal bands. The sterna are white scaled, except for a region of the antennal shaft. The position of the subapi-
narrow apical portion. cal setae (2-A and 3-A) as well as the width of the tra-
Male: Similar to the female, but the contrast cheal trunks are valuable discriminative characteristics
between the dark and light scales on the wing veins between Cx. mimeticus and Cx. theileri. In the former
seems to be weaker. The palps are longer than the pro- species the subapical setae are inserted between 1/3 and
boscis, with blackish brown scales and usually 3 dorsal 1/2 of the distance between the apical setae (4-A to
patches of pale scales, one broad median patch on pal- 6-A) and the antennal seta (1-A) (Fig. 8.71a); in the lat-
pomere III, and two narrow basal patches on palpom- ter, they are located adjacent to the apical setae. The
eres IV and V, and the apex of palpomere V is covered labral seta (1-C) of Cx. mimeticus is relatively thick-
with pale scales. The proboscis has a median pale ring. ened in the middle, and often denticulated in the apical
The antennae are brown scaled, with pale rings. The part. The postclypeal seta (4-C) has 2–4 branches, the
10.3 Genus Culex Linnaeus 273

Biology: Cx. mimeticus is a polycyclic, orophilic

(associated with mountainous regions) species. It is
quite common in some parts of the Mediterranean
region. The larvae occur in small, shallow pools in
dried-up streams and torrent beds containing growth
of Spirogyra (Aitken 1954a), rock pools and in
shallow margins and backwaters of rapidly flowing
mountain streams overgrown with aquatic vegetation.
The breeding water is usually crystal clear with a pH
ranging between 5.2 and 6.0 (Ribeiro et al. 1977). The
larvae may be associated with those of An. atroparvus,
An. claviger, An. marteri, An. petragnani, An. super-
pictus, An. cinereus hispaniola, Cx. p. pipiens, Cx.
theileri, Cx. perexiguus, Cx. hortensis, Cx. impudicus,
Cx. territans, and Cs. longiareolata (Gutsevich et al.
1974; Ribeiro et al. 1977). They are reported from an
altitude of 3,055 m in Tibet (Feng 1938). The species
is moderately orophilic in Portugal, occuring from 150
to 1,100 m (Ribeiro et al. 1989). The females are zoo-
phylic, but occasionally enter houses and bite humans
(Sicart 1951).
Distribution: Oriental region, southern parts of the
Fig. 10.100 Larva of Cx. mimeticus
Palaearctic (Mediterranean, Middle East, Iran, Nepal,
Tibet, India, Vietnam, China, Japan). In Europe it is
recorded in the southern parts of the continent in
France, Italy, former Yugoslavia, Macedonia, Bulgaria,
inner frontal seta (5-C) has 3–5 branches, the median Greece, Cyprus, and Russia.
frontal seta (6-C) has 2–3 branches, and the outer fron-
tal seta (7-C) is 5–7 branched. The comb has 20–35
scales (usually 25–30), each scale with a distinct, strong Culex (Culex) perexiguus Theobald 1903
median spine and lateral rows of small spines
(Fig. 8.70a). The siphon is straight, gradually tapering The species is closely related to Cx. univittatus and
apically, and the siphonal index is 4.5–7.0, usually exhibits a very similar external morphology in all life
about 6.0 (Fig. 10.100). The number of pecten teeth is stages. Thus the following description of Cx. perex-
12–18 (usually 13–15), most often evenly spread over iguus, based on Harbach (1988), will highlight the dif-
the basal third of the siphon. Five to six pairs of sipho- ferences between the two species as there is some
nal setae (1-S) are inserted beyond the pecten. The chance that Cx. univittatus might occur in some parts
basalmost 3–4 pairs of tufts have 4–5 branches, they are of the Mediterranean region. However, Eritja et al.
at least twice as long as the width of the siphon at the (2000) recognised Cx. univittatus as a species occur-
point of their insertion. The two distal pairs of tufts ring in Spain according to findings of Encinas Grandes
have 2–3 thin branches, their length equal to the siphon (1982).
width at the point of their insertion, and a penultimate Female: A small sized mosquito. The proboscis is
tuft is articulated laterally. The saddle entirely encircles dark, with whitish scales ventrally except at the base.
the anal segment, and the saddle seta (1-X) has 2 The pedicel and flagellomeres have few pale scales.
branches. The upper anal seta (2-X) has 2 branches, The head has golden brown scales, and the vertex is
with the dorsal branch more than half as long as the pale scaled with forked brown scales laterally. The
ventral branch. The lower anal seta (3-X) is single and integument is brownish, the scutal scales are narrow
about as long as the siphon. The anal papillae are 1.5–2 and golden brown and pale scales form a pair of faint
times longer than the saddle. submedian spots. The postpronotum has golden brown
274 10 Subfamily Culicinae

scales which become paler posteriorly. The upper and tion necessary). The ventral arm of the paraproct is
lower posterior border of the mesepisternum and ante- long and recurved at the apex.
rior part of the mesepimeron have patches of white Larva: The head is broader than long, and the anten-
scales. The legs are dark scaled on the anterior surface, nal seta (1-A) has 19–27 branches. The frontal setae 5-C
and the hind tibia has a more or less distinct longitudi- and 6-C usually have 2–3 branches. The number of
nal anterior pale stripe (Fig. 6.55a). The tarsomeres are comb scales is 35–55, each individual scale is elongated
dark scaled dorsally, with pale scales ventrally. The and rounded apically. The siphon is usually long and
wings are dark scaled, with a short line of pale scales slender, and the siphonal index may vary (Fig. 10.102).
on the costa (C). The abdominal terga have slightly The number of pecten teeth is 8–15; the larger basal
convex white basal bands connected with the basolat- teeth are widely spaced, each with 3–4 lateral denticles.
eral patches. The sterna are whitish scaled, sometimes The siphonal seta (1-S) consists of five pairs of lateral
with dark scales, scattered or in patches. tufts usually positioned beyond the pecten. In Cx. uni-
Male: Tergum IX has two slightly elevated lobes vittatus the number of pairs is 5–6 and they are inserted
with long, spaced setae. In Cx. univittatus the lobes more ventrolaterally, with the two basalmost tufts (1a-S
seem to be almost flat and the coverage of setae is and 1b-S) attached within or close to the pecten. All
denser. The gonocoxite has numerous long and short tufts in both species have short branches not exceeding
setae (Fig. 10.101). The subapical lobe is slightly the width of the siphon at the point of insertion. The
divided; the proximal portion has 3 long and strong saddle entirely encircles the anal segment, and the anal
setae, and the distal portion has three shorter hair-like papillae are short.
setae and one broad, spatulate seta. In Cx. univittatus Biology: The species is common during summer
the latter seta is narrower. The gonostylus is expanded and autumn. The larvae can be found in many kinds of
beyond the middle, and has two setae and a short api- stagnant water collections, e.g. clean to moderately pol-
cal spine. The aedeagus has a stout ventral arm and luted swamps, ponds, streams, pools, wells, usually
concave apex, without any spines, which is shorter with emergent vegetation, and occasionally in man-
than the dorsal arm (Fig. 7.62b). In Cx. univittatus the made containers. The adult females probably prefer to
ventral arm is as long as the dorsal arm, and they seem feed on birds (Harbach 1988). This has also been
to be in line in a lateral view of the aedeagus (prepara- reported for Cx. univittatus from Turkmenia (Gutsevich

Fig. 10.101 Hypopygium of Cx. perexiguus Fig. 10.102 Larva of Cx. perexiguus
10.3 Genus Culex Linnaeus 275

et al. 1974). Martini (1931) reported the species (as Cx. discern between pipiens, molestus, and quinquefascia-
univittatus) as biting humans inside houses at night. tus females and overlapping was considerable (Kruppa
Distribution: This species is recorded in Portugal, 1988). Thus, there is no reliable characteristic yet for
Spain, Italy including Sicily, Macedonia, Bulgaria, discrimination between pipiens and molestus.
Greece, and Turkey (Snow and Ramsdale 1999). Cx. The former Cx. quinquefasciatus Say and Cx. quin-
perexiguus is found in Asia Minor, south western Asia quefasciatus pallens Coquillet are currently regarded
towards India, and in northern Africa (Harbach 1988). as subspecies of Cx. pipiens (Miller et al. 1996). They
Medical importance: From Israel and Egypt Cx. freely hybridize but show a difference in the male
perexiguus has been reported as a vector of WNV hypopygial morphology (Kruppa 1988). Cx. pipiens
(Harbach 1988). pipiens and Cx. torrentium are two separate sibling
Notes on systematics: The species name which species (Harbach 1985; Dahl 1988; Harbach 1988;
has hitherto been used for European material is Cx. Miller et al. 1996) defined by genetic characteristics
univittatus, but Harbach (1999) stated that Cx. uni- and different morphology in some life stages.
vittatus is restricted to the temperate highlands in the
East African Subregion of the Afrotropical Region
and identified a few specimens from Greece, Italy, Culex (Culex) pipiens pipiens Linnaeus 1758
and Turkey as Cx. perexiguus based on characteris-
tics of the male genitalia and larvae. He suggested Female: A medium sized mosquito, with a yellowish
regarding the species which occurs in southern brown to dark brown integument. The antennae are
Europe, that it should be rather Cx. perexiguus than dark, and the pedicel and flagellomere I have a few
Cx. univittatus, although Eritja et al. (2000) con- tiny white scales. The palps are mainly black scaled,
firmed the presence of Cx. univittatus in Spain. and the proboscis has cream coloured scales ventrally.
The head has dark forked scales and some paler scales
laterally. The scutum has delicate golden brown scales,
Culex Pipiens Complex which are lighter laterally. The scutellum has narrow,
pale yellow scales and dark setae. The postpronotum
The complex consists of several species, subspecies, has golden brown scales. The pleurites have yellowish
forms, races, physiological variants, or biotypes or white scale patches on the mesepisternum.
according to various authors. At present it includes the Postspiracular and prealar scales are absent, or rarely a
names Cx. pipiens pipiens Linnaeus, Cx. p. pipiens few scales may be present. The absence of scales in
biotype molestus Forskal, Cx. p. quinquefasciatus Say, Cx. p. pipiens provides an almost reliable characteris-
Cx. p. pallens Coquillett, Cx. restuans Theobald, and tic for separation from Cx. torrentium females which
Cx. torrentium Martini in the Holarctic as well as two have a few prealar scales when undamaged. The coxae
Australian members, Cx. australicus Dobrotworsky have a small patch of dark scales, the femora have a
and Drummond and Cx. globocoxitus Dobrotworsky. yellowish apical border but otherwise are dark scaled,
The status of the three first names has been and the hind femur has mostly whitish scales. The tib-
­taxonomically stabilized by designation of neotypes iae and tarsi are dark scaled, the hind tibia lacks a lon-
(Sirivanakarn and White 1978; Harbach et al. 1984, gitudinal pale stripe (Fig. 6.55b). The scaling of the
1985). It is now generally accepted that the former wings is dark, and the subcosta (Sc) intersects the costa
Cx. pipiens molestus (Harbach et al. 1984) is not sep- (C) beyond the furcation of R2+3 (Fig. 6.52b). The
arated from the subspecies Cx. pipiens pipiens and is abdominal terga are predominantly dark scaled; ter-
designated as a biotype, as no genetical differences gum II has a small basomedian whitish spot, and terga
have been found (Bourguet et al. 1998). However, III–VII have whitish to yellowish, narrow basal bands
new data based on protein electrophoresis revealed a which expand laterally (Fig. 6.54b). The sterna are yel-
significant genetic distance between the two forms lowish scaled.
(Becker et al. 1999). Male: The subapical lobe of the gonocoxite has
The females of the complex are very difficult to seven large, simple and one broad scale like setae
separate in field material. In several reared populations (Fig. 10.103). The gonostylus is broad with several
it took eight variables and a discriminant analysis to small and two spiniform setae apically. The aedea-
276 10 Subfamily Culicinae

Fig. 10.103 Hypopygium of Cx. p. pipiens

gus has several complicated plates and lobes of

which the ventral and dorsal arms are diagnostic
characteristics and are used for the so called DV/D Fig. 10.104 Larva of Cx. p. pipiens
formula (Sirivanakarn and White 1978; Ishii 1991).
The shape of the ventral arm is slender, blade-like
with a sharply pointed apex. The dorsal arm is tubu- ranges between 4.8 and 5.0 (Fig. 10.104). The number
lar, stout, and distinctly truncated at the apex of pecten teeth is 13–17, evenly spaced up to seta
(Fig. 7.64b). The ventral arm of the paraproct varies 1a-S. Each pecten tooth has a long pointed tip and
in length from being an inconspicuous knob to a con- three lateral denticles. The siphonal tuft (1-S) consists
spicuous extension which is never recurved. The of four widely spaced 2-branched pairs of setae which
paraproct has numerous stout setae forming a brush- arise distal to the pecten in an irregular row. The anal
like crown. It is possible to ­distinguish it from Cx. papillae are elongate, and the dorsal pair is twice as
torrentium by the blunt apex of the dorsal arm and a long as the saddle. The larvae of the species complex
different shape of the ventral arm of the paraproct, are very similar. Those of Cx. p. pipiens and Cx. tor-
which is long, sclerotized, and recurved at the apex rentium can only be distinguished from each other
in Cx. torrentium. when the specimens are very well preserved; differ-
Larva: The head is wider than long, and the ences in abdominal setation are as indicated in the
antenna is shorter than the head. The postclypeal seta keys (Fig. 8.77c). The larvae of Cx. p. quinquefascia-
(4-C) is short and simple, and all frontal setae are tus have a significantly shorter siphon (the siphonal
long. The inner frontals (5-C) have 5–6 branches, the index is about 4.0).
median frontal seta (6-C) is 4–5 branched, and the Biology: Females usually do not feed before enter-
outer frontals (7-C) have 6 branches. The prothoracic ing winter shelters; the specimens which have taken a
setae 1-P to 3-P are long and single, 4-P has 2 branches small blood meal before overwintering have a poorer
and is somewhat shorter than the other setae, 5-P and chance of surviving (Mitchell and Briegel 1989).
6-P are single and long; 7-P is 2-branched and long. Overwintering females lay their eggs on the water sur-
The metathoracic seta 1-T is shorter than half the face in batches as egg rafts of usually 150–240 eggs.
length of 2-T. The number of comb scales is about 40, The larvae hatch within 1 or 2 days and complete their
each individual scale is short and widened at the apex, development to adults in about one to a few weeks,
and evenly fringed. The siphon is slender, evenly depending on the temperature. They are able to inhabit
tapered towards the apex, and the siphonal index nearly every kind of water source. The first larvae
10.3 Genus Culex Linnaeus 277

often occur together with those of Anopheles species which have not confirmed a species specific status
and can be found in semi permanent waters, larger (Bourguet et al. 1998). However, the males can be sep-
pools with vegetation, rice fields, along river edges in arated by morphological characteristics (Sirivanakarn
still zones, and in inundation areas; occasionally even and White 1978; Kruppa 1988).
in tree-holes. The larvae frequently occur in man-made
water bodies such as flooded cellars, construction sites,
water barrels and tin cans, metal tanks, ornamental  ulex pipiens pipiens biotype molestus
C
ponds, and containers in gardens and in churchyards. Forskal 1775
They even tolerate a small amount of salinity and can
occur in rock pools. The species can develop up to sev- The biotype cannot be distinguished from Cx. p. pipi-
eral generations per year depending on climatic condi- ens on a single morphological characteristic in adults.
tions. The females are anautogenous, ornithophilic, Kruppa (1988) found a statistical difference in the
eurygamous, and diapausing in wintertime. Occasion- ­larval mentum between pipiens, quinquefasciatus,
ally they have been observed to feed on wild mammals and molestus in reared strains. No reliable genetic
or on mice in the laboratory. In southern France, anau- marker was found to separate molestus from pipiens
togenous populations with stenogamous males of Cx. (Bourguet et al. 1998). However, four biological crite-
p. pipiens have been reported from the field. Its bio- ria for the biotype molestus have been established:
type molestus occurs more frequently in human autogeny, stenogamy, anthropophily, and facultative
environments. diapause.
Distribution: Cx. p. pipiens is widespread in the Female and male: Colouration, setae, and scaling
Holarctic region and found throughout Europe. Its dis- of head, thorax, abdomen, wings, and legs as in Cx. p.
tribution seems to be more northern in the easternmost pipiens (Harbach et al. 1984). The males are stenoga-
European parts than in Scandinavia. Its northern bor- mous, meaning copulation with females in very lim-
ders throughout Europe need renewed analysis, as it ited spaces without swarming is possible. This has
has not always been distinguished from Cx. torren- led to a search for male morphological characteristics
tium. It has been introduced into Australia and also to distinguish between pipiens and molestus
into South America and eastern and South Africa. (Oljenicek and Zoulova 1994). The first character
In the southeasternmost areas of the northern hemi- was found in the length of palpomere IV, which gave
sphere Cx. p. pipiens occurs sympatrically with Cx. a reliable difference from that of molestus, being 1.5
p. quinquefasciatus. times longer than that of pipiens, a result in contrast
Medical importance: Cx. p. pipiens seems to play to earlier observations (Harbach 1988). The second
a minor role as an arbovirus vector in Europe. character is the average length of the antennal seta
Nevertheless, one report of high incidence of WNV compared to the average length of the antenna,
from Romania (Nicolescu 1998) and a record of low expressed in an antennal index. This index is 3.5 in
incidence of Ockelbo virus from wild caught females pipiens and ranges between 4.1 and 4.4 in molestus.
(Lundström 1994) demonstrate the capacity of the spe- These morphometric parameters were measured on
cies for arboviruses. reared material.
Notes on systematics: The species is highly vari- Larva: The morphological characteristics are so
able in its pattern of integument and scaling colour, variable that only identification based on eight charac-
hence it has numerous synonyms worldwide. From ters with statistical analysis gave some discrimination
European material nine valid synonyms exist (Knight between pallens, molestus, and pipiens. More reliable
and Stone 1977; Knight 1978; Ward 1984, 1992). Two is the discrimination between all three mentioned taxa
further invalid subspecies descriptions on European against Cx. p. quinquefasciatus (Kruppa 1988).
material and now treated as synonyms, are the former However, it is claimed by many authors that a differ-
Cx. p. torridus Iglisch and Cx. p. erectus Iglish (Dahl ence in the siphonal length can be found with a shorter
1988; Harbach 1988). There are different views as to siphon in molestus than in pipiens (Oljenicek and
the specific status of Cx. pipiens and Cx. quinquefas- Zoulova 1994). Previously, this was correlated with
ciatus. They are still regarded as one species based on highly polluted larval habitats characterized by a high
their mode of hybridisation and molecular studies content of ammonia (Gabinaud et al. 1985).
278 10 Subfamily Culicinae

Biology: A well-accepted biological character of Culex (Culex) pipiens quinquefasciatus Say 1823
the biotype molestus is the autogeny of the females,
which might even occur in several forms (obligate Closely resembling Cx. p. pipiens in colouration, differ-
or facultative) as among other culicid species ing in the yellowish brown not reddish or dark brown
(O’Meara 1985; Clements 1992). Without taking scales on the scutum and in the structure of the lateral
any blood meal the females lay much fewer eggs aedeagal plates of the hypopygium (Gutsevich et al.
and can bite readily after the first batch (Harbach 1974). In Cx. p. quinquefasciatus the inner division is
et al. 1984). Females do not have an obligate dia- simple, represented by a broad leaf like ventral arm
pause. They can reproduce throughout the winter in which is strongly divergent laterally and the dorsal
dark, warm urban habitats containing water or over- arms parallel or subparallel and distally strongly
winter in unheated cellars or similar man-made tapered into a point (Sirivanakarn 1976) (Fig. 7.66.c).
shelters. The mortality in winter shelters is very In Cx. p. pipiens the ventral arm is sickle shaped,
high (95–100%) and mainly caused by the lack of smaller, shorter, and narrower and the dorsal arms
fat body reserves obtained in the larval stage, by divergent and uniformly thick, with a truncated apex
entomopatogenic fungi and spiders. Males and (Fig. 7.66a, Fig. 10.103).
unmated females do not survive the winter (Petrić The females of the two subspecies cannot be distin-
1985; Petrić et al. 1986). The males are stenoga- guished with certainty but in some regions such as
mous; they readily mate in confined spaces without Australia, the difference in the pale banding on the
swarming. The most common larval habitats are terga may enable separation. In Cx. p. quinquefascia-
dark and moist cellars of large buildings in towns, tus the distinct basolateral pale spots are apparently
underground sewage constructions, and man-made not connected with the evenly broad or slightly medi-
water containers in dark, humid places. ally produced basal pale bands, whereas in Cx. p. pipi-
Distribution: Females of the complex, registered ens biotype molestus the pale bands on the terga are
as molestus because of biting humans both indoors and not constricted laterally (Russell, pers. commun.).
outdoors, have been reported from many of the largest Biology: The “Southern House Mosquito” is one
cities throughout Europe and temperate regions of the of the most troublesome mosquitoes, biting, like other
world. There are records even from very northern cit- Culex, almost exclusively at night (Edwards 1941). It
ies in the European parts of Russia. No recent sum- occurs abundantly in houses and in practically all
mary of the occurrence of molestus throughout Europe types of human and animal shelters in urban commu-
or other continents is available. nities throughout the tropics at diverse altitudes up to
Medical importance: One of the major bridge vec- 2,300 m above sea level (Mara 1945). The larvae can
tors of WNV worldwide. Cx. p. pipiens biotype moles- be found in any type of habitat which contains water
tus and Cx. restuans account for more than 80% of the ranging from fresh and clear to brackish, turbid and
total risk, a surrogate for human WNV infections in polluted with decayed organic matter from garbage
the northeastern United States. The threat of these two and human waste accumulated in ground pools,
species is nearly 16 times higher than that for the four ditches, drains, sewages, dumping areas, latrines, sep-
other important vectors of WNV, Oc. japonicus, Ae. tic tanks, and in various kinds of artificial containers.
vexans, Oc. trivittatus, and Cx. salinarius (Kilpatrick In general, Cx. p. quinquefasciatus is uncommon in
et al. 2005). small containers, but common in large ones
Notes on systematics: Cx. molestus was described (Sirivanakarn 1976). The adults are fairly abundant
as a species by Forskål 1775 on Egyptian material. throughout the year and are commonly found resting
Harbach et al. (1984) selected a neotype and at the during the day in dark places in wardrobes, bathrooms,
same time stated that molestus was not a valid species. under tables, and similar places inside houses. The
All claims to identify molestus on morphological females are vicious biters at night, indoors or outdoors
characteristics failed. This might depend on an exten- and feed principally on blood of humans from sunset
sive gene flow between the populations. A certain until dawn. They also frequently attack birds such as
hybridization between the forms has been postulated poultry and, to a lesser extent, other domestic animals,
for natural conditions and was tested in laboratory including dogs, cats, and pigs. The range of hosts for
experiments (Chevilon et al. 1995). the blood meal is broad but different populations vary
10.3 Genus Culex Linnaeus 279

in this respect. The females are stenogamous and not some whitish scales. A patch of prealar scales is
autogenous and they can develop several generations present in most newly emerged specimens. The coxae
per year without diapause (Dobrotworsky 1965; have patches of light scales, the femora are dark, ventrally
Gutsevich et al. 1974). whitish, with a white knee spot. The tibiae are dark
Distribution: Widespread throughout the tropics scaled, ventrally whitish, and the hind tibia has no lon-
and subtropics of the world. gitudinal pale stripe. All the tarsomeres are dark brown
Medical importance: Cx. p. quinquefasciatus is with some light ventral scaling. The wing veins are
one of the most serious pests of man in the tropics and covered with brownish, elongated scales. The abdo-
has been incriminated as the principal vector of noctur- men is dark brown with pale yellowish basal bands on
nal periodic bancroftian filariasis in various parts of the all segments which are not expanded laterally.
Oriental region. It is an important vector of Brugia Male: Although there seem to be some constant
malayi (Malayan filariasis) and Dirofilaria immitis (dog features in the scaling of the proboscis and legs of the
heartworm) and some plasmodia of birds. In some parts males, the most reliable characteristics for distinguishing
of Southeast Asia, it has also been reported to be a host Cx. p. pipiens from Cx. torrentium are found in the
of certain arboviruses, notably Chikungunya and hypopygium (Fig. 10.105). The dorsal arm of the aede-
Japanese encephalitis but there is apparently no conclu- agus is pointed and twisted at the apex and not blunt as
sive evidence to indicate that it plays a role in the natu- in Cx. p. pipiens. In Cx. torrentium the ventral arm of
ral transmission of these diseases. This may in part be the paraproct is always long and recurved, without
due to the fact that it rarely bites reservoir animals such much variability in shape. In Cx. p pipiens it varies
as pigs infected with Japanese encephalitis virus. It is a from being vestigious to conspicuous, but is never
vector of St. Louis encephalitis and Western Equine recurved. The shape of the cercal sclerite of the parap-
encephalitis in the Americas (Gutsevich et al. 1974; roct is broader and shorter in Cx. torrentium than in
Sirivanakarn 1976). Cx. p. quinquefasciatus is the pre- Cx. p. pipiens.
dominant vector of WNV in the southeastern and much Larva (Fig. 10.106): The larvae differ from those
of the western parts of the United States (Reisen et al. of Cx. p. pipiens and its biotype molestus in some very
2004; Kilpatrick et al. 2005). subtle characteristics. Harbach et al. (1985) found
some differences in the thoracic and abdominal seta-
tion as indicated in the keys (Fig. 8.77a).
Culex (Culex) torrentium Martini 1925

The species is very similar to Cx. p. pipiens in all

stages, except for larval seta 1-T (Harbach et al. 1985),
the prealar scale patch (Service 1968a), the pointed
and twisted apex of the dorsal arm of the aedeagus and
the curved ventral arm of the paraproct in the male
hypopygium, and the pattern of the egg chorion (Dahl
1988). Wild caught females are larger in average body
size than those of Cx. p. pipiens. This character is very
subtle and needs much experience to recognise it.
Martini (1931) highlights some differences in scaling
which seem to give some guidance for specimens from
central and east Europe.
Female: The proboscis is dark with a whitish mid-
part and pale scaling ventrally, and the palps are dark
brown scaled. The antenna is dark with a whitish tinge.
The head has yellowish flat scales on the occiput and
vertex and around the eyes, the setae are golden to dark
brown. The scaling on the scutum is brownish, api-
cally lighter, and on the pleurites is brownish with Fig. 10.105 Hypopygium of Cx. torrentium
280 10 Subfamily Culicinae

Culex (Culex) theileri Theobald 1903

Female: A large mosquito, with a brown general colou-

ration. The most striking feature is the presence of a
longitudinal pale stripe on the anterior surface of all
the femora and tibiae, particularly on the fore and mid
legs. The palps are predominantly brown scaled, pal-
pomeres III and IV have pale scales dorsally, some-
times largely pale scaled. The proboscis is brown
scaled with more or less numerous pale scales predom-
inating in the middle, but not forming a distinct ring.
The head has white, yellowish or golden brown narrow
decumbent scales and brown erect scales. The scutum
has golden brown scales medially, yellowish white
laterally, and is whitish at the prescutellar area. The
postspiracular area has a broad patch of pale scales.
The upper and lower mesepisternal patches of scales
are fused forming a stripe at the posterior margin of the
mesepisternum. The femora and tibiae of the fore and
Fig. 10.106 Larva of Cx. torrentium mid legs have an anterior longitudinal white stripe
along their whole length (Fig. 6.53a), and sometimes
the fore femur has a linear row of white spots instead.
Biology: The larvae occur throughout the warmer The tarsomeres of the fore and mid legs are entirely
season, often together with those of Cx. p pipiens in dark. Tarsomere I of the hind leg has a distinct white
both unpolluted and polluted habitats, such as edges of stripe on its anterior surface, but the remaining tarsomeres
slow running streams, in vegetation at borders of lakes, are completely brown scaled. The basal half of the
semipermanent pools, marshy areas, man-made con- costa (C) has pale scales. Sometimes the subcosta (Sc)
tainers, and reservoirs of sewage plants. The develop- and radius (R) also carry some pale scales (Aitken
ment seems to be slower than in Cx. p pipiens which 1954a). The other wing veins are entirely dark scaled.
might result in only one generation per year in north- There are pale scales on tergum I and sometimes
ern areas. Females are ornithophilic and have never median scale patches on terga II and III. Terga IV–VII
been reported to bite humans, not even in laboratory have broad basal pale bands which are usually triangu-
colonies. Both sexes are most active in nectar feeding larly produced posteriorly, sometimes with median
between 2200 and 0300 hours (Andersson and Jaenson yellowish dots, which may form a pale median longi-
1987). However, in captivity the females live longer tudinal stripe. Tergum VIII is completely covered with
and lay their eggs more scattered through time and in yellowish scales.
smaller batches. The pattern of the eggs’ exochorion is Male: The palps are longer than the proboscis at
more widely spaced in Cx. torrentium than in Cx. p least for the length of palpomere V, brown scaled, with
pipiens, this characteristic needs verification from more or less numerous pale scales which sometimes
other geographic areas (Dahl 1988). form rings. The lobe of tergum IX has 10–12 setae.
Distribution: The species seems to have a wide The subapical lobe of the gonocoxite has 4 flattened
distribution in the temperate Palaearctic region and blade-like setae, a thin hair-like seta and a leaf shaped
neither its southernmost or northernmost borders are seta which is relatively broad and elliptical
well established. (Fig. 10.107). The gonostylus is sickle shaped with a
Medical importance: In northern Europe, Ockelbo slender subapical spine. The ventral arm of the aedea-
virus (Alpha virus) has been isolated from Cx. gus has 2–4 strong lateral teeth, and the dorsal arm is
pipiens/Cx. torrentium. In the laboratory, the vector simple and pointed apically.
competence of Cx. torrentium was much higher than Larva: The antennal shaft is strong, 3/4 of the length
that of Cx. pipiens (Lundström 1994). of the head, with a darker base and apical part. The
10.3 Genus Culex Linnaeus 281

frontal seta (5-C) is 2–5 bran­ched, the median fron-

tal seta (6-C) has 2–4 branches, and the outer frontal
seta (7-C) is 6–10 branched. The number of comb
scales ranges between 12 and 44, usually with 20–30
scales (Fig. 10.108). Each individual scale has a
strong median spine, with or without lateral rows of
smaller spines. The siphon slightly tapers apically, and
the siphonal index ranges from 4.0 to 8.0, usually 5.0–
6.0. The main tracheal trunks are broad, at least half as
wide as the siphon, with an oval cross section. The
pecten is restricted to the basal third of the siphon,
with 5–15 widely spaced teeth. Five, sometimes six
pairs of siphonal setae (1-S), are inserted beyond the
pecten (an odd number of setae could be present as
well). The three basal pairs are subequal in length, 4–6
branched, situated in a zig-zag row on the ventral sur-
face of the siphon, and are about as long as the width
of the siphon at the point of insertion. The two distal
Fig. 10.107 Hypopygium of Cx. theileri pairs are weaker and shorter, inserted laterally and sub-
ventrally, with 2–5 branches. The saddle seta (1-X) has
1–3 branches, the upper anal seta (2-X) has 3–4
branches, and the lower anal seta (3-X) is single and
longer than the siphon. The ventral brush has 14 well
developed cratal setae (4-X), without precratal setae.
The anal papillae are about as long as the saddle, slen-
der, pointed, and both pairs are of similar length.
Biology: A polycyclic species recorded from a broad
range of elevations. It is reported to be common at
altitudes of 1,000–3,000 m in the Himalayan areas
(Sirivanakarn 1976). The larvae occur in spring in
flooded meadows, stagnant or slowly moving streams,
ditches, rock pools, drains, swamps, and rice fields but
also frequently in artificial containers and strongly pol-
luted waters (Aitken 1954a; Sirivanakarn 1976; Ramos
et al. 1978). They usually breed in fresh or slightly saline
water (2 g NaCl/l), but tolerate a salinity up to16.6 g
NaCl/l and pH 5.5–9.5 (Gutsevich et al. 1974; Ramos
et al. 1977; Pires et al. 1982). The larvae can often be
found in association with those of An. algeriensis, An.
Fig. 10.108 Larva of Cx. theileri atroparvus, An. claviger, An. labranchiae, An. maculi-
pennis, An. superpictus, Ae. vexans, Ae. vittatus, Oc.
caspius, Oc. detritus, Cx. modestus, Cx. laticinctus, Cx.
p. pipiens, Cx. perexiguus, Cx. hortensis, Cx impudicus,
antennal seta (1-A) is multiple-branched (up to 30 Cs. longioreolata, Cs. annulata, Ur. unguiculata
branches), and the subapical setae 2-A and 3-A are (Coluzzi 1961; Bozkov et al. 1969; Ramos et al. 1977;
inserted close to the apex (Fig. 8.71c), and not separated Pires et al. 1982). The females are zoophilic, but some-
from the apical seta as in Cx. mimeticus. The labral seta times feed on humans and bite mainly in the open, occa-
(1-C) is dark, strong, spiniform, and gradually tapering. sionally in large numbers, also entering houses and other
The postclypeal seta (4-C) is 1–3 branched. The inner buildings (Gutsevich et al. 1974; Ramos et al. 1977).
282 10 Subfamily Culicinae

Distribution: Scattered through the Ethiopian The small subgenus consists of about ten species
(south, east and north Africa), Palaearctic (Medit­ only. The majority of this is distributed in the Ethiopian
erranean, Ukrainian steppes, Crimea), Middle East, region including Madagascar or in westernmost Asia.
and the east Oriental region (India, Burma, China). One species, namely Cx. hortensis, is regularly found
In Europe it is reported from Portugal, Spain, France, in the European region with a distribution in the
Italy, former Yugoslavia, Greece, Hungary, Bulgaria, and Mediterranean area and central Europe. Another spe-
Ukraine. cies of Maillotia, Cx. deserticola, which was trans-
Medical importance: In South Africa, Sindbis virus ferred from subgenus Neoculex (Harbach 1985), has a
and WNV were isolated from wild populations (McIntosh very limited distribution in Europe. There is one doubt-
1975). Cx. theileri is known to be a carrier of Rift Valley ful record from Corsica (Schaffner 1998) and one con-
Fever virus and canine Dirofilaria in North Africa and firmed record from the Zaragosa Province in Spain
Portugal (Smith 1973; Ribeiro et al. 1983, 1988). (Ramos et al. 1998). The species was found in an area
well known as a faunistic refuge regarding other taxa
of insects (Eritja et al. 2000). Because of its isolated
occurrence in only one location, Cx. deserticola is not
10.3.3 Subgenus Maillotia Theobald included in the keys, and no detailed morphological
description is given.
The palps of the females are much shorter than the
­proboscis. The head has mixed white and dark to golden
scales. The scutum and pleurites have many whitish Culex (Maillotia) hortensis Ficalbi 1889
and dark, somewhat narrow scales, sometimes in more
distinct patterns. Prealar scales and usually postspirac- Female: The general appearance of the female is simi-
ular scales are present. A white knee spot is present, and lar to Cx. territans with greyish unspotted wings but
the tarsi are uniformly dark scaled. The abdomen may usually paler scaling on the scutum and thorax. The
or may not have pale basal bands or lateral patches. The relative broad pale apical bands on the abdominal terga
wing veins are covered with long, narrow dark scales. and their distinct median widening at least on some
Mohrig (1969) mentioned an important wing character- terga differentiate the females from the Cx. territans
istic, which separates species of the subgenus Maillotia and other Culex species in Europe. The proboscis is
from those of the subgenera Culex and Neoculex. In usually entirely dark scaled, sometimes with scattered
Maillotia, the ending of the subcosta (Sc) into the costa pale scales on the ventral surface. The scaling of the
(C) corresponds roughly with the branching of veins palps is variable, often with pale scales at the apex
R2+3. The palps of the males are longer than the proboscis. forming a ring on the palpomere V, but sometimes
The gonocoxite has a mesally displaced subapical lobe entirely dark scaled. The occiput has light scales, the
bearing broad, heavy spines and a flat apical distention eyes are bordered with whitish scales, and the vertex is
which reaches beyond the joint of the gonocoxite and whitish with some dark scales. The scutum has dark
gonostylus. The latter is bent and broad with several setae and is mostly brownish scaled, very often whitish,
setae and one apical spine. The aedeagus is insignifi- narrow scales form lateral stripes, and the scutellum
cant, the paraproct is broad and crowned with denticles always has whitish narrow scales. The mese­pisternum
and stout spines. The head of the larvae is usually and mesepimeron have a few pale scale patches. The
broader than long. Seta 3-P is nearly as long as setae coxae have white scales on the ventral surface, and the
1-P and 2-P. The comb scales are arranged in an irregu- femora are white scaled, the hind femur has dark scales
lar patch, each individual scale is usually elongated and dorsally. White knee spots are present, and the tibiae
fringed with numerous thin spines. The siphon is very and tarsomeres are dark with a few white scales on the
long and slender. The pecten has widely spaced teeth, ventral surface. The apex of the hind tibia has a white
and the siphonal tufts (1-S) are arranged in a more or spot which is sometimes difficult to detect. The wing
less regular ventral row covering at least 2/3 of the veins are entirely dark scaled, except for the basal 1/5
siphonal length, and some distal tufts are laterally of the costa which has pale scales. The end of Sc is
displaced. The cratal setae (4-X) are situated close to nearly aligned with the furcations of R2+3 and M
the anal papillae. (Fig. 6.56a). Terga I–III have broad pale apical bands
10.3 Genus Culex Linnaeus 283

Fig. 10.109 Hypopygium of Cx. hortensis

Fig. 10.110 Larva of Cx. hortensis

with a median widening, the rest of the terga have siphon. The ventral brush consists of 12–14 tufts of
narrow pale apical bands. cratal setae (4-X).
Male: The palps are almost completely devoid of Biology: Little is known about the phenology and
setae. The lobes of tergum IX are inconspicuous. This general biology of Cx. hortensis as the species is
species is easily differentiated from all other European rather uncommon and seems to occur in large num-
members of the genus Culex by a broad, flattened, bers only sporadically. The larvae usually occur in
sclerotized process at the apex of the gonocoxite clear water with a certain amount of algae and other
(Fig. 10.109), which extends distinctly beyond the vegetation, but also in rice fields, small ponds, unused
base of the gonostylus. The gonostylus is bent, and the wells, or garden pots. Hibernation takes place in the
aedeagus has a dorsal and ventral bridge. The paraproct female stage; daytime resting sites are dark places,
has denticles and several rows of spines. e.g. wooden stables. The females usually do not feed
Larva: The head is wider than long, and the anten- on humans.
nae are long and slender, apically with extremely long Distribution: In Europe, Cx. hortensis is frequently
spines. The antennal seta (1-A) has about 10 branches, found in the Mediterranean region. It occurs on the
and the antennal shaft is covered with ­several short Canary Islands and is distributed through Spain,
spicules around the insertion point of 1-A. The inner France, Italy, and Greece up to central Europe, where
and median frontal setae (5-C and 6-C) have 2 it is rarer. It can also be found in north Africa, Middle
branches, and the outer frontal seta (7-C) has at least Asia, and India.
5 branches. The prothoracic seta 3-P is nearly as long
as 1-P and 2-P (Fig. 8.66a). The comb scales are
arranged in an irregular triangular spot, and each indi-
vidual scale may be of two shapes, either long, narrow
10.3.4 Subgenus Neoculex Dyar
and pointed or shorter and rounded apically. The
siphon is long and slender, and the siphonal index is Small to medium sized species, the vertex has erect and
between 6.5 and 8.0, with at least 4–5 pairs of long narrow scales. The palps are not longer than one quarter
siphonal tufts (1-S) situated in a more or less ventral of the length of the proboscis, with few scales. The
row (Fig. 10.110). The number of pecten teeth is 12, scutum has stout acrostichal and dorsocentral setae, and
and they are widely spaced towards the middle of the is covered with narrow uniform scales and bare areas in
284 10 Subfamily Culicinae

between. The pleurites are sparsely scaled, and the coxae

are without scales. The tarsi are dark scaled. Pale trans-
verse bands of the terga, if present, are located at the
apex of each tergum. The palps of the males are as long
as or longer than the proboscis, and the claws of the hind
legs have a subbasal tooth. The gonocoxite is covered
with more or less dense setae, but typical scales are
absent. The subapical lobe has spine-like or hair-like
setae, broad transparent scale-like setae are absent, and
the gonostylus is simple. The apex of the paraproct is
usually adorned with one row of large denticles. The
aedeagus is simple, formed by one pair of sclerites Fig. 10.111 Hypopygium of Cx. impudicus
connected by 1 or 2 transverse tergal bridges. The thorax
and abdomen of the larvae have minute spicules, visible
under high magnification (200×) only. The numerous is covered with greyish brown or blackish narrow scales.
comb scales are slender and elongated, and bordered The acrostichal and dorsocentral setae are brown, and
with thin spines. The siphon is long and ­slender, some- long blackish setae are situated at the margins of the
times slightly widening at the apex, the siphonal index is scutum and at its posterior part. The integument of the
usually more than 7.0, and the main tracheal trunks are pleurites is brown or ashy grey with patches of pale
narrow. The pecten teeth are slender, covering between scales on the antepronotum, propleuron, mesepisternum
1/5 and 1/3 the length of the siphon. The siphonal tufts and mesepimeron, and one lower mesepimeral seta is
are situated in an irregular row at the ventral surface of present. The coxae have patches of pale scales, and the
the siphon. femora are dark scaled on the dorsal surface, with pale
The subgenus Neoculex consists of < 30 species, scales ventrally, and an indistinct knee spot. The hind
mainly distributed in Africa and the Australian region. tibia is dark at the apex or with only a few pale scales,
Three distinct species are reported from the European and all the tarsi have dark scales. The wings are entirely
region. A remarkable fact is that no member of the sub- dark scaled. The terga are dark scaled with median nar-
genus Neoculex is known to take its blood meal from rowed or interrupted apical bands. The sterna are usu-
humans. In nature they were observed to feed exclu- ally pale scaled, occasionally two basal patches of dark
sively on frogs, small mammals and birds (Mohrig scales may be present on each side of some sterna.
1969). The egg laying behaviour seems to be typical Male: The palps are well covered with setae. The
for the subgenus (Mattingly 1970). The egg rafts are gonocoxite is prominently exposed (hence the specific
usually not laid directly upon the water surface, but name), compact in appearance, slightly longer than
above the water line. The hatching larvae reach the broad at its base and covered with numerous long and
water by wriggling down after emergence. conspicuous setae on its outer surface (Fig. 10.111).
The densely setose gonocoxite is unique for this spe-
cies and makes identification of males of Cx. impudi-
Culex (Neoculex) impudicus Ficalbi 1890 cus an easy matter. The subapical lobe is situated
beyond the middle of the gonocoxite with two long
Female: A small black mosquito, which differs from the pointed setae which are recurved at their apices, one of
similar Cx. territans by the apical pale bands on the which has a more or less sigmoid form. Additionally,
abdominal terga which are narrowed in the middle, the lobe bears several smaller, pointed and apically
sometimes interrupted and incomplete, forming triangu- recurved setae and numerous short, thin, straight setae.
lar lateral patches. The pale spot at the apex of the hind The gonostylus is constricted subapically, then extends
tibia, typical for Cx. hortensis, is weakly defined or into a “T”-shaped apical part, a feature unique among
completely absent. The proboscis is dark brown scaled. European Culex members. The apex of the paraproct is
The occiput has greyish brown setae, a row of white flat inwardly curved with a row of several mesally directed
scales around the eye margin, and a pair of long brown denticles and several spines. The aedeagus is made up
setae projecting forward between the eyes. The scutum of two simple plates connected by 2 transverse bridges
10.3 Genus Culex Linnaeus 285

Neoculex, the females of Cx. impudicus prefer to feed

on amphibians and are not known to feed on humans.
Distribution: Cx impudicus is mainly distributed in
the Mediterranean region. It is a common species in
southern and central Portugal (Ribeiro et al. 1988) and
reported from Spain, France, Italy, Corsica, Sardinia,
Sicily, and Greece. In northern Africa it can be found
in Algeria and Tunisia and it is recorded from Iran
(Knight and Stone 1977).

Culex (Neoculex) martinii Medschid 1930

Female: A small mosquito, which differs from the

other members of the subgenus Neoculex and those of
the subgenus Culex by the abdominal terga, which are
dorsally covered with uniform reddish brown scales,
and pale apical or basal transverse bands are absent.
Fig. 10.112 Larva of Cx. impudicus
The general abdominal colouration of Cx. martinii is
similar to Cx. modestus, but it is distinguished from the
at the base and close to the apex, with 3-4 small den- latter species by the longer hind tarsomere I and by the
ticles at their apices. wing venation. In Cx. modestus the subcosta (Sc) ends
Larva: The larvae are extremely difficult to disti- distinctly distal to the level of the cross vein (r-m),
guish from those of Cx. territans. Both species closely whereas in Cx. martinii Sc ends more or less at the
resemble each other in chaetotaxy and other character- level of r-m. The proboscis is dark scaled, slightly
istics. As indicated in the keys, Cx. impudicus usually swollen at the apex, the palps are very short with dark
has anal papillae blunt ended and about half as long as scales, and the clypeus is brownish. The vertex and
the saddle, subequal in length (Fig. 10.112). On the occiput have small brownish scales, with patches of
other hand, in Cx. territans larvae the anal papillae are broader pale scales at the sides. The integument of the
pointed, usually as long as the saddle, and the ventral
pair may be slightly shorter than the dorsal.
Unfortunately, the length of the papillae may vary
between specimens, and other distinct characteristics
to distinguish between the two species do not exist.
Biology: The larvae can be found in fresh and stag-
nant water, generally with considerable vegetation and
in well-shaded places (Aitken 1954a). They occur in
pools, small ponds, rock pools, ditches, marshes or
along the edges of streams. Occasionally, they are
found in rice fields (Rioux 1958). The larvae are often
associated with those of An. maculipennis s.l., An. clav-
iger, and Cs. annulata. In northern Africa, they fre-
quently occur together with larvae of An. algeriensis,
Cx. hortensis, Cx. p. pipiens, or Cs. longiareolata
(Sicart 1940; Senevet and Andarelli 1959). Hibernation
seems to take place in the adult stage. The larvae are
most abundant between May and August; the popula-
tion peak of the adults is usually reached in late sum-
mer. Like the other European members of the subgenus Fig. 10.113 Hypopygium of Cx. martinii
286 10 Subfamily Culicinae

scutum is yellowish, and covered with small, golden

brown scales and long brownish setae. The integument
of the pleurites is brownish-yellowish with dark setae.
The femora have brownish scales, slightly lighter on
the ventral surface, and a knee spot is absent. The tib-
iae and tarsi are entirely dark scaled, and the tarsi are
without pale rings. The wings have dark scales on all
veins. The abdominal terga are reddish brown, without
pale transverse bands, and the sterna are entirely
yellowish pale scaled.
Male: The palps are dark, and longer than the pro-
boscis by about the length of palpomere V, and not
swollen apically. The gonocoxite is short and stout
(Fig. 10.113), slightly more than twice as long as it is
wide, and the subapical lobe is situated well beyond
the middle of the gonocoxite, with 2 moderately long,
stout spines and a row of several stronger setae located
distal to the spines. The gonostylus is short and broad,
distinctly widened beyond the middle, with 2 small
setae situated close together at about 2/3 of its length.
The apical spine of the gonostylus is relatively long,
and blunt ended. The apex of the paraproct is widened
with a convex row of apical denticles and several small
setae inserted subapically. The aedeagus is divided Fig. 10.114 Larva of Cx. martinii
into two simple plates connected by apical and basal
transverse bridges.
Larva: The head is distinctly broader than long. (1-X) has 2 branches, the upper anal seta (2-X) has 4
The antenna is about 3/4 the length of the head, slightly branches, and the lower anal seta (3-X) is single. The
curved in the basal part and entirely covered with spic- ventral brush is composed of 11–12 tufts of cratal seta
ules. The antennal seta (1-A) has 22–26 branches. The (4-X), and the anal papillae are about half as long as
inner frontal seta (5-C) is 2-branched, the median fron- the saddle.
tals (6-C) are exceptionally long, reaching close to the Biology: Cx. martinii is not a very common species,
apex of the antenna, with 1–2 branches, and the outer thus the information about its biology is very limited.
frontal seta (7-C) has about 5 branches. The comb is In Germany, a considerable number of larvae were
composed of a patch of 35–40 elongated scales, each found once in a boggy alder forest in October (Mohrig
scale is apically rounded and fringed with thin spines. 1969). It is not known if this is the preferred breeding
The siphon is long and slender, evenly tapered towards site of the species or whether it breeds in a wide vari-
the apex, the siphonal index is 7.5–11.0, and the main ety of habitats. Nothing is known about the number of
tracheal trunks are narrow (Fig. 10.114). The pecten generations per year in Europe, the hibernation prin-
has 11–16 teeth occupying the basal 1/5 of the siphon, ciples, the time of appearance of the adults, their period
and each pecten tooth has 3–4 short lateral denticles. of main flight activity or host-seeking behaviour. It
4–6 pairs of siphonal tufts (1-S) are situated in an seems likely that the species does not feed on humans
irregular row at the ventral surface of the siphon, 1–2 but prefers to bite amphibians and/or birds, like the
apical tufts are laterally displaced, and usually the other European members of the subgenus Neoculex.
basalmost tuft (1a-S) is inserted beyond the last pecten Distribution: Cx. martinii is mainly distributed in
tooth. Each tuft has 2–5 branches, slightly longer than the eastern Mediterranean region, Asia Minor, and
the width of the siphon at the point of insertion, and the middle Asia. It is reported from Italy, former
apical tufts are shorter. The anal segment is elongated, Yugoslavia, Croatia, Hungary, Turkey, Germany, and
and entirely surrounded by the saddle. The saddle seta in northern Africa from Morocco.
10.3 Genus Culex Linnaeus 287

Culex (Neoculex) territans Walker 1856 remaining terga are dark brown scaled with evenly
narrow apical bands of pale scales usually joining a
Female: The proboscis and palps are dark scaled, and small pale triangular patch on each side. Tergum VIII
the proboscis is slightly swollen at the apex. The is almost entirely dark. The sterna have pale scales
clypeus and pedicel are dark brown, the first flagellom- often with a greenish tinge.
ere is slightly swollen, and the flagellum is dark brown Male: The last two palpomeres have long setae.
with black setae. The occiput has narrow curved pale The subapical lobe of the gonocoxite has 2 basalmost
to golden scales and brown erect forked scales, and setae which are long and broad, flattened, slightly sin-
broad whitish scales laterally. The integument of the uous and with recurved apices (Fig. 10.115). A few
scutum is usually light brown, sometimes darker, and other setae are located distally, similar in appearance,
covered with narrow light brown scales, paler scales but smaller, and additionally 1 or 2 long and hair-like
on the anterior and lateral margins of the scutum and setae are present. The gonostylus usually tapers evenly
the prescutellar space. Dark setae at the margin of the from the base towards the apex. The apical spine of the
scutum are relatively long. The scutellum is brown gonostylus is somewhat expanded at the tip. The para-
with greyish narrow scales and long black setae. The proct is without ventral arms, and the paraproct crown
antepronotum is densely covered with pale scales. The has an inwardly curved row of denticles. The aedeagus
pleurites are dark brown or greyish with patches of consists of two simple plates which are connected by
broad whitish scales. The femora are dark scaled on transverse bridges at the base and close to the apex;
the anterior surface, and pale posteriorly, with small the plates are ornamented with small denticles at their
pale knee spots. The tibiae are dark anteriorly and pale apices.
on the ventral surface, and the apex of the hind tibia is Larva: The head is distinctly broader than long,
without a pale spot. The tarsi are entirely dark scaled, the antennae are about as long as the head, inwardly
although a pale stripe may be present on tarsomere I. curved, densely covered with spicules from the base
The wings are entirely covered with narrow dark to the insertion point of the antennal seta (1-A), and
scales, and the cross veins are well separated. The end distinctly narrowed from the insertion point to the
of Sc is distinctly displaced towards the wing base
compared to the furcations of R2+3 and M (Fig. 6.56b).
Tergum I has a median patch of pale scales, and the

Fig. 10.115 Hypopygium of Cx. territans Fig. 10.116 Larva of Cx. territans
288 10 Subfamily Culicinae

apex. Seta 1-A has 25–32 branches, and is situated at ulation maximum is reached in late summer. The
about 2/3 the length of the antennal shaft. The frontal females are not known to bite humans, but predom-
setae are long, the inner (5-C) usually has 2 branches, inantly feed on amphibians, especially Rana sp.,
the median (6-C) is usually single and situated nearly reptiles and birds.
in front of the inner setae, and the outer frontal seta Distribution: Cx. territans is widely distributed
(7-C) has 8–9 branches. The comb has 50 or more, throughout Europe. Its range stretches into central Asia
apically rounded scales which are completely fringed and northern Africa. In the Nearctic region it is found
(Fig. 8.70b). The siphon is long and slender, with a in Canada and the United States including Alaska.
siphonal index of 6.0–7.0, tapering to near the apex, Note on systematics: Cx. territans was formerly
where it slightly but distinctly expands, and the main synonymized with Cx. apicalis Adams, which was
tracheal trunks are narrow (Fig. 10.116). The pecten originally described from Arizona, United States.
has 12–16 teeth occupying the basal ¼ to 1/3 of the After a revision of the subgenus Neoculex in the
siphon, each pecten tooth with 1 or 2 rather stout lat- United States, Bohart (1948) gave evidence that
eral denticles on their ventral margin. Seta 1-S con- they are two distinct species with a distribution of
sists of 4–6 pairs of tufts, usually commencing at the Cx. apicalis in the southern parts of the United
point where the pecten ends, and rarely the basalmost States and that of Cx. territans in the northern states
tuft may arise slightly within the pecten. Each tuft and Alaska. The European species were first identi-
has 2–4 branches of variable length, usually twice as fied as Cx. apicalis, but it was shown by Mattingly
long as the width of the siphon at the point of its ori- (1953) and others that they were identical with Cx.
gin. The distalmost tuft is shorter and arises slightly territans. Thus, all European records in the litera-
out of line laterally. The saddle completely encircles ture of Cx. apicalis prior to 1950 actually referred to
the anal segment and is spiculate on the dorso-apical Cx. territans.
part, the saddle seta (1-X) is usually 2-branched, the
upper anal seta (2-X) has about 4 branches, and the
lower anal seta (3-X) is very long and is single. The
ventral brush has about 7 pairs of multiple-branched 10.4 Genus Culiseta Felt
cratal setae (4-X). The anal papillae are pointed, and
are usually as long as the saddle, the ventral pair may The genus was formerly known under the name
be slightly shorter than the dorsal pair. Theobaldia Neveu-Lemaire 1902 but later on it was
Biology: In the northern regions, Cx. territans realized that this name was already being used by a
has probably only one generation per year, but in genus of molluscs since 1885. According to the rules
the southern parts of its distribution range, it is of nomenclature the name Theobaldia was conse-
polycyclic, as is typical for other Culex species. quently replaced by the name Culiseta Felt.
Preferred larval habitats are permanent bodies of The genus embraces mainly medium-sized to
water such as ponds, swamps, pools along streams, large, dark mosquitoes. The females have a straight
edges of lakes, or drainage channels with a slow proboscis and short palps. Prespiracular setae are
water-flow, often associated with dense vegetation. present, usually of pale colour, but postspiracular
The larvae prefer cooler water in shaded situations setae are absent. The prealar area has setae, but is
(Mohrig 1969) and are often found together with usually found without scales. The base of the radius
those of An. maculipennis s.l. and An. claviger. (R) has a few setae which are more numerous on the
Gutsevich et al. (1974) reported about larval habi- ventral surface of the wing. The abdomen is blunt
tats being in strong sunshine in temperate latitudes ended, the cerci are short and rounded apically, the
and completely shaded in southern regions. The lar- claws are simple, without a subbasal tooth, and pul-
vae are rarely found in heavily polluted water. In villi are absent. In males the length of the palps may
the Nearctic they also occur in artificial containers vary in individuals of the different subgenera. The
and other small bodies of water (Wood et al. 1979). gonocoxite is rather long, a basal lobe is present, but
Adult females reappear from hibernation in early an apical lobe may be present or absent. The gonosty-
spring and the first larvae can be found from the lus is simple, the apical spine is not longer than its
end of April or early May, until September, the pop- maximum width (except in Cs. glaphyroptera), and
10.4 Genus Culiseta Felt 289

claspettes are absent. The larvae are large to very shaped rafts on the water surface, similar to the species
large with the head being wider than long. The comb of the genus Culex.
scales are numerous and blunt ended, and the sipho- The subgenus Allotheobaldia is represented by only
nal tuft (1-S) is always present, inserted near the base one species, Cs. longiareolata, which is distributed in
of the siphon, and the pecten is present. The anal seg- the southern Palaearctic region.
ment is completely surrounded by the saddle (except
in Cs. longiareolata), which is pierced by one or
more tufts of precratal setae (4-X).  uliseta (Allotheobaldia) longiareolata
C
The larvae of the genus are generally found in semi- (Macquart 1838)
permanent and permanent pools, rarely in other loca-
tions. As regards the feeding behaviour of the adult Female: Cs. longiareolata can easily be distinguished
females, some species are known to feed exclusively from all other European species of the genus Culiseta
on birds, but others, especially those of the subgenus by its distinct longitudinal pale stripes on the scutum,
Culiseta, readily attack humans and other mammals which resemble a lyre in shape and the femora and
and are known to be severe biters. tibiae with pale scales aggregated into conspicuous
The distribution of the genus Culiseta is almost spots or stripes. The proboscis is blackish brown, the
world wide, but largely confined to the more temperate palps are dark brown with pale scales, the latter
zones of the Holarctic region. It is a relatively small ­predominating on the dorsal part. The tips of the palps
genus including approximately 40 valid species and are almost entirely pale. The antennae are blackish
subspecies, which are spread over seven subgenera. brown, and the pedicel and first two flagellomeres have
Throughout the European region, 10 species of three white scales. The head has dense white scaling along
subgenera, Allotheobaldia, Culicella, and Culiseta, are the margins of the eyes, broad white scales also in the
recorded. median line of the vertex and on the lateral parts of the
In the European members of the genus Culiseta, occiput. The scutum has light brown, narrow scales.
both adult and larval morphological characteristics A narrow acrostichal stripe of pale scales extends from
can be found to distinguish the three subgenera. Such the anterior margin to the scutellum. In addition, there
an extent of congruity in larval and adult subgeneric are narrow dorsocentral and lateral stripes, which are
characteristics cannot be found in any other European connected over the transverse suture. The scutellum
genus of the Culicidae. Furthermore, the subgenera and pleurae have patches of white scales except on the
Culiseta and Culicella exhibit striking differences upper part of the postpronotum, where the scales are of
regarding their larval and adult behaviour, which will a creamy yellowish colour. The legs are blackish brown
be described in more detail in the subgeneric with pale spots and longitudinal stripes on the femora,
sections. tibiae and tarsomeres I. All the tarsi have pale basal
bands on tarsomeres I–III, and tarsomere V is usually
entirely dark. The wing veins are covered with dark
scales except the costa (C), which is covered with pale
 ubgenus Allotheobaldia
10.4.1 S
scales along its entire anterior surface. Dark scales are
Broelemann aggregated at the base of RS, cross veins (r-m and
m-cu) and the furcations of M and Cu giving an appear-
The females have a conspicuous colouration pattern on ance of spots. The cross veins are well separated. The
the scutum, and the palps of the males are shorter than scales of the terga vary in colour, but usually form broad
the proboscis, and distinctly swollen at the apex. The white basal bands. A mixture of yellowish creamy and
gonocoxite is without an apical lobe, and tergum IX brown scales is more frequently found on the last terga.
has two prominent lateral lobes. The head of the larva Tergum VIII is usually entirely white scaled.
is small with mouthparts adapted to feed on the sub- Male (Fig. 10.117): The main characteristic that
strate. The antennae are short, with a weakly devel- distiguishes Cs. longiareolata from all other European
oped antennal seta (1-A). The siphon is short and not members of Culiseta is the conspicuous tergum IX,
sclerotized at the base, and the saddle is weakly developed which is expanded laterally into two long and slender,
and plate shaped. The females deposit the eggs in boat- sclerotized lobes bearing tiny spine-like setae at their
290 10 Subfamily Culicinae

outer frontal setae (7-C) with 3–4 branches

(Fig. 8.79a). The number of comb scales shows great
variation (40–75), and seta 3-VIII is strongly devel-
oped with multiple branches (Fig. 10.118). The
siphon is more or less conical in shape, with an index
between 1.5 and 2.0. The pecten has 7–13 short teeth
arranged in an irregular row and occupying up to 80%
of the length of the siphon. The basalmost teeth are
smaller and inserted in the unsclerotized basal part of
the siphon. The siphonal tuft (1-S) is shorter than seta
3-VIII, with 10–15 branches arising close to the mar-
gin of the sclerotized part of the siphon. The anal seg-
ment has a plate shaped saddle extending along about
half of its lateral sides. The saddle has dense short
spines at its posterior margin, the saddle seta (1-X) is
short, not more than half the length of the saddle. The
length of the anal papillae varies according to the
salinity of the breeding water, but is 0.5–1.5 times as
long as the anal segment.
Fig. 10.117 Hypopygium of Cs. longiareolata
Biology: The larvae can be found in rock holes and
in any kind of artificial container, e.g. wooden and
metal barrels, or tanks built of concrete, and wells.
Rarely do they occur in natural water bodies like pools,
ditches, and drain canals. The larvae are able to toler-
ate a slight salinity and a high degree of pollution and
are often likely to be found together with those of Cx.
p. pipiens and Cx. mimeticus. At temperatures of
20–25°C the larval development lasts about 20–22
days. The larvae spend most of their time at the surface
of the breeding site and rarely descend to the bottom.
The pupae of Cs. longiareolata are able to lie passively
on the bottom of their breeding sites for a length of
time (Peus 1954). Hibernation takes place in the larval
stage. In the temperate climatic zones adults can be
found from February to November. The females of Cs.
longiareolata do not enter dwellings and rarely bite
humans outside but are regarded as vectors of blood
parasites in birds. In populations from Turkmenia,
Fig. 10.118 Larva of Cs. longiareolata autogenous egg deposition has been observed (Rioux
et al. 1975).
Distribution: In Europe, Cs. longiareolata is
apices (Fig. 7.69a). The gonostylus is broadened api- widely distributed in the Mediterranean region from
cally, bluntly ending with two short, pointed subapical Spain and Portugal in the west to the European part of
spines. The aedeagus is thick and strongly sclerotized. Turkey in the east, in France as far north as Paris, and
Larva: The antennae are short, and the antennal in Switzerland and southern England. It has also been
seta (1-A) is articulated in the apical third of the recorded from the Canary Islands, Madeira, and the
antenna, is short and usually 2-branched, rarely with Azores. This species can be found in southern Ukraine
1 or 3 branches. The head has single inner and median and the lower Volga area as far as the northern slopes
frontal setae (5-C and 6-C), rarely 2-branched, and of Caucasus. Outside Europe the distribution stretches
10.4 Genus Culiseta Felt 291

from middle and southwest Asia, to India and Pakistan eres. It closely resembles Cs. litorea and Cs. morsi-
and middle Africa. tans but differs from the latter in having a mainly dark
proboscis with pale scales laterally and ventrally in its
middle third and the dark scales on most of the
abdominal sterna are usually aggregated to form an
10.4.2 Subgenus Culicella Felt inverted “V” (Fig. 6.58a,b). In Cs. morsitans the pro-
boscis is usually entirely dark scaled and the dark and
The wings are usually without spots, except in Cs. pale scales on the abdominal sterna are intermixed.
ochroptera which may have an indistinct dark spot at However, these two characteristics show some varia-
the base of R4+5.The cross veins (r-m and m-cu) are tion, e.g. the proboscis of Cs. morsitans with a few
well separated, the distance between them being at scattered pale scales or sometimes the abdominal
least the length of m-cu (Fig. 6.57a). The indistinct tar- scale colouration patterns of Cs. fumipennis are very
sal pale ringing shows the tendency to include both the indistinct. The most reliable diagnostic characteristics
basal and apical parts of the tarsomeres. The palps of are the narrow pale basal rings on all tarsomeres of the
the males are as long as or longer than the proboscis, the hind legs of Cs. fumipennis. In Cs. morsitans tarso­
gonocoxite is without an apical lobe, and the aedeagus meres IV and V of the hind legs are entirely dark. There
is weakly sclerotized. The antennae of the larvae are are no other distinct characteristics to distinguish
longer than the head, with antennal seta (1-A) arising females of these two species. The differences between
from a point near to the apex, well developed and Cs. fumipennis and Cs. litorea may be found on the
multiple branched in the form of a broad fan. The fore legs. In Cs. fumipennis the pale rings include the
mouthparts are adapted for suspension feeding. The apical and basal parts between tarsomeres III–IV and
siphon is long and slender, with an index of > 5.0. The IV–V (Fig. 6.59a), and in Cs. litorea the apical parts
pecten consists of a few small inconspicuous teeth at of tarsomeres III and IV are entirely dark scaled
the base of the siphon, except for Cs. fumipennis, which (Fig. 6.59b).
has in addition to the pecten teeth several stout, spine-
like setae on the ventrolateral surface of the siphon.
The external morphology of the larvae is adapted to
their behaviour as suspension feeders. Usually they are
found breathing at the water surface, but they can
spend hours submerged. They are sometimes attached
to active respiratory parts of plants from which they
may take air bubbles. Others lie on the ground of the
breeding sites with their backs towards the bottom, pro-
ducing a flow of water with their mouthparts and filter-
ing microorganisms. The species of the subgenus
hibernate in the larval or egg stage. The eggs are depos-
ited singly on the ground above the residual water
level, as species of the genera Aedes and Ochlerotatus
usually do. In the European region the subgenus
Culicella consists of four species.

Culiseta (Culicella) fumipennis (Stephens 1825)

Female: Cs. fumipennis is a large mosquito with a

dark brown scutum and unspotted wings. The abdo­
minal terga are dark brown scaled with basal, yellowish
white bands of uniform width. The legs are largely
dark with narrow pale rings at the bases of the tarsom- Fig. 10.119 Hypopygium of Cs. fumipennis
292 10 Subfamily Culicinae

Male (Fig. 10.119): The gonocoxite is slender and antennal seta (1-A) is large and multiple-branched.
conical. The basal lobe has 3–4 strong setae. The aedea- The inner (5-C) frontal seta is 2–4 branched, the
gus is weakly sclerotized, with lateral sclerites converg- median (6-C) is 2-branched and the outer (7-C) has
ing apically. The male genitalia of Cs. fumipennis and 5–6 branches. The comb consists of 120–160 long and
Cs. morsitans can be separated with certainty only when slender scales fringed with small, fine spines. Seta
directly compared to each other. In Cs. fumipennis the 3-VIII has 4–6 long branches. The siphonal tuft (1-S)
gonostylus is much slender and abruptly constricted consists of 4–5 branches and is distinctly longer than
shortly beyond the base, the ratio of its median width to half of the siphon. A pair of conspicuous long, multi-
its entire length is about 1:16. In Cs. morsitans the gono- ple-branched tufts is situated dorsally near the tip of
stylus is stout, and more gradually tapered towards the the siphon. Seta 9-S on the posterolateral valves is
apex and the ratio of the median width to the entire strongly developed, and hook shaped. The anal seg-
length is about 1:12. The median lobe of tergum VIII ment is long, completely surrounded by the saddle
bears up to 3 stout spine-like setae in Cs. fumipennis, with 6 tufts of precratal setae (4-X) piercing through it,
and 3–7 strongly sclerotized longer setae in Cs. morsi- and the saddle seta (1-X) is single. The anal papillae
tans. These two characteristics combined should enable are lanceolate, and about half as long as the saddle.
one to distinguish between the two species with a cer- Biology: In Sardinia, larval catches were recorded
tain confidence. from January through April (Marchi and Munstermann
Larva: In the larval stage Cs. fumipennis is easy to 1987), but in the central and more northern parts of
distinguish from all other European members of the Europe, the larvae of Cs. fumipennis first occur in
subgenus Culicella by its siphon (Fig. 10.120). It bears, spring during the months of April and May. The pre-
in addition to the pecten teeth, large isolated spine-like ferred breeding sites are open, unshaded water bodies
setae irregularly scattered on its ventrolateral surface. such as shallow temporary pools with rich vegetation
The most distal one extends well beyond the middle of or covered with duckweed (Lemna sp.). The larvae
the siphon. The antennae are longer than the head, the also occur among the grassy margins of permanent
ponds or swamps. They are often associated with lar-
vae of Cs. morsitans, Cx. territans and Cx. hortensis,
occasionally with those of An. claviger. They feed on
microorganisms and spend most of their time sub-
merged. Very rarely the larvae can be found in water
with a high salinity (Martini 1931). Little is known
about the feeding habits of the adult females. They
were never observed to enter any kind of dwellings or
bite humans and domestic animals. It is likely that they
do not feed on mammals, but take their blood meals
from birds or reptiles, like Cs. morsitans. Although
adult females were captured in the middle of the year,
in July and August, it is not known if Cs. fumipennis
has more than one generation per year.
Distribution: Cs. fumipennis is a Holarctic species,
widely distributed throughout the whole of Europe,
from southern Scandinavia to the east Baltic and south-
wards to the Ukraine and northern Caucasus. It is
recorded from nearly every country in central and
southern Europe and occurs around the Mediterranean
basin to northern Africa.
Notes on systematics: Cs. setivalva was formerly
regarded as a valid species (Knight and Stone 1977)
but was put under synonymy of Cs. fumipennis
Fig. 10.120 Larva of Cs. fumipennis (Danilov 1984; Ward 1992).
10.4 Genus Culiseta Felt 293

Culiseta (Culicella) litorea (Shute 1928)

Female: Cs. litorea was first described as a variety of

Cs. morsitans (Shute 1928), but subsequently raised to
a specific rank, mainly because of striking differences
in the male hypopygium (Marshall and Staley 1933).
The females, like those of Cs. fumipennis, have largely
pale scaled sterna with a pattern of dark scales forming
an inverted “V”, but the pattern is not always visible,
especially in pinned specimens. In this case Cs. litorea
might be easily confused with Cs. morsitans. The sep-
aration between Cs. litorea and Cs. fumipennis is far
more difficult. According to Marshall (1938) the pale
rings on the last two tarsal joints of the fore and mid
legs are less distinct in Cs. litorea than in Cs. fumipen-
nis, and on the hind legs of Cs. litorea the rings are
either inconspicuous or absent. Because none of these
differences are absolute, it might be impossible to
identify Cs. litorea females with certainty, especially if
the determination is based on a single or a few
specimens. Fig. 10.121 Hypopygium of Cs. litorea
Male: The male genitalia are very distinctive and
the only reliable means to distinguish Cs. litorea from
its close relatives. The gonocoxite is more or less twice
as long as it is wide, parallel sided and blunt ended
(Fig. 10.121). The basal lobe is elongated and bears 2
stout setae, one of which reaches as far as or beyond
the apex of the gonocoxite. In Cs. fumipennis and Cs.
morsitans the gonocoxite is more slender and conical,
tapering towards the apex and none of the conspicuous
stout setae of the basal lobe reaches the apex of the
gonocoxite. Furthermore, the male palps of Cs. litorea
are usually shorter than the palps of the two other spe-
cies. Marshall and Staley (1933) found the ratio of the
length of the palps to the length of the proboscis to be
about 1.14–1.22 in Cs. litorea and about 1.33–1.40 in
Cs. morsitans, but Service (1970b) reported an overlap
of this character in the two species, which is therefore
not always reliable for a positive identification.
Marshall (1938) mentioned a further diagnostic char-
acter. The base of the gonostylus appears to be dis-
tinctly more bulbous in Cs. litorea than in the two other
species. Fig. 10.122 Larva of Cs. litorea
Larva (Fig. 10.122): The larvae of Cs. litorea are
readily distinguished from those of Cs. fumipennis by
having no isolated spine-like setae in addition to the
pecten teeth, but the separation from Cs. morsitans is can be found in the length of the siphonal tuft (1-S)
less reliable. The only characteristic which might allow compared to the length of the siphon. In British popu-
identification of fourth-instar larvae of the two species lations Marshall (1938) found in Cs. morsitans the
294 10 Subfamily Culicinae

length of 1-S usually less than, and in Cs. litorea more length of the proboscis, and are mainly dark scaled
than, 0.4 times the length of the siphon. However, with a few pale scales at the tip. The pedicel is brown,
Aitken (1954a) found larvae of Cs. litorea from and the flagellum of the antennae is blackish brown
Sardinia with the length of 1-S being less than 0.4 with black setae. The vertex has long dark setae, and
times the length of the siphon, and Rioux (1958) was the occiput has narrow yellowish-white scales and
unable to distinguish larvae of the two species from dark erect forked scales dorsally and broad yellow-
the Mediterranean area by this characteristic. There is ish-white scales laterally. The integument of the
a considerable overlap in the above mentioned ratios scutum is dark brown, with narrow brown and yel-
between the two species, which invalidates reliable lowish-golden scales. There is golden scaling mainly
larval identification (Service 1970b). on the acrostichal and dorsocentral stripes, on either
Biology: The biology of Cs. litorea closely resem- side of the prescutellar area, on the anterior part of
bles that of Cs. morsitans in many aspects. Larval the supraalar area and on the anterior submedian area.
habitats are pools, small ponds or ditches, but unlike The scutellum is dark brown with patches of narrow
Cs. morsitans, which can commonly be found in both yellowish-white scales and long dark setae on the
open (sunlit) and densely shaded situations, the larvae lobes. The mesepisternum, mesepimeron and lower
of Cs. litorea are always restricted to habitats of the part of the postpronotum have small patches of whit-
first type. It is mainly a coastal species that can tolerate ish scales. The prespiracular setae are yellowish,
slightly brackish water, but larvae are not restricted to numerous, but postspiracular setae are absent. The
salt water habitats, where they can often be found femora and tibiae are dark brown, with pale scales at
together with those of Oc. detritus. Frequently they the ventral surface. Pale knee spots are well devel-
can be found in semipermanent fresh water habitats or oped, and all tibiae have pale rings at their apices.
channels with a rich growth of vertical vegetation The tarsi are dark with faint pale rings involving both
(Rioux 1958). Aitken (1954a) found larvae in a large ends of the joints. Rings at the joints of tarsomeres
coastal fresh water marshes, containing abundant III–IV and IV–V are inconspicuous or absent on the
growth of cattails (Typha sp.). Cs. litorea feeds princi- fore and mid legs and always absent on the hind legs.
pally on avian blood, occasionally a few females were
found to bite reptiles or mammals, including humans
(Cranston et al. 1987). Hibernation takes place in the
larval stage and they are able, like Cs. morsitans, to
survive under a cover of ice during the winter months
(Rioux 1958).
Distribution: Cs. litorea is known from Ireland,
England, France, Spain, and Italy (Sardinia) in Europe
and from Algeria. It has a more restricted distribution
than Cs. morsitans.

Culiseta (Culicella) morsitans (Theobald 1901)

Female: The general appearance of Cs. morsitans is

in many respects very similar to Cs. litorea and Cs.
fumipennis in all stages. The few characteristics
which might facilitate distinction between the three
relatives are given in the descriptions of the two latter
species. Cs. morsitans is a rather large species. The
proboscis is uniformly dark scaled, occasionally with
a few pale scales in its middle third, and slightly
swollen in its apical part (Fig. 6.58c). The clypeus is
dark brown, the palps are about one quarter of the Fig. 10.123 Hypopygium of Cs. morsitans
10.4 Genus Culiseta Felt 295

The wing veins are entirely dark scaled, without description of the latter. The head is exceptionally
spots, and the scales are narrow and dark brown. The large in relation to the body, and > 1.5 times wider
cross veins r-m and m-cu are widely separated and than long. The antennae are as long as or slightly lon-
without scales. The terga are dark brown with narrow ger than the head, spiculate, and curved with a darkly
yellowish white basal bands. The sterna are mainly pigmented, tapering apex. The antennal seta (1-A) is
covered with pale scales, less numerous dark scales large, forming a fan-like tuft with 18–25 branches,
are irregularly scattered, not forming any pattern inserted at the upper third or quarter of the antennal
(Fig. 6.58d). shaft and reaching well beyond its tip. The postcly-
Male (Fig. 10.123): The hypopygium is very similar peal seta (4-C) is small and single, and situated ante-
to that of Cs. fumipennis; for differential characteristics riorly to the frontal setae. The inner (5-C) and median
see the description of the latter. The posterior margin of (6-C) frontal setae have 2-3 branches, 6-C is very
tergum VIII has a broadly rounded lobe bearing a group long (Fig. 8.85c). The outer frontal seta (7-C) has 6–8
of 3–7 stout, spine-like setae. The lobe of tergum IX is branches. The prothoracic setae (1-P to 7-P) are very
slightly elevated with long hair-like setae (Fig. 7.69c). long, usually with 1–2 branches. The lateral abdomi-
The gonocoxite is conical, about 2.5 times as long as it nal setae on segments I and II (6-I and 6-II) have 3–4
is wide at its base, tapering apically, and the basal lobe branches, those on segments III–VI (6-III to 6-VI)
of the gonocoxite is well developed with 2–4 conspicu- are single. The comb consists of > 90 scales closely
ously stout setae. The gonostylus is slightly bulbous at arranged in a large triangular patch (Fig. 10.124).
the base, gradually tapering towards the apex. The api- The individual scales are long and narrow in the mid-
cal spine of the gonostylus is short and stout. The para- dle, slightly widened at the base, with the apical part
procts are strongly sclerotized, with 2, rarely 3 apical rounded and fringed with small spines laterally and
teeth. The aedeagus is weakly sclerotized and pointed apically. The siphon is straight, long and slender, and
at the apex. slightly tapered towards the apex. The siphonal index
Larva: Very similar to Cs. litorea; to distinguish ranges from 5.0 to 7.0, and the pecten consists of
between the two species in the larval stage see the 6–11 teeth which are confined to the basal fifth or
quarter of the siphon. The smaller basal teeth usually
arise from the membrane proximal to the siphon, and
the distal teeth are detached. The siphonal tuft (1-S)
has 4–5 branches, and is distinctly longer than the
basal width of the siphon. The anal segment is long
and narrow, and completely ringed by the saddle. The
saddle seta (1-X) is single, and slightly shorter than
the saddle. The ventral brush consists of 12–15 cratal
setae (4-X) and 5–6 precratal setae which pierce the
saddle. The anal papillae are variable in length, lan-
ceolate, and the dorsal pair might be slightly shorter
than the ventral pair.
Biology: Cs. morsitans is a monocyclic species.
The eggs are deposited during early summer in the
moist substrate above the residual water level.
Hatching occurs in autumn when heavy rainfall leads
to a rise of the water level in the breeding site.
Usually the larvae grow to the second or third-instar
in the same year. Depending on the weather condi-
tions, fourth-instar larvae can sometimes be found
prior to November, but pupation never occurs until
the next spring (Marshall 1938). During wintertime
the larval development is postponed. The larvae
Fig. 10.124 Larva of Cs. morsitans often descend to the bottom of the breeding site,
296 10 Subfamily Culicinae

where they lie in an inverted position with their head Culiseta (Culicella) ochroptera (Peus 1935)
setae and tip of the siphon in contact with the ground.
They are able to survive for considerable periods Female: Females of Cs. ochroptera may be confused
under a cover of ice, but complete freezing of the with Cs. morsitans at first glance, but they are usually
breeding site leads to a high mortality. Although smaller in size and more slender than the latter. The
hibernation usually takes places in the larval stage, most striking differences are the generally more brown-
newly hatched first-instar larvae can be observed in ish colouration of Cs. ochroptera (general colouration
early spring. This is in accordance with the situation of Cs. morsitans more greyish) and the tibiae of the
in the Nearctic region, where Cs. morsitans overwin- fore legs which are predominantly yellowish scaled,
ters in the egg stage in most of Canada and first- whereas the fore tibiae of Cs. morsitans are mainly
instars appear from April on (Wood et al. 1979). In dark scaled. The proboscis of Cs. ochroptera is usually
Europe, the larvae can be found from autumn to densely covered with pale scales, with a dark apex.
spring/early summer in a variety of breeding sites, The palps are dark brown, sometimes with pale scales
including pools, small ponds or ditches and even in at the apices of palpomeres III and IV. The antennae
slowly flowing waters. They occur predominantly in are dark brown, and the base of flagellomere I is whit-
swampy woodlands and temporary water bodies in ish-yellow. The head has narrow pale scales and broad
forests or at their edges in both, open and shaded erect black scales. Along the margin of the eyes there
situations. They are able to tolerate a considerable are long, curved, dark setae. The anterior part of the
amount of salinity and also develop in slightly brack- scutum is uniformly golden brown or rusty brown
ish water. In springtime the larvae can often be found without pale scales. The supraalar and prescutellar
together with those of Oc. rusticus and first-instars areas have narrow, whitish brass coloured scales,
of Oc. punctor and Oc. communis, and later in the which usually form indistinct, narrow, longitudinal
year they occur together with larvae of An. claviger. stripes from the middle of the scutum. The scu­te­llum
In Britain they have been found with larvae of Cs. is brown with patches of whitish brass coloured scales
fumipennis and Cs. litorea (Cranston et al. 1987). on the lobes. The posterior margin of the scute­llum has
The adults emerge from April on and can be observed dark, slightly curved setae. The postnotum is ochre
until October. The females take their blood meal brown coloured. The postpronotum has uniformly
mainly from birds and occasionally from reptiles and brown scales. The femora are dark on the anterior sur-
small mammals. It is assumed that in central Europe face, and pale yellow on the posterior surface with a
the females attack humans very rarely, if ever, but white patch of scales at their apices. The tibiae of the
Horsfall (1955) reported that Cs. morsitans was a fore legs are pale yellowish scaled except for a narrow
serious pest in eastern Europe and in the former longitudinal dark stripe on the anterior surface. The
USSR. The daytime resting sites of the adults are tibiae of the mid and hind legs are pale on the anterior
hollows of trees and uninhabited buildings or cellars, and posterior surface and dark on the ventral and dor-
but they are rarely found in leafy shrubbery or in sal surface. The tarsi of the mid and hind legs have
grassy vegetation (Service 1971b). narrow pale basal rings on tarsomeres I–III and some-
Distribution: Cs. morsitans is widely distributed times a few pale scales at their apices, and tarsomeres
throughout the Palaearctic region. It is very common IV and V are entirely dark. The pale rings are often
in almost every European country and its range indistinct. The costa (C) has a varying number of pale
stretches from southern Scandinavia into northern or ochre coloured scales along the entire anterior mar-
Africa and from the Northern Sea and Atlantic Ocean gin, but other scales on the wing veins are dark. At the
eastwards to west Siberia and southwest Asia. The base of R4+5 the dark scales may be aggregated to form
form dyary (Coquillett) that was formerly regarded as a small but distinct dark spot. The colouration of the
a distinct species, but recently put under synonymy of abdominal terga may be variable. Typically the terga
morsitans (Wood et al. 1979; Ward 1984), can be found are brown scaled with yellowish scales forming indis-
in the Nearctic region. tinct narrow basal and apical bands, and tergum VIII is
Medical importance: Cs. morsitans was found to completely pale scaled. Sometimes the apical bands or
be a carrier of Ockelbo virus in Sweden (Francy et al. both the apical and basal bands are absent, and isolated
1989). pale scales are scattered at the bases of the terga. The
10.4 Genus Culiseta Felt 297

Male: The median lobe of tergum VIII has 6–8

strong setae arranged in an irregular row, and the
lobes of tergum IX usually have 7–10 slightly curved
setae. The gonocoxite is elongated, and is at least
2.5 times as long as it is wide at its base (Fig. 10.125).
The basal lobe of the gonocoxite has 5–8 strong
setae, which are slightly inwardly curved. The
paraproct is strongly sclerotized, with 1–2 teeth at
the apex. The aedeagus is more or less oval, and
weakly sclerotized.
Larva: The larvae of Cs. ochroptera resemble
superficially those of Cs. morsitans, but they are read-
ily distinguishable from the latter by having the inner
frontal seta (5-C) with 5–9 branches (Fig. 8.85a) and
the comb scales at the posterior margin of the comb
with strongly sclerotized longitudinal mid ridges
(Fig. 10.126). In Cs. morsitans the inner frontal seta
is 2–3 branched and the comb scales lack sclerotized
mid-ridges. Cs. ochroptera has an antenna which is
slightly longer than the head, dark pigmented at the
base and in the tapering apical part. The postclypeal
Fig. 10.125 Hypopygium of Cs. ochroptera seta (4-C) has 2–4 small branches, the median frontal
seta (6-C) is always 2 branched, and the outer frontal
seta (7-C) has 7–13 branches. The comb consits of
60–95 scales of different shape, some with a dark
longitudinal mid ridge. The siphonal index is 5.0–7.0,
and the siphon slightly tapers apically. The pecten
has 7–10 teeth, the 2–3 distal teeth are single spines
without lateral denticles on the ventral margin and
more widely spaced. The siphonal tuft (1-S) has 5–10
branches. The anal segment is longer than broad, and
the saddle completely surrounds the segment. The
upper anal seta (2-X) has 12–23 branches, and the
lower anal setae (3-X) is 2–3 branched. The ventral
brush has 10–22 tufts of cratal setae (4-X) and 5–8,
usually 6, precratal setae. Often only 1 precratal seta
is not situated on the saddle. The anal papillae are
narrow and lanceolate, and 1.5–2.0 times longer than
the saddle.
Biology: Cs. ochroptera is a very rare mosquito and
therefore the knowledge about its biology is scanty. In
central and eastern Europe the larvae can be found in
peat bogs, where they sometimes appear associated
with larvae of Cs. alaskaensis. In the east of their dis-
Fig. 10.126 Larva of Cs. ochroptera and enlarged comb scales
tribution range they can also occur in large shallow
marshes, in forest ponds, and ditches or at the muddy
sterna have a diffuse pattern of intermixed pale and shores of lakes. It seems likely that Cs. ochroptera has
dark scales. at least two generations per year and that hibernation
apparently takes place in the larval or the egg stage,
298 10 Subfamily Culicinae

but Gutsevich et al. (1974) reported hibernation of and palps are mainly dark scaled with a few scattered
adult females in the eastern Ukraine. The females pale scales in the basal half of the proboscis and
rarely bite humans; they seem to feed mainly on birds throughout the palps. The antennae are dark brown,
and amphibians. and the pedicel and first flagellomere have yellowish-
Distribution: Forest zones of the Palaearctic region, white scales on the inner surface. The occiput has nar-
from central Europe through west Siberia to northeast row curved whitish scales and dark erect forked scales
China. Its southernmost distribution range reaches on its dorsal part and broad whitish scales on its lat-
Romania. It is also distributed from Sweden and eral part. The integument of the scutum is dark brown,
Finland southeast to the Caucasus. with dark and whitish scales. Two indistinct longitudi-
nal narrow stripes or patches of pale scales may be
visible, and the lateral parts of the scutum are usually
lighter than the median part. The scutellum has nar-
10.4.3 Subgenus Culiseta Felt row whitish scales and dark setae on the lobes. The
pleurites have sparse patches of narrow curved pale
The cross veins (r-m and m-cu) are in one line or scales, and the prespiracular setae are yellowish. The
slightly separated, and the distance between them is femora anteriorly are dark brown with pale scales
not longer than the length of m-cu (Fig. 6.57b). If the intermixed, and the posterior surface and apices are
tarsi are pale ringed, the rings are confined to the basal white scaled, with no subapical pale ring. The tibiae
parts of each tarsomere. The palps of the males are as are dark brown with scattered pale scales, and the tarsi
long as or longer than the proboscis, and the last two are dark with pale basal rings on tarsomeres II-III of
segments are distinctly swollen. The aedeagus is the fore and mid legs and on tarsomeres II–IV of the
strongly sclerotized, and pointed towards the apex and hind legs. Tarsomere I of the hind leg is without a
often curved or hooked. The larvae have antennae
shorter than the head, and the antennal seta (1-A) is
weakly developed. The siphon is short, and the index
is <4.0. The pecten is short and often prolonged
towards the end of the siphon by a row of long, thin
setae. The larvae are mainly bottom feeders, they spend
most of their time submerged at the bottom of their
breeding sites feeding on the substrate. The females of
the subgenus hibernate as adults. They deposit the eggs
in boat shaped egg rafts on the surface of the water like
the species of the genus Culex. In the Palaearctic region
the subgenus is represented by five species and one
subspecies.

Culiseta (Culiseta) alaskaensis (Ludlow 1906)

Female: Cs. alaskaensis is a large mosquito resem-

bling both Cs. annulata and Cs. subochrea in having a
median longitudinal pale band on tergum II and con-
spicuous spots on the wings, resulting from aggrega-
tions of dark scales in certain areas. But unlike Cs.
alaskaensis, the other two species are ornamented
with a subapical white ring on the femora and a median
white ring on tarsomeres I of all legs. In addition, the
pale basal rings on tarsomeres II–IV are much less
distinct than in the other two species. The proboscis Fig. 10.127 Hypopygium of Cs. alaskaensis
10.4 Genus Culiseta Felt 299

median light ring (Fig. 6.62b). The wing veins have branched and inserted near the middle of the antenna.
narrow dark scales, which are aggregated in some The postclypeal seta (4-C) is short, thin and
areas forming conspicuous spots. The costa (C), sub- 3-branched. The inner frontal seta (5-C) has 5–7
costa (Sc) and R1 have scattered pale scales through- branches, the median (6-C) is 2–3 branched and the
out their length. The base of the subcosta (Sc) bears a outer (7-C) has 8–11 branches (Fig. 8.80a). The comb
dense tuft of yellowish setae on the ventral side of the consists of 35–50 comb scales arranged in a triangu-
wing. The terga are blackish brown with rather broad lar patch (Fig. 10.128). The siphon is short and broad,
basal white bands, which are widened laterally, espe- slightly tapered apically, with a siphonal index of
cially on the last segments. The sterna are white 2.5–3.0. The pecten has 6–8 spine-like teeth on the
scaled, with a few dark scales intermixed. basal 1/5 of the siphon followed by an even row of
Male (Fig. 10.127): The two hypopygial character- 16–18 hair-like setae extending to near the apical
istics which distinguish Cs. alaskaensis from Cs. quarter of the siphon. The anal segment is completely
annulata and Cs. subochrea are firstly a group (2–10) surrounded by the saddle, and the saddle seta (1-X) is
of short dark stout setae located in the middle of the inconspicuous, and much shorter than the saddle. The
posterior margin of tergum VIII, and secondly the ventral brush is well developed with 3–4 precratal
slightly convex apical lobe of the gonocoxite which is setae (4-X), at least two of them piercing the saddle.
covered with short thin setae. Both characteristics are The anal papillae are of variable length, at least as
absent in Cs. annulata and Cs. subochrea. The lobe of long as the saddle, and pointed.
tergum IX has a row of long curved setae. The gono- Biology: Larvae of Cs. alaskaensis can be found
coxite is covered with many long setae on the outer from late spring on, in a variety of habitats. They
surface, and the basal lobe has 2, or rarely 3, strong favour small open pools formed by melting snow
setae. The gonostylus is curved and tapered apically, which do not dry up in summer. These pools usually
and the apical spine is short and bifurcated. The aedea- have a considerable amount of fallen leaves at the
gus is sclerotized, long, conical, tapered, and hooked bottom and little aquatic vegetation, in the tundra
at the apex. they inhabit swamps. The larvae are often associated
Larva: The antennae are less than half as long as with those of Oc. excrucians, Oc. flavescens and Oc.
the head, and the antennal seta (1-A) is multiple- cantans. In the northern parts of its distribution
range Cs. alaskaensis is apparently a monocyclic
species with one generation per year. In the more
temperate southern regions several generations per
year can be expected (Mohrig 1969). The species
apparently hibernates as adult females in tree cavi-
ties, caves, and cellars, often together with Cx. p.
pipiens. The females leave their winter habitats usu-
ally earlier than other mosquito species. Cs. alas-
kaensis frequently feeds on humans. In the tundra
zones it is well known as the large snow-melt mos-
quito that readily attacks humans and reindeer in
early spring.
Distribution: Cs. alaskaensis is a Holarctic species
that is typical of the boreal and tundra zones of
Fennoscandia, Siberia and Alaska. In the Palaearctic it
is distributed from Britain and Norway in the west to
the far East. In central Europe, its southern distribution
stretches towards the northern slopes of the Alps. In
this part of its distribution range, Cs. alaskaensis is
usually restricted to the higher mountains. Outside
Europe it can be found in mountainous regions of Iran,
Fig. 10.128 Larva of Cs. alaskaensis Pakistan, and northern India.
300 10 Subfamily Culicinae

Notes on systematics: A subspecies of Cs. alas-

kaensis, ssp. indica Edwards 1920, has been described
with a distribution range from the Caucasus to Middle
Asia and southern India. Its general colouration is
much lighter than the nominate form, the scutum is
covered with golden yellowish scales and the pale
basal bands on the terga are often broader. The male
genitalia and larvae do not distinctly differ from the
nominate form.

Culiseta (Culiseta) annulata (Schrank 1776)

Female: Cs. annulata is a large, dark brown mosquito

with whitish markings on the abdomen and the legs.
It can be distinguished from Cs. alaskaensis by the Fig. 10.129 Hypopygium of Cs. annulata
presence of subapical white rings on the femora and
conspicuous white rings in the middle of tarsomeres
I. Cs. annulata is closely related to Cs. subochrea, the also at the bases of tarsomeres II–IV, and tarsomeres
characteristics distinguishing the two species are V of all the legs are entirely dark scaled (Fig. 6.62a).
given in the description of the latter. The proboscis of The wings are largely covered with dark scales, which
Cs. annulata is speckled with pale and dark scales, are aggregated to form distinct dark spots at the base
which are darker in the apical part, and the labellum of RS, at the cross veins and the furations of R2+3 and
is dark brown. The clypeus is dark brown, the palps M. Some scattered pale scales are mainly found in the
are dark with scattered pale scales, which are espe- basal part of the costa (C), subcosta (Sc), and radius
cially abundant at the apices and with a conspicuous (R). The cubitus (Cu) is entirely dark scaled. The
pale spot at the joint of palpomeres II–III. The anten- cross veins (r-m and m-cu) usually form a straight
nae are dark brown, and the pedicel has a few whitish line (Fig. 6.63a). The abdominal terga have whitish
scales on the inner surface. The head has pale narrow basal bands, and the apical parts are uniformly dark
scales and dark erect forked scales on the occiput, scaled. Tergum II has a narrow basal band and a char-
and the eyes are bordered with yellowish white scales acteristic longitudinal median white band. Tergum
and dark, stout setae. The scutum has narrow dark VIII is predominantly pale scaled. The sterna have
brown and pale scales. The posterior submedian area yellowish white scales.
has two pale spots, and the prescutellar area has whit- Male: The posterior margin of tergum VIII is usu-
ish scales. The scutellum is brown with whitish scales ally without stout setae or occasionally a few setae
and black setae, and the postnotum is brown or dark may be present. The lobe of tergum IX has 8–12 hair-
brown. The pleurites have patches of broad, whitish like setae. The gonocoxite is conical, gradually tapered
scales, and the postpronotum is predominantly pale towards the tip (Fig. 10.129). The basal lobe of the
scaled. Hypostigmal, subspiracular, and postspiracu- gonocoxite is well developed, with 2 (rarely 3) strong
lar patches are present. The mesepimeral patch of setae conspicuously stouter than the rest.
scales almost reaches the lower margin of the mese- The apical lobe is usually absent or indistinct.
pimeron. Prespiracular setae and lower mesepimeral The gonostylus is long and slender, with a short apical
setae are present. The legs have dark brown scales spine. The paraproct is strongly sclerotized, recurved,
and conspicuous white rings. The femora are pre- with apical teeth, and the sclerites of the aedeagus are
dominantly dark scaled with scattered pale scales, separated and also strongly sclerotized.
distinct white subapical rings and pale knee spots, Larva: The head is broader than long, and the
and the tibiae have pale and dark scales intermixed antennae are less than half as long as the head and
basally and are white scaled apically. Tarsomere I has straight. The antennal seta (1-A) is inserted just beyond
a noticeable white ring in the middle and white rings the middle of the antennal shaft, with 10–15 branches,
10.4 Genus Culiseta Felt 301

Biology: In central Europe the larvae usually

occur from early spring onwards. The population
increases in the summer months and reaches its max-
imum in September. Depending on the latitude of its
occurence, Cs. annulata may have 1–3 generations
per year. The eggs are laid in rafts, which are com-
posed of approximately 200 eggs. The species breeds
in a wide variety of permanent and semipermanent
habitats including natural and artificial water recipi-
ents, both in open and shaded situations. Larvae can
be found in stagnant pools, ponds, ditches, water
troughs, and other artificial containers such as barrels
collecting rain water. Dense populations could be
found in tanks containing manure water, so it seems
probable that a high content of nitrogen provides an
additional attraction for the females to lay their eggs
(Mohrig 1969). The larvae are able to tolerate a high
content of salinity and can also be found in brackish
water (Marshall 1938). Aitken (1954a) found larvae
breeding in a tree-hole in Corsica. In artificial
Fig. 10.130 Larva of Cs. annulata containers they are often found in association with
those of Cx. p. pipiens. In natural breeding sites the
larvae occur together with those of Cs. subochrea
and Cs. morsitans (Natvig 1948). Hatching of Cs.
not reaching to the apex of the antenna. The distance annulata larvae takes place 3–5 days after egg depo-
between the postclypeal setae (4-C) is about the same sition, the larval development depends on the tem-
as the distance between the inner frontal setae (5-C) perature. Martini (1931) estimated the overall time
(Fig. 8.82a). 5-C has 4–8 branches, the median frontal from egg deposition to the emergence of the adult
seta (6-C) has 1–3 branches, and the outer seta (7-C) being 18 days at a temperature of 20–23°C and 16
has 6–14 branches (Fig. 8.78a). The comb usually con- days at a temperature of 24–27°C, above 31°C no lar-
sists of 35–50 scales, rarely more (Fig. 10.130). The vae survived. Usually the species hibernates in the
individual scales are slightly narrowed in the middle adult stage and the first females appear in early spring
part, blunt ended and uniformly fringed with small when they leave their winter shelters. At this time
spines. The siphon distinctly tapers apically, with a they readily attack humans and mammals during the
siphonal index of 3.2–4.0. The siphonal tuft (1-S) is day, but in the summer months they show a more
inserted close to the base of the siphon, usually with nocturnal biting activity and frequently enter houses
9–10 branches, and is about as long as the width of the or stables to feed on humans or domestic animals.
siphon at the base. The pecten has 11–18 spine-like Occasionally they may also take their blood meal
teeth, followed by a row of 11–21 thin, hair-like setae from birds. In former Yugoslavia, the females could
occupying approximately 2/3 the length of the siphon. be sampled more efficiently in CO2 baited traps than
The saddle completely encircles the anal segment, and on humans (Petric 1989). The females of Cs. annu-
its ventral surface is only half as long as its dorsal sur- lata can often be found inside houses even during the
face. The saddle seta (1-X) is much shorter than the day from early autumn on, when they search for their
saddle, usually with 3 branches. The upper anal seta winter habitats. They hibernate in cellars, attics of
(2-X) has 13–19 branches, and the lower anal seta dwellings, or in sheds of domestic animals, where they
(3-X) has 3 branches. The ventral brush usually has can be extremely annoying during wintertime, when the
16–18 cratal setae (4-X) and 2–3 precratal setae, 1 or 2 hibernation is interrupted by rising temperatures or
of which perforate the saddle. The anal papillae are humidity. Winter habitats can also be found far away
lanceolate, and usually as long as the saddle. from human settlements in tree cavities, stacks of
302 10 Subfamily Culicinae

wood, or other natural shelters. When the winter is

mild, or in the southern range of its distribution,
hibernation can also take place in the larval stage.
Distribution: Cs. annulata is widely distributed
throughout Europe, but it is more common in the north
than in the south, where it seems to be largely replaced
by Cs. longiareolata (Edwards 1921). The distribution
range of Cs. annulata extends into northern Africa,
Asia Minor, and southwest Asia.
Medical importance: The species is known to be a
potential vector of Tahyna virus (Ribeiro et al. 1988)
and transmitter of some plasmodia of birds (Gutsevich
et al. 1974).

Culiseta (Culiseta) bergrothi (Edwards 1921)

Female: The integument is dark brownish with some

lighter pleural parts. The colour of the light scales is
variable, from white to creamy white. The antennae
have some white scales on the pedicel, and the eyes
are bordered with white scales. The proboscis is covered
with black scales, and the palps are dark with
scattered pale scales. The vertex has white flat scales,
and the occiput has upright narrow golden scales and Fig. 10.131 Hypopygium of Cs. bergrothi
brown setae. The scutum is covered with narrow
bronze scales and a more or less distinct varying
pattern of white scales and bronze brown setae. White and the knee spots are white. Tarsomeres I–V of all
broader scales cover the front, sides, and back of the the legs are dark, with occasionally some white scales
scutum in an irregular pattern and form a narrow, on tarsomere I; the claws are simple. The wing veins
incomplete acrostichal stripe. Dorsocentral stripes of are covered with elongated, dark scales, and spots are
narrow white scales and a postacrostichal patch of always present, although often inconspicuous. The
white scales are usually present forming a scutal pat- spots result from aggregations of dark scales at the
tern similar to that of Cs. subochrea. However, sub- furcations of R2+3 and M and the cross veins (r-m and
median stripes are not present. The scutellum is m-cu). The lining up of r-m and m-cu can vary from
covered with whitish scales and light setae. The nearly a straight line to a slight displacement of m-cu
antepronotal and propleural setae are long and domi- towards the wing root, but never distal to r-m. The
nating, the postpronotum has narrow bronze and abdomen is dark with pale basal bands on the terga,
some lower, broader whitish scales. The mesepister- which are narrower in the last segments. The sterna
nal patch is large with elongated white scales in its are pale with some scattered dark scales.
upper part, and the mesepimeron is covered with Male: Somewhat smaller than the males of other
scales in its upper third. Usually not more than 15 northern European Culiseta species. They share the
prespiracular setae and not more than 10 lower mese- feature of having an extremely long tarsomere I of the
pisternal setae are present (Fig. 6.61a). The coxae of fore leg (exceeding the length of tarsomeres II–V of
the fore and hind legs have long, conspicuous setae. about one fifth) with males of Cs. fumipennis. The
The femora have white scales on the ventral surface median lobe of tergum VIII has 4–18, usually >10,
and a mixture of white and dark scales on the dorsal strong spine-like setae (Fig. 7.71b). The gonocoxite
surface. The tibiae are dark with either light dorsal has long and numerous setae laterally and apically
stripes or mixed scales, especially on the front legs, (Fig. 10.131). The basal lobe is weakly developed,
10.4 Genus Culiseta Felt 303

ventral brush has 3–4 precratal setae (4-X), usually

two of them piercing the saddle. The anal papillae
are very long and slender.
Biology: In the northern parts of its distribution
range the species breeds in open pools and has only
one generation per year. The larvae inhabit swamps
and pools in the southern tundra and shaded forest
pools in coniferous and mixed forests, they may also
tolerate polluted water. In the southern parts of its
distribution range several generations per year may
occur. Hibernation takes place in the female stage
(Gutsevich et al. 1974) and larvae can be found
together with other early spring species, such as Oc.
communis. In Scandinavia the larvae have been
recorded until the summer months. The females are
most abundant from June to August. They predomi-
nantly bite cattle and other mammals and seldom
enter houses.
Distribution: This northern species is found
throughout the tundra and northern taiga zone of the
Palaearctic, as well as in high mountainous areas both
in Scandinavia (Natvig 1948) and in Japan (Tanaka
Fig. 10.132 Larva of Cs. bergrothi
et al. 1979).

with two strong spine-like setae of almost equal length. Culiseta (Culiseta) glaphyroptera (Schiner 1864)
The apical lobe is indistinct, and covered with dense
setae. The gonostylus is long, more than half as long as Female: Cs. glaphyroptera is very similar to Cs. ber-
the gonocoxite, and the apical spine is blunt ended. grothi, the other member of the subgenus Culiseta
The paraproct is strongly sclerotized, with a curved with entirely dark tarsomeres. However, it is easy to
apex, bearing 3–4 teeth. The aedeagus is oval shaped, distinguish males and females of these two species
slightly sclerotized in the lateral parts with sigmoid, (Natvig 1948). In Cs. bergrothi the eyes are distinctly
pointed tips. bordered with light scales and the palps are dark with
Larva: The head is considerably broader than scattered pale scales. On the other hand, in Cs. glaphy-
long, and the antennae are about half as long as the roptera the eyes are not bordered with light scales and
head. The antennal seta (1-A) has 4–6 branches situ- the palps are entirely dark. The head has whitish scales
ated slightly proximal to the middle of the antennal laterally, the vertex has a tuft of short light scales
shaft (Fig. 8.83c). The frontal setae 5-C and 6-C are between the eyes, and the occiput in the posterior part
nearly in a row, with multiple branches. The protho- has upright dark brown scales. The proboscis and palps
racic setae are all very long. Numerous comb scales are dark brown. The integument of the scutum is dark
are arranged in a triangular spot (Fig. 10.132). Each brown with golden brown sickle-shaped scales, which
scale has a long, narrow stem, which is rounded api- form a narrow acrostichal stripe on the anterior part of
cally and fringed with small spines. The siphon is the scutum and two dorsocentral and lateral, more
slightly tapered apically, with a siphonal index of indistinct, stripes. The scutellum is dark with scales of
3.0–3.5. The pecten has 12–15 spine-like teeth, and the same colour as on the scutum. The pleurites of the
each tooth has 2–3 slender lateral denticles, fol- thorax have patches of whitish flat scales. The lobes of
lowed by a row of longer hair-like setae which reach the antepronotum are blackish brown with pale narrow
distally about 2/3 the length of the siphon. The anal scales. The number of prespiracular setae usually
segment is entirely encircled by the saddle, and the ranges from 16 to 22 and that of the lower mesepister-
304 10 Subfamily Culicinae

Fig. 10.133 Hypopygium of Cs. glaphyroptera

nal setae from 12 to 18 (Fig. 6.61b). The legs are dark

scaled, and the posterior surface of the femora and
tibiae has light scales, which sometimes form a
longitudinal stripe, the knee spot is distinct and Fig. 10.134 Larva of Cs. glaphyroptera
yellowish white. The tarsomeres are entirely covered
with dark brown scales, and pale rings are absent
(Fig. 6.60a). The wing veins are dark scaled, and the Larva: The head is broader than long, and the
cross veins are slightly separated. Wing spots are antennae are 2/3 the length of the head, and slightly
absent or only weakly developed. When present, the curved inwardly. The antennal seta (1-A) is inserted
spots result from aggregations of dark scales at the fur- close to the middle of the antennae and is about half as
cations of R2+3 and M and the cross veins (r-m and long as the antennal shaft, usually with 10 branches
m-cu). The terga are dark brown with indistinct bands (Fig. 8.83a). The postclypeal setae (4-C) are situated
of light brown to pale scales in the basal third of before the inner frontals and are close together. The
each tergum. The sterna are more or less uniformly frontal setae are well developed, the inner frontals
covered with yellowish white scales, or sometimes (5-C) have 7–9 branches reaching to the labrum, the
narrow bands of brownish scales are present at their median (6-C) have 5–7 branches and the outer (7-C)
posterior margins. are 8–12 branched. The comb consists of approxi-
Male: The lobe of tergum IX has numerous long, mately 70 scales, which are arranged in a crescent
thin setae. The gonocoxite is relatively short, and the shaped patch (Fig. 10.134). The comb scales are elon-
basal lobe is well developed with two long and promi- gated with a broad base and rounded apex. The sipho-
nent setae which are strongly bent in the middle nal index is 3.4–3.5. The pecten has 15–21 spine-like
(Fig. 10.133). The apical lobe has a characteristic tuft teeth followed by a row of 19–22 longer hair-like setae
of long scale-like setae. The gonostylus is long and reaching to the apical quarter of the siphon. The sipho-
expanded subapically, and the apical spine of the gono- nal tuft (1-S) is inserted close to the base of the siphon,
stylus, unlike in other species of the subgenus Culiseta, with 8 branches which are distinctly longer than the
is long. The aedeagus is cylindrical in its proximal width of the siphon at the point of its origin. The anal
part, tapered beyond the middle, and the tips are segment is completely surrounded by the saddle, which
strongly sclerotized. is half as long ventrally as it is dorsally. The saddle
10.4 Genus Culiseta Felt 305

seta (1-X) is short with 1–2 branches. The upper anal lata the integument is more brownish and the pale
seta (2-X) usually has 14 branches, forming a fan, and scutal scales are creamy white. The legs of Cs. subo-
the lower anal seta (3-X) has 3–4 branches. The ventral chrea are more speckled than those of Cs. annulata
brush has 13–16 tufts of cratal setae (4-X) on the com- owing to a greater number of pale scales scattered on
mon base, with five precratal setae, three of which the femora, tibiae, and tarsomeres I; hence, in the
pierce the saddle. The anal papillae are 1.5–2.5 times general appearance the contrast of pale and dark colour
longer than the saddle, and pointed. of the legs is not so conspicuous. The subapical white
Biology: Cs. glaphyroptera can only be found in rings on the femora are less distinct and the yellowish
mountainous regions. The larvae are mostly restricted white basal rings on the tarsi are much broader than
to partly shaded, cool breeding sites. They usually in Cs. annulata. The spots on the wings formed by
occur in the beds of small mountain rivers or streams aggregated dark scales are less obvious in Cs. subo-
and in depressions in larger rocks, where the water chrea and in addition to some pale scales on the costa
remains after the first flood in spring. They prefer water (C), subcosta (Sc), and radius (R), more or less
with fallen leaves and a rich amount of detritus rather numerous pale scales are scattered along the cubitus
than a clean stony bottom with a poor development of (Cu). In Cs. annulata vein Cu is entirely dark scaled.
algae and other organisms. Occasionally the larvae can In Cs. subochrea the cross veins r-m and m-cu are
be found in ground pools close to small brooks and usually slightly separated, the distance between them
sources together with Cx. territans. Apfelbeck (1928) not being longer than the vein m-cu (Fig. 6.63b). In
reported common findings of Cs. glaphyroptera larvae Cs. annulata the cross veins usually form a straight
in tree-holes of mountain forests in former Yugoslavia, line. The terga of Cs. subochrea have indistinct pale
where they were found in association with typical tree- bands formed by yellowish scales, the dark areas in
hole breeders such as An. plumbeus and Oc. genicula- the apical half of the terga are scattered with more or
tus during the summer months. Later in the year, at the less numerous yellowish scales. In Cs. annulata the
end of November, the larvae disappeared, but adults terga have more distinct whitish basal bands and the
could be found in sheltered situations, such as in caves. apical half of the terga lack pale scales, they are uni-
Cs. glaphyroptera hibernates in the adult stage. Little formly dark scaled.
is known about the feeding behaviour of the females. It Male (Fig. 10.135): In Cs. subochrea the basal lobe
seems likely that they feed on birds or small mammals of the gonocoxite carries 3–5 strong setae conspicu-
which inhabit the forest. ously stouter than the rest and the median lobe of ter-
Distribution: The species is widely distributed gum VIII usually bears several stout setae. In Cs.
throughout the mountains of central and southeastern
Europe. In addition, it has been found in the mountain-
ous regions of western Ukraine and Crimea. It was
thought that Cs. glaphyroptera must also be present in
the northern parts of Europe, but Natvig (1948) exam-
ined material from Scandinavia and clearly demon-
strated that all specimens formerly referred to as Cs.
glaphyroptera were in fact Cs. bergrothi. As a conse-
quence, Cs. glaphyroptera was erased from the list of
Fennoscandian mosquitoes (Dahl 1997).

Culiseta (Culiseta) subochrea (Edwards 1921)

Female: Cs. subochrea is very similar to the closely

related Cs. annulata in all stages and only the diffe­
rences between the two species are mentioned here.
The scutal integument and most of the scutal scales
are yellowish in Cs. subochrea, whereas in Cs. annu- Fig. 10.135 Hypopygium of Cs. subochrea
306 10 Subfamily Culicinae

annulata the number of strong setae on the basal lobe 1938). Larvae were found in rice fields with clean
is 2, rarely 3 and the median lobe of tergum VIII is water, associated with those of An. atroparvus and Cx.
usually devoid of stout setae. Furthermore, Peus (1930) pipiens (Ribeiro 1988), but they exhibit a remarkable
referred to the number of thin setae on the lobe of ter- preference for saline breeding sites (Rioux 1958;
gum IX, which ranges from 13 to 24 in Cs. subochrea Mohrig 1969; Gutsevich et al. 1974). The females bite
and from 8 to 12 in Cs. annulata. Unfortunately, these humans and domestic animals and they are more
characteristics are variable and overlap to a certain exophagic than those of Cs. annulata. They were
degree, thus they cannot be precisely used in all cases, reported to feed on humans during the day and far
especially if the identification is based on a single away from dwellings (Rioux 1958). An autogenous
hypopygium with 3 strong setae on the basal lobe. In egg laying of one female reared in the laboratory was
this case it is most likely that the specimen belongs to observed (Marshall 1938).
Cs. subochrea when the median lobe of tergum VIII Distribution: Cs. subochrea, a Palaearctic species,
bears several stout setae and to Cs. annulata, when the can be found in nearly all European countries, reach-
stout setae are absent. ing from southern Fennoscandia to the Mediterranean
Larva: In Cs. subochrea the distance between the region including western and central Europe, but it is
postclypeal setae (4-C) is less than the distance between not a very common mosquito. Its range stretches into
the inner frontal setae (5-C) (Fig. 8.82b), whereas in north Africa and the near East and it is widely distrib-
Cs. annulata both pairs of setae are usually about the uted in middle Asia.
same distance apart. Again, the two ranges of variation Note on systematics: The taxonomic status of Cs.
overlap considerably and it is not always possible to subochrea is still controversial. It was originally
distinguish larvae of the two species according to this regarded as being merely a variety (desert form) of Cs.
characteristic. No other structural differences between annulata, but then rose to species rank due to its distri-
the larvae of the two species seem to exist, but Ribeiro bution not being confined to desert areas and the con-
et al. (1977) pointed out that in the material from spicuous colouration of the adults (Edwards 1921).
Portugal, the length of the siphonal tuft (1-S) is dis- Likewise, Peus (1930) referred to several hypopygial,
tinctly shorter than the width of the siphon at the base pupal, and larval characteristics differentiating the two
in Cs. subochrea, and the length of 1-S is about the species and this was confirmed by Marshall (1938).
same as the width of the siphon at its base in Cs. annu- Later it was brought back to subspecies status of Cs.
lata. So far this observation has not been verified with annulata by Maslov (1967), in accordance with the
material from other locations. opinion of other Russian authors (Shtakelberg 1937;
Pupa: A characteristic which seems to be generally Monchadskii 1951). This change was based on the
constant and enables one to distinguish between Cs. comparison of characteristics and their variability of
subochrea and Cs. annulata with certainty, is found in both forms in almost all of the distribution range. The
the pupal stage. The minute denticles which fringe the authors stated an overlap in distribution of the subspe-
pupal paddle are long and pointed in the former spe- cies and its nominative form in western and central
cies and considerably shorter and blunt ended in the Europe (Gutsevich et al. 1974). Based on material
latter one. from Portugal, Cs. subochrea was re-ranked as a valid
Biology: Owing to the rare findings of Cs. subo- species by Ribeiro et al. (1977) and this was followed
chrea in western and central Europe, the biological by others (Ward 1984). This opinion is supported by
data are scanty, but its biology seems to be similar to the fact that larvae of both forms could be found sym-
that of Cs. annulata. Hibernation usually takes place in patrically in the same breeding sites in many localities
the adult female stage preferably in farm buildings and of western and central Europe (Peus 1951; Aitken
cellars, but in its southern distribution range the larvae 1954a; Rioux 1958). The specific characteristics were
may also hibernate and the dormant phase of the always retained but intermediate forms are not known,
females does not last very long. Several generations indicating that the gene flow between both forms is
per year may occur. As in Cs. annulata, the larvae can inhibited. Further research, based on morphological
be found both in fresh water habitats, like ditches, and genetical studies, demonstrate that Cs. subochrea
ponds or garden tanks, and habitats with a varying should be regarded as a distinct species (Cranston et al.
degree of salinity up to > 1/3 that of sea water (Marshall 1987).
10.5 Genus Coquillettidia Dyar 307

10.5 Genus Coquillettidia Dyar Abdominal segment X is long and slender, and the
saddle c­ ompletely encircles the segment.
Larvae of all members of the genus obtain the oxy-
The proboscis of the females is moderately long
gen from the submerged parts of aquatic plants by pen-
(about 1.5 times longer than the thorax), and uni-
etrating the plant tissue with their highly specialized
formly broad. The palps are short, 1/4 the length of
siphon. The pupae are also attached to plant tissues in
the proboscis or shorter. The vertex is covered with
order to take oxygen from the aerenchyma by their
numerous erect forked scales. The acrostichal, dorso-
sclerotized, pointed respiratory trumpets. The cuticle
central, and lateral setae of the scutum are well devel-
of the trumpets is softened subapically at a line of
oped. The scales on the scutum are usually narrow,
weakness, and breaks off prior to the time of adult
and decumbent. Prespiracular setae are absent in all
emergence. The females lay the eggs on the water sur-
subgenera, and postspiracular setae are absent in the
face in rafts of variable shape.
subgenus Coquillettidia. The upper mesepisternal
The species are grouped in three subgenera,
setae are well developed, and upper mesepimeral
Austromansonia (only one representative from New
setae are usually present. The mesepisternal and
Zealand), Rhynchotaenia (13 species mostly recorded
mesepimeral patches are small, with decumbent pale
from the Neotropical, some from the southern Nearctic
scales. The legs usually have pale rings. Tarsomere I
region), and Coquillettidia. The last subgenus con-
of the hind legs is shorter than the hind tibia. The
tains 43 species, more than half of them are distrib-
claw lacks a subbasal tooth, and typical pad-like pul-
uted in the Ethiopian region, the rest in the Oriental
villi are absent. The wing veins are covered with a
and Australian regions, one in the Nearctic region.
mixture of pale and dark, narrow, and broad scales.
Only two species of the subgenus occur in the
The abdomen is truncated, and segment VIII is short
Palaearctic region, these are Cq. buxtoni and Cq.
and broad. The cerci are short and blunt. The palps of
richiardii.
the males are about as long as the proboscis, and pal-
pomere V is generally covered with numerous long
setae. The fore and mid legs have a pair of claws,
unequal in shape and size. Abdominal segment VIII 10.5.1 Subgenus Coquillettidia Dyar
has a distinctly sclerotized tergum, and segment IX is
bilobed with sparse long setae. The basal lobe of the Coquillettidia (Coquillettidia) buxtoni
gonocoxite is small but distinct, and tapers apically. It (Edwards 1923)
bears one or more setae as long as or longer than the
lobe. The gonostylus is usually short, enlarged api- Female: Readily distinguished from Cq. richiardii by
cally with a short apical spine. Claspettes are absent, the presence of exclusively or mostly dark coloured
and the apex of the paraproct is pointed or denticu- scales on the proboscis, palps, wing veins, and tar-
lated. The head of the larva is wider than long, and someres. The scales are blackish brown pigmented
slightly sclerotized. The antennae are extremely long, with structural metallic purple. The head has pale
at least 1.5 times as long as the head. The part beyond decumbent scales and brown upright scales. The
the articulation of the antennal seta (1-A) is slender scutum has golden brown scales, which are paler
and whip-like. Abdominal segment I has the lateral around the wing base and at the posterior margin. The
tracheal branches extended into a pair of heart shaped femora and tibiae are dark scaled with scattered ochre
air-sacs which lie partly in the metathorax. The siphon coloured scales. The latter form an indistinct longitu-
is short, conical, and strongly sclerotized. The lobes dinal stripe on the ventral surface and spots at the
of the spiracular openings are dark, sclerotized, and apex. The dark scales on the wing veins are narrower
folded together. They form a tapered saw-like pierc- than in Cq. richiardii but still broader than in mem-
ing apparatus for penetrating aquatic plant tissue in bers of the genus Culex. The terga are mainly dark
order to obtain oxygen. A similar modification of the coloured with a violet hue, whitish scales are restricted
siphon is characteristic for larvae of some other none- to triangular basolateral patches, sometimes con-
European genera or subgenera, e.g. Culex (Lutzia), nected by narrow basal bands, and the sterna have
Mimomyia (Mimomyia), and Hodgesia (Gillett 1972). pale basal bands.
308 10 Subfamily Culicinae

Male: The palps are longer than the proboscis. The

hypopygium is quite similar to that of Cq. richiardii.
The lobes of tergum IX possess 4–5 thin setae. The
main difference between the two species is found in
the shape of the gonostylus. In Cq. buxtoni the basal
half of the gonostylus is stem-like, not constricted in
the middle. The apical half is considerably bulky and
then gradually narrows towards the apex. The outer
margin of the gonostylus bears four small and tiny
setae apically (Fig. 10.136b).
Larva: Closely resembles that of Cq. richiardii.
The head is about 1.5 times wider than long. The post-
clypeal seta (4-C) is multiple-branched. The inner
frontal seta (5-C) is short and 8-branched. The median
frontal seta (6-C) has 5–7 branches and the outer fron-
tal seta (7-C) has 9 branches. The comb consists of
16–22 scales arranged in an irregular row, dorsally in a
Fig. 10.136 Hypopygium of (a) Cq. richiardii partly doubled row. The individual scales have a
and gonostylus of (b) Cq. buxtoni
pointed terminal spine. Seta 1-VIII has 5–7, usually 6
branches (Fig. 8.87b), setae 2-VIII and 3-VIII are
2-branched, and 4-VIII and 5-VIII are usually 3–4
branched. Setae 2-VIII, 4-VIII and 5-VIII are at most
half as long as seta 3-VIII. The abdominal segment X
resembles that of Cq. richiardii but the saddle is cov-
ered with numbers of rows containing 2–8 spicules on
a common base (Fig. 10.137b). The saddle seta (1-X)
is 4-branched.
Biology: Because of its limited distributional range
and rarity, the data on the biology of the species are
scanty. The larvae were found attached to the roots of
Acorus sp. and Typha sp. (Coluzzi and Contini 1962).
Eggs are laid in boat-shaped rafts (Guille 1975). The
females bite humans in open areas (Gutsevich et al.
1974).
Distribution: Mediterranean subregion of the
Palaearctic. In Europe the species is present in Spain,
France, and Italy, and also reported from Romania and
Ukraine (Snow and Ramsdale 1999).

Coquillettidia (Coquillettidia) richiardii

(Ficalbi 1889)

Female: The scales on the wing veins are much

broader than those of any other European species
(Fig. 6.6b). The apex of the proboscis is slightly
broader and distinctly darker than the preceding por-
Fig. 10.137 Larva of Cq. richiardii and spicules on the saddle tion, and sometimes the pale scales form a median
of (a) Cq. richiardii; (b) Cq. buxtoni ring. The base of the proboscis has intermixed
10.5 Genus Coquillettidia Dyar 309

yellowish and brown scales, sometimes with the dark 10–25 scales, each individual scale has a well devel-
scales predominating. A pale ring is present in the oped terminal spine (Fig. 10.137). Seta 1-VIII is
middle of tarsomere I of all the legs, a pattern similar inserted into the dorsal half of abdominal segment
to that of Cs. annulata and Cs. subochrea. The palps VIII, with 2–4 branches. Setae 2-VIII, 3-VIII, 4-VIII
are short, not exceeding 1/4 the length of the probos- and 5-VIII are articulated medioventrally and have 2–4
cis, and are covered with mixed yellowish and brown branches. The siphon is very short and conical, and
scales. The vertex has yellowish golden narrow, forms a piercing apparatus. The siphonal tuft (1-S) is
curved, decumbent scales and dark erect forked inserted ventrolaterally near the middle of the siphon,
scales. The scutum is brown coloured, with narrow, and pecten teeth are absent. In addition to 1-S, two
curved brown and golden scales. The mesepisternal pairs of single setae and two pairs of curved spine-like
and mesepimeral patches have broad, whitish scales. setae with hooked ends are present which support the
The femora and tibiae are basally sprinkled with yel- penetration of the siphon into the plant tissue.
lowish and brown scales, and apically pale scaled. Abdominal segment X is elongated, longer than wide,
Tarsomere I of all the legs has a pale ring in the mid- and is completely encircled by the saddle. The saddle
dle, which is sometimes indistinct or absent. If so, the is covered with short and stout, usually single spicules,
legs are mainly covered with pale scales. Broad pale rarely 2 or 3 on a common base (Fig. 10.137a). The
basal rings are usually present at tarsomeres I–III of saddle seta (1-X) is 2–3 branched, inserted quite apart
the fore legs and all tarsomeres of the mid and hind from the posterior margin. The upper (2-X) and lower
legs. Pale rings are particularly distinct on the hind (3-X) anal setae are multiple-branched, 2-X is half as
tarsomeres. The wing veins are covered with broad, long as 3-X. The cratal setae (4-X) have 10–14 tufts
intermixed yellowish and brown scales. The terga are and 2 precratal setae (4-X) are widely separated. The
brown scaled, with scattered pale scales more numer- anal papillae are lanceolate, subequal in length, and
ous at their bases. Basolateral triangular patches of shorter than the saddle.
yellowish scales are present, and the scales may form Biology: The species has one generation per year
inconspicuous basal bands which are constricted in in the north (Service 1969) and 2–3 generations in the
the middle similar to those of Oc. punctor. The sterna south (Gutsevich et al. 1974). The females deposit
are pale scaled. the eggs in rounded rafts. The larvae hatch in inter-
Male: The palps are nearly as long as the proboscis. vals of up to 2 weeks after oviposition (Guille 1975)
The lobes of tergum IX have 8–10 setae. The gonocoxite and usually hibernate in the third or fourth-instar.
is short and stout. The basal lobe is heavily sclerotized Larvae and pupae live submerged and obtain oxygen
with a strong rod-like spine. The gonostylus is wid- from the aerenchyma of aquatic plants and move very
ened basally just above the articulation to the gonocox- little. Breeding sites may be various permanent water
ite, distinctly constricted and flexed in the middle, bodies rich in Acorus sp., Typha sp., Phragmites sp.,
enlarged again at the beginning of the distal third and Glyceria sp., Sparganium sp., Ranunculus sp., and
then tapered apically (Fig. 10.136a). The outer side of Carex sp. (Shute 1933; Natvig 1948; Guille 1976).
the gonostylus has 6–7 tiny setae and two more setae Pupation takes place from end of May to early June.
on its inner side, just beyond the middle. The apical In Serbia, blood searching females have been recorded
spine of the gonostylus is short. The apex of the para- from June to September, but usually have a seasonal
proct is strongly sclerotized and denticulated. peak during July (Petric 1989). Females can be very
Larva: The head is wider than long. The antennae numerous and a severe nuisance to humans and
are very long, 1.5–2.0 times longer than the head. The domestic animals, in the surroundings of fresh waters
long-terminal filament is hardly visible on a white or slightly saline marshes, lakes, old river beds, and
background. The antennal seta (1-A) has 15–20 estuaries. Also frequent indoor feeding on humans
branches. The postclypeal seta (4-C) usually has 5–6 has been recorded in England (Shute 1933) and occa-
branches, situated anterior to the frontal setae. The sionally in Portugal (Ribeiro et al. 1988). Nuisance is
inner frontal seta (5-C) is short, matching the postcly- usually restricted to the surroundings of the breeding
peal seta. The median frontal seta (6-C) is long, with sites but females can use ascendant air currents to
4–5 branches. The outer frontal seta (7-C) has 9 invade, in considerable number, areas up to altitudes
branches. The comb consists of an irregular row of of 800–900 m (Gilot et al. 1976). Females prefer to
310 10 Subfamily Culicinae

feed on mammals (Service 1968c; Ribeiro et al. 1988; The antennal seta (1-A) is confined to the basal half of
Petric 1989) but may also take their blood meal from the antennal shaft, with 4 or more branches. The inner
birds (Service 1969) and amphibians (Shute 1933). and median frontal setae (5-C and 6-C) are long, multi-
Jaenson et al. (1986b) found the species in horse sta- ple-branched. The setae of the thorax and abdomen are
bles and human bait collections. In England, the very long, particularly the lateral setae 6-III to 6-VI.
peaks of biting activity occurred after sunset and just Conspicious sclerotized plates are present on the dorsal
after sunrise (Shute 1933; Service 1969), while a surface of all or at least on one of the segments VI–VIII.
nocturnal biting activity was typical for a population The siphon is without a pecten but with a single pair of
from Serbia (Petric 1989). Biting activity was siphonal tufts (1-S). The siphonal index is at least 2.5,
recorded at a temperature between 9 and 26°C and a often much more. The saddle completely encircles the
relative humidity between 30 and 92%. Swarming of anal segment. The ventral brush is made up of 12 or
males could be observed one hour after sunset and at more cratal setae (4-X). The dorsal pair of the anal
dawn (Marshall 1938). In the laboratory, copulation papillae is longer than the ventral pair. The larvae
was observed in small cages of 40 × 40 × 120 cm. The develop in tree-holes, bamboo stumps, axils of brome-
species has been reported as autogenous, but some liads (arboreal or dendrolimnocolous species). All spe-
females may be unable to develop the first egg batch cies are rare, none of them being known as a nuisance.
without taking a blood meal (Guille 1975). The small genus comprises 24 species spread
Distribution: Cq. richiardii is a common species throughout the Neotropical and Oriental regions, a few
throughout Europe and widely distributed in the west- of them ranging northwards into the Palaearctic and
ern Palaearctic region. Nearctic regions, some are isolated on Madagascar
Medical importance: Females infected with WNV, and Mauritius, but none are found in continental Africa.
and Omsk haemorrhagic fever virus (OHF) were Or. pulcripalpis is the only member of the genus found
detected in wild populations (Detinova and Smelova in the Palaearctic region (Gutsevich et al. 1974; Dahl
1973). and White 1978).
Note on systematics: Guille (1975) stated that some
authors consider the nearctic species Cq. perturbans
as a geographic race of Cq. richiardii. Similarity in
both morphological and biological characteristics of Orthopodomyia pulcripalpis (Rondani 1872)
the two species should stimulate further investigation.
Female: It differs from most of the other Palaearctic
mosquitoes by its conspicious pattern of white scales
on a black background producing several easily recog-
10.6 Genus Orthopodomyia Theobald nised characteristics. The proboscis has black scales
and a moderately broad ring of white scales within the
The palps of the females are 1/3 as long as the probos- apical half. The palps are nearly half as long as the
cis. The vertex is covered with erect forked scales. The proboscis, black, with a white ring at the base and in
postpronotum usually has 2 setae, and postspiracular the middle, and the apex is white. The antennae are
setae are absent. Tarsomeres I on the fore and mid legs black, the pedicel is covered with white scales, and
are distinctly longer than the other four tarsomeres 3–5 basal flagellomeres may have a median line of
together. The combined length of tarsomeres IV and V white scales. The head is black, and covered with a
is shorter than tarsomere III of the fore and mid legs. mixture of black and white scales. The posterior mar-
The abdomen is parallel sided with a truncated end, the gin of the eyes dorsally is covered with white scales.
cerci are blunt and moderately projecting. The palps of The scutum is covered with narrow black scales, dis-
the males are slender, and about as long as the probos- tinctly ornamented with three pairs of narrow, white
cis. Palpomere V (sometimes also palpomere IV) is longitudinal stripes. A dorsocentral pair of stripes
greatly reduced without dense, long setae. The hypopy- extends from the anterior margin to the posterior third
gium is similar to those of the genus Culiseta and sub- of the scutum, where it is broken. It continues on over
family Anophelinae. The general colouration of the the prescutellar dorsocentral area as a wider stripe con-
larvae is red or pink, and violet-blue before pupation. verging and ending on the scutellum. The second pair
10.6 Genus Orthopodomyia Theobald 311

Fig. 10.138 Hypopygium of Or. pulcripalpis

of stripes is confined to the posterior submedian area.

The third pair of stripes almost completely borders the
scutum. All the legs are covered with black scales with
a metallic shine, with white spots on the femoro-tibial Fig. 10.139 Larva of Or. pulcripalpis
and tibio-tarsal articulations. The dorsal surface of the
femora is speckled with white scales. Tarsomere IV of
the fore legs is not as long as it is broad (Fig. 6.4a). The Larva (Fig. 10.139): In all instars the larvae are
fore and mid tarsi are entirely black scaled, sometimes easily recognised by the absence of pecten teeth and
with weakly developed, narrow basal white rings, most the pinkish colouration. The head is dark and rounded.
conspicuous at the base of tarsomere I of the mid legs. The antennae are straight, < 1/4 the length of the head,
Tarsomeres I–IV of the hind legs have white rings at without spicules. The antennal seta (1-A) is articulated
both ends of each tarsomere, and tarsomere V is com- at the end of the basal third of the antennae, with 3–7
pletely white. The wing veins have dark brown scales, short fan-like branches. The postclypeal setae (4-C)
and the bases of the subcosta (Sc) and radius (R) have are long, with 5–7 branches. The frontal setae are long
patches of silvery white scales. The abdomen is black- and multiple-branched. The inner (5-C) is 5–8
ish brown, covered with scales of the same colour as branched, the median (6-C) is 9–10 branched extend-
the scutum, with moderately broad basal bands of ing well beyond the anterior margin of the head, and
white scales. the outer (7-C) is of similar length and branching as
Male: The palps are distinctly longer than the probos- 4-C. The thorax has very long lateral setae. The abdo-
cis, black scaled, with white rings at the articulations of men distinctly narrows towards the end, with long lat-
the palpomeres, and palpomere V is entirely white. The eral setae. The section of the main tracheal trunks
basal lobe of the gonocoxite is conical, with 4–5 large within the thorax and abdominal segments V–VII is
spine-like setae (Fig. 10.138). The gonostylus is rela- enlarged. Sclerotized plates are usually present on
tively narrow, and slightly expanded in the basal half. abdominal segment VI, and always present on seg-
The apical spine of the gonostylus is inserted laterally ments VII and VIII (Fig. 8.4a). The plate is broadest
close to the apex, and subdivided into five finger-like on segment VII and extends down to its lateral sides.
­serrations. It is longer than the width of the gonostylus at On segment VIII it is narrower but nearly encircles the
the point of insertion. Claspettes are absent. segment. The plate on segment VI is small and narrow,
312 10 Subfamily Culicinae

and restricted to its dorsal part. The comb consists of Note on systematics: The original spelling pulcri-
23–30 scales arranged in two rows. Most of the scales palpis, first published by Rondani in 1872, was
have a pointed terminal spine. Seta 3-VIII is strongly replaced by the spelling pulchripalpis by Verrall in
developed, resembling the siphonal tuft. The siphonal 1901 and adopted by Knight and Stone (1977). The
index is 3.5–4.0. The siphonal tuft (1-S) is composed correct original spelling was revived after Snow (1985)
of 8–13 long branches, inserted at the basal 2/5 of the and adopted by Ward (1992).
siphon. The pecten is absent, and narrow sclerites are
laterally positioned in front of the saddle. The saddle
completely encircles the anal segment, and is narrowed
 enus Uranotaenia
10.7 G
ventrally. The saddle seta (1-X) is short and inserted at
the posterior margin of the saddle. The upper anal seta Lynch Arribalzaga
(2-X) forms a short, asymmetrical fan with 9–14
branches, the length of the branches increases progres- The species of the genus Uranotaenia are generally
sively towards the lower anal seta (3-X). 3-X is single small dark mosquitoes, which are characterized by
and very long. The ventral brush has 12–14 cratal setae having short palps in both sexes, the proboscis is usu-
(4-X). The anal papillae are lanceolate, and the dorsal ally swollen at the tip and the antennae of the males are
pair is twice as long as the ventral pair. very plumose. The scutum has stripes or spots of flat
Biology: It is a polycyclic species, the larvae occur metallic shining scales, the antepronotal lobes are well
throughout the season from May to October in south- separated. The pleural setae are reduced in number,
ern Bulgaria (Bozkov et al. 1969) and from June to and the scales usually form only 1 or 2 patches or
October in Greece. Hibernation takes place in the stripes. The wings exhibit a characteristic venation
fourth larval stage; the larvae can survive the freezing pattern with the anal vein (A) sharply bent apically,
of the water surface (Shannon and Hadjinicolaou ending before or at the same level as the furcation of
1937). The larvae breed in water with a high pH- the cubitus (Cu). The abdomen of the females is blunt
value, in tree-holes (dendrolimnocolous) or holes in ended, and the cerci are short and rounded. The male
the roots of elm, oak, beech, horsechestnut, olive, and genitalia have a short, somewhat conical shaped
plane-tree (Shannon and Hadjinicolaou 1937; gonocoxite with a moderately developed basal lobe.
Munstermann et al. 1985). Large tree-holes that can The gonostylus is short with a small apical spine, and
support a permanent presence of water are preferred claspettes are absent. The larvae are small with a dark
breeding sites. Larvae are often found in association head and short antennae. The inner (5-C) and median
with those of An. plumbeus, Oc. pulcritarsis, Oc. (6-C) frontal setae are stout and spine-like in many
geniculatus, Oc. echinus, and Oc. berlandi (Rioux species. The abdominal segment VIII is covered with
1958; Coluzzi 1968; Bozkov et al. 1969). An ornitho- characteristic sclerotized plates on its lateral parts. The
philic host preference has been reported (Ribeiro pecten teeth and siphonal seta (1-S) are present and the
et al. 1988). Any attempt to feed the females on saddle completely encircles the anal segment. The lar-
humans in the laboratory failed (Shannon and vae rest with their bodies almost parallel to the water
Hadjinicolaou 1937). According to Gutsevich et al. surface, unlike most culicines and may be, at the first
(1974) the females rarely bite humans and are most glance, confused with anophelines. Eggs may be
active during the day in shaded places. deposited either in boat shaped rafts or laid singly on
Distribution: Or. pulcripalpis is a Palaearctic the water. Very little is known about the adult feeding
species, mainly distributed in the Mediterranean behaviour.
region, Black Sea coast, and Transcaucasia. In Uranotaenia is a relatively large genus, which occurs
Europe it extends northwards to Belgium and south- mainly in regions with tropical climates and only a few
ern England. species are found in the more temperate zones of the
Medical importance: The vectorial capacity of the Holarctic region. About 207 valid species have been
genus Orthopodomyia is not well studied, although recorded in the genus, which is divided into two sub-
many of its members prefer birds as hosts and ­probably genera, namely Uranotaenia Lynch Arribalzaga and
play a role in amplification of avian arboviruses Pseudoficalbia Theobald (Peyton 1972; Knight and
(Zavortink 1968). Stone 1977; Ward 1984, 1992). The only species occur-
10.7 Genus Uranotaenia Lynch Arribalzaga 313

ing in the Palaearctic region, Ur. unguiculata, is placed

in the subgenus Pseudoficalbia, which is characterized
by having no suture between the prealar area and the
mesepisternum.

 ubgenus Pseudoficalbia
10.7.1 S
Theobald

Uranotaenia (Pseudoficalbia) unguiculata

Edwards 1913

Female: A dark mosquito notable for its conspicu-

ous stripes of flat silvery scales along the lateral mar-
gin of the scutum. It can be distinguished from all
Fig. 10.140 Hypopygium of Ur. unguiculata
other European species by the shape of its anal vein,
which is sharply bent apically and ends slightly
before or at the same level as the furcation of the
cubitus (Cu) (Fig. 6.2a). The proboscis is blackish
brown with patches or an indistinct line of pale scales
on the ventral surface, and markedly swollen at the
apex. The antenna is brown, and the pedicel has
light scales. The head is mainly dark scaled with sil-
very scales along the eye margins and on the occiput.
The scutum is covered with blackish or dark brown
scales. Distinct ­lateral stripes of flat silvery scales
stretch from the anterior margin to the wing base.
A similar stripe runs across the pleurites stretching
from the antepronotum to the mesepimeron. The
scutellum has blackish brown scales. The legs are
largely dark, with patches of white scales at the tips
of the femora and tibiae, and pale longitudinal stripes
on the anterior surface of the fore and mid femora.
The tibiae often have a diffuse pale ring in the mid-
dle, with dark brown tarsomeres. The wing veins are
dark scaled, and the bases of the subcosta (Sc) and
radius (R) have pale scales. The terga are covered Fig. 10.141 Larva of Ur. unguiculata
with dark brown iridescent scales, often with trian-
gular spots of white scales which can be found Larva (Fig. 10.141): It is easily recognised by its
mainly on the last segments, and the sterna have light sclerotized plates on the lateral parts of abdominal
scales. segment VIII, from which 5–8, usually 6, dark spine-
Male: The palps are considerably shorter than the like comb scales arise in a row along the posterior
proboscis. The gonocoxite is broad and short, and margin. The antennae are short, almost without spic-
irregularly conical shaped (Fig. 10.140). The small ules and with a tiny single antennal seta (1-A), which
flattened basal lobe bears several long, stout setae. The arises close to the middle of the antennal shaft. The
gonostylus is broad and flattened dorsoventrally with head is dark and slightly broader than long with the
the inner margin sigmoid shaped, and the apical spine base of the labrum located more anteriorly than in
of the gonostylus is pointed. other species. The mouth brushes are distinctly bent
314 10 Subfamily Culicinae

apically. The labral seta (1-C) is strongly developed. shores of lakes, which are overgrown with Lemna
This is an adaptation to the feeding behaviour of the sp., Scirpus sp., and Phragmites sp. They can also be
larva, which feeds on the surface film from below, found often in shaded localities. The larvae prefer
while bending its head backwards with the body in a fresh water and are only occasionally found in water
horizontal position. The inner (5-C) and median (6-C) with a slight salinity. They often occur together with
frontal setae are long, stout and single, 5-C rarely 2–3 larvae of An. hyrcanus, An. sacharovi, Cx. p. pipiens,
branched. The inner setae are located close together Cx. modestus, and Cx. theileri. Larvae of Ur. ungui-
behind the median setae. The outer frontal setae (7-C) culata can be found from May to early October with
have 4–7 branches. Abdominal segment VIII has the a peak in August. The adults are most abundant
above mentioned sclerotized plates laterally. The in late summer, this may lead to the presumption
siphon is nearly conical and slightly tapered towards that the species hibernates in the adult stage. It
the apex, with a siphonal index of 3.2–4.0. The pecten seems likely that the females of Ur. unguiculata
consists of 13–20 weakly pigmented teeth, with the do feed on blood, but rarely bite humans or mam-
distal tooth reaching to the point of insertion of the mals even though they may be capable of doing
siphonal tuft (1-S). The tuft has 7–12 branches and so. In a population from Turkmenistan autogeny has
arises near the middle of the siphon. The saddle com- been observed (Rioux et al. 1975). Other species
pletely encircles the anal segment, and its posterior of the genus are known to feed on amphibians
margin is covered with distinct tiny spicules. The (Remington 1945).
saddle seta (1-X) is 3–5 branched, and is about the Distribution: Ur. unguiculata is a frequent species
same length as the saddle. The ventral brush has 8–11 throughout the Mediterranean region. In Europe, its
multiple-branched tufts of cratal setae (4-X), and pre- distribution range stretches as far north as Germany
cratal setae are absent. The anal papillae are lanceo- (Becker and Kaiser 1995). In eastern Europe the spe-
late, pointed or rounded at the end and generally cies can be found in the southern Ukraine and the
shorter than the anal segment. Volga delta with further occurrence in Middle and
Biology: The favoured larval breeding sites of southwest Asia to Iran and Pakistan.
Ur. unguiculata are pools, ditches, or canals with Note on systematics: A subspecies of Ur. unguicu-
stagnant or little flow of water and a rich growth of lata, ssp. pefflyi is recorded from the Arabian penin-
aquatic vegetation. They are also common in shallow sula (Knight and Stone 1977).
 Part III
Identification Keys, Morphology, Ecology
and Distribution of Important Vector
and Nuisance Species – Worldwide

Reaching the final number of species to be included nuisance and/or vector species. Perhaps about 5% are
on the list was not an easy task, especially for the nui- to be regarded as representing a serious threat on
sance species since the literature about this aspect of account of their vicious biting habits and/or vectorial
their impact was quite scarce and outdated. Addition- capacities, based upon a preference for human blood
ally, the question: “Are the primary vector mosquitoes as food.
also nuisance mosquitoes?” was difficult to answer. The selected species are divided into two groups.
Clearly with species such as Ae. aegypti, Cx. p. quin- The first includes those species that are recognised as
quefasciatus, An. funestus and An. gambiae (Gillies major disease vectors and/or which are responsible for
and deMeillon 1968, Doannio et al. 2006, Kulkarni severe biting nuisance, and which are therefore con-
et al. 2007), they are both. However in many cases it sidered to be of primary importance. For these species
is difficult to establish the relative importance of a description of the fourth-instar larvae and the adult
mosquito nuisance and mosquito-borne disease. Even female, the biology, medical importance and distribu-
for one species, factors such as local meteorology, tion range are provided. The second group includes
socio-economic development, or the occurrence or those species with lower vectorial capacity and/or lim-
introduction of pathogens, may alter the relative impor- ited distribution, that are considered to be of secondary
tance of the two types of impact in different parts of its importance. Although some species responsible for
range. In selecting species to include in this book, we locally important biting nuisance, and/or which are
have gave higher priority to disease transmission, as vectors of potential or secondary importance have
this can occur even with low numbers of mosquitoes, therefore been excluded from the keys and description,
while nuisance occurs only when relatively high most of these species are nonetheless mentioned in the
populations are present. introductory paragraphs for each continent, and their
The importance of Anopheles is confined almost general distribution according to Walter Reed
exclusively to the tropical and subtropical parts of the Biosystematics Unit (WRBU) is given.
world, corresponding primarily to their role in trans- Keys are provided for adult females only, bearing in
mission of malaria. In many temperate areas, such as mind that it is the blood-seeking individuals that are
most of Europe and the United States, socio-economic most often encountered. In addition, we provide descrip-
development and public health measures have suc- tions for the larval stage as well as species biology and
ceeded in eradicating malaria. For example, no anoph- distribution. However, descriptions of male genitalia are
elines from the U.S.A. have been included in the key omitted given that encountering male mosquitoes is less
or in the species description, because of their low cur- likely, and adult male ­sampling is usually carried out
rent status as potential vectors in this region. only in proximity to breeding sites.
Of the ca. 3500 species of Culicinae, the large majority All the characters used in the keys have been
are harmless to man. Most of them are adapted to selected according to the species composition in each
diverse animal hosts and feed on human blood only continent.
occasionally, if at all (Malaya, Toxorhynchites). Many Some cosmopolitan nuisance and/or vector species
are either so rare as to be of no importance, or so rural are included in the keys of most continents (Ae. aegypti,
and modest in habits that they cannot be regarded as Ae. albopictus, Cx. p. pipiens biotype molestus and
316 

Cx. p. quinquefasciatus) and have been described in precise yet completely unambiguous keys. In order to
the chapter on the European mosquitoes. Some other cope with this problem and to improve the level of
widely distributed species are included in the keys of accuracy, some important additional characters were
more than one continent, and described under the con- usually included (in smaller font and after a dash at
tinent where they are most important. each thesis/antithesis) to guide the reader through the
Having selected only a few out of hundreds of species numerous genera and species of the region, that are
in each region, it was not possible to create short, not mentioned in the text nor included in the key.
Chapter 11
Africa

There is no doubt that with statistics of several circumluteolum] (central and southern Africa); Ae.
hundred bites/man/night inflicted by Cx. p. africanus [Stegomyia africana] (central Africa); Oc.
quinquefasciatus 1 and Cx. antennatus in Kinshasa caspius1 (northern Africa); Oc. detritus1 (northern
(Coene 1993; Karch et al. 1993), these mosquitoes Africa); Oc. caballus (eastern and southern Africa);
could be classified as both voracious biters and Cx. duttoni (central and southern Africa) and Cx. p.
important vectors, at least in some countries. pipiens biotype molestus1 (northern Africa) (Scirocchi
Unfortunately, the vectorial capacity, pest status, and et al. 1990; Jupp 1996; Hassan and Onsi 2004; Muturi
distribution range cannot be defined so clearly for other et al. 2007). Furthermore, Ae. africanus, Ae. luteo-
important species. African anophelines of secondary cephalus [Stegomyia luteocephala] (Tropical Africa),
importance that could be involved in malaria Ae. opok [Stegomyia opok] (central Africa), Ae. taylori
transmission are An. labranchiae1 (North Africa), An. [Diceromyia taylori] (central and southern Africa)
merus (costal East Africa) and An. sergentii1 (North could be important dengue vectors in the Afro-tropical
Africa). Ae. furcifer [Diceromyia furcifer] (with a region (Rueda 2004).
patchy distribution in eastern, western and southern In addition, Cx. sitiens is listed as a major pest in
Africa) may also be involved in the transmission of Australia and consequently described there, but is
Chikungunya, dengue and yellow fever viruses also included in the key to African females, although
(Germain et al. 1980; Jupp 1996; Diallo et al. 1998). it is of lesser importance there. The same is true for
Apart from being potential vectors of malaria, Cx. tritaeniorhynchus, described in the Asia section.
yellow fever, Sindbis, Chikungunya, Rift Valley fever and Cx. neavei is given in the key only in order to avoid
West Nile viruses (Huang 1990; Jupp 1996), species confusion (misidentification) with the very similar
included in the next group can cause considerable nui- Cx. univittatus.
sance where they occur: An. multicolor1 (northern For further reading on the morphology, identification,
Africa); An. rufipes (central and southern Africa); biology, distribution, and disease vector status of the
Ae. albocephalus (south eastern, southern and south species mentioned, the reader is referred to Kerr (1933),
western Africa); Ae. circumluteolus [Neomelaniconion Evans (1938), Edwards (1941), De Meillon (1947),
Lewis (1948), Hopkins (1952), Muspratt (1955, 1956),
Gillies and De Meillon (1968), Mattingly (1971), Smith
1
Species described in Chaps. 9 and 10 concerning European (1973), McIntosh (1986), Anonymous (1993, 2000),
mosquitoes Jupp (1996), Huang (2001), Rueda (2004).

N. Becker et al., Mosquitoes and Their Control, 317

DOI 10.1007/978-3-540-92874-4_11, © Springer-Verlag Berlin Heidelberg 2010
318 11 Africa

11.1 Key to African Female Mosquitoes

1 Palps as long as proboscis. Scutellum evenly rounded or slightly trilobed and uniformly setose (Fig. 11.1a).
Abdominal terga and sterna completely or largely missing scales. – Proboscis is neither strongly recurved nor
tapering towards apex. Anopheles..................................................................................................................... 2
Palps distinctly shorter than proboscis. Scutellum trilobed, setae arranged in three sets (Fig. 11.1b).
Abdominal terga and sterna uniformly and densely covered with scales. – Proboscis is neither strongly recurved
nor tapering towards apex. Prespiracular setae absent. Anal vein (A) evenly curved, ending distinctly beyond furcation of
cubitus (Cu). Alula with narrow fringe scales........................................................................................................ 4

Fig. 11.1. Scutellum of: (a) Anopheles sp.; (b) Aedes sp.

2 (1) Abdominal segments with laterally projecting tufts of dark scales on terga II–VII (Fig. 11.2a). – Hind tar-
someres I–IV at least with apical pale rings, hind tarsomere V and about apical half of IV pale. Wing with abundant pale
areas, costa (C) with at least 4 pale spots...........................................................................An. pharoensis (p 326)
Abdominal segments without laterally projecting tufts of scales (Fig. 11.2b). – Hind tarsomeres IV and V not
entirely pale, sometimes almost entirely dark........................................................................................................ 3

a b

Fig. 11.2 Abdomen of: (a) An. pharoensis; (b) Anopheles sp. Fig. 11.3 Tibiae of: (a) An. gambiae s.l.; (b) An. funestus

3 (2) Legs speckled with pale scales (sometimes sparsely) (Fig. 11.3a). – Palps with 3–4 pale rings. Tarsomeres I–IV
with conspicuous pale rings at least at their apices. Wing with a pale interruption on vein R1 (sometimes fused with the pre-
ceding pale area) within the third main dark area (Fig. 7.3a). Pale fringe spots at terminations of all veins, sometimes absent
at tips of Cu2 and/or A. . ................................................................................... Anopheles Gambiae Complex (p 323)
11.1 Key to African Female Mosquitoes 319

Legs not speckled, mainly dark (Fig. 11.3b). – Palps with 3 pale rings, terminal comprising the apex. Subapical
pale ring much narrower than subapical dark ring. Hind tarsomeres dark or with narrow apical pale rings. Wing without
pale interruption within third main dark area. Pale spots on the wing not confined to costa (C) and R1. Costa with at least one
pale spot on its basal half. Basal area of vein R1 entirely pale, preaccessory dark spot on R1 absent or if present, narrower
or only slightly broader than adjoining pale spots. Vein Cu1 with one pale spot. Tip of anal vein (A) dark, no fringe
spot present......................................................................................................................An. funestus (p 322)
4 (1) Postspiracular setae absent (Fig. 11.4a). Pulvilli present, well developed (pad-like). – Antenna with flagellomere
I about as long as flagellomere II. Erect forked scales not restricted to occiput, numerous on vertex too. Scutum without
silvery spots. Scutellum with all scales narrow. Paratergite without scales. Femora and tibiae either without
longitudinal stripes, or if stripes are present on any of them, the hind tibia has a pale apical spot and the anterior stripe does
not reach the apex. Tarsomere I of fore legs usually shorter than tarsomeres II–V together. Tarsomere IV of fore legs not
reduced, distinctly longer than broad. All tarsal claws simple. Wing scales narrow. Abdomen rounded apically, cerci short,
hardly visible. Culex........................................................................................................................................ 5
Postspiracular setae present (Fig. 11.4b). Pulvilli absent or not well developed (hair-like). – Back of the
head, pleurites, and posterolateral corners of abdominal terga not covered with broad silvery scales............................. 10

Fig. 11.4 Lateral view of thorax of: (a) Culex sp.; (b) Mansonia sp.

5 (4) Proboscis with distinct broad median pale ring (Fig. 11.5a). Lower mesepimeral setae absent. Tarsomeres
of all legs with narrow, indistinct basal and apical pale rings. Rings usually more distinct on tarsomeres
I–III, on bases of tarsomeres and on hind legs............................................................................................. 6
Proboscis without pale ring in the middle but often with a pale midventral area (Fig. 11.5b).
Usually only one lower mesepimeral setae present. Tarsi all dark.............................................................. 7
6 (5) Anterior surface of mid femur with numerous scattered pale scales (Fig. 11.6a). Tibiae sometimes with
indistinct longitudinal pale stripes. Small apical patches or bands of pale scales sometimes present on
tergum VII and/or VIII..................................................................................................... Cx. sitiens (p 366)
Anterior surface of mid femur without scattered pale scales (Fig. 11.6b). Tibiae dark anteriorly. Tergum
VII and/or VIII without apical bands or patches. – Anterior and middle part of scutum predominantly dark scaled,
numerous pale scales present near scutellum..................................................................... Cx. tritaeniorhynchus (p 349)
320 11 Africa

Fig. 11.5 Proboscis of: (a) Cx. sitiens; (b) Cx. univittatus Fig. 11.6 Mid leg of: (a) Cx. sitiens; (b) Cx. tritaeniorhynchus

7 (5) Postspiracular scales present (Fig. 11.7a). Prealar scales present. Costa (C) with small spot of pale
scales on lower edge close to base........................................................................................................... 8
Postspiracular scales absent (Fig. 11.7b). Prealar scales absent. Wing scales entirely dark................... 9

Fig. 11.7 Lateral view of thorax of: (a) Cx. univittatus; (b) Cx. p. quinquefasciatus

8 (7) Mid femur with longitudinal pale stripe rarely broken (Fig. 11.8b). Hind femur with long dark apical
dorsal stripe starting within 1/5 from its base (Fig. 11.8a). Terga with broad white basal transverse
bands rounded posteriorly and confluent with basolateral patches....................... Cx. univittatus (p 329)
Mid femur without longitudinal pale stripe or rarely broken stripe is present (Fig. 11.8d).
Hind femur with short dark apical dorsal stripe starting within about 1/2 from its base (Fig. 11.8c).
Terga with narrow white basal transverse bands sometimes reduced to median spot. Bands or spots
absent on terga VI–VII..............................................................................................................Cx. neavei

Fig. 11.8 Hind and mid femora and tibia of: Fig. 11.9 Abdomen of: (a) Cx. p. pipiens; (b) Cx. antennatus
(a, b) Cx. univittatus; (c, d) Cx. neavei
11.1 Key to African Female Mosquitoes 321

9 (7) Terga with well developed pale basal bands (Fig. 11.9a). – Scutal scales usually fawn (pale brown) coloured
(reddish-brown in Cx. p. pipiens). Pale spot at tip of hind tibia inconspicuous. Veins R2 and R3 just about 2.5 times
as long as R2+3......................... Cx. p. pipiens biotype molestus and Cx. p. quinquefasciatus (p 277, 278)
Terga, at least the first few, without pale basal bands (Fig. 11.9b). – Mesepimeron with a distinct patch of scales
in the middle. Tergum V with small basolateral patch of pale scales and terga VI and VII with broad lateral longitudinal
stripe of pale scales................................................................................................... Cx. antennatus (p 328)
10 (4) Claws of fore legs with subbasal tooth or wing scales narrow (Fig. 11.10a) or both. – Proboscis without a
white ring. Head with erect forked scales not numerous, restricted to occiput. Scales of scutellum all broad. Postprocoxal
membrane without scales. Femora with white knee spot. Mid femur without three large white patches on anterior surface.
Hind tarsomere V entirely white. Aedes subgenus (Stegomyia)................................................................... 11
Claws all simple. Wing scales usually broad and conspicuous (Fig. 11.10b), many asymmetrical. – Erect
forked scales numerous, not restricted to occiput. Subspiracular area without scales. Mansonia........................... 12

Fig. 11.10 Wing scales of: (a) Aedes sp.; (b) Mansonia sp.

11 (10) Scutum without acrostichal stripe on anterior part, but with two narrow white dorsocentral stripes sepa-
rated from anterior margin. Lateral white stripes broad, continuing over transverse suture to the end of
scutum, lyre shaped (Fig. 11.11a). – Clypeus with white scale patches. Mesepimeron with two well separated white
scale patches. Anterior portion of mid femur with a longitudinal white stripe............................. Ae. aegypti (p 198)
Scutum with a white acrostichal stripe extending from the anterior margin to the beginning of the pres-
cutellar area, where it forks to end at the anterior margin of the scutellum (Fig. 11.11b).
– Clypeus without white scale patches. Mesepimeron with white scale patches forming V-shaped pattern. Anterior portion
of mid femur without a longitudinal white stripe.............................................................. Ae. albopictus (p 201)

Fig. 11.11 Scutum of: (a) Ae. aegypti; (b) Ae. albopictus Fig. 11.12 Hind leg of: (a) Ma. africana; (b) Ma. uniformis
322 11 Africa

12 (10) Submedian area of scutum with three pairs of pale patches or stripes. Median area without distinct
dorsocentral stripes of pale scales. Anterior surfaces of mid and hind tibiae with about 6–10
detached pale patches (Fig. 11.12a). Basal half of hind femur with rings of dark scales reaching ventral
margin......................................................................................................................Ma. africana (p 330)
Submedian area of scutum with a pair of continuous pale longitudinal stripes. Central area of scutum
with dorsocentral stripes of pale scales. Anterior surfaces of mid and hind tibiae with mostly confluent
creamy white patches (Fig. 11.12b). Basal half of hind femur paler, dark scales restricted to upper ante-
rior surface.............................................................................................................Ma. uniformis (p 330)

11.2 Species Description R4+5 usually entirely dark scaled, sometimes with a
pale area in the middle. Wing fringe with pale spots
Anopheles (Cellia) funestus Giles 1900 at the terminations of the veins except anal vein (A),
spots sometimes very small and indistinct.
Female: A very small dark species. Proboscis dark Integument of abdomen dark brown, devoid of
scaled, palps with 3 pale rings of variable but mod- scales, including the cerci, and clothed with numer-
erate width, the apical pale ring embracing entire ous pale setae.
palpomere V or only a part of it, but tip of palps Larva: A small dark species with unusually large
always pale, the median pale ring at joint of pal- tergal plates. Head capsule with two dark brown pig-
pomeres III and IV, the dark intervening ring usu- mented transverse bands, antenna about half as long
ally considerably longer than either pale ring, the as the head, usually heavily pigmented, with numer-
basal pale ring at apex of palpomere II and some- ous and conspicuous spicules. Antennal seta (1-A)
times including base of palpomere III. Vertex with minute, inserted at about 1/4 to 1/3 from the base
pale erect scales, darker erect scales on occiput, of the antennal shaft. Inner and outer clypeal setae
frontal tuft moderately developed, with about 6–10 (2-C and 3-C) slender, single, the pair of 2-C well
long, whitish scales. Integument of scutum with a separated, 3-C slightly more than half as long as 2-C.
median pale area and contrasting dark brown areas Postclypeal seta (4-C) single, distinctly shorter than
laterally, median area clothed with very narrow pale 3-C, exceeding the base of 2-C by about 1/2 of its
scales. Integument of pleurites dark brown, with own length, frontal setae (5-C to 7-C) long and plu-
pale transverse bands, prespiracular setae sometimes mose. Prothoracic setae 1 and 2 (1-P and 2-P) well
absent, when present, very small and about 1–3 in developed, arising from large sclerotized tubercles,
number. Fore coxae sometimes with a few scales on which are broadly fused, 1-P sometimes with mark-
anterior part, remainder without scales. Legs pre- edly flattened stem, 2-P twice as long as 1-P or lon-
dominantly dark scaled, tibiae usually with small ger, with 14–16 branches, 3-P about half as long as
apical pale spots (Fig. 11.3b). The hind tarsi are 1-P, single. Metathoracic palmate seta (1-T) well
usually entirely dark, but sometimes the scales at developed with slender lanceolate leaflets. The ven-
the extreme apices of the tarsomeres are obscurely tral surfaces of the abdominal segments bear con-
pale, giving the appearance of very narrow indis- spicuous rows of spicules, especially evident on
tinct rings. Wing veins predominantly dark scaled, segments IV–VI. Palmate setae well developed on
the degree of pale and dark scaling variable. Costa abdominal segments I–VII (1-I to 1-VII), those of
(C) usually with 4 pale spots always markedly segments I and II smaller than the others. Typical
shorter than the corresponding dark areas, but vary- leaflets on segments III–VII light in colour distally
ing in width, basal quarter of costa usually entirely with a contrasting dark pigmented area just basal to
dark, sometimes with one pale interruption. Vein shoulders, filaments long and slender, serrate at base
11.2 Species Description 323

and sharply differentiated, about half as long as the long periods when disturbed. Apart from its important
blades. Tergal plates very large and sometimes heav- role in malaria transmission, An. funestus may act as a
ily pigmented, on abdominal segments IV–VII they major pest and is closely adapted to humans in many
are more than half as long as the segment, and dis- aspects of its behaviour. It is one of the most
tinctly wider than the distance between the bases of anthropophilic mosquitoes known, in many areas
the palmate setae of each segment, the shape of the attacking humans even in the presence of abundant
plates is rather variable, but commonly somewhat alternative hosts such as sheep and cattle. The females
rectangular with the posterior margin slightly con- usually feed inside houses after 2200 hours up to dawn,
vex (Fig. 11.13). Setae 0 on segments III–VII (0-III entering of the houses starts one hour after sunset with
to 0-VII) more prominent than in most other a peak around 2300 hours (Gillies and De Meillon
Anophelines, usually with 1–2 branches situated on 1968). After the blood meal they stay inside the houses
the tergal plate, occasionally at or just outside its lat- and rest on the upper part of the walls or in the roof. In
eral margin. Lateral abdominal setae 6 on segments many areas An. funestus spends the greater part of its
IV and V (6-IV and 6-V) long, usually with about 3 adult life in houses, which has made it one of the most
branches. Pecten commonly of irregular appearance, vulnerable species to control with residual insecticides
with 5–6 long and 6–7 short teeth, arrangement vari- (Gillies and De Meillon 1968).
able, the short teeth and some long ones finely ser- Distribution: Widely distributed in tropical and
rated in basal half, saddle seta (1-X) long and southern Africa
single. Medical importance: An. funestus is generally
Biology: Larvae of An. funestus can mainly be regarded as one of the most important vectors in Tropical
found in bodies of clear water that are either large and and South Africa, and is a vector of bancroftian filariasis
more or less permanent, e.g. swamps, weedy banks of (Evans 1938; Gillies and De Meillon 1968).
streams, rivers, furrows or ditches, protected portions
of lake shore, ponds, etc., especially when weedy, or
water such as seepages, which are fed from underground Anopheles Gambiae Complex
permanent sources, and sometimes in flooded rice
fields (Evans 1938). The larvae show little tolerance This complex comprises, so far, a group of seven
for saline waters and they have never been found in sibling species. Some of them are the major vectors
brackish water in nature; they may stay submerged for of human malaria and other diseases in Sub-Saharan
Africa, others are of little importance or vary in
importance with local conditions. Formerly regarded
as a single species with ecological salt water variants,
the complex has been shown to include at least four
freshwater species, An. gambiae s.s., An. arabiensis,
An. quadriannulatus s.s. (species A), and An. quadri-
annulatus species B, one species which breeds in
highly mineralized water, An. bwambae, and two salt
water species, An. melas and An. merus. No morpho-
logical characters that can universally be applied for
differentiation have been found, and although charac-
ters for separating the species at the population level
have been demonstrated by Coluzzi (1964), the iden-
tification of individual specimens is often impossible
(Gillies and Cotzee 1987). The separation of the sib-
ling species was formerly based on differences in the
banding pattern of polytene chromosomes in the
ovarian nurse cells (Hunt 1973; della Torre 1997) and
Fig. 11.13 Larva of An. funestus, terga I–IV enzyme variation detected via gel electrophoresis
324 11 Africa

(Mahon et al. 1976; Miles 1979), and it is now mainly

based on molecular techniques (Scott et al. 1993;
Fanello et al. 2002). Thus, a description of the gen-
eral morphological characters of females and larvae
is given, followed by a short summary of the bionom-
ics and distribution of the species of the complex. For
further information on the distribution see Coetzee et
al. (2000).
Female: A medium sized species. Proboscis entirely
dark scaled, labellum somewhat lighter. Palps with
3–4 pale rings. When 3 rings are present, the apical
one is broad, including the entire palpomere V and the
apex of palpomere IV. The subapical and basal rings
are much narrower, located at the apices of palpomeres
II and III. The broad apical ring may be interrupted by
Fig. 11.14 Larva of An. gambiae s.s, terga I–IV
a dark area, resulting in the formation of 4 pale rings.
Pedicel with a few pale scales. Vertex with a prominent
frontal tuft of long pale setae projecting forwards. half as long as 2-C, single or with few lateral branches,
Integument of scutum and pleurites of variable colour, postclypeal seta (4-C) very slender and shorter than
usually light brown or greyish. Median area of scutum 3-C, with 1–3 branches. Frontal setae (5-C to 7-C) plu-
covered with creamy or yellowish scales of moderate mose, middle frontal seta (6-C) much shorter than inner
width except near transverse suture, where the scales frontal seta (5-C) and outer frontal seta (7-C) about half
are broad but somewhat transparent. Upper and lower as long as 5-C or less. Prothoracic seta 1 (1-P) without
mesepisternum with groups of 3–5 setae each, 8–13 conspicuous basal tubercle, poorly developed, with
upper mesepimeral setae usually present. Femora, tib- 5–14 branches, 2-P with small basal tubercle, about 1.5
iae, and tarsomeres I of all legs spotted, speckled, or times as long as 1-P, with 10–13 branches, 3-P about
mottled to various extents (Fig. 11.3a). Fore tarsi with half as long as 2-P, single. Palmate seta on abdominal
broad pale rings involving both ends of tarsomeres segment I (1-I) poorly developed, with about 7–11 nar-
I–III, tarsomere IV with a pale ring at apex, tarsomere row undifferentiated leaflets, palmate setae 1-III to
V entirely dark. Hind tarsi with narrow, pale rings at 1-VII fully developed, usually small, with about 14–18
apices of tarsomeres I–IV, tarsomere V usually entirely lanceolate and distinctly shouldered leaflets, the fila-
dark. Wing field largely pale but with much variation ment about 1/2 as long as the blade. Lateral abdominal
of the pale and dark markings. A pale interruption on setae on segments IV–VI (6-IV to 6-VI) split into 2–3
vein R1 (sometimes fused with the preceding pale area) slender branches near base (Fig. 11.14). Tergal plates
within the third main dark area. Pale fringe spots at very small, that on segment V not wider than half the
terminations of all veins, sometimes absent at tips of distance between the bases of the pair of palmate setae
Cu2 and/or A. Additionally a pale fringe spot usually (1-V). Pecten with about 4–5 long teeth regularly alter-
present between Cu2 and anal vein (A) and basal to nating with groups of 3–6 short teeth (arranged more
vein A. Integument of abdomen light brown, mainly irregularly with no definite pattern in An. melas), only
closed with pale setae. Tergum VIII and sometimes the short teeth finely serrated. Saddle seta (1-X)
tergum VII with a variable number of narrow yellow- single.
ish scales, sterna usually devoid of scales.
Larva: Antenna covered with small and inconspicu-
ous spicules. Antennal seta (1-A) short and single, Anopheles (Cellia) gambiae s.s. Giles 1902
inserted below the middle of the antennal shaft. Inner
clypeal seta (2-C) slender, aciculate or with a varying This species is regarded to be currently in the state of
number of fine lateral branches in the distal half. The diverging into two different species, the Mopti (M) and
pair of 2-C inserted wide apart, much closer to 3-C than Savannah (S) strains, although the two strains are still
to each other. Outer clypeal seta (3-C) usually less than considered as a single species (Gentile et al. 2001;
11.2 Species Description 325

della Torre et al. 2005). The genome of An. gambiae Anopheles (Cellia) arabiensis Patton 1905
s.s. was sequenced in 2002, but there is controversy
over the choice of the strain used. Biology: As noted above, no major differences in the
Biology: The larvae may occur in a great variety larval biology of An arabiesis and An. gambiae s.s.
of breeding places, especially in shallow open collec- have been discovered. The females of An arabiesis are
tions of water completely or partially exposed to also highly anthropophilic, but when alternative mam-
direct sunlight, e.g. ground pools, transient rain pools, malian hosts are available, they show a much greater
drains, car tracks, hoof prints around ponds, pools tendency than the females of An. gambiae s.s. to feed
left by receding rivers, water holes and rainwater col- on these animals. In addition, they show a higher ten-
lections in depressions (Gillies and De Meillon 1968). dency to feed and rest outdoors (exophagic, exophilic).
More permanent habitats such as recently flooded In general An arabiensis tends to predominate in arid
rice fields and edges of seasonal swamps are also savannas, whereas An gambiae s.s. is the dominant
occupied by the larvae of this species. In all men- species in humid forest zones (Coetze et al. 2000).
tioned breeding sites they are often associated with Distribution: Tropical and southern Africa, Saudi
the larvae of An. arabiensis. An. gambiae s.s. is capa- Arabia, Yemen
ble of growing very rapidly; under optimal condi- Medical importance: As with An. gambiae s.s.,
tions, the development from the egg to the adult may An. arabiensis is an important vector of malaria wher-
be completed within 6–8 days (De Meillon 1947). ever it occurs.
The females are regarded as being highly anthropo-
phylic and readily bite humans mainly indoors but
also outdoors. The main biting activity takes place Anopheles (Cellia) quadriannulatus s.l.
during the night, particularly from midnight to Theobald 1911
0400 hours. Depending on local populations, the rest-
ing and feeding behaviour is diverse. Resting indoors The sibling species A and B of An. quadriannulatus are
after the blood meal is widespread, but it is also recognised as allopatric members of the Anopheles
known that populations in the West African savannah Gambiae Complex, based on evidence of genetic
show a tendency to fly out of houses after feeding incompatibility between crosses of southern African and
(Gillies and Coetzee 1987). The females take their Ethopian populations. An. quadriannulatus s.s. (species
first blood meal usually 24 h after emergence; a high A) is widespread in southern Africa, whereas An.
proportion of them feed again the same night after quadriannulatus species B occurs in Ethopia (Hunt
oviposition. The dispersal capacity of the females is et al. 1998; Fettene et al. 2002; Fettene and Temu 2003).
considered to be low; usually they are found within Biology: The breeding preferences of the larvae of
1–3 km from their breeding sites. Apart from this, the An. quadriannulatus s.l. are not essentially different
long range transport by planes or ships is well docu- from those of the other freshwater species. The larvae
mented, e.g. the invasion and establishment of the could be found in semi permanent pools in dry river
species in north eastern Brazil in the 1930s, followed beds (Gillies and Cotzee 1987). The females exhibit a
by the most devastating epidemics of malaria in tro- strong zoophilic biting behaviour, e.g. biting of cattle
pical America with > 20,000 fatal cases. A joint erad- and other domestic animals is very common. The bit-
ication campaign finally led to the extinction of this ing activity reaches a peak before midnight and
alien species in Brazil in 1941 (Soper and Wilson decreases towards dawn. This species shows a toler-
1943). ance to relatively cool conditions on highland plateaux
Distribution: Tropical and southern Africa (White 1974).
Medical importance: This species is one of the Distribution: Widespread in southern Africa (An.
most important vectors of malaria in Africa; wherever quadriannulatus s.s.), reported from Mozambique,
it occurs it is responsible for intense disease transmis- South Africa, Swaziland, Uganda, Zambia, Zimbabwe,
sion. Apart from its association with high endemic and Ethiopia (An. quadriannulatus species B).
malaria it is also responsible for epidemics and is a Medical importance: Because of its strong zoophilic
vector of periodic bancroftian filariasis as well (Gillies biting behaviour, this species is not regarded as an
and De Meillon 1968). important vector of malaria.
326 11 Africa

Anopheles (Cellia) bwambae White 1985 trunks and underneath vegetation (Gillies and De
Meillon 1968).
The main characteristic of An bwambae is the excep- Distribution: West African coastal salt marsh areas.
tional broad apical band of the female palps, which Recorded from Angola, Benin, Cameroon, Congo, Cote
includes the entire palpomere V and nearly the apical d’Ivoire, Democratic Republic of the Congo, Equatorial
half of palpomere IV (White 1973, 1985). No further Guinea, Gabon, Gambia, Ghana, Guinea, Guinea Bissau,
morphological characters in the larvae, pupae or eggs Liberia, Madagascar, Mauritius, Nigeria, Senegal, Sierra
exist to enable identification of individual specimens Leone, Togo
(Gillies and Coetzee 1987). Medical importance: Due to a much reduced
Biology: The larvae mainly breed in sun-exposed sporozoite rate compared to An. gambiae s.s. this spe-
ground pools with muddy and polluted water, which is cies plays a minor role in malaria transmission, except
highly mineralized (sulphate, chloride, bicarbonate) and when present in very large numbers (Bryan 1983). An.
derived from hot springs. In the type locality, breeding melas is also capable of transmitting Bancroftian filari-
is intense and continuous throughout the year (Gillies asis (Blacklock and Wilson 1941).
and Coetzee 1987). The females attack humans out-
doors in large numbers, but also enter houses when
human settlements are present. The outdoor resting Anopheles (Cellia) merus Dönitz 1902
sites of the adults are primarily tree trunks and but-
tresses in the forest (White 1973). Biology: The larvae often occur in large brackish
Distribution: Only known from the small area of lagoons, ponds, swamps and pools that are flooded at
the Rift Valley, Uganda spring tides and subsequently diluted by rainfall; the
Medical importance: Compared to An. gambiae water is sometimes dark and shows a high content of
s.s. this species is of minor importance as a vector of organic pollution (Gillies and De Meillon 1968). The
malaria (White 1973). females are regarded as being zoophilic with cattle
being the preferred host, but in the absence of domestic
animals, they readily bite humans indoors and outdoors
Anopheles (Cellia) melas Theobald 1903 and can be caught resting indoors by day in consider-
able numbers. The outdoor resting sites are similar to
An. melas has long been recognised as a variety of An. those of An. melas.
gambiae and is the most distinct member of the com- Distribution: Brackish habitats in eastern Africa,
plex. The integument of the adults is somewhat darker inland as well as coastal. Reported from the Comoros,
than in the freshwater species and the speckling of the Kenya, Madagascar, Mauritius, Mozambique, Somalia,
legs is much reduced. In the larvae, the pecten with the South Africa, Swaziland, Tanzania, Zimbabwe
long and short teeth arranged irregularly with no defi- Medical importance: As with An. melas the impor-
nite pattern separates this species from those of An. tance of An. merus as a vector is limited, but in localities
merus as well as the freshwater species (Gillies and De where it is abundant, it may play a major role in malaria
Meillon 1968). transmission. In addition An. merus can act as a vector
Biology: The larvae occur mainly in mangroves, of Bancroftian filariasis (Bushrod 1981).
salt marshes, lagoons and tidal swamps in pools and
ponds. They are capable of breeding in waters with
very high salinity; the eggs of An. melas show a Anopheles (Cellia) pharoensis Theobald 1901
markedly higher tolerance to desiccation than the
other members of the complex (Gillies and De Female: A pale species of medium size. Proboscis dark
Meillon 1968). The adults usually do not disperse far scaled, palps shaggy in basal portion, with 4 pale rings
from their saline habitats. They are regarded as being at apices of palpomeres II–V, sometimes additional
strongly anthropophilic, biting man indoors and out- pale scales present on dorsal and median surface,
doors. When biting indoors the females usually leave clypeus pale brown to blackish. Pedicel with a few
the habitations soon after the blood meal. The out- small scales, flagellum dark. Vertex with greyish white
door resting sites include shaded earth banks, tree erect scales and a prominent frontal tuft of elongated
11.2 Species Description 327

white scales, occiput covered with dark erect scales. 2 (1-P and 2-P) well developed, arising from a well
Integument of scutum pale greyish, with a darker sclerotized common tubercle. 1-P with the stem slightly
median line and dark bare posterior dorsocentral stripes flattened and sometimes rather elongated, with 20–24
and dark bare oval spots in front, scutum more or less branches and about 3/4 as long as 2-P, 3-P slightly
evenly covered with whitish or greyish scales, setae shorter than 1-P, single. Palmate setae developed on
dark. Scutellum clothed with whitish scales and dark abdominal segments I–VII (1-I to 1-VII), 1-I with
setae. Integument of pleurites usually pale yellowish about 15 leaflets, which usually have well defined
brown, mesepisternum with several spots of whitish shoulders and filaments, but these may be barely indi-
flat scales, prespiracular setae usually very fine, upper cated. Palmate setae on abdominal segments II–VII
mesepimeral setae numerous. Coxae usually with (1-II to 1-VII) of variable shape in the width of the
numerous white scales, femora and tibiae prominently leaflets, number of serrations and length of the fila-
pale scaled on inner surface, otherwise speckled, with ments. Lateral abdominal setae 6 on segments IV–VI
irregular bands, patches or spots of pale scales. Fore (6-IV to 6-VI) with 2 branches. Tergal plates of moder-
and mid tarsi with tarsomeres I and II broadly pale at ate size, the width of those on abdominal segments IV
apices, tarsomeres III usually more narrowly pale api- and V about half the distance between the palmate
cally, tarsomeres IV and V dark or sometimes with setae following them (Fig. 11.15). Pecten usually with
white tips. Hind tarsi with broad pale apical rings on 3–5 long teeth and groups of short teeth in between,
tarsomeres I–IV, tarsomere V entirely pale scaled. short teeth with conspicuous secondary spicules.
Wing veins covered with pale and dark scales forming Saddle seta (1-X) single.
contrasting spots in a variable pattern. Costa (C), usually Biology: The larvae are primarily found in large
with three large dark areas and one small dark apical vegetated fresh water swamps, but also breed along
area, basal 1/5 of costa usually mainly pale, or with 1 lake shores and among floating plants such as Pistia
or 2 small dark spots. Radius (R) similar to costa but and Potamogeton. They are also found in reservoirs,
often with pale interruptions in dark areas and basally rice fields, streams, ditches and overgrown wells
mainly pale, or with dark areas mostly broken up into (Gillies and De Meillon 1968). The females feed pre-
a variable number of small spots. Other wing veins dominantly on domestic animals, but enter houses readily
predominantly pale scaled, number of dark spots vari- at night and bite humans; the main daytime resting sites
able. Wing fringe with pale spots at the terminations of are outdoors, particularly in the vegetation. They start
all the veins, an additional pale spot sometimes present biting in large numbers soon after dusk, the attack con-
in basal portion. Terga II–VII densely clothed with tinuing at a high level until midnight. In arid regions
greyish or yellowish scales, which are more numerous
towards their basal margins, and with prominent lat-
eral projecting tufts of dark scales (Fig. 11.2a). Sterna
of most segments with numerous broad, yellowish and
whitish scales, cerci densely clothed with scales.
Larva: Colour usually green, but often pale yel-
lowish brown, sclerotisation of head capsule extremely
variable. Antenna densely covered with small spicules,
antennal seta (1-A) minute, inserted at about 1/4 from
the base of antennal shaft. Inner clypeal seta (2-C)
long, pinnately branched on distal half, the pair of 2-C
inserted wide apart, the distance between the bases of
the pair of 2-C distinctly larger than the distance
between 2-C and 3-C. Outer clypeal seta (3-C) dendri-
form, usually divided into 2–3 unequal branches near
the base and these subdivided to form about 20–45
ultimate branches. Postclypeal seta (4-C) usually about
half as long as 2-C, with 2–5 branches, frontal setae
Fig. 11.15 Larva of An. pharoensis, terga I–IV
(5-C to 7-C) long and plumose. Prothoracic setae 1 and
328 11 Africa

An. pharoensis is capable of remarkably long migratory (Fig. 11.16) and the larger distal pecten teeth with larger
flights of 29–45 km (Gillies and De Meillon 1968). and fewer (2–3) lateral denticles than in the two other
Distribution: Tropical and southern Africa, Egypt, species. In living larvae of Cx. antennatus the abdominal
Israel, Syria segments III and V with dark pigment granules giving
Medical importance: A well known vector of the abdomen a two-banded appearance to the naked
malaria in Egypt. In tropical Africa, it is of lesser eye, which is absent in the others (Harbach 1988).
importance compared to An. gambiae s.l. and An. Biology: The larvae of Cx. antennatus can mainly be
funestus (Gillies and De Meillon 1968). found in stagnant fresh water bodies, they rarely breed in
polluted water (Hopkins 1952). Common larval habitats
include rice fields, stream pools, springs, ponds, swamps,
Culex (Culex) antennatus (Becker 1903) ditches, seepages, and animal footprints. The breeding
places usually contain emergent vegetation (Harbach
Female: A small brown species with prominent lateral 1988). Females feed primarily on livestock and man.
longitudinal pale stripes on abdominal terga VI and VII. They bite both indoors and outdoors from late afternoon
Proboscis predominantly dark scaled with paler scales on and in the evening and seek resting sites away from
on ventral surface of distal half, palps about 1/5 the buildings (Zimmerman et al. 1985). In suburban areas of
length of proboscis, dark scaled. Antenna blackish, Kinshasa, Zaire Cx. antennatus was recorded as the
pedicel with some small scales or setae on mesal side. major nuisance species (Karch et al. 1993).
Head with numerous erect forked dark scales, curved Distribution: Egypt, Israel, Ethiopian Region south
decumbent scales mostly pale yellowish. Integument of to Angola and Bechuanaland, Iran
scutum brown, scutum clothed with reddish to golden Medical importance: Cx. antennatus has been
brown curved scales with some pale yellowish scales on found naturally infected with West Nile virus in Egypt
front margin and prescutellar area, scutellum with very (Taylor et al. 1956) and Rift Valley Fever virus in
fine curved pale yellowish scales on all lobes. Integument Nigeria (Lee 1979).
of pleurites brownish yellow, patches of pale scales
present on upper and lower part of mesepisternum and
upper and anterior part of mesepimeron, pleurites with
6–9 prealar setae, 4–5 upper mesepisternal setae, 5–9
lower mesepisternal setae, 5–8 upper mesepimeral setae,
and 1 lower mesepimeral seta. Femora and tibiae mainly
dark scaled on anterior surface, pale posteriorly, hind
femur mainly pale scaled, with dorsal line of dark scales
gradually widening to the apex, all tarsi dark scaled,
somewhat paler scales ventrally. Wing veins entirely
dark scaled, rarely with some pale scales at base of costa
(C), haltere pale, more or less same colour as pleurites.
Terga II–VII almost entirely brown scaled, terga II–V
with small basolateral patches of pale scales, which are
usually not visible from above, terga VI and VII with
prominent lateral longitudinal pale stripes, tergum VIII
largely pale scaled (Fig. 11.9b). Venter entirely pale
scaled, sternum VIII with lateral patches only, median
area devoid of scales.
Larva: Very closely resembling the larvae of Cx.
perexiguus and Cx. univittatus. In Cx. antennatus the
labral seta (1-C) is longer, the inner (5-C) and espe-
cially median (6-C) frontal setae nearly always have
2 branches, rarely 3-branched. The siphon is generally
slightly longer, siphonal index usually more than 6.0 Fig. 11.16 Larva of Cx. antennatus
11.2 Species Description 329

Culex (Culex) univittatus Theobald 1901 ventrolateral tufts with 2–4 branches (Gutsevich et al.
1974). The two basalmost tufts (1a-S and 1b-S) are
The typical form of this species may be recognised attached within or close to the pecten. The tufts are
without much difficulty by the presence of an anterior inserted more laterally toward the apex. The main tra-
pale stripe on the mid femur stretching over its whole cheal trunks are broad with oval cross section. The anal
length (Jupp 1971), a similar stripe on the hind tibia papillae are variable in length; the dorsal pair is slightly
and the presence of postspiracular and prealar scale longer than the ventral pair (Hopkins 1952).
patches. The species is closely related to Cx. perex- Biology: The larvae are most common in pools in
iguus (see description of European species) and exhib- marshy land and at the edges of swamps but occur also
its a very similar external morphology in all life stages. in stagnant or semistagnant streams and ditches, bor-
In Africa, adults could be confused with Cx. antenna- row pits, etc. Vegetation is usually present, but there is
tus, Cx. neavei, Cx. quasiguiarti and Cx. simpsoni seldom dense shade. It prefers fresh water but accord-
(Edwards 1941). ing to Gutsevich et al. (1974) could develop in slightly
Female: Legs largely dark, front and mid femora saline water (with 0.2% of salt and pH of 7.2 to 9.7) or
and tibiae in many specimens with vague lines of white even in strongly saline waters of up to 1% (Senevet
scales extending their whole length anteriorly (Fig. 1947). Mara (1945) reported larvae from man-made
11.8b). The hind femur also bears white scales anteri- containers at altitudes above 2,000 m in Eritrea in
orly on the basal 1/2 continued as a narrow pale stripe association with those of Ae. aegypti, Cx. p. quinque-
to near the apex (Fig. 11.8a). Hind and sometimes the fasciatus, Cx. laticinctus and Cs. longiareolata.
mid tibia with a line of whitish scales extending most Gutsevich et al. (1974) stated that females feed mainly
of the length on the anterior surface but separate from on birds, while Jupp (1996) reported a great variation
the conspicuous white spot at the tip (Edwards 1941; in anthropophily between populations. According to
Sirivanakarn 1976). The abdominal terga have pale Lewis (1947), Cx. univittatus and Cx. neavei have dif-
basal bands that are rather broad, slightly convex on ferent biting habits in the Sudan, the latter being far
terga II–V and narrow and even in width on the rest of more anthropophilic than the former, but De Meillon
the terga, confluent with basolateral patches but may be (1947) found Cx. univittatus to be a persistent biter of
disconnected and sometimes reduced to small median humans and monkeys in Bechuanaland.
basal spots or rarely absent. The sterna are creamy-
white scaled, usually with dark apicolateral patches and
a dark median line (Jupp 1996).
Larva: Besides the great similarity to Cx. perexiguus
the larva resembles those of Cx. decens, Cx. tritaenio-
rhynchus and Cx. antennatus. From Cx. decens it may
be separated by its shorter siphon and the possession of
two branches of abdominal setae 6 on segments III–VII
(6-III to 6-VII), from Cx. tritaeniorhynchus by the much
shorter siphon and the fact that the antennal seta 1-A is
inserted beyond 2/3 (at about 3/4) from the base of the
antennal shaft, and from Cx. antennatus by the fact that,
in the latter species, the inner frontal seta (5-C) is nearly
always 2-branched and the pecten teeth have the lateral
denticles larger and fewer (2–3 against 3–5) (Hopkins
1952). The siphon is usually long and slender, and the
siphonal index may vary between 5.9 and 7.6, a higher
index corresponding to larger specimens. The number
of pecten teeth is 10–14, each tooth with 3–5 lateral den-
ticles, spreading little beyond the basal 1/4 of the siphon
(Fig. 11.17). The most distal tooth may be widely
spaced. The siphonal seta (1-S) consists of 5–6 pairs of Fig. 11.17 Larva of Cx. univittatus
330 11 Africa

Distribution: Cx. univittatus is common throughout Biology: There is a great similarity between Ma.
a large part of the Afro-tropical Region with the excep- africana and Ma. uniformis in appearance and behav-
tion of the forested areas (Edwards 1941; Harbach iour of biting, mating and oviposition. Further­more, the
1988) two species often occur together in nature (Laurence
Medical importance: Despite the statement that 1960). The breeding places are mainly the same, Ma.
females mainly feed on birds, Gutsevich et al. (1974) africana has presumably a slightly more marked prefer-
reported Cx. univittatus to be an important vector of ence for moderately clean water. Larvae are found in
West Nile virus in Asia but this most probably applies permanent water habitats with floating and emergent
to Cx. perexiguus (Reuben et al. 1994). In South Africa, vegetation (Hopkins 1952). Eggs are laid in compact
Cx. univittatus is a primary vector of both Sindbis and masses of about 150 eggs, each attached to the ventral
West Nile viruses (Jupp 1996). surfaces of leaves of aquatic plants, mainly of water let-
Notes on systematics: Jupp (1971) resurrected Cx. tuce (Pistia stratiotes) (Horsfall 1955). Females are
neavei Theobald 1906 to species status from Cx. univit- vicious biters, particularly at night, and they readily feed
tatus var. neavei (Edwards 1922). Cx. univittatus and Cx. on man and other mammals outdoors and inside dwell-
neavei are morphologically and biologically distinct all- ings (Muspratt 1955; Laurence 1960). Ma. africana is
opatric species in South Africa. At two of three localities everywhere recognised as a pestiferous mosquito;
of overlapping of the distribution ranges, few intermedi- human blood is its preferred blood meal (Kerr 1933).
ates were detected, but it was considered that these were Distribution: Tropical and southern Africa
accidental hybrids and that the two species largely coex-
ist at these places without interbreeding. Reproductive
isolation was due to differences in mating behaviour  ansonia (Mansonioides) uniformis
M
(Jupp 1971) (see also comments under Cx. perexiguus). (Theobald 1901)

Female: A medium sized mosquito of yellowish brown

 ansonia (Mansonioides) africana
M appearance, legs with many pale markings and ringed
(Theobald 1901) tarsi. It closely resembles Ma. africana (for differ-
ences see under the latter species). Proboscis shorter
Female: It closely resembles Ma. uniformis differing than fore femur, mottled but mostly pale on basal 3/4
from the latter in having the pale scales of the scutum and predominantly dark apically. Clypeus pale brown,
aggregated into spots but not forming stripes. The palps about 1/3 as long as the proboscis, covered with
scutum usually bears three groups of pale greyish
scales laterally, on the anterior and posterior submedian
areas and the third and largest spot above the wing
root, usually another patch of greyish scales is present
in front of the prescutellar space. In Ma. africana the
white markings of the femora are more sharply defined
and the tibiae also have distinctly defined white spots
(Fig. 11.12a). The short stout spines along the apical
margin of tergum VIII differ slightly in arrangement
between the two species. In Ma. africana the lateral
spines are straight and more widely separated from the
median ones, sternum VIII with several small lobes,
not broadly bilobed as in Ma. uniformis.
Larva: Nearly identical with that of Ma. uniformis,
only separable from the latter by the form of seta 3 on
abdominal segment VIII (3-VIII), which usually is
long and has 2 branches in Ma. uniformis, while that
of Ma. africana is much shorter and has 3–5 branches
(Fig. 11.18). Fig. 11.18 Larva of Ma. africana
11.2 Species Description 331

mixed white, yellow and dark scales, tip with whitish of antenna. Ocular area covered with anteriorly directed
scales. Pedicel yellowish brown, with several dark denticles. Labral seta (1-C) long and conspicuous.
short setae on ventromesal side. Vertex covered with Postclypeal seta (4-C) with 2–4 branches, inner frontal
pale narrow curved scales and brown erect forked seta (5-C) with 2–5 branches, both very small and dif-
scales, whitish broad scales laterally along the eye ficult to detect. Median frontal seta (6-C) also small,
margin. Integument of scutum brown, scutum covered with 4–9 branches, outer frontal seta (7-C) larger, usu-
with narrow golden and pale scales, pale scales often ally with 5–10 branches. Prothoracic seta 1–3 (1-P to
with a greenish tint and forming broad continuous 3-P) long, reaching slightly beyond anterior margin of
submedian stripes. Prescutellar dorsocentral area with head, 1-P with 2 branches, 2-P and 3-P single.
pale scales, prescutellar area bare. A few pale scales Abdominal seta 6 on segments I–VI (6-I to 6-VI) sin-
scattered in anteromedian area, 3–5 pairs of acros- gle. Comb usually with 2 scales, individual scale long
tichal setae on anterior part of scutum. Scutellum and apically rounded, without fringe of small spines.
brown, each lobe with pale narrow curved scales and Seta 3 on abdominal segment VIII (3-VIII) always
5–8 long brown setae, each lateral lobe with 1–4 addi- long and with 2 branches (Fig. 11.19). Siphon short
tional short setae. Postpronotum with white narrow and conical, heavily sclerotized beyond the middle,
curved scales and 7–14 postpronotal setae arranged in modified for piercing tissues of plants, siphonal seta
a single row. Integument of pleurites brown, patches (1-S) with 2 subequal branches arising before the heav-
of white broad scales on propleuron, upper and lower ily sclerotized part, pecten absent. Anal segment lon-
posterior mesepisternum and upper mesepimeron. ger than wide, completely ringed by the saddle, saddle
Pleural setae pale yellowish brown, located on seta (1-X) short, with 3–6 branches, inserted well
propleuron, postspiracular area, along upper and pos- before the posterior margin of the saddle. Upper and
terior margins of mesepisternum and upper part of lower anal setae (2-X and 3-X) about the same length,
mesepimeron. A row of 2–5 lower mesepimeral setae multiple branched. Ventral brush well developed, with
along the anterior margin in the middle of mesepim- 10–11 cratal setae (4-X) and 2–4 small precratal setae
eron. Fore and mid coxae with both dark and pale (4-X) piercing the saddle. Anal papillae shorter than
scales, hind coxa without scales or with only a few the saddle, blunt ended.
pale scales at apex. Hind legs with femora mostly pale Biology: The larvae of Ma. uniformis are primarily
scaled on basal half (Fig. 11.12b), otherwise dark found in open swamps not shaded by trees, especially
scaled with mottling and patches of pale scales, tibiae lake shore swamps, and in swampy rivers. They
likewise, fore and mid tarsomeres I–III and hind tar- may also be encountered in large natural ponds and
someres I–V with broad pale basal rings, tarsomeres I
of all legs with median pale ring as well. Wing veins
mottled with very broad and asymmetrical dark and
yellow scales, fringe scales slender and all dark.
Haltere with dark scaled knob. Tergum I with a median
patch of yellow scales, occasionally intermixed with a
few dark scales, remaining terga mostly dark scaled
with some mottling and pale lateral patches, tergum
VIII with many short stout spines along apical mar-
gin, lateral spines curved and slightly separated from
the median ones. Sterna mostly pale scaled, sternum
VIII bilobed, lobes largely rounded.
Larva: Head distinctly broader than long. Antenna
at least 1.5 times as long as the head, with an indistinct
dark ring at base and another at level of origin of anten-
nal seta (1-A), antennal shaft with numerous spicules.
Antennal seta (1-A) inserted at basal 1/3 of shaft, with
10–18 branches, A-2 and A-3 inserted at apical 1/3 of
antennal shaft, long and reaching distinctly beyond tip Fig. 11.19 Larva of Ma. uniformis
332 11 Africa

slow moving streams and in old overgrown burrow (Stojanovic and Scott 1966). The females feed ­readily
pits (Hopkins 1952; Tanaka et al. 1979). They have on humans as well as on a wide variety of mammals,
the unique larval structure of a piercing siphon which the flight range of the adults is limited to about
allows them to attach to a wide range of aquatic 3–6 km making this species more of a nuisance to
grasses, sedges and aquatic plants such as water hya- those living near fresh water areas. Ma. uniformis can
cinth (Eichhornia crassipes) and water lettuce (Pistia prove a major pest problem in parts of Africa and
stratiotes). With the modified siphon they pierce northern Australia (Russell 1996).
stems and roots of aquatic vegetation in order to Distribution: Ethiopian, Oriental and Australasian
obtain oxygen. The eggs are attached to the ventral Regions, Japan
side of leaves of aquatic plants. Adults are stenoga- Medical importance: In the tropical region the
mous and mate readily in small cages (Laurence species is the primary vector of Wuchereria bancrofti
1960). The first blood meal is taken approximately (Bancroftian filariasis) and Brugia malayi (Malayan
24 h after emergence and immediately after each ovi- filariasis) as well as Chikungunya fever (Horsfall 1955;
position. Ma. uniformis females are more aggressive Stojanovich and Scott 1966). Ross River virus (RR)
during the night but will feed during the day in pro- has been isolated from wild caught Ma. uniformis in
tected or shaded areas, they enter houses only to feed Northern Australia (Russell 1993).
Chapter 12
Asia

In addition to the anopheline species that were included [Tanakaius togoi], a possible vector of W. bancrofti,
in the key and descriptions for the Asian continent, Brugia malayi, Dirofilaria immitis and Japanese
many others could also be considered as primary encephalitis (JE) virus (Tanaka et al. 1979). Many
malaria vectors but with a relatively restricted distribu- other Aedes and Ochlerotatus species are widespread
tion (An. aconitus from India to Indonesia, An. arabi- noxious pests in temperate Asia such as Ae. cinereus1,
ensis on the Arabian Peninsula, An. sacharovi1 from Ae. vexans1, Oc. caspius1, Oc. communis1, Oc. dorsa-
the Middle East to Afghanistan, An. sergentii1 from the lis1, Oc. excrucians1, Oc. fitchii, Oc. hexodontus1, Oc.
Middle East and Arabian Peninsula to Pakistan, An. impiger1, Oc. nigripes1, Oc. pionips1, Oc. punctor1, Oc.
superpictus1 from the Middle East and Central Asia), sticticus1, Oc. vigilax (Gutsevich et al. 1974). Most of
or widely distributed secondary vectors such as the day them are described in Chap. 10 and should be identi-
biting An. pulcherrimus (from the Middle East through fied using the key for European mosquitoes
Central to South and East Asia) (Gutsevich et al. 1974; (Chaps. 6–8).
Anonymous 1999, http://www.wrbu.org), or even pests The notorious pest and dengue vector species
of a different territorial scale (An. superpictus, An. pul- Ae. aegypti1 [Stegomyia aegypti] and Ae. albopictus1
cherimus). An. multicolor1 is considered to be of pri- [Stegomyia albopicta] are widespread from the Middle
mary importance for Asia, hence is included in the key East to Southeast Asia, China and Japan, and are also
but described in Chap. 9. included in the key. In addition, mosquitoes of the Oc.
In South, Southeast and East Asia, females of niveus [Downsiomyia nivea] subgroup could be impor-
Armigeres subalbatus may bite voraciously through- tant dengue vectors in the Oriental Region (Rueda
out the day and may be involved in the transmission of 2004).
Wuchereria bancrofti, the causative agent of Mansonia females (Ma. annulata, Ma. indiana and
Bancroftian filariasis (La Casse and Yamaguti 1950; Ma. uniformis) readily bite man and can also success-
Thurman 1959; Tanaka et al. 1979). Some members of fully transmit B. malayi (Carter 1950; Wharton 1962).
the genus, such as Ar. aurolineatus, Ar. malayi, Ar. They are widely distributed through South, Southeast
annulipalpis and Ar. flavus, are quite widespread, but and East Asia. Ma. uniformis is included in the key as it
many others are important pests of limited distribution, is the most widespread and significant pest species in
especially in coconut growing areas. They are primar- the mosquito fauna of three continents (Africa, Asia
ily forest mosquitoes but some members of the genus and Australia – AAA). The closely related Cq. richiar-
show potential for becoming domestic pests dii1 readily attacks man across the Middle East and
(Macdonald 1960; Lee et al. 1988). Because of their Central Asia (Gutsevich et al. 1974).
important pest status, their relatively restricted distri- Together with the most important Asian Culex mos-
bution and the strong similarities between many species, quito, Cx. tritaeniorhynchus, which is described below,
they are included in the key within the genus Armigeres. the cosmopolitan human pests Cx. p. pipiens biotype
Another day biter worth mentioning is Oc. togoi molestus1 (also a vector of Sindbis and West Nile
viruses, and primary vector of periodic Bancroftian
1
Species described in Chaps. 9 and 10 concerning European filariasis) and Cx. p. quinquefasciatus1 (a primary vec-
mosquitoes. tor of W. bancrofti, vector of avian malaria, and dog

N. Becker et al., Mosquitoes and Their Control, 333

DOI 10.1007/978-3-540-92874-4_12, © Springer-Verlag Berlin Heidelberg 2010
334 12 Asia

heartworm) are also included in the key (Sirivanakarn Thailand (Bram 1967a) and Cx. vishnui is an important
1976; Harbach 1988). The same is true for the primar- vector of JE (Sirivanakarn 1976).
ily bird and pig feeding bridge vector of AAA distribu- For further reading on the morphology, identification,
tion, Cx. sitiens, responsible for transmission of biology, distribution and disease vector status of the
Japanese B encephalitis and B. malayi in Thailand species mentioned, the reader is referred to Christophers
(Harbach 1988). (1933), Barraud (1934), Reid (1953), Stojanovich and
Two zoophilic Culex species distributed in South, Scott (1965a,b), Bram (1967a), Cagampang-Ramos
Southeast and East Asia will readily bite man in the and Darsie (1970), Mattingly (1971), Huang (1972,
absence of an animal host. Cx. gelidus is a potential 1979), Smith (1973), Sirivanakarn (1976), Tanaka
vector of Japanese encephalitis (JE) in Malaysia and et al. (1979), Harrison (1980), Rattanarithikul (1982),

Harbach (1988), Darsie and Pradhan (1990, 1991), Reuben et al. (1994), Anonymous (1999), Ree (2003), Rueda
(2004).

12.1 Key to Asian Female Mosquitoes

1 Palps as long as or slightly shorter than proboscis. Scutellum evenly rounded or slightly trilobed and uni-
formly setose (Fig. 12.1a). Abdominal terga and sterna completely or largely missing scales – Proboscis is
neither strongly recurved nor tapering towards apex. Anopheles............................................................................. 2
Palps distinctly shorter than proboscis. Scutellum trilobed, setae arranged in three sets (Fig. 12.1b).
Abdominal terga and sterna uniformly and densely covered with scales. – Proboscis is neither strongly recurved

Fig. 12.1 Scutellum of: (a) Anopheles sp.; (b) Aedes sp.

nor tapering towards apex. Tip of proboscis is neither swollen, upturned nor hairy. Antenna long, flagellomeres slender, cylin-
drical. Scutum without narrow median longitudinal stripe of broad decumbent silvery white scales. Prespiracular setae
absent. Postnotum without patch of setae. Tarsomere I of fore legs usually shorter than tarsomeres II–V together. Tarsomere
IV of fore legs not reduced, distinctly longer than broad. Anal vein (A) evenly curved, ending distinctly beyond furcation of
cubitus (Cu)................................................................................................................................................... 12
2 (1) Costa (C) with two pale spots excluding humeral and basal spots (these spots usually not present in An.
lesteri and An. sinensis) subgenus Anopheles (Fig. 12.2a). – Palps with pale rings. Basalmost pale ring not

Fig. 12.2 Wing of: (a) An. hyrcanus; (b) An. multicolor
12.1 Key to Asian Female Mosquitoes 335

broader than others. Hind femur without pale ring. Femorotibial joint of hind legs without tuft of black and white scales.
Apical pale rings on hind tarsi narrow, tarsomere IV usually without basal pale ring. Basal 1/4 of costa completely dark
scaled or speckled with pale scales. Pale apical fringe spot usually present. Anal vein (A) pale with two dark spots.
An. hyrcanus group................................................................................................................................ 3
Costa with at least four pale spots in addition to humeral and basal spots (Fig. 12.2b). Subgenus Cellia........ 4
3 (2) Mid coxa with a distinct upper patch of pale scales. Pale apical fringe spot quite large, stretches at least
from R1/R2 to R4+5. Basal dark spot on cubitus (Cu) small, separated by its own length from middle
dark spot on anal vein (A). Pale fringe spot at the end of cubitus (Cu2) usually present (Figure 12.3a). –
Wing pattern blurred. Some pale scales scattered on R1 between subcostal and preapical pale spots. Apical dark spot on anal
vein (A) longer than that on Cu2........................................................................................... An. sinensis (p 340)
Mid coxa without upper patch of pale scales (a few scales occasionally present). Pale apical fringe spot
usually very small, stretches between R1/R2 and R3. Basal dark spot on cubitus (Cu) fairly long, approach-

Fig. 12.3 Wings of: (a) An. sinensis; (b) An. lesteri Fig. 12.4 Hind leg of: (a) An. sundaicus; (b) An. minimus

ing to within its own length or less of the middle dark spot on anal vein (A). Pale fringe spot at the end of
vein Cu2 absent (Fig. 12.3b)..............................................................................................An. lesteri (p 339)
4 (2) Femora and tibiae speckled with pale and dark scales to a variable extent, sometimes spotted and ringed
(Fig. 12.4a)................................................................................................................................................... 5
Femora and tibiae not speckled (Fig. 12.4b). – Fore tarsomeres entirely dark-scaled or with very narrow pale
rings........................................................................................................................................................ 8

Fig. 12.5 Hind tarsus of: (a) An. maculatus; (b) An. sundaicus Fig. 12.6 Palps and proboscis of:
(a) An. dirus; (b) An. stephensi; (c) An. sundaicus
336 12 Asia

5 (4) Hind tarsomere V and apical part of IV entirely pale-scaled (Fig. 12.5a). – Palps with three distinct pale rings.
Vein R2 short, usually less than twice the length of vein R2+3. Vein R4+5 with two dark spots. Abdominal terga II and III
without scales or with some pale curved and/or narrow spatulate scales on posteromedian area. Tergum IV without scales or
with a few posteromedially. Terga V–VII with numerous pale scales but occasionally only on tergum VII. Dark scales usually
present only on last two terga. Posterolateral corners of terga VII and/or VIII, rarely also tergum VI, with patches of dark
scales. Abdominal sterna without scale tufts....................................................................... An. maculatus (p 345)
Hind tarsomeres III–V predominantly dark scaled, usually with narrow pale apical rings (Fig. 12.5b)......... 6
6 (5) Palps with four pale rings (Fig. 12.6a). – Apical and subapical pale rings unequal in width. Hind legs with tibiotar-
sal joint broadly and conspicuously ringed with white scales...................................................... An. dirus (p 342)
Palps with three pale rings (Fig. 12.6b).......................................................................................................7
7 (6) Palps with apical and subapical pale rings equal in width. Apart from rings palps usually speckled with
pale scales (Fig. 12.6b).................................................................................................. An. stephensi (p 347)

Fig. 12.7 Scutum of: (a) An. multicolor; (b) An. culicifacies Fig. 12.8 Wing of: (a) An. culicifacies; (b) An. fluviatilis;
(c) An. minimus

Subapical pale ring much narrower than apical and equal to basal ring. Palps usually not speckled
(Fig. 12.6c)..............................................................................................................An. sundaicus (p 348)
8 (4) Median, fossal and supraalar areas of scutum covered with narrow but distinct creamy scales, somewhat
broader on fossae (Fig. 12.7a). – Apex of palps dark. Fore tarsomeres with narrow apical pale rings nearly twice the
width of tarsomere. .................................................................................................... An. multicolor (p 182)
Median area of scutum without scales (setae present), or with slender seta-like pale scales at postacrostichal
and prescutelar areas (Fig. 12.7b). – Apex of palps pale. Legs entirely dark scaled, or some tarsomeres with apical
pale rings or dorsal patches not wider than tarsomere width.......................................................................................... 9
9 (8) Base of radius (R) below humeral cross vein (h) with a patch of grey or black scales (Fig. 12.8a).
– Subapical dark ring on palps much wider than apical pale ring. Fore tarsomeres dark scaled. Vein R4+5 usually dark
except at base...........................................................................................................An. culicifacies (p 341)
Base of radius (R) below humeral cross vein (h) with only white or yellowish scales (Fig. 12.8b,c). – Vein
R4 +5 usually mainly pale scaled.........................................................................................................................10
12.1 Key to Asian Female Mosquitoes 337

Fig. 12.9 Palps and proboscis of: (a) An. fluviatilis; (b) An. minimus; (c) An. flavirostris

10 (9) Palps with subapical dark ring wider than apical pale ring and 3–5 times wider than narrow subapical
pale ring (Fig. 12.9a)............................................................................................... An. fluviatilis (p 344)
Palps with subapical dark ring variable, from slightly wider (mostly twice) than apical and subapical
pale rings, to much smaller or even absent (Fig. 12.9b). – Costa usually with presector pale spot or at least some
pale scales basal to sector pale spot. Wing fringe without pale spot at termination of anal vein (A). ...........................11

Fig. 12.10 Lateral view of thorax of: (a) Culex sp.; (b) Mansonia sp.

11 (10) Proboscis usually entirely dark scaled (Fig. 12.9b). Fore tarsomeres I–IV with very small dorsoapical
pale patches or pale rings (mainland Southeast Asia and Indian subregions).......... An. minimus (p 346)
Proboscis usually with ventral pale scale patch (Fig. 12.9c). Fore tarsomeres entirely dark scaled
(confined to Philippines and Indonesia)................................................................ An. flavirostris (p 343)
12 (1) Postspiracular setae absent (Fig. 12.10a). All tarsal claws simple. Pulvilli present, well developed (pad-
like). – Antenna with flagellomere I about as long as flagellomere II. Erect forked scales not restricted to occiput, numer-
ous on vertex too. Scutellum with all scales narrow. Wing scales narrow. Alula with narrow fringe scales. Abdomen
rounded apically, cerci short, hardly visible. Culex......................................................................................... 13
Postspiracular setae usually present (Fig. 12.10b) and/or claws on fore legs with subbasal tooth. Pulvilli
absent or not well developed (hair-like)................................................................................................. 15
338 12 Asia

Fig. 12.11 Proboscis of: (a) Cx. sitiens; Fig. 12.12 Mid leg of: (a) Cx. sitiens; (b) Cx. tritaeniorhynchus
(b) Cx. p. quin­quefasciatus

13 (12) Proboscis with distinct broad median pale ring (Fig. 12.11a). Lower mesepimeral setae absent.
Tarsomeres of all legs with narrow, indistinct basal and apical pale rings. Rings usually more distinct at
bases of hind tarsomeres I–III................................................................................................................ 14

Fig. 12.13 Proboscis of: (a) Armigeres sp.; (b) Aedes sp.

Proboscis without pale ring in the middle but often with a pale midventral area (Fig. 12.11b).
Usually one lower mesepimeral setae present. Tarsi all dark. – Postspiracular patch of pale scales
absent.................................... Cx. p. pipiens biotype molestus and Cx. p. quinquefasciatus (p 277, 278)
14 (13) Anterior surface of femora (particularly mid femur) with numerous scattered pale scales (Fig. 12.12a).
Narrow apical bands and/or small median apical patches of pale scales sometimes present on tergum
VII and/or VIII............................................................................................................. Cx. sitiens (p 366)
Anterior surface of mid femur without scattered pale scales (Fig. 12.12b). Tibiae dark anteriorly. Tergum
VII and/or VIII without apical bands or patches. – Anterior and median part of scutum dark scaled, pale scales
present only near scutellum............................................................................. Cx. tritaeniorhynchus (p 349)

Fig. 12.14 Wing scales of: (a) Mansonia sp.; (b) Aedes sp.
12.1 Key to Asian Female Mosquitoes 339

15 (12) Proboscis laterally compressed with apical 1/3 slightly curved downwards (Fig. 12.13a). – Postspiracular
scales present. Postspiracular setae present and palps less than 1/3 of proboscis or postspiracular setae absent and palps at
least half as long as proboscis.......................................................................................................... Armigeres
Proboscis more or less straight and cylindrical (Fig. 12.13b). – Postspiracular area bare.......................... 16
16 (15) Claws all simple. Wing scales mostly broad and many conspicuously asymmetrical (Fig. 12.14a).
Abdomen rounded apically, cerci short, hardly visible. Mansonia – Erect forked scales numerous, not restricted

Fig. 12.15 Head of: (a) Aedes (Stegomyia) sp.; Fig. 12.16 Scutum of: (a) Ae. aegypti; (b) Ae. albopictus
(b) Aedes (Ochlerotatus) sp.

to occiput, decumbent scales narrow. Submedian area of scutum with a pair of continuous pale longitudinal
stripes. Central area of scutum with dorsocentral stripes of pale scales. Anterior surfaces of mid and hind tibiae with
mostly confluent creamy white patches. Basal half of hind femur paler, dark scales restricted to upper anterior
surface......................................................................................................................Ma. uniformis (p 330)

erect scales numerous, not restricted to

Claws usually with subbasal tooth. Wing
occiput (Fig. 12.15b). Abdominal segment
scales mostly narrow, if broad then not con-
VII usually distinctly narrower than VI. Cerci
spicuously asymmetrical (Fig. 12.14b).
usually long, easy visible. Aedes,
Abdomen tapering apically, gradually from
Ochlerotatus....................................................
segment V–VII or segment VII distinctly nar-
(see key for Europe) (p 95)
rower than VI. – Pleural scale patches well devel-
18 (17) Scutum with a white acrostichal stripe extend-
oped..................................................................
ing from the anterior margin to the beginning
17
of the prescutellar area, where it forks to end at
17 (16) Decumbent scales of vertex largely broad.
the anterior margin of scutellum (Fig. 12.16b)..
Erect scales not numerous, restricted to
Ae. albopictus (p 201)
occiput (Fig. 12.15a). Cerci relatively short.
Scutum without acrostichal stripe on anterior
– Terga with white basolateral patches and at least
part, but with two narrow white dorsocentral
some with white basal bands. Aedes subgenus
stripes separated from anterior margin. Lateral
(Stegomyia).....................................................
white stripes broad, continuing over trans-
18
verse suture to the end of scutum, lyre shaped
Decumbent scales of vertex largely narrow
(Fig. 12.16a)....................................................
and/or, if scales of vertex are largely broad,
Ae. aegypti (p 198)
340 12 Asia

lower, sunnier water than those of An. lesteri. As a

result, An. sinensis appears 2-4 weeks earlier than An.
lesteri, which is particularly abundant late in the sea-
son when the rice plants shade the water (Wilkerson
et al. 2003). The females of An. lesteri readily enter
houses to bite man and seek for resting sites; the spe-
cies may hibernate in both the egg and adult stages.
Distribution: Borneo, China, Guam, Japan, Korea,
Malaysia, Philippines, Thailand, Vietnam.
Medical importance: An. lesteri is considered as
the main vector of malaria in eastern and southern
China, Japan and Korea (Harrison and Scanlon 1975;
Tanaka et al. 1979; Wilkerson et al. 2003).

 nopheles (Anopheles) sinensis

A
Wiedemann 1828
Fig. 12.17 Larva of An. lesteri, terga I–IV
Female: Proboscis dark scaled, palps slightly shorter
than proboscis, predominantly dark scaled, with white
scales at tip and 3 narrow, sometimes indistinct pale
12.2 Species Description rings at the joints of palpomeres II–III, III–IV and
IV–V. Pedicel dark brown, with few small pale scales,
 nopheles (Anopheles) lesteri
A clypeus brown to dark brown, with a tuft of dark
Baisas and Hu 1936 brown scales laterally. Vertex with pale erect scales on
median part and dark erect scales laterally, frontal tuft
Female: Very similar to that of An. sinensis, it differs with long pale scales projecting forward, numerous
from the latter chiefly by the combination of the fol- dark setae along eye margin. Integument of scutum
lowing characters: costa (C) usually entirely dark on light brown, usually with a dark brown median stripe
basal half, without scattered pale scales, humeral cross extending backwards to prescutellar area and dark
vein (h) bare; median area of vein R4+5 with fewer dark dorsocentral stripes on anterior half. Scutum sparsely
scales or often entirely pale, pale fringe spot at termi- covered with very fine curved yellowish scales and
nation of vein Cu2 usually absent (Fig. 12.3b). Mid longer stout golden setae, scutellum clothed with long
coxa often bare of scales, if few scales are present, not yellowish setae and small fine curved pale scales.
forming a distinct patch as in An. sinensis. Integument of pleurites light brown to greyish, usu-
Larva: Almost indistinguishable from that of An. ally with darker areas forming an upper and lower
sinensis, lateral abdominal seta 6 on segments IV and dark band, sometimes with a few scales on lower
V (6-IV and 6-V) usually with 3 branches (Fig. 12.17), mesepisternum, lower mesepimeral setae absent. Legs
6-III rarely with > 20 branches, 6-I usually with < 21 dark brown on dorsal surface, pale ventrally, fore
branches, but characters are variable. Seta 9-II with femur swollen towards the base. Coxae, particularly
5–9 branches (10–18 in An. sinensis). mid coxae, with a distinct patch of pale scales. Tarsi
Biology: Larvae are found in cool, clean, ground predominantly dark scaled, fore and mid tarsomeres
water habitats that include marshes, ground pools, I–III and hind tarsomeres I–IV with narrow apical
ponds, rice fields and other collections of water. pale rings, which are sometimes incomplete, rings on
Compared to the larvae of An. sinensis, those of An. les- fore tarsi usually broader than those on mid and hind
teri seem to prefer places which are cooler and more legs. Wing veins covered with pale and dark scales
shaded (Tanaka et al. 1979). This can be observed forming contrasting spots. Costa (C) frequently with
especially in rice fields where both species are often scattered pale scales on basal half, with subcostal and
found together. Larvae of An. sinensis tolerate shal- preapical pale spots, subcostal pale spot includes costa
12.2 Species Description 341

mented and rather large, leaflets slightly serrated in

apical part with sharply pointed tips. Lateral abdomi-
nal setae 6 on segments IV and V (6-IV and 6-V) usu-
ally with 2 branches. Tergal plate on segment VIII
large, about 2/3 as long as wide. Pecten with 7–9 long
teeth and about double that number of short teeth.
Saddle seta (1-X) as long as or longer than the saddle,
upper and lower anal setae (2-X and 3-X) multiple
branched, ventral brush with about 9 pairs of cratal
setae (4-X). Anal papillae tapering, of variable length
(Fig. 12.18).
Biology: Larvae are found in shallow habitats, usually
with fresh water and emergent vegetation and exposed
to direct sunlight, they are characteristic of open agri-
Fig. 12.18 Larva of An. sinensis cultural lands (particularly rice fields). They have also
been collected in ground pools, pools beside rivers,
marshes, stream margins, ditches, seepages, and shal-
(C), tip of subcosta (Sc) and vein R1, preapical pale low grassy ponds. In mountainous areas they are con-
spot includes costa (C), and veins R1 and R2. Humeral fined to the valleys (Reid 1968; Harrison and Scanlon
cross vein often with one or a few scales. Wing apex 1975). The females are regarded as being zoophilic,
with large pale fringe spot, extending at least to termi- but readily bite humans (Strickman et al. 2000). They
nation of vein R4+5. Vein R4+5 with basal and apical feed indoors or outdoors and tend to leave the houses
dark spots and an area in between with mixed pale and after taking a blood meal.
dark scales. Media (M) usually dark scaled on basal Distribution: Cambodia, China, India, Japan, Korea,
half or more, cubitus (Cu) with short basal dark spot. Malaysia, Singapore, Taiwan, Thailand, Vietnam.
Vein Cu1 with dark basal and apical scales, Cu2 pale Medical importance: Possible vector of Brugia
scaled except for dark scales at apex. Anal vein (A) malayi and vector of malaria in China (Harrison and
pale scaled except small dark spot in the middle and Scanlon 1975).
dark scaled tip, pale fringe spot at termination of vein
Cu2 usually present (Fig. 12.3a). Haltere stem pale,
knob with dark scales. Integument of abdomen dark Anopheles (Cellia) culicifacies Giles 1901
brown, clothed with long yellowish setae, devoid of
scales except a median tuft of erect dark scales close Female: Small to medium sized species with a yellow
to the apical margin of sternum VII. brown culicine-like appearance. Proboscis dark scaled,
Larva: Head slightly longer than wide. Antenna paler at the tip. Palps slightly shorter than proboscis
about half as long as the head, straight, with spicules with 3 narrow pale rings, the apical ring involving the
largely confined to inner surface, antennal seta (1-A) entire palpomere V, and two narrow rings at joints of
long, inserted slightly below the middle of antennal palpomeres II–III and III–IV. Dark area between apical
shaft, with multiple branches. Inner clypeal seta (2-C) and preapical pale rings much wider than apical ring.
single, the pair of 2-C situated close together, outer Pedicel dark grey or brown, without scales, vertex with
clypeal seta (3-C) about half as long as 2-C, strongly pale erect scales, long pale scales forming the frontal
dendriform. Postclypeal seta (4-C) usually with 3 tuft weakly developed or absent. Integument of scutum
branches, frontal setae (5-C to 7-C) long and plumose. pale greyish with darker acrostichal and dorsocentral
Prothoracic seta 1 (1-P) not arising from a sclerotized stripes, scutum usually devoid of scales except some
tubercle, single or with 2–3 branches near apex, 2-P long erect pale scales at the front margin, sparsely
with a prominent sclerotized base, plumose, 3-P longer clothed with short pale setae (Fig. 12.7b). Scutellum
than 1-P, single. Palmate setae partially developed with covered with long and short dark setae. Pleurites with-
pale and slender leaflets on abdominal segments I and out scales, about 4 prealar setae and about 13 upper
II (1-I and 1-II), 1-III to 1-VII well developed, pig- mesepimeral setae present, lower mesepimeral setae
342 12 Asia

pointed, with a broad base, at least half as long as

the blade. Lateral abdominal seta 6 on segments
IV–VI (6-IV to 6-VI) with 2–4 branches split at
some distance from base, tergal plates <1/2 the
width of the corresponding segments, a pair of small
submedian oval plates present (Fig. 12.19). Pecten
with 3–4 long and 10–13 short teeth, all teeth finely
serrated on basal half. Saddle seta (1-X) single, about
1.5 times as long as the saddle.
Biology: An. culicifacies is regarded as a tempo-
rary pool mosquito, the larvae are found in fresh water
in irrigation ditches, rain pools, pools in riverbeds,
along the margins of small streams, partially shaded
or fully exposed to sunlight, in shallow tanks, pits and
wells. The habitats may contain all types of vegeta-
tion, such as submerged, emergent or floating, and
often with abundant green algae (Harrison 1980).
Fig. 12.19 Larva of An. culicifacies, terga I–IV When disturbed, the larvae move rapidly to the bot-
tom of their breeding sites where they may remain
immobile for up to 3–5 min. They are rarely found in
absent. Legs predominantly dark scaled, femora and brackish water and are uncommon in rice fields. The
tibiae with few pale scales at apices, tarsi usually not adults show an unusual behaviour that may be useful
ringed or some tarsomeres with narrow apical pale in identification, they rest with the body horizontal to
rings or patches. Wing with a variable pattern of dark the surface like culicine mosquitoes (Harrison 1980).
and pale spots. Costa with a humeral pale area at base In some localities females are zoophilic, feeding
and with an opposing dark area on R1, vein R4+5 mainly actively on cattle and birds at dusk, but in most areas
or entirely dark scaled. Wing fringe with conspicuous they prefer humans as a host; they are primarily
apical pale spot between apices of R1 and R3, with only endophagic, and rest inside human and bovine shel-
2 indistinct pale spots at terminations of M3+4 and Cu1 ters after the blood meal. Flight ranges of up to 3 km
(Fig. 12.8a). Integument of abdomen light to dark have been observed (Foote and Cook 1959).
brown, entirely devoid of scales, clothed with long Distribution: Afghanistan, Bahrain, Cambodia,
pale brown setae. China, Eritrea, Ethiopia, India, Iran, Iraq, Laos,
Larva: Antenna long and slender, somewhat Myanmar, Nepal, Oman, Pakistan, Sri Lanka, Thailand,
darker near apex, with short spicules on inner sur- Vietnam, Yemen.
face, antennal seta (1-A) short and single, inserted Medical importance: This species is one of the
at about 1/3 from base at the outer surface of the most important malaria vectors wherever it occurs.
antennal shaft. Inner and outer clypeal setae (2-C
and 3-C) single, the pair of 2-C long and inserted
wide apart, 3-C about 2/3 to 3/4 as long as 2-C.  nopheles (Cellia) dirus
A
Postclypeal seta (4-C) single, distinctly shorter than Peyton and Harrison 1979
3-C, frontal setae (5-C to 7-C) long and plumose,
5-C much longer than 6-C and 7-C. Prothoracic seta Female: Proboscis uniformly dark scaled, labium
1 and 2 (1-P and 2-P) arising from separate basal somewhat lighter. Palps slightly shorter than probos-
tubercles, both with a stout stem and pinnately cis, predominantly dark scaled, with a pale apex and
branched, 1-P distinctly shorter than 2-P, 3-P single, 3 narrow apical pale rings on palpomeres II–IV, the
about half as long as 2–P. Palmate setae developed ring of palpomere IV is slightly larger than those on
on abdominal segments I–VII (1-I to 1-VII), seta1-I palpomeres II and III (Fig. 12.6a). Vertex clothed
less developed than the others. Leaflets uniformly with erect pale scales and a small tuft of long pale
pigmented, apices slightly darker, filament long and scales projecting forward, occiput with dark erect
12.2 Species Description 343

scales. Integument of scutum light brown to brown seta (1-A) inserted below middle of antennal shaft,
with darker spots above transverse suture and poste- usually at 1/3 from the base. Inner clypeal seta (2-C)
rior prescutellar area, anterior margin of scutum with long, single with minute branches on apical half, outer
a tuft of long thin pale scales, otherwise scaling of clypeal seta (3-C) single, less than half as long as 2-C.
scutum sparse, and with long dark setae along poste- Postclypeal seta (4-C) with 1–2 branches, usually
rior lateral margin. Scutellum clothed with a few extending forward to near or beyond base of 2-C.
short, pale scales and long dark setae. Integument of Frontal setae (5-C to 7-C) long and plumose, 5-C con-
pleurites light brown with darker areas forming a dis- spicuously longer than the antenna and extending
tinct band on upper portion. Mesepisternum with 3–7 beyond the anterior margin of the head. Prothoracic
upper and 1–4 lower mesepisternal setae; 4–6 prealar seta 1 (1-P) arising from a prominent sclerotized
and 3–7 upper mesepimeral setae present. Wing veins tubercle, either entirely joined or partially connected
covered with pale and dark scales forming a contrast- by posterior bridge or sometimes entirely separate
ing pattern, pale scales on most veins light cream, from common tubercle of setae 2-P and 3-P. Tubercle
scales of presector pale spot and sector pale spot of seta 1-P with a prominent spine arising from its
shiny white, strongly contrasting with other pale posterior margin, setae 1-P and 2-P with a stout stem,
spots. Humeral pale spot usually present and promi- plumose, 3-P sometimes with 1–2 branches, usually
nent, rarely absent. Haltere with pure white scales on single. Palmate setae on abdominal segments I and II
knob. Femora, tibiae, and tarsomeres of all legs with (1-I and 1-II) small, weakly developed, with narrow,
extensive pale speckling, hind leg with a prominent nearly transparent lanceolate leaflets, palmate setae
broad pale ring covering the tibio-tarsal joint. Tergum 1-III to 1-VI fully developed, with 15–22 moderately
VII with few scales on apical margin, tergum VIII broad, lanceolate leaflets, usually with smooth mar-
covered with narrow, elongated pale golden scales on gins, rarely with minute serration close to apices (Fig.
apical half, sternum VII with a median patch of dark 12.20). Lateral abdominal setae 6 on segments IV–VI
scales at posterior margin, sternum VIII with basolat- (6-IV to 6-VI) usually with 2–3 branches. Pecten with
eral patches of pale scales. 3–5 long teeth alternating with 7–12 short teeth.
Larva: Integument of head entirely light brown to Saddle spiculous at posterior margin, saddle seta
yellowish, sometimes with dark spots. Antenna about (1-X) long, single, inserted inside or at ventral margin
half as long as the head, sparsely spiculous. Antennal of saddle.
Biology: The immature stages are particularly
abundant in the rainy season and found in various
small, shallow shady temporary ground pools, animal
footprints, puddles on foot paths, pools in dry stream
beds, springs, streams, wheel ruts, rock pools, bamboo
stumps, and depressions in hollow logs, sometimes
with organic matter and turbid water (Sallum et al.
2005). The females readily bite man indoors and out-
doors from early evening on, with a peak biting activity
between 2000 and 2300 hours.
Distribution: Cambodia, China, Laos, Thailand,
Vietnam.
Medical importance: Primary vector of human
Plasmodium parasites in forested and hilly forested
areas throughout its distribution range (Kobayashi
et al. 2004; Trung et al. 2004). However, An. dirus
seems to be adapted to human changes in the environ-
ment and it is suspected to be an efficient vector of
human malarial parasites in areas of commercial tree
crop plantations and gem mining areas (Sallum et al.
Fig. 12.20 Larva of An. dirus s.s., terga I-IV 2005).
344 12 Asia

are large, particularly on tergum IV, with 2–6 branches,

rarely single. Another difference may be found in the
shape of the large tergal plate on abdominal tergum II.
In An. flavirostris the posterior margin of the plate is
concave (Fig. 12.21), whereas in An. minimus the pos-
terior margin is convex.
Biology: The larvae are typically found in slow
flowing streams of clear fresh water with grassy mar-
gins, in ground pools, irrigation channels, drains and
shallow wells. This species is particularly prevalent in
streams opened up to sunlight through land settlement
or lumbering operations (King 1932). The females
feed on both man and cattle and are regarded as being
exophilic. Harrison (1980) considered An. minimus
and An. flavirostris geographically isolated, with the
latter confined mainly to the Philippines, much of
Indonesia, and Sabah, Malaysia. All the previous
Fig. 12.21 Larva of An. flavirostris, terga I–IV
records of An. minimus in these areas should be
regarded as An. flavirostris.
Distribution: Indonesia, Malaysia, Philippines.
Note on systematics: The Anopheles Dirus Medical importance: Primary malaria vector in the
Complex includes seven distinct species, namely An. Philippines and has been the main target of malaria
dirus s.s., An. cracens, An. scanloni, An. baimaii, An. eradication efforts for a long time (Harrison 1980). It
elegans, An. nemophilous, and An. takasagoensis. All has also been incriminated as a vector of W. bancrofti.
members of the complex may be distinguished by
slight morphological differences in the females as well
as in the fourth larval stage (Sallum et al. 2005).
Additionally, the complex can be separated based on
distinct banding patterns on the sex chromosomes and
the salivary gland polytene chromosomes (Baimai
et al. 1988).

Anopheles (Cellia) flavirostris (Ludlow 1914)

Female: Closely related to An. minimus and regarded

as a subspecies of minimus for a long time. The main
differences as indicated in the keys, the distinct pale
scaling on the apical half of the proboscis in An. flavi-
rostris may consist of a fairly definite patch of yellow-
ish scales ventrally and laterally beginning near the
middle or the apical third and narrowing toward the
tip, usually separated from the labella by darker scales
(Fig. 12.9c).
Larva: A reliable character to separate An. flaviro-
stris from An. minimus involves the development and
branching of seta 0 on abdominal terga IV–VII. In An.
flavirostris setae 0-IV to 0-VII are small, with 1–2
branches, whereas in An. minimus setae 0-IV to 0-VII Fig. 12.22 Larva of An. fluviatilis, terga I–IV
12.2 Species Description 345

Anopheles (Cellia) fluviatilis James 1902 small pale scales. Vertex with a well marked fron-
tal tuft of long whitish scales, occiput with numer-
Female: Very similar to An. minimus, reliable differ- ous erect pale scales, darker scales behind.
ences are found only in the palpal ringing patterns. The Integument of scutum light brown to greyish, with
palps with 3 pale rings, a broad apical ring and 2 indistinct darker lines along acrostichal and dorso-
­narrow subapical and basal rings at joints of palpom- central areas, and distinct dark spots above the
eres II–III and III–IV, the subapical pale ring much transverse suture. Median area covered with creamy
shorter than the apical, intervening dark ring broad, white scales, a lateral stripe of rather broad scales
usually 3 or more times as broad as the subapical pale present. Scutellum clothed with narrow scales and
ring; proboscis all dark (Fig. 12.9a). Another character moderately long pale setae. Integument of pleurites
which may separate the two species can be found on light brown, with paler areas forming a lower band,
the costa (C), which is entirely dark scaled in the basal mesepisternum usually with some scales. Mid
third in An. fluviatilis (Fig. 12.8b), whereas An. mini- coxae with a few pale scales, femora, tibiae, and
mus has a presector pale spot of variable length (Fig. tarsomeres I of all legs extensively speckled with
12.8c). pale scales. Hind tarsi with a broad apical pale ring
Larva (Fig. 12.22): Almost not distinguishable which covers the entire tarsomere V and the apical
from that of An. minimus. part of tarsomere IV and two broad rings at joints
Biology: The immature stages of An. fluviatilis can of tarsomeres II–III and III–IV (Fig. 12.5a). Wing
be found in essentially the same type of habitat as with 4 large dark spots involving costa (C), sub-
those of An. minimus, they breed especially at grassy costa (Sc) and R1, radius (R) usually entirely pale
edges of foothill streams and in stream pools, springs, at base and with the middle dark spot interrupted
and irrigation channels, sometimes at the edges of by small pale areas. Small dark spots on wing field
swamps and lakes, in drains, ponds, and tanks variable in size. Anal vein (A) usually with 3 dark
(Christophers 1933). The larvae have never been spots, more dark spots at base of Cu and apices of
observed in large numbers, dispersed breeding over Cu 1, Cu 2, M 1 and M 2, pale fringe spots at the termi-
immense areas is responsible for the importance of this nations of all veins. Abdomen with a variable
species (Foote and Cook 1959). The females readily amount of scales on terga, usually increasing in
bite man and cattle, they will enter houses and feeding number toward the posterior segments, mixed with
generally occurs before midnight, they are regarded as long pale setae, small tufts of dark scales at poste-
strong fliers (Christophers 1933). Adults are recorded rior corners of terminal terga may be present.
at altitudes up to 2,000 m in Kashmir, in southern India Larva: Antenna with spicules on inner surface,
they are usually not found below 300 m. antennal seta (1-A) inserted at about 1/3 from base
Distribution: Afghanistan, Bahrain, Bangladesh,
China, India, Iran, Iraq, Kazakhstan, Nepal, Oman,
Pakistan, Saudi Arabia, Sri Lanka, Taiwan, Vietnam,
Yemen.
Medical importance: An important malaria vector,
at least in parts of the Middle East and India (Reid
1968).

Anopheles (Cellia) maculatus Theobald 1901

Female: Proboscis dark, palps about as long as pro-

boscis, with erect dark scales towards the base, and
with 3 distinct white rings, the apical and preapical
rings broad and of about equal width, separated by
a narrow dark ring, and a narrow basal pale ring at
Fig. 12.23 Larva of An. maculatus, terga I–IV
the joint of palpomeres II and III. Pedicel with
346 12 Asia

of antennal shaft. Inner and outer clypeal setae (2-C without scales, vertex with pale erect scales, long slen-
and 3-C) single, sometimes finely branched on dis- der whitish scales forming a prominent frontal tuft.
tal half. The pair of 2-C inserted wide apart, 3-C Scutum with a median pale area and contrasting darker
slightly more than half as long as 2-C. Postclypeal areas laterally, sometimes with faint dark acrostichal
seta (4-C) single, placed nearly in posterior line and dorsocentral lines, small median tuft of pale scales
with 2-C, slightly shorter than 3-C and reaching on anterior margin of scutum, median area clothed
well beyond the bases of the inner and outer cly- with pale setae and setose scales. Scutellum covered
peals. Prothoracic seta 1 and 2 (1-P and 2-P) with with short pale setae and a row of long dark setae.
separate conspicuous basal tubercles, both with a Integument of pleurites light to dark brown, often with
stout stem and pinnately branched, 1-P short, sin- continuous pale transverse band. 2–4 prealar setae, 3
gle. Seta 1-I not of palmate type, 1-II weakly devel- upper and 3–4 lower mesepisternal setae, 3-8 upper
oped, leaflets without or with indistinct filaments. mesepimeral setae present, lower mesepimeral setae
Palmate setae well developed on abdominal seg- absent. Coxae pale, devoid of scales, legs uniformly
ments III–VII (1-III to 1-VII), leaflets broad, with a dark scaled, tarsi without pale rings or with very nar-
varying amount of pigmentation, filament well dif- row faint pale patches or rings at the joints (Fig. 12.4b).
ferentiated, 1/3 to 2/3 the length of the blade, Wings with dark and pale spots forming a variable
sharply pointed. Lateral abdominal seta 6 on seg- colour pattern, base of costa (C) usually with a presector
ments V and VI (6-V and 6-VI) with 3–6 branches, pale spot or at least a few pale scales on one wing,
6-IV with 4–7 branches (Fig. 12.23). Tergal plates costa (C) with 4–5 pale spots of varying width. Wing
small to medium sized, pecten similar to that of An. fringe with pale spots at termination of all veins except
stephensi. anal vein (A) (Fig. 12.8c). Integument of abdomen
Biology: The larvae of An. maculatus are primarily dark brown, clothed with light and dark setae, entirely
found in hilly areas in partially shaded small pools devoid of scales.
along the margins of fast flowing streams and rivers Larva: Antenna straight, dark distally, spiculate on
with grassy edges, but also in drains, springs, borrow inner surface, antennal seta (1-A) inserted at about 1/3
pits, rice fields, polluted water, hoof prints and artifi- from base of antennal shaft. Inner and outer clypeal
cial containers (Christophers 1933; Stojanovich and setae (2-C and 3-C) single, stout, 3-C about 1/2 to 2/3
Scott 1966). Often they are especially numerous in as long as 2-C, postclypeal seta (4-C) single and slen-
recently cleared areas where trees have been cut and
the soil is disturbed (Reid 1968). The female feed
readily on man and cattle at night, they frequently
enter houses but leave immediately after the blood
meal; during the day they rest outdoors in low
vegetation.
Distribution: Bangladesh, Cambodia, China, India,
Indonesia, Laos, Malaysia, Philippines, Taiwan,
Thailand, Vietnam.
Medical importance: Malaria vector and a vector
of W. bancrofti (Reid 1968).

Anopheles (Cellia) minimus Theobald 1901

Female: Proboscis dark scaled, palps as long as pro-

boscis, with 3 pale rings, a narrow basal ring at joint of
palpomeres II and III, and 2 broad apical rings, the
subapical ring as broad as the apical ring, the interven-
ing dark ring usually as long as the preapical ring,
rarely longer (Fig. 12.9b). Clypeus dark brown and Fig. 12.24 Larva of An. minimus, terga I–IV
12.2 Species Description 347

der, about half as long as and extending beyond the Medical importance: Important malaria vector
base of 2-C, frontal setae (5-C to 7-C) long and plu- and also vector of W. bancrofti (Reid 1968).
mose. Prothoracic setae 1 and 2 (1-P and 2-P) arising Note on systematics: There are four sibling species
from basal sclerotized tubercles, which sometimes recognised in the Anopheles Minimus Complex,
may be narrowly fused, 1-P less than half as long as namely species A, B, C, and E (Green et al. 1990;
2-P, both with a stout stem and multiple branches, 3-P Somboon et al. 2000). Harrison et al. (1990) considered
single. Metathoracic palmate seta (1-T) well developed species A as being probably An. minimus Theobald.
with slender lanceolate leaflets. Palmate setae well
developed on abdominal segments I–VII (1-I to 1-VII),
that of segment I smaller than the others. Leaflets light Anopheles (Cellia) stephensi Liston 1901
in colour distally with a contrasting dark pigmented
area just basal to shoulders, filament slender, serrated Female: Medium sized species. Proboscis dark scaled,
at base and well differentiated, about half as long as palps with a broad pale ring at the apex and a broad
the blades. Tergal plates very large on segments III– pale ring at the joint of palpomeres III and IV, the dark
VII, more than half the width of the segment, distinctly area in between is distinctly narrower than either ring,
wider than the distance between the bases of the pal- a narrow pale ring at the joint of palpomeres II and III,
mate setae of each segment, enclosing small median and patches of pale scales on the dorsal surface of pal-
posterior tergal plates. Setae 0 on segments III–VII pomere III, which are characteristic for the species
(0-III to 0-VII) usually large and prominent with 1–4 (Fig. 12.6b). Pedicel with small pale scales. Vertex
branches arising outside the tergal plate. Lateral with a well marked frontal tuft of long whitish scales,
abdominal setae 6 on segments IV–VI (6-IV to 6-VI) occiput with numerous erect pale scales. Integument
long, with 3–4 branches (Fig. 12.24). Pecten with 4–8 of scutum light brown to greyish, lateral areas dis-
long and 6–10 short teeth, length of the long teeth vari- tinctly darker and contrasting with the median area,
able, all teeth finely serrated in basal half. Saddle seta and a darker spot at the presutellar area. Median stripe
(1-X) single, longer than the saddle, anal papillae covered with pale narrow scales and lateral tufts of
slightly shorter than anal segment. white scales, supraalar area with a distinct stripe of
Biology: An. minimus inhabits foothill and hilly pale scales. Scutellum clothed with whitish scales and
areas, the larvae are most commonly found along the long yellowish setae. Integument of pleurites light
shaded grassy edges of clear, sunlit and slowly flowing brown, bare of scales, with 2–3 prespiracular setae and
streams and springs, less frequently margin of swamps, 5–6 upper mesepimeral setae. Femora and tibiae
irrigation channels, and rice fields. The larvae nor- speckled with pale scales, those of hind legs usually
mally attach to grass and vegetation with their hooked with pale scales on ventral surfaces. Tarsi predomi-
upper and lower anal setae (2-X and 3-X) to resist cur-
rents (Harrison 1980). Other larval habitats include
rock pools, sand pools next to streams, and seepage
pools. The females readily attack man and cattle and
are found in houses and cattle sheds, they are regarded
as being anthropophilic and endophagic. Resting col-
lections on vegetation and piled wood around bovine
shelters at night also proved to be a good collection
technique for this species (Harrison 1980). The exten-
sive use of DDT spraying during the 1940s to 1960s
obviously led to a selection pressure toward a zoophilic
behaviour and has favoured the survival of that portion
of the population feeding outdoors and not coming
into contact with DDT.
Distribution: Bangladesh, Cambodia, China, India,
Japan, Laos, Malaysia, Pakistan, Taiwan, Thailand,
Vietnam. Fig. 12.25 Larva of An. stephensi, terga I–IV
348 12 Asia

nantly dark scaled, fore tarsus with apical and basal Anopheles (Cellia) sundaicus (Rodenwaldt 1925)
pale rings at joints of tarsomeres I–II and II–III, mid
and hind tarsi with apical pale rings more narrow, hind Female: Medium sized species with conspicuous
tarsomere V entirely dark scaled. Wing with 4 large speckled legs. Proboscis entirely dark scaled, label-
dark spots at anterior margin involving costa (C), sub- lum somewhat lighter. Palps as long as proboscis, pre-
costa (Sc) and R1. Small dark spots at bases of M1, dominantly dark scaled with a broad apical pale ring,
cubitus (Cu), Cu1, and anal vein (A), wing fringe usu- and 2 narrow preapical pale rings, the apical ring
ally with spots of pale scales at terminations of all includes the entire palpomere V and the apical portion
veins. Abdomen clothed with long pale setae and terga of palpomere IV and is about as long as the preceding
VII and VIII heavily covered with narrow scales and dark area (Fig. 12.6c). Pedicel sometimes with a few
pale setae. minute scales. Occiput covered with erect pale scales,
Larva: Antenna with spicules on inner surface, vertex with a tuft of long pale scales projecting for-
antennal seta (1-A) inserted at about 1/3 from base ward. Integument of scutum greyish brown, with
of antennal shaft. Inner and outer clypeal setae (2-C darker areas laterally. Anterior margin of scutum with
and 3-C) single, the pair of 2-C inserted wide apart, a median tuft of narrow pale scales, broader scales lat-
3-C about 2/3 as long as 2-C. Postclypeal seta (4-C) erally. Median part of scutum covered with short pale
single, about as long as 3-C and reaching well beyond hair-like curved scales, scutellum clothed with long
the bases of the inner and outer clypeals. Frontal pale brown setae. Pleurites with a few scales some-
setae (5-C to 7-C) long and plumose. Prothoracic times present on mesepisternum, upper mesepimeral
seta 1 and 2 (1-P and 2-P) arising from separate basal setae numerous. Wing veins covered with pale and
tubercles, both pinnately branched, 1-P slightly dark scales forming characteristic spots. Preapical
shorter than 2-P. Palmate setae well developed on dark spot longer than pale areas, dark spots other than
abdominal segments III–VII (1-III to 1-VII), leaflets those on costa (C) and radius (R) mostly small. Pale
uniformly pigmented, with a short filament, which is fringe spots at terminations of all veins and between
broad at base and about 1/4 as long as the blade. Seta anal vein (A) and base of wing, an additional pale
1-I not of palmate type, 1-II poorly developed (Fig. fringe spot between Cu2 and anal vein (A) very rarely
12.25). Lateral abdominal seta 6 on segments IV–VI present. Coxae without scales, femora, tibiae, and tar-
(6-IV to 6-VI) with 3–4 branches split at some dis- someres I of all legs with conspicuous pale yellowish
tance from base, tergal plates rather small. Pecten speckling. Mid and hind femora with pale scaling on
with 3–5 long and 8–11 short teeth, all teeth serrated
on basal half.
Biology: Under natural conditions, the larvae of An.
stephensi can be found in clean water in stream or river
pools, shaded or exposed to the sun, in drains, pools,
and irrigation channels. In urban areas they are found
in a wide variety of artificial containers, including cis-
terns, wells, flooded cellars, tubs and fountains, and
any kind of artificial reservoirs (Christophers 1933).
The larvae are very shy and rapidly sink to the bottom
when disturbed, and they may remain down for long
periods (Stojanovich and Scott 1966). The females
readily feed on man and rest commonly in dwellings
and cow sheds.
Distribution: Afghanistan, Bahrain, Bangladesh,
China, Egypt, India, Iran, Iraq, Oman, Pakistan, Saudi
Arabia, Thailand.
Medical importance: Important vector of malaria
on the Arabian Peninsula and large cities in the Indian
subcontinent. Fig. 12.26 Larva of An. sundaicus, terga I–IV
12.2 Species Description 349

ventral surface, all femora and hind tibiae with pale Distribution: Bangladesh, Cambodia, China, India,
scales at apices. Fore tarsi with pale apical rings on Indonesia, Malaysia, Singapore, Taiwan, Thailand,
tarsomeres I–III and narrow basal rings on tarsomeres Vietnam.
II–IV, tarsomere V entirely dark scaled. Scaling of Medical importance: This species is an important
mid tarsi similar but pale rings narrower, hind tarsi vector of malaria throughout its distribution range
with apical rings on tarsomeres I–IV, tarsomere V (Reid 1968).
entirely dark scaled (Fig. 12.4a). Integument of abdo-
men dark to light brown, clothed with golden setae
and a few pale scales at posterior margins of terga and Culex (Culex) tritaeniorhynchus Giles 1901
sterna VII and VIII and cerci.
Larva: Antenna rather slender, antennal seta (1-A) Female: Relatively small, reddish brown species.
inserted at about the middle of the antennal shaft. Inner Proboscis predominantly dark scaled, with a narrow
clypeal seta (2-C) slender, single, the pair of 2-C median pale ring, sometimes pale scaling extending to the
inserted wide apart, much closer to 3-C than to each base ventrally. Palps about 1/5 the length of the proboscis,
other. Outer clypeal seta (3-C) about half as long as entirely dark scaled or sometimes with pale scales on
2-C, single, postclypeal seta (4-C) slightly shorter than apex of palpomere IV. Antenna dark, pedicel yellowish to
3-C, arising rather far back and extending beyond light brown. Head with decumbent scales predominantly
bases of 2-C and 3-C. Frontal setae (5-C to 7-C) long golden or yellowish, erect scales of vertex entirely dark
and plumose. Prothoracic seta 1 (1-P) without conspic- brown, lateral patch of broader scales yellowish white.
uous basal tubercle, slender, with 8–15 branches, 2-P Integument of scutum reddish brown to brown, scutum
with indistinct basal tubercle, about 1.5 times as long predominantly covered with narrow dark reddish brown
as 1-P, with 10–13 branches, 3-P about half as long as or golden brown scales, a few paler scales at anterior and
2-P, single. Palmate seta on abdominal segment I (1-I)
weakly developed, with 3–6 moderately broad leaflets
but usually without obvious serrations or well defined
filaments, 1-II to 1-VII fully developed, leaflets evenly
pigmented, with sharply defined filaments with pointed
tips and narrow base, nearly as long as the blade.
Lateral abdominal setae on segments IV–VI (6-IV to
6-VI) long and split into 2–3 slender branches near
base. Tergal plates very small and narrow, posterior
plates present on segments III–VII (Fig. 12.26). Pecten
with about 4–5 long and 10–11 short teeth, the number
and length very variable. Posterior margin of saddle
with numerous spicules, lower anal seta (3-X) with
6–8 long branches. Anal papillae about twice as long
as anal segment.
Biology: An. sundaicus is primarily a coastal spe-
cies, the larvae are mainly found in sunlit brackish
pools or salt swamps with vegetation and algae, but
they also breed in small tidal creeks and pools without
vegetation and sometimes inland in fresh water in vari-
ous places (Reid 1968). Females prefer to feed on cat-
tle but readily bite man indoors and outdoors, the main
biting activity takes place during the early evening
and, to a lesser extent, throughout the night. The adults
rest by day both outdoors and indoors, the females are
strong fliers, a flight range of up to 5 km is recorded
(Christophers 1933). Fig. 12.27 Larva of Cx. tritaeniorhynchus
350 12 Asia

lateral margin, and prescutellar area. Scutellum covered oval patch. Siphon long and slender, slightly tapering
with pale yellowish scales. Integument of pleurites red- towards apex, siphonal index about 5.7–7.0. The pecten
dish brown. Mesepisternum with small patches of pale is composed of 10–15 teeth at the basal 1/4 of the siphon,
scales in upper portion and lower posterior margin, mese- distal pecten teeth with five to six lateral denticles.
pimeron with a small anterior upper scale patch and The siphonal seta (1-S) consists of 5–6 pairs of widely
sometimes with a few scales among the upper mesepim- spaced tufts, inserted subventrally, except the subapi-
eral setae. Lower mesepimeral setae absent. Femora and cal tuft (1e-S), which is inserted laterally. All tufts with
tibiae dark scaled anteriorly, with pale scales posteriorly 3–4 branches as long as or slightly longer than width
(Fig. 12.12b). Tarsi predominantly dark scaled with nar- of siphon at point of insertion (Fig. 12.27). Anal seg-
row basal and apical pale rings on tarsomeres I–IV, more ment completely encircled by the saddle, saddle seta
distinct on fore legs. Wing veins entirely dark scaled, (1-X) usually with 2–3 branches, shorter than the sad-
sometimes with a short line of pale scales at the base of dle. Upper anal seta (2-X) with 2–3 branches, lower
the costa (C). Haltere pale scaled, knob with dark scales. anal seta (3-X) single, longer than the siphon. Ventral
Tergum I with median posterior patch of dark scales, brush with 6 pairs of cratal setae (4-X). Anal papillae
terga II–VII with narrow, slightly convex basal elongate, about as long as the saddle.
pale bands and basolateral pale patches, tergum VIII Biology: The larvae can be found in various tem-
largely pale scaled with narrow apical dark band. Sterna porary and permanent ground water habitats that are
mostly pale scaled, sometimes with small dark lateral sunlit and contain vegetation, including ground
patches. pools, streams, swamps, shallow marshes, irrigation
Larva: Head slightly wider than long. Antenna ditches, rice fields, and animal hoof prints (Bram
about 0.7 times as long as the head, with numerous 1967a; Harbach 1988). The females feed primarily
spicules, dark at the base and narrowing toward the on domestic animals such as cattle and pigs, but will
apex. Antennal seta (1-A) inserted at about 2/3 from bite man in their absence (Bram 1967a). They mainly
the base of the antennal shaft, with multiple branches. bite outdoors between sunset and midnight, but may
Labral seta (1-C) relatively short and sharply pointed, enter cattle sheds and dwellings and bite man during
dark. Postclypeal seta (4-C) single, about as long as any time of the night (Gutsevich et al. 1974;
the distance between the bases of the pair. Frontal setae Sirivanakarn 1976).
(5-C to 7-C) long and aciculate, inner frontal seta (5-C) Distribution: Widely distributed throughout the
with 3–4 branches, median frontal seta (6-C) with 2–3 Oriental region extending west into the Middle East,
branches, outer frontal seta (7-C) about as long as 5-C eastern Mediterranean and large parts of the Ethiopian
and 6-C, with 5–10 branches. Prothoracic setae 1–3 region, also found in the southeastern and eastern
(1-P to 3-3P) long and single, 4-P strong with 2 Palaearctic region.
branches. Lateral abdominal seta 6 on segments III and Medical importance: Most important vector of
IV (6-III and 6-IV) with 2–3 branches, 6-V and 6-VI Japanese encephalitis virus (JE) in the oriental region,
usually with 2 branches. The comb consists of about particularly in Southeast Asia (Bram 1967a;
40–50 small evenly fringed scales arranged in a broad Sirivanakarn 1976).
Chapter 13
Australia

In addition to An. farauti described below, two more of Ross River and Barmah Forest viruses (Russell et al.
malaria vectors of secondary importance in Australia 1999, http://medent.usyd.edu.au).
are An. annulipes s.l. (inland distribution NSW, VIC, Cx. p. quinquefasciatus,1 is a significant nuisance in
SA, TAS, QLD, NT, WA) and An. bancroftii (northern many urban areas, Ae. aegypti1 is an important pest and
Australia). The former species may be involved in the vector particularly in northern Queensland, and the inva-
transmission of human filaria, dog heartworm and sive Ae. albopictus,1 are also included in the key.
Ross River virus. Moreover, Ae. cooki [Stegomyia cooki], Ae. hebri-
Russell (2006) stated that “whatever happens from deus [Stegomyia hebridea], Ae. hensilli [Stegomyia
here with mosquito nomenclature, we can all be hensilli], Ae. polynesiensis [Stegomyia polynesiensis],
assured that in Australia, as in other continents, Aedes Ae. rotumae [Stegomyia rotumae], Ae. scutellaris
by any name will bite as badly”. In addition to those [Stegomyia scutellaris], Oc. notoscriptus [Rampamyia
included in the first group of species responsible for notoscripta] may also be important dengue vectors for
serious biting nuisance (Russell personal commun.), the South Pacific Islands and Australian Region
the following three can also cause biting nuisance in (Rueda 2004).
Australian wetlands, but with no evidence from the For further detailed information on morphology,
field for any role in the transmission of human disease: identification, biology, distribution and disease vector
Oc. bancroftianus (inland regions of NSW, NT, QLD, status of the species mentioned, the reader is referred
SA, VIC, WA); Oc. vittiger (NSW, NT, QLD, SA, to Skuse (1889), Edwards (1924), Mackerras (1927),
VIC) and Verrallina funerea (costal northern NSW, Lee (1944), Marks (1949), Mattingly (1961, 1971),
NT, QLD). In addition to being a significant nuisance Belkin (1962a,b), Dobrotworsky (1965), Huang
pest in some localities, Cq. linealis (coastal and inland (1968), Tyson (1970), Smith (1973), Lee et al. (1988),
NSW, VIC, SA) should also be considered as a vector Rueda (2004), Reinert and Harbach (2005b).

13.1 Key to Australian Female Mosquitoes

1 Palps about as long as proboscis. Scutellum evenly rounded or slightly trilobed and uniformly setose (Fig. 13.1a).
Abdominal terga and sterna completely or largely missing scales. – Wing with contrasting pattern of dark and light
scales, veins R3+4, M, and Cu1 evenly curved beyond cross vein m-cu, Anopheles. Proboscis dark-scaled except for narrow incon-
spicuous pale ring at apex and rarely a few pale scales ventrally on basal half. Scutum speckled with broad decumbent yellowish
scales. Knob of haltere dark-scaled.....................................................................................................An. farauti (p 356)
Palps distinctly shorter than proboscis. Scutellum trilobed, setae arranged in three sets (Fig. 13.1b). Abdominal
terga and sterna uniformly and densely covered with scales. – Prespiracular setae absent. Anal vein (A) evenly curved,
ending distinctly beyond furcation of cubitus (Cu). Alula with fringe of narrow scales...............................................................2

Species described in Chap. 10 concerning European mosquitoes.

1

N. Becker et al., Mosquitoes and Their Control, 351

DOI 10.1007/978-3-540-92874-4_13, © Springer-Verlag Berlin Heidelberg 2010
352 13 Australia

Fig. 13.1 Scutellum of: (a) Anopheles sp.; (b) Aedes sp.

2 (1) Postspiracular setae absent (Fig. 13.2a). All tarsal claws simple, without subbasal tooth. – Tarsomere I of fore
legs usually shorter than tarsomeres II–V together. Tarsomere IV of fore legs not reduced, distinctly longer than broad.
Abdomen rounded apically, cerci short, hardly visible............................................................................................ 3
Postspiracular setae present (Fig. 13.2b) and/or at least the claws of fore tarsi with subbasal tooth. –
Proboscis not strongly curved. Palps less than 2/3 as long as proboscis...................................................................... 6

Fig. 13.2 Lateral view of thorax of: (a) Culex sp.; (b) Mansonia sp.

3 (2) Pulvilli present, well developed (pad-like) (Fig. 13.3a). Hind tarsal claws very small and inconspicuous.
Culex............................................................................................................................................................ 4
Pulvilli absent or not well developed (hair-like) (Fig. 13.3b). Hind tarsal claws quite large and conspicu-
ous. Coquillettidia. – Scutum usually uniformly yellowish to orange, scutal scales scanty, very narrow. Abdominal terga
with light golden scales and some dark purplish scales. Legs dark scaled, hind femur with pale golden scales on basal 1/3 of
anterior surface......................................................................................................... Cq. xanthogaster (p 367)
4 (3) Proboscis with distinct median pale ring (Fig. 13.4a). Lower mesepimeral setae absent. At least some
tarsomeres with distinct basal or basal and apical pale rings. – No broad erect scales in front of supraalar setae.
One or more of abdominal terga II–VI with more or less complete transverse pale bands. Pale bands on terga II–IV largely
or entirely basal................................................................................................................................................ 5
Proboscis without median pale ring but often with pale midventral area (Fig. 13.4b). Usually only one lower
mesepimeral setae present. Tarsi without distinct pale rings. – Pale spot at tip of hind tibia inconspicuous. Terga with
well developed pale basal transverse bands. Sterna pale, without large black central patches.................................................
.......................................................................................................................... Cx. p. quinquefasciatus (p 278)
13.1 Key to Australian Female Mosquitoes 353

Fig. 13.3 Pulvilli of: (a) Culex sp.; (b) Coquillettidia sp. Fig. 13.4 Proboscis of: (a) Cx. sitiens; (b) Cx. p. quinquefasciatus

5 (4) Fore tibia usually with a line of small pale spots on anterior surface among row of setae. Terga dark scaled
with pale basal bands extended medially (Fig. 13.5a). Sterna pale scaled with incomplete apical dark
bands. – Hind tarsomeres I–IV with pale basal rings, tarsomere V all dark........................ Cx. annulirostris (p 365)
Fore tibia usually without pale spots on anterior surface among row of setae. Terga with basal bands not
extended medially (Fig. 13.5b). Sterna with apical dark bands complete. – Mid and hind tibiae with indistinct
longitudinal pale stripes. Mid femur usually with numerous scattered pale scales on anterior surface..Cx. sitiens (p 366)
6 (2) Wing scales usually narrow, if broad then not strongly asymmetrical (Fig. 13.6a). Claws of fore legs usu-
ally with subbasal tooth............................................................................................................................... 7
Wing scales all broad and conspicuously asymmetrical (especially on Cu) (Fig. 13.6b). Claws all
simple, without subbasal tooth. – Erect forked scales numerous, not restricted to occiput. Lower mesepimeral setae
present. Scutum with dorsocentral stripes of pale scales and a pair of continuous pale longitudinal stripes on submedian
area..............................................................................................................................Ma. uniformis (p 330)
7 (6) Head with decumbent scales mainly broad. Erect scales not numerous, restricted to occiput (Fig. 13.7a).
– Proboscis without a white ring. Scutum with white/silvery scales in lines or patches. Scales of scutellum all broad. Femora
with white knee spot. Tarsi with conspicuous pale markings. Hind tarsomere V entirely white. Aedes subgenus
(Stegomyia).................................................................................................................................................. 8
Head with decumbent scales largely narrow and/or (if scales of vertex are largely broad) erect scales
numerous, not restricted to occiput (Fig. 13.7b).......................................................................................... 9

Fig. 13.5 Abdomen of: Fig. 13.6 Wing scales of: Fig. 13.7 Head of: (a) Aedes (Stegomyia) sp.;
(a) Cx. annulirostris; (b) Cx. sitiens (a) Aedes sp.; (b) Mansonia sp. (b) Ochle­rotatus sp.
354 13 Australia

8 (7) Scutum without acrostichal stripe on anterior part, but with two narrow white dorsocentral stripes sepa-
rated from anterior margin. Lateral white stripes broad, continuing over transverse suture to the end of
scutum, lyre shaped (Fig. 13.8a). – Clypeus with white scale patches. Mesepimeron with two well separated white
scale patches................................................................................................................... Ae. aegypti (p 198)
Scutum with a white acrostichal stripe extending from the anterior margin to the beginning of the pres-
cutellar area, where it forks to end at the anterior margin of scutellum (Fig. 13.8b). – Clypeus without white
scale patches. Mesepimeron with V-shaped white scale patch.. .......................................... Ae. albopictus (p 201)
9 (7) Decumbent scales of vertex largely broad. Cerci short, broad and blunt (Fig. 13.9a). Ochlerotatus sub-
genus (Finlaya) – Proboscis with a distinct median pale ring. Scutum with silvery stripes forming a lyre shaped pattern.
Postpronotal patch of dark scales with a small but distinct group of silvery scales at lower posterior portion. Mid femur
with a median longitudinal silvery stripe. Wing scales all dark........................................Oc. notoscriptus (p 358)
Decumbent scales of vertex largely narrow. Cerci long and slender, tapering (Fig. 13.9b).................. 10

Fig. 13.8 Scutum of: (a) Ae. aegypti; (b) Ae. albopictus Fig. 13.9 End of abdomen of: (a) Ochlerotatus (Finlaya) sp.;
(b) Ochlerotatus (Ochlerotatus) sp.

10 (9) Palps 2/3 length of proboscis (Fig. 13.10a). Wing membrane conspicuously clouded on base and across
furcation of Rs and cross veins r-m, m-cu. Ochlerotatus subgenus (Mucidus) – Scutum with tufts of twisted
erect pale scales. Legs more or less shaggy. Wing very densely scaled with mixed brown, pale yellowish and white
scales........................................................................................................................ Oc. alternans (p 357)
Palps less than 1/3 length of proboscis (Fig. 13.10b). Wing membrane usually not spotted, uniformly
clear or uniformly clouded. Ochlerotatus subgenus (Ochlerotatus)...................................................... 11

Fig. 13.10 Palps of: (a) Ochlerotatus (Mucidus) sp.; Fig. 13.11 Hind tarsus of: (a) Oc. vigilax; (b) Oc. sagax
(b) Ochlerotatus (Ochlerotatus) sp.
13.1 Key to Australian Female Mosquitoes 355

11 (10) Tarsi of all legs with distinct white basal rings (Fig. 13.11a). – Head and sides of scutum with narrow
scales................................................................................................................................................. 12
Tarsi without distinct white basal rings (Fig. 13.11b). Scutum with bronzy-brown and creamy white
scales. Scutellum with narrow scales only. At least one strong lower mesepimeral seta present. Wing
dark scaled, pale scales, if present, relatively few and only along anterior border. Abdomen with distinct
pale basal transverse bands........................................................................................... Oc. sagax (p 362)
12 (11) Wings entirely dark scaled. At least one lower mesepimeral seta present (Fig. 13.12a). Femora speckled
with white scales anteriorly........................................................................ Oc. camptorhynchus (p 360)
Wings with at least some white scales. Lower mesepimeral seta absent (Fig. 13.12b)......................... 13

Fig. 13.12 Lateral view of thorax of: (a) Oc. camptorhynchus; (b) Oc. vigilax

13 (12) Wings with numerous symmetrical broad scales (Fig. 13.13a). – Pale basal bands of abdominal terga narrow,
sometimes incomplete, the dark portions of the terga usually conspicuously speckled with pale scales, especially on ter-
minal segments........................................................................................................... Oc. theobaldi (p 363)
Wing scales normal in size and shape (Fig. 13.13b).............................................................................. 14

Fig. 13.13 Wing scales of: (a) Oc. theobaldi; (b) Oc. vigilax Fig. 13.14 Proboscis of: (a) Oc. vigilax; (b) Oc. normanensis
356 13 Australia

14(13) Basal 2/3 of proboscis with ventrolateral pale scaling sometimes forming complete ring (Fig. 13.14a).
Hind tarsomere V with a broad white ring...................................................................Oc. vigilax (p 364)
Proboscis dark scaled, sometimes with a few scattered pale scales on basal half. (Fig. 13.14b). Hind
tarsomere V without, or with very narrow, basal white ring............................. Oc. normanensis (p 360)

13.2 Species Description knob dark scaled. Integument of abdomen dark brown,
setae pale golden, more numerous on last segments,
Anopheles (Cellia) farauti s.l. Laveran 1902 scales absent on terga I–V and sterna I–VI, a few scales
on terga VI and VII and sternum VII, rather dense
Female: Medium sized species, proboscis entirely scaling on tergum VIII and sternum VIII.
dark scaled except for a very narrow apical pale ring, Larva: Head strongly and unevenly pigmented,
labellum light brown. Palps as long as proboscis and usually with a conspicuous pattern of dark areas.
dark scaled, usually with 3–4 pale rings, the apical and Antenna strongly pigmented, covered with small
subapical rings broad, sometimes with variable num- ­spicules, antennal seta (1-A) minute and single, arising
ber of paler scales dorsally near base. Pedicel with a near base on outer surface of antennal shaft. Inner cly-
few small white scales. Integument of head dark peal setae (2-C) widely separated, inserted closer to
throughout, occiput with erect scales short and broad, outer clypeal setae (3-C) than to each other. 2-C usu-
white dorsally and dark laterally, vertex with a frontal ally strongly aciculate, 3-C more than half the length of
tuft of very long slender white scales forwardly 2-C, frequently barbed. Postclypeal seta (4-C) usually
directed. Integument of scutum light yellow brown, with 1–2 branches and extending beyond insertion
with dark spots anterior to scutal angle and a dark points of 2-C and 3-C. Frontal setae (5-C to 7-C) plu-
prescutellar area. Scutum sparsely covered with mod- mose, gradually decreasing in size. Prothoracic setae
erately broad decumbent yellowish scales, scales 1–3 (1-P to 3-P) usually arising from a heavily sclero-
somewhat longer anteriorly and above wing roots. tized common tubercle, stem of 1-P usually strongly
Scutellum with a few whitish scales smaller than on swollen, seta 3-T usually with lanceolate leaflets, not
scutum, scutal and scutellar setae golden brown. strongly palmate. Abdominal seta 1-I usually distinctly
Integument of pleurites usually with light and darker palmate, always with distinct flattened leaflets, palmate
areas, antepronotum with a dorsal patch of broad erect setae 1-II to 1-VII well developed, leaflets usually nar-
dark scales and numerous dark setae. Upper mesepis- row and serrated at least on those of middle segments.
ternum with 5–7 setae and a small patch of broad
decumbent light scales, lower mesepisternum usually
with 4 setae and a small patch of similar scales, 4–10
upper mesepimeral setae present, all pleural setae
rather light. Legs with light brown to blackish scales
and with yellowish white scale markings. Femora and
tibiae extensively speckled with pale scales, tarsomere
I of all tarsi with pale apex and a variable number of
pale spots. Fore tarsomere I-IV pale at base and apex,
tarsomere V pale or dark, all tarsomeres usually much
paler ventrally. Mid and hind tarsomeres II–IV with
narrow apical pale rings, tarsomeres V usually all dark.
Wing with contrasting pattern of dark and pale scales,
costa (C) with 4 large dark spots and 3 small dark spots
basally, usually a small dark sector spot between basal
and median dark spots. Wing fringe dark scaled, with
pale spots at apices of all veins. Haltere pale at base, Fig. 13.15 Larva of An. farauti
13.2 Species Description 357

Abdominal setae 6-IV and 6-V usually with 2 branches. Medical importance: Primary malaria vector, effi-
Anal segment with conspicuous spicules at posterior cient vector of human filariasis (Wuchereria bancrofti)
margin, saddle strongly pigmented and reaching half (Belkin 1962a).
way down the ventral sides of the anal segment, saddle Note on systematics: An. farauti is a member of
seta (1-X) arising at some distance from ventral and the Anopheles Punctulatus Complex, which comprises
posterior margins of saddle (Fig. 13.15). Upper caudal of at least four distinct species: the nominative form
seta (2-X) with lateral branches, slightly shorter than An. punctulatus, An. farauti No.1, An. farauti No.2,
lower caudal seta (3-X). Ventral brush with 7–9 pairs of and An. koliensis (Belkin 1962a; Bryan 1974). Adults
cratal setae (4-X), anal papillae about twice as long as may be distinguished by the colouration patterns of the
saddle, pointed. proboscis; the larvae differ in the ratios of the clypeal
Biology: The natural breeding sites of An. farauti setae 2-C and 3-C and in the structure of the ­prothoracic
consist primarily of river and stream margins with setae 1-P to 3-P. The members of the complex are
vegetation, springs, seepage areas, ponds, lagoons, undoubtedly the most important vectors of malaria and
and temporary ground pools of all sizes, in open coastal filariasis wherever they occur. Because of its wide dis-
areas or in wide river valleys. An. farauti has a definite tribution range, An. farauti is the most important, and
preference for open sunlit areas but is frequently found sometimes the only, vector in the South Pacific (Belkin
in large numbers under partial shade. Very often the 1962a).
breeding habitats are associated with flotage and emer-
gent or surface vegetation (Belkin 1962a). The larvae
are remarkably tolerant to organic pollution and may  chlerotatus (Mucidus) alternans
O
occur in brackish water with a salinity up to 70% of (Westwood 1835)
that of sea water. When the population becomes
extremely abundant, the larvae will breed in artificial Female: A very large mosquito, speckled with yellow,
containers to a limited degree. Larvae have been light brown, and white scales and shaggy palps, legs
reported from boats, canoes, tanks, oil drums, water and abdomen. Palps about 2/3 length of proboscis
collections in canvas, and even in small tin cans which is darker at apex and base but paler in the mid-
(Horsfall 1955). An. farauti does not utilize water col- dle. Antenna slightly shorter than proboscis, light
lections in or on plants or plant parts, such as tree- brownish yellow, pedicel with a conspicuous patch of
holes, leaf axils, coconut shells, or cacao pods. Females small broad white scales. Central portion of vertex
feed on a wide variety of hosts, including humans. largely with narrow scales, brownish yellow laterally,
They feed on humans very readily and are most incon- and a median longitudinal stripe of pure white scales;
spicuous when approaching to feed; their bites are sides of vertex with some broad brownish yellow
usually not felt at all. Feeding activity usually begins scales followed by broad white scales, erect scales
at dusk and probably continues through the night to very numerous and long, largely brownish yellow.
dawn. Occasional attacks in the daytime have been Scutum with mottling of brown, white and yellowish
reported not only in shaded areas but even in bright broad and narrow scales but in an indefinable pattern,
sunlight (Belkin 1962a). The females feed most com- acrostichal and dorsocentral setae short, very numer-
monly in the open but will enter dwellings as well; ous. Scutellum with numerous white scales on all
some remain there after the blood meal. Generations lobes, some scales short and decumbent, majority long
are continuous, with a marked decline in population and erect. Pleurites with numerous broad white scales,
during parts of the year when precipitation is low. pleural setae golden or very pale, lower mesepimeral
The flight range of the females is as far as 1.6 km, setae in a patch of about 10 near the middle of sclerite.
usually less (Horsfall 1955). Only one blood meal is Coxae with white and scattered yellowish scales, fem-
required for the development of the first batch of ora and tibiae largely yellow with some white scales at
eggs; oviposition occurs 48–72 h after engorgement their bases. Tarsi with brown or light brown scales,
(Bryan 1974). and with conspicuous whitish rings, basal and median
Distribution: Australia, New Hebrides, Solomon on tarsomere I and basal on tarsomeres II–V. Light
Islands, New Guinea, Moluccas, Bismarck Archi­ rings indefinite or sometimes absent on fore and mid
pelago, Indonesia. legs, conspicuous on hind leg. Wing veins very densely
358 13 Australia

covered with brown, pale yellowish and white broad

scales, wing fringe with dark and pale spots. Scaling of
terga II–VII largely yellow, with variable basal lateral
and basal median patches of white scales, sometimes
connected by narrow transverse basal white bands,
sterna largely whitish scaled, distal ones with yellow
or brownish apicolateral patches.
Larva: Large and distinct individuals with the
mouth brushes modified for predation, the brushes are
reduced in number, curved distally and strongly thick-
ened. The head is moderately pigmented, the posterior
portion somewhat darker, antenna short and slender,
<1/2 as long as the head, distal portion darker. The
antennal seta (1-A) is situated well beyond the middle
of the antenna and usually has 2 branches. The labral
seta (1-C) is long and slender and the clypeal (4-C) and
frontal setae (5-C to 7-C) are single. Integument of
thorax and abdomen without distinct spicules, protho-
racic setae 1-P to 3-P single, 4-P with 3–4 branches.
The comb is arranged in an irregular patch of about
5–6 rows of short scales which are broadened and
fringed apically. The siphon is rather long, slightly
tapering toward its apex, the siphonal index is about
3.7–4.5. The pecten extends to about 1/3 from the base
of the siphon and consists of about 20 or more slender
teeth, which are more or less evenly spaced, the basal Fig. 13.16 Larva of Oc. alternans
teeth are very short, each tooth usually has a strong
lateral denticle. The siphonal tuft (1-S) is multiple
branched and inserted beyond the pecten well below
the middle of the siphon (Fig. 13.16). The saddle is humans and other animals throughout the day and
moderately large extending more or less half way night and may disperse several kilometers from their
down the sides of the anal segment and bears short larval habitats in search of a blood meal.
and strong spines on its posterior dorsal border. The Distribution: East and Northern Australia, New
saddle seta (1-X) is single, the upper (2-X) and lower Guinea, New Caledonia.
(3-X) anal setae are both single, arising from a promi-
nent process with strong ventral sclerotisation. The
ventral brush consists of about 7–8 cratal setae (4-X) Ochlerotatus (Finlaya) notoscriptus (Skuse 1889)
and 5–6 precratal setae extending over the greater part
of the midventral line of the anal segment. Anal papi­ Female: A small to medium sized dark species with
llae short and pointed, about 1/4 the length of the anal conspicuous silvery markings on the scutum and
segment. ringed legs. Proboscis predominantly dark scaled
Biology: The larvae are mainly found in brackish with a distinct narrow median pale ring, palps dark
water swamps on the coast along with those of Oc. with a varying number of silvery scales at the tip,
vigilax, but also in fresh water ground pools inland pedicel of antenna with a large mesal patch of silvery
often associated with larvae of Oc. vittiger. They are scales. Vertex with a rather conspicuous but short
predacious on other mosquito larvae. The females of frontal tuft of silvery or yellowish scales, a narrow
Oc. alternans can reach reasonably high levels in many complete line of densely packed silvery white scales
areas following extended periods of rain (Russell around the eye margin, erect scales dark, rather
1996). They are very aggressive biters and will attack numerous but short. Scutum covered with narrow
13.2 Species Description 359

dark scales and with silvery, sometimes golden scales

arranged in narrow stripes forming a very conspicu-
ous lyre shaped pattern. A narrow median acrostichal
stripe extends to prescutellar area where it divides
into more or less definite prescutellar stripes, a pair of
anterior dorso­central stripes, yellowish or golden,
sometimes reduced or absent, a pair of lateral stripes
to scutal angle where each broadens and curves over
the transverse suture and then continues as prescutel-
lar dorsocentral stripes, a pair of supraalar stripes
usually strongly developed, a pair of conspicuous
large patches of broad silvery scales in front of wing
roots. Acrostichal and dorsocentral setae strongly
developed. All lobes of scutellum with broad flat sil-
very or slightly yellowish scales, paratergite with
conspicuous silvery scales. Pleurites with several
patches of broad silvery scales, lower mesepimeral
setae absent. Coxae with patches of silvery scales,
femora dark with narrow longitudinal silvery stripes
from base to near apex on anterior and posterior sur-
Fig. 13.17 Larva of Oc. notoscriptus
faces. Tibiae with anterior and posterior stripes of
silvery or whitish scales, usually nearly reaching
apex, short or poorly developed on anterior surface of
fore tibia and posterior surface of hind tibia. Hind tar- 3/4 of the anal segment, spicules at its posterior dor-
sus with conspicuous large basal white rings and usu- sal margin well developed but relatively short.
ally very narrow apical incomplete rings on tarsomeres Saddle seta (1-X) 2–4 branched, upper anal seta
I–IV, tarsomere V variable from completely white to (2-X) with 3–4 branches, lower anal seta (3-X)
completely dark. Wing scales all dark. Abdominal single. Ventral brush with 6 pairs of cratal setae
terga largely dark scaled with basolateral silvery (4-X), precratal setae absent. Anal papillae pointed,
patches or narrow bands separated from lateral the dorsal pair about as long as the saddle, the ven-
patches, sterna mostly pale scaled with more or less tral pair shorter.
distinct basolateral silvery markings, distal segments Biology: Oc. notoscriptus is a semi domestic
may be predominantly dark. species breeding readily in artificial containers of
Larva: Head light brown, antenna about half as all types, e.g. water tanks, tin cans, flower pots and
long as the head, straight, uniform in width, without in coconut husks and shells. The natural breeding
spicules, antennal seta (1-A) inserted well beyond the places are usually tree-holes but the larvae can also
middle of antennal shaft, single. Labral seta (1-C) be found in leaf axils of various plants and even rock
very stout and conspicuously hooked in distal half, and ground pools. Females readily attack humans by
postclypeal seta (4-C) small, with multiple branches, day in shaded areas but also feed during evening,
inner and median frontal setae (5-C and 6-C) single, night and early morning. Overwintering takes place
5-C displaced anteriorly, outer frontal seta (7-C) with in the larval stage. Oc. notoscriptus is one of the
3–4 branches. Prothoracic seta 1 (1-P) 2-branched, major domestic pest species in south eastern
2-P single, 3-P with 3 branches. The comb consists of Australia.
19–24 fringed scales arranged in 2 or 3 rows. Siphon Distribution: Australia, New Guinea, New Zealand,
short and stout, siphonal index usually about 1.7–2.5, New Caledonia.
siphonal tuft (1-S) with 3–4 branches, inserted well Medical importance: Oc. notoscriptus is
beyond the middle of the siphon (Fig. 13.17). The believed to be a suitable vector for Barmah Forest
pecten consists of 12–13 teeth, individual tooth with virus, Ross River virus and heartworm in dogs
a prominent lateral denticle. The saddle covers about (Russell 1996).
360 13 Australia

 chlerotatus (Ochlerotatus) camptorhynchus

O
(Thompson 1868)

Female: A medium sized dark mosquito with pale

rings on all legs. Proboscis extensively mottled, par-
ticularly on ventral side, sometimes almost completely
pale scaled, palps about 1/5 the length of proboscis,
mottled. Pedicel dark with a few pale scales and black
setae. Vertex usually clothed with narrow curved and
erect forked pale scales, elongate patches of narrow
bronze scales close to posterior eye margin. Integument
of thorax dark brown. Scutum uniformly clothed with
narrow curved golden scales although there are a few
paler median patches particularly close to its posterior
margin. Pleurites with several patches of broad white
scales, 3–4 lower mesepimeral setae present (Fig.
13.12a). Femora, tibiae and tarsomeres I of all legs
mottled with white scales, tarsomeres II–V with pale
basal rings. Wings completely dark scaled. Abdominal
terga dark scaled, usually with patches of white scales Fig. 13.18 Larva of Oc. camptorhynchus
on terga I and II and convex basal bands on terga
III–VI, but these bands may be either narrow and
almost straight or triangular, sometimes reaching the throughout the year in southern parts of Australia, and
posterior margin of the terga. Sterna pale scaled with may disperse widely from their larval habitats. They
median and sometimes apicolateral patches of dark are extremely vicious biters and readily attack humans
scales, the patches may be reduced to a few scales. and other animals including birds during the day, at
Larva: Antenna short, <1/2 as long as the head, dusk and after sunset. The species is a major pest in
antennal seta (1-A) inserted beyond the middle of coastal areas in southern Australia.
the antennal shaft. Inner frontal seta (5-C) with 3–4 Distribution: Southern coasts of Australia.
branches, median frontal seta (6-C) with 2–3 branches, Medical importance: Ross River virus has been
outer frontal seta (7-C) with 8–10 branches. isolated from this mosquito in Victoria and Tasmania
Prothoracic setae 1-P with 2 branches, 2-P single; (Russell 1996).
3-P with 2–4 branches. The comb consists of 24–33
fringed scales arranged in an irregular or triangular
patch. The siphonal index is about 2.0–2.3, the  chlerotatus (Ochlerotatus) normanensis
O
pecten consists of 22–24 teeth, each tooth with 3–4 (Taylor 1915)
lateral denticles. The siphonal tuft (1-S) has 7–8
branches and is inserted well beyond the middle of Female: A small to medium sized species. Proboscis
the siphon. The saddle covers about half of the anal and palps dark scaled (Fig. 13.14b), sometimes with a
segment, saddle seta (1-X) single, upper anal seta few scattered pale scales on basal half of proboscis.
(2-X) with 6–7 branches, and lower anal seta (3-X) Pedicel brown, clothed with small flat dark brown or
single. The ventral brush consists of 18–19 tufts, mixed dark and white scales. Integument of head dark
usually with 2–3 precratal setae (4-X). The anal brown, vertex and occiput clothed with narrow curved
papillae are very small and globular, but prominent silvery white scales and narrow curved bronze black
(Fig. 13.18). scales, and numerous dark brown erect forked scales.
Biology: Oc. camptorhynchus breeds mainly in Scutum covered with fine narrow curved bronze black
brackish swamps and marshes in open country; it is scales and scattered golden scales, the dark scales
typically a coastal species but occurs in inland riverine always predominating. Acrostichal and dorsocentral
areas with brackish influence. Adults may be active setae strong and dark, numerous dark setae also lateral
13.2 Species Description 361

and above the wing roots. Scutellum brown, clothed The siphonal tuft (1-S) with 5–13 long branches, arises
with narrow curved silvery scales, the median lobe slightly below the middle of the siphon. The tuft is
sometimes with some dark scales also, 6–10 long dark more than twice as long as the width of the siphon at
setae on each lobe. Integument of pleurites brown, the point of its insertion (Fig. 13.19). The pecten
antepronotum with narrow curved silvery scales, extends over the basal 1/4 to 1/3 of the siphon, consist-
sometimes with narrow curved or broader dark scales ing of 5–13 teeth each with 1–4 rather variable lateral
above, ­postpronotum with mixed narrow curved dark denticles, the apical or preapical denticle being promi-
and ­silvery scales. Patches of narrow curved scales on nent. The distalmost tooth is the longest, and they
sub- and postspiracular areas and paratergite, patches decrease in size basally, the most basal often being
of broad silvery scales on upper portion and lower pos- very small and scale-like. The saddle covers slightly
terior margin of mesepisternum, prealar area and upper >1/2 of the anal segment, with a very irregular ventral
part of mesepimeron. Pleural setae dark or pale, 2–6 margin and a row of short pointed spicules at its poste-
upper mesepisternal setae, a row of 5–8 long and sev- rior margin. The saddle seta (1-X) is single and about
eral shorter lower mesepisternal setae, about 12–15 half as long as the saddle. The upper anal seta (2-X)
prealar setae, 10–14 upper mesepimeral setae, lower has 9–17 branches, about twice the length of the sad-
mesepimeral setae absent. Legs dark scaled with mot- dle, the lower anal seta (3-X) is single, and about twice
tled femora and tibiae, tarsomeres with narrow pale as long as 2-X. The ventral brush consists of 12–14
basal rings. Wings dark scaled, extensively mottled cratal setae (4-X), each tuft with 9–16 branches, 1–2
with pale scales on all veins, although the mottling is precratal setae (4-X) present. The anal papillae are
much reduced toward the apex of the wing. Haltere long, tapering and pointed, 2–3 times longer than the
pale, with white scaled knob, occasionally with a few saddle; the lower pair is slightly longer than the upper
dark scales also. Integument of abdomen dark brown. pair.
Tergum I with mixed dark and pale scales medially Biology: Larvae of Oc. normanensis can be found
and white lateral patches. Terga II–VII dark scaled in temporary ground pools and swampy areas resulting
with basal pale bands or median patches, usually dis- from heavy rain, fully or partially exposed to the sun.
continuous with large basal lateral white patches, the Frequently the larvae may be encountered together
bands may be narrow or fairly wide, straight or some-
what produced medially. Sterna usually dark scaled,
with mottling of white scales mainly laterally toward
the base, sternum VII often entirely dark scaled, cerci
long and dark.
Larva: Head about 2/3 as long as broad, antenna
approximately 3/4 as long as the head, slightly curved,
tapering toward its apex and clothed with spicules,
more dense in the basal half. The antennal seta (1-A)
has 3–9 branches arising at about the middle of the
antennal shaft. The labral seta (1-C) is straight, slender
and pointed. Inner frontal seta (5-C) 2–3 branched,
median frontal seta (6-C) single, outer frontal seta
(7-C) with 1–4 branches, but usually with 2 branches.
The prothoracic setae (1-P to 3-P) are all single, of dif-
ferent lengths and arise from a common sclerotized
tubercle, 3-P is the longest and strong, 2-P is less than
half as long as 3-P and fine. The comb consists of
13–20 slender scales arranged in 2–3 rows, each scale
with an elongated median spine and a narrow base.
The siphonal index is approximately 3.0, the siphon is
slightly tapering beyond the insertion point of the siph-
onal tuft (1-S), and the tracheal trunks are very narrow. Fig. 13.19 Larva of Oc. normanensis
362 13 Australia

with those of An. annulipes s.l., Oc. alternans, Oc. sometimes with 2 branches, outer frontal seta (7-C)
vigilax, Oc. vittiger and Cx. annulirostris. The pools with 4–8 branches. Prothoracic setae 1 and 2 (1-P and
may occur in natural depressions, dry water courses, or 2-P) single, 3-P with 1–2 branches. The comb is com-
man-made excavations, including country road gutters posed of 8–14 scales arranged in a single row, indi-
and hoof prints. The water may be clear or muddy, and vidual comb scales with prominent terminal spine
sometimes slightly polluted by animal manures. and fringed with small spicules basally. Siphon
Females of Oc. normanensis readily bite man during slightly tapering toward apex, siphonal index 2.3–2.8.
the day (Marks 1949). It is a common species in north- Siphonal tuft (1-S) inserted at about the middle of
ern Australia where it is a major nuisance mosquito. siphon, rather small, distinctly shorter than the width
Distribution: Australia. of siphon at the point of its origin, with 3–4 branches.
Medical importance: Vector of Murray Valley The pecten consists of 20–25 teeth with at least one
Fever and Ross River virus (Russell 1996). detached tooth inserted beyond siphonal tuft (1-S)
(Fig. 13.20). Saddle almost entirely encircling anal
segment, saddle seta (1-X) single, upper anal seta
 chlerotatus (Ochlerotatus) sagax
O (2-X) with 9–12 branches, lower anal seta (3-X) sin-
(Skuse 1889) gle. The ventral brush consists of 14–16 tufts of cratal
setae (4-X), 1–2 precratal setae present. Anal papillae
Female: A moderately large species of dark appearance lanceolate, about as long as or longer than the
with distinct pale scaling on abdomen and pleurae. saddle.
Proboscis dark scaled, palps sometimes mottled at base, Biology: The larvae of Oc. sagax can be found in
pedicel with narrow pale scales on dorsal surface. Vertex temporary ground pools, shallow pools, roadside ditches
clothed with narrow pale scales, occiput with numerous or irrigation channels with fresh water, exposed to the
creamy erect forked scales. Integument of scutum dark, sun or shaded, with or without vegetation. They breed in
scutum covered with narrow bronze scales, some larger the open, but are more common in and near woodland.
pale scales laterally and around prescutellar area.
Scutellum with narrow pale scales and long setae on all
lobes. Integument of pleurites dark brown, densely
clothed with several patches of broad pale scales.
Mesepimeral scale patch not reaching the lower margin
of mesepimeron, 3–8 lower mesepimeral setae present.
Coxae with decumbent pale scales, fore and mid femora
mottled, hind femur mostly pale scaled and mottled over
most of its length, with dark apex. All tibiae and basal
half of tarsomeres I extensively mottled, rest of tarsi
dark scaled (Fig. 13.11b), or at most with traces of white
rings on tarsomeres I and II. Wings predominantly dark
scaled, some pale scales present at base of costa (C) and
sometimes also at bases of subcosta (Sc) and vein R1.
Haltere with stem and knob pale scaled. Terga dark
scaled with moderately broad pale basal bands often
extended medially and sometime reaching the apical
margin on last segments, sterna predominantly pale
scaled, with small apicolateral patches of dark scales.
Larva: Head wider than long, antenna <1/2 as
long as the head, slightly swollen basally, and spicu-
late. Antennal seta (1-A) inserted at about the middle
of antennal shaft or slightly below, with 3–6 branches.
Postclypeal seta (4-C) with 2–3 small branches, inner
and median frontal setae (5-C and 6-C) single, 5-C Fig. 13.20 Larva of Oc. sagax
13.2 Species Description 363

(Dobrotworsky 1965; Liehne 1991; Russell 1993). The The comb consists of 16–24 slender pointed scales
females readily bite man and domestic animals in arranged in 2–3 rows, each with a coarse fringe basally
the daytime, but also feed at dusk, night and dawn. The and a prominent median spine. Siphon slightly taper-
adults are generally most abundant in spring; the species ing toward apex, siphonal index 3.3–3.9. The pecten is
can be a major pest in spring in some riverine areas, and restricted to the basal 1/4 of the siphon and consists of
particularly after flooding even in summer and autumn 9–15 teeth, each tooth with 2–5 lateral denticles, the
(Russell 1993). distalmost tooth is the longest, the teeth decreasing in
Distribution: Widely distributed in southeastern size toward the base, the most proximal often being
Australia. very small and scale-like. Siphonal tuft (1-S) with 4–9
long branches arise slightly below the middle of
siphon. Seta 9-S on the ventral valve is very stout and
 chlerotatus (Ochlerotatus) theobaldi
O forwardly curved (Fig. 13.21). Saddle covers about
(Taylor 1914) 2/3 of the anal segment, with irregular ventral margin
and a row of short pointed spicules at its posterior mar-
Female: A medium sized species of mottled dark gin. Saddle seta (1-X) single, about 2/3 as long as
appearance. Proboscis mainly dark scaled or mottled saddle. Upper anal seta (2-X) with 7–13 branches,
but with extensive pale area on ventral surface, palps about twice as long as saddle, lower anal seta (3-X)
with whitish scales medially and at apex, and ­sometimes single. The ventral brush consists of 15–17 tufts, each
with some mottling also. Head with broad pale scales with 6–10 branches, with 1–2 precratal setae (4-X).
laterally and along the eye margin, erect forked scales Anal papillae long and pointed, about twice as long as
dark bronzy, pedicel with several pale scales. Scutum the saddle.
covered with narrow curved golden and creamy scales, Biology: Larvae of Oc. theobaldi have been found
usually with some admixture of bronze black scales on in clear or slightly muddy rain water in grassy edged
the transverse suture and along the midline, some gutters of country roads, in small rain filled pools and
larger pale areas toward the rear. Pleurites with several in hoof prints (Marks 1949). Adults may become active
patches of pale scales. Femora and tibiae moderately in spring and be apparent throughout the year in
to extensively mottled with pale scales, hind legs with
femur, tibia and tarsomere I mottled, all tarsomeres
with basal white rings, although tarsomere V may be
all dark. Wing dark scaled with extensive mottling of
broad symmetrical pale scales on all veins (Fig.
13.13a). Abdominal terga dark with pale lateral patches
and basal bands which may not be complete and there
may be some mottling on terminal segments, sterna
pale scaled with some scattered dark scales or apical
bands or lateral patches.
Larva: Head about 2/3 as long as broad, antenna
about 2/3 the length of the head, slightly curved and
tapering, clothed with spicules. Antennal seta (1-A)
about 1/2 as long as antenna, with 4–7 branches
inserted slightly below the middle of the antennal
shaft. Labral seta (1-C) long, straight and slender,
postclypeal seta (4-C) minute with 6–10 branches.
Inner frontal seta (5-C) with 2 branches, median fron-
tal seta (6-C) single, outer frontal seta (7-C) with 2–4
branches, arising a short distance behind base of
antenna. Prothoracic setae 1–3 (1-P to 3-P) without
sclerotized tubercles, 1-P with 1–3 branches, about 1/2
as long as 2-P, which is single, 3-P long and strong. Fig. 13.21 Larva of Oc. theobaldi
364 13 Australia

warmer areas providing natural flooding or irrigation. with some pale scales. Sterna predominantly pale scaled
In inland areas, after heavy rains, they may appear in with dark apicolateral patches.
large numbers, sometimes invading towns. Day biting Larva: Antenna about half as long as the head,
is usually apparent as the species readily attacks slender and adorned with small, sharply pointed spic-
humans and other animals but they will bite also in the ules of varying number. Antennal seta (1-A) with 3–4
evening and at night in forests, scrubs or open country. branches inserted at about the middle of antennal shaft.
Oc. theobaldi may act as a major pest following exten- Labral seta (1-C) long and slightly curved, inner fron-
sive rain or flooding in western parts of its distribution tal seta (5-C) with 1–2 branches, median frontal seta
range and can disperse for many kilometers when there (6-C) single, outer frontal seta (7-C) with 6–7 branches.
are major larval populations. Prothoracic seta 1 (1-P) single, 2-P and 3-P with 2
Distribution: Australia. branches. The comb scales are arranged in an irregular
Medical importance: The species was success- triangular patch, individual scale small, strongly
fully infected with Murray Valley encephalitis virus in fringed and usually with a differentiated median spine.
laboratory studies and Ross River virus has been iso- Siphon short and stout, siphonal index about 1.5–2.0.
lated from natural populations, but its role in transmis- The pecten with 8–12 teeth, evenly and closely spaced,
sion of human disease is doubtful (Russell 1996). not reaching to the middle of the siphon (Fig. 13.22).
Siphonal tuft (1-S) with 7–9 branches inserted within
or beyond the pecten. Saddle almost covering anal seg-
 chlerotatus (Ochlerotatus) vigilax
O ment but incomplete, with a few short spicules at its
(Skuse 1889) posterior margin, saddle seta (1-X) single. Ventral
brush with 12–14 cratal setae (4-X), 1–3 precratal
Female: A medium sized mosquito of dark appearance setae present. Anal papillae short, narrow and
with pale ringed legs. Proboscis with yellowish or light pointed.
golden scales on basal 2/3 on ventral side (Fig. 13.14a),
sometimes forming a complete large ring. Palps <1/5
the length of proboscis, largely dark scaled with pale
apex. Pedicel of antenna with a few small dark scales.
Head with narrow decumbent scales, pale posteriorly
and sometimes in the middle, dark anteriorly, erect
scales dark, lateral and ventral broad scales largely
pale. Integument of scutum dark brown, scutal scales
all narrow, mostly dark bronze brown with some pale
golden scales intermixed. Scutellum with narrow yel-
lowish scales on all lobes, paratergite with a patch of
small whitish scales near the middle. Pleurites with
several patches of broad pale scales, namely propleural
patch, postspiracular patch, upper and lower mesepis-
ternal patches, mesepimeral patch restricted to upper
portion of sclerite, lower mesepimeral setae absent
(Fig. 13.12b). Femora and tibiae largely dark scaled,
mottled with pale scales, particularly ventrally and on
hind leg. Hind tarsus dark scaled with pale basal rings
on tarsomeres I–V (Fig. 13.11a). Wing predominantly
dark scaled (Fig. 13.13b) with scattered pale scales
mainly along the anterior border, some scattered pale
scales on the other veins, particularly along cubitus
(Cu), haltere knob largely pale scaled. Abdominal terga
largely dark scaled, terga II–VI with straight basal pale
bands and lateral pale patches, apices of terga V and VI Fig. 13.22 Larva of Oc. vigilax
13.2 Species Description 365

Biology: Oc. vigilax primarily breeds in brackish waters Terga VII–VIII with narrow, basal bands, tergum VIII
in mangrove swamps and salt marshes, ­occasionally usually broadly pale at apex, narrow apical dark bands
it is found in rock holes and freshwater ground pools. on sterna often incomplete.
Adults are most abundant in the summer months and Larva: As with the females, the larvae of Cx. annu-
are active from mid spring through autumn; the females lirostris closely resemble those of Cx. sitiens, differing
are very aggressive biters and attack humans and from the latter in the following characteristics: labral
domestic animals readily during the day in sheltered seta (1-C) dark, slender and spiniform, frontal setae
areas, but also at evening and night, with a peak about (5-C to 7-C) and antennal seta (1-A) stronger and
sunset (Belkin 1962a). This species is essentially darker than in Cx. sitiens. All abdominal setae darker
coastal and associated with estuaries and mangrove and stronger, 7-I with 2 branches. Comb scales usually
zones, but is reported to be a powerful flier and may be arranged in 4 irregular rows. Siphonal index extremely
found at considerable distances from the larval habitats variable, ranging from 5.0 to more than 10.0. Siphonal
(Mackerras 1927). Oc. vigilax is the major coastal pest setae (1-S) with 5 or 6 pairs of tufts, each with 6–10
species in large parts of southern and eastern Australia, branches, arranged in subventral rows (Fig. 13.23),
because it can disperse and be windblown for many none of the distal tufts detached laterally (as in Cx.
kilometers and can create nuisance problems over large sitiens). Saddle completely encircling anal segment,
and diverse areas. ventral part only slightly narrowed, saddle seta (1-X)
Distribution: Coasts of Australia, New Guinea, usually with 3 branches. Anal papillae slender, taper-
New Caledonia, Philippines, Indonesia, Thailand, ing apically, usually about as long as the saddle or
Indochina, Formosa, Solomon Islands, Fiji Islands, slightly longer.
New Zealand. Biology: Cx. annulirostris utilizes a variety of
Medical importance: Because of repeated virus ground pools as breeding habitats, the larvae can
isolations from natural populations, Oc. vigilax is frequently be found in pools, ponds, swamps, ditches,
regarded as the major vector of Ross River and Barmah
Forest viruses in coastal areas of New South Wales,
the species is also known to carry dog heartworm
(Russell 1996).

Culex (Culex) annulirostris Skuse 1889

Female: A medium sized mosquito of brownish to

dark appearance, extremely similar to Cx. sitiens and
very difficult to distinguish between females of the two
species. Cx. annulirostris differs in the following char-
acters: Median pale ring of proboscis broader, about
1/4 of its total length or slightly more. Acrostichal and
dorsocentral setae more strongly developed and longer
than in Cx. sitiens. Anterior surface of fore femur
evenly speckled with pale scales along the whole
length, anterior surface of fore tibia with a row of small
yellowish spots among anterior setae, anterior surface
of hind femur extensively speckled with pale scales.
Scales on all wing veins more numerous and longer
than in Cx. sitiens. Terga II–V with basal pale bands
relatively broad, moderately to strongly produced in
the middle (Fig. 13.5a), not straight and narrow as in
Cx. sitiens, basal band on tergum II sometimes incom-
plete or represented by a median triangular pale patch. Fig. 13.23 Larva of Cx. annulirostris
366 13 Australia

channels, and rice fields containing emergent vegeta- pale, erect scales usually entirely dark brown, occiput
tion. On occasion, they have been collected also from with lateral patch of broad whitish scales. Integument of
cacao shells and bamboo stumps (Dobrotworsky 1965; scutum dark brown; scutum mottled with variable spots
Delfinado 1966; Sirivanakarn 1976). In the South of coarse dark and pale scales, dark brown to golden
Pacific, the ­larvae have been reported to breed in almost brown scales usually predominant, pale yellow to golden
any type of permanent or temporary water, standing or scales on anterior and lateral margins, across the middle
flowing, clean or with a very high organic content, and around prescutellar area. Acrostichal and dorsocen-
fresh or brackish, in open sunlit as well as in strongly tral setae short and indistinct, supraalar setae strong and
shaded situations. They have been commonly found dense. Scutellum with pale yellowish scales and several
breeding in canoes and in various types of artificial strong setae. Antepronotum with several narrow dark or
containers such as shallow wells, cement tanks or rock golden brown scales, postpronotum with dark brown or
pools containing algae (Belkin 1962a). In south east- golden brown scales in the middle and pale scales pos-
ern Australia breeding places include freshwater wet- teriorly. Patches of pale scales on propleuron, upper and
lands and low-lying grassy areas that are commonly lower mesepisternum and mesepimeron distinct.
inundated following rain as well as irrigation. The Numbers of pleural setae are 9–17 prealar, 4–8 upper
adults are generally active from spring to late autumn, mesepisternal, 5–10 lower mesepisternal, 7–12 upper
they are regarded as the major summer pest of inland mesepimeral, lower mesepimeral setae absent. Scale
riverine areas, and the flight range is about 5–10 km patch of fore coxa pale on upper surface, largely dark or
(Russell 1996). The females feed readily on humans with a mixture of dark and pale scales on lower surface,
but also on other mammals and birds. It is a very scale patch on mid coxa dark above, pale below, scale
vicious mosquito, which may bite during the day but is patch on hind coxa entirely pale. Femora with whitish
particularly active after sunset, both indoors and in the knee spots, anterior surface of fore femur predominantly
open (Dobrotworsky 1965). Cx. annulirostris is con- dark scaled with a more or less definite whitish stripe on
sidered as a nuisance or serious pest of humans in most basal half, apical half speckled with pale scales, poste-
of its distribution range. rior surface whitish scaled. Anterior surface of mid
Distribution: Southern and western Australasian femur dark scaled except at base, speckled with pale
Region, Fiji Islands, Micronesia, South Pacific, Indonesia, scales, posterior surface whitish scaled. Anterior surface
Philippines. of hind femur largely pale, with narrow band of dark
Medical importance: Cx. annulirostris is an effi- scales at apex. Fore tibia largely dark scaled, without a
cient vector of a range of arboviruses in the laboratory row of pale spots among anterior setae (as in Cx. anu-
and has been incriminated in field studies as a vector of lirostris), mid and hind tibiae largely dark, sometimes
many arboviruses (including Murray Valley encepha- speckled with pale scales. Tarsi mainly dark scaled, hind
lites, Kunjin, Barmah Forest, Ross River viruses and tarsomere I pale scaled ventrally, tarsomeres I–III with
Japanese encephalites) in Australia. It is also able to narrow apical and basal pale rings, tarsomeres IV and V
carry dog heartworm and is probably a major vector of entirely dark scaled. Wing scales dark on all veins,
myxomatosis (Russell 1996). In New Guinea it is an sometimes some pale scales present at base of costa (C).
important vector of W. bancrofti (Belkin 1962a). Tergum I with a median patch of dark scales, terga III–
VIII with narrow, straight basal pale bands connected
with elongated basolateral pale spots, pale basal band on
Culex (Culex) sitiens Wiedemann 1828 tergum II somewhat widened in the middle (Fig. 13.5b).
Terga VII and VIII additionally with narrow apical pale
Female: Medium sized species, proboscis dark scaled, bands, that of tergum VII often strongly produced in the
with clearly marked median pale ring which occupies middle. Sterna II–VII with broad basal pale bands and
about 1/5 of its total length (Fig. 13.4a). Palps about 1/5 narrow apical dark bands.
of the length of proboscis, with some pale scales at apex, Larva: Antenna shorter than the head, with numer-
remainder dark, sometimes with pale scales laterally at ous spicules mostly restricted to basal part, distal part
base. Pedicel yellow, mesal surface dark brown with darker with a few spicules laterally. Antennal seta (1-A)
tiny setae and scales. Narrow decumbent scales of vertex inserted well beyond the middle of antennal shaft, multiple
13.2 Species Description 367

branched, setae 2-A and 3-A inserted subapically. Labral

seta (1-C) strongly flattened, dark, apex usually blunt.
Postclypeal seta (4-C) single, inner frontal seta (5-C)
with 5–8 branches, median frontal seta (6-C) with 3–6
branches (usually 4), outer frontal seta (7-C) with 8–10
branches. Prothoracic setae 1-P to 3-P strong, unequal
in length and single, 4-P shorter than the former, with 2
branches. Abdominal seta 6-I usually 3 branched, 7-I
about as long as 6-I, always single, 6-II with 3 branches,
6-III to 6-VI with 2 branches. The comb is composed of
about 35–40 small scales arranged in a broad triangular
patch, individual comb scale rather short and evenly
fringed with small spines. Siphonal index 3.6–4.9,
siphon with a dark basal ring and evenly tapering toward
the apex. The pecten consists of 6–17 evenly spaced
teeth restricted to the basal 1/4 to 1/3 of the siphon, the
distalmost teeth with 7–8 lateral denticles. Siphonal
tufts (1-S) usually with 7 pairs of multiple branched
setae, the basal tufts with 5–8 branches each, about
twice as long as diameter of siphon at point of origin.
One distal pair (1e-S) distinctly shorter and inserted lat-
erally, the others in an irregular row near ventral mid-
line, the distalmost pair (1g-S) about as long as 1e-S
(Fig. 13.24). Saddle completely encircling the anal seg-
ment, ventral part distinctly narrowed, dorsal posterior
Fig. 13.24 Larva of Cx. sitiens
margin with numerous spicules. Saddle seta (1-X) sin-
gle and rather long, upper anal seta (2-X) with 3–6
branches, lower anal seta (3-X) single. Ventral brush
usually with 12 tufts of cratal setae (4-X), anal papillae Medical importance: Possible vector of Japanese
very short, rounded, about half as long as saddle. encephalitis (JE). It has been found naturally infected
Biology: Cx. sitiens breeds primarily in coastal with Brugia malayi in Thailand (Harbach 1988).
brackish water habitats including pools, puddles,
ponds, wells, ditches and rock pools, in tidal marshes
and mangrove swamps. The larvae are occasionally  oquillettidia (Coquillettidia) xanthogaster
C
found in artificial containers such as canoes, boats, (Edwards 1924)
cement tanks, jars, cans in the vicinity of sea beaches,
harbors or piers in populated areas. The larvae and Female: A very distinctive mosquito of yellowish to
pupae are very adaptable and show a high tolerance of orange appearance. Proboscis and palps dark scaled,
salinity, occurring in fresh, brackish and even pure sea palps about 1/5 the length of the proboscis. Pedicel with
water (Hopkins 1952; Delfinado 1966; Sirivanakarn setae but no scales. Integument of head yellowish or
1976; Harbach 1988). Females feed primarily on birds light brown, decumbent scales golden, numerous later-
and pigs, but will bite man as well; in some areas of the ally, erect scales golden to light brown, very long.
South Pacific Cx. sitiens is reported as a vicious mos- Integument of scutum usually uniformly yellowish,
quito (Bram 1967a). sometimes darkened on midline, supraalar and pres-
Distribution: Cx. sitiens occurs in coastal areas of cutellar areas; scutal scales scanty, very narrow.
the Oriental Region, south western Asia, eastern Africa, Scutellum usually dull light brown or yellowish, with-
Madagascar, Ryukyu Archipelago, Korea, northern out any distinct scales. Pleurites uniformly yellowish,
Australia and many islands in the South Pacific. scales all broad, silvery. Mesepisternum with scales
368 13 Australia

largely confined to lower portion, mesepimeron with a

small patch of scales. Postspiracular setae absent, one
lower mesepimeral seta present. Legs dark scaled, hind
femur with pale golden scales on basal 1/3 of anterior
surface. Wing veins uniformly covered with dark ­narrow
scales, haltere knob with light brown scales. Abdominal
terga with light golden scales and some dark purplish
scales, sterna largely golden scaled, darker scales in
indistinct triangular apical median patches.
Larva: Head slightly broader than long, uniformly
pigmented. Antenna very long, more than twice as
long as the head, distal part of antenna flexible, about
as long as or longer than the basal part, which is covered
with small but distinct spicules. Antennal seta (1-A)
inserted at about the apical 1/3 of basal part, with mul-
tiple branches. Labral seta (1-C) very dark and stout,
moderately long, postclypeal seta (4-C) usually with 4
branches. Frontal setae (5-C to 7-C) multiple branched,
gradually increasing in length. Prothoracic setae 1 and
2 (1-P and 2-P) single, 3-P about half as long as the
others, with 4-5 branches. Abdominal segments II–V Fig. 13.25 Larva of Cq. xanthogaster
with seta 3 (3-II to 3-V) rather strongly developed,
usually with 1–2 branches. The comb consists of 7–9
scales arranged in a single row, individual scale long (2-X and 3-X) with multiple branches, unequal in
and slender, with a prominent median spine and fringed length. Ventral brush with 8 tufts of cratal setae (4-X),
with small lateral spicules. Setae 3-VIII to 5-VIII precratal setae absent. Anal papillae about as long as
inserted very close together, seta 3-VIII very long, the saddle, pointed.
always single and usually inconspicuously feathered. Biology: The larvae of Cq. xanthogaster can be
Siphon short and conical, heavily sclerotized at the found in grassy freshwater swamps, lagoons and
base and beyond the middle, modified for piercing creeks, usually heavily shaded and overgrown with
plant tissue, siphonal seta (1-S) usually with 4 branches. various aquatic plants (Belkin 1962a). Eggs are laid in
Anal segment much longer than wide, completely rafts on the water surface. The adults rest primarily on
encircled by the saddle, which is moderately pig- vegetation in the immediate vicinity of their breeding
mented except for a dark basal ring, and with numer- sites, the females are persistent and vicious biters in
ous small spicules dorsally. Saddle seta (1-X) short, early morning and during the day close to the breeding
multiple branched, inserted dorsally near the posterior places (Perry 1949). This species is a major pest in
margin of the saddle, 3 pairs of short, multiple branched many parts of northern Australia (Russell 1996).
accessory setae present on saddle as well, resembling Distribution: Australia, New Hebrides, New
the saddle seta (Fig. 13.25). Upper and lower anal setae Caledonia.
Chapter 14
Central and South America

A survey of mosquito breeding places in a municipal ferox is described in the North America section, having
cemetery in Curitiba, Paraná State, Brazil, revealed the status of a major pest there too. It is also widespread
about 60,000 flower vases, with the potential to sup- (from Mexico to Argentina) throughout Central and
port a population of approximately 12 million Cx. p. South America and together with other Psorophora sp. is
quinquefasciatus1 and Oc. fluviatilis [Georgecraigius a great nuisance in some areas (Anonymous 1992, 1994,
fluviatilis] larvae per year (Lozovei and Chahad 1998a–c, 2002). Accordingly, Ps. ferox is included in the
1997). key of Central and South America and described in
The primary Central and South American pest species Chap. 15 (North America).
Oc. albifasciatus, a vector of WEE, occurs in very large In addition to the seven primary vectors of malaria,
numbers in Argentina, and at densities above the economic four other anophelines of secondary importance An. albi-
threshold of 2,500 mosquitoes captured per night, will tarsis (Guatemala to Argentina, most important in Central
affect beef and dairy production (Gleiser and Gorla 2007). America), An. aztecus (Central America), An. bellator
Two more important Ochlerotatus pest species; Oc. tae- (Carribean Islands and Brazil) and An. cruzii (Costa Rica
niorhynchus and Oc. sollicitans are troublesome in Central to Argentina) are also worth mentioning (Anonymous
America and Caribbean. Oc. mediovittatus [Gymnometopa 1992, 1994, 1998a–c, 2002).
mediovittata] could be an important dengue vector in For further, more detailed information on the mor-
Central America and Venezuela (Rueda 2004). phology, identification, biology, distribution, and dis-
However, Cx. p. quinquefasciatus1 is the main nui- ease vector status of the species mentioned, the reader
sance mosquito throughout Central and South America, is referred to Lane (1953), Garcia and Ronderos (1962),
especially in urban areas. Over 200 bites/person/night Cova Garcia et al. (1966), Bram (1967b), Mattingly
have been recorded in several areas of the Martinique (1971), Smith (1973), Vargas (1974), Cova Garcia and
island (Yebakima 1996). It is included in the key together Sutil Oramas (1977), Faran (1980), Faran and Linthicum
with Cx. p. pipiens1, Ae. aegypti1 and Ae. albopictus1, (1981), Clark-Gil and Darsie (1983), Darsie (1985),
the cosmopolitan and invasive species described in Mitchell and Darsie (1985), Wilkerson and Strickman
Chap. 10 (culicine mosquitoes of Europe). Psorophora (1990), Rueda (2004), Reinert et al. (2005).

14.1 Key to Central and South American Female Mosquitoes

1 Palps about as long as proboscis. Scutellum evenly rounded or slightly trilobed and uniformly setose
(Fig. 14.1a). Abdominal terga and sterna completely or largely missing scales. – Proboscis not strongly recurved
and not tapering towards apex, Anopheles. Integument of scutum without a silvery longitudinal stripe. Wing scales of two
or more colours. Vein R4+5 with several pale spots or largely pale scaled. Hind femur without a tuft of erect scales on distal
third. Hind tarsomeres II–V not all with pale rings, sometimes entirely dark scaled.. ................................................... 2

Species described in Chap. 10 concerning European mosquitoes.

1

N. Becker et al., Mosquitoes and Their Control, 369

DOI 10.1007/978-3-540-92874-4_14, © Springer-Verlag Berlin Heidelberg 2010
370 14 Central and South America

Palps distinctly shorter than proboscis. Scutellum trilobed, setae arranged in three sets (Fig. 14.1b).
Abdominal terga and sterna uniformly and densely covered with scales. – Proboscis not strongly recurved and
not tapering towards apex. Postnotum without a tuft of setae. Squama with fringe of setae. Anal vein (A) ending well beyond
the furcation of cubitus (Cu). Veins R2 and R3 at least as long as vein R2+3, usually much longer..................................... 8

Fig. 14.1 Scutellum of: (a) Anopheles sp.; (b) Aedes sp. Fig. 14.2 Hind tarsus of: (a) An. albimanus; (b) An. darlingi;
(c) An. pseudopunctipennis

2 (1) Tarsomeres III and IV of hind legs entirely white (Fig. 14.2a,b). Acrostichal and dorsocentral areas of
scutum with numerous scales. Anopheles subgenus (Nyssorhynchus) – At least half of anal vein (A) pale scaled.
At least some of abdominal terga II–VII with scales and posterolateral scale tufts....................................................... 3
Tarsomeres III and IV of hind legs not entirely white, could be completely dark (Fig. 14.2c). Acrostichal
and dorsocentral areas at most with scattered scales. Anopheles subgenus (Anopheles) – Hind leg without
distinct, large tibiotarsal patch of pale scales......................................................................................................... 6
3 (2) Tarsomere V of hind legs with a basal dark scaled ring (Fig. 14.2a)........................................................... 4
Tarsomere V of hind legs completely pale scaled (Fig. 14.2b). – Palpomere IV with scattered white scales on
mediolateral surface. Scutellum usually with more than 12 large, dark setae on posterior margin. Anteromedian mesepimeral
patch of pale scales present. Upper mesepimeral patch absent. Costa (C) with basal dark spot about four times as long as
second pale spot. Vein R3 with three dark spots. Sternum I completely devoid of scales................. An. darlingi (p 378)
4 (3) Palpomere IV all dark or with yellow to golden brown (never white or creamy) scales on mediolateral
surface (narrow apical pale ring sometimes present). Palpomere V entirely pale. Tarsomere V of fore
legs usually entirely dark scaled. Abdominal tergum II without a pair of posterolateral tufts of dark
scales (Fig. 14.3a)..................................................................................................... An. albimanus (p 376)
Palpomeres IV and V almost entirely pale scaled, separated by a dark ring. Tarsomere V of fore legs variable.
Abdominal tergum II with pair of posterolateral tufts of dark scales (Fig. 14.3b). – Anteromedian part of mese-
pimeron without a patch of pale scales. Upper mesepimeron usually without pale scales. Tarsomere IV of fore legs predomi-
nantly dark scaled, or if pale in more than apical 1/3, then at least the apical half of fore tarsomere V pale scaled. Tarsomere II
of hind legs with basal dark ring covering at least 1/4 length of tarsomere. If dark ring covers less than 1/4, then humeral light
spot on costa (C) less than 1.5 length of basal dark spot on C. Pale wing spots at least on costa (C) and radius (R) creamy to
yellowish, not white. Subcostal pale spot of costa (C) usually less than 1/2 the length of subcostal dark spot........................ 5

Fig. 14.3 Palps of: (a) An. albimanus; (b) An. aquasalis Fig. 14.4 Hind tarsus of: (a) An. aquasalis; (b) An. nuneztovari
14.1 Key to Central and South American Female Mosquitoes 371

5 (4) Tarsomere II of hind legs with basal dark ring covering 1/3 to 1/2 length of tarsomere. Hind tarsomere V
with a narrow dark basal ring (Fig. 14.4a). (separation from An. benarrochi uncertain)..............................
.................................................................................................................................... An. aquasalis (p 377)
Tarsomere II of hind legs with basal dark ring covering less than 1/3 the length of the
tarsomere. Hind tarsomere V with basal half dark (Fig. 14.4b). – Costa (C) with humeral pale spot less than twice
the length of basal dark spot.......................................................................................... An. nuneztovari (p 380)
6 (2) Tarsi entirely dark scaled (Fig. 14.2c). – Costa (C) with only two pale spots. Anal vein (A) with less than four dark
spots.. ..........................................................................................................An. pseudopunctipennis (p 374)
Tarsi not entirely dark scaled (Fig. 14.5a,b). – Hind tarsomeres I–IV with several irregular dark and pale scaled spots
or rings. Hind tarsomere V mainly pale scaled with median dark ring or spot. Wing not indented at junction of subcosta (Sc)
and costa (C). Scales of wing broad, mainly on basal portion of wing. Costa with two pale spots near the junction of the
subcosta. Abdomen usually with short dorsolateral scale tufts.................................................................................. 7
7 (6) Upper mesepimeron with a small patch of pale scales. Hind tarsomere V usually pale scaled, sometimes
with a small dark spot (Fig. 14.5a)............................................................................. An. calderoni (p 374)
Upper mesepimeron bare. Hind tarsomere V usually with a median dark ring (Fig. 14.5b).........................
.............................................................................................................................An. punctimacula (p 375)

Fig. 14.5 Hind tarsus of: (a) An. calderoni; Fig. 14.6 Dorsal view of thorax of: (a) Haemagogus sp.;
(b) An. punctimacula (b) Ae. aegypti

8 (1) Prespiracular setae present (Fig. 14.7a). – Postspiracular setae present. Abdomen tapering apically, cerci long, easy
visible, Psorophora. Scutum with dark brown and golden yellow scales mixed, without forming specific pattern. Femora
without subapical ring of pale scales. Apices of femora without erect scales. Tarsomeres IV and V and often apex of tarso-
mere III of hind tarsus pale scaled. Wing veins uniformly dark scaled or relatively few pale scales present at anterior border.
Abdominal terga with apicolateral patches of pale scales.................................................................Ps. ferox (p 395)
Prespiracular setae absent (Fig. 14.7b). – Antenna subequal to proboscis, not short, thick and tapering. Flagellomere
I without a prominent tuft of setae or scales. Mid and hind femora without large tuft of semi erect scales.................... 9

Fig. 14.7 Lateral view of thorax of: (a) Psorophora sp.; (b) Ochlerotatus sp.
372 14 Central and South America

9 (8) Lobes of antepronotum very large, narrowly separated at midline of scutum, commencing before ante-
rior margin of scutum (Fig. 14.6a). Scutum covered with broad, decumbent scales with bright metallic
shine (green, blue, copper or bronze with silver scales only in supraalar area), Haemagogus. – Pleurites
with single vertical line of pale scaled patches. Lower mesepisternal seta well developed (separation from Hg. capricorni
uncertain). ............................................................................................................Hg. janthinomys (p 381)
Lobes of antepronotum small and broadly separated, commencing beyond anterior margin of scutum
(Fig. 14.6b). Scutum covered with narrow scales without metallic shine. – Flagellomere I of similar length
as flagellomere II. Apex of proboscis not distinctly swollen. Tarsomere I of fore legs usually shorter than tarsomeres II–V
together. Tarsomere IV of fore legs not reduced, distinctly longer than broad........................................................ 10
10 (9) Postspiracular setae present (Fig. 14.8a) and/or claws of fore legs with subbasal tooth....................... 11
Postspiracular setae absent (Fig. 14.8b). All tarsal claws simple. – Antennae not longer than proboscis.
Flagellomere I and II of similar length. Vertex and occiput with narrow decumbent scales. Scutum with acrostichal setae.
Usually no more than 1 or 2 lower mesepimeral setae present. Hind tarsal claws very small and inconspicuous. All tarsi
with well developed pulvilli. Hind tarsomere I as long as or longer than hind tibia. Tarsomeres usually without distinct
white rings. When pale rings are present, they are narrow and basal. Wing scales usually narrow. Costa (C) without alter-
nating brown and yellow scaled areas. Culex subgenus (Culex)..................................................................... 15

Fig. 14.8 Lateral view of thorax of: (a) Ochlerotatus sp.; (b) Culex sp.

11 (10) Wing scales usually narrow, if broad then not strongly asymmetrical (Fig. 14.9a). Claws of at least fore
legs usually with subbasal tooth............................................................................................................ 12
Wing scales mostly broad and many conspicuously asymmetrical (Fig. 14.9b). Claws all simple, with-
out subbasal tooth. Mansonia subgenus (Mansonia) – erect forked scales numerous, not restricted to occiput.
Palps about 1/3 as long as proboscis. Palpomere III more than twice as long as palpomere II. Scutum without anterolateral
golden scaled spots. Postspiracular setae present. Upper mesepimeral scale patch present. Femora speckled with pale
scales, without rings or spots. Hind tibia without erect scales. Hind tarsomere I without a median pale ring. Abdominal
terga with dark and pale scales. Abdominal terga VII and VIII with row of fine spines apically (on tergum VIII visible only
when dissected).. .......................................................................................................... Ma. titillans (p 385)
12 (11) Decumbent scales of vertex largely broad. Erect scales not numerous, restricted to occiput
(Fig. 14.10a). – Scutum with white or silvery scales in lines or patches. Scales of scutellum all broad. Femora with
white knee spot. Aedes subgenus (Stegomyia)........................................................................................... 13
Decumbent scales of vertex largely narrow and/or (if scales of vertex are largely broad) erect scales
numerous, not restricted to occiput (Fig. 14.10b). Ochlerotatus........................................................... 14
14.1 Key to Central and South American Female Mosquitoes 373

Fig. 14.9 Wing scales of: (a) Aedes sp.; (b) Mansonia sp. Fig. 14.10 Head of: (a) Aedes (Stegomyia) sp.; (b) Ochlerotatus sp.

13 (12) Scutum with a white acrostichal stripe extending from the anterior margin to the beginning of the
pre­scutellar area, where it forks to end at the anterior margin of scutellum (Fig. 14.11a).
............................................................................................................................... Ae. albopictus (p 201)
Scutum without acrostichal stripe on anterior part, but with two narrow white dorsocentral stripes sepa-
rated from anterior margin. Lateral white stripes broad, continuing over transverse suture
to the end of scutum, lyre shaped (Fig. 14.11b).......................................................... Ae. aegypti (p 198)

Fig. 14.11 Scutum of: (a) Ae. albopictus; (b) Ae. aegypti Fig. 14.12 Abdomen of: (a) Cx. nigripalpus; (b) Cx. p. pipiens

14 (12) Wing veins with pale and dark scales. – Scales on wing intermixed, not forming distinct spots. Terga with a median
longitudinal pale stripe. ......................................................................................... Oc. albifasciatus (p 382)
Wing veins entirely dark scaled. – Hind tibia with distinct pale stripe on anterior surface, sometimes encircling tibia.
Hind tarsomeres completely dark scaled. Scutum with large patch of silvery white/yellowish scales on anterior 2/3.
Posterior 1/3 often with narrow stripes (e.g. prescutellar dorsocentral stripe) in continuation of large pale scaled patch.
Terga without pale basal bands, basolateral spots can be present. Posterior terga usually with indistinct longitudinal
pale stripe.................................................................................................................Oc. scapularis (p 383)
374 14 Central and South America

15 (10) Pale basal bands on abdominal terga usually absent, if present they are narrow, or pale scaling restricted
to lateral patches (Fig. 14.12a). – Palps short, less than 1/4 length of proboscis. Lower mesepimeral seta present.
Mesepisternum with two patches of broad pale scales, each patch usually of less than 6 scales. Tergum VII mostly covered
with dark scales.. .....................................................................................................Cx. nigripalpus (p 384)
Abdominal terga with a rather broad (about 1/4 of the terga) basal transverse band of pale scales
(Fig. 14.12b). Bands rounded on posterior margin and constricted sublaterally, rather narrowly
joining (sometimes disconnected) lateral pale patches. – Pale spot at tip of hind tibia inconspicuous...............
............................................ Cx. p. pipiens biotype molestus and Cx. p. quinquefasciatus (p 277, 278)

14.2 Species Description Biology: An. calderoni has been encountered only
at elevations < 250 m (north western Peru) and between
200 and 400 m (western Venezuela) (Rubio-Palis and
 nopheles (Anopheles) calderoni
A
Moreno 2003). The larvae are found in small streams,
Wilkerson 1991
small irrigation canals and swamps, mostly in dense
emergent vegetation, but especially associated with
Female: An. calderoni is very similar to An. puncti-
Typha sp. (Wilkerson 1991).
macula in all live stages and the two species are very
Distribution: Peru, Venezuela.
difficult to differentiate; nevertheless, both are regarded
Medical importance: This species must be regarded
as distinct species. In An. calderoni the upper mesepim-
as an important malaria vector at least in the lowlands
eron is clothed with a small patch of pale scales, and the
of northwestern Peru.
hind tarsomere V usually is pale scaled (Fig. 14.5a),
sometimes with a dark spot, whereas in An. punctimac-
ula the mesepimeron is bare of any scales and the hind  nopheles (Anopheles) pseudopunctipennis
A
tarsomere V usually has a median dark ring. Additional Theobald 1901
differences exist in the ornamentation and colour pattern
of the wing veins, and in the larvae, in the mean number Female: Medium sized species. Proboscis dark scaled,
of branches of certain setae (Fig. 14.13); for more infor- palps about as long as the proboscis, yellowish white
mation see Wilkerson (1991). at tip and with 2 narrow white rings at joints of basal
palpomeres, remainder of palps dark scaled. Integument
of head brown, occiput covered with erect forked
scales, which are whitish in the middle, otherwise dark
brown. Scales of vertex pale, a prominent set of long
frontal scales directing forward. Integument of scutum
dark brown, with a median broad greyish stripe, which
is sparsely covered with narrow yellowish scales,
acrostichal and dorsocentral setae pale, the dark lateral
areas with longer dark setae. Scutellum with long
brown and yellowish setae. Integument of pleurites
brown with some darker areas. Legs almost entirely
dark scaled, apices of femora and tibiae with whitish
scales, tarsi dark (Fig. 14.2c). Wing veins covered with
dark and pale scales arranged in a well defined pattern
of dark and pale spots and lines. Basal portion of costa
(C) dark scaled, with two pale spots at junction of sub-
costa (Sc) and near apex of wing, vein R4+5 narrow
white at base, followed by a dark area, a broad white
Fig. 14.13 Larva of An. calderoni, terga I–IV area and a narrow dark tip, anal vein (A) with basal
14.2 Species Description 375

half white, apical half dark, tip white. Haltere stem season when the streams are not subject to flushing by
pale, knob dark scaled. Integument of abdomen dark heavy rainfall (Carpenter and La Casse 1955). A com-
brown, clothed with brown setae, scales absent. mon character of all breeding sites is the presence of
Larva: Antenna <1/2 as long as the head, smooth floating vegetation and particularly green algae. The
on outer surface, spiculate on inner surface. Antennal feeding habits and host preferences of the adults appear
seta (1-A) short, usually single, inserted below the to differ markedly in the different regions, raising the
middle of the antennal shaft. Inner clypeal setae (2-C) possibility of different forms or varieties. In its more
situated close together, closer to each other than to southern distribution range the species is anthropo-
outer clypeal setae (3-C), all setae long, subequal in philic, the females feed at night and will enter houses
length and single. Postclypeal seta (4-C) long and to take a blood meal. A flight range of 6–10 km is
single, all frontal setae (5-C to 7-C) long and plu- recorded (Gorham et al. 1973).
mose. Prothoracic seta 1 (1-P) short, usually with 2–4 Distribution: An. pseudopunctipennis is probably
branches beyond the base, 2-P and 3-P arising from a the most widespread anopheline mosquito in the New
common tubercle, 2-P long and stout, with many lat- World, ranging from the western and southern United
eral branches, 3-P single, about twice as long as 1-P. States through Central America, Colombia, Venezuela
Palmate setae on segments I and II (1-I and 1-II) rudi- and the Antilles and southward following the Andes to
mentary, well developed on segments III–VII (1-III north eastern Argentina. The species can be found
to 1-VII), leaflets long and slender, with serrations from lowland to dry mountains and plateaus up to an
beyond the middle. Lateral abdominal seta 6 on seg- altitude of about 2,600 m.
ments I–III (6-1 to 6-III) long and plumose. Posterior Medical importance: An. pseudopunctipennis is
spiracular plates each with a long and slender sclero- regarded as an important vector of malaria in some but
tized projection arising from the posterior margin. not all areas of its wide distribution range.
These are bent upward at right angles to the plates and
project through the water surface (Fig. 14.14). The
pecten plate with 7–8 long teeth alternated by 1 or  nopheles (Anopheles) punctimacula
A
2 shorter teeth. Dyar and Knab 1906
Biology: The larvae are frequently found in sunny
habitats including sidepools of streams, in lagoons and Female: A large species with speckled legs. Proboscis
canals, in swamp meadows, or poorly kept drainage long and slender, dark scaled. Palps predominantly
systems (Aitken 1954b). They are abundant in shallow, dark scaled, palpomere V with basal white ring, pal-
receding streams in mountainous areas during the dry pomere IV with narrow basal white ring, palpomere
III often with a few white scales at the base. Pedicel
dark brown with a few pale scales. Vertex with a tuft
of long pale scales projecting forward, a few whitish
scales along the eye margin, occiput covered with
erect forked scales, pale anteriorly, dark posteriorly.
Integument of scutum grey, with 3 larger conspicuous
dark spots, anterior margin of scutum with a promi-
nent median tuft of long white setae and elongated
white scales. Scutum clothed with long yellowish
setae, scutellum with a median dark spot, covered
with long dark setae. Mesepimeron without any scale
patches. Femora and tibiae predominantly dark scaled
with many white spots on dorsal surfaces. Fore tar-
somere I dark with several white spots and white apex,
tarsomeres II–IV with white scales at base and apex,
tarsomere V entirely white scaled. Mid tarsomere I
dark with several white spots and white apex, tarsom-
Fig. 14.14 Larva of An. pseudopunctipennis eres II–IV with several white rings, tarsomere V with
376 14 Central and South America

a dark ring in the middle. Hind tarsomere I dark on

dorsal surface, yellowish ventrally, the dorsal part
with several white spots, tarsomere II with narrow
white rings at base and apex and several white spots,
tarsomeres III and IV with white rings at base, apex
and middle, tarsomere V usually with a dark ring in
the middle (Fig. 14.5b). Wing veins covered with
broad pale and dark scales forming a characteristic
pattern. Costa (C) with 3 prominent dark spots, involv-
ing also subcosta (Sc) and radius (R). Subapical white
spot very small, cubitus (Cu) with pale and dark scales
intermixed. Wing fringe predominantly dark, inter-
rupted by conspicuous white spots. Halter stem pale,
knob dark and pale. Integument of abdomen dark
brown, covered with long brown setae. Lateral tufts of Fig. 14.15 Larva of An. punctimacula
dark brown scales on terga II–VII.
Larva: Antenna sparsely spiculous, antennal seta
(1-A) very large, about 2/3 the length of the antenna, also enter dwellings and readily feed on humans; their
with multiple branches, inserted at basal 1/3 of anten- flight range is about 3 km.
nal shaft. Inner clypeal seta (2-C) long, single, the Distribution: Central America, Mexico, Venezuela,
pair of 2-C situated close together, outer clypeal seta Trinidad, Colombia, Brazil, Peru, Ecuador, Bolivia,
(3-C) nearly as long as 2-C, usually dendriform Argentina.
beyond the middle, sometimes with a few branches Medical importance: An. punctimacula is an effi-
apically. Postclypeal seta (4-C) small, with 2–3 cient malaria vector in much of its distribution range.
branches, frontal setae (5-C to 7-C) long and plu-
mose. Prothoracic setae 1 to 3 (1-P to 3-P) not arising
from a common tubercle, P-1 about 1/2 as long as  nopheles (Nyssorhynchus) albimanus
A
2-P, with long lateral branches, 2-P long and strong, Wiedemann 1820
pinnately branched, 3-P short and single. Palmate
setae rudimentary on segments I and II (1-I and 1-II), Female: Medium sized greyish species. Proboscis
well developed on abdominal segments III–VII (1-III dark scaled, palps about as long as proboscis, pre-
to 1-VII), with 15–20 leaflets. Individual leaflet short dominantly dark scaled, palpomere V entirely white
and broad, strongly pigmented at the base, margin (Fig. 14.3a), apices of palpomeres II and III with
serrated beyond the middle, apex smooth, pointed. narrow ring of white scales. Occiput with white erect
Tergal plate on abdominal segment VIII larger than forked scales dorsally, dark scaled laterally, vertex
the others. Lateral abdominal setae 6 of segments IV with frontal tuft conspicuous, white. Flagellomere I
and V (6-IV and 6-V) long and slender, single, seta of antenna with a conspicuous tuft of white scales.
6-VI with 2–4 branches, seta 5-VIII with 3–5 Integument of scutum grey or greyish brown with 3
branches. The pecten plate bears 15–16 short and conspicuous dark spots. Scutum clothed with grey
long teeth regularly alternating, about 7 long teeth. scales and pale setae, the setae more numerous later-
Saddle seta (1-X) not inserted on the saddle, but close ally. Scutellum covered with greyish scales and yel-
to its ventral margin (Fig. 14.15). lowish brown setae. Antepronotum with a patch of
Biology: The larvae of An. punctimacula may be erect dark scales in upper part, upper and lower part
found in jungle pools, temporary grassy pools, swamps, of mesepimeron with a few pale scales. Prespiracular
and along mountain streams up to an elevation of setae present, postspiracular setae absent. Femora
1,500 m. The breeding sites are usually well shaded and tibiae predominantly dark scaled, sparsely
and rich in organic matter (Ross and Roberts 1943; speckled with pale scales, with white scales at api-
Horsfall 1955). The females are regarded as being zoo- ces, mid and hind femora each with a pale subapical
philic with a preference for domestic animals, but they spot. Fore tarsus with tarsomere I narrowly white
14.2 Species Description 377

ringed at apex, tarsomeres II and III white apically,

tarsomeres IV and V entirely dark. Mid tarsus with
narrow indistinct white rings at apices of tarsomeres
I and II, tarsomeres III–V entirely dark. Hind tarsus
with tarsomere I entirely dark except for a few white
scales at apex, tarsomere II dark on basal half and
white on apical half, tarsomeres III and IV entirely
white, tarsomere V dark basally and white apically
(Fig. 14.2a). Wing scales dark and yellowish white,
arranged on the veins in contrasting lines and spots,
haltere with the stem pale, knob dark scaled.
Integument of abdomen dark brown to black, clothed
dorsally with long setae and few pale scales, the
scales more numerous in the middle of the last seg-
ments. Tufts of dark scales present laterally on terga
III–VII, absent on tergum II. Sterna V–VII with a
few scattered pale scales laterally, a conspicuous Fig. 14.16 Larva of An. albimanus, terga I–IV
submedian patch on sternum II.
Larva: Antenna shorter than the head, with very
strong short spicules on inner surface, antennal seta and floating algae, and frequently have muddy bot-
(1-A) short, only slightly longer than width of anten- toms and turbid or polluted water. The larvae exhibit
nal shaft at point of origin, inserted on basal 1/3 of a strong preference for breeding sites exposed to
shaft, with 2–4 branches. Inner and outer clypeal full sunlight, they are rarely found in densely shaded
setae (2-C and 3-C) single, finely to strongly acicu- pools (Belkin et al. 1970). The adults are strong fli-
late, their bases about equally spaced one from ers and feed readily on humans and domestic ani-
another. Postclypeal seta (4-C) single or apically mals, particularly horses and cattle. They may also
branched, frontal setae (5-C to 7-C) long, plumose. enter houses to feed at night, but usually return to
Prothoracic setae 1 and 2 (1-P and 2-P) arising from the jungle or breeding grounds before daylight.
a common sclerotized tubercle, 1-P about half (Carpenter and La Casse 1955). The species may be
as long as 2-P, both setae with shaft thickened and found throughout the year, predominantly in the
with many lateral branches, 3-P small, single. lowlands, its elevation limit may be restricted to less
Metathoracic palmate seta (3-T) with numerous than 500 m.
slender transparent leaflets. Palmate setae well devel- Distribution: Antilles, Central America, Mexico,
oped on abdominal segments I–VII (1-I to 1-VII), United States (Florida, Texas), Venezuela, Surinam,
smaller on segments I and II, leaflets slender, with Brazil, Ecuador, Colombia, Peru, Uruguay.
smooth margins, not serrated. Lateral abdominal seta Medical importance: An. albimanus is generally
6 on segments I–III (6-I to 6-III) long, plumose, on regarded as the principal lowland vector of malaria
segments IV–VI (6-IV to 6-VI) long and usually throughout much of Central America, northern South
single (Fig. 14.16). The pecten plate has 3–4 long America and the West Indies.
teeth alternated by 2–3 shorter teeth laterally and
6–7 shorter teeth in the middle.
Biology: The larvae of An. albimanus are found  nopheles (Nyssorhynchus) aquasalis
A
in a wide variety of mostly permanent water habi- Curry 1932
tats, either fresh or brackish, e.g. irrigation ditches,
ground pools, ponds, and shallow margins of Female: Medium sized species, proboscis slender, dark
streams, lakes and swamps; water filled hoof prints scaled. Palpomere V entirely white scaled, palpomere
in cow pastures are also often inhabited (Carpenter IV with narrow dark rings at base and apex, palpomere
and La Casse 1955). The various breeding sites usu- III with a narrow white ring at apex, rarely with an
ally contain abundant floating, emergent vegetation indistinct line of pale scales dorsally (Fig. 14.3b).
378 14 Central and South America

Pedicel dark with a few pale scales, vertex with a tuft

of long pale scales projecting forward. Integument of
scutum greyish brown, with a darker median line and 3
conspicuous dark spots, covered with curved pale
scales and dark setae, supraalar setae long and pale.
Scutellum covered with pale scales and long dark
setae. Femora and tibiae with dark scales on dorsal
surfaces and yellowish scales ventrally. Fore tarsomere
I dark dorsally and yellowish ventrally, with a narrow
apical pale ring, tarsomeres II and III with more than
the basal half dark scaled and pale scales apically, tar-
someres IV and V entirely dark. Mid tarsomeres I–III
narrowly ringed with pale scales at the apex, tarsom-
eres IV and V entirely dark scaled. Hind tarsomere I
dark scaled dorsally and yellowish ventrally, tarsomere
II with 1/3 to 1/2 of the basal portion with dark scales,
remainder white, tarsomeres III and IV all white, tar- Fig. 14.17 Larva of An. aquasalis, terga I–IV
somere V with a narrow dark basal ring (Fig. 14.4a).
Wing veins covered with pale and dark scales produc-
ing pale and dark spots of variable appearance, second coast, however, it is capable of breeding in fresh water,
pale spot on costa (C) usually longer than the follow- and sometimes is collected several kilometers from the
ing dark spot. Haltere stem pale, knob dark. Integument coast. The habitats may be permanent or temporary,
of abdomen dark brown, covered with long brown and with or without aquatic vegetation. Females read-
setae, terga II–VII with lateral tufts of dark brown ily feed on humans and livestock; they are usually exo-
scales. philic and exophagic, and show a crepuscular biting
Larva: Antenna with dense spicules on inner sur- behaviour with a major peak at dusk and a minor peak
face, antennal seta (1-A) short, inserted well below the at dawn (Berti et al. 1993). After the blood meal they
middle of the antennal shaft, with 3–4 branches. Inner rest in the nearby vegetation, such as tall grasses. The flight
and outer clypeal setae (2-C and 3-C) long, single, dis- range of this species does not usually exceed 3–5 km
tinctly feathered beyond the middle. The distance (Horsfall 1955). Adult populations may occur in great
between the bases of the pair of 2-C slightly shorter numbers, especially during the rainy season.
than the distance between 2-C and 3-C. Postclypeal Distribution: Panama Canal Zone, Colombia,
seta (4-C) with 2–3 branches, frontal setae (5-C to 7-C) Ecuador, Brazil, Guianas, Venezuela, Trinidad, Tobago,
long and plumose. Prothoracic seta 1 (1-P) of palmate Lesser Antilles, Costa Rica, Nicaragua.
type, with 12–15 lanceolate leaflets, not arising from a Medical importance: An. aquasalis is regarded
common tubercle with 2-P, which is long with a strong as the main vector of coastal Plasmodium vivax
shaft and laterally branched, 3-P long, single. Palmate malaria from north eastern Venezuela to southern
setae developed on abdominal segments I–VII (1-I to Brazil (Fleming 1986).
1-VII), 1-I with about 14 leaflets, not pigmented and
much smaller than 1-II to 1-VI, which have about 20
narrow and lanceolate leaflets. Tergal plates oval, larg- Anopheles (Nyssorhynchus) darlingi Root 1926
est on abdominal segment VIII. Lateral abdominal
setae 6 of segments IV to VI (6-IV to 6-VI) long and Female: Medium sized greyish species, proboscis
single, rarely with 2 branches (Fig. 14.17). The pecten slender, dark scaled. Palpomere V entirely white
plate bears about 14 straight teeth, long and short teeth scaled, palpomere IV dark at base and apex with a few
irregularly arranged. white scales in the middle, palpomere III dark with a
Biology: An. aquasalis is a typical brackish water conspicuous white ring at apex and a few white scales
breeder, the larvae can primarily be found in swamps, dorsally, palpomere II dark scaled with a few white
usually mangroves, pools, and ditches along the sea scales at apex. Pedicel dark with a few pale scales.
14.2 Species Description 379

Vertex with a tuft of long pale scales projecting for-

ward, occiput covered with erect forked scales, pale
anteriorly, dark posteriorly. Integument of scutum dark
grey, with a median longitudinal black line and 3 con-
spicuous dark spots, anterior margin of scutum with a
prominent tuft of long white setae and white scales.
Scutum clothed with curved yellowish white scales
and short dark setae, scutellum covered with pale
scales and long dark setae. Femora and tibiae with
dark scales on dorsal surface and yellowish scales ven-
trally. Fore tarsomere I dark scaled, with a narrow api-
cal pale ring, tarsomeres II and III with a broad apical
white ring, tarsomeres IV and V entirely dark scaled. Fig. 14.18 Larva of An. darlingi
Mid tarsomeres I–III narrowly ringed with pale scales
at the apex, tarsomeres IV and V entirely dark scaled.
Hind tarsomere I dark scaled dorsally, somewhat paler project up through the water surface into the air when
ventrally, with a very narrow apical white ring, tarsom- the larvae are resting. The pecten plate bears 3–4 long
ere II with the basal half dark, apical half white, tar- teeth and 11–13 short ones with a single long tooth at
someres III–V all white scaled (Fig. 14.2b). Wing the ventral end. The other long teeth are more or less
veins covered with pale and dark scales in a more or evenly spaced, the last two or three teeth at the dorsal
less variable pattern, second pale spot on costa (C) end of the pecten are short ones.
usually much shorter than the following dark spot. Biology: The larvae of An. darlingi occur in fresh
Subcostal and preapical pale spots both small. Haltere water or water of low salt content usually in partial
with stem pale, knob dark. Integument of abdomen shade, sometimes in full sunlight. Usually they can
dark brown, terga with yellowish scales in the middle be found among floating vegetation or debris in
and lateral tufts of dark brown scales, sternum I devoid ditches, irrigation canals, stream pools, ponds, lakes
of scales, cerci with brown and white scales. or lagoons, especially in larger water bodies. The
Larva: Antenna sparsely spiculate, mainly on inner water is always clear, never turbid or polluted (Root
surface, antennal seta (1-A) short, inserted at the basal 1926; Komp 1942). It is evidently a mosquito which
1/3 of the antennal shaft, with 2–4 branches. Inner and requires high humidity and rainfall and seems to be
outer clypeal setae (2-C and 3-C) long and slender, susceptible to dry seasons. The species is found pre-
single, finely aciculate, the pair of 2-C inserted closer dominantly along large river valleys and is not pres-
to each other than they are to 3-C. Postclypeal seta ent in areas where the dry season is long (Linthicum
(4-C) with 2–4 branches, frontal setae (5-C to 7-C) long 1988). The females are endophagic and endophilic,
and plumose. Prothoracic seta 1 (1-P) of stellate type, they prefer human hosts to domestic animals and
arising from a distinct tubercle, with about 8 branches readily enter dwellings and bite humans, predomi-
radiating from a short stem, 2-P long with a strong shaft nantly at night. In much of its distribution range it is
and laterally branched, 3-P about 1/4 as long as 2-P, the most important domestic species (Ross and
single. Palmate setae developed on abdominal seg- Roberts 1943). The post-feeding resting sites in
ments I–VII (1-I to 1-VII), 1-I and 1-VII smaller than houses are usually vertical surfaces mostly within
the others, each seta with 17–20 lanceolate, smooth and 2 m of the floor (Horsfall 1955).
sharply pointed leaflets. Tergal plate on abdominal seg- Distribution: Brazil, Argentina, Bolivia, Peru,
ment VIII much larger than tergal plate on segment Colombia, Venezuela, Guianas, Honduras, Guatemala,
VII. Lateral abdominal setae 6 of segments IV–VI Belize, Mexico.
(6-IV to 6-VI) long and slender, single. A unique char- Medical importance: An. darlingi is evidently the
acter for the species is found on the spiracular plate. most efficient and important malaria vector throughout
Laterally on the posterior margin arises a pair of promi- its distribution range because of its domestic habits
nent tubercles, bearing at their tips very fine, single and and its high susceptibility to Plasmodium spp.
long setae (Fig. 14.18). These setae extend dorsally and (Linthicum 1988).
380 14 Central and South America

 nopheles (Nyssorhynchus) nuneztovari

A Larva: Head moderately to very heavily pig-
Gabaldon 1940 mented, slightly longer than broad. Antenna more
than half as long as the head, usually lighter than
Female: Medium sized to large species, with the remainder of head, moderately spiculate, mainly on
integument generally dark to very dark brown and a inner surface. Antennal seta (1-A) short, with 5–7
considerable contrast between light and dark regions. branches, about as long as width of antenna at point
Proboscis slender, entirely dark scaled. Palps pre- of insertion, inserted at about 1/4 from base of
dominantly dark scaled, palpomeres II and III with antenna. Inner and outer clypeal setae (2-C and 3-C)
narrow apical white rings, palpomere IV with a broad single, feathered in apical half, the pair of 2-C
median white ring, sometimes apical part also white widely separated, 3-C slightly shorter than 2-C.
scaled, palpomere V usually entirely white scaled, Postclypeal seta (4-C) with 1–4 branches, moder-
occasionally with a few dark scales at base. Occiput ately long and usually extending to near or beyond
covered with many erect scales, pale anteriorly base of 2-C, frontal setae (5-C to 7-C) long and plu-
becoming progressively darker on the posterior por- mose. Prothoracic setae 1 and 2 (1-P and 2-P) usu-
tion and laterally. Vertex with a few decumbent whit- ally sharing a common sclerotized tubercle,
ish scales and a conspicuous tuft of long pale scales sometimes base of 1-P not sclerotized. 1-P of pal-
projecting forward. Clypeus bare, pedicel with a dor- mate type with 9–12 pigmented, moderately broad
solateral row of light scales. Anterior margin of leaflets, 2-P with 12–18 branches, 3-P small and
scutum with a median tuft of elongated whitish scales. single. Metathoracic seta 3-T of palmate type, with
Scutum clothed with small, lanceolate, yellowish 11–15 semitransparent, narrow leaflets. Palmate
white, decumbent scales on acrostichal area, extend- setae developed on abdominal segments I-VII (1-I
ing from anterior margin to prescutellar area, and to 1-VII), 1-III to 1-VI with 23–31 long pointed
dorsocentral stripe, on scutal fossal and supraalar leaflets, 1-I and 1-VII with fewer and slightly shorter
area, additionally with numerous moderately long, leaflets. Lateral abdominal setae 6 of segments
dark setae. Scutellum covered with light scales and IV–VI (6-IV to 6-VI) long and single. Pecten with
very long, dark setae. Upper and lower mesepisternal 15–19 variable long and short teeth, usually one
scale patches present, mesepimeral scale patch usu- long tooth in the middle and 2–3 long teeth dorsally.
ally absent. 1–2 long, upper mesepisternal setae and Anal segment with short thin spicules posteriorly,
about 7 long, pale mesepimeral setae present. Coxae saddle with irregular ventral margin (Fig. 14.19).
with small patches of pale scales, mid femur with a Saddle seta (1-X) single, distinctly longer than the
distinct whitish knee spot. Fore tarsomeres I–IV with saddle, inserted near its ventral margin. Upper and
narrow to moderately broad pale apical rings, tarsom- lower anal seta (2-X and 3-X) single, plumose or
ere V pale in apical half. Mid tarsomeres I and II with laterally branched. Anal papillae about as long as
a narrow apical pale rings, tarsomeres III and IV usu- the saddle, and pointed.
ally all dark scaled, sometimes tarsomere III with a
narrow apical pale ring, tarsomere V with apical part
pale. Hind tarsomere II dark in basal 1/3, tarsomere
III and IV usually entirely pale scaled, very rarely
dark basally, tarsomere V with basal half dark, apical
half pale (Fig. 14.4b). Wing veins covered with pale
and dark scales in a diagnostic pattern as described in
the keys. Light spots usually creamy, not white, at
least on anterior veins. Large dark wing spots dis-
tinct. Wing fringe dark scaled, with pale spots at ter-
minations of most veins and a pale spot between base
of wing and anal vein (A). Integument of abdomen
dark brown, covered with long brown setae, terga
II–VII with lateral tufts of conspicuous dark brown
scales. Fig. 14.19 Larva of An. nuneztovari
14.2 Species Description 381

Biology: The larvae of An. nuneztovari are usually seta (4-C) small, multiple branched, inner frontal seta
found in fresh water habitats in open marshy areas, (5-C) single, placed far forward, median frontal seta
ponds and lakes often at the grassy margins, small or (6-C) single and long, outer frontal seta (7-C) with 2–4
large permanent or temporary ground pools, animal or branches. Integument of thorax densely spiculate.
wheel tracks, and along stream margins, fully exposed Prothoracic setae 1 to 3 (1-P to 3-P) arising from a
to sunlight or partially in shade (Faran 1980). Aquatic common tubercle, P-1 and P-3 with multiple branches,
vegetation may be abundant and algae are often pres- 2-P single. The comb consists of 6–8 scales; individual
ent. They may also be encountered in the interior or in comb scales are elongated, with a prominent median
clearings within the forest, and in areas of secondary spine and laterally fringed with minute spines. The
growth (scrub) such as around villages. The females teeth arise from a sclerotized plate, one or more scales
exhibit a variable feeding and resting behaviour in dif- occasionally detached from the plate. Siphonal index
ferent parts of their distribution range, however during 2.5–2.9, pecten with about 10–14 teeth extending to
the peak season they are regarded as being predomi- near the middle of the siphon. Siphonal seta (1-S) with
nantly endophagic and endophilic, readily feeding on 2–3 branches, inserted beyond the pecten. Anal seg-
humans at night. The principal time the females enter ment slightly longer than broad, the saddle reaching
dwellings is 2200–2400 hours. After the blood meal half way down the segment. Spines on posterior mar-
this species usually rests 1 m high or less on the walls gin of saddle well developed, much elongated and con-
inside houses (Faran 1980). spicuous dorsally. Saddle seta (1X) long, with 2 or
Distribution: Venezuela, Guianas, Brazil, Bolivia, more branches (Fig. 14.20). Upper anal seta (2-X) with
Colombia, Panama. 3–5 branches, lower anal seta (3-X) long and single.
Medical importance: An. nuneztovari is a major Ventral brush well developed, precratal setae (4-X)
vector of malaria in western Venezuela and northern absent, grid strongly sclerotized. Anal papillae 1.0 to
Colombia as well as in Suriname. 1.5 times the length of the saddle, and pointed.
Biology: Hg. janthinomys is found almost exclu-
sively in primary tropical rain forest throughout most of
 aemagogus (Haemagogus) janthinomys
H its range and is decidedly arboreal in habit (Arnell
Dyar 1921 1973). It breeds primarily in tree-holes, the eggs are laid
above the water line and hatch when flooded. Eggs can
Female: Distinctive species ornamented with green or
blue scales of metallic shine that are visible even under
a hand lens. Dark scales of proboscis, palps, wings and
legs predominately purple, with some violet reflections.
Palps short, about 1/6 the length of the proboscis.
Decumbent scales of vertex and occiput bluish with
green tinge. Antepronotal lobes well developed (Fig.
14.7a), much larger than in other genera, clothed with
greenish blue scales. Scutum covered with dark green
and bluish green scales, sometimes silvery scales on
supraalar area, scutellum with dark green to bright blue
scales. Fore and mid coxae with patches of purple scales
near middle, hind femur with silvery scales on anterior
surface in a conspicuous stripe to near apex. Dark scales
of terga mixed with purple scales with some violet
reflections and dark bluish green scales at distal margins
of terga V–VII, more numerous laterally, dark scales of
sterna purple with bluish green scales distally.
Larva: Head rounded, antenna short, adorned with
a few spicules only, antennal seta (1-A) single, inserted
at about the middle of the antennal shaft. Postclypeal Fig. 14.20 Larva of Hg. janthinomys
382 14 Central and South America

remain viable for many months, sometimes multiple

flooding and desiccation cycles are required to induce
hatching. Adults of some Haemagogus spp. do not fly
far from their breeding sites in the tree canopy, where
they feed on monkeys. However, Hg. janthinomys will
readily leave the tree canopy and feed at ground level on
forest ruminants and humans, especially in damaged
forests and along forest edges. Adults feed during the
day between 0600 and 1800 hours, with a single peak of
activity between 1000 and 1600 hours. Hg. janthinomys
usually feeds on the lower limbs and feet of humans.
The females can survive 2–3 months in the laboratory,
although survival rates in nature are much lower. In the
rain forests of Central America, the species reaches its
maximum density at elevations between 100 and
1,000 m, the population size is strongly related to the
rainy season (Anonymous 2002).
Distribution: Argentina, Bolivia, Colombia, Costa
Rica, Ecuador, French Guiana, Guyana, Honduras,
Nicaragua, Panama, Paraguay, Peru, Suriname, Tobago
and Trinidad and Venezuela.
Medical importance: This species is the primary Fig. 14.21 Larva of Oc. albifasciatus
vector of sylvatic yellow fever which is endemic in
several areas in South America, it may become even more
important with the deforestation process continuing. Larva: Head broader than long, antenna <1/2 as
long as the head, sparsely spiculate. Antennal seta
(1-A) small, inserted beyond the middle of the anten-
 chlerotatus (Ochlerotatus) albifasciatus
O nal shaft. Prothoracic seta 1 (1-P) with 3 branches, 2-P
(Macquart 1838) small and single. The comb usually consists of >18
short scales arranged in two irregular rows; individual
Female: Proboscis dark scaled, palps short, about 1/5 comb scale with a prominent median spine and later-
the length of the proboscis, concolourous. Pedicel ally fringed with small spines. Siphon short and stout,
blackish, flagellum of antenna about as long as probos- siphonal index about 2.0. The pecten with 9–13 teeth
cis. Occiput covered with narrow pale scales and pale reaching to near the middle of siphon, the two distal-
forked erect scales, broader dark scale laterally. most teeth slightly detached and without lateral denti-
Integument of scutum brown, scutum with rather broad cles (Fig. 14.21). The saddle covers about half of the
submedian stripes of coppery brown scales, remainder anal segment, saddle seta (1-X) single. Upper anal seta
of scutum yellowish scaled. Scutal setae predominantly (2-X) with multiple branches, lower anal seta (3-X)
dark, lighter above wing root, scutellum with pale long and single.
scales and setae. Pleurites and coxae with patches of Biology: The larvae can be found in temporary
whitish scales. Femora, tibiae and tarsomeres I pre- shallow ground pools of variable size, with or without
dominantly dark scaled, speckled with pale scales, tar- vegetation, mainly in the flood plains of river systems
someres I sometimes with an indistinct basal ring, or along lake shores. In the Andean valleys, breeding
tarsomeres II–V entirely dark scaled. Wing veins sites were encountered at an elevation of 2,300 m
clothed with pale and dark scales intermixed, halter (Luduena Almeida and Gorla 1995). Females deposit
with stem and knob blackish. Terga dark scaled, with a the eggs on muddy soils, the larval development may
median longitudinal pale stripe which broadens toward last less than 8 days, when the temperatures are appro-
the apical margins of each tergum, and basolateral spots priate. In the subtropical zones of its distribution range,
of pale scales. Sterna almost entirely pale scaled. adult activity and larval development may continue
14.2 Species Description 383

throughout the year, in the more temperate areas Oc. more obvious posteriorly and often forming an indis-
albifasciatus is a typical multivoltine flood water mos- tinct longitudinal band. Sterna mostly pale scaled,
quito and especially abundant after heavy rainfall. small apicolateral patches of dark scales on distal
Females are persistent biters and readily attack humans segments.
and domestic animals, mainly at dusk. Besides being a Larva: Head distinctly wider than long. Antenna
serious pest to humans, the species may cause great uniform in width, about half as long as the head,
economic loss in cattle farms. sparsely spiculate, antennal seta (1-A) small, with
Distribution: Brazil, Bolivia, Paraguay, Chile, about 3 branches, inserted near middle of antennal
Uruguay, Argentina, from tropical to temperate areas. shaft, not reaching its tip. Postclypeal seta (4-C)
Medical importance: Oc. albifasciatus is a com- small, with 2–3 branches, inner and median frontal
petent vector of the Western equine encephalitis virus setae (5-C and 6-C) inserted far forward, single,
(WEE) (Mitchell et al. 1987). outer frontal seta (7-C) with multiple branches,
reaching beyond insertion point of antennal seta
(1-A). Prothoracic setae 1 and 2 (1-P and 2-P) single,
 chlerotatus (Ochlerotatus) scapularis
O 3-P slightly shorter, with 1–2 branches. Lateral
(Rondani 1848) abdominal seta 6 on segments I and II (6-I and 6-II)
usually with 2 branches, 6-III to 6-VI single. The
Female: Small to medium sized species. Proboscis comb consists of 20–27 scales arranged in irregular
dark scaled, usually distinctly paler ventrally. Palps double to triple rows, individual scales evenly fringed
short, <1/5 the length of the proboscis, dark scaled. apically. Siphonal index 2.0–2.6, pecten with about
Pedicel brown, darker on inner surface. Occiput with 11–18 evenly spaced teeth extending slightly beyond
broad median patch of narrow decumbent whitish the middle of the siphon. Siphonal seta (1-S) multi-
scales, broad decumbent brown and whitish scales ple branched, much shorter than the width of the
laterally. Erect forked scales numerous, extending siphon at the point of its origin, inserted beyond dis-
over most of vertex and occiput, straw coloured. talmost pecten tooth. Anal segment completely
Integument of scutum dark brown, scutum with a ringed by the saddle, saddle seta (1-X) single, shorter
large rounded spot of light scales from anterior than the ­saddle. Lower anal seta (3-X) long, single,
promontory to scutal angle and posteriorly to near upper anal seta (2-X) with multiple branches, less
level of posterior end of paratergite, sometimes with than half as long as 3-X. Ventral brush large, with
posterior extensions along dorsocentral line to scutel- about 8 pairs of cratal setae (4-X), precratal setae
lum and surrounding prescutellar bare space, scales absent. Anal papillae usually more than twice as long
silvery white, often yellowish on lateral border. as the saddle, pointed (Fig. 14.22).
Posterior part of scutum predominantly with dark Biology: Oc. scapularis breeds in a wide variety of
scales, acrostichal and anterior dorsocentral setae temporary or semipermanent freshwater habitats, pri-
absent. Scutellum with pale scales on the lobes. marily temporary rain filled or stream overflow pools,
Pleurites with patches of broad whitish scales. Scales but also in swamps and marshes in either sunlit or in
on mesepisternum not reaching anterior angle, sepa- partial shade (Carpenter and La Casse 1955; Belkin
rate from prealar scale patch, upper part of mesepim- et al. 1970). The females attack humans readily, they are
eron with patch of scales. Lower mesepimeral setae especially active during the afternoon and early evening,
absent. Fore and mid legs with conspicuous white but will bite at any time when disturbed. They may
stripes on posterior surfaces of femora and basal tar- cause a considerable nuisance problem and are able to
someres, tibiae dark, posterior surfaces pale. Hind disperse as far as 4 km from their breeding sites. In areas
leg with basal 2/3 of femur pale scaled and a con- of prolonged association with humans, Oc. scapularis is
spicuous white stripe on anterior surface of tibia, adapting to human habitations and is becoming more
occasionally nearly encircling tibia, and continued concentrated around dwellings in rural and semirural
on tarsomeres I and II. Wing veins covered with nar- areas, even entering buildings to bite (Arnell 1973).
row, dark scales, halter largely pale. Terga covered Distribution: From the southwestern United States
with dark scales, terga II–VII with large basolateral through Central and South America to Argentina,
white patches and basomedian patches of pale scales, Greater Antilles, Trinidad.
384 14 Central and South America

late, the portion beyond the constriction darker and with

few spicules. Antennal seta (1-A) large, multiple
branched, inserted at apical 1/3 of antennal shaft, reach-
ing well beyond the tip of the antenna, labral seta (1-C)
rather stout, attenuate apically. Postclypeal seta (4-C)
short, single, inner and median frontal setae (5-C and
6-C) usually with 3 branches, extending beyond anterior
margin of head. Outer frontal seta (7-C) long, multiple
branched. Thorax densely clothed with fine spicules.
Prothoracic setae 1 to 3 (1-P to 3-P) long, single, 4-P
long, usually with 2 branches, 5-P and 6-P long, single,
7-P long, with 2–4 branches. Abdominal setae 6-I and
6-II usually with 3 branches, 6-III and 6-VI slightly
shorter, usually with 2 branches. The comb is composed
of >30 scales arranged in a triangular patch, individual
comb scale rounded apically and fringed with small
spines. Siphon long and slender, siphonal index 6.0–8.0.
The pecten consists of about 12 (9–15) teeth restricted
to basal 1/4 of siphon, individual pecten tooth with 2–6
lateral denticles. Siphonal setae (1-S) with 4 pairs of
tufts inserted beyond the pecten, basalmost tuft (1a-S)
Fig. 14.22 Larva of Oc. scapularis
usually with 2 branches, occasionally single, as long as
or longer than the basal width of the siphon, second and
third tufts (1b-S and 1c-S) usually with 2–3 branches
Culex (Culex) nigripalpus Theobald 1901 and inserted somewhat laterally, distalmost tuft (1d-S)
small, with 1–3 branches (Fig. 14.23). Anal segment
Female: Medium sized species. Proboscis dark scaled, completely ringed by the saddle; saddle with numerous
usually paler ventrally on basal half, palps short, <1/4 strong spicules on posterior margin. Saddle seta (1-X)
as long as proboscis, dark scaled. Occiput with narrow usually single, sometimes with 2 branches, slightly
curved pale golden brown scales and dark erect forked shorter than the saddle. Upper anal seta (2-X) with 3
scales dorsally, with a patch of broad whitish scales branches, 1 long and 2 short, lower anal seta (3-X) long
laterally. Integument of scutum brown, scutum cov- and single. Ventral brush well developed, with about
ered with fine dark bronze brown scales. Scutellum 6–7 pairs of cratal setae (4-X), precratal setae absent.
with dark bronze brown scales and brown setae on all Anal papillae variable in length, 1–3 times as long as the
lobes. Postpronotum with narrow dark bronze scales in saddle, tapered apically.
upper part, pleurites with few or no scales. Integument Biology: The larvae of Cx. nigripalpus can be found
of mesepimeron lighter than remainder of pleurites, a in semipermanent or permanent habitats in ditches,
few small broad pale scales on upper and lower part of grassy pools, and marshes. Occasionally they are found
mesepisternum and a few narrow scales on upper in leaf axils of plants or artificial containers (Carpenter
mesepimeron. Legs dark scaled, with metallic blue and La Casse 1955). The larvae are able to tolerate a
green reflection, posterior surface of femora and tibiae wide range of conditions in their breeding sites, such
pale scaled. Wing scales narrow, all dark. Terga clothed as salinity, sunlight, organic matter, etc. (Belkin et al.
with dark brown to black scales, often with metallic 1970). Cx. nigripalpus is generally regarded as an out-
reflections. Narrow pale basal bands occasionally present door species, but where adults are numerous they read-
on some segments, basolateral pale patches present on ily enter houses. Both the adults and larvae may be
terga V–VII (Fig. 14.12a), sterna pale scaled. found throughout the year in their southern distribu-
Larva: Antenna shorter than the head, distinctly tion range (Carpenter and La Casse 1955). The females
constricted beyond insertion point of antennal seta readily bite humans and are regarded as a major pest in
(1-A), the portion below the constriction pale and spicu- the southern United States (Darsie and Day 2004).
14.2 Species Description 385

and numerous dark erect forked scales. Integument of

scutum dark brown, scutum clothed with narrow
curved dark brown scales intermixed with golden
brown lanceolate scales, whitish to golden brown
scales present, primarily on supraalar and prescutellar
dorsocentral areas. Scutal setae very numerous.
Scutellum with whitish to golden narrow scales and
dark brown setae on all lobes. Scaling of pleurites
sparse, small patches of whitish scales on upper part of
mesepisternum and along its lower posterior margin, a
few scales on upper part of mesepimeron, 3 or more
lower mesepimeral setae present, upper mesepimeral
setae numerous, postspiracular setae present. Femora
and tibiae dark scaled, speckled with pale scales, pos-
terior surface of mid and hind femora predominantly
pale scaled, very small pale knee spots more or less
distinct on all femora. Tarsomeres I–IV of fore and
mid legs each with a narrow but conspicuous basal
white ring, all tarsomeres of hind leg with white basal
rings. Wing veins covered with very broad, strongly
asymmetrical scales, predominantly dark but with
scattered whitish scales throughout. Haltere stem pale,
knob dark scaled. Tergum I with a small median patch
of pale scales. Terga II–VII predominantly dark scaled,
with more or less numerous pale scales laterally and
with few to many yellow and whitish scales apically.
Apex of tergum VII with a row of short stout pointed
Fig. 14.23 Larva of Cx. nigripalpus spines. Tergum VIII with many short stout spines in a
curved posterior row and an irregular anterior row.
Sterna II–VII with an irregular and variable mixture of
Distribution: Antilles, southern United States, dark and pale scales.
Mexico, Central America, northern South America. Larva: Head distinctly broader than long. Antenna
Medical importance: Principal vector of St. Louis about twice as long as the head, sparsely clothed with
encephalitis (SLE) and important vector of West Nile small but distinct spicules on basal half. Antennal seta
virus (WNV) in Florida (Darsie and Day 2004) and (1-A) multiple branched, inserted at a notch on basal
northeastern United States (Kilpatrick et al. 2005). third of antennal shaft, a pair of long stout setae (2-A
and 3-A) arising near the middle of the shaft and
extending slightly beyond its tip. Labrum distinctly
Mansonia (Mansonia) titillans (Walker 1848) produced at base of labral seta (1-C). Postclypeal seta
(4-C), inner and median frontal setae (5-C and 6-C),
Female: Medium sized brown to dark brown species small, with multiple branches, outer frontal seta (7-C)
moderately speckled with whitish scales on palps, moderately long with multiple branches. Prothoracic
wings, femora, tibiae, tarsomeres I and abdomen. seta 1 (1-P) long, usually with 2–3 branches, 2-P short,
Proboscis dark scaled, speckled with pale scales, and single, 3-P short, with multiple branches. Abdominal
with a narrow white ring beyond the middle. Palps setae 6 on segments I–VI (6-I to 6-VI) single. The
about 1/3 as long as the proboscis, predominantly dark comb consists of 6–8 scales arranged in a single row,
scaled, with scattered white scales. Pedicel brown, the dorsal scales are long and slender, with a promi-
darker on inner surface, a few whitish scales on dorsal nent median spine and fringed with small lateral
and inner surfaces. Occiput with pale lanceolate scales spinules on basal part, ventrally the scales are much
386 14 Central and South America

shorter than 3-X. Ventral brush well developed, with

about 4 pairs of cratal setae (4-X) and 4 precratal setae
piercing the saddle. Anal papillae shorter than the sad-
dle, and pointed.
Biology: Eggs are deposited as masses glued to the
undersides of leaves of aquatic plants such as Pistia
sp. (Horsfall 1955). After hatching, the larvae attach
themselves to the submerged roots of aquatic plants
from which they obtain oxygen. The pupae also
remain attached to the roots of the plants until time
for emergence of the adults. Water lettuce (Pistia
statiotes) and water hyacinth (Eichhornia crassipes)
are believed to be the preferred host plants for the
larvae and pupae of Ma. titillans, but some other host
plants are also involved (Carpenter and La Casse
1955; Belkin et al. 1970). The females are fierce bit-
ers and readily attack humans and domestic animals,
they are most active at dusk and again at dawn but
will feed at any time after sundown. The females are
Fig. 14.24 Larva of Ma. titillans known to fly several kilometers from swamps,
marshes, ponds, and lakes where their immature
smaller (Fig. 14.24). Siphon short and conical, heavily stages develop. The species is often extremely abun-
sclerotized beyond the middle, modified for piercing dant and constitute a serious pest problem to humans
plant tissue. Siphonal seta (1-S) usually with 4–5 and livestock.
branches arising before the heavily sclerotized part, Distribution: Southern United States (Florida,
pecten absent. Anal segment longer than wide, com- Texas), Mexico, Central and South America, Antilles.
pletely encircled by the saddle; saddle seta (1-X) short, Medical importance: The Venezuelan equine
usually with 6 branches, inserted well before the pos- encephalitis (VEE) virus has been isolated from wild
terior margin of the saddle. Upper and lower anal setae caught Ma. titillans; the species is known to be a vec-
(2-X and 3-X) with multiple branches, 2-X slightly tor of filariasis (Carpenter and La Casse 1955).
Chapter 15
North America

Anyone who has identified a litre jar packed with for the last species, they are described and keyed under
mosquitoes collected in a CDC trap from North Dakota the chapters on the mosquitoes of Europe.
to find 10,000 Ae. vexans1 for every one Oc. melani- The second tier of mosquitoes causing nuisance
mon, knows that all mosquitoes are not created equal. with either confirmed or potential vector capability in
The person collecting a hundred Ae. albopictus1 for the USA are, according to their ranking (McKnight
every one Cx. p. quinquefasciatus 1 in landing rate 2005): Oc. trivittatus, Oc. nigromaculis, Oc. canadensis
counts in Texas has an even deeper understanding canadensis, Cs. inornata, Oc. triseriatus, Cs. incidens,
of that fact (McKnight 2005). An. crucians, Cx. erythrothorax, Oc. sierrensis, An.
It is not surprising that Ae. vexans1 and Ae. albopictus1 freeborni, Cx. nigripalpus, An. punctipennis,
were the top two on a list of the 13 most voracious biters Oc. melanimon, Oc. atlanticus, An. quadrimaculatus,
across the USA (McKnight 2005). Consequently, Oc. stimulans, Oc. increpitus, Oc. sticticus,1 Oc. japonicus.
because of their major pest importance, they are included Many are involved in virus transmission and some,
in the key but their description is given under Europe. such as An. quadrimaculatus, An. freeborni, and
Cx. p. pipiens biotype molestus1 and Cx. p. quinquefas- An. pseudopunctipennis, are potential vectors of malaria
ciatus1 are also included in the keys being the top pest in North America.
species and important vectors of West Nile virus. For further reading on the morphology, identification,
Some other species also cause significant nuisance in biology, distribution, and disease vector status of the
a number of states of the USA (Oc. dorsalis1) and Canada: species mentioned, the reader is referred to Carpenter
Oc. hexodontus1 (being the main pest), Ae. vexans,1 Oc. and La Casse (1955), Mattingly (1971), Smith (1973),
communis,1 Oc. dorsalis,1 Oc. impiger,1 Oc. nigripes,1 Wood et al. (1979), Darsie and Ward (1981, 2005),
Oc. punctor,1 Oc. solicitans,1 and Cq. perturbans. Except Rueda (2004).

15.1 Key to North American Female Mosquitoes

1 Palps about as long as proboscis. Scutellum evenly rounded or slightly trilobed and uniformly setose
(Fig. 15.1a). Abdominal terga and sterna completely or largely missing scales. – Proboscis not tapering towards
apex and not strongly recurved............................................................................................................ Anopheles
Palps distinctly shorter than proboscis. Scutellum trilobed, setae arranged in three sets (Fig. 15.1b).
Abdominal terga and sterna uniformly and densely covered with scales. – Proboscis not tapering towards
apex and not strongly recurved. Postnotum without a tuft of setae. Veins R2 and R3 at least as long as vein R2+3, usually much
longer. Anal vein (A) ending well beyond the furcation of cubitus (Cu). Squama with fringe of setae............................. 2

1
Species described in Chap. 10 concerning European mosquitoes.

N. Becker et al., Mosquitoes and Their Control, 387

DOI 10.1007/978-3-540-92874-4_15, © Springer-Verlag Berlin Heidelberg 2010
388 15 North America

Fig. 15.1 Scutellum of: (a) Anopheles sp.; (b) Aedes sp.

2 (1) Prespiracular setae present (Fig. 15.2a). – Postspiracular setae present. Abdomen tapering apically, cerci long, easily
visible. Psorophora...........................................................................................................................................3
Prespiracular setae absent (Fig. 15.2b). – Lobes of antepronotum are small and broadly separated, commencing beyond
anterior margin of scutum. Scutum covered with narrow scales without metallic shine. Tarsomere I of fore legs usually shorter
than tarsomeres II–V together. Tarsomere IV of fore legs not reduced, distinctly more long than broad.. ............................. 4

Fig. 15.2 Lateral view of thorax of: (a) Psorophora sp.; (b) Ochlerotatus sp.

3 (2) Femora usually with a narrow subapical ring of pale scales (Fig. 15.3a). Wing veins with pale and dark
scales. – Tarsomere I of hind legs with basal and median pale rings. Pale and dark scales on wing veins randomly mixed
(not grouped)................................................................................................................. Ps. columbiae (p 394)
Femora without subapical ring of pale scales (Fig. 15.3b). Wing veins uniformly dark scaled or if a few pale
scales are present, they are restricted to the anterior border (veins C and Sc). – Scutum with dark brown and golden
yellow scales mixed, without forming specific pattern. Apices of femora without erect scales. Abdominal terga with apicolateral
patches of pale scales. Tarsomeres IV and V and often apex of tarsomere III of hind tarsus pale scaled............. Ps. ferox (p 395)

Fig. 15.3 Hind leg of: (a) Ps. columbiae; Fig. 15.4 Lateral view of thorax of: (a) Ochlerotatus sp.; (b) Culex sp.
(b) Ps. ferox
15.1 Key to North American Female Mosquitoes 389

4 (2) Postspiracular setae present (Fig. 15.4a) and/or claws of fore legs with subbasal tooth. – Wing scales usually
narrow, if broad then not conspicuously asymmetrical. (for Canadian nuisance species see key for Europe)............. 5
Postspiracular setae absent (Fig. 15.4b). All tarsal claws simple................................................................ 9
5 (4) Proboscis without a pale ring (Fig. 15.5a)................................................................................................... 6
Proboscis with distinct broad median ring of pale scales (Fig. 15.5b). Decumbent scales of vertex largely narrow
and/or (if scales of vertex are largely broad) erect scales numerous, often not restricted to occiput. Ochlerotatus............... 8

Fig. 15.5 Proboscis of: (a) Ae. aegypti; (b) Oc. sollicitans

6 (5) Proboscis as long as fore femur or slightly shorter (Fig. 15.6a). Erect scales not numerous, restricted to
occiput. Scutellum with broad, white and straight scales. – Scutum with white or silvery scales in stripes
or patches. Femora with white knee spot. Aedes subgenus (Stegomyia).............................................................. 7
Proboscis distinctly longer than fore femur (Fig. 15.6b). Erect scales numerous, not restricted to occiput.
Scutellum with narrow, yellowish or pale and curved scales. – Basal pale rings on tarsi very narrow, usually not excee­
ding more than 1/4 of the length of the tarsomeres (pale rings better visible against a dark background and with a blue light filter).
Terga with white transverse basal bands constricted in the middle giving them a bilobed pattern.............. Ae. vexans (p 194)

Fig. 15.6 Head and thorax of: (a) Ae. aegypti; (b) Ae. vexans

7 (6) Scutum with a white acrostichal stripe extending from the anterior margin to the beginning of the pres-
cutellar area, where it forks to end at the anterior margin of scutellum (Fig. 15.7a).. Ae. albopictus (p 201)
Scutum without an acrostichal stripe on anterior part but with two narrow white dorsocentral stripes sepa-
rated from anterior margin. Lateral white stripes broad, continuing over transverse suture to the end of
scutum, lyre shaped (Fig. 15.7b)..................................................................................... Ae. aegypti (p 198)
390 15 North America

  8 (5) Wing veins with pale and dark scales. Terga with a median longitudinal pale stripe (sometimes
disconnected) (Fig. 15.8a). – Hypostigmal scales present. Tarsomere I of hind tarsi with conspicuous pale basal and
median rings.............................................................................................................. Oc. sollicitans (p 391)
Wing veins dark scaled, few pale scales present at the base of costa (C). Terga without a median
longitudinal pale stripe, pale scales form relatively narrow basal transverse bands (Fig. 15.8b).
...................................................................................................................... Oc. taeniorhynchus (p 393)

Fig. 15.7 Scutum of: (a) Ae. albopictus; (b) Ae. aegypti Fig. 15.8 Abdomen of: (a) Oc. sollicitans; (b) Oc. taeniorhynchus

  9 (4) Hind tarsal claws very small and inconspicuous. All tarsi with well developed pulvilli. Wing scales usu-
ally narrow (Fig. 15.9a). – Antennae not longer than proboscis. Flagellomere I and II of similar length. Vertex and
occiput with narrow decumbent scales. Scutum with acrostichal setae. Pale scales on abdominal terga grouped mainly on
basal part of terga forming bands and/or lateral patches. Culex subgenus (Culex)............................................. 10
Hind tarsal claws not very small. Pulvilli absent. Most of wing scales broad and conspicuous (Fig. 15.9b).
– Tarsi ringed. Tarsomere I of hind tarsus with a median pale ring.....................................Cq. perturbans (p 400)

Fig. 15.9 Wing scales of: (a) Culex sp.; (b) Coquillettidia sp.

10 (9) Tarsomeres with distinct basal and apical pale rings, particularly on hind legs (Fig. 15.10a). – Proboscis
with a pale ring near the middle. Anterior surface of femora and tibiae with a longitudinal stripe of pale scales or rows
of pale patches. Hind tarsi with rather broad basal and apical pale rings. A V-shaped dark marking on all abdominal
sterna............................................................................................................................Cx. tarsalis (p 398)
Tarsomeres usually without pale rings (Fig. 15.10b). When pale rings are present, they are indistinct,
narrow and basal. – Integument of scutum, pleurites, and coxae light brown, brown or dark brown but never reddish
brown....................................................................................................................................................... 11
15.2 Species Description 391

Fig. 15.10 Hind tarsus of: (a) Cx. tarsalis; (b) Cx. p. pipiens Fig. 15.11 Abdomen of: (a) Cx. p. quinquefasciatus;
(b) Cx. salinarius; (c) Cx. restuans

11 (10) Abdominal terga with rather broad (about 1/4 of the terga) basal bands of pale scales (Fig. 15.11a)......... 12
Pale basal bands on abdominal terga usually narrow or pale scaling restricted to lateral patches
(Fig. 15.11b). – Pleurites with several patches of broad pale scales, each patch usually comprised of 6 or more scales.
Terga VII and VIII almost completely covered with yellowish scales..........................................Cx. salinarius (p 397)
12 (11) Pale basal transverse bands rounded on posterior margin and constricted sublaterally, rather narrowly
joining (sometimes disconnected) lateral pale patches, tergum VIII predominantly pale scaled
(Fig. 15.11a). Scutum without spots of pale scales....................................................................................
............................................ Cx. p. pipiens biotype molestus and Cx. p. quinquefasciatus (p 277, 278)
Pale basal transverse bands with nearly straight posterior margin and broadly joining the lateral patches
(particularly on terga III–V), tergum VIII predominantly dark scaled (Fig. 15.11c). Scutum usually with
submedian spots of pale scales close behind scutal angles.......................................Cx. restuans (p 396)

broad, flat, pale yellowish scales, and small lateral

15.2 Species Description patches of dark scales. Erect forked scales on cen-
tral part of occiput pale, those on lateral region dark,
 chlerotatus (Ochlerotatus) sollicitans
O a dense tuft of pale setae projecting between the
(Walker 1856) eyes. Integument of scutum black, scutum densely
covered with narrow, golden brown scales dorsally,
Female: A medium sized dark brown species with and dark bronze brown scales laterally, anterior
ringed proboscis, speckled wings and conspicuously margin and prescutellar area with somewhat paler
pale ringed tarsi. Proboscis dark scaled, with a white scales, often a pair of narrow, rather indefinite, sub-
ring near the middle (Fig. 15.5b). Palps dark, more median stripes of pale yellow to golden yellow
than 1/4 as long as the proboscis with a few pale scales extending nearly the full length of scutum.
scales at the tip. Pedicel brown, with pale scales on Scutal setae dark in anterior part, golden in poste-
inner and dorsal surfaces, clypeus prominent, dark rior part. Scutellum with golden scales and darker
brown, without scales. Occiput with a broad median setae on the lobes. Paratergite with pale scales.
patch of narrow golden yellow scales, submedian Integument of pleurites and coxae brown, pleurites
patches of narrow, dark, bronze brown scales and with several patches of broad pale scales. Scale
392 15 North America

patch on mesepisternum reaching to anterior angle,

not distinctly separated from prealar patch.
Mesepimeron bare on lower portion. 0–1 lower
mesepimeral setae present. Femora and tibiae exten-
sively speckled with pale scales, posterior surface
pale, knee spots white. Hind leg with tarsomere I
ringed with pale scales at base and a yellowish ring
at the middle, tarsomeres II–IV with broad, pale
basal rings, tarsomere V entirely white scaled. Fore
and mid tarsi similarly marked but with rings nar-
rower on tarsomeres I–III, absent on tarsomere IV.
Tarsomere V of front tarsus varies from entirely
dark to nearly all white, tarsomere V of mid tarsus
mostly white, with some scattered dark scales. Wing
veins covered with broad, dark and pale scales
evenly intermixed, dark scales predominating on
costal edge. Haltere entirely pale scaled. Tergum I
with a median patch of yellowish white scales, terga
II–VII with a median longitudinal pale stripe and
narrow basal transverse pale bands and small lateral
pale patches (Fig. 15.8a). Sterna all predominantly
pale scaled, some dark scales on distal segments.
Larva: Head broader than long, antenna about half
as long as the head, sparsely clothed with spicules,
Fig. 15.12 Larva of Oc. sollicitans
antennal seta (1-A) a multiple tuft, inserted near the
middle of the antennal shaft. Postclypeal seta (4-C)
small, 2–3 branched, inner and median frontal setae Biology: The larvae of Oc. sollicitans occur mostly in
(5-C and 6-C) long, usually single, outer frontal seta salt marshes and mangrove swamps in coastal areas, they
(7-C) with 6–10 branches. Prothoracic seta 1 (1-P) may breed even in footprints in salt marshes and coral
long, single, 2-P about half as long as 1-P, single, 3-P rockholes (Belkin et al. 1970). The species has been
short, usually with 1–2 branches. The comb consists of found also in brackish water swamps in many of the
11 to 21 comb scales, arranged in an irregular patch, inland states in the US (Carpenter and La Casse 1955).
individual comb scale with a long median spine and Oc. sollicitans is multivoltine, overwintering in the egg
fringed with small lateral spines. Siphon stout, sipho- stage. The eggs are laid on the moist mud of salt marsh
nal index 2.0–2.5, tracheal trunks broad. The pecten is pools, they are able to hatch within minutes after being
composed of about 15–27 evenly spaced teeth reach- flooded, and the development of the immature stages
ing slightly beyond the middle of the siphon, occasion- may be complete within a week after hatching (Wood
ally 1–2 apical teeth are slightly detached, individual et al. 1979). The larvae and adults are most abundant
pecten tooth with 1–3 lateral denticles. Siphonal tuft from April or May to October in the marshes along the
(1-S) with 4–8 branches, inserted beyond the pecten, northern Atlantic coast. The adults are strong fliers and
about as long as the apical width of the siphon. Anal often migrate in large numbers to communities many km
segment completely ringed by the saddle, the saddle from the salt water marshes in which they breed. The
without distinct spicules at its posterior margin females are persistent and troublesome biters, attacking
(Fig. 15.12). Saddle seta (1-X) single, shorter than the humans at any time during the day or night, even
saddle. Upper anal seta (2-X) multiple branched, lower in strong wind and may cause a great nuisance. The adults
anal seta (3-X) long and single. The ventral brush is large rest in the vegetation during the daytime and will attack
with 7–8 pairs of cratal setae (4-X), precratal setae anyone invading their resting sites, even in full sunlight.
absent. Anal papillae variable in length, usually short, Distribution: Nearctic Region (eastern coastal and
but may be as long or longer than the saddle. inland saline areas), Greater Antilles.
15.2 Species Description 393

 chlerotatus (Ochlerotatus) taeniorhynchus

O (1-A) small, with 2–3 branches inserted slightly
(Wiedemann 1821) before the middle of the antennal shaft not reaching
the tip. Postclypeal seta (4-C) small, 2–3 branched,
Female: A medium sized to rather small, dark spe- inner and median frontal setae (5-C and 6-C) long,
cies with ringed tarsi and banded abdomen. Proboscis single, outer frontal seta (7-C) short, multiple
dark scaled, with a conspicuous white ring near the branched. Prothoracic seta 1 (1-P) long, single, 2-P
middle, palps short, about 1/5 the length of the pro- short, single, 3-P short, usually with 2 branches. The
boscis, dark with white scales at the tips. Pedicel comb consists of about 9 to 20 scales arranged in an
brown, with a patch of silvery scales on inner side. irregular patch, individual scales small, apically
Occiput with a median patch of pale to golden brown rounded, prominent median spine absent. Siphon
lanceolate scales, a large patch of broad decumbent stout, siphonal index 1.5–2.0, tracheal trunks broad.
white scales laterally, the eye margins narrowly The pecten is composed of 11–17 short evenly spaced
white scaled. Broad decumbent scales predominantly teeth, reaching the middle of the siphon or slightly
whitish, a few dark scales dorsally and in a lateral beyond. Siphonal seta (1-S) multiple branched,
patch. Erect scales very numerous, usually all dark, inserted beyond the pecten, shorter than the width of
sometimes pale on central part, setae dark brown, the siphon at the point of its insertion (Fig. 15.13).
dense on vertex and projecting between eyes. Anal segment completely ringed by the saddle, sad-
Integument of scutum dark brown, scutum clothed dle with numerous spicules at its posterior margin.
with narrow dark golden brown scales becoming Saddle seta (1-X) single, shorter than the saddle.
pale yellowish on the anterior margin, the prescutel- Upper anal seta (2-X) multiple branched, lower anal
lar space and above the wing roots. Paratergite with seta (3-X) long and single. Ventral brush well devel-
small broad whitish scales, scutal setae short and oped, usually with 8 pairs of cratal setae (4-X), pre-
dark. Scutellum with pale yellowish scales and cratal setae absent. Anal papillae usually much
brown setae on all lobes. Pleurites dark brown, with shorter than the saddle.
patches of broad flat whitish scales, present on
propleuron, postspiracular and subspiracular areas.
Patch on mesepi­sternum extending about halfway to
anterior angle, separate from prealar patch.
Mesepimeron with a patch of scales on upper half,
lower half bare. Sometimes one lower mesepimeral
seta present. Femora and tibiae dark scaled, pale on
posterior surface, knee spots white. Fore and mid
tarsi dark, with narrow basal pale rings on tarsom-
eres I–III, on tarsomeres IV and V the rings are
reduced or absent. Hind tarsi dark, tarsomeres I–IV
each with a broad basal white ring, tarsomere V usu-
ally entirely pale. Claws of fore and mid leg all with
subbasal tooth, hind claws simple. Wing scales all
narrow and dark except for a few pale scales at base
of costa (C), haltere pale scaled. Tergum I with a
median patch of dark scales, a few white scales often
intermixed. Terga II–VI dark scaled with narrow pale
basal bands and conspicuous pale lateral patches, the
two patches on terga VI and VII are visible from a
dorsal view, apices of terga VI and VII with a narrow
row of pale scales, cerci slender, black (Fig. 15.8b).
Larva: Head broader than long, antenna less than
half as long as the head, slightly tapering towards
apex, spicules very small and sparse. Antennal seta 1 Fig. 15.13 Larva of Oc. taeniorhynchus
394 15 North America

Biology: The natural breeding sites of Oc. taenio- scutum, on the prescutellar area, a patch above wing base,
rhynchus are temporary pools in mangroves and grass and a small submedian patch near middle of scutum.
salt marshes in coastal areas, these breeding sites are Scutellum with long narrow whitish scales and dark setae
influenced by tides and rainfall. Larvae have also been on the lobes. Pleurites and coxae blackish brown, with
found in inland brackish water swamps, in areas far patches of broad whitish scales. Mesepisternum with few
removed from the coast (Carpenter and La Casse 1955). scales reaching the anterior angle, prealar patch present.
Occasionally, they breed in fresh water in temporary Mesepimeron with scales on upper portion not reaching
ground pools and in irrigation and stream overflows in the lower margin. Femora dark brown scaled, with white
the coastal lowlands (Belkin et al. 1970). The species scales intermixed, posterior surfaces largely pale scaled,
reaches its greatest abundance along the coastal regions each femur with a narrow subapical pale ring, knee spots
of the southern United States and the Caribbean region, white (Fig. 15.3a). Tibiae dark scaled with numerous
usually following high tides or a combination of high small white spots on dorsal surfaces. Hind tarsi with basal
tides and heavy rains during the summer and early fall. white rings on all tarsomeres, tarsomere I with a median
The females are severe biters and will attack at any time white ring as well. Fore and mid tarsi similarly marked but
during the day when they are disturbed. In late after- with white rings reduced or lacking on tarsomere IV,
noon and particularly at dusk and after, they actively absent on tarsomere V. Tarsal claws all simple, without
search for blood and will attack humans and livestock subbasal tooth. Wing scales rather broadly triangular, dark
outdoors and will also invade dwellings (Belkin et al. brown and pale intermixed, the dark ones predominating,
1970). As with Oc. sollicitans, they are strong fliers and wing fringe entirely dark scaled. Tergum I with a median
often migrate in large numbers many km away from patch of pale scales, terga II and III with white to pale yel-
their breeding grounds. The males begin to swarm at lowish triangular scale patch apically, divided into paired
twilight over the top of bushes or small trees, these submedian patches on terga IV–VII. Sterna with dark and
swarms usually last not longer than 30 min (Apperson pale scales intermixed, the pale ones predominating, the
1991). In the warmer parts of continental US, Oc. tae- black ones tending to form median apical spots on distal
niorhynchus is the common coastal species and some- terga.
times appears in enormous numbers when the conditions Larva: Antenna shorter than the head, slightly
are favourable (Howard et al. 1917). tapering towards apex, sparsely covered with spicules.
Distribution: American coasts and inland saline Antennal seta (1-A) long, multiple branched, inserted
areas, Massachusetts to Brazil and California to Peru, near middle of antennal shaft. Postclypeal seta (4-C)
Antilles, Galapagos Islands. small, multiple branched, all frontal setae (5-C to 7-C)
Medical importance: Oc. taeniorhynchus is a natural with more than 4 branches, their insertion points more
vector of dog heartworm (Dirofilaria immitis) and or less in a straight line. The comb consists of 5–6
Venezuelan equine encephalitis (VEE) (Apperson 1991). scales located on the posterior margin of a weakly
sclerotized plate, individual comb scale thorn shaped,
with the larger basal spines about 1/3 as long as the
 sorophora (Grabhamia) columbiae
P prominent median spine. Siphon moderately widened
(Dyar and Knab 1906) in the middle and tapering towards the apex, siphonal
index about 3.0, ­tracheal trunks broad. The pecten is
Female: Medium sized to rather large species. Proboscis composed of 3–6 widely spaced teeth, not reaching the
dark scaled at base and apex, with a large, median ring of middle of the siphon, individual pecten tooth with 1
yellowish white scales. Palps short, about 1/4 as long as lateral denticle. Siphonal tuft (1-S) about as long as
proboscis, dark scaled with pale tip. Pedicel dark brown, apical width of siphon, multiple branched, inserted at
with a patch of pale scales on inner surface. Occiput distal third of siphon (Fig. 15.14). Anal segment lon-
clothed dorsally with narrow curved white to pale violet ger than wide, completely ringed by the saddle, saddle
scales and numerous black erect forked scales, a dorsolat- seta (1-X) small, with 2–3 branches. Upper anal seta
eral patch of broad flat dark scales followed by broad (2-X) short, multiple branched, lower anal seta (3-X)
whitish to light brown scales laterally. Setae along margins long, single. Ventral brush well developed, extending
of eyes numerous, black. Integument of scutum blackish along the ventral line almost to the base of the anal
brown, scutum covered with fine narrow bronze brown to segment. Anal papillae long, about 2–3 times as long
blackish scales, and narrow pale scales along the edge of as the saddle, evenly tapering and pointed.
15.2 Species Description 395

 sorophora (Janthinosoma) ferox

P
(von Humboldt 1819)

Female: Small to medium sized, dark species, dark

scales predominantly metallic with purplish irides-
cence. Scales on scutum mixed dark and golden, with-
out definite pattern, hind tarsus with tarsomeres IV
and V completely white scaled. Proboscis slightly
longer than fore femur, palps about 1/4 as long as pro-
boscis, with dark scales of metallic shine. Antenna
slightly shorter than proboscis, pedicel light to dark
brown, mesal surface with a few short dark setae but
no scales. Integument of head dark brown, shining.
Occiput covered dorsally with broad curved whitish
yellow to golden yellow scales, paler anteriorly, with
broad decumbent yellowish scales laterally. Erect
forked scales yellowish, numerous on posterior half of
occiput. Integument of scutum dark brown to black,
shining. Scutum sparsely clothed with rather broad
dark brown and golden yellowish scales in no definite
pattern, the dark scales more abundant in the median
area. Scutal setae brown, paratergite bare. Scutellum
Fig. 15.14 Larva of Ps. columbiae with rather broad yellowish white scales and dark
brown setae on the lobes. Pleurites densely clothed
with greyish white scales. Hypostigmal, subspiracular
and postspiracular patches present. Scales on mese-
pisternum reaching lower margin and anterior angle,
Biology: The females lay their eggs on damp soil, mesepimeral patch reaching near lower margin. Coxae
in depressions subject to flooding by rainfall or over- with patches of silvery white scales, femora dark with
flow from streams and irrigation canals (Carpenter deep violet shine, pale on posterior surface, knee spots
and La Casse 1955). Areas covered by rice provide poorly developed. Tibiae and tarsi of fore and mid
good oviposition sites for Ps. columbiae, whereas legs dark violet, tarsomeres IV and V of hind tarsus
areas bare of vegetation are of lesser importance and often the apex of tarsomere III are white scaled.
(Horsfall 1942). Larvae can also be found in all sorts Apical part of hind tibia and tarsomeres I and II of
of ground puddles but principally in open ones, often hind tarsus with long and erect scales, appearing rather
without vegetation and muddy and in ditches along shaggy and with purple reflection (Fig. 15.3b). All
roads. The overwintering eggs hatch in early summer, claws with pronounced subbasal tooth, those of hind
immediately after they have become flooded. There legs smaller. Wing scales dark violet, narrow. Haltere
may be several generations per year (Wood et al. stem pale, knob dark scaled. Tergum I with a median
1979). The larval development is relatively short, patch of dark violet scales, terga II–VI predominantly
usually requiring 4 to 10 days. The females are per- dark scaled with violet reflection, with apicolateral
sistent biters, attacking humans and domestic animals triangular patches of yellowish golden scales. Sterna
at any time during the day or night. In the southern II–VI predominantly yellowish, with scattered violet
United States, the species can be an abundant and scales not forming bands, sternum VII mainly dark
troublesome pest, especially in rice fields (Horsfall violet scaled.
1942). Because of its abundance in rice fields, Ps. Larva: Head distinctly broader than long. Antenna
columbiae is commonly referred to as the dark rice much longer than the head, clothed with conspicuous
field mosquito. sharp spicules, antennal seta 1 (1-A) long, multiple
Distribution: United States, Canada, Grand branched, inserted near middle of antennal shaft.
Cayman Islands, Mexico. Labral seta (1-C) long, slightly curved, postclypeal
396 15 North America

seta (4-C) small, with 2–3 branches. Inner and median Biology: The larvae of Ps. ferox can be found in
frontal setae (5-C and 6-C) equal in length, usually temporary rain filled pools, particularly in or near for-
with 2 branches, 6-C occasionally with 3 branches, ested areas, in overflow pools along streams, and
outer frontal seta (7-C) multiple branched, insertion occasionally in potholes in stream beds after summer
points of 5-C to 7-C nearly in a straight line. The comb rains, usually in a shaded situation. The development
is composed of 6–8 scales in a curved row on the pos- of the immature stages is very fast, and they occur
terior margin of a weakly sclerotized plate, individual from March to November in the southern United
comb scale thorn shaped, the larger basal spines about States and from early May to September in the north
1/3 as long as the prominent median spine. Siphon mod- (Carpenter and La Casse 1955). Larvae and pupae are
erately to strongly widened in the middle and tapering easily alarmed and stay for long periods at the bottom
towards the apex, siphonal index about 4.0, acus dis- of their breeding sites, where they are difficult to see
tinct. Pecten with 3–5 widely spaced teeth on basal 1/4 among the numerous dead leaves and other organic
of siphon, individual pecten tooth with 1–3 lateral den- debris (Belkin et al. 1970). The females are persistent
ticles. Siphonal tuft (1-S) minute, much shorter than and painful biters feeding during the day in the shade
apical width of siphon, multiple branched and inserted of bushes or wooded areas and even attacking in the
laterally beyond middle of siphon, sometimes difficult open on cloudy days. Their main activity is after dark
to detect (Fig. 15.15). Anal segment longer than wide, and they prefer to remain within forested areas (Wood
completely ringed by the saddle, saddle seta (1-X) et al. 1979).
short and inconspicuous, usually multiple branched. Distribution: Southeastern Canada, eastern United
Upper anal seta (2-X) short, multiple branched, lower States, South and Central America, Greater and Lesser
anal seta (3-X) long, single. Ventral brush usually with Antilles
8 cratal setae (4-X) on a very poorly developed grid,
and about 10–12 precratal setae extending almost the
entire length of the anal segment and piercing the sad- Culex (Culex) restuans Theobald 1901
dle. Anal papillae much longer than the saddle, slender
and gradually tapering to a sharp point. Female: Medium sized species. Proboscis dark scaled
with some pale scales on ventral surface, palps short, less
than 1/5 as long as proboscis, dark scaled. Occiput clothed
with narrow curved yellowish scales and dark brown
erect scales dorsally, with broad yellowish scales later-
ally. Integument of scutum light brown, scutum clothed
with fine narrow curved golden brown scales, paler on
anterior and lateral margins and on the prescutellar dorso-
central area. A pair of distinct pale scaled submedian
spots usually present near middle of scutum. Scutellum
with narrow pale golden scales and brown setae on the
lobes. Pleurites with small patches of broad pale scales on
upper parts of mesepisternum and mesepimeron. Legs
dark scaled with metallic blue-green reflection. Femora
and tibiae with pale scales on posterior surfaces and api-
ces, tarsi entirely dark scaled or with indistinct pale basal
rings. Wings entirely clothed with narrow dark scales.
Tergum I with a median patch of dark bronze brown
scales, terga II–VII dark brown scaled, each with a more
or less straight basal band of yellowish scales, usually
broadly joined with basolateral patches of pale scales
(Fig. 15.11c). Sterna mostly pale scaled.
Larva: Antenna shorter than the head, evenly taper-
Fig. 15.15 Larva of Ps. ferox ing towards the apex, spiculate. Antennal seta (1-A)
15.2 Species Description 397

multiple branched, inserted near middle of antennal Biology: The larvae of Cx. restuans can be found
shaft, not reaching to its tip. Postclypeal seta (4-C) short, in a wide variety of aquatic habitats, such as ditches,
with 2–3 branches, inner and median frontal setae (5-C temporary puddles with decaying vegetation, pools
and 6-C) with 4–8 branches, outer frontal seta (7-C) in streams, rock and woodland pools, and in various
multiple branched. Prothoracic setae 1 and 2 (1-P and artificial containers (Carpenter and La Casse 1955).
2-P) long, single, 3-P long, with 1–2 branches. Lateral As with Cx. pipiens, the females of Cx. restuans
abdominal seta 6 on segments I and II (6-I and 6-II) with hibernate in basements, caves, and hollow trees
2 branches, 6-III to 6-VI long and single. The comb con- (Wood et al. 1979). The population reaches its peak
sists of 30–40 scales arranged in an irregular triangular in the spring and early summer throughout most of
patch, individual comb scale rounded apically and its range, and occurs in lesser numbers during late
fringed with small spines. Siphon slightly widened near summer and autumn. The females prefer to feed on
middle and tapering towards the apex, siphonal index birds, but mammals are also readily attacked, they
4.0–5.0. The pecten is composed of about 12 to 20 teeth are regarded as painful biters. They feed on humans
on the basal 1/3 of the siphon, individual pecten tooth outdoors at dusk and during the day in shaded areas
with 1–4 lateral denticles. The siphonal setae (1-S) con- (Breeland et al. 1961).
sist of 3 pairs of long single setae, unequal in length and Distribution: United States, southern Canada,
irregularly placed on the siphon and a pair of small sub- Mexico.
apical setae with 2–3 branches, all setae inserted beyond Medical importance: Viruses of Eastern and
the pecten (Fig. 15.16). Anal segment completely encir- Western equine encephalitis (WEE and EEE) were
cled by the saddle, saddle with spicules on its posterior isolated from wild caught Cx. restuans females
margin, saddle seta (1-X) with 1–2 branches, slightly (Carpenter and La Casse 1955). According to
shorter than the saddle. Upper and lower anal setae (2-X Kilpatrick et al. (2005) Cx. restuans together with
and 3-X) single, 2-X almost as long as 3-X. Ventral Cx. p. pipiens biotype molestus may be responsible
brush well developed, confined to the grid, precratal for up to 80% of the human West Nile Virus (WNV)
setae (4-X) absent. Anal papillae about 2–3 times as infections in the northeastern United States.
long as the saddle, tapered.

Culex (Culex) salinarius Coquillett 1904

Female: Medium sized species. Proboscis dark

scaled, usually paler on ventral side, palps short,
less than 1/5 the length of the proboscis, dark
scaled. Occiput clothed dorsally with narrow curved
golden brown scales and dark erect forked scales,
yellowish white scales along the margins of the
eyes, and with a patch of broad whitish scales later-
ally. Integument of scutum dark brown, scutum
covered with narrow curved golden brown scales,
somewhat paler on the anterior and lateral margins
and on the prescutellar dorsocentral area. Scutellum
with narrow yellowish scales and brown setae on all
lobes. Pleurites with several small patches of broad
pale scales, each patch usually with more than 6
scales. Legs dark scaled, posterior surfaces of fem-
ora and tibiae largely pale scaled, tarsi entirely dark
scaled. Wing veins covered with narrow dark scales.
Tergum I with a median area of dark brown scales,
terga II–VI predominantly dark brown scaled with
Fig. 15.16 Larva of Cx. restuans metallic bluegreen reflection, often with narrow to
398 15 North America

moderately broad basal bands and basolateral

patches of pale scales. Tergum VII and VIII often
entirely covered with yellowish scales (Fig. 15.11b),
sterna with yellowish white scales.
Larva: Antenna shorter than the head, constricted
beyond the insertion point of the antennal seta (1-A),
the part below the constriction pale and spiculate, the
part beyond the constriction darker and with few spic-
ules. Antennal seta (1-A) large, multiple branched,
inserted at apical 1/3 of the antennal shaft, reaching
well beyond its tip. Postclypeal seta (4-C) short, sin-
gle, inner frontal seta (5-C) long, with 3–6 branches,
median frontal seta (6-C) long, with 3–4 branches,
outer frontal seta (7-C) long, multiple branched.
Prothoracic setae 1 and 2 (1-P and 2-P) long, single,
3-P long, with 1–2 branches. Lateral abdominal seta 6
on segments I and II (6-I and 6-II) with 3 branches,
6-III to 6-VI usually with 2–3 branches. The comb
consists of about 50 small scales arranged in an irreg-
ular triangular patch, individual comb scale broadly
rounded apically and fringed with subequal spines.
Siphon long and slender, siphonal index about 6.0–
7.0. The pecten is composed of about 10–16 teeth
extending on the basal 1/4 of the siphon, individual
pecten tooth with 2–4 lateral denticles. Usually 4–5
pairs of siphonal setae (1-S) present, with 2–4 branches
each and inserted beyond the pecten. The proximal
seta (1a-S) as long or longer than the basal width of Fig. 15.17 Larva of Cx. salinarius
the siphon, the penultimate seta inserted laterally
(Fig. 15.17). Anal segment completely encircled by
the saddle, saddle seta (1-X) with 2 branches, some- ing the daytime in shelters outside buildings. Cx. sali-
times single, slightly shorter than the saddle. Upper narius reaches its greatest numbers in the Atlantic and
anal seta (2-X) with 1 long and 2 shorter subequal Mexican Gulf coastal regions. The females bite read-
branches, lower anal seta (3-X) long, single. Ventral ily outdoors and occasionally enter dwellings to feed
brush well developed, confined to the grid, precratal on humans.
setae (4-X) absent. Anal papillae varying in length, Distribution: Eastern United States, south eastern
usually 1.0–1.5 times as long as the saddle, pointed. Canada, Mexico, Bermuda.
Biology: The larvae of Cx. salinarius are found in Medical importance: Cx. salinarius is an impor-
various habitats either in fresh or foul water, in tant vector of West Nile virus (WNV) in the northeast-
swampy edges of lakes, grassy pools, ditches, ponds, ern United States (Kilpatrick et al. 2005).
marshes of various types, and occasionally in rain bar-
rels, cattle tracks, and sometimes in stump holes
(Carpenter and La Casse 1955). Larval development Culex (Culex) tarsalis Coquillett 1896
begins early in the season and continues at a rather
uniform rate throughout the summer and into early Female: Medium sized species. Proboscis mostly
fall in most of its distribution range (Ross 1947). In dark scaled, with a rather broad white ring just
the extreme south, larvae and adults can be found at beyond the middle. Palps short, dark scaled except
any time during the year, but farther north the females for a few white scales at the tip and at the apex of
hibernate. The adults are frequently found resting dur- palpomere III. Occiput with narrow white scales in
15.2 Species Description 399

a median triangular patch, narrow white scales an irregular triangular patch, individual comb scale
around the eye margins. Erect forked scales on dor- rounded apically and fringed with subequal spines.
sal surface dark, a few pale ones on the median area, Siphon slender, evenly tapering towards apex,
broad white scales on the lateral region of occiput. siphonal index about 4.5–5.5. The pecten is com-
Integument of scutum dark brown to black, scutum posed of about 10–15 teeth extending on the basal
covered with narrow reddish brown scales dorsally, 1/3 of siphon, individual pecten tooth with 1–5 lat-
narrow whitish scales along lateral margin anterior eral denticles. Five pairs of multiple branched
to transverse suture, on prescutellar dorsocentral siphonal setae (1-S) present, all inserted in a
area, supraalar area, and narrow posterior dorsocen- straight ventral line, the proximal pair (1a-S) often
tral stripes. Two small mid-dorsocentral whitish inserted near or slightly below apex of pecten
spots often present. Scutellum with narrow whitish (Fig. 15.18). Anal segment completely encircled
scales and brown setae on all lobes. Pleurites with by the saddle, saddle seta (1-X) usually with 2–3
small patches of broad whitish scales confined to branches, occasionally single, shorter than the sad-
posterior margin of mesepisternum and upper part dle. Upper anal seta (2-X) with 3 branches, 1
of mesepimeron. Upper part of postspiracular area branch nearly as long as the lower anal seta (3-X),
with a row of whitish scales. Posterior surfaces of which is single. Ventral brush well developed, con-
femora and tibiae pale scaled, anterior surfaces dark fined to the grid, precratal setae (4-X) absent. Anal
brown, with a median longitudinal stripe of white papillae varying in length, usually 1.0–1.5 times as
scales or a row of pale spots on anterior surfaces of long as the saddle, tapering.
femora. Femora and tibiae with white scales at api- Biology: The larvae can be found in permanent
ces. Hind tarsi with broad basal and apical white and semipermanent water bodies in a variety of habi-
rings (Fig. 15.10a). Fore and mid tarsi with tarsal tats including ditches, irrigation systems, ground
bands narrower on tarsomeres I–III, reduced or
absent on tarsomeres IV and V. Wing veins covered
with narrow dark scales, a few white scales usually
at base of costa (C) and scattered along subcosta
(Sc). Tergum I with a median patch of dark brown
scales, usually with a few pale scales intermixed,
tergum II dark scaled, with a median basal triangu-
lar patch of pale scales. Terga III–VII dark scaled,
with prominent basal bands of white or yellowish-
white scales, tergum VIII often entirely pale scaled.
Sterna mostly pale scaled, with a V-shaped marking
of dark scales on each sternum.
Larva: Antenna more than 2/3 as long as the
head, distinctly constricted beyond the insertion
point of the antennal seta (1-A), the portion below
the constriction spiculate, dark near base, remain-
der pale, portion beyond constriction darker and
with fewer spicules. Antennal seta (1-A) large,
multiple branched, inserted at distal 1/3 of anten-
nal shaft, reaching well beyond its tip. Postclypeal
seta (4-C) small, single. Frontal setae (5-C to 7-C)
multiple branched, of more or less equal length.
Prothoracic setae 1 and 2 (1-P and 2-P) long, sin-
gle, 3-P long, with 1–2 branches. Lateral abdomi-
nal seta 6 on segments I-V (6-I to 6-V) usually
with 3 branches, 6-VI with 2–3 branches. The
comb consists of about 50 small scales arranged in Fig. 15.18 Larva of Cx. tarsalis
400 15 North America

pools, marshes, pools in stream beds, rain barrels, face. Occiput with yellowish lanceolate scales and
hoofprints, and ornamental pools (Ross 1947; dark erect forked scales, a few pale forked scales on
Carpenter and La Casse 1955). Foul water in corrals vertex. Integument of scutum dark brown and black,
and around slaughter yards appear to be favourite scutum covered with pale yellowish scales and a few
larval habitats in many localities. In colder climates, smaller brown scales, submedian area of scutum
adult females pass the winter in hibernation in base- without scales. Scutellum with few pale golden scales
ments, cellars, caves, abandoned mines, and rodent and brown setae on all lobes. Pleurites with patches
burrows (Carpenter and La Casse 1955; Wood et al. of greyish white scales confined to posterior margin
1979). Larval development usually begins during the of mesepisternum and upper part of mesepimeron.
late spring and continues until early autumn through- Prespiracular and postspiracular setae absent. Femora
out most of its range, with several generations pro- and tibiae speckled with pale and dark scales, the api-
duced per year. Although females of Cx. tarsalis ces of the femora almost entirely dark-scaled, hind
feed on domestic and wild birds like other Culex, tibia with a ring of pale scales near the apex. Tarsomere
they seem to prefer mammals as hosts (Wood et al. I of all legs dark scaled, with a narrow white ring
1979). They are painful and usually persistent biters, basally and a broader white ring a little beyond mid-
attacking at dusk and preferably after dark, and read- dle, tarsomeres II–V each with basal half white, api-
ily entering dwellings for blood meals. During the cal half dark. Wing scales broad, mixed dark and
day they hide in sheltered places. This mosquito is a yellow, the dark scales predominating. Terga dark
serious pest to livestock, poultry, and humans scaled, with yellowish basolateral patches and occa-
(Lungstrom 1954). sionally with narrow basal pale bands. Sterna with
Distribution: United States, south western Canada, dark and pale scales intermixed, the pale scales more
Mexico. numerous on the basal part of each sternum, abdomen
Medical importance: The vector competence of bluntly ended.
this species has been demonstrated not only in the Larva: Head much broader than long. Antenna
laboratory, but as a major vector in outbreaks of slender and long, more than twice as long as the head,
encephalitis viruses in California (Reeves 1990). Cx. sparsely spiculate basally. Antennal seta (1-A) with
tarsalis is believed to be the main vector of Western multiple branches, arising from a notch on basal third
equine encephalites virus (WEE) under natural condi- of antennal shaft, a pair of short setae inserted at the
tions. The virus has been isolated from wild caught middle of the shaft. Postclypeal seta (4-C) small, mul-
females on several occasions in areas in which the dis- tiple branched, frontal setae (5-C to 7-C) multiple
ease was both epidemic and epizootic. The viruses of branched, 5-C much shorter than 6-C and 7-C.
both St. Louis and California Encephalitis (SLE and Prothoracic setae 1 to 3 (1-P to 3-P) arising from a
CE) have been isolated from this mosquito (Carpenter common sclerotized tubercle, 1-P and 2-P single, 3-P
and La Casse 1955). Cx. tarsalis together with Cx. p. with multiple branches. The comb consists of 8–15
quinquefasciatus play an important role in the West scales arranged in a single irregular row, individual
Nile virus (WNV) transmission in most of the western comb scale with a very prominent median spine and
United States (Goddard et al. 2002; Reisen et al. 2004, fringed on basal half with short spinules. Siphon short,
2008). strongly attenuated and heavily sclerotized beyond
middle, the attenuated part of siphon bears saw-like
projections dorsally and strong hooks apically, forming
 oquillettidia (Coquillettidia) perturbans
C a stout piercing organ. Siphonal seta (1-S) a multiple
(Walker 1856) tuft, arising before the heavily sclerotized part of the
siphon, pecten absent. Anal segment elongated, much
Female: Moderately large species. Proboscis dark longer than wide, completely encircled by the saddle.
scaled apically, speckled with yellowish scales basally Saddle seta (1-X) a short multiple tuft, inserted well
and with a broad median ring of pale scales. Palps before the posterior margin of the saddle. Upper and
about 1/5 as long as proboscis, mottled with dark and lower anal setae (2-X and 3-X) multiple branched, 2-X
pale scales. Pedicel light brown on outer surface, shorter than 3-X. Ventral brush well developed, cratal
darker and with a patch of pale scales on inner sur- setae (4-X) usually restricted to the grid but often with
15.2 Species Description 401

marshes. After hatching, the small larvae attach

­themselves with their modified siphon to the roots or
submerged stems of plants where they remain through-
out development. The pupa also attaches itself to plants
by means of the modified respiratory trumpets and
remains there until the adult is ready to emerge
(Carpenter and La Casse 1955). The larvae are associ-
ated mainly with plants of Typha, Sagittaria, Nymphea,
Juncus, Phragmites, Carex and Calla (Ross 1947).
They are difficult to collect, as they quickly drop off
the host plant whenever they are disturbed. The winter
is passed in the larval stage, there appears to be no lar-
val diapause, and the adults emerge in the spring and
summer (Wood et al. 1979). The females are fierce bit-
ers and usually take their blood meal during the night.
They occasionally attack humans during daylight
hours in shady places. The adults are strong fliers with
a flight range of more than 10 km and are important
pests in communities near shallow lakes, swamps, and
marshes which are partly overgrown with emergent
aquatic vegetation.
Distribution: United States, southern Canada,
Fig. 15.19 Larva of Cq. perturbans Mexico.
Medical importance: The virus of Eastern Equine
1–2 minute precratal setae piercing the saddle. Anal Encephalitis (EEE) has been isolated from wild caught
papillae shorter than the saddle, pointed (Fig. 15.19). females of Cq. perturbans in southern USA (Carpenter
Biology: The eggs are laid in floating rafts on the and La Casse 1955). It plays a minor role in human
surface of water in areas of heavy emergent vegetation. West Nile virus (WNV) infections in the northeastern
Larvae are mainly found in permanent bogs and United States (Kilpatrick et al. 2005).
 Part IV
Control of Mosquitoes
Chapter 16
Biological Control

16.1 Introduction subsequently developed within the target populations.

Moreover, despite the beneficial effects of traditional
Biological control, in the broadest sense, is defined as insecticides, they also often have unwanted characteris-
the reduction of the target population by the use of tics, such as their non-selectivity which frequently
predators, parasites, pathogens, competitors, or toxins causes ecological damage. As public awareness of
from microorganisms (Woodring and Davidson 1996). environmental issues increased, regulations controlling
Biological control aims to reduce the target population the application of chemicals were tightened. As a result,
to an “acceptable” level and, at the same time, to avoid a renaissance in the biological control of mosquitoes
adverse effects to the ecosystem. As far as mosquito took precedence in the 1960s and 1970s. By 1964,
control is concerned, biological control measures Jenkins had already listed more than 1,500 parasites,
should integrate the protection of humans from mos- pathogens, and predators as potential candidates for
quitoes with conservation of the biodiversity, while biological control. Today, the literature on mosquito
avoiding toxicological and eco-toxicological effects. antagonists is immense (Notestine 1971; Lacey and
As a result, the regulatory power of the ecosystem is Lacey 1990; Legner 1995; Medrano 1993; Quiroz-
maintained by protecting the existing community of Martínez and Rodríguez-Castro 2007; Mogi 2007).
mosquito predators. One of the major advantages of biological control
The use of beneficial organisms for the control of measures is that existing predators are conserved,
mosquitoes was first recognised in the late nineteenth which will in turn assist the control effort by preying
century, when attempts were made by introducing upon newly-hatched mosquito larvae after the control
predators such as dragonflies (Lamborn 1890). operation, thereby, considerably enhancing the effi-
However, mass breeding and successful introduction cacy of the current control measures.
of predators, such as hydra, flatworms, predacious By promoting the conservation of existing popula-
insects or crustaceans, often introduces a range of tions of predators, parasites or pathogens, there are
problems. However, such problems did not occur, or two major strategies for the augmentation of the popu-
occurred only to a limited extent, with the use of fish, lation of mosquito antagonists.
such as the mosquito fish, Gambusia affinis (western “Inoculation” refers to the release of small numbers
mosquitofish) and G. holbrooki (eastern mosqui- of predators, parasites, or pathogens into the habitat of
tofish), which were successfully introduced into many the target organisms. The antagonists become estab-
countries to control mosquito larvae in the early 1900s lished, they reproduce and multiply under favourable
(Bellini et al. 1994; Legner 1995; Walton 2007; living conditions in the new habitat, resulting in a sus-
Chandra et al. 2008). tained suppression of the target population which can
With the discovery and large-scale use of synthetic be achieved by successive generations of mosquito
insecticides in the 1940s and 1950s, biological control enemies. For instance, the inoculation of fish into
of mosquitoes was unfortunately no longer considered newly-flooded rice fields is a very common practice in
to be an important method. mosquito control (Bellini et al. 1994; Walton 2007).
However, the initial euphoria that greeted the success “Inundation” means the release of an overwhelm-
of synthetic insecticides rapidly dissipated as resistance ing number of predators, parasites, pathogens, or their

N. Becker et al., Mosquitoes and Their Control, 405

DOI 10.1007/978-3-540-92874-4_16, © Springer-Verlag Berlin Heidelberg 2010
406 16 Biological Control

toxins into the mosquito habitat. Such mass release of 16.2.1 Vertebrate Predators
organisms or applied pathogens (toxins) can have an
immediate effect through a significant reduction of
16.2.1.1 Fish (Osteichthyes)
the target population. For instance, inundation con-
trol is successfully practiced with microbial patho-
The best known aquatic predator of mosquitoes is the
gens which are produced in artificial cultures, e.g.
mosquito fish, G. affinis, which is native to south-east
Bacillus thuringiensis israelensis (B.t.i.) and B. spha­
United States, eastern Mexico, and the Caribbean, and
ericus (B.s.). Only rarely do the antagonists become
the common guppy, Poecilia reticulata, which is native
established in the habitat, for example, B.s. is able to
to tropical South America. Both fish are effective pre­
recycle under certain conditions (Becker et al.
dators because their upward-facing mouth enables
1995a).
them to consume mosquito larvae living on or close to
A prerequisite for the successful use of predators,
the water surface. Other biological attributes of these
parasites or pathogens is the precise knowledge of the
viviparous fish are their high reproduction rate, small
biology of the antagonist in question and its interaction
size (3–6 cm), and high tolerance to variations in tem-
with the ecosystem. For example, the introduction of
perature, organic pollution, and salinity. G. affinis can
foreign faunal elements such as predators, risks dam-
survive water temperatures below 13°C and even over-
aging or displacing existing populations of predators.
winters in areas with short periods of frost, but P. reti­
For instance, introduced fish may reduce numbers of
culata is restricted to subtropical and tropical climates.
aquatic insects, crustaceans or amphibians which
The latter is used particularly in urban areas against
would otherwise be effective predators of mosquito
Cx. p. quinquefasciatus, which usually occurs in
larvae. Rare indigenous species which do not feed on
masses in highly polluted water bodies, but the effi-
mosquito larvae may also be endangered. A thorough
cacy of the fish can be variable (Sjogren 1972; Dua
understanding of predator/prey or parasite/host rela-
et al. 2007).
tionship is therefore of fundamental importance for the
Gambusia affinis is the most widely disseminated
successful and ecologically sound use of antagonists.
organism for mosquito control (Walton 2007). As early
Different species of mosquitoes inhabit very different
as 1937, Hackett reported on the value of G. affinis for
habitats, and have developed various life strategies by
the control of malaria in Europe. It is thought that G.
adapting to habitats with very different abiotic and
affinis may have contributed significantly to the reduc-
biotic conditions. Antagonists can only successfully
tion of malaria in Turkey and Iran (Tabibzadeh et al.
reduce a target population if their own life strategy is
1970; Inci et al. 1992). In the USA, mosquito fish are
adapted to the target population.
commonly bred by local mosquito abatement districts
and selectively released for control, in an Integrated
Mosquito Management (IMM) programme. In California,
they are used successfully in rice fields against the
16.2 Predators immature stages of An. freeborni and Cx. tarsalis.
Whereas stocking at a rate of more than 500 female
In general, predators of immature mosquito stages mosquito fish/ha in rice fields gave excellent control of
are more effective than predators of adults (Fig. 16.1). Cx. tarsalis (Hoy and Reed 1971; Steward et al. 1983),
As a rule, mosquito larvae and pupae are concentrated significant reduction rates against An. freeborni were
at their breeding sites and are more easily available to only achieved when more than 4,000 fish/ha were used
predators than the widely dispersed adults. Moreover, (Kramer et al. 1987a, b, 1988a, b). The inundative
adult mosquitoes evade many predators as they are release of 4,800 mosquito fish/ha was effective against
mostly nocturnal. Mosquitoes have the characteris- Ps. columbiae in Arkansas rice fields (Davey and
tics of typical r-strategists (meaning, a high rate of Meisch 1977a–c). In California, a reduction rate of
reproduction and a relatively short life cycle). >70% was observed in a population of Cx. quinquefas­
Predators are particularly effective if they have a sim- ciatus by the inundative release of mosquito fish in
ilarly high rate of reproduction and/or a high rate of urban underground storm drains. Generally, mosquito
feeding, like fish. fish are most effective in water bodies where the
16.2 Predators 407

Fig. 16.1 Importance of some mosquito predators in the food web (size of arrows refers to importance)

vegetation is less dense and the mosquito larvae are Ae. aegypti, the vector of dengue and dengue haemor-
more accessible. rhagic fever (DHF). In Southern California, Sjogren
The South American species P. reticulata is a popu- (1971) and Mian et al. (1985, 1986) successfully tested
lar aquarium fish which has been introduced into many ­guppies against mosquitoes in sewage plants.
countries through the ornamental fish trade. This guppy Before the discovery of B.t.i., the use of fish was
frequently inhabits sewage ditches in subtropical and lauded as being one of the most successful biological
tropical countries, where it definitively contributes to weapons for the control of mosquitoes. Many critics,
the reduction of larval populations of Cx. p. quinque­ however, disapprove of the use of mosquito fish
fasciatus, the main vector of bancroftian filariasis. Sasa because of their concern for the native fish fauna. G.
and Kurihara (1981) discussed the use of guppies in affinis is omnivorous and feeds not only on inverte-
filariasis control programmes. In Sri Lanka, free-living brates, which can themselves be useful predators, but
fish were caught and introduced into mosquito breed- also on the eggs and offspring of indigenous fish. The
ing sites (Sabatinelli et al. 1990). In Malaysia, the fish introduction of G. affinis may have some adverse
are also used in water containers for the control of effects on extensive aquatic predator populations
408 16 Biological Control

c­ onsisting of water beetles, water bugs, copepods, proteins or for sale (Xu, personal communication;
dragonflies or urodelans and can greatly repress eco- ICMR Bulletin 2000).
nomically important fish species such as carp. Representatives of the Cyprinodontidae produce
Schoenherr (1981) and Lloyd (1987) reported that hard-shelled eggs that are resistant to drought. In
more than 30 species of native fish have been adversely China, Oryzias latipes is also used in rice fields to con-
affected by the introduction of G. affinis. trol mosquitoes (Xu, personal communication;
For this reason, it is essential to study the biology of Sugiyama et al. 1996). These widely distributed fish
predacious organisms with special reference to prey grow to about 4 cm in length and feed predominantly
selectivity, reproductive potential, and their benefit as on mosquito larvae or insects falling onto the water
predators in relation to costs and the environmental surface. Despite their small size, one fish eats on aver-
damage they might cause, before they are actually age, 51 Anopheles or 118 Culex fourth-instar larvae/
released. The ecosystem must also be carefully evalu- day. In Asia, a species belonging to the labyrinth fish,
ated to determine the potential effect of the released such as Macropodus opercularis, M. chinensis, and
organisms on the existing biota. This process is even Tanichthys albonubes, are avid feeders of mosquitoes.
more important if non-indigenous species are to be In the Americas, the cyprinodontid Cynolebias bel­
released (Hurst et al. 2006; Chandra et al. 2008). lottii breeds in temporary waters. The eggs can survive
The indiscriminate use of G. affinis for mosquito dry periods. Therefore, the fish can be successfully
control is no longer recommended by the World Health used as predators in rice fields (Coykendall 1980;
Organization because of its aggressiveness towards Walters and Legner 1980; Gerberich and Laird 1985).
numerous aquatic organisms and also because of its Shallow floodlands, which form mass breeding sites
doubtful contribution to the control of mosquito-borne for mosquitoes, can be deepened into permanent water
diseases (Service 1983). bodies or connected by ditches to accomodate fish if it
Fish are also, occasionally, introduced because of is considered environmentally sound. The fish and
their ability to consume aquatic vegetation. As pre­ their offspring are then able to invade the breeding
dators, they can reduce the number of mosquitoes, but sites of floodwater mosquitoes such as Ae. vexans. In
as consumers of aquatic plants, they can also reduce field investigations in Germany, native fish species demon-
the niches for the larval development of mosquitoes. In strated an impressive feeding performance. Fish, of
California, the subtropical cichlids Tilapia zilli, approximately 5 cm in length, were kept in cages in
Orechromis mossambia, and O. hornorum were found mosquito breeding sites and fed with fourth-instar
to be useful (Asimeng and Mutinga 1992). larvae of Ae. vexans. At water temperatures averag-
Because of the risk to an existing community which ing 22°C, the following feeding rates of fourth-instar
can result from the introduction of non-indigenous larvae/day were recorded: Cyprinus carpio: 302;
organisms, native fish should be used as a component Carassius carassius: 238; Tinca tinca: 185;
in an integrated mosquito management (IMM) pro- Gasterosteus aculeatus: 178; Abramis brama: 148;
gramme. In China, the grass carp, Ctenopharygodon Rutilus rutilus: 147; Alburnus alburnus: 113;
idella, and the common carp, Cyprinus carpio, are Leucaspius delineatus: 99; Scardinius erythrophthal­
used in rice fields as young fish. During flooding of the amus: 80 and Gobio gobio: 63. Feeding rates of more
rice fields, the fish not only contribute to the control of than 1,000 Aedes/Ochlerotatus larvae within 12 h
mosquito breeding but also feed on rice pests, such as were shown by the larger species C. carassius and
grasshoppers, which fall onto the water surface. In S. erythrophthalamus (Gebhard 1990).
addition, the fish also manure the rice cultures with
their excreta. Furthermore, the grass carp, as a plant
feeder, prevents the growth of weeds. The beneficial 16.2.1.2 Amphibians (Amphibia)
effects of the grass carp led to an increase in the total
rice yield by more than 20%. If the rice fields are Urodela (newts) and their larvae are important pre­
drained before the harvest, the fish are kept for another dators of immature stages of mosquitoes (Sack 1911;
year in permanent main irrigation ditches. Because of Martini 1920b; Twinn 1931; Blum et al. 1997). In
their relatively fast growth, carp can subsequently be feeding experiments in Europe, Triturus cristatus and
used for personal requirements, either as a source of T. vulgaris proved to be voracious consumers of mos-
16.2 Predators 409

quitoes (Kögel 1984). Whereas 2-week-old larvae of Becker 2003). To determine the composition of the
T. cristatus devoured about 15 third-instar larvae of birds’ diet, the neck-ring method was applied to nest-
Cx. p. pipiens, 5–10-week-old Triturus larvae captured lings of the House Martin (Delichon urbica), the Reed
~100 fourth-instar larvae/day. The feeding rate of Warbler (Acrocephalus scirpaceus), the Pied
T. vulgaris and T. cristatus is approximately the same. Flycatcher (Ficedula hypoleuca), the Great Tit (Parus
In contrast to urodelans, anurans have little effect as major), and the Blue Tit (Parus caeruleus). The aerial
predators on mosquitoes. In a 3-year study in the flood- insect abundance in these areas was also investigated
plains of the Rhine River 2,163 anuran specimens of using a cone trap on a vehicle.
the taxa Rana arvalis, R. temporaria, R. dalmatina, R. The main activity period of the nuisance mosqui-
esculenta s.l., Hyla arborea, Bufo bufo, and Pelobates toes (e.g. Aedes vexans) in the area was during dusk,
fuscus were subjected to stomach flushing (Blum et al. whereas the frequency with which the flight-hunting
1997). Most of the prey species observed were House Martin fed its nestlings began to decrease
beetles (Coleoptera), springtails (Collembola), snails approximately 60 min before sunset. This may explain,
(Gastropoda), spiders (Araneae), ants (Formicidae), in part, the low numbers of mosquitoes found in the
and woodlice (Isopoda), which all belong to the epi- diet of the House Martin nestlings. Out of a total of
geal fauna. Only 0.1% of the prey were Culicidae, 6,761 insects which were identified from the nestlings’
mostly adult Ae. vexans. The only anuran known to food, less than 1% belonged to the family Culicidae
consume Culicidae at a higher rate is Bombina bom­ (Fig. 16.2). These birds preferred feeding their nest-
bina. Lac (1958) reported 5.7% and 16.7% of Cx. pipi­ lings aphids (Aphidina, during first brood; Staphylini‑
ens and An. maculipennis s.1. larvae respectively. dae and Brachycera, during second brood).
Additionally, 140 food samples were taken from
birds which collect insects from or near the vegeta-
16.2.1.3 Birds (Aves) tion. Within these samplings, only 5 mosquitoes were
found (4.4% of the bird’s diet); although, car trap
In general, birds are not considered to be important samples over many years indicate that adult mosqui-
predators of mosquitoes, although mosquitoes are a toes are present each summer in these areas. The Great
source of food for some bird species (Blotzheim 1985). Tit and Blue Tit preferred to feed their nestlings with
For example, the duck, Anas platyrhynchos, was larvae of Lepidoptera, while the Reed Warbler and
repeatedly observed filtering out larvae of Ae. vexans Pied Flycatcher preferred mainly flightless inverte-
from mass breeding sites along the Rhine River brates (e.g. caterpillars, spiders, aphids). Among the
valley. Dipterans in the bird diet, larger species (e.g. Tipulidae,
There are two main reasons for the relatively insig- Syrphidae) were more common. Mosquitoes did not
nificant role of birds as predators of adult mosquitoes. make up a significant proportion of the birds’ diets.
Firstly, the activity phases of mosquitoes and birds do
not overlap to any great extent. Most mosquitoes are
active at dusk, whereas the majority of birds search for 16.2.1.4 Bats (Mammalia: Chiroptera)
food during the day when most of the mosquito spe-
cies are resting in vegetation. Secondly, floodwater Whereas the majority of insectivorous birds are day-
mosquitoes occur irregularly, only after flooding and light hunters, bats, in contrast, usually hunt during
are, therefore, not available as a stable food-source in the night. Therefore, the activity patterns of both bats
seasons when flooding does not occur. As a conse- and most of the mosquito species show a consider-
quence, insects, such as midges (Chironomidae) which able overlap. After dusk, the bats emerge from their
breed mainly in permanent waters and appear in large roost, and at the same time the flight activity of mos-
numbers more or less every year, are a more reliable quitoes is increasing.
source of food for birds than floodwater mosquitoes. World-wide, there are about 1,000 known bat spe-
An analysis of the diet of birds living in the flood- cies, the majority being exclusively insectivorous and
plain areas of the Upper Rhine Valley (Germany) exhibiting a large variety of hunting strategies. Most
showed that the portion of mosquitoes in the diet of effective mosquito hunters might be gleaning species,
the investigated bird species is low (Timmermann and e.g. Bechstein’s bats (Myotis bechsteinii), that take
410 16 Biological Control

Jun 91 Aug 91

11
Aphidinae
1301
708
Staphylinidae
6
177
Rest Coleoptera
23
191
Brachycera
27
6
Culicinae
0
258
Nematocera
50
92
Hymenoptera
12
84
Auchenorrhyncha
8
14
Heteroptera
6
0
Trichoptera
13
13
Others
11

0 200 400 600 800 1000 1200 1400

Number of prey organisms (in 39 food balls)

Fig. 16.2 Prey of house martin Delichon urbica in the Upper Rhine area

their prey from foliage and hunt closely to vegetation, generally considered today that bats are beneficial in
or species like Daubenton’s bats (M. daubentonii), that terms of controlling pest insects (Tuttle 2000).
fly and hunt closely over the surface of open water However, bats are not considered an effective compo-
bodies (Arnold et al. 1998). nent in mosquito control programmes, but they are an
Mosquito feeding by bats was recorded repeat- important group of organisms which should be pro-
edly, mostly by analyzing guano samples, but the tected by the use of target-specific control agents.
amount of mosquitoes consumed varied consider-
ably. Studies on the diet of bats, carried out throughout
Europe, showed a great variety of nocturnal insects
providing food resources for bats, such as moths 16.2.2 Invertebrate Predators
(Lepidoptera), beetles (Coleoptera), lacewings
(Planipennia), caddisflies (Trichoptera), mayflies Countless invertebrates are known as predators of
(Ephemeroptera), and midges (Chironomidae) (Swift mosquitoes, especially, of the larvae. The biology and
et al. 1985; Rydell 1986; McAney et al. 1991; Wolz importance of the predators have been investigated in
1993). A study of the trophic ecology of Daubenton’s numerous studies (Lamborn 1890; Hinman 1934;
and Nathusius’ bats in southwest Germany (Arnold Kühlhorn 1961; Jenkins 1964; James 1967; Service
et al. 2000) showed that mosquitoes are not an impor- 1977; Kögel 1984; Collins and Washino 1985; Quiroz-
tant food source for these bat species. Under rare con- Martinez and Rodriguez-Castro 2007). Although
ditions, when they occur in dense populations, invertebrates have been shown to be effective pre­dators
mosquitoes might become a major prey for some bat of mosquitoes, they are seldom used in control pro-
species, like the Northern Bat (Eptesicus nilssonii) that grammes due to the great difficulties and the high costs
relies heavily on mosquitoes and other dipteran insects involved in mass rearing of these organisms.
during the summer in northern Sweden (Rydel 1990). Nevertheless, their role as mosquito predators is
The majority of bat species are opportunistic hunt- beyond dispute. Mosquitoes can rarely develop in large
ers that focus on insects occurring in large numbers on numbers at breeding sites where predacious inverte-
their hunting grounds (Gloor 1995), therefore, it is brates are abundant. In this section, different groups of
16.2 Predators 411

0 5 10 15 20 25 30 35
Coleoptera: Laccophilus sp. 10

Guignotus pusillus 5
Rhantus sp. 20
Hydrophilus caraboides 30
Heteroptera: Notonecta glauca 25
Gerris lacustris 15
Odonata: Aeshna cyanea 30
Coenagrion sp. 10
Crustacea: Cyclops sp. 2
Araneae: Argyroneta aquatica 25
Turbellaria: Mesostoma sp. 5
Coelenterata: Hydra sp. 10
Aedes larvae/day

Fig. 16.3 Average feeding rate of some invertebrate predators of mosquito larvae

invertebrates and their importance as predators will be populations by Mesostoma sp. in California’s rice
discussed (Fig. 16.3). fields, which led to an extensive investigation into the
mass rearing of these flatworms.
In central Europe, Bothromesostoma sp. sometimes
16.2.2.1 Hydra (Coelenterata) occurs in abundance in ephemeral waters where it can
completely suppress Ae. vexans populations (Becker
In feeding experiments, polyps of the genus Hydra killed, 1984). This flatworm is an efficient predator which
on average, between 6 and 21 mosquito larvae/day. Polyps feeds mainly on mosquito larvae and has consequently
frequently contribute considerably to the reduction of adapted its way of life to that of the prey. Like their
mosquitoes in permanent water bodies (Qureshi and Bay prey, the turbellarians can survive dry periods as
1969). Because of their beneficial effects, Chlorohydra drought-resistant eggs and hatch during summer
viridissima (Pallas) were used in a number of field experi- floods. At high summer temperatures, they develop
ments (Lenhoff 1978; Cress 1980). within a week, to 7 mm long organisms to the repro-
ductive stage and produce ~20 eggs. In laboratory
experiments, a turbellarian consumed up to 67 mos-
quito larvae during its development.
16.2.2.2 Flatworms (Turbellaria)

Flatworms are one of the most thoroughly investigated

groups of predators (Legner 1991, 1995). Turbellarians, 16.2.2.3 Spiders and Mites (Arachnids)
like Mesostoma sp., secrete slime to catch mosquito
larvae. When the larva sticks to the mucous secretion Spiders are commonly known to be predators of adult
and tries to escape, the flatworm becomes aware of its mosquitoes, particularly at day resting places and shel-
prey, smothers it and sucks it up with its pharynx. ters for hibernation (Service 1973a). Some species are
Some Mesostoma species, such as M. ehrenbergii, hunters of aquatic organisms. Representatives of
can make a significant contribution to the reduction of Pisauridae and Lycosidae, hunt on the water surface
mosquitoes. Case and Washino (1979) reported a con- and occasionally capture mosquito larvae, pupae
siderable reduction of Cx. tarsalis and An. freeborni or emerging adults (Bishop and Hart 1931). Their
412 16 Biological Control

i­mportance as predators is, however, considered to be ern Vietnam, where copepods of the genus Mesocyclops
slight (Kühlhorn 1961). were used for the effective control of Ae. aegypti by
One of the most effective arachnid predators of inoculation into wells, large cement tanks, ceramic
mosquito larvae is the aquatic spider Argyroneta jars, and other domestic containers. The use of
aquatica. This fascinating species builds webs under Mesocyclops sp. was complemented by community
the water to catch its prey. In aquarium experiments, participation with respect to recycling, to eliminate
the maximum ­feeding rate was 29 fourth-instar mos- unused and discarded containers.
quito larvae/day (Kögel 1984). In permanent pools,
these spiders can lead to a significant reduction of
mosquitoes. 16.2.2.5 Insects (Insecta)
Water mites (Hydrachnellae) can also contribute to
the suppression of larval mosquito populations. For Odonata
example, in laboratory experiments the small water
The importance of dragonflies (Odonata) as mosquito
mite Piona nodata consumed up to 18 mosquito lar-
predators has been known for a long time. Both the
vae/day (Kögel 1984). When the adult mosquitoes
nymphs and the adults catch mosquitoes (Kögel 1984;
emerge, some mites attach themselves to the emerging
Sebastian et al. 1990). Dragonfly nymphs usually
adult and use it as a carrier to disperse to new
have a long development and, therefore, occur mainly
habitats.
in permanent waters. In feeding experiments,
anisopteran nymphs proved to be extremely voracious.
According to Kögel (1984), nymphs of Aeshna cyanea
16.2.2.4 Crustaceans (Crustacea)
consumed up to 100 mosquito larvae/day (average 30
larvae/day). Zygopteran nymphs, such as Coenagrion
The tadpole shrimp, Triops cancriformis, is consid-
puella, are usually less efficient as predators (on average,
ered to be a predator of mosquito larvae. The shrimp
10 third-instar larvae/day).
eggs can survive dry periods for several years and the
In rice fields in Japan, ~208 dragonfly nymphs/m2
larvae hatch after flooding, often in association with
were recorded. Such mass occurrences classified them
Aedes/Ochlerotatus larvae. In California, attempts
among the most important predators of mosquitoes in
were made to control Aedes/Ochlerotatus and
rice field ecosystems (Mogi 1978).
Psorophora species with T. longicaudatus (Tietze
and Mulla 1987, 1991).
Among the crustaceans, copepods are important
Heteroptera
predators of mosquito larvae (Miura and Takahashi
1985; Marten and Reid 2007). It is more their occur- The majority of water bugs (Hydrocorisa and
rence in enormous numbers than their rate of feeding Amphicorisa) are voracious consumers of mosquitoes.
which makes them important predators of mosquitoes. However, there is a significant variation in feeding
In laboratory experiments, Megacyclops viridus and behaviour of different families.
Acanthocyclops vernalis consumed 1–2 first and sec- Corixidae: In feeding experiments, one of the most
ond-instar larvae of Ae. vexans/day (Kögel 1984). abundant corixids in central Europe, Sigara striata,
Hintz (1951) reported that Cyclops sp. caught about 5 captured 2–3 early larval instars of Ae. vexans/day. The
first and second-instar larvae of Ae. aegypti/day. larger but less common species, Corixa punctata
Because of their small size, copepods mainly capture (1 cm), consumed up to 45 larvae/day, and even Cymatia
early instar mosquitoes, but as predators, they are only coleoptrata (6 mm) consumed up to 47 early larval
effective when present as adults before the mosquito instars of Ae. vexans/day (Kögel 1984). Although the
larvae hatch. The use of Mesocyclops aspericornis, Corixidae are usually common in mosquito breeding
which has been introduced into artificial containers, sites, their importance as mosquito predators is rather
wells, and terrestrial crab burrows, has led to a reduc- slight because of their mostly omnivorous feeding hab-
tion of >90% of Ae. aegypti and Ae. polynesiensis in its (Washino 1969).
Asia (Riviere et al. 1987a, b; Kay et al. 1992). Similar Naucoridae: One of the most common species in
results have been achieved by Vu et al. (1998) in north- Europe, Ilyocoris cimicoides, proved to be extremely
16.2 Predators 413

Coleoptera
Because of their abundance and great voracity, many
water beetles and their larvae are effective preda-
cious aquatic insects (Baldwin et al. 1955; Trpis
1960; Kühlhorn 1961; James 1966, 1967; Bay 1972;
Service 1973a; Nelson 1977; Kögel 1984).Their
ability to inhabit and reproduce in great numbers in
various mosquito-breeding habitats further enhances
their significance. The following section briefly out-
lines the differences between individual representa-
tives of the different water beetle families as mosquito
predators.
Fig. 16.4 Ranatra linearis feeding on a mosquito larva
Dytiscidae: Dytiscids are the most important
predators among the water beetles (Nelson 1977).
voracious. The feeding rate of adult bugs was on Not only the large species of the subfamily Dytiscinae,
­average, >20 mosquito larvae/day, and their nymphs but also the medium-sized species of the subfamily,
consumed as many as 35 larvae of Ae. vexans/day Colymbetinae, and the small sized species of the sub-
(Kögel 1984). families, Hydroporinae, Noterinae, and Laccophilinae
Nepidae: The widely distributed water scorpion, can show high rates of feeding on mosquito larvae.
Nepa cinerea, consumed 10–18 fourth-instar larvae of The large larvae of Dytiscus marginalis and D. cir­
Ae. vexans daily (Kögel 1984). This heteropteran cumflexus feed predominantly on larger creatures
inhabits the shallow littoral of stagnant waters, where such as tadpoles and small fish. However, their young
it is certainly one of the most important predators. larvae can consume more than 100 Ae. vexans fourth-
Ranatra linearis can also frequently be observed instar larvae/day. Among the medium-sized dytisc-
feeding on mosquito larvae (Fig. 16.4). ids, Rhantus species are the most efficient predators.
Notonectidae: Amongst the Heteroptera, notonectids In laboratory experiments, the adults of R. consputus
are known for their voracious feeding on ­mosquito lar- and R. pulverosus captured up to 40 third and fourth-
vae in permanent and semipermanent waters (Hinman instar larvae/day (Kögel 1984). While swimming,
1934; Hazelrigg 1975, 1976; Murdoch et al. 1984; they are able to rapidly to seize the prey with their
Legner 1995). For this reason, Notonecta undulata and front legs. Not only the adults of Rhantus spp., but
N. unifasciata were mass-cultured for use in rice fields also their larvae are frequently found in temporary
in California (Sjogren and Legner 1989). In experiments Aedes/Ochlerotatus breeding sites, where they feed
with N. glauca, the daily average feeding rate was 25 mainly on mosquito larvae. Depending on the larval
third-instar larvae of Ae. vexans (Kögel 1984). stage, they consume between 4–6 Ae. vexans larvae
Pleidae: Although Plea leachi (size 2–3 mm) is one up to a maximum of even 20 fourth-instar larvae/day.
of the smallest predators, it is able to catch up to 20 The adults of Agabus species do not consume as
mosquito larvae/day (Kögel 1984). many larvae of Aedes/Ochlerotatus as do Rhantus
Gerridae and Hydrometridae: The Gerridae and spp. adults. In Europe, Agabus spp. are especially
Hydrometridae live on the water surface, usually in abundant in swampy alder forests populated by the
large numbers. They feed mainly on insects, which fall immature stages of snow-melt mosquitoes. Among
onto or emerge from the water surface. Gerris lacustris the dytiscids, the representatives of the Hydroporinae
can sometimes be observed seizing mosquito larvae out and Laccophilinae achieve very high feeding rates.
of the water. Whereas this hunting behaviour is rather an In laboratory experiments, the larvae of Coelambus
exception in the Gerridae, Hydrometra stagnorum is impressopunctatus captured up to 8 third- and fourth-
more specialized for pulling mosquito larvae and even instar larvae of Ae. vexans; the larvae of Hygrotus
pupae out of the water. In laboratory experiments, inaequalis and Hyphydrus ovatus, up to 3 Aedes/
Hydrometra sp. captured up to 15 mosquito ­larvae/day Ochlerotatus larvae, and Hydroporus palustris, up to
(Pruthi 1928). a maximum of 10 Aedes/Ochlerotatus larvae/day
414 16 Biological Control

(Kögel 1984). Whereas the adults of these beetles larvae. In North America, species of the genus
capture fewer mosquito larvae than do their larvae, Toxorhynchites have been closely studied for decades
the adults of Laccophilus spp. are highly voracious. as antagonists of nuisance/vector mosquitoes
Even the very small species Guignotus pusillus (Gerberg and Visser 1978; Trpis 1981; Lane 1992).
(about 2 mm long) can contribute to the reduction of The females of these carnivorous mosquitoes, which
newly-hatched first-instar mosquito larvae. Some occur mainly in warm climates, do not suck blood but
beetles of the subfamily Colymbetinae, such as feed on nectar. They prefer to lay their eggs in natural
Colymbetes fuscus are quoted as potential predators and artificial water containers where the voracious
of mosquito larvae (Kühlhorn 1961; Jenkins 1964). and cannibalistic larvae feed upon other mosquito
Gyrinidae: Because of their mode of living on the larvae. They are, therefore, suitable for the control of
water surface, gyrinids are voracious predators mainly container-breeding mosquitoes. Toxorhynchites sp.
of Anopheles larvae (Laird 1947; James 1966). were reared and released to control Ae. aegypti and
Spercheidae: Although the adults of this family are Ae. albopictus, which breed predominantly in artifi-
not particularly carnivorous, the larvae are considered cial containers (Riviere et al. 1987b; Miyagi et al.
to be voracious predators with a feeding rate of up to 1992; Tikasingh 1992). The inundating release or
13 first and second-instar larvae of Ae. vexans/day inoculation of Toxorhynchites spp. females, combined
(Kögel 1984). with the application of adulticides, can lead to a sig-
Hydrophilidae: Adult hydrophilids are known to be nificant reduction of vector mosquitoes (Focks et al.
herbivorous. However, the larvae of some species feed 1986). The advantage of this process is that
on mosquito larvae and are, therefore, relatively impor- Toxorhynchites spp. females, when searching for
tant predators of mosquitoes (Nielsen and Nielsen breeding sites, can naturally disperse into habitats
1953; Hintz 1951). Remarkably, the larvae of that are difficult for humans to find and treat.
Helochares obscurus can capture up to 14 larvae/day Unfortunately, the level of control is usually not sat-
(Kögel 1984). Of all the beetle larvae tested in the lab- isfactory because of the insufficient number of breed-
oratory, those of Hydrophilus caraboides proved to be ing sites often used by Toxorhynchites spp. for
the most voracious. In laboratory experiments, they oviposition, the production of a low number of eggs
consumed a maximum of 67 larvae, with an average of and the lack of synchrony between predator–prey life
30 fourth-instar Ae. vexans larvae/day. The larvae are cycles. Other species of mosquitoes, which feed on
frequently observed on the water surface seizing prey larvae of Culicidae, occur mainly in the tropics and
with their well-developed mandibles. belong to the genera Anopheles, Armigeres, Culex,
Eretmapodites and Psorophora.
In Europe, where Toxorhynchites species do not
occur, other dipterans closely related to Culicidae,
Trichoptera
such as the Chaoboridae, are important predators of
The importance of caddisfly larvae as predators of mosquitoes. The larvae of Chaoboridae can remain
mosquitoes has been pointed out in many publica- motionless horizontally in the water body, where they
tions (Martini 1920b; Baldwin et al. 1955; James seize their prey with antennae modified for capturing.
1961, 1966; Service 1973a). They are the most impor- In the breeding sites of snow-melt mosquitoes, the
tant predators of snow-melt mosquitoes in semi-per- larvae of Mochlonyx culiciformis can contribute
manent water bodies in swampy woodlands. The ­substantially to the reduction of mosquito larvae.
2–3 cm long larvae of Phryganea sp. and Limnephilus Mochlonyx culiciformis have adapted their develop-
sp. have often been observed capturing larvae of ment to that of its’ prey, therefore, its’ larvae can fre-
snow-melt mosquitoes. quently suppress mosquito populations significantly,
particularly if the larval development of the predator
precedes that of the mosquito. In laboratory experi-
ments, a fourth-instar larva of M. culiciformis cap-
Diptera
tured, on average, eight early instars of mosquitoes or
Among the Diptera, carnivorous larvae of Culicidae one fourth instar larva/day (Becker and Ludwig
and Chaoboridae are common predators of mosquito 1983). Taking into consideration the long period of
16.3 Parasites 415

development of about 2 months and the frequent Females lay their eggs in the substrate of mosquito
abundance of M. culiciformis larvae in snow-melt breeding sites, where they can survive periods of
waters, its importance as a of snow-melt mosquitoes drought. When flooded and when environmental
is evident (Chodourowski 1968). In semi-permanent ­conditions are suitable, the young nematode larvae
and permanent waters, the larvae of Chaoborus spp. (10–20 mm) hatch from their eggs and penetrate as
are efficient predators and appear mostly in late sum- pre-parasites through the cuticle of the target larvae,
mer with dense populations. With an average feeding by piercing the integument of the host and entering
rate of 4 early instar mosquito larvae/day, they are not through the narrow opening. The larvae grow into
quite so voracious as M. culiciformis (Skierska post-parasites inside the host larva in a little over a
1969). week, or up to several weeks in cold climates. The
Dipterans which can be predacious on adult post-parasite (1–3 cm long) leaves the host by boring
mosquitoes are the Dolichopodidae, Empididae, through the larval cuticle, which leads to the death of
Ceratopogonidae, and Muscidae (genus Lispe) the host larva (Fig. 16.5). The post-parasites grow to
(Lamborn 1920; Peterson 1960; Laing and Welch sexual maturity in the substrate of the water body,
1963; Service 1965; Clark and Fukuda 1967). forming females and males. After copulation, the
females lay eggs in the soil of streams or ponds where
they remain until the mermithid larvae hatch under
favourable conditions, migrate to the surface and
search for a suitable host. In a few cases, infected host
16.3 Parasites larvae are able to pupate and emerge (Blackmore
1994). In this way infected adults spread the parasites
Parasites, in this context, are understood as multicel- from pool to pool or even reinfect upstream habitats
lular invertebrates which complete at least one phase
of their development within a single host. The most
important parasites of mosquitoes are mermithid
nematodes.

16.3.1 Nematodes

Two families of nematodes are of importance as insect

parasites, the Steinernematidae and the Mermithidae
(Petersen 1985; Weiser 1991).
The Steinernematidae are effective parasites of
­terrestrial insects, particularly of larvae that develop in
the soil. The use of nematodes such as Steinernema
spp. or Heterorhabditis spp. for the control of Diptera,
including Musca domestica, is still rather ­controversial.
As for mosquito larvae, it was found that they can only
be successfully infected in the laboratory. (Gaugler
and Kaya 1990).
Aquatic mermithid parasites are more important for
the biological-control of mosquitoes. Several species
of mermithid nematodes have been tested as biological-
control agents, in various parts of the world (Petersen Fig. 16.5 Post-parasite of Romanomermis culicivorax inside an
1985; Rojas et al. 1987; Vladimirova et al. 1990; Aedes larva and boring through the cuticle of the larva (Picture
Platzer 2007). courtesy of B. Spreier, Germany)
416 16 Biological Control

when they die on the edge of aquatic habitats and (2) Entomophthorales, and (3) Deuteromycetes. The
release the parasite. Mastigomycotina are mainly aquatic organisms. They
Several species of Romanomermis (R. culicivo­ develop motile zoospores, which are able to propel
rax, R. iyengari, R. nielseni) are of great interest for themselves through the water by means of their fla-
the control of mosquitoes because their life cycle is gella. Once they have located a suitable host, they pen-
completed within only a few weeks, and they can be etrate and develop a mycelium. Fungal pathogens of
mass-reared. Appropriate methods for the mass- Diptera are known in the groups Blastocladiales,
rearing of R. culicivorax have been developed Chytridiales, and Lagenidiales.
(Petersen 1980). A moist substrate of sand contain- About 30 species of Coelomomyces belong to the
ing eggs for the inoculation of mosquito breeding Blastocladiales, and infections with Coelomomyces
sites became available commercially during the spp. are known from more than 50 mosquito spe-
1970s. Unfortunately, these parasites could not be cies. At first, it proved difficult to infect mosquito
widely used because of difficulties with transporta- larvae in the laboratory. Successful infections were
tion and with maintenance of the eggs, as well as possible on a regular basis, when Whisler et al.
with sensitivity of the nematodes towards particular (1974) showed that there is an alternation of hosts in
environmental conditions, such as low water tem- which copepods as well as mosquito larvae are
perature or high salinity. involved (Fig. 16.6). Upon infection, a mycelium
forms inside the mosquito larva. Yellowish to brown-
ish coloured sporangia form at the tips of the hyphae,
and the haploid zoospores are developed in these by
16.4 Pathogens meiosis (Figs. 16.7–16.9).
Once the zoospores are released, they infect cope­
pods, such as Acanthocyclops vernalis, in which a het-
Macroorganisms such as fish have been used for
erothallus is formed which produces isogametes.
decades as biological control tools in many mosquito
A biflagellated zygote is formed through fusion of the
control programmes. However, fish and other ­predators
isogametes. This is the only infectious stage for mos-
as well as mermithid nematodes have specific ecologi-
cal requirements and can only be used where their pre-
ferred living conditions are met. The life cycle of the
predator is frequently not adapted to that of the target
organism so that it is unable on its own to bring about
an effective reduction of the target population. Mass
rearing and release of the predators or parasites is often
expensive or even impossible. This limits their large-
scale use in a number of specific habitats. Special
attention has, therefore, been given to the search for
microbial-control agents.
Over the past few decades, efforts on an international
scale have led to the discovery of a great variety of
pathogens, including entomopathogenic fungi, proto-
zoa, bacteria, and viruses (Chapman et al. 1972; Weiser
1991; Davidson and Becker 1996; Becnel 2006).

Fig. 16.6 Life cycle of Coelomomyces psorophorae. (a) Zygote

infective for mosquito larvae; (b) development of hyphal bodies
16.4.1 Fungi (mycelium) and sporangia at the tip of hyphae; (c) release of
zoospores; (d) +I– zoospores infect copepode; (e) each zoospore
develops to a thallus and gametangia which release isogametes;
The fungi that most commonly attack Diptera, belong +I– isogametes fuse to the mosquito infecting zygote (Whisler
to the following three groups: (1) Mastigomycotina, et al., 1974)
16.4 Pathogens 417

Lagenidium giganteum (Lagenidiales), which goes

through an asexual and a sexual developmental stage,
has shown the most promising results (Lacey and
Undeen 1986; Kerwin and Washino 1988; Kerwin
1992). When introduced into a mosquito breeding
site, the motile biflagellated zoospores attach them-
selves to the larval cuticle. Upon penetration, a fun-
gal mycelium forms inside the larval haemocoel
which results in the death of the larva within 2–3
days. In the cadaver, sporangia are developed in
which asexually produced zoospores are formed. The
zoospores are released through vesicles on the sur-
face of the larval cadaver. Several further asexual
Fig. 16.7 Larva of Ae. vexans infected with Coelomomyces cycles take place or the fungus undergoes a sexual
psorophorae
cycle which terminates with the formation of oospores
which are also infectious for mosquito larvae and are
characterized by their great persistence at the breed-
ing site (Fig. 16.10).
After successfully rearing L. giganteum in an
­artificial medium, the fungus was released in large-
scale field trials (Kerwin and Washino 1988). High
levels of infection were achieved when masses of zoo-
Fig. 16.8 Formation of a sporangium of Coelomomyces
spores were applied. Unfortunately, zoospores are
psorophorae at the tip of a hypha in an anal papilla of an shortlived and disappear from the habitat in the
Ae. vexans larva absence of mosquito hosts. Storage of the zoospores is

Fig. 16.9 Sporangium of Coelomomyces psorophorae (SEM,

magnification 850×)

quito larvae. It penetrates through the cuticle into the

larval haemocoel. The initial hopes that a satisfactory
Fig. 16.10 Life cycle of Lagenidium giganteum (after
parasite for mosquito control had been discovered, Woodring and Davidson). (a) biflagellated zoospores (magni-
soon proved unrealistic due to this complex life cycle fied compared to larva) encyst on the cuticle of the mosquito
and associated difficulties in the mass production of larva; (b) after penetration mycelium develops in the larva and
kills it within two to three days. In the cadaver sporangia with
the fungi. The same is true for Coelomycidium sp.
exit tubes for the release of asexual zoospores or sexual
(Chytridiales). oospores by fusion of hyphal segments are developed
418 16 Biological Control

also difficult. On the other hand, the oospores can per- Other fungi, such as Tolypocladium sp. and
sist in the environment, but unfortunately, they only Culicinomyces sp., are infectious to mosquito larvae
­germinate ­asynchronously, and consequently high- and can be produced in artificial media. When the
density mosquito populations are only rarely elimi- spores of Culicinomyces clavisporus are ingested by
nated by a knock-down effect. A combination of mosquito larvae, they penetrate the gut wall and proli­
different agents which deliver a knock-down and a ferate in the larval body. After the death of the larva,
long-term effect, such as B.t.i. preparations, together the fungus sporulates on the surface of the cadaver.
with oospores of L. giganteum, could improve the However, effective use of this fungus in mosquito con-
efficacy of the latter. trol is unlikely because of its lack of persistence and
The Entomophthorales form various conidia which adequate recycling ability, difficulties in storage, and
mainly infect terrestrial insects or their immature the high dosages required.
stages. Entomophthora culicis can infect mosquitoes
as they emerge from their pupae (Weiser 1991).
Deuteromycete fungi, such as Beauveria sp.,
Metarhizium sp., Paecilomyces sp. or Verticillium sp., 16.4.2 Protozoa
are not host-specific and are not primary pathogens of
Diptera. However, their conidia can infect adult mos-
The protozoa contain the largest number of mosquito
quitoes, for example, in their shelters during hiberna-
parasites. The best studied are the microsporidian
tion or resting. In recent years, Beauveria bassiana
intracellular parasites. Larvae infected with microspo-
and Metarhizium anisopliae have been tested as bio-
ridia can easily be recognised even in the field by their
logical-control agents against adult malaria mosqui-
milky-white colour. However, despite the great scien-
toes such as An. gambiae s.l. and An. stephensi with
tific interest of this group of parasites, no one has yet
very encouraging results (Scholte et al. 2003, 2004,
succeeded in using them as microbial-control agents.
2005). In laboratory studies, the infection of An. ste­
This is mainly due to their complex life cycle, which
phensi with Beauveria brassiana reduced malaria
makes mass production difficult, and their frequently
transmission by 98% (Blanford et al. 2005). Similar
low pathogenicity and persistence.
results have been achieved with An. gambiae s.l.
A common feature of all microsporidia is the devel-
(Achonduh and Tondje 2008). The infected mosqui-
opment of spores which contain a polar filament inter-
toes died before they became infectious to humans,
nally (Fig. 16.11). This is ejected in the host’s gut, and
and transmission of Plasmodium sp. was also reduced
by interrupting mosquito feeding. In a field study,
black cotton sheets impregnated with conidia of M.
anisopliae were hung from the ceilings in five tradi-
tional houses in a rural Tanzanian village. Mosquitoes
were then collected from these houses for 3 weeks
and checked for longevity and fungal infection. About
23% female An. gambiae became infected, resulting
in a shortening of the life span by 4–6 days compared
to mosquitoes collected in five untreated houses.
Calculations showed that the use of fungal-impreg-
nated sheets could significantly reduce the number of
infective bites in malarial areas from once/night to
once every 3 weeks or even less. Apart from its
­pathogenicity to e.g. An. gambiae and Cx. quinque­
fasciatus, M. anisopliae exhibits characteristics such
as ease and cheap mass-production, considerable
shelf-life, safety for vertebrates, and world-wide dis-
tribution to make it an attractive agent for bio-control Fig. 16.11 Ultrastructure of a spore of Amblyospora sp. (F =
of adult mosquitoes in sub-Saharan Africa. polar filament, Pk = polar body, Pp = polaroplast, n = nucleus)
16.4 Pathogens 419

16.4.3 Bacteria

Mosquitocidal bacteria have been known since the

early 1960s when the first strains of Bacillus sphaeri­
cus with larvicidal activity were discovered (Kellen
and Meyers 1964). However, these strains were not
sufficiently toxic to merit commercial development.
The discovery of the gram-positive, endospore-form-
ing soil bacterium B.t. ssp. israelensis (B.t.i.) in the
Negev desert of Israel in 1976 (Goldberg and Margalit
1977) and of the potent strains of B.s. in recent years,
have inaugurated a new chapter in the control of mos-
quitoes and blackflies (Singer 1973; Weiser 1984;
Becker and Margalit 1993). The newly-discovered
subspecies of B.t. is target-specific and highly toxic to
Fig. 16.12 Life cycle of Amblyospora spp. (after Woodring
larvae of most mosquito species and blackfly larvae.
and Davidson)
New strains of B.s., such as strain 2362, isolated from
an adult blackfly in Nigeria (Weiser 1984), and strain
2297, isolated in Sri Lanka (Wickramasinghe and
in this way, the infectious nucleus is able to penetrate
Mendis 1980), are much more potent than the first iso-
into the host. Two groups of microsporidia are known
lates and are particularly active against larvae of Culex
as mosquito pathogens. The first group, which includes
species and An. gambiae (Ragoonanansingh et al.
the genera Nosema and Vavraia, develops asexually
1992; Fillinger et al. 2003; Majambere et al. 2007).
and forms only one type of spore. Under laboratory
New strains are still being isolated, which are at least
conditions, infection of mosquito larvae can be
as active as the current commercial strain 2362 (Park
achieved relatively simply, by feeding them with
et al. 2007).
spores. The second group, which includes the genera
The actinomycete, Saccharopolyspora spinosa,
Amblyospora and Parathelohania, has a complex
was collected from the soil in a rum distillery on a
developmental cycle (Fig. 16.12).
Caribbean Island in 1982. During fermentation, the
An infected mosquito female transmits the spores
active compound, spinosad, which contains a tetracy-
in a vertical direction, transovarially, to the next gen-
clic ring system to which two different sugars are
eration. In the mosquito larva, the spores can divide
attached, is produced by the bacteria (Thompson et al.
meiotically, develop countless haploid spores in the
1997; Sparks et al. 1998). Spinosad-based products
larval fat body and are released when the larva dies
have an excellent environmental and mammalian toxi-
(Fig. 16.12).
cological profile and are effective as bio-control
If spores are ingested by a copepod, they repro-
agents against a broad range of agriculturally impor-
duce asexually once again (Andreadis 1985; Sweeney
tant insect pests as well as against mosquitoes and
et al. 1985). If, on the death of the copepod, the hap-
tsetse flies (de Deken et al. 2004; Romi et al. 2006).
loid spores are released and ingested by a mosquito
larva, the sexual phase begins with fusion of the
cells, which again form diploid spores. Female mos-
quito larvae which are only lightly infected, can 16.4.3.1 Bacillus thuringiensis israelensis (B.t.i.)
again transmit the diploid spores transovarially to
the larvae of the next generation. This complex This Bacillus produces protein toxins during sporula-
developmental cycle prevents any mass-rearing of tion that are concentrated in a parasporal body (PSB),
the parasites and makes it unlikely at present for called the protein crystal (Fig. 16.13).
these micosporidia to be used in mosquito control These proteins are highly toxic to mosquito and
(Sweeney and Becnel 1991; Micieli et al. 2000; blackfly larvae. The selectivity of the Bacillus toxins
Becnel and Johnson 2000). derives from a variety of factors.
420 16 Biological Control

(Charles et al. 2000; Lüthy and Wolfersberger 2000;

Boisvert 2005).
The insecticidal effect of B.t.i. emanates from the
parasporal body, which contains four major toxin pro-
teins of different molecular weight, referred to as the
Cry4A (125 kDa), Cry4B (135 kDa), Cry10A (58 kDa)
and Cry1lA (68 kDa) (Delecluse et al. 1996). These
toxins bind to specific glycoprotein receptors on the
Fig. 16.13 B. thuringiensis israelensis with spore (left) and
parasporal body, so-called protein crystal (right). (Micrographs
larval midgut brush border (Charles and Nielsen-
courtesy of J.-F. Charles, Pasteur Institute, Paris) LeRoux 1996a,b).
A fifth toxin, called the CytA protein (27 kDa),
binds to lipids and does not exhibit the specific bind-
ing mechanism which the Cry proteins do (Höfte and
(1) The target-organism must ingest the protein crys-
Whiteley 1989; Federici et al. 1990; Priest 1992).
tal (inactive protoxin), and this depends on its
The protoxin structure contains three domains
feeding habits.
(Fig. 16.15). Domain I consists of a bundle of seven
(2) The protoxin has to be solubilized in the alkaline
alpha-helices, which can insert into the gut cell mem-
midgut milieu of the target insect (pH >10).
brane, creating a pore through which ions can pass
(3) The target-organism must possess suitable pro-
freely. Domain II contains three antiparallel beta-
teases to convert the protoxin into biologically
sheets, which are thought to bind to receptors in the
active toxins.
midgut. Domain III is a beta-sandwich, which obvi-
(4) The target-organism must possess surface receptors
ously prevents further cleavage of the active toxin by
(glycoproteins) on the midgut epithelial cells to
gut proteases (Li et al. 1991).
which the toxins can bind.
Neither the spore nor the living bacilli appear to be
This process disturbs the osmo-regulatory mechanisms involved in the insecticidal process. The more or less
of the cell membrane, thereby, swelling and bursting spherical PSB is formed at the end of sporulation and
the midgut cells (Fig. 16.14). Non-target organisms do consists of three types of protein inclusions separated
not activate the protoxin into the toxin because of their by thin layers. The largest inclusion is round, of slight
acidic gut milieu, or remain undamaged because of the electron density and occupies approximately 50% of
lack of specific receptors on their intestinal cells the total volume of the PSB. The second type of inclu-

Fig. 16.14 (a) midgut epithelium of a healthy Ae. aegypti larva; (b) 30 min after ingestion of the B. thuringiensis israelensis
protein crystals, swelling of midgut cells and reduction of microvilli; (c) 1 h after ingestion cell is about to lyse (micrographs
courtesy of J.-F. Charles, Pasteur Institute, Paris)
16.4 Pathogens 421

characterization of the different toxin genes have been

accomplished (Bourgouin et al. 1986; Thorne et al.
1986; Ward and Ellar 1988). These results open the
possibility of cloning the various toxin genes into host
organisms to increase the persistence or mosquitocidal
properties.

16.4.3.2 Bacillus sphaericus (B.s.)

In addition to B.t.i., a second spore-forming bacte-

rium, B.s., has become increasingly important in
recent years. The high potential of B.s. as a bacterial-
control agent lies in its spectrum of efficacy and its
ability to recycle or to persist in nature under certain
conditions, which means that long-term control can
Fig. 16.15 The B.t.i. toxin (Cry4B) structure (Graph courtesy be achieved (Hertlein et al. 1979; Mulligan et al.
of Chanan Angsuthanasombat, Mahidol University, Bangkok, 1980; Lacey 1990; Ludwig et al. 1994; Silva-Filha
Thailand)
et al. 2001). The time-span between retreatments can
thus be extended and personnel costs reduced. This
opens up the possibility of a successful and cost-
sion (about 20% of the volume of the PSB) is moder- effective control of Culex species, particularly of Cx.
ately electron-dense and rod-shaped, and the third type pipiens as vector of West Nile virus and Cx. p. quin­
of inclusion (about 25% of the PSB) is spherical and quefasciatus, which is the most important vector of
highly electron-dense (Ibarra and Federici 1986; lymphatic filariasis, usually breeding in highly pol-
Federici et al. 1990). luted water bodies in urban areas.
The mosquitocidal properties of each single solu- B. sphaericus can easily be identified by its round
bilized and purified protein have been evaluated in spore located terminally in a swollen sporangium
many studies (Beltrao and Silva-Filha 2007; Alam (Fig. 16.16). Most recent knowledge indicates that
et al. 2008). All tests have shown that each type of B.s. toxins kill only mosquito larvae and, when higher
protein is mosquitocidal, but none is nearly as toxic dosages are applied, larvae of Psychodidae also.
as the intact PSB. This high toxicity of the PSB is Certain mosquito species, such as Cx. p. quinquefas­
caused by a synergistic interaction of the 25 kDa pro- ciatus and An. gambiae, are highly susceptible,
tein (split from the 27 kDa protein) with one or more whereas, Ae. aegypti larvae are more than 100-fold
of the higher molecular weight proteins (Ibarra and less susceptible. Blackfly larvae, other insects, mam-
Federici 1986; Chilcott and Ellar 1988; Chang et al. mals, and other non-target organisms are not suscep-
1993). It is assumed that CytA may function as a tible to B.s. toxins. A particularly attractive feature
Cry11A receptor in the mosquito midgut (Perez
et al. 2005). It is thought that the synergism in the
mode of action among the proteins reduces the prob-
ability of resistance.
The high toxicity of the PSB to a great variety of
mosquito and blackfly species is the most remarkable
property of B.t.i. Only at significantly higher dosages
are some other Nematocera species affected, but no
other organisms are harmed.
Fig. 16.16 B. sphaericus with round spore and the parasporal
It has been shown in many studies that plasmids
protein inclusion (dark structure on the right site of the spore)
with a molecular weight of 60–94 MDa play an essen- which is located in a coated “spore crystal complex” (micro-
tial role in the crystal toxin production. Cloning and graph courtesy of J.-E Charles, Pasteur Institute, Paris)
422 16 Biological Control

of B.s. is its potential to persist and recycle under 16.4.3.3 Environmental Safety
certain field conditions. Appropriate formulations
have shown a significant residual activity against lar- The exceptional environmental safety of bacterial-con-
vae of Culex p. pipiens and Cx. p. quinquefasciatus trol agents has been confirmed in numerous laboratory
in highly polluted breeding habitats (Hertlein et al. and field tests. The U.S. Environmental Protection
1979; Nicolas et al. 1987; Davidson and Yousten Agency (USEPA) categorizes the risk posed by B.t.
1990; des Rochers and Garcia 1984; Lacey 1990; strains to non-target organisms as minimal to nonexistent
Becker et al. 1995). and approved the use of B.t.i. formulations as early as
The mosquitocidal efficacy of B.s. is based on two 1981. In safety tests on representative aquatic organisms,
different types of toxins: (a) parasporal protein inclu- it was shown that, in addition to plants and mammals,
sions called binary toxin (Bin) and (b) mosquitocidal none of the taxa tested, such as Cnidaria, Turbellaria,
toxins (Mtx1: 100 kDa; Mtx2: 31 kDa; Mtx3: 36 kDa). Rotatoria, Mollusca, Annelida, Acari, Crustacea,
The parasporal protein inclusions are located in a Ephemeroptera, Odonata, Heteroptera, Coleoptera,
coated “spore crystal complex” and consist of proteins Trichoptera, Pisces, and Amphibia, appeared to be
of two different molecular weights, a 42-kDa toxin affected when exposed in water containing large amounts
(BinA) and a 51-kDa binding domain (BinB). Both are of bacterial preparations (Table 16.1; Becker and Margalit
required for a high level of mosquitocidal activity and 1993; Boisvert and Boisvert 2000).
are crystallized during sporulation (Broadwell et al. Even within the Diptera, the toxicity of B.t.i. prepara-
1990; Baumann et al. 1991; Berry et al. 1991; Priest tions are restricted to mosquitoes and a few nematocer-
1992; Davidson and Becker 1996). The Mtx toxins do ous families (Colbo and Undeen 1980; Miura et al.
not form crystals and degrade quickly upon synthesis 1980; Ali 1981; Garcia et al. 1981; Molloy and Jamnback
during the vegetative stage (Park et al. 2007). The 1981; Margalit and Dean 1985; Mulla et al. 1982; WHO/
mode of action and receptor-binding is similar to that IPCS 1999). In addition to mosquito and blackfly larvae,
in B.t.i. (Davidson 1988; Davidson and Youston 1990; only those of the closely related Dixidae are sensitive to
Charles et al. 1996b, 2000). B.t.i. Larvae of Psychodidae, Chironomidae, Sciaridae,
These two microbial-control agents were rapidly and Tipulidae are generally far less sensitive than those
developed with the support of industry, universities, of mosquitoes or blackflies (Table 16.2).
and national and international organizations, such as In contrast to B.t.i., the toxins of B.s. are toxic to a
the World Health Organization (WHO). The WHO much more restricted range of target insects. Blackfly
Pesticide Evaluation Scheme (WHOPES), which larvae as well as other insects (except for Psychodidae),
­promotes and coordinates the testing and evaluation mammals, and other non-target organisms are not sus-
of pesticides for public health, have evaluated ceptible to B.s.
­microbial-control agents as safe and efficient control Toxicological tests were carried out using various
agents for public health programmes (WHO/CDS/ mammals. B.t.i. preparations, when given orally, sub-
WHOPES/2004.8). Following extensive safety tests and percutaneously, intraperitoneally, ocularly, through
and environmental impact studies, the bacilli were inhalation and scarification, appeared to be innocuous
quickly put into use. This rapid exploitation was even at high dosages of l08 bacteria/animal (WHO
aided by a series of useful properties of the bacterial- 1982a,b, 2000).
control agents. In addition to the relative ease with Another important aspect is the widespread ­occurrence
which they can be mass-produced, bacterial-control of both bacilli in the soil. They are natural components of
agents are highly efficient, environmentally safe, easy the soil micro-ecosystem and not an artificial, man-made
to handle, stable when stored, cost-effective, and suit- product, where toxic residues may remain after applica-
able for integrated mosquito management (IMM) tion against nuisance/vector species.
programmes based on community participation.
Furthermore, the costs for development and registra- 16.4.3.4 Ease of Handling
tion of these agents are many times lower than those
of a conventional chemical insecticide. The risk of No special equipment is required for the application of
resistance, especially when B.t.i. products are used, is bacterial-control agents. Generally, simple knapsack
much lower compared to conventional insecticides. sprayers are adequate for accessible breeding sites.
16.4 Pathogens 423

Table 16.1 Organisms not affected by B. thuringiensis israelensis

Taxa Dosage (ppm) Species
Cnidaria 100 Hydra sp.
Turbellaria 180 Dugesia tigrina, Bothromesostoma personatum
Rotatoria 100 Brachionus calciflorus
Mollusca 180 Physa acuta, Aplexa hypnorum, Galba palustris,Anisus leucostomus, Bathyomphalus
contortus, Hippeutis complanatus, Pisidiuim sp.
Annelida 180 Tubifex sp., Helobdella stagnalis
Acari 180 Hydrachnella sp.
Crustacea 180 Chirocephalus grubei, Daphnia pulex, Daphnia magna, Ostracoda, Cyclops strenuus,
Gammarus pulex, Asellus aquaticus, Orconectes limosus
Ephemeroptera 180 Cloëon dipterum
Odonata 180 Ischnura elegans, Sympetrum striolatum, Orthetrum brunneum
Heteroptera 180 Micronecta meridionalis, Sigara striata, Sigara lateralis, Plea leachi, Notonecta
glauca, Ilyocoris cimicoides, Anisops varia
Coleoptera 180 Hvphydrus ovarus, Guignotus pusillus, Coelambus impressopunctatus, Hygrotus
inaequalis, Hydroporus palustris, Ilybius fuliginosus, Rhantus pulverosus,
Rhantus consputus, Hydrobius fuscipes. Anacaena globulus, Hydrophilus
caraboides, Berosus signaticollis
Trichoptera 180 Limnophilus sp.
Pisces 180 Esox lucius, Cyprinus carpio, Perca fluviatilis
Amphibia (larvae) 180 Triturus alpestris, Triturus vulgaris, Triturus cristatus, Bombina variegata, Bufo
bufo, Bufo viridis, Bufo calamita, Rana esculenta, Rana temporaria

Standard ULV, airblast or mist blower equipment may application of granules. Safety precautions are mini-
also be used. In dense vegetation or wide-spread breed- mal (compared to the use of toxic agents). Because of
ing sites, aerial applications are preferable. Rotary the rapid knock-down effect and the high level of effi-
seeders or pressurized air sprayers are suitable for the ciency, the success of the treatment can generally be
monitored within a day or two after application.
Table 16.2 Susceptibility of larvae of nematoceran and
brachyceran flies to B. thuringiensis israelensis (tested Product:
VectoBac TP, Potency: 5000 ITU/mg) 16.4.3.5 Cost-Effectiveness
Family Dosage (ppm) Mortality (%)
Simuliidae Compared to conventional insecticides, the applica-
Simulium damnosum s.1. 0.4 100 tion of bacterial-control agents is cost-effective when
Culicidae integrated control strategies are designed. For instance,
Aedes/Ochlerotatus spp. 0.2 100
the German Mosquito Control Association
Dixidae
Dixa spp. 2 100
(Kommunale Aktionsgemeinschaft zur Bekämpfung
Chaoboridae der Stechmückenplage-KABS), mosquito abatement
Chaoborus spp. 180 No effect project in Germany effectively suppresses mosquitoes
Psychodidae emerging from a floodplain area of >600 km2 involving
Psychoda alternata 1 100 an average 100 km2 of actual breeding grounds/year.
Sciaridae The total annual budget of the KABS is €3 million.
Bradysia sp. 3 90 More than 3 million residents of the area are effectively
Chironomidae
protected from a serious nuisance (campaign costs/per-
Chironomus sp. 1.8 90
Xenopelopia sp. 4 50 son/year: € 0.92). In a cost-benefit analysis, the benefit
Tipulidae for the welfare of the society in this region 3.8 times
Tipula spp. 30 50 higher than the costs for the campaign (Hirsch and
Ceratopogonidae 180 No effect Becker, 2009). Environmental considerations which
Syrphidae cannot be expressed in monetary terms, should also be
Tubifera sp. 180 No effect included in these economic calculations.
424 16 Biological Control

16.4.3.6 L
 ack of Potential for Resistance the population is exposed to the toxin. Floodwater
Development mosquitoes and most blackflies migrate considerably.
This behaviour produces a substantial gene flow within
The development of resistance to chemical insecticides their populations which should at least slow the onset
represents a serious problem. Bacterial-control agents, of resistance.
however, appear less likely to provoke resistance However, resistance to B.s. toxins has been dem-
because their mode of action is more complex (Davidson onstrated in both the laboratory and the field (Yuan
1990; Wirth et al. 2005). However, in comparison, et al. 2000). In southern France, a population of Cx.
resistance in the stored grain pest, Plodia interpunc­ pipiens developed a level of resistance of more than
tella, to the Lepidoptera specific B. thuringiensis 16,000-fold after 18 applications of B.s. treatments
kurstaki (B.t.k.) has been demonstrated in the labora- (Sinegre et al. 1994). Nielsen-LeRoux et al. (1995)
tory (McGaughey 1985). Studies have shown that the demonstrated in a laboratory population of Cx. pipi­
commercial use of B.t. preparations in agriculture can ens, that resistance at a level of 100,000-fold to B.s.
lead to resistance within a few years. For example, the binary toxin can be caused due to a change in the
diamondback moth, Plutella xylostella, which was receptor on midgut brush-border membranes. In
repeatedly treated with B.t.k. preparations on farms in other cases, binding to the receptor took place, but
Hawaii, was found to be 41 times more resistant than there was no toxicity. In all cases, resistance was
populations that were only minimally exposed to B.t.k. shown to be recessive (Charles and Nielsen-LeRoux
(Tabashnik et al. 1990). Similar resistance phenomena 1996b). It seems that the risk of resistance to bacte-
have not yet been observed with B.t.i. formulations. rial toxins is inversely proportional to the complex-
Resistance studies have been conducted by the ity of the mode of action, which is definitely less
KABS with populations of Ae. vexans which were con- complex with B.s. than with B.t.i. toxins.
stantly exposed to B.t.i. products over a period of more
than 25 years and were, therefore, subjected to constant
and intense selection pressure. These mosquitoes were
compared with Ae. vexans populations taken from a 16.4.3.7 Formulations
remote location which had never been exposed to B.t.i.
products and had never been under selection pressure. A basic requirement for the successful use of bacterial-
No reduction in the sensitivity of these mosquitoes to control agents is the development of effective formu-
B.t.i. products could be detected (Becker and Ludwig lations suited to the biology and habitats of the
1993; Ludwig and Becker 2005). Similar results were target-organisms. Formulations are available as water
obtained by Kurtak et al. (1989) and by Hougard and dispersable granules (e.g. Vectobac WDG and Vectolex
Back (1992). They found that after 10 years of intensive WDG), wettable powder (WP), fluid concentrates (e.g.
applications of B.t.i. in West Africa, the susceptibility of Vectobac 12AS and Aquabac), corn-cob (Vectobac G
the blackfly, Simulium damnosum, had not changed. and Vectolex G), pellets, tablets (e.g. Vectobac DT/
The complex mode of action of B.t.i. toxins partly Culinex tablets), briquettes, and ice granules contain-
explains the relative absence of resistance. The lethal ing the bacilli toxins (Table 16.3).
changes in the midgut cells are induced only by the Biorational mixtures of toxins of both bacilli (B.t.i.
synergistic effects of the different toxin proteins pres- and B.s.), such as VectoMax,® inhibit specific advan-
ent in the parasporal body of B.t.i. This combination tages. Mixed populations of culicine and/or Anopheles
reduces the likelihood of resistance. On the other hand, populations can be successfully controlled by applying
when the gene encoding a single toxin protein was a single product. The likelihood for resistance against
cloned into a microorganism and then fed to larval B.s. can be significantly reduced or even avoided
mosquitoes, resistance was induced within a few gen- (Zahiri et al. 2002).
erations (Georghiou and Wirth 1997). Genetic engineering techniques can be used to
Resistance is less likely when there is a variable improve mosquito larvicides based on both bacteria
gene pool of target populations. The large size of many B.t.i. and B.s. as well as to reduce the risk for resistance
mosquito and blackfly populations, thus, inhibits the against B.s. toxins. The best of these recombinants con-
development of resistance because only a portion of tain all major B.t.i. endotoxins, specifically, Cry4A,
16.4 Pathogens 425

Table 16.3 Some commercially available Bacillus thuringiensis water with spores, can be successfully used for control
israelensis and Bacillus sphaericus products used in mosquito of container-breeding mosquitoes such as Cx. p. pipi­
and blackfly control programmes
ens or Ae. aegypti or even against An. gambiae (Becker
Potency
Product Formulation (ITU/mg) et al. 1991; Kroeger et al. 1995; Mahilum et al. 2005).
B. thuringiensis israelensis (against mosquito and blackfly In addition to commercially available granules
larvae) based on ground corn-cobs, sand granules can also
Aquabac®1 Primary powder 7,000 serve as a carrier for wettable powder formulations:
Icepearls3 Ice granules 120 50 kg fire-dried quartz sand (grain size 1–2 mm) with
Teknar HP-D®2 Fluid concentrate 1,200 0.8–1.4 l of vegetable oil (as a binding material) and
Teknar TC®2 Technical powder 10,000
1.8 kg of B.t.i. powder (activity >5.000 ITU/mg) should
Teknar G®2 Granules 200
VectoBac I2AS®2 Fluid concentrate 1,200 be mixed in a cement mixer. This mixture is sufficient
VectoBac TP®2 Technical powder 5,000 to treat 2–3 ha. Recently, more cost-effective granules
VectoBac WG®2 Water dispersible 3,000 were developed in the form of ice pellets (Becker
granules 2003). Ice granules can be easily produced when water
VectoBac DT®2,4 Tablets 2,200 ­suspensions containing the bacterial toxins are frozen
Culinex Tab plus®2,4 Tablets 2,200
into small ice cubes or “pearls” (3–5 mm) and kept in
Lossquito®5 Fluid concentrate 1,200
cold storage rooms until used. The advantages of using
Bacillus sphaericus (against mosquito larvae) ice granules are:
Spherimos®2 Fluid concentrate 120
VectoLex WDG2 Water dispersible 650 BsITLJ/mg (1) The toxins are bound in the ice pellet, so loss of active
granules material by friction during application is avoided.
VectoLex®2 Granules 50 BsITLJ/mg
(2) As the specific weight of ice is less than that of
Combined B.t.i./B. sphaericus product
VectoMax G2 Granules 50 BsITU/mg
water, the ice pellets remain in the upper water
VectoMax WSP2 Water soluble pouches50 BsITU/mg layer where they release the toxins into the feeding-
1
Becker Microbial Products, USA zone of mosquito larvae as they melt.
2
Valent BioSciences Corp., USA (3) The ice pellets penetrate dense vegetation and do
3
Icybac GmbH, Germany not stick to leaves even when it is raining and is
4
Culinex GmbH, Germany less sensitive to wind.
5
BioDalia, Israel
(4) There is increased swath because the friction is
reduced due to the physical properties of ice.
(5) The production is cost-effective and
Cry4B, Cry11A, and Cyt1A, plus the binary (Bin)
(6) the “carrier” is water.
endotoxin of B.s. The presence of Cyt1A in these
recombinants, which synergizes Cry toxicity and delays The amount of active material/ha can, thus, be signifi-
resistance to these proteins and the B.s. binary toxin, cantly reduced when compared with granules based on
should enable long-term use of these recombinants sand.
with little if any development of resistance (Federici When appropriately stored, most preparations based
et al. 2007). on bacterial toxins can be kept for long periods without
A few hundred grams or even less of powder, half to losing activity. Experience has shown that powder or
two litres of liquid concentrate or a few kilograms of corn-cob formulations lose no or only little of their
granules/ha, are usually enough to kill all mosquito activity even after many years in storage. On the other
larvae. In some situations, a long-term effect can be hand, the activity of fluid concentrates may be more
achieved if larger amounts are used (Becker and labile. Preparations should, therefore, be re-tested in
Margalit 1993; Becker and Rettich 1994; Russell et al. bioassays according to WHO guidelines when they
2003; Rydzanicz et al. 2009). With the production of have been stored for more than a year.
tablets, water-soluble pouches or briquette formula- Standardized methods for bioassays have been
tions, progress has been made towards achieving long- developed to determine the LC50 values using standard
term effects (Kahindi et al. 2008; Su 2008). formulations (de Barjac 1983; Dulmage et al. 1990;
Tablet formulations, based on B.t.i. or B.s. sterilized Skovmand and Becker 2000). The procedure for bio-
by g-radiation to prevent contamination of drinking assays is described in Chap. 4.
426 16 Biological Control

16.4.3.8 F
 actors Influencing the Efficacy 0.16
of Bacterial-Control Agents 0.14
0.12
In addition to the different susceptibility of various 0.10

BTI [mg / l]
mosquito species to bacterial toxins, a variety of fac- 0.08
tors can influence their efficacy (Becker et al. 1993; 0.06
Ludwig et al. 1994; Puchi 2005, Sorensen et al. 2007). 0.04
This efficacy depends upon the developmental stage of 0.02
the target-organisms, their feeding behaviour, organic 0.00
5 8 1.5 25
content of the water, the filtration effect of target-lar- Temperature [°C]
vae as well as that of other non-target organisms, pho-
tosensitivity, and other abiotic factors, such as water Fig. 16.17 Impact of the temperature on the B. thuringiensis
israelensis sensitivity of second-instar larvae of Aedes vexans
temperature and depth, the sedimentation rate, as well (values are given as LC90)
as, the shelf-life of B.t.i. and B.s. formulations (Mulla
et al. 1990; Becker et al. 1992). The long-term effect is
also strongly influenced by the recycling capacity of bioassays, the second-instar larvae of Ae. vexans are
the agent (Aly 1985; Becker et al. 1995a). more than ten times less sensitive at 5°C than at
Species and Instar Sensitivity: Larvae lose their 25°C (5°C: LC90 = 0.145 ± 0.065 mg/l; 25°C:
­sensitivity to bacterial toxins as they develop (Becker LC90 = 0.0142 ± 0.007 mg/l) (Becker et al. 1992). The
et al. 1992). For instance, the second-instar larvae of Ae. same effect was found when the fourth-instar larvae
vexans are about 11 times more sensitive than the were tested. Application of bacterial formulations
fourth-instar larvae, at a water temperature of 25°C should be conducted at a temperature threshold of 8°C
(second-instars: LC 90 = 0.014 ± 0.007 mg/l; fourth- when Aedini species are to be controlled (Fig. 16.17).
instars: LC90 = 0.149 ± 0.004 mg/l). The differences in Size of the Water Body: Because bacterial toxins
sensitivity are less at temperatures between 8 and 15°C. diffuse throughout the entire body of water, deep water
Nonetheless, the second-instars of Ae. vexans are more requires higher rates than shallow water of the same
than twice as sensitive as the fourth-instars at a water surface area. Because larvae of many mosquito species
temperature of 15°C (second-instars: LC90 = 0.062 feed near the surface, effectiveness depends on the
± 0.025 mg/l; fourth-instars: LC90 = 0.145 ± 0.004 mg/l). concentration and durability of the toxins in the upper
In field experiments, only half the dosage required to portion of the water body.
kill the third-instar larvae is needed for the second-instar Larval Density: Bioassays with Ae. vexans have
larvae. If the fourth-instar larvae are dominant, then the shown that with higher numbers of larvae, the amounts
dosage must be doubled again. It is, therefore, recom- of B.t.i. toxins must be increased (Becker et al. 1992).
mended that control measures commence while the lar- At a density of 10 fourth-instar larvae/150 ml
vae are at an early developmental stage. water, the LC50 value was 0.0162 ± 0.004 mg/l; with
Large differences in sensitivity can also be distin- 75 larvae, the LC50 was ~7 times higher
guished between various mosquito species due to differ- (LC50 = 0.1107 ± 0.02 mg/l). The presence of other
ences in their feeding habits and their ability to activate filter-feeding organisms, such as Cladocera, cause
the protoxin and the toxin to be bound to midgut cell similar effects. In tests with B.t.i. preparations, the
receptors. For instance, larvae of Cx. pipiens were found LC50 and LC90 values were 5 and 6 times higher at a
to be 2–4 times less susceptible to B.t.i. toxins than density of 90 Daphnia sp./150 ml than were those
Aedini larvae of the same instar. By contrast, larvae of without Daphnia sp.
Cx. pipiens are highly sensitive to the toxins of B.s., State of Nutrition: The state of nutrition and the amount
whereas Aedes/Ochlerotatus larvae are much less so. of available food influence the sensitivity of mosquito
Temperature: The feeding rates of mosquito lar- larvae to microbial-control agents. In laboratory studies,
vae are influenced by water temperature (Fig. 16.17). two or three times more B.t.i. toxins were required for an
For instance, the feeding rate of Ae. vexans decreases equal level of mortality in the presence of added food (or
as temperature decreases, and this is accompanied polluted water) compared with clean water (Mulla et al.
by a reduction in consumption of bacterial toxins. In 1990).
16.4 Pathogens 427

Sunlight: Although radiation, such as that from a applied. This, indirectly, produces a sustained suppres-
Cobalt60 source, is well suited for the sterilization of sive effect (Mulla 1990; Becker 1992).
B.t.i. products without significantly reducing their Bacterial-control agents can be mixed with other
­toxicity (Krieg 1986; Becker 2002), strong sunshine larvicides, such as preparations that are applied to alter
appears to reduce their larvicidal effect. For example, the surface film which enhances diffusion over the
B.s preparations were active for >3 times longer in water surface and destroys mosquito pupae that are not
shaded water than in water exposed to the sun. The affected by microbial toxins (Roberts 1989).
LC90 values obtained with B.t.i. powder (6,000 ITUs/ The WHO “primary health care concept” increas-
mg) in bioassays with third-instar Cx. p. pipiens in ingly seeks to involve local residents in the search for
sunny sites (6,000–12,000 lux for 7 h) and in shaded solutions to health care problems. Bacterial-control
sites (<150 lux) at the same time and under identical agents have a considerable safety advantage over syn-
conditions (t = 25 ± 1°C) were very different (Becker thetic insecticides because neither the operator nor the
et al. 1992). The LC90 value was 0.054 ± 0.008 ppm occupants of treated sites become exposed to potentially
under shaded conditions, whereas it was ~4 times dangerous chemicals. For this reason, such preparations
higher at sunny sites (LC90 = 0.235 ± 0.036 ppm). are particularly well suited for use by volunteers.
Recycling Processes: A particularly attractive feature Applications of bacterial toxins do not harm benefi-
of B.s. is its high efficacy against Culex and Anopheles cial organisms, such as honey bees, silkworms, or
species and its potential to persist and recycle under cer- aquatic animals such as fish, shrimps or oysters. These
tain field conditions (Des Rochers and Garcia 1984). In formulations can, therefore, be used in ecologically sen-
laboratory tests, it was shown that the presence of mos- sitive areas. Because they are biodegradable, no toxic
quito larval cadavers in the water contributes to the residues remain after their use. Their environmental
maintenance of toxic levels of B.s. Larval cadavers seem safety permits bacterial-control agents to be accepted
to contain all the nutrients necessary, both for vegetative both by officials and the general public. Indigenous iso-
multiplication of the bacteria and for toxin synthesis lates found in the country in question can be used.
associated with the sporulation process. Aly (1985) was
also able to demonstrate, experimentally, the germina-
tion of B.t.i. in the gut of Aedini larvae. When compared 16.4.3.10 U
 se of Microbial-Control Agents
with other environmental conditions, it seems that larval in Integrated Mosquito and Vector
cadavers are of crucial importance for the recycling pro- Management Programmes
cesses (Becker et al. 1995a).
Many control programmes aim at integrated biological
It is important to understand the impact of all these
control (IBC) strategies, which collectively affect the
­factors on routine treatments, particularly because it allows
protection of humans against mosquitoes and the con-
the correct calculation of the optimal dosage, the selection
servation of biodiversity with minimal impact on the
of the right formulation in various environmental situa-
environment. When the ecosystem is compared with a
tions, and the optimal timing for application against differ-
web and each group of organisms represents one single
ent mosquito species (Becker and Rettich 1994).
mesh, the control strategy is to effectively reduce one
single mesh (representing mosquitoes) without affect-
16.4.3.9 S
 uitability for Integrated Mosquito ing other meshes in the “food web.”
Control Programmes with Community This goal could only be optimally achieved when
Participation microbial-control agents are used as a component in the
overall IBC strategy. The conservation and encourage-
Bacterial-control agents are particularly well suited for ment of predators are important components of IBC.
the use in integrated programmes because their toxic Therefore, microbial agents and biological control
effect is selective, so they do not affect predatory methods are integrated with environmental management
organisms. These agents and predators can therefore (e.g. improving of ditch systems for regulating water
be included as additional elements in an integrated levels and creating permanent habitats for aquatic pred-
management strategy. The effect of predators can ators, such as fish). IBC programmes have been suc-
­continue after the bacterial-control agents have been cessfully implemented in the US, Canada and Europe.
428 16 Biological Control

For the successful implementation and use of flooding depends on the snow-melt in the Alps and on
microbial-control agents, the following prerequisites rainfall, and it is necessary to constantly monitor the water
are necessary (see chapter 22): entomological investi- flow in the Rhine and in the flood plains. During flooding,
gations, precise mapping and logging data on all major Ae. vexans and other floodwater species hatch within
breeding sites, assessment of effective dosages in bio- minutes or hours, at temperatures exceeding 8°C. Prior to
assays and conducting field tests, adaptations of appli- control measures, the larval density and the larval stages
cation techniques compatible to the requirements in are checked by dip samples at representative breeding
the field, design of the control strategy as well as train- sites to justify actions taken and to establish correct dos-
ing of the field staff and finally, dealing with govern- ages and the appropriate formulations applied. One day
mental bureaucracies. after the application, spot samplings by dipping are taken
Mosquitoes breed in a great variety of habitats. Almost to check mosquito density to establish treatment
everywhere, where stagnant waters are present, the prob- efficacy.
abilities of finding mosquito larvae will be high. Therefore, Depending upon the extent of the flooding, 20–30%
the formulations and dosages considered, must be com- of the potential breeding sites (~600 km²) are treated
patible with the ecology of breeding sites and factors routinely by the 400 collaborators of the KABS. About
affecting the efficacy of microbial-control agents. 200–400 g of Vectobac WDG (3,000 ITU/mg) or 0.5–1
Two different modes of application of B.t.i. prepa- litre of the liquid concentrate Vectobac 12AS (1,200
rations should be considered: aerial and ground appli- ITU/mg) are dissolved in 9–10 litres of filtered pond
cations. Helicopters equipped with conventional water for each hectare treated and applied by knapsack
buckets, booms, and nozzles or rotary mist atomizers sprayers (Fig. 16.18). For polluted breeding sites or
and/or fixed-wing aircrafts are commonly used to treat
densely vegetated or/and large surface areas. For
ground treatments, the knapsack sprayers or motorized
backpack blowers are the conventional equipment used
with diluted material or granular formulations.
Various commercial products of B.t.i. and B.s. are
used in many countries, on almost all continents
(Becker and Margalit 1993; Russell et al. 2003; Puchi
2005; Boisvert 2005; Kahindi et al. 2008). In North
America, microbial-control agents have been success-
fully used for ~25 years in nuisance insect control pro-
grammes and since the beginning of the new millennium
to control mosquitoes transmitting West Nile virus. In
Quebec, each year, more than 50 tons of formulations
of B.t.i. are used against spring species (Aedes and
Ochlerotatus) and summer species (Culex,
Coquillettidia, Anopheles) to reduce populations of
potential vectors of West Nile virus. Similary, in other
Canadian provinces and/or various states in the US and
in Germany, adulticides are seldom used to control
mosquito populations.
For the past 3 decades in Germany, B.t.i. and B.s. prep-
arations have been successfully used against floodwater
mosquitoes (Ae. vexans) and Culex spp. (Cx. p. pipiens
biotype molestus). Over 3,000 km2 of breeding sites have
been treated with B.t.i. preparations in the past 3 decades,
resulting in a reduction of the mosquito population every
year by >90%. The flood plains of the Rhine are usually Fig. 16.18 Ground application of microbial-control agents by
inundated several times each summer. The extent of the means of knapsack sprayers
16.4 Pathogens 429

when late instar larvae are present, the dosage has to be about 1 million Culinex-B.t.i./B.s. tablets are success-
increased. fully used by residents against Cx. p. pipiens, especially
During the most severe floods, usually a third of in rainwater containers.
the area has to be treated with B.t.i. granules which
are dispensed with the aid of a helicopter (dosages:
10–20 kg/ha). From 1981 to 2009, 100 tons of B.t.i. 16.4.3.11 Monitoring the Programme
powder and fluid concentrate and almost 1,000 tons
of B.t.i. ice and sand granules mixed with quartz sand, Approximately 8% of the KABS budget is invested in
vegetable oil and B.t.i. powder were used, to treat monitoring mosquito populations, mosquito resis-
thousands of hectares of floodwater mosquito breed- tance and environmental impact. All the studies con-
ing sites by ground application or by helicopters ducted to date, have demonstrated that the introduction
(Fig. 16.19). of B.t.i. and B.s. have reduced the numbers of nui-
Control of urban mosquito species is mainly carried sance mosquitoes to an acceptable level without any
out by the residents. To assist with this, KABS provides adverse effects on the diversity and beauty of the
information on the biology of Cx. p. pipiens biotype ecosystem.
molestus and the appropriate control measures. Monitoring Mosquito Abundance: Monitoring po-­
Vectobac® DT/Culinex® tablets, which contain toxins of pulations of adult mosquitoes is achieved by setting adult
one or both bacilli, have been very successful. They kill mosquito traps placed at strategic sites throughout the
Culex larvae in water containers over a period of several flood inundation area. The CO2-baited CDC/EVS traps
weeks. In drainage systems and large cesspools with are set overnight twice/month, from April to September.
eutrophic water bodies, B.s., as a liquid or powder for- Mosquitoes trapped from areas where no control mea-
mulation, is applied against Culex larvae. Each year, sures have been undertaken serve as points of reference
and are compared to the numbers of mosquitoes trapped
from treated areas, to determine efficacy of control mea-
sures. It has been shown that since the widespread appli-
cation of B.t.i. preparations in 1981, mass occurrences of
mosquitoes have been successfully suppressed. Naturally,
these control strategies have received an extremely posi-
tive reception among the local residents.

16.4.3.12 Monitoring Environmental Impact

It became essential to document the environmental

impact of B.t.i. and B.s. preparations, to provide a sci-
entific basis for rebutting arguments commonly raised
to deter mosquito control by lobby groups. Before
large-scale application of microbial-control agents was
undertaken, the most important members of various
aquatic groups (Cnidaria to Amphibia) were screened
in the laboratory and in small-scale field trials for their
susceptibility to microbial-control agents. This study
showed that in addition to mosquitoes (Culicidae) and
blackflies (Simuliidae), only a few species of nuisance
midges (e.g. Chironomidae) were affected by B.t.i.
toxins. For the most part, these nuisance midges were
much less susceptible to B.t.i. toxins than the target-
Fig. 16.19 Aerial application of B.t.i. granules organisms.
430 16 Biological Control

The development of insects in treated and untreated (ITNs) and indoor spraying, focus only on the control of
waters is regularly monitored using emergence traps. endophagic and endophilic anophelines, exophagic and
The occurrence and abundance of insects in treated exophilic species could still transmit malarial pathogens.
areas is routinely assessed by light traps. All investiga- Therefore, research on the development of locally
tions have shown that whereas the numbers of Aedes/ viable IVM/IMM strategies, including larval control
Ochlerotatus mosquitoes are drastically reduced, all and development, testing and/or implementation of sus-
other insects continue to develop in the water and, as tainable, environmentally-sound, and cost-effective
winged adults, provide a food source for birds, amphi­ alternative strategies to DDT use, was strongly
bians, and bats. ­encouraged (WHO 2004b). Mosquito larval control, by
use of larval source management (LSM), is the manage-
ment of mosquito breeding sites using larvicides, such as
B.t.i. or B.s. preparations, natural predators or imple-
16.4.3.13 Monitoring Resistance
menting water management techniques to reduce vector
populations. Contrary to adult vectors, the developmen-
Mosquito populations should be checked at regular
tal stages of mosquitoes are usually confined in great
intervals for resistance development. Resistance has
numbers within relatively small aquatic habitats, there-
not yet been detected after more than 25 years of B.t.i.
fore, control efficacy is greatly enhanced.
applications (Ludwig and Becker 2005). To prevent
Control of vector-mosquito populations in their
development of resistance to B.s. in Culex, B.s. and
aquatic larval habitats offers an opportunity to sig-
B.t.i. preparations are used alternately in the overall
nificantly enhance the protection afforded by existing
management plan for this species. Combined products
vector management strategies and consequent
like VectoMax which contains toxins of both bacilli can
malaria reduction (Killeen et al. 2000a,d; Fillinger
be used against mixed populations of floodwater and
and Lindsay 2006; Dongus et al. 2007; Walker and
Culex spp. and so reduce the risk for resistance against
Lynch 2007; Worrall 2007). Vector-mosquito popu-
B.s. toxins.
lation suppression, afforded by larval control, may
also reduce selection pressure towards resistance to
insecticides utilized for ITN/LLIN and IRS by
16.4.3.14 T
 he Role of Microbial-Control Agents reducing the rate of insect-chemical contact in local-
in Malaria Control Programmes ized populations.
Specifically, the use of B.t.i. and B.s. preparations for
The recently initiated global campaign against malaria, mosquito-larval control has been demonstrated to be
particularly in Africa, lead by major international orga- highly effective for the control of malaria vector-mos-
nizations, such as Roll Back Malaria (RBM), World quitoes in Africa (Killeen et al. 2002a,b; Yohannes et al.
Health Organization (WHO), President’s Malaria 2005; Fillinger and Lindsay 2006; Majambere et al.
Initiative (PMI), Bill and Melinda Gates Foundation 2007; Walker and Lynch 2007; Fillinger et al. 2008).
(BMGF), and Global Fund to fight AIDS, tuberculosis Cost analysis also indicates that bio-control of
and malaria (GFATM), aim to significantly reduce larval mosquito populations is within the cost-range
malaria-related mortality after full implementation of of other interventions that have been described as
the programme. The cornerstones of these strategies among the most cost effective. Worrall (2007) con-
include the extension of the facilities for rapid case- cluded that the cost/person, protected by larval con-
detection and disease treatment, prophylactics, personal trol under various African scenarios, range from
protection, such as long-lasting insecticide treated nets US$0.94–2.50/person/year, correlating negatively
(LLINs) against adult vector-mosquitoes and indoor with human population density. Fillinger and
residual spraying (IRS) (RBM 2005; Makundi et al. Lindsay (2006) suggested an even lower estimate of
2007; Protopopoff et al. 2007a,b; Aregawi et al. 2008). less than US$0.90/person/year.
The emergence of resistance to both, pesticides and Cost is not the only factor that should be consid-
drugs, is the most dangerous and difficult problem to ered, control should also be ecologically sound. The
solve (Etang et al. 2004; N’Guessan et al. 2007). cost analyses above, did not consider the additional
Furthermore, the use of insecticide treated bed-nets benefits of using biological larval control, namely,
16.4 Pathogens 431

reducing the use of chemical larvicides and development

of insecticide resistance, lack of impact on non-target
organisms, and safety of workers and the human popu-
lation at large.

16.4.4 Viruses

None of the viruses, at present, are suitable for the Fig. 16.20 Iridescent viruses in the fat body of an Aedes
control of Diptera, although a number of viruses have cantans larva, 160 000 (left) 7500× (right)
been isolated from different members of the order
(Hunter-Fujita et al. 1998).
Nuclear polyhedrosis virus and cytoplasmic poly- Iridescent virus infections are most common in mos-
hedrosis virus are both known as common pathogens quito larvae (Fig. 16.20). The infected larvae are blue-
of Lepidoptera, but these viruses are less frequent in green or violet iridescent. None of these viruses or any of
Dipteran populations and usually have low pathoge- the parvoviruses, known to be infectious for Ae. aegypti,
nicity; therefore, they are not practical for controlling Cx. p. pipiens or Simulium vittatum, can yet be used as
mosquitoes. potential microbial-control agents (Weiser 1991).
Chapter 17
Environmental Management of Mosquitoes

17.1 Introduction or safety impacts of pesticide use, the need for more
sustainable approaches to pest and vector manage-
ment, and the desirability of communities taking more
The concept of environmental management for mosquito
ownership of local pest and vector management.
control spans a broad range of measures, designed to
Environmental management of mosquitoes may
suppress mosquito populations and the risk of ­d isease
include a very wide range of interventions, such as
transmission. In 1980, the WHO Expert Committee
proper water storage containers, proper water man-
on Vector Biology and Control defined three basic
agement practices (including every possible effort to
categories of environmental management for vector
reduce stagnant water), modifications to existing
control:
sewage works, changes in rice husbandry and laser-
• Environmental modification: long-lasting physical leveling (if available) of agricultural fields to drasti-
transformation of vector habitats. cally reduce stagnant water at tail-ends of fields,
• Environmental manipulation: temporary changes to redesign of bus shelter roofs, ditching of salt marshes,
vector habitat as a result of planned activity to pro- routine collection and proper disposal of certain items
duce conditions unfavourable to vector breeding. of urban refuse, making earnest attempts to screen-
• Changes to human habitation or behaviour – efforts out adult mosquitoes from entering homes, training
to reduce human/vector/pathogen contact. of health department personnel and community activ-
ists, soliciting cooperation and support of local politi-
Before the introduction of synthetic insecticides in the cians, and the preparation and distribution of
mid twentieth century, environmental management educational leaflets about mosquitoes to communi-
measures were the primary techniques used for mos- ties. Such interventions often require a multidisci-
quito control and disease reduction. In Malaysia, plinary approach, perhaps involving entomologists,
Watson (1911) showed that draining and filling swamp civil engineers, agronomists, ecologists, behavioural
areas resulted in a dramatic fall in the numbers of scientists, economists, local politicians, and community
malaria cases. Ross (1913) described the importance representatives.
of “proofing” buildings against mosquito entry as an Environmental management concepts may some-
essential part of malaria prevention. In the USA, ditch- times be difficult to elucidate and/or implement. The
ing of salt marshes became very widespread in the efficacy of environmental management measures, such
1930s to abate mosquito nuisance (Carlson 2006). The as source reduction, may not bear a simple linear cor-
advent of highly effective synthetic insecticides in the relation with the numbers or proportion of mosquito
mid-twentieth Century initially resulted in a wane in breeding sites removed. Gu et al. (2006) argued that
interest in environmental management measures, but source reduction exerts its effect not only by reducing
in recent decades there has been a resurgence in incor- the number of adult mosquitoes produced, but also by
porating these concepts into integrated mosquito man- extending generation times by forcing the remaining
agement (IMM) programmes. This is a result of several gravid females to spend more time searching for ovi-
factors, including the onset of insecticidal resistance, position sites. Whatever the mechanisms involved, the
concern over the potential for unwanted environmental benefits of source reduction are substantial, especially

N. Becker et al., Mosquitoes and Their Control, 433

DOI 10.1007/978-3-540-92874-4_17, © Springer-Verlag Berlin Heidelberg 2010
434 17 Environmental Management of Mosquitoes

because these concepts result in long-term reduction of received little critical attention and evaluation. Lindsay
mosquito breeding sites. Newton and Reiter (1992) and Snow (1988) found that the number of An. gam-
used a deterministic model of dengue transmission to biae in houses in Gambia with closed eaves was 43%
argue that techniques such as source reduction, that less than in houses with open eaves. Children who
provided a long-term reduction of Aedes aegypti slept without bed nets were found to be at lower risk of
[St. aegypti] populations, were actually more effective malaria in houses without eaves openings, as compared
and sustainable than ultra low volume (ULV) insecti- to houses with open eaves.
cide treatment, in combating dengue outbreaks. On the island of Sao Tome off the coast of west
Africa, houses built on stilts had about half the number
of An. gambiae in them than houses built at ground
level (Charlwood et al. 2003). This tendency for greater
17.2 E
 nvironmental Management mosquito activity close to ground level is also seen in
of Mosquitoes in Urban Areas Cx. quinquefasciatus, where Howell and Chadee
(2007) found that the numbers of mosquitoes resting in
houses on stilts was significantly reduced compared to
Urban areas provide an ideal habitat for many mos-
houses built at ground level.
quito species, with abundant availability of blood
Lindsay et al. (2003) reviewed a range of modifica-
meals, and a wide range of water bodies, ranging
tions to dwellings and concluded that they were often
from flower vases at cemeteries, bromeliad plants and
of low cost, were long-lasting, and had the potential to
rain-filled coconuts, to highway drainage structures
reduce the intensity of malaria transmission in many
and faulty sewage systems. Appropriate environmen-
parts of the world.
tal management interventions will range from the
design of urban structures, to the provision of infor-
mation to cemetery visitors, to public information 17.2.2 Construction Sites
websites. The following sections will highlight some
of the more important and well-documented exam-
ples of environmental management concepts in reduc- Construction sites will often host a variety of water
ing mosquito breeding sites in urban areas, but is by bodies, including water storage containers, water-filled
no means exhaustive. excavations, flooded basements, wheel ruts, and tempo-
rary drainage systems. Such habitats will host a range
of mosquitoes, including Aedes, Culex and Anopheles
species (Baumgartner 1987; BoonTeng 1997). In some
17.2.1 D
 enying Mosquito Access to Urban cases, mosquito breeding within a site is believed to be
responsible for a disease outbreak amongst those working
Areas and into Homes
on the site itself (Adak et al. 1994). Prevention of
mosquito breeding in such areas is typically achieved
A number of mosquito species tend to disperse and feed by a combination of education and awareness for deve­
close to ground level. Bellini et al. (1997) working with lopers on the need to avoid standing water, and law
Ae. caspius in the Po delta in Italy, found that this species enforcement where guidance and regulations are not
flies close to ground level, and proposed that a barrier of followed (WHO 1986; Seow-Boo 2001).
3-4 m height and 2.7 km long, would prevent mosquitoes
moving from wetlands to residential and tourist areas,
without the need for insecticide use. Although such tech- 17.2.3 Water Storage Containers
niques have been previously proposed, there is little evi-
dence of them being used in practice. In many areas, water supply is not available directly
Proofing dwellings against the entry of mosquitoes from a main system to every home, instead it is supplied
is one of the oldest techniques used to reduce nuisance via a community standpipe, pump, well, or vehicles,
biting and disease transmission (Ross 1913). However, and will then typically be stored in or close to the home
although such techniques and details have become part in a water container(s). Even where running-water is
of vernacular architecture around the world, they have available in the home, then the supply may be intermit-
17.2 Environmental Management of Mosquitoes in Urban Areas 435

tent or unreliable, which eventually results in local stor- areas was particularly important in determining the
age (Barrera et al. 1995). Water storage containers degree of Culex breeding, with L-shaped drains being
around the home are typical breeding sites for Ae. much less important than U-shaped drains in terms of
aegypti and Ae. albopictus [St. albopictus], but may also mosquito production.
support a number of other species (Brown et al. 1992;
Kusumawathie et al. 2002). In terms of environmental
management, preventing mosquito production from
17.2.5 S
 ewage and Waste-Water
such sources is typically achieved by use of tight-fitting
lids over the containers (Kittayapong and Struckman Processing
1993). However, the degree to which such lids are used
in practice may depend on the intended use of the water Sewage processing facilities, through the presence
and the size and shape of containers available. of large volumes of water, rich in nutrients, and
Phuanukoonnon et al. (2005) working in Thailand found often at slightly elevated temperature, can provide
that 96% of drinking water containers were covered by highly favourable conditions for mosquito develop-
well-fitting lids, while only 36% of containers of water ment. Such facilities are typically located close to pop-
intended for washing, were covered. ulation centres, hence create the possibility of biting
nuisance, or even the risk of disease transmission.
Ensink et al. (2007) working in Faisalabad,
Pakistan, found that poorly maintained urban waste-
17.2.4 Drainage Systems water stabilization ponds supported large populations
of several mosquito species, including Cx. quinque-
Given the function of building and highway drainage fasciatus, An. stephensi, and Anopheles culicifacies.
systems, they are particularly prone to the formation of A subset of the ponds was fitted with a screen to
standing water, especially where blockages, leaks or remove large debris from the incoming water, floating
malfunctions occur. Surveys in Queensland, Australia debris and emergent vegetation were removed from
showed that 14% of roof gutters with standing water the ponds, and cracks in the concrete lining of the
contained either Ae. aegypti or Oc. notoscriptus larvae ponds were mended. In the ponds subject to this inter-
(Montgomery and Ritchie 2002). The authors empha- vention, the percentage of water samples positive for
sized the need to include gutters in source reduction both Anopheles and Culex larvae, fell dramatically
exercises. In Singapore, the gutters on city bus shelters compared to the control ponds.
were commonly blocked and therefore supported mos- Epibane et al. (1993) studied the mosquito fauna in
quito breeding. A new bus shelter was designed to sewage treatment ponds in California, in which water
avoid the need for gutters, which prevented this prob- hyacinth (Eichornia sp.) was used as part of the water
lem (Seow-Boo 2001). Surface water drainage sys- treatment process. Despite the active aeration of the
tems, such as stormwater catch basins and sumps often ponds, and the presence of Gambusia sp, they sup-
favour the development of mosquito larvae (Kwan ported large populations of various Culex species. A
et al. 2008), partly because of the accumulation of grid of garden sprinklers were installed and operated
organic debris that may impede flow and result in stag- nightly, to provide a pulsating pattern of falling water
nant water. Preventing and resolving mosquito prob- across the surface of the ponds. The water spray was
lems in such areas requires extensive multiagency considered to prevent, deter, and disrupt oviposition
cooperation, and may involve challenging and some- on the water surface, resulting in a reduction in larval
times unique changes requiring extensive construc- counts by about 95%. Similar results were obtained by
tion/modification (a very costly proposition), including Ayler (1991) using a sprinkler system on stagnant
re-shaping of structures and channels, changes to cov- water tanks on sewage treatment plants in Florida.
ers of sumps to prevent mosquito access, or removal of Whelan (1998) discusses a range of design features
emergent aquatic vegetation (Metzger et al. 2002, 2008; of waste-water processing facilities, such as steep sides
Messer 2002; Kluh et al. 2002; Fox and Absher 2002). to water holding ponds, exposed location to enable
Cairncross et al. (1988) working in Pondicherry wind action on the water surface to create unfavourable
showed that the choice of drain cross-section in urban conditions for oviposition and larval development, the
436 17 Environmental Management of Mosquitoes

absence of emergent vegetation, and choice of disposal 17.2.7 Urban Sanitation

routes for the fully processed water.
Where processed urban waste-water is disposed of
The immature stages of container-breeding mosquitoes,
by application to free-water surface constructed wet-
such as Ae. aegypti and Ae. albopictus, will be found
lands, large areas of favourable mosquito habitat may
not only in municipal features of the environment such
be created. A variety of techniques have been devel-
as drains and water storage or processing facilities, but
oped and assessed to mitigate mosquito problems
also in a vast number of smaller and often ephemeral
(Walton 2002, 2003). Thullen et al. (2002) found that
water bodies. Although DF/DHF vectors are very
deepening the water, but at the same time creating
dependent on such habitats, malaria and filariasis vec-
numerous small raised hummocks within the water
tors may also be found frequently in such niches
successfully improved water quality and also reduced
(Biswas et al. 1992). These urban water bodies may be
mosquito numbers. Alternatively, mosquito numbers
semi-natural, e.g. cut ends of bamboo, coconut shells,
may be minimized by periodic draining and drying of
tree-holes, bromeliad plants, or they may be artificial
the wetland cells, providing that it coincides with a
e.g. empty drink cans, plant pots, ant traps, used vehicle
period of little or no rainfall (Mayhew et al. 2004).
tyres, etc. In the urban environment, there may be a
Sanford et al. (2003) found that the duration of drying
great diversity and number of such containers.
was critical, with two weeks drying being the period
Manrique-Saide et al. (2008) classified Ae. aegypti
most likely to produce large larval mosquito numbers
breeding sites in Mexico into 15 different basic catego-
when the cell was re-flooded.
ries. Focks and Chadee (1999) working in Trinidad
found that the density of containers holding Ae. aegypti
ranged from 61 to 399/ha.
17.2.6 Cemeteries Destruction, disposal, recycling or regular emptying
of such containers and larval sites can have a significant
Cemeteries are potentially significant in terms of mos- effect on larval indices, and on disease transmission
quito production, because of their presence in urban (Soedarmo 1994). However, such improvements are
areas, the use of large numbers of small artificial water often difficult to achieve by direct action by health or
containers (i.e. vases for flowers), numerous adult city authorities, because the majority of containers may
mosquito resting sites amongst graves, and availability be on private land to which access is proble­matic, and
of carbohydrate from flowers. In Brazil, cemeteries because container numbers could increase again if
have been recorded with up to 6,100 artificial breeding behaviour of residents remain unchanged. As an alterna-
sites per ha (Vezzani 2007). Mosquito species known tive to direct action, organizations responsible for vector
to occur commonly in flower vases include Ae. albopic- control have often embarked either on programmes of
tus, Ae. aegypti, Cx. pipiens, Ochlerotatus spp. (e.g. community participation (see Sect. 17.4.1 below), and/or
Oc. japonicus), and Culiseta spp. Cemeteries are cul- legislation requiring landowners or occupiers to remove
turally sensitive areas, so simply removing or prohibit- potential breeding sites (see Sect. 17.4.2 below).
ing vases is not appropriate, and some cemetery staff
may earn an income from replacing fresh flowers in
vases. Depending on the local situation, source reduc-
tion possibilities may include: 17.3 E
 nvironmental Management
Frequent emptying of water-filled containers, although in of Mosquitoes in Rural Areas
practice this may be very difficult to carry out.
Filling flower vases with wet sand or soil.
Replacing real flowers with artificial flowers in vases 17.3.1 Agriculture
with a perforated base.
Education of cemetery staff and visitors about the
importance of preventing mosquito breeding (Schmidt Rice production is widespread throughout tropical
2003). and subtropical regions and often (but not always)
Regulations to prevent visitors introducing water-filled involves flooding of rice fields. Flooded rice fields are
containers into the cemetery, although in practice such
regulations may be ignored (Vezzani and Velasquez recognised as major potential sources of both nuisance
2003). and disease vector mosquitoes in various regions.
17.3 Environmental Management of Mosquitoes in Rural Areas 437

Insecticide use for control of rice pests may provide countries, and in some areas there are movements to
collateral control of these mosquitoes, and insecti- reinstate former wetland areas (Walton 2002, 2003).
cides may also be applied specifically for control of Given the wildlife importance of saline and fresh water
mosquito larvae. Nonetheless, mosquito problems wetlands, environmentally acceptable alternatives to
persist in rice fields. A number of approaches have insecticide use for mosquito control in these areas have
been used to prevent mosquito breeding by intro- been developed.
ducing changes in agricultural practices. In Sri On salt marshes, a wide variety of environmental
Lanka, for example, a programme was implemented management approaches to mosquito management
to educate rice farmers in the benefits of adjusting field have been used. The most widely used techniques are
levels to avoid uneven flooding and puddles, in pre- discussed below:
venting seepage from the levees around rice fields, in Grid-ditching was very widely used in the USA during the
ensuring that the water flow in channels feeding pad- 1930s, with an estimated 90% of the coastal salt marshes
dies is fast enough to prevent breeding, and in periodic on the Atlantic coast grid-ditched to reduce mosquito
drainage of paddies before mosquito emergence could populations (Clarke et al. 1984). The process consisted of
the excavation of parallel ditches at 50–100 m intervals
occur. Results showed a significant drop in Anopheles across the marsh, connecting to tidal channels. Efficacy of
spp. densities, but had a limited impact on Culex and the technique was limited, and channels frequently
Aedes numbers (Yasuoka et al. 2006). became blocked by silt where they entered tidal water.
Keiser et al. (2005) used alternate flooding and Open-marsh water management is a process of exca-
drying of rice fields as part of an integrated programme vating channels across the marsh, sometimes using rotary
to limit production of culicine vectors of Japanese excavators, which link otherwise isolated pools to each
other and to the tidal source. It appears to work by flush-
encephalitis. ing mosquito larvae out of the marsh into areas where they
Alternative approaches include encouraging the are unable to survive, allowing larval predators such as
water-fern (Azolla microphylla) to grow on the water fish to have access to and colonise the pools, and also
in the rice fields. Rajendran and Reuben (1991) showed appears to alter the characteristics of the site, thereby
reducing mosquito oviposition. Runnelling is a variation
that when fully established, the mat of vegetation pro- of open-marsh water management that uses shallower
duced by the water-fern can reduce numbers of Cx. channels (Dale et al. 1993).
tritaeniorhynchus and other species by up to 80%.
Impoundment is a process of constructing raised bunds
However, mosquito populations still reached problem- (levees) around the marsh, and has been widely used since
atic levels in the period before the relatively slow- the 1950s. The bunds are typically punctuated by culverts
growing fern became established. that allow the water level within the marsh to be altered by
Lacey and Lacey (1990) have provided a compre- controlling water flow. Typically, water levels would be held
high during the summer when the risk of mosquito breeding
hensive review of the history and practice of environ- is highest, and as a result mosquito production could be
mental management of mosquitoes in rice production. almost entirely prevented. Rotational impoundment manage-
ment is a fine-tuning of the process that aims to manage mos-
quito populations and keep broader environmental impact to
a minimum, by limited flooding during the summer followed
by extensive flooding in autumn (Carlson 2006).
17.3.2 Natural Wetlands
There is extensive literature on the environmental
impact of such changes on salt marsh ecology. The
Mosquito production in salt marsh or freshwater wet- efficacy and impact of the changes is likely to result
lands can be intense, and this can create problems not only from selection of the intervention, but on
where residential or resort areas are situated close to the quality with which the work is carried out. Dale
such habitats. Such problems have been recognised in and Knight (2006) in Australia, compared the envi-
Australia (Oc. vigilax), the USA (Ae. sollicitans), ronmental impact of grid-ditching, open-water marsh
Europe (Ae. caspius), and elsewhere. Historically, such management, and runnelling, using ten different
problems were often addressed by complete drainage ecological parameters. They concluded that although
of the marsh, or by filling and reclamation (Carson none of the techniques completely destroyed the
2006). More recently, with the recognition that natural marsh, grid-ditching had the most impact, while
wetlands are an important wildlife and biodiversity runnelling (i.e. a version of Open-Marsh Water
resource, such measures have largely ceased in many Management) had the least negative impact, while
438 17 Environmental Management of Mosquitoes

still providing a useful reduction in mosquito popu- companies. However, the removal of smaller but
lations. Carlson (2006) in Florida concluded that a no less important larval sites, such as a variety of
mixture of salt marsh management techniques were small containers, are best implemented by the local
beneficial to local ecology, and a combination of community.
rotational impoundment management, and open- Techniques for raising awareness and gaining
marsh water management was the most acceptable cooperation of the community are not limited to use in
approach. environmental management, but are also relevant to
Natural freshwater wetlands may also be very sig- other areas such as the use of insecticide treated nets.
nificant in terms of mosquito production. Schäfer et al. In practice, community-driven campaigns are often
(2004) working in Sweden raised concerns about the preceded by preliminary survey work (e.g. Knowledge,
risk of mosquito nuisance and of transmission of Attitudes, Perceptions – KAPs) to assess the residents’
Sindbis virus by mosquitoes from natural wetlands and existing knowledge and understanding of the issues
from wetland areas constructed for biodiversity or relating to mosquito problems and management in
amenity purposes. Proposals included limiting the size their area. This enables the final intervention to be
of constructed wetland areas, and their proximity to more appropriately targeted.
human settlements. Interventions intended to gain community support
In central Europe, the larger rivers, such as the and cooperation may consist of any or all of the
Rhine and Danube, formerly had extensive natural following:
flood plains that were flooded during the spring snow
• Direct communication with residents, health centre
melt, and at intervals over the rest of the year. These
visitors, farmers, community leaders, etc., via public
natural flood plains contained many permanent and
meetings, workshops, school visits, theater events,
semi-permanent water bodies, which acted as reser-
workplace meetings, and practical demonstrations.
voirs for a variety of beneficial wildlife, that provided
• Distribution of brochures and literature to individ-
a check on the mosquito populations, particularly Ae.
ual households.
vexans, which tended to develop during periods of
• Mass media (posters, newspaper, radio, television,
flooding. However, a process of canalisation has
internet).
taken place in many areas, and many natural flood
plains were reclaimed. Although flood catchment The preference of Ae. aegypti and Ae. albopictus for
areas were provided, the water table is lower and the household and peridomestic containers has tradition-
water coverage is temporary, resulting in reduction of ally led to a strong emphasis on improving public
their value as reservoirs of beneficial wildlife. awareness and cooperation in DF and DHF control
However, in recent years there has been a process of campaigns (Becker 1992). However, community mobi-
environmental management of existing flood plains lization toward environmental management is just as
to re-create permanent and semi-permanent water relevant to malaria (Kibe et al. 2006), filariasis
bodies. This has enabled the establishment of a larger (Panicker and Dhanda 1992), and West Nile virus
and more diverse population of beneficial vertebrates ­control (Schaffner 2008).
and invertebrates. Formerly, such campaigns were planned in the
context of education alone, i.e. the belief that if the
facts concerning mosquitoes and the risk of infesta-
tion were supplied to communities, the necessary
action would then inevitably take place as a result.
17.4 E
 nvironmental Management More recently, however, campaigns have become
of Mosquitoes and Human Issues more sophisticated. Geounuppakul et al. (2007)
reported on a programme aimed at enhancing indi-
vidual empowerment, ownership, and self-esteem in
17.4.1 Community Participation relation to malaria control. The objective was that as
a result of the intervention, individuals and commu-
Some environmental management measures, such as nities would acquire the drive and self-confidence to
changes to drainage or waste-water processing, are largely adopt, implement, and maintain appropriate malaria
the responsibility of governmental agencies or utility control measures.
17.4 Environmental Management of Mosquitoes and Human Issues 439

However, detailed assessments of the effectiveness larval indices, the effectives of the individual compo-
of public awareness and public behavioural-change nents of the programme were unclear. Further work
campaigns are relatively sparse. The general view is would be required to identify which components were
that although dissemination of information may be actually effective.
readily achieved, transforming this into public action
is more challenging. Certainly, programmes to enhance
public participation in vector control must be locally
17.4.2 R
 egulations for Environmental
led, as beliefs, superstitions, practices, and ecological
conditions greatly differ from area to area. Seow-Boo Management of Mosquitoes
(2001) suggests that sociologists and behavioural
scientists are key to ensuring the effectiveness of Although the environmental management of mosqui-
community-based programmes. toes is ideally achieved with the support, cooperation,
Schreiber and Cuda (1994) found that in Florida, and involvement of the general public, there may be
the impact of distribution of information to residents occasions where that support is not forthcoming from
varied according to the socio-economic status of the particular individuals or organizations. Given that mos-
community. Significant reductions in numbers of quitoes may present a threat to the general public,
containers were achieved in low-income communi- whether as a nuisance or as a disease vector, some coun-
ties, but not in middle- to high-income communities. tries or states have passed legislation intended to reduce
Schreiber and Morris (1995) assessed the effective- the risk of mosquito breeding (i.e. statutory environ-
ness of printed educational materials intended to mental management), which could be used against par-
encourage residents to remove containers and poten- ticular individuals or organizations where their action or
tial mosquito development sites from their properties inaction might create a risk to public health.
in Florida. Communities were provided with either no In the USA, Ae. albopictus is particularly associated
information, black-and-white printed information, or with used tyre disposal sites. The state of Illinois has
full-colour printed information. Results showed that passed legislation to limit the storage of used tyres and
in terms of the numbers of potential mosquito devel- to require proper disposal and recycling (Novak 1995).
opment containers remaining on residential proper- In Singapore, the Control of Vectors and Pesticide Act
ties, the black-and-white leaflet resulted in no empowers city authorities to inspect premises for poten-
improvement compared to the provision of no infor- tial mosquito breeding sites, to require the owner or
mation, while the full-coloured information resulted occupier to abate breeding sites, and to perform the
in a significant reduction. ­necessary work and recover costs if need be (Seow-Boo
Heintze et al. (2007) carried out a systematic 2001). Fines may be imposed (and progressively
review of published studies on the effectiveness of increased) if subsequent offences occur. However, the
community-based interventions for control of dengue author stresses that removal of breeding sites through
vectors. The studies reviewed, included a wide range increased awareness is the preferred approach, rather
of measures directed at local communities, including than relying on the threat of prosecution. Nonetheless,
mass media (posters, radio, television, newspaper, where owners or occupiers persistently fail to discharge
etc.), direct distribution of materials to individual their responsibility, legislation can be useful as the last
households, and meetings with residents and commu- resort. In Italy, regulations also exist that require resi-
nity leaders. The review concluded that although dents to remove mosquito breeding sites from their
community-based approaches, together with other property, but local authorities are sometimes to reluctant
related interventions, were able to reduce Aedes to use legal powers to address mosquito problems.
Chapter 18
Chemical Control

18.1 History practice of insecticide use. These exceptionally

potent, biodegradable compounds may be used in
The development and evolution of the chemical indus- the field at rates as low as 20 g/ha, which is 10–100-
try has led to many major advances in pest, vector, and fold lower than more conventional insecticides and
pathogen control. However the beneficial effects of eventually leads to a lower burden of residues in the
these advances has not been felt equally around the environment. Unfortunately, although they are an
world. In many developing countries, and even in some impressive achievement, the synthetic pyrethroids
developed countries, pests and vectors are still causing are not the perfect answer to the insecticide prob-
problems for which technical solutions already exist. lem, since they have a high toxicity on many aquatic
In attempting to review the present status of species, vertebrates, invertebrates, and several ben-
insecticides used for mosquito control, it may be eficial insects.
helpful to briefly examine the recent past. The adverse effects of indiscriminate and excessive
The first recorded use of a synthetic organic insecti- use of DDT, were dramatically portrayed by the pub-
cide, dinitro-o-cresol, occurred in 1892, and by the lication of Rachel Carson’s “Silent Spring” (1962).
1930s a range of such compounds had been discovered As a result of the problems with chlorinated hydrocar-
and found limited use (Cremlyn 1978). From the 1920s bons, alternative methods were explored. These alter-
onwards, the increasing potency of insecticides as natives included insecticides developed as an outcome
tools for insect control led to their growing predomi- of rational leads from basic entomological research on
nance as preferred method for insect control. metabolic disrupters, moult inhibitors, and behaviour
A series of dramatic discoveries during the late modifiers of insects. Highly potent inhibitors of chitin
1930s provided new synthetic insecticides, which had synthesis in the insect integument were developed in
enormous potential for widespread use, and which fur- the early 1970s in the Netherlands. Since the target
ther reinforced the emphasis on a chemical approach site of action for these chemicals is known and is sus-
to insect control. ceptible to disruption only in certain species at certain
In 1939, the “wonder” insecticide of the chlori- times during the life cycle, these materials are thought
nated hydrocarbon group, dichlorodiphenyltrichlo- to have fewer serious deleterious effects on nontarget
roethane, best known as DDT, was introduced. This species. A second example is based on the discoveries
was soon followed by the development of organo- that insect juvenile hormones regulate many develop-
phosphates (OP) in Germany, which had been evolv- mental functions in insects and that they are unique to
ing since 1932, when Lange and von Krueger first arthropods. This initiated the synthesis of juvenoids in
synthesized organofluorophosphate esters. In the the early 1980s for selective insect control. As with
early 1950s, carbamates were created in Switzerland. other alternative strategies for insect control, the full
Between the 1960s and 1970s, the discovery and potential of juvenoids in selective and environmen-
development of photostable pyrethroids, mainly in tally sound insect control has not been fully realized
Japan and the UK, led to profound changes in the to date.

N. Becker et al., Mosquitoes and Their Control, 441

DOI 10.1007/978-3-540-92874-4_18, © Springer-Verlag Berlin Heidelberg 2010
442 18 Chemical Control

Increased research on genetic control of vectors As late as in 1955, Plasmodium spp. infected
was carried out during the 1960s and 1970s. Numerous approximately 500 million people causing malaria
areas of genetic techniques such as translocations, throughout the world. The annual death rate from this
cytoplasmatic incompatibility, meiotic drive and ster- debilitating disease was reduced from 6 million in 1939
ile hybrids were investigated, but few practically appli- to 2.5 million in 1965 and to less than 2 million today.
cable. Similarly, much research was conducted on Although a clinical manufacturing facility has been
chemosterilisants, but none of the compounds became opened to produce a vaccine that uses a weakened form
operational in vector control programmes. It is also of malaria parasite, as a main component of “whole-
important to note the extensive research on the evalua- parasite” vaccine, it is still to be seen if today’s technol-
tion and development of biological agents such as ogy will allow it to overcome obstacles that have
viruses, bacteria, protozoa, fungi, nematodes, and prevented production so far. Through the judicous use
other parasites, predators, and pathogens. So far, with of insecticides, similar progress has been made in
the exception of bacterial agents, none of these have reducing the incidence of other important tropical dis-
emerged as widely useful tools in vector control eases. However, in spite of the progress made, it appears
(Mulla 1994). that there still remains the ever-lurking danger to
The use of B. thuringiensis var. israelensis (B.t.i.), humans from mosquito-borne diseases such as malaria,
which was introduced into integrated mosquito man- dengue fever, encephalitis, yellow fever, Chikungunya
agement (IMM) at the beginning of the 1980s, is dis- fever, lymphatic filariasis, etc. The number of deaths
cussed in detail in Chap. 16. resulting from all wars appears insignificant compared
The effects of pesticides on nontarget organisms to the toll inflicted by vector-borne diseases.
and the environment have been a source of worldwide The current strategy in successfully implementing
contention for more than 20 years, and form the basis pest and vector management programmes is to care-
for most legislation intended to control or prohibit the fully select from a variety of techniques, the combina-
use of specific pesticides. The most readily identified tion of control options that is best suited to achieve the
adverse effects of pesticides on nontargets were those objectives, and at the same time to preserve the eco-
of the persistent organochlorine insecticides (e.g. logical balance. This approach, which has to maintain
DDT) and their metabolites or conversion products on a high flexibility, has gained much support not only
certain species of fish and birds. Consequences less among scientists, but also among the general public in
readily identifiable include the effects of pesticide resi- the last 20 years, and is referred to as integrated pest
dues in food and the environment, on humans and management (IPM) and integrated vector management
domestic animals. (IVM) in public health programmes.
Due to difficulties in recognizing the diversity Since vector population management constitutes an
of the ecological relationships between nontarget important element in the current global strategy for the
and target organisms, mistakes were made in the control of major vector-borne diseases, chemical con-
nonselective use of pesticides. However, these mis- trol remains an important component in an integrated
takes do not appear to have had permanent or irre- approach to vector control especially during epidemic/
versible consequences on nontargets and the epizootic situations.
environment. Great efforts have been made to safe-
guard the protection and preservation of nontarget
organisms.
These environmental problems were not the only 18.2 Insecticides
ones to become evident as synthetic organic insecti-
cides came into widespread use. Resistance rapidly When millions of humans are killed or disabled annu-
increased in a number of agriculturally and medically ally from vector-borne diseases, and the global dam-
important insect species. The need for higher dosages age by insects, vector-borne diseases, weeds, and
and more frequent applications of insecticides to com- rodents is estimated at > $100 billion annually, it
bat these pesticide-induced problems has, on occa- becomes apparent that the control of various harmful
sion, been disastrous, especially when these control organisms is essential for the future development of
products were used indiscriminately. human health, agriculture, and industry. In the process
18.2 Insecticides 443

of accommodating these vital human requirements, form an important component in mosquito control
pesticides have consequently become an indispens- management. The microbial agents play a substantial role
able part of global integrated vector management in mosquito control programmes in Europe and the
programmes. United States, and are discussed in Chaps. 11 and 16.
On an average, 547 tonnes of active ingredients of
organochlorines, 437 of OPs, 24 of carbamates, and
162 tonnes of pyrethroids were reportedly used annu-
18.2.1 Classification of Insecticides ally for vector control at the global level during 2003–
2005 (Table 18.1). A recent publication by Zaim and
Insecticides used in mosquito control belong to four Jambulingam (2007) on global insecticide use in vec-
major chemical groups, chlorinated hydrocarbons, tor-borne disease control gives an overview on chem-
OPs, carbamates, and pyrethroids, and a special class icals by class of insecticides used to control vectors
referred to as insect growth regulators (IGRs). worldwide. The use of organochlorines, exclusively
The first generation of insecticides are the stomach DDT, was reported to World Health Organization
poisons, such as arsenicals. The second generation Pesticide Evaluation Scheme (WHOPES) only from
includes the contact insecticides: chlorinated hydro- the African Region. The use of OPs was reported from
carbons, OPs, carbamates, and pyrethroids. After hav- all regions; about 84% of their total use was in the
ing extensively studied the various physiological region of the Americas and 1–6% in countries from
effects of the juvenile hormone, Williams in 1976 other regions. Compared with other classes of insecti-
suggested that their analogs (juvenoids) could be used cides, the use of carbamates is limited, with 80% of
as insect-specific control agents to which pest species their total use globally in the African region, the
may be unable to develop resistance. He referred to remaining use was in the region of the Americas (11%),
this class of compounds as “third-generation pesti- the South-East Asia region (8%), and the East
cides.” The fourth generation of insecticides is derived Mediterranean region (1%). Carbamates were not used
from the entomopathogenic abilities of some microbi- in the Western Pacific Region and in the European
als. Commercial preparations based on bacteria have region. The use of pyrethroids was higher in countries
been available since the beginning of the 1980s and from the region of the Americas (57% of total use)

Table 18.1 Global use of insecticides for vector control reported to WHOPES, in kg of active ingredient, by class of insecticide
and WHO region, 2003–2005 (Zaim and Jambulingam 2007)
WHO region V/VHO region
Eastern South-East Western
Year Class African Americas Mediterranean European Asia Pacific All regions
2003 OC 423,868 0 0 0 0 0 423,868
OP 19,251 151,509 21,619 6,350 22,326 6,483 227,538
C 3,900 3,835 1,000 0 1,600 0 10,335
PY 8,407 123,007 9,282 1,288 14,992 14,957 171,933
2004 OC 389,210 0 0 0 0 0 389,210
OP 327 401,508 19,594 3,600 6,691 3,816 435,536
C 321 2,473 400 0 1,600 0 4,794
PY 1,201 81,482 21,092 872 9,300 13,499 127,446
2005 OC 827,648 0 0 0 0 0 827,648
OP 15,543 550,465 22,230 0 44,644 15,760 648,642
C 56,701 1,735 465 0 2,560 0 61,461
PY 31,211 71,355 15,752 2,072 5,645 60,203 186,238
Average OC 546,909 0 0 0 0 0 546,909
OP 11,707 367,827 21,148 3,317 24,554 8,686 437,239
C 20,307 2,681 622 0 1,920 0 24,230
PY 13,606 91,948 15,375 1,411 9,979 29,553 161,872
C carbamate; OC organochlorine; OP organophosphate; PY pyrethroid
444 18 Chemical Control

Table 18.2 Global use of insecticides for vector control reported to WHOPES, in kg of active ingredient, by type
of application and class of insecticide, 2003–2005 (Zaim and Jambulingam 2007)
Amount of insecticide used (kg active ingredient)
Type of application Class of insecticide 2003 2004 2005 Average
Indoor residual spraying Organochlorines 423,868 389,210 827,648 546,909
Organophosphates 48,312 32,070 91,232 57,205
Carbamates 6,242 4,417 61,235 23,965
Pyrethroids 82,164 71,183 55,128 69,492
Treatment of mosquito nets Pyrethroids 15,838 4,694 31,819 17,450
Larviciding Organophosphates 90,725 89,426 83,136 87,762
Space spraying Organophosphates 84,243 311,948 473,994 290,062
Pyrethroids 49,675 50,336 98,021 66,011

Table 18.3 Insecticides used most extensively for vector control reported to WHOPES, in kg of active ingredient,
2003–2005 (Zaim and Jambulingam 2007)
Class Compound 2003 2004 2005 Total Average
Organochlorines DDT 423,868 389,210 827,648 1,640,726 546,909
Organophosphates Chlorpyrifos 2,998 2,425 7,041 12,464 4,155
Chlorpyrifos-methyl 9,048 2,931 6,460 18,439 6,146
Fenthion 3,924 3,205 3,019 10,148 3,383
Fenitrothion 19,515 56,565 97,084 173,164 57,721
Malathion 97,741 243,714 428,955 770,410 256,803
Pirimiphos-methyl 4,654 38,316 29,372 72,342 24,114
Temephos 89,338 87,738 76,519 253,595 84,532
Carbamates Bendiocarb 1,600 2,056 59,759 63,415 21,138
Propoxur 8,735 2,738 1,702 13,175 4,392
Pyrethroids Alpha-cypermethrin 19,394 29,436 26,102 74,932 24,977
Bifenthrin 171 732 803 1,706 569
Cyfluthrin 3,988 3,221 3,852 11,061 3,687
Cypermethrin 80,548 26,581 21,293 128,422 42,807
Deltamethrin 16,874 18,267 48,005 83,146 27,715
Etofenprox 5,256 4,355 5,248 14,859 4,953
Lambda-cyhalothrin 6,887 16,725 4,956 28,568 9,523
Permethrin 38,582 25,236 72,708 136,526 45,509

than in other regions. The European region reported space spraying and for treatment of mosquito nets
the lowest (1%) use of pyrethroids (Table 18.2). increased over the 3-year reported period, it showed a
About 60% of the insecticides reportedly used for decline for indoor residual application. The quantity
vector control (all classes of insecticides) during for organochlorines, OPs and carbamates used for
2003–2005 were for indoor residual spraying (IRS), residual applications, however, increased consider-
followed by space treatments (30.7%), larviciding ably (Table 18.3).
(7.6%) and insecticide treated mosquito nets (1.5%). All the above mentioned compounds include
The use of organochlorines and carbamates at the substances that cause mosquito mortality and may
global level was limited to IRS in the endemic areas of be categorized in various ways. They could also be
developing countries. Of the total annual use of OPs, classified according to their uses on the stage of
however, 66% was for space treatments, 20.2% for insect life cycle acted upon: larvicides or adulti-
larviciding and 13.2% for IRS. cides (Table 18.4), or by their mode of action
While about 43% of the total use of pyrethroids against the insects: stomach poison, contact poison,
was for indoor residual application, and 45% for space fumigant, etc.
spraying, the remaining 11% was used for treatment One of the WHO classifications of insecticides is
of mosquito nets. Though the use of pyrethroids for on the basis of the acute toxicity to laboratory animals.
18.2 Insecticides 445

The hazard of a compound is assessed by determining the Finally, insecticides can be classified as inorganic,
lethal effect on test animals, usually rats, when applied to natural organic, and synthetic organic. Most of the
their skin (dermal toxicity) or when it is ingested (oral insecticides used today for mosquito control fall in the
toxicity). The dose, which is statistically determined to last category. A list of insecticides, which may be used
be lethal to 50% of the test animals (LD50), is assumed in mosquito control according to the WHO Operational
to be a measure of the hazard to man and other mam- Manual on the application of insecticides for control of
mals. The latest WHO-recommended classification of the mosquito vectors of malaria and other diseases
pesticides by hazard was issued in 2004 (Table 18.5). (WHO 2004) is given in Table 18.6.

Table 18.4 Main uses of synthetic organic insecticides by chemical group

Adulticides
Chemical group Larvicides Space application Residual application
Chlorinated hydrocarbons X
Organophosphorus X X X
Carbamates X X
Pyrethroids X X X

Table 18.5 WHO criteria for classifying pesticides by hazard (WHO 2006)
LD50 for rat (mg/kg body weight)
Class of toxicity by
physical state of product Oral Dermal
or formulation Solids Liquids Solids Liquids
IA Extremely hazardous 5 or less 20 or less 10 or less 40 or less
IB Highly hazardous >5–50 >20–200 >10–100 40–400
II Moderately hazardous >50–500 >200–2,000 >100–1,000 400–4,000
III Slightly hazardous >500 >2,000 >1,000 >4,000
IIIU a.i. unlikely to present >2,000 >3,000 - -
acute hazard in normal use

Table 18.6 List of insecticides that may be used in mosquito control, WHO (2004)
Active ingredient Use Chemical type or class Toxicity class
Allethrin L, A PY III
Alpha-cypermethrin A PY II
Bendiocarb A C II
Bifenthrin A PY II
Bioresmethrin A PY III
Chlorpyrifos L, A OP II
Chlorpyrifos-methyl L OP II
Cypermethrin A PY III U
Cyfluthrin A PY II
DDT A OC II
Deltamethrin L, A PY II
Diazinon L, A OP II
Dichlorvos L, Aa OP IB
Diflubenzuron L IGR III U
Etofenprox A PY III U
Fenitrothion L, A OP II
Fenthion L, A OP IB
Jodfenphos L, A OP III U
(continued)
446 18 Chemical Control

Table 18.6 (continued)

Active ingredient Use Chemical type or class Toxicity class
Lambda-cyhalothrin A PY II
Malathion L, A OP III
Methoprene L IGR III U
Methoxychlor A OC III U
Naled L, A OP II
Permethrinb L, A PY II
Pirimiphos-methyl L, A OP III
Propoxur A C II
Pyrethrins A n.o. II
Pyriproxyfen L IGR III
Resmethrin A PY III
surface film L SF -
Temephos L OP III U
a
Fumigant may be dangerous in oil solution
b
May be dangerous in oil solution
Use: L larvicide; A adulticide; IGR Insect growth regulator
Chemical type: OC Chlorinated hydrocarbons; OP Organophosphates; C carbamates; PY pyrethroids;
SF Surface film; n.o. natural organic

18.2.2 Insecticide Formulations especially with microbial agents or IGRs, can be made
more persistent and affordable by appropriately devel-
The active ingredient (a.i.) of an insecticide is rarely oped formulations, which release the agent slowly and
suitable for application without further processing. at the appropriate depth where it will be most easily
Once the active ingredient is manufactured it is then encountered by the target larvae.
formulated, that is to say it is processed into a usable The safety of space treatments has been increased
form for direct application, or for dilution prior to an by development of water-based formulations or
application. The formulation is the form in which the replacement of emulsifiable concentrates (EC) by sus-
pesticide is available at the market. pension concentrates.
It is usually necessary to add other nonpesticidal Technical concentrates (TC/TP) are liquids or pow-
substances to the a.i. so that the resulting formulation ders containing a high concentration of a.i, which can
allows ease of handling, transportation, safety, appli- then be manufactured, packaged, shipped, or reformu-
cation, effectiveness, and storage. To meet these needs, lated into more dilute formulations. Chemicals are
insecticides may be formulated in a number of ways, rarely used in this form, except for some ultra-low-
to enhance their effectiveness, simplify their prepara- volume (ULV) adulticides.
tion for application, and meet different requirements of Solution concentrates are liquids containing a high
larviciding and adulticiding. Each formulation may be concentration of an a.i. that has been diluted with oil or
supplied in a variety of concentrations. The concentra- petroleum solvents. These SC may also be used undi-
tion of a formulation is designated either on a weight- luted for ULV applications, and are commonly used
to-weight basis, when both the a.i.and the formulation for thermal aerosol application (fogging) when further
are solid, such as DDT 5% dust, or on a weight-to- diluted with highly refined oils or kerosene.
volume basis, when the a.i. is solid and the formulation Emulsifiable concentrates (EC) consist of active
liquid, such as chlorpyrifos 400 g/l emulsifiable ingredient dissolved in an organic solvent combined
concentrate. with emulsifying agents. These products can then be
By improvement of the formulations, the effective- diluted with water to an appropriate concentration in
ness, persistence and/or safety of insecticides can also the spray tank before use. The emulsifying agent or
be increased. An example is the recent development agents cause the technical product and organic solvent
of a slow-release larvicidal formulation, designed to solution to disperse evenly in the water when mixed by
last longer when applied into the water. Larviciding, stirring. It is sometimes necessary to maintain a level
18.2 Insecticides 447

of agitation in order to keep the chemical evenly dis- tion. The diluents in some wettable powders are abra-
persed in the tank. ECs are used for larviciding when sive and can wear down pumps and nozzles, which
dispersion throughout water is required and they may have to be regularly checked and replaced (Wade
also be used undiluted as ULV applications. They are 1997). Most applications inside houses are accom-
occassionally used for residual applications to imper- plished with WDP. They are usually applied at high
vious surfaces such as houses in urban and semiurban volume rates with low concentrations of the a.i.
areas. Soluble powders (SP) are similar to WP, except they
ULV formulations, as a rule, have a low volatility, so form true solutions in water. Since they dissolve com-
reducing the evaporation of airborne droplets. ULV pletely in water, they do not need constant agitation nor
insecticides are applied as mists or aerosols in space are they known to abrade equipment.
applications. By definition, ULV treatment is an appli- Granules (GR) are inert carriers impregnated or
cation technique in which less than 5 l/ha of liquid coated with the solution concentrate of a technical
insecticide is applied. This method of operation has product. They are made by applying a liquid formula-
resulted in substantial savings through speed and reduc- tion of an active ingredient to coarse particles of an
tion in labor requirements, but demands very accurate absorptive material such as attapulgite, clay, or corn
application, since the droplet size of ULV formulation is cobs, or to a nonsorbent material such as sand or other
of considerable importance. mineral or nonmineral substance. Even frozen water in
the form of ice cubes, may be used as a carrier for
Droplet size affects: some materials such as microbial agents, and has been
(a) The chances of penetrating through vegetation and recently used successfully for aerial treatments of
other obstacles to reach the target flooded habitats (Becker 2003). Granular treatments
(b) The total number of droplets/unit volume of the can be made at any time of the day since they can be
product applied and the toxicity of the average applied aerially in winds up to 20 km/h without signifi-
droplet cant drift.
(c) The distribution of droplets on treated surfaces Vapourizing strips are special formulations of insec-
and ticides, mainly for household use, which are usually
(d) The time for which a droplet remains airborne, and made from polymeric materials containing a volatile
therefore its ability to drift downwind. compound. They release vapours that are lethal to the
insects when exposed to air or heat.
Both favorable and unfavourable results from using Aerosols: The active ingredients must be soluble in
ULV applications have been reported. Disparity in the volatile, pressurized petroleum solvent to which a
results obtained has been primarily due to weather con- propellant is added. Fluorocarbon propellant was used
ditions, application rate and the degree of penetration initially, but has now been largely replaced by the less
into the target area. As might be expected, applications detrimental propane/butane mixtures, or with carbon
at higher label rates together with good penetration of dioxide. When the petroleum solvent is atomized, it
dwellings have proved to be the best control of adult evaporates rapidly leaving the microdroplets of toxi-
vector populations (Gratz 1991). cant suspended in the air. Aerosols commonly produce
Water dispersible powders or Wettable powders droplets well below 10 µm in diameter. The push-­
(WDP/WP) are, as the name suggests, insoluble pow- button variety of aerosol dispenser was first developed
ders that resemble dust, but which may be dispersed in during World War II. More recently, total release aero-
water. The technical product can be either a solid or sols have been designed to discharge the entire con-
liquid. Liquid technical products and concentrates can tents in a single application and are available for home
be absorbed onto an inert solid, and then used as a owners as well as for commercial operators. They are
water dispersible powder. Solid formulations are effective primarily against flying insects and provide
ground to a fine powder and surface-active agents little residual effect.
added to promote dispersion of the particles without Tablets (usually water dispersible tablets WT) and
excessive foaming when they are added to water. Slow release systems blend an a.i with a material from
Wettable powders form a suspension rather than a which it will be released or evaporate at a controlled
solution when added to water, and need regular agita- rate in the course of time. Ingredients that are volatile
448 18 Chemical Control

or subject to degradation, e.g. by sunlight, remain Hand-operated compression sprayer: These sprayers
active much longer in these formulations. are designed to apply insecticides onto surfaces with
Microencapsulated products are a form of a slow- which the insect will come into contact, or into a breed-
release formulation in which the a.i. is enclosed in a ing site. The formulation and water are either mixed
material such as polyamide, neoprene, polyvinyl chlo- before filling the tank or mixed within it. The tank is
ride or polyester. The active ingredient can diffuse then pressurized by a hand-operated plunger. A trigger
from the matrix. Microcapsule suspensions (CS/MC) on the lance of the sprayer controls the release of the
are of two types: material through a nozzle. Filtering the water while
filling the sprayer, routine maintenance by qualified
(a) Porous wall capsules usually containing diazinon,
personnel and routine nozzle checks and calibration,
chlorpyrifos, permethrin, etc., through which the
are essential in maintaining the equipment’s effective-
a.i. is slowly released over time
ness (Wade 1997). Abrasion from particles in the water
(b) Nonporous capsules (e.g. fenitrothion), remain
can cause deterioration of the nozzle opening, resulting in
intact until ruptured or burst by tarsal contact with
an excessive increase in the control product applied,
insect vectors
which in turn may result in application of an incorrect
Encapsulated materials generally demonstrate a or uneven dosage rate. A drawback of the hand-oper-
reduced absolute mortality together with extended ated compression sprayer is that as the tank is emptied,
residuality (Wade 1997). To this date, the formulations pressure decreases causing a fall in the discharge rate,
offering the most lasting residual effect are those in unless the sprayer is provided with a pressure regula-
which the a.i. is present in microemulsion together tor. Many of the problems with these sprayers at the
with a surface film forming system “Secondary system treatment-sites are related to a lack of proper cleaning
EWs” (S-EW). at the end of each day.
Pellets and briquettes are larger in size than gran- Mist blowers (power-operated): These can either be
ules, varying in size from 1.5 cm in diameter for pel- portable or vehicle-mounted. Portable knapsack mist
lets (tablet-like shape) to several cm for briquettes. The blowers are powered by a two-stroke engine producing
size and weight of briquettes vary depending on the a high velocity air stream in which the insecticide for-
carrier and amount of other additives present. Both mulation is atomized as a fine mist. The output rate can
pellets and briquettes release the a.i. as they dissolve be adjusted through flow restrictors. At high flow-rates,
and disintegrate in mosquito-breeding habitats. large droplets are produced. Large droplets coat sur-
Extended residual briquettes (XR) are designed to faces, whereas the smaller droplets act as an aerosol
release effective levels of an a.i. over a longer period impacting insects in flight or at rest. Although the for-
into the environment. Release of the a.i. occurs by dis- mulation is diluted in water, the overall volumes
solution of the briquette. XR-briquettes are of a special applied with mist blowers are still relatively small.
value in permanent, hard-to-reach breeding sites, or in Knapsack mist blowers can cover a large area in a rela-
situations where a pre- or post flood treatment provides tively short time, and provide ease of access to areas
a long-term effect. where vehicle-mounted equipment cannot reach. The
disadvantage of the portable knapsack mist blowers is
the risk of burns from the engine, and discomfort
caused by heat, vibration, and noise.
18.2.3 Insecticide Application Techniques Aerosol generators (power-operated): These are
often referred to as cold aerosol or cold foggers, and
The success of an insecticide application programme are typically used to apply ULV adulticide treatments
depends very much on the quality and performance of with either technical insecticide (rarely), or formula-
the equipment used. Manuals on mosquito control tions diluted in oil or water. Only formulations recom-
refer to a wide range of application equipment for mended for ULV use by the manufacturer should be
delivering insecticide to the target-site. In this section, applied by this equipment. These machines can be
the more commonly used application equipment in hand-held or truck-mounted, depending on their size.
mosquito control is briefly described, according to The volume of material used per unit area is much
WHO/CTD/WHOPES (1997). lower than with thermal foggers or mist blowers.
18.3 Chemical Groups of Insecticides 449

Table 18.7 Insecticides suitable as cold aerosol sprays and for thermal fogs for mosquito control (WHO 2006)
Dosage of ai.b (g/ha) Toxicity: oral LD50 of ai.a
Insecticide Chemical Cold Thermal for rats (mg/kg body weight)
Chlorpyrifos OP 10–40 150–200 135
Cyfluthrin PY 1–2 - 500
Cypermethrin PY 1–3 - 7,180
Cyphenothrin PY 2–5 - 2,250–2,640
Deltamethrin PY 0.5–1.0 - >2,940c,d
D-phenothrin PY 5–10 - >10,000
Etofenprox PY 10–20 10–20 >40,000
Fenitrothion OP 250–300 270–300 503
Fenthion OP 150 - 330d
Malathion OP 112–693 500–600 >4,000
Naled OP 56–280 - 430
Permethrind PY 5–10 - >4,000b,c
Pirimiphos-methyl OP 230–330 180–200 2,018
Propoxur C 100 - 95
Zeta-cypermethrin PY 1–3 - 86
PY Synthetic pyrethroid; OP organophosphorus; C Carbamate
a
ai. active ingredient
b
Because of their low dermal toxicity and on the basis of experience with their use, these products have been classified
in the WHO Hazard Classification in Class III, Table 5 (WHO/PCS/94.2)
c
Dermal toxicity
d
Also used in mixtures with knock-down agents or synergists

By using ULV aerosol generators, a larger area can be insecticide formulation can be more difficult with air-
covered more quickly. Portable ULV aerosol genera- craft than with ground application equipment. However,
tors may also be used for indoor treatment, when currently available computerized technology now pro-
access is difficult with compression sprayers. With vides very accurate treatment of the target-area.
ULV aerosol generators, the calibration of the flow Insecticides, which have a rapid knock-down effect
rate and the uniformity of the droplet size is particu- on mosquitoes and are relatively harmless to other
larly important. organisms, are best suited for space treatments.
Thermal foggers (power-operated): These machines, Organophosphorous compounds first became widely
which are either portable or vehicle-mounted, are pre- used for such applications, and various formulations of
ferred by some vector control agencies where the dense carbamates and synthetic pyrethroids are now avail-
fog generated is perceived (mistakenly) as indicating able. According to the WHO operational manual on
high efficacy. In most parts of Europe, however, the the application of insecticides for control of mosquito
dense, visible fog may raise safety concerns among the vectors (2006a), there are 15 active ingredients suit-
public. The droplet size is far less controlled than with able for cold aerosol and thermal fogs applications
ULV machines, and a wide range of droplet sizes from (Table 18.7).
1–200 µm are produced. In such situations, some insec-
ticide will be wasted due to convection currents or early
fallout. Moreover, the heat from these thermal foggers 18.3 Chemical Groups of Insecticides
can be detrimental to the insecticide used.
Aerial application equipment: Large-scale and
emergency vector control programmes often employ 18.3.1 Chlorinated Hydrocarbons
aircraft to apply insecticides. The aircraft are well
suited for the rapid treatment of large areas where there The chlorinated hydrocarbons contain carbon, chlo-
is no access to the target-site, or when vegetation is rine, and hydrogen. They are also referred to by other
dense. Aerial treatment can be used for adulticiding and names: organochlorines, chlorinated organics, chlori-
larviciding applications. Accurate placement of the nated insecticides. The chlorinated hydrocarbons can
450 18 Chemical Control

be divided into subgroups according to structural 1947 (Busvine 1978); a problem which grew steadily,
differences, but they have in common high chemical sta- but so insidiously that it has attracted little attention
bility, low solubility in water, moderate solubility in except from those concerned with pest/vector con-
organic solvents, and a low vapour pressure (Hill and trol. On the other hand, in the 1960s, the problem of
Waller 1982). The stability and solubility of the chlori- environmental residues became front-page news. As
nated hydrocarbons means that they are highly persis- could be expected, there was a widespread official
tent, and this may lead to long-term contamination of reaction in the form of safety regulations. The result
the environment and gradual bio-accumulation in ani- was a virtual banning of organochlorines in many
mals at the higher end of the food chain. For these rea- countries.
sons they have been banned by most developed DDT still, however, remains an important com-
countries. The broad spectrum of activity of these ponent in malaria control in some rural areas or
compounds, their persistence and their hazard to the countries, where it is available and legal to use and
environment explain why their use in insect pest man- where the local vector species are still susceptible
agement is largely considered inappropriate, although (Chavasse and Yap 1997). Even so, the assessment
there are still situations where this group is still an of the efficacy/resistance to DDT in an area is essen-
important control option, e.g. in some malaria vector tial for planning an effective malaria control
control programmes in endemic countries. strategy.
DDT still continues to be a substantial part of
vector control programmes in a number of countries.
With the increase in IRS in many internationally and
DDT: 1,1,1-trichloro-2,2-di
nationally funded malaria control programmes and
(4-chlorophenyl)ethane
affirmation by WHO that DDT is appropriate for use
in the absence of longer-lasting insecticide formula-
Cl
tions in some endemic malaria settings, DDT has
Cl Cl
been reintroduced as a major malaria control inter-
vention in Africa (Coleman et al. 2008). A total of
10 countries from the African region reported the
use of DDT to control malaria vectors. An estimated
annual average of 547 tonnes of DDT was used
(2004–2007) to control malaria (Zaim and
Cl Cl Jambulingam 2007).
Resistance to DDT was first noted just 11 years
DDT is probably the best known and paradoxically, after its introduction (WHO 1957). Because DDT-
the most infamous chemical of the 20th century. It has resistant insects were usually fully susceptible to
been recognised as the most useful insecticide ever subsequent classes of insecticide, such as the organo-
developed. phosphates, carbamates and synthetic pyrethroids,
The great advantages of DDT include its persis- these classes of insecticides replaced DDT. Later on,
tence and its relative inexpensiveness to produce, so as resistance developed, many programmes made an
that it may be readily used on a large scale to protect attempt to revert back to DDT as the insecticide of
people living in disease endemic areas of the world. choice. However, because DDT and pyrethroids
Outstanding success was achieved by residual house- share a common target site in the sodium channel of
spraying against endophilic malaria vectors. Bruce- insects (Soderlund and Bloomquist 1989), cross-
Chwatt (1971) pointed out that DDT has saved some resistance had developed to both classes of insecti-
15 million lives by malaria control alone. cides in many locations due to a mutation in the
As is well known, some insecticides have caused target-site (kdr) (Martinez-Torres at al. 1998; Ranson
problems during the past few decades for two rea- et al. 2000).
sons: pest resistance and environmental pollution. The production and use of DDT are strictly
The first of these began with DDT-resistant flies in restricted by an international agreement (Stockholm
18.3 Chemical Groups of Insecticides 451

Convention on Persistent Organic Pollutants; www. of nerve-acting insecticides, indicating some differ-
pops.int/documents/convtex 2007). The Conven- ences in the mode of action. DDT disturbs the bal-
tion’s objective is to protect both human health and ance of sodium and potassium ions within the sensory
the environment from persistent organic pollutant neurons, thereby causing spontaneous firing, and pre-
substances, DDT being identified as one from the venting normal passage of impulses. This major
group. However, exemption was given for the pro- symptom of DDT poisoning, results from its ability
duction and public health use of DDT for IRS to to induce repetitive firing on sense organs, giant
control vector-borne diseases, mainly because of axons, presynaptic terminals, and smaller nerve
absence of equally effective and efficient alterna- fibers. Whether a given neuron fires repetitively or
tives. Among the 12 insecticides currently recom- not depends upon the membrane properties of the
mended for this intervention by WHO, DDT is the nerve cell itself, and on the elevation of the negative
one with the longest residual activity when applied after-potential, which contributes to the repetitive
on walls and ceilings (6–12 months, depending on discharge. The relative effectiveness of this after-
dosage and nature of substrate). There are strict con- potential in generating repetitive firing depends upon
ditions to be met when using DDT. Prerequisites for the properties of the sodium gate of the particular
safe and effective implementation of IRS include fiber. A further aspect of this process is that DDT
susceptibility status of vectors, proper monitoring interferes with the stabilizing action of Ca2+ at the
of insecticide resistance and all relevant information axonal surface, and therefore leads to membrane
reported to WHO (Zaim and Jambulingam 2007). destabilization. The disruption is transmitted to the
The overview of the recent global use of DDT is rest of the nervous system, causing the muscles to
given in Table 18.8. twitch, which is usually followed by convulsions and
death. DDT is a relatively slow acting insecticide,
and has the unusual quality of being more toxic to
18.3.1.1 Mode of Action
insects as the ambient temperature is reduced, a nega-
In insects, DDT produces tremors throughout the body tive correlation that is also characteristic of some
and hyperexcitability, subsequently followed by loss pyrethroids. Gammon (1978) showed that the chemi-
of movement (ataxia). Beyond this point, an apparent cal had excitatory effects on both peripheral and cen-
paralysis develops, which may be completed over sev- tral neurons and the effects on central neurons became
eral hours after application. more pronounced as the temperature was reduced.
Although the compound produces symptoms con- A few striking points concerning DDT should be
sistent with a toxic action on the nervous system, highlighted to understand some of the well documented
there are differences between DDT and other groups problems associated with it. One of the most remarkable

Table 18.8 Global use of DDT for vector control reported to WHOPES, in kg of active ingredient, WHO
African Region, 2003–2005, (Zaim and Jambulingam 2007)
WHO region Country 2003 2004 2005
African Eritrea NA 6,552 10,109
Ethiopia 272,243 255,163 275,195
Madagascar 45,000 30,000 0
Mauritius 872 899 625
Mozambique NA NA 307,688
Namibia 52,143 25,837 39,611
South Africa 53,610 62,112 65,575
Swaziland NA NA 7,538
Zambia NA 8,648 13,308
Zimbabwe NA NA 108,000
Total 10 countries 423,868 389,210 827,649
NA denotes data not available
452 18 Chemical Control

points of DDT is its chemical stability. This important 18.3.2.1 Mode of Action
property results in having a long half-life in the soil,
the aquatic environment, and in plant and animal tis- OPs exert their toxic action at synapses by inhibiting
sues. It is not readily broken down by microorgan- cholinesterase (ChE), an important enzyme in the ner-
isms, enzymes, heat or ultra violet light. Secondly, vous system. It is well established that as OPs inhibit
DDT has been reported in the literature to be probably acetylcholinesterase (AChE), the acetylcholine (ACh)
the most water-insoluble compound ever synthesized. concentration then rises in treated insects (reviewed by
However, it is soluble in lipids and, as a consequence Corbett 1974). OPs interact with AChE in the same
of its resistance to metabolism, it is readily stored in way as ACh does, phosphorylating the same serine
the fatty tissue of any animal ingesting it, either alone hydroxyl that ACh acetylates. OPs inhibit the enzyme
or dissolved in food, even when it is part of another almost irreversibly, with dephosphorylation occurring
animal. It accumulates in every predator, as well as in over a period measured in weeks or months, contrary
those that eat plants bearing traces of DDT. The prin- to some other chemical groups, such as carbamates,
cipal result of this movement in the food chain is where the action of decarbamilation occurs from min-
bioaccumulation. utes to less than 8 h (Taylor 1980). This has led some
The history of DDT’s development and usage shows to refer to OPs as irreversible inhibitors and carbam-
that there is a need for an informed and cautious ates as reversible ones. This inhibition, resulting in the
approach to pesticide usage. It is essential to conduct accumulation of acetylcholine, interferes with the neu-
basic research before we encourage widespread appli- romuscular junction, producing rapid twitching of
cation of any particular product, to enable us to iden- muscles and final paralysis of the insect. However, the
tify and restrict, if not to avoid those products that may precise sequence of events between enzyme inhibition
pose dangers to the environment and to health. and death is still not fully understood. The excess ace-
tylcholine has widespread harmful effects, which may
include the uncontrolled hormone release known to
accompany insect poisoning (Maddrell 1980).
18.3.2 Organophosphates Several insecticides which have been performing
an important role in mosquito control worldwide,
The chemically less stable OP insecticides partially belong to the group of OPs. Perhaps the most impor-
replaced the persistent chlorinated hydrocarbons. The tant one is malathion, which is also the oldest and most
term OP is usually used as a generic name to include widely used aliphatic OP.
all insecticides containing phosphorus. The OPs have
several other commonly used names: organic phospho-
rous, phosphorus insecticides, phosphorus esters or
phosphoric acid esters. They are all derived from phos- Malathion: 2-(dimethoxyphosphinothioylthio)
phoric acid. The OPs have two distinctive features, a butanedioic acid diethyl ester
lower chemical stability and they are generally much
more toxic to vertebrates than the organ-ochlorine
O
insecticides. Their lower persistence brought them into O
use as alternatives to persistent organochlorines, par- S O
ticularly to DDT. However, unfortunately, resistance O P
to OPs also developed, and became more widespread
as these compounds were more widely used. This situ- O S
ation led to a plea by WHO to encourage commercial
companies to continue the search for alternative com-
O
pounds suitable for pest control (WHO 1976).
However, in the recent report of WHO, (Zaim and
Jambulingan 2007) the OPs continue to be used in Malathion was introduced in 1950, for agriculture,
­vector control in the second half of the 20th and the urban pest control and mosquito control. Because of its
beginning of 21st century. fast action and exceptionally low acute toxicity to
18.3 Chemical Groups of Insecticides 453

humans and other warm blooded animals, it became (48.3–55.2 kPa) is required to consistently achieve the
the insecticide of choice. droplet size criteria on the Cythion label.
As a public health insecticide, malathion has found As the efficacy of ULV applications against mos-
its most common use as a ULV formulation to control quitoes is based on the premise of an airborne droplet
adult mosquitoes. Its low mammalian toxicity allows impinging on a flying mosquito, this method is often
the application of the compound in urban areas where ineffective against indoor resting species, due to the
dense mosquito populations are a nuisance or threaten decreased number of droplets reaching individual tar-
human health. Many of the ULV applications of mala- get mosquitoes. In such situations, ULV adulticiding is
thion are carried out by aircraft or helicopters. Aerial not recommended due to the behaviour pattern of the
ULV malathion applications are still effective at a rate species.
of 320 g/ha, in regions where resistance to OPs has The broad-spectrum, nontarget activity of malathion
not yet developed. The application equipment has to makes this compound undesirable in most natural
be calibrated to dispense droplets small enough to environments.
remain suspended in the air, but large enough to con-
tain a sufficient amount of insecticide to kill an adult
mosquito. Results of aerial ULV treatments world- Naled: 1,2-dibromo-2,2-dichloroethyl
wide show that success of ULV applications depend dimethyl phosphate
greatly on weather conditions. Above all, the wind
speed has to be less than 3 m/s, and the time of appli- Br O
cation preferably dusk, which coincides with the
activity of the species being controlled. The presence Br P
of inversion conditions, are also important in maxi- O O
mising efficacy of the application. Cl O
Malathion is also applied by ULV ground equip- Cl

ment. A maximum vehicle speed of 16 km/h for such

treatments often limits the area that can be treated dur- Naled (Dibrom) has been a widely used brominated
ing the period of mosquito activity. Any increase in the aliphatic OP with low mammalian toxicity. Naled
speed of the vehicle should only take place if the insec- was one of the choices for adult mosquito control
ticide output is also increased correspondingly. throughout the United States, but has been with-
Fortunately, most truck-mounted cold aerosol genera- drawn from further use (Mulla 1994). In the
tors used for ULV applications are also equipped with Americas, it was also widely applied in large mos-
variable flow-control systems. These systems, when quito-breeding areas by ULV or conventional appli-
properly calibrated, automatically adjust to dispense cations. Mount et al. (1968) reported moderate
the correct amount of insecticide relative to the vehicle efficacy of Naled with caged Oc. taeniorhynchus
speed. The effect of operating pressure on the droplet when ULV treatments were applied at a dosage of
volume median diameter (VMD) at various flow rates approximately 9.0 ml a.i./ha. The results presented
for malathion ULV applications is well documented. by Linley et al. (1988) showed that ULV treatments
Nevertheless, for any particular situation the aerosol with Naled did not effectively control Oc. taenio-
droplets have to be collected, counted, and measured rhynchus. In Florida, ULV treatments with Naled
using an appropriate procedure: collect droplets on with vehicle-mounted equipment were used by many
Teflon coated plates, count them using a compound mosquito control districts, but also had some impact
microscope at a magnification 200×, take into consider- on Culicoides spp. (Ceratopogonidae).
ation the insecticide spread factor (for malathion 0.69) Howard and Oliver, (1997) based on 11 years’
and analyze the data. Dukes et al. (1990) determined analysis (1984–1994) of data from New York swamp
that an increase in the flow rate required a corresponding habitats of the primary enzootic vector (Cs. melanura)
increase in the blower pressure, to maintain the labeled of eastern equine encephalitis (EEE), showed the effect
malathion (Cythion) droplet median diameter of 17 mm. of Naled treatments on the vector population. Naled
For a flow rate of 254.3 ml/min, at the maximum treatments accomplished only short-term reductions in
vehicle speed of 32 km/h, a machine pressure of 7–8 psi the mosquito abundance. Despite repeated applications,
454 18 Chemical Control

populations of Cs. melanura increased 15-fold in DDVP is also an aliphatic OP with a very high vapour
some parts of the treated area, which discredits the pressure, giving it strong fumigant qualities. Apart
suggestion that Naled applications could reduce the from being known as an a.i. used in vapourizing strips,
risk of EEE. from which it is slowly released, DDVP also serves as
Hurricanes and tropical storms often have a signifi- an effective mosquito adulticide applied in a mixture
cant impact on mosquito-borne diseases because they with kerosene or diesel (Vapona 7 or Nuvan 7) by ther-
result in an increase in mosquito-breeding habitats mal fog generators. Thermal fogs using dichlorvos can
caused by flooding. In the USA, when mosquito abun- achieve an immediate and high level of reduction of
dance and potential disease emergence are imminent, adult outdoor mosquitoes. The disadvantage of such
aerial applications of Naled are implemented, as in the treatments is generally low persistence, and therefore
post-hurricane Rita situation when Air Force Aerial DDVP treatments must be repeated at fairly short
Application Flight took action in four Texas counties. intervals to ensure continued suppression of adult mos-
A significant (90%) decline in mosquito abundance quito populations. Since the mammalian toxicity of the
was observed as determined by post treatment evalua- product is very high (oral LD50 for rats is 56 mg/kg),
tion (Breidenbaugh et al. 2008). In 2004, Florida expe- DDVP is in WHO toxicity class 1b, and its use has
rienced an extraordinary hurricane season with four been discontinued in most European countries. The
major hurricanes traversing the state within 3 months. other disadvantage is its very poor selectivity to the
Because of the potential threat of arboviral diseases, entomofauna. Its only advantage is the speed of action
including West Nile virus (WNV) and EEE, ULV aer- as an adulticide, an advantage in epidemic situations.
ial applications with Naled were initiated. Although
Naled has been associated with adverse human health
effects following ULV aerial applications (CDC 2003), Fenitrothion: Dimethoxy-(3-methyl-4-
the extent to which humans are exposed to Naled dur- nitrophenoxy)-thioxophosphorane
ing large-scale aerial applications has yet to be accu-
rately quantified. To estimate the potential health risk, O
CDC and Florida Department of Health assessed
N+
human exposure to ULV aerial application of Naled. –O S
The data suggest that aerial applications of Naled do
not result in increased levels accumulated in humans, P
provided that the product is used according to label O O
instructions (Duprey et al. 2008). In large-scale mos- O
quito control programmes, Naled is typically applied
via aircraft with the inert carrier, naphtha. For effective
mosquito control, the maximum rate for ULV surface Fenitrothion is a phenyl derivate of OPs (with a ben-
and aerial applications is typically c. 200 ml/ha. These zene ring), and this moiety is critical in improving sta-
ULV applications produce very fine droplets that stay bility compared with the aliphatic OPs. Fenitrothion
aloft and kill mosquitoes on contact. ULV applications under various trade names (Acothion EC 20,
are utilized to minimize exposure and risks to people, Fenitrothion 20 EC, etc.) has been extensively used in
wildlife, and the environment, (U.S. EPA, 2002). Europe, especially as a larvicide in closed water sys-
tems (sewage and waste-water containers). However, in
France it has produced resistance in Aedes/Ochlerotatus
Dichlorvos (DDVP): 2,2-dichlorovinyl dimethyl and Culex species and also in extensively irrigated
phosphate crops in Spain, where resistant strains of An. atropar-
vus and Cx. theileri have developed (Grandes and
Sagrado 1988). Studies conducted by Wesson (1990)
O
have demonstrated that the larvae of 26 strains of Ae.
Cl P albopictus [St. albopicta] from the United States,
O O Brazil, southeast Asia, and Japan, showed different
O levels of susceptibility to fenitrothion when it was
Cl applied at the baseline susceptibility concentration of
18.3 Chemical Groups of Insecticides 455

0.02 mg a.i./l. Rodríguez et al. (2007) showed that when Directive 91/414/CE, based on possible risks to birds.
Ae. aegypti from Cuba, with a high level of temephos In general, uses of fenthion were withdrawn by the
resistance, was subjected to temephos selection to eval- EU in 2005. Concerns over the potential adverse
uate the potential of this OP for mosquito control, after effects of fenthion on estuarine biota appear to be
six generations of selection, little or no cross-resistance unclear, although there were records of fenthion acute
was observed to the OPs, malathion and fenitrothion. LC50 figures for mosquitoes, which exceeded those for
Insecticidal properties of fenitrothion microcap- some mysids and pink shrimp. The degree to which
sules (CS) as a residual formulation were studied on the risk might be apparent for nontarget estuarine
An. albimanus females (Kawada et al. 1995). communities depends on various factors such as mix-
Residual efficacy of the microencapsualted formula- ing and dilution of the product, characteristics of local
tion at the rate of 1 g/m2 was almost equivalent to habitats, weather conditions, and potential for cumu-
that of WP at the rate of 2 g/m2 on a plywood surface lative effects of repeated applications during a season
and was superior to that on an unglazed pottery sur- (Clark et al. 1987).
face. Greater than 50% mortality was maintained for Wesson (1990) showed in a larval bioassay that fen-
>28 weeks after treatment by fenitrothion CS on a mud thion can be successfully used in controlling Ae.
surface with 10 min contact at the rate of 2 g/m2. albopictus at a rate of 0.02 mg a.i./l. This rate was
Microcapsule particles were observed to be mechan- effective in suppressing 25 out of 26 tested strains of
ically broken (trampled) by mosquito contact and the this species. The LC95 values for the remaining strain
amount of fenitrothion released from the CS increased (originating from the US) showed a 4-fold higher tol-
as contact time increased. erance compared to susceptible strains.
Fenthion is sold under various trade names such as
Baytex, Lebaycid, and Queletox. The most important
formulation types are EC and WP. The products are
Fenthion: Dimethoxy-[3-methyl-4-(methylthio) mostly registered and sold in the Middle and Far East
phenoxy]-thioxophosphorane and Africa.

S
S
Diazinon: Diethoxy-[(2-isopropyl-6-methyl-4-
pyrimidinyl)oxy]-thioxophosphorane
P
O O
O

Fenthion is another phenyl derivate with contact and N N S

stomach action and broad-spectrum activity against
sucking and biting pests. In addition to agriculture, fen- P
O O
thion also has uses in veterinary applications and in
O
public health vector control.
The product was commonly applied peri-focally dur-
ing the Ae. aegypti eradication campaign in the Americas.
Fenthion is used as a component in an overall mosquito
control programme in some regions of Florida. Diazinon was probably the first heterocyclic OP deri-
The U.S. EPA concluded that fenthion applications, vate from this group. The heterocyclics have gener-
especially when repeated at frequent intervals, may ally longer-lasting residues than many of the aliphatic
cause mortality in a variety of bird species, including or phenyl derivates. Diazinon was first available in
raptors feeding on exposed birds (EPA 2001). 1952 and is sold under a variety of brand names,
The European Commission (EU 2004) concluded including DZN and Knox Out 2FM. The product is
that fenthion cannot be included in Annex I to chemically related to malathion and chlorpyrifos.
456 18 Chemical Control

Diazinon has agricultural, commercial, and house- However, in 1974, control failures in these habitats
hold uses, but household uses predominate. It has been were observed (Georghiou et al. 1975). Susceptibility
commonly used as a residual fly spray and as an adul- tests conducted by Wesson (1990), showed that some
ticide against indoor mosquitoes. It has a relatively low of the 26 Ae. albopictus (St. albobicta) strains (from
mammalian toxicity, and has a very good record for Brazil and southeast Asia) exposed at a concentration
urban pest control, largely because it is effective against of 0.01 mg a.i./l, displayed tolerance to this insecti-
a wide range of household insect pests. cide. However, the majority of strains tested were still
Inside living organisms, diazinon is transformed susceptible to the chlorpyrifos concentration used.
into a molecule called diazoxon. Diazinon, and the Chlorpyrifos in various formulations has provided
more potent diazoxon kill insects by interfering with very good control and long persistence in a variety of
nervous system function. Not all of diazinon’s toxico- container types (Glancoy et al. 1968). Its mammalian
logical effects stem from its inhibition of AChE. toxicity would exclude it from use in potable water
Diazinon and other OPs inhibit numerous enzymes containers, but it is a useful product in larval habitats
with molecular structures that are similar to AChE. such as flower vases at cemeteries, and in small waste-
According to EPA, “Organophosphates are efficiently water containers. Chlorpyrifos has also been used for
absorbed by inhalation, ingestion, and skin penetra- ULV treatments in the US.
tion,” Exposure by “multiple routes can lead to seri- The use of this compound in open-water systems
ous additive toxicity.” EPA (April 2000) estimated inhabited by fish is not recommended because of
exposure via multiple routes following both lawn care toxicity to fish.
application of liquid formulations and crack-and-
crevice indoor applications as exceeding “level of
concern.” For exposures following residential applica- Pirimiphos methyl: 0, [2-(diethylamino)-
tions, a single application can lead to exposure via all 6-methyl-4-pyrimidinyl] 0,0-dimethyl
three routes. phosphorothioate

Chlorpyrifos: O,O-diethyl O-3,5,6-trichloro-2-pyridyl N

phosphorothioate

N N S
Cl Cl
S
P
O O
P
O
O O N Cl
O

Pirimiphos methyl, also a heterocyclic OP, (trade name

Actellic), became the insecticide of choice in some
endemic malarial regions after resistance was recorded
Chlorpyrifos is a heterocyclic OP and as the a.i. in the in Anopheline species to some other OPs, carbamates
formulation Dursban E 48, has been used as a larvicide and to some synthetic pyrethroids. Resistance of
to control Aedes/Ochlerotatus, Anopheles and Culex An. sacharovi in Turkey to phoxim, chlorpyrifos,
species in many countries in the tropics, North America propoxur, and tolerance to malathion, was reported by
and Europe. However, resistance appeared quickly when Ramsdale (1975) and Davidson (1982). However, surface
it was applied frequently in Culex habitats in southern treatment of pirimiphos-methyl 50% EC at 0.9 g/m2
France (Sinegre et al. 1984). In California, Schaefer caused a significant decrease in parous rate and 96.9%
and Dupras (1970) demonstrated that application of reduction in resting density. The persistence on different
chlorpyrifos resulted in a fairly long-term control of surface materials for 7 weeks post application resulted
mosquito larvae in polluted water sources. Mosquito in mortality rates of 73–98% (Kasap et al. 1992). For
abatement districts used chlorpyrifos to treat waste-water. residual mosquito control, pirimiphos methyl may be
18.3 Chemical Groups of Insecticides 457

used at rates of up to 2 g a.i./m2. The optimum volume A reduction of adult density by up to 95.4% was
will vary with the type of surface encountered. achieved when temephos was applied in 1% sand gran-
Mosquito larvae in shallow water (~10 cm deep) may ule formulation to water-bodies containing larvae of
be controlled with 1 part of pirimiphos-methyl 50% Ae. aegypti in Thailand. When temephos EC was
EC mixed with 99 parts of water (0.5%) and applied at applied in India and Burkina Faso, the period of larval
a volume of 100 l/ha (10 ml/m2). At rates of 0.5–0.1% control following a single application, lasted up to 8
a.i., depending on the water depth, suppression of weeks (Geevarghese et al. 1977; Hervy and Karnbou
mosquito larvae, with retreatments after 5–8 days, can 1978).
be achieved. Resistance to temephos has appeared in some
areas following intensive use of the compound. It
was reported by Sinegre (1984) in parts of France, in
Temephos: [4-(4-dimethoxyphosphinothioyloxyphenyl)
agricultural zones of Spain by Grandes and Sagrado
sulfanylphenoxy]-dimethoxy-sulfanylidene-
(1988), in the Dominican Republic by Mekuria et al.
phosphorane
(1991) and recently in India, Baruah (2004).
An increased level of tolerance elsewhere, such as
S
S S in the Caribbean islands (Georghiou et al. 1987) and
French Polynesia, has been reported, but it is assumed
P P that the level of temephos resistance is not high enough
O O O O
O O to disrupt its operational use. Wesson (1990) examined
the OP larval susceptibility of 26 Ae. albopictus strains.
Three U.S. strains and one Japanese strain had LC95
Temephos is a heterocyclic OP, available under the values at or above the diagnostic concentration, which
trade name Abate. It has been used as a mosquito for temephos was 0.04 mg a.i./l. The tolerance level of
larvicide for a longer period of time than most other one strain from the Americas increased 3-fold. All
products. Due to its very low mammalian toxicity, Brazilian and Southeast Asian strains had LC95 values
with an LD50 of 2,030 mg/kg (WHO class III N), it is below the diagnostic concentration. Following reports
used in various aquatic habitats, including water by several authors, Breaud (1993) reviewed mosquito
intended for human consumption. The only insecti- resistance to temephos in Florida. The most abundant
cide compounds that have been toxicologically Culex and Aedes/Ochlerotatus species already showed
approved as safe for use in potable waters are teme- tolerance to temephos in 1979 (6× and 39×), with a
phos, permethrin, methoprene, and products based tendency to develop resistance to other larvicides and
on B. thuringiensis israelensis (WHO 1991; WHO adulticides from the OP group in the region. In labora-
IPCS 1992). The disadvantage of temephos is a dis- tory studies using temephos and fenthion, two com-
agreeable smell. monly used larvicides under the Urban Malaria Scheme
Temephos has a different profile from other larvi- in India showed that the LC50 and LC90 values for teme-
cides (IGRs and microbials) used in the control of phos against Ae. aegypti were 0.0177 and 0.0559, for
mosquito larvae, in that it is effective against all larval An. stephensi 0.0148 and 0.0472, Cx. quinquefasciatus
instars of Aedes/Ochlerotatus, Culex and Anopheles. 0.0157 and 0.0480, and for Cx. vishnui group of mos-
However, it also affected populations of Podura aqua­ quitoes 0.043 and 0.0118 ppm, respectively. The results
tica (Collembola) and immature stages of Odonata, obtained, revealed that there is a 62.8 and 94.12 times
Ephemeroptera, Coleoptera, and Diptera: Chironomidae increase in the LC50 and LC90 of Cx. quinquefasciatus,
(Zgomba et al. 1983; Zgomba 1987). which indicates that the species has developed resis-
Sand granule formulations containing 1–5% a.i. tance to temephos. The 6.32 and 8.34-fold increase in
have been successfully used as larvicides in a wide Ae. aegypti and 2.27 and 2.34-fold increase in LC50 and
range of flood-water situations controlling Aedes/ LC90 values of An. stephensi are indicative of develop-
Ochlerotatus. The application rate depends on water ment of tolerance against temephos. Reports from
quality and ranges from 10 to 20 kg/ha for 1% teme- South America demonstrate (Seccacini et al. 2008)
phos. It can be applied by hand, by ground equipment, that acquired resistance by Ae. aegypti to the product is
from a boat or by helicopter and fixed-wing aircraft. widespread.
458 18 Chemical Control

Thavara et al. (2005) tested the efficacy of teme- 18.3.3.1 Mode of action
phos 1% GR at 1 and 10 g/200 l water in jars (0.05 and
0.5 mg a.i./l). Their results showed that even at 1 g/200 l The mode of action of carbamates is basically the same
water, which is 1/20 of the recommended dosage used as that of OPs. They affect the activity of AChE, which
in the control programme, the level of control was catalyzes the hydrolysis of ACh, the chemical neu-
about 100% for up to 20 weeks or longer. rotransmitter, which acts at synapses in the nervous
Temephos has been used for the control of Ae. system of the insect. Following the inhibition of the
aegypti in Thailand for over 30 years. The current enzyme caused by carbamylation, ACh accumulates
dosage used in the Ae. aegypti control programme in thus prolonging the action of the neurotransmitter at
Thailand is 10 g of 1% sand granules/100 l water in the cholinergic synapses. The resulting hyperexcita-
water-storage containers. Thavara et al. (2005) tion of the nervous system is accompanied by convul-
showed that the magnitude of release-profile and sions, paralysis and ultimately leads to death of the
efficacy of temephos 1% GR (sand granules) against insect (Eldefrawi 1985). However, in the case of car-
Ae. aegypti larvae in water-storage containers was bamates, the enzyme inhibition is more easily reversed
adequate in the initial period of 2–3 weeks after than with OPs and the insects can recover at lower dos-
treatment. Following this period, the efficacy of the ages (Dent 1991).
granules increased substantially where 92–100% Carbamates have a broad spectrum of activity
inhibition of emergence even at the lowest dosage of and usually act by contact or stomach action. They
1 g/100 l (0.05 mg/l a.i.) was obtained for an addi- have been used effectively against vectors that have
tional 5 weeks. Based on this evidence, it is desir- developed resistance to the organochlorines and
able to study the efficacy of lower dosages of OPs.
temephos than those currently used in Ae. aegypti
control. It was also suggested (Mulla et al. 2004)
that the use of controlled-release formulations or Propoxur: 2-isopropoxyphenyl N-methylcarbamate
sachets that are retrievable during cleaning and
washing could be more practical, desirable and cost-
O
effective. In those many tropical and sub-tropical
countries where DF and DHF are considered the
most important vector-borne diseases of public O N
health importance, (Gubler et al. 1998), Ae. aegypti H
and Ae. albopictus play a crucial role in their trans- O
mission. At present, the only effective method is to
combat the vector mosquitoes, primarily using
insecticides. Controlling or preventing DF and DHF
is therefore still heavily dependent on the use of
insecticides, although insecticide resistance devel-
opment represents a threat. One of the most commonly used products containing
propoxur, as a contact and stomach poison, is Baygon.
Endophilic mosquitoes can be effectively suppressed
by residual treatments of walls and ceilings of human
18.3.3 Carbamates dwellings with propoxur WP. The residual application
using a knapsack sprayer will typically provide 3
Carbamates are derivates of carbamic acid, and were months of control. For outdoor area treatments to con-
first introduced in 1951 by the Geigy Chemical trol mosquitoes by ground or aerial ULV application,
Company in Switzerland. However, early compounds Baygon ULV 120 may also be used. Ground treatments
lacked stability, and it was not until the discovery of with propoxur ULV may be carried out with undiluted
the highly active N-methyl carbamates that this group material at a flow rate of 250 ml/min, and a vehicle
was developed, and became an important group of speed of 8 km/h, or with a correspondingly increased
insecticides. amount at higher speeds.
18.3 Chemical Groups of Insecticides 459

To examine the potential for synergism between could be controlled by selective applications at a rate
carbamate and pyrethroid insecticides, Corbel et al. of 40 ml/m2 and a dosage of 400 mg a.i./m2.
(2003) tested permethrin and propoxur as representa-
tives of these two classes of compounds. Larvicidal
activity of both insecticides was assessed separately
and together on a susceptible strain of Cx. quinque- 18.3.4 Pyrethroids
fasciatus. When mixed at a constant ratio (permethrin
: propoxur 1:60 based on LC50), significant synergy Pyrethroids are a new class of highly active synthetic
occurred between them. Synergistic effects were insecticides. They emerged from prolonged efforts to
attributed to the complementary modes of action by improve the biological activity and chemical stability
these two insecticide classes acting on different com- of the natural pyrethrins, long known for their insecti-
ponents of nerve impulse transmission. Apart from cidal effects. Natural pyrethrins consist of a mixture of
raising new possibilities for Culex control, it seems insecticidal esters, extracted from the flower heads of
appropriate to consider using such mixtures or com- Chrysanthemum spp.
binations for insecticide-treated mosquito nets in sit- Commercial production of “Dalmatian insect pow-
uations with insecticide-resistant Anopheles malaria der” ground from flowers of C. cinerariaefolium
vectors. started in Dalmatia, and was widely used by 1840
(Casida 1980). Flower production then moved to
California, and at the beginning of the twentieth cen-
tury, cultivation started in Japan, well known for its
Bendiocarb: 2,2-Dimethyl-1,3-benzodioxol-4-yl) long existing chrysanthemum horticulture tradition.
N-methylcarbamate However, between 1935 and 1940, the extract from
pyrethrum flowers grown in Kenya replaced the
O Japanese product, because it contained a higher con-
centration of pyrethrins. Since the development of
pressurized aerosol containers in 1941 for the delivery
N O
H of pyrethrum, the product could be applied in droplets
smaller than 30 mm, which increased the efficacy and
O
cost-effectiveness of the pyrethrins. Because of its low
mammalian toxicity, pyrethrins is commonly used for
the control of house flies, mosquitoes, and other indoor
O
pests. Pyrethrum extract is also commonly incorpo-
rated into burning coils, the smoke of which repels,
Bendiocarb has been widely used as a residual house- knocks-down, or kills mosquitoes within homes
hold insecticide (Ficam 80 WP) by pest control opera- (Baillie and Wright 1985).
tors against cockroaches and flies, and in public health The effectiveness of pyrethrins was first enhanced
adult mosquito control, both as a residual spray and for by the addition of synergists such as piperonyl butox-
ground or aerial ULV applications. ide (PBO) in 1949. Synergists are not insecticidal by
Evans (1993) showed that deposits of bendiocarb themselves, but increase the potency of pyrethrum
caused very low irritation of mosquitoes without formulations by inhibiting their biodegradation
repellency, which makes it suitable for use where (Yamamoto 1973).
residual insecticides are selectively applied to the Synthetic pyrethroids, which are more stable than
mosquito resting-sites within buildings. Selective pyrethrins, have partially replaced or supplemented the
treatments are sometimes used in house spraying for use of the three other major classes of insecticides in
vector control, in order to reduce insecticide use. several areas of pest/vector control. An active area of
Arredondo-Jimenez et al. (1992) reported that selec- pyrethroid use is in the control of various vectors and
tive applications of bendiocarb were equally effective nuisance mosquitoes. Besides causing a knock-down
for control of An. albimanus in Mexico. Asinas et al. effect, pyrethroids may also have a repellent or anti-
(1994) showed that in the Philippines, An. flavirostris feeding action.
460 18 Chemical Control

There is evidence that pyrethroids can also be effec- many characteristics with DDT; one intriguing
tively applied as mosquito larvicides. This potentially feature is that they become more toxic to insects as
allows application of permethrin as a larvicide in an the temperature is lowered (a negative temperature
IMM programme, because permethrin has an approval coefficient).
for use in drinking water at a concentration of 15 mg/l Commercially available natural pyrethrins and their
(WHO 1991). However, the use of pyrethroids in water “first generation” synthetic analogs, such as allethrin
bodies inhabited by fish is not recommended due to and resmethrin, are broken down by UV light, as in
toxicity to fish. sunlight. Hence there is an advantage of application at
A large number of pyrethroid compounds have been night. The second group of these potent insecticides is
synthesized during the last few decades, some of which a wide range of “second generation” photostable ana-
are exceptionally potent. As a result, research aimed at logs, such as permethrin and cypermethrin.
producing new insecticidal compounds has involved Pyrethroids are also commonly mixed with the syn-
not only chemical substitution within molecules of ergist piperonyl butoxide (PBO), which slows down
interest, but also resolution and purification of the most the metabolic degradation of the active ingredients.
active isomers. The widespread distribution of insecti- Pyrethroids, as broad-spectrum insecticides, are
cide-impregnated mosquito nets is a major component also toxic to beneficial insects, including honeybees
of the WHO global strategy for malaria control, espe- and predators of common pests. Fish toxicity is of par-
cially in sub-Saharan Africa, where more than 90% of ticular concern in view of the potential use of pyre-
the world’s malaria cases are reported annually (Lines throids in aquatic habitats for the control of mosquito
1996). To date, six pyrethroids – the only group of larvae, against which pyrethroids have demonstrated
insecticides currently considered suitable for impreg- excellent activity (Mulla et al. 1978). Selective control
nation of mosquito nets – have been evaluated and rec- of mosquito larvae without affecting fish can nonethe-
ommended (WHO/CDC/WHOPES/2001.2) for this less be achieved by using the correct dosage.
purpose. They are: alpha-cypermethrin, cyfluthrin, del- Application rates of 2 ppb deltamethrin or 45 ppb per-
tamethrin and lambdacyhalothrin (alpha-cyano pyre- methrin had no effects on reproduction of mosquito
throids), and etofenprox and permethrin (non cyano fish, while mosquito larvae were effectively eliminated
pyrethroids). (Mulla et al. 1981).
Beside malaria prevention, protection against nui- Pyrethroids now have many uses in addition to con-
sance insects, especially Cx. quinquefasciatus, which ventional surface or space treatments. For example,
keep people awake at night, is also an important motiva- pyrethroid aerosols are now widely used in aircraft, to
tion for the use of mosquito nets. However, pyrethroid prevent the transfer of mosquitoes from areas in which
resistance in this species is already widespread in the mosquito-borne disease is endemic, to unaffected
tropical world, including Africa. areas. This usage is carried out under the International
Health Regulations. Pyrethroids are also widely used
to treat clothing, to prevent mosquitoes and other
18.3.4.1 Mode of action blood-feeding arthropods from alighting. Bednets are
also very widely treated with pyrethroids, to deter bit-
Considerable progress in the synthesis of these materials ing by nuisance and disease vector mosquitoes. A very
has been made, since the mode of action of pyrethroids wide range of domestic insecticide products, including
has become better understood (reviewed by Elliott aerosols, coils, and vapourizing devices, also contain
1980). Pyrethroids are neurotoxic to insects, and fly- various pyrethroid active ingredients.
ing insects are in general, rapidly knocked-down.
The lethal activity of pyrethroids seems to involve
action on both peripheral and central neurons, while
the knock-down effect is most probably produced by 18.3.4.2 Resistance
peripheral intoxication.
The close similarity in action between pyrethroids By 1992, pyrethroid resistance had already been
and DDT is an interesting phenomenon, which is detected in at least 40 arthropod species, and this
still far from being understood. Pyrethroids share number will have increased considerably since then
18.3 Chemical Groups of Insecticides 461

(Georghiou, 1992). Cross-resistance or multiple-resis- the behavioural response of the target mosquito spe-
tance generated by DDT and pyrethroids is the main cies, and the pyrethroid resistance status in the area.
mechanism by which this resistance has arisen.
Resistance to pyrethroids was exhibited first by those
insects that were already resistant to DDT, e.g. house
Alpha-cypermethrin: (S)-a-cyano-3-
flies, (Busvine 1951; Sawicki 1978) and some mos-
phenoxybenzyl-(1R,3R)-3-(2,2-dichlorovinyl)-2,2
quito species (Cx. tarsalis, Ae. aegypti and two
dimethylcyclopropanecarboxylate and (R)-a-­cyano-
Anopheles spp.) as reported by Prasittisuk and Busvine
3-phenoxybenzyl-(1 S,3 S)-3-(2,2-dichlorovinyl)-2,2
(1977) and Plapp and Hoyer (1968).
dimethylcyclopropanecarboxylate
Much information on pyrethroid resistance has been
derived from studies on the house fly. The most impor-
tant of several pyrethroid-resistance mechanisms is
knock-down (kd) resistance, a mechanism which
O O
results in broad resistance to pyrethroids, DDT, and
DDT analogs. Kd resistance induced by DDT con-
fers inherent cross-resistance against the knock-down
O
effect of pyrethroids, and vice versa. Developing resis-
tance against pyrethroids may curtail the otherwise
promising prospects for the use of these compounds as Cl
N
pest and vector control agents.
Cl
Pyrethroid resistance of malaria vectors has already
developed in several malarious countries and is increas-
ingly common in Africa (Hargreaves 2000), and the Alpha-cypermethrin is a nonsystemic, broad-spectrum
absence of a suitable alternative insecticide class for pyrethroid with rapid knock-down activity. It is
impregnation of mosquito nets may undermine the effective upon contact and through ingestion against
gains in malaria control and personal protection being target pests at relatively low application rates. As other
made through improved coverage with treated nets. members of the chemical group, it acts by preventing
The efficacy of a pyrethroid used for impregnation transmission of nerve impulses, by blocking the passage
of mosquito nets is the result of the insecticide’s intrin- of sodium ions through channels in nerve membranes,
sic activity and the behaviour of the target mosquito in thus preventing signals passing down axons. Typically,
response to it. This is of particular relevance for fast- this intoxication results in a rapid “knock-down” (kd)
acting insecticides, such as pyrethroids and DDT with and mortality.
knock-down and irritant properties. The intrinsic activ- It is used to control a wide range of chewing and
ity can be tested with adult mosquitoes using WHO sucking insects. In public health, it is used to control
cones. However, natural avoidance behaviour, blood- cockroaches, mosquitoes, flies, and other insect
feeding inhibition and mortality can be obtained only pests. It is also used in animal health as an ectopara-
in field conditions. siticide. The International Programme on Chemical
Recent field studies in pyrethroid-resistant areas of Safety (IPCS) initially made a full evaluation of
Côte d’Ivoire, in experimental huts N’Guessan (2001) cypermethrin in 1989 and later a full evaluation of
and on a larger scale (Dossou-Yovo 2000), indicated alpha-cypermethrin in 1992. IPCS concluded that
that pyrethroid-impregnated mosquito nets reduce when applied according to good agricultural prac-
malaria transmission despite a high frequency of the tice, exposure of the general population to alpha-
knock-down resistance (kdr) gene. WHO recom- cypermethrin is low and is unlikely to present any
mended that this should be confirmed in other studies, hazards. With good work practices, hygiene mea-
especially where pyrethroid-resistance mechanisms sures, and safety precautions, the use of alpha-cyper-
other than the kdr gene may be involved. methrin is unlikely to present a hazard to those
When selecting pyrethroids for mosquito control occupationally exposed to it.
and personal protection, specific attention should be Evaluations of alpha-cypermethrin by the FAO/
given to the various properties of these insecticides, WHO and Joint FAO/WHO Expert Committee on Food
462 18 Chemical Control

Additives JECFA (2003) are in agreement with those (Ritchie 2005). Bifenthrin is chosen because of its low
of IPCS. A review concluded that alpha-cypermethrin mammalian toxicity, strong substrate-binding properties
fulfils the safety requirements and that residues arising (Lee et al. 2004), and low irritancy against mosquitoes
from the proposed uses with good plant protection compared with other insecticides (Hougard et al. 2002),
practice, should have no harmful effects on human or including deltamethrin.
animal health (EU 2004). Successful dengue control in north Queensland
The main formulations available for use in public was achieved using LOs in combination with
health applications (primarily IRS), are WP and SC source reduction and interior pyrethroid applica-
(SC is also used for bed net treatment). The EC formu- tion (Ritchie 2005). The findings reported here,
lation is also used to control ectoparasites on animals. affirm the use of bifenthrin-treated LOs, but also dem-
These formulations are registered and sold in Europe, onstrate that competition with alternative breeding
South America, Africa, Australia, and Asia. sites is likely to reduce field efficacy. Williams et al.
(2007) confirmed that bifenthrin-treated LOs have the
potential for use against Ae. aegypti and that they are
Bifenthrin: 2-Methyl-3-phenylphenyl) effective in the field for at least 4 weeks. Given that
methyl (1S,3S)-3-[(Z)-2-chloro-3,3,3- untreated ovitraps were more acceptable for Ae. aegypti
trifluoroprop-1-enyl]- 2,2-dimethylcyclopropane-1- oviposition, the removal of alternative oviposition sites
carboxylate before deployment of LOs in the field should maxi-
mize their effectiveness.
O F
McGinn et al. (2008) assessed the efficacy of Bistar
F 80 SC as a barrier treatment of Australian military
F
tents, Northern Territory, Australia. There was a mean
O
increase in protection of 81% against mosquitoes
Cl entering treated tents and 90.4% increase in protection
against biting, predominantly by Cx. annulirostris.

Cyfluthrin: [(R)-cyano-[4-fluoro-3-(phenoxy)phenyl]
In some operations in Africa and India, bifenthrin, a methyl] (1R,3R)-3-(2,2-dichloroethenyl)-2,2-
non alpha-cyano pyrethroid insecticide, (Talstar 80 dimethylcyclopropane-1-carboxylate
SC, Bistar 80 SC) has been chosen even in areas where
there is vector resistance to commonly used pyre-
throids (permethrin and deltamethrin). Bifenthrin- F
Cl
impregnated bed nets offer considerable personal
protection. The results presented by Chouaibou (2006) O
Cl O
confirm that bifenthrin at 50 mg/m2 could be recom-
mended for mosquito net impregnation. O

Lethal ovitraps (LOs) containing insecticide-treated N

ovistrips are used as a lure-and-kill device for the con-
tainer-breeding dengue vectors Ae. aegypti and Ae.
albopictus. Lure-and-kill strategies involve using phero- In response to the statement “…properly applied and
mones or kairomones to attract insects to a lethal device. timed ULV insecticide application could be effective
This ensures a targeted delivery of a minimum amount in suppressing dengue vectors at the time of an epi-
of insecticide, enhancing control efficacy while mini- demic…” (Gratz 1991), a number of field efficacy tri-
mizing nontarget impact. Although lure-and-kill has als of ULV cyfluthrin for the rapid control of Ae.
been successfully used to control other dipterans such as aegypti were conducted in Thailand. Sulaiman et al.
tsetse flies (Brightwell et al. 1991), its application in (1998) evaluated cyfluthrin and malathion ULV appli-
mosquito control is in its infancy. LOs with a cloth strip cations on dengue vectors in high-rise apartment
treated with bifenthrin are used in north Queensland buildings in Kuala Lumpur. Both products showed
18.3 Chemical Groups of Insecticides 463

adulticidal effects, but cyfluthrin had more significant Resmethrin: 5-benzyl-3-[({[(3R)-2,2-dimethyl-3-

larvicidal effect than malathion. Sulaiman et al. (2000) (2-methylprop-1-en-1-yl) cyclopropyl]
also evaluated deltamethrin/s-bioallethrin/piperonyl carbonyl}oxy)methyl]furan
butoxide and cyfluthrin against dengue vectors in
Malaysia and found that both demonstrated adulticidal
and larvicidal effects. According to Sulaiman et al. O
(2002), Solfac UL 015 (containing cyfluthrin 1.5 g/l),
was diluted in diesel and applied 5 times over a 2–3
month period from a vehicle-mounted cold aerosol O
O
generator. The treatment caused adult knock-down 1 h
after application outside and inside houses. There was
no significant difference between cypermethrin and
cyfluthrin in terms of adult mortality both inside and
outside houses. These results indicate that both cyper-
methrin and cyfluthrin had adulticidal effects on Ae.
albopictus. Cyfluthrin also had a slightly higher mor-
tality effect on the larvae than cypermethrin.
Resmethrin is used for mosquito control primarily
against urban Culex species, which are vectors of St.
Etofenprox: 1-ethoxy-4-[2-methyl-1-([3-(phenoxy) Louis Encephalitis (SLE) and West Nile Virus (WNV),
phenyl]methoxy)propan-2-yl]benzene applied as ULV applications in the Americas. Since
some of the Culex species have developed resistance to
compounds from other chemical groups, resmethrin
has gained significance. Resmethrin is commercially
available as Scourge, containing 12% a.i. and 36%
O synergist (PBO). It has been shown that a pair of treat-
O
ments on successive evenings can increase mortality
for a longer period. In addition, Reiter et al. (1990)
O
demonstrated that resmethrin treatment resulted in an
impressive reduction (74–84%) of the oviposition rate
Etofenprox is a non ester pyrethroid but still it acts of Culex mosquitoes following the day of application
on the chloride channel of insect nervous systems as and this impact was observable for at least 8 days fol-
pyrethrins and pyrethroids do. Etofenprox disturbs lowing the application.
insect nervous systems following direct contact or IVM strategies played an increasingly important
ingestion and is active against a broad range of role especially when WNV outbreaks occurred in
pests. It is used in agriculture, horticulture, viticul- the USA. Control measures in California relied on
ture, forestry, animal health, and against public pyrethroids as the chosen products to suppress adult
health pests. mosquito populations (Gammon 2007). These are
In the public health sector, etofenprox is used either usually applied aerially at night onto trees contain-
by direct application in infested areas or indirectly by ing roosting birds, the primary WNV hosts.
impregnating fabrics, such as mosquito nets. Pyrethroids are quite potent, but with generally low
The WHO hazard classification (2004) of etofen- avian toxicity. An advantage of application at night
prox (trade name Trebon) is “U”: “unlikely to present is that they are more effective, as the temperature is
acute hazard in normal use”. The use of etofenprox in reduced. Moreover, those containing a chrysan-
public health is mainly as EC and EW as formulations, themic acid moiety readily break down in sunlight
containing 10% a.i., as, evaluated by WHOPES (1997, ensuring rapid dissipation during the daylight hours.
1999). There are however other formulations, such as The principal pyrethroids used as adulticides in the
a WP, that are also used in public health and agricul- USA are the natural pyrethrins, resmethrin, and phe-
ture in many countries. nothrin, which are all chrysanthemates.
464 18 Chemical Control

Deltamethrin: [cyano-(3-phenoxyphenyl)-methyl] quito behaviour, vector control strategies will con-

3-(2,2-dibromoethenyl)-2,2-dimethyl-cyclopropane-1- tinue to be hampered by not knowing which of several
carboxylate insecticide effects are actually responsible for pre-
venting disease transmission inside homes. Das et al.
N (1986) conducted a study to determine the suscepti-
bility status of multiresistant An. culicifacies popula-
O
tions using deltamethrin at a concentration of 0.025%.
Br O The strains tested showed very high resistance to
O
DDT and dieldrin and well pronounced resistance to
Br malathion. With deltamethrin, however, all the tests
showed 100% mortality, which implies that DDT and
dieldrin resistance did not confer cross-resistance to
Deltamethrin, a commonly used synthetic pyrethroid deltamethrin. By contrast, the organochlorine- and
in public health has been the mainstay for IRS, used to malathion-resistant An. gambiae in Sudan, was cross-
combat malaria transmission in Asia (Pothikasikorn resistant to pyrethroids (Davidson and Curtis 1979).
et al. 2005). Deltamethrin (K-Othrine) can also be used for
Most pyrethroids are known to elicit behavioural ground and aerial ULV applications.
responses in insects (Roberts and Andre 1994;
Roberts et al. 1997; Chareonviriyaphap et al. 2001).
Permethrin: 3-Phenoxybenzyl(1RS)-cis,trans-3-
In Thailand, deltamethrin for IRS was first launched
(2,2-dichlorovinyl)-2,2-
in 1994. The extensive use of pyrethroids since that
dimethylcyclopropanecarboxylate
time has been a major stimulus for field evaluation of
the behavioural responses of malaria vectors. One of
O
the most important malaria vectors in Thailand, An.
minimus remains a significant vector because of its O
major endophagic and anthropophagic behaviours O
(Chareonviriyaphap et al. 2003). However, the pat-
tern of An. minimus behaviour elicited by deltamethrin
is quite different from behaviour elicited by DDT. Cl
An. minimus females almost disappeared from the
DDT-treated huts during the second half of the night,
Cl
whereas they continued to bite in the deltamethrin-
treated huts throughout the night (Polsomboon et al.
2008). This difference is consistent with observations Permethrin-impregnated bed nets and clothing provide
on house-invading behaviour of An. vestitipennis after good temporary protection against mosquitoes. In tests
huts were treated with deltamethrin and DDT (Grieco conducted in Florida, Schreck et al. (1984) reported
et al. 2000). In the An. vestitipennis studies, there permethrin-treated clothing alone provided 89.1% pro-
were higher numbers of mosquitoes entering the hut tection from Oc. taeniorhynchus, compared with
treated with deltamethrin than with DDT, indicating 94.4% protection provided by the combination of per-
the higher spatial repellency of DDT compared to methrin-treated uniforms and topically applied repel-
deltamethrin. Specifically, there was a 97% reduction lents. A study conducted in Alaska showed that
of mosquitoes entering a hut treated with DDT, permethrin-treated clothing alone reduced biting of
whereas there was only a 66% reduction of An. vesti- Cs. impatiens by 93%, compared with 99% protection
tipennis in the deltamethrin-treated hut (Grieco et al. obtained with treated clothing and repellent (Lillie
2000). Deltamethrin did not have as dramatic reduc- et al. 1988).
tion on the biting population as DDT did, signifi- In recent publications (Munhenga et al. 2008), it was
cantly reducing An. minimus biting inside huts. In confirmed that the presence of permethrin resistance in
conclusion, without a better understanding of the An. arabiensis populations from Zimbabwe may occur
relationship between insecticide residues and mos- at significant levels, which further emphasizes the
18.3 Chemical Groups of Insecticides 465

importance of periodic and ongoing insecticide suscep- efficacy lasted up to 6 weeks post treatment. In con-
tibility testing of malaria vector populations. trast, Culex spp. were not reduced by these treatments
Synthetic pyrethroid formulations have often been (Trout et al. 2007). The same study indicated that
based on organic solvents and carriers, but due to envi- lambda-cyhalothrin applied as a barrier to low-lying
ronmental concerns, water-based formulations to vegetation does not properly target adult daytime
reduce the environmental impact have now been intro- resting-sites for Culex spp. but they can reduce Aedes
duced. Meisch et al. (1997) conducted trials with oil- spp. Lambda-cyhalothrin 2.5 capsule suspension (CS),
based Permanone 31–36 (permethrin 31% and a new water-based microencapsulated formulation
36%PBO) and water-based Aqua Reslin (permethrin (2.5% a.i., w/v), is reported to have wash-resistant
20% and 20% PBO) formulations of permethrin at properties and longer persistence when applied to bed
rates of 2.03 and 3.93 g a.i./ha against An. quadrimac- net material than other formulations (Sahu et al. 2008).
ulatus and Cx. quinquefasciatus. Results indicate sig- The estimated protection factor based on malaria inci-
nificantly greater control of both species at the higher dence was 86% for the treated nets. The results of the
application rates for both formulations. study showed that the use of bed nets treated with a CS
formulation of lambda-cyhalothrin at 10 mg a.i./m2
was acceptable to the community, and retreatment of
Lambda-cyhalothrin: 3-(2-chloro-3,3,3-trifluoro-1- nets at 9-month intervals can significantly reduce den-
propenyl)-2,2-dimethyl-cyano(3-phenoxyphenyl) sity and survival of An. fluviatilis and incidence of fal-
methyl cyclopropanecarboxylate ciparum malaria.

Metofluthrin: 2,3,5,6-tetrafluoro-4-
methoxymethylbenzyl (E,Z) (1R,3R)-2,2-dimethyl-3-
O (prop-1-enyl) cyclopropane carboxylate

O F F
O Cl H3C CH3 F CH3
F CH3 O
F
O
F
N H H
O F

In 1989, the pyrethroid lambda-cyhalothrin (Icon) Metofluthrin (SumiOne®, Eminence®) is a novel

became available. Schaefer et al. (1990) conducted a vapouractive pyrethroid discovered by Sumitomo
laboratory and field evaluation of the compound against Chemical Co. Ltd., registered in Japan in 2005 and is
Cx. tarsalis adults and reported that lambdacyhalothrin under worldwide development for environmental
offered high potential for aerosol applications. health use. Metofluthrin has extremely high knock-down
The increased threat of mosquito-borne diseases activity against various insect pests, especially mos-
coupled with a decreased tolerance of nuisance mos- quitoes, as well as high volatility and low mammalian
quitoes in the United States, has encouraged vector toxicity. It is used in mosquito mats and coils, and also
management professionals to offer mosquito control various new formulations and devices such as paper
services for homeowners. Lambda-cyhalothrin (0.1%) emanators, fan-driven devices, and resin formulations.
at its maximum label concentrations has been used as Metofluthrin is >40 times as active as d-allethrin
a barrier treatment for managing mosquito populations against southern house mosquitoes (Cx. quinquefas-
in suburban residential properties and its residual effi- ciatus) when used in mosquito coils (Ujihara et al.
cacy was evaluated in reducing adult mosquito popula- 2008). The vapour pressure of metofluthrin (1.87 × 10−3
tions. Lambda-cyhalothrin treatment significantly Pa at 25 ºC) is >2 times and >100 times higher than
reduced Aedes spp. Treated sites had 85.1% fewer Ae. d-allethrin and permethrin, respectively. The product
albopictus bites than the untreated control and residual vapourizes at ambient temperature without heating,
466 18 Chemical Control

whereas other conventional pyrethroids need heating There are two major groups of IGRs, that differ in their
for evaporation. High vapour pressure and insecticidal modes of action:
activity of metofluthrin could lead to new mosquito
(1) The chitin synthesis inhibitors, such as diflubenzuron,
control devices that need no external energy for vapour-
cyromazine, and triflumuron, interfere with new cuticle
ization, with lower cost and longer efficacy. A signifi-
formation, resulting in moult disruption, and
cant reduction in mosquito density in metofluthrin-treated
(2) The juvenile hormone analogs, which interfere with
sites was maintained up to 6 weeks post treatment,
the metamorphic processes affecting development
depending on the feeding habits (Kawada et al. 2004).
to the adult stage.
An interesting finding of this study is that exophilous
species were impacted in spatial outdoor metofluthrin Nine countries from the WHO regions (except the
treatments. There are very few reports on the efficacy African region) reported the use of IGRs for vector
of antimosquito products in outdoor situations. Jensen control (Table 18.9). However, some countries did not
et al. (2000) reported that only mosquito coils and submit records of their IGR use, since many national
MN-diethyl-3-methylbenzamide (DEET) products mosquito control programmes apply larvicidal IGRs to
significantly reduced mosquito landing rates relative to control nuisance, but not for disease vectors. Overall
untreated controls in the field. use of these products is substantially larger than is
recorded (Table 18.8).
Benzoylurea compounds (diflubenzuron and
18.3.5 Insect Growth Regulators (IGRs) novaluron) belong to the chitin synthesis group, while
the juvenile hormone mimics include methoprene,
fenoxycarb and pyriproxifen.
All compounds belonging to this group disrupt the
normal growth and development of insects. They were
developed as a result of rational leads from basic ento-
mological research on metabolic disrupters, moult 18.3.5.1 B
 enzoylphenyl Ureas
inhibitors, and behaviour modifiers of insects. Since (diflubenzuron and novaluron)
the target site of action for these chemicals is known
and susceptible to disruption only at certain times dur- The insecticidal activity of the benzoylphenyl urea
ing their life cycle, these materials are thought to have analogs was discovered in 1970 by Philips-Duphar
fewer serious detrimental effects on nontarget species. Company in the Netherlands.

Table 18.9 Global use of insect growth regulators for control of vector-borne diseases reported to WHOPES, in kg of active
ingredient, 2003–2005, (Zaim and Jambulingam 2007)
Amount of active ingredient (kg)
Region Country Disease Compound 2003 2004 2005
Americas Argentina Dengue Triflumuron 15 NR NR
Brazil Dengue Diflubenzuron NR 5 0
Triflumuron NR <1 <1
Methoprene NR 2 <1
Colombia Dengue Pyriproxyfen NR NR 4
Eastern Mediterranean Saudi Arabia Malaria Pyriproxyfen NR 45 45
Yemen Malaria Pyriproxyfen NR NR 1
European Turkey Malaria Diflubenzuron 950 966 1,250
South-East Asia Indonesia Malaria and dengue Methoprene 6,043 7.5 0
Pyriproxyfen 0 5 9
Western Pacific New Zealand Ross River Virus Methoprene 1,765 837 1,766
Singapore Dengue Pyriproxyfen NR NR <1
NR not reported
18.3 Chemical Groups of Insecticides 467

Diflubenzuron: 1-(4-chlorophenyl)-3-(2,6- N-acetylglucosamine units catalyzed by the enzyme

difluorobenzoyl)urea chitin synthetase, is inhibited.
After an IGR treatment, symptoms are not gener-
Cl ally observed until the moulting process is initiated.
F O O The degree of the disruption of ecdysis (moulting of
the old cuticule) is related to the dosage, and is char-
acteristic for each benzoylphenyl urea analog and
N N the insect species (ecdysal disruption may occur in
H H the larval–pupal moult too). The range of effects
include:
F
(1) Ecdysis is prevented completely, so that the insect
dies within the old cuticle.
Diflubenzuron was the first compound shown to be (2) Ecdysis is initiated, but not completed. In some
effective against insects, and resulted from the combi- cases, the exuvia splits normally but the ecdysis
nation of two herbicides, dichlobenil and diuron. The proceeds no further. In others, the moult proceeds
resulting compound was ineffective as an herbicide, until the old cuticle remains attached only to some
but was toxic to insects. Surprisingly, the compound’s of the last abdominal segments.
action was very different from that of other insecti- (3) In some cases, the old cuticle is almost completely
cides used at that time. The mortality was invariably shed from the body, but remains attached to the
connected with the process of moulting. Treated adults head-capsule and mandibular region, and prevents
were not killed, but their reproductive capacity was further feeding or development.
strongly reduced. The chemistry and the symptoms of Benzoylphenyl ureas exhibit several unique charac-
the benzoylphenyl urea analogs were unique and they teristics. In general, they are more toxic when they
became a new class of insecticides. are ingested by the target organism. Application of
diflubenzuron, or other IGR larvicides from the same
group, in the field should therefore coincide with
Novaluron: (RS)-1-[3-chloro-4-(1,1,2-trifluoro-2- active feeding of the target insect. The second charac-
trifluoromethoxyethoxy)phenyl]-3-(2,6- teristic concerns the “activity window” of the benzo-
difluorobenzoyl)urea ylphenyl ureas. Peak activity occurs at distinct times
of the insect’s development, primarily during peaks in
chitin synthesis. In practical terms, susceptibility of
F F larvae is greatest prior to each moulting. Treatments
F should therefore be applied either at the time of the
O
F O O O F greatest susceptibility of the insects or alternatively;
the treatment should have a sufficient residual activity
F F
N N Cl to span the next “activity window.” The third charac-
H H
teristic concerns the prolonged larval life after a toxic
F dose is acquired. Even after exposure at the suscepti-
ble stage, the insect may live in a moribund state for
many days before dying. Tests with various mosquito
species by Mulla and Darwazeh (1975) showed little
18.3.5.1.1 Mode of action or no adult emergence for 27 days after diflubenzuron
treatment of larval sites. Mortality was recorded dur-
Studies on the benzoylphenyl urea mode of action, ing larval and pupal stages as well as during adult
implicate the enzyme chitin synthetase as the actual eclosion.
biochemical moiety, which interacts with the toxicant. A synchronized larval population is not essential
Post et al. (1974) showed that the last step in the for the effective use of these products, since all larval
chitin synthesis process, the polymerization of the instars are susceptible to diflubenzuron treatment.
468 18 Chemical Control

However, it is advisable to conduct treatments during other in the adult. During the larval stage, it suppresses
the early larval stages of development. Field tests by metamorphic changes. In the adult, juvenile hormone
Schaefer et al. (1975) revealed that several Aedes/ is required for several reproductive functions such as
Ochlerotatus spp. and Cx. tarsalis resistant to OPs ovarian development, yolk synthesis, pheromone pro-
were effectively controlled in all larval stages by duction, and accessory gland development. It is evi-
diflubenzuron. dent that upsetting the titre of juvenile hormone at
In the aquatic habitats where diflubenzuron was certain periods during the life-history will adversely
applied, the impact of the active ingredient on a large affect metamorphosis. Moreover, such an induced titre
number of nontarget species has been assessed. In gen- might have a domino effect and disrupt other hormonally
eral, detrimental effects were detected as temporary, controlled functions.
even after repeated treatments. (Ali and Mulla 1978; The morphogenetic effect of the JHA compounds is
Miura and Takahashi 1975; Zgomba et al. 1983; primarily seen during the larval–pupal transformation,
Zgomba 1987). and may result in various degrees of incomplete meta-
Recent publications by Thavara et al. (2007) showed morphosis. They also influence the endocrine physiology
results of two diflubenzuron formulations: tablet of the insect, which may result in abnormal morpho-
(40 mg a.i./tablet) and granular (2% a.i), which were genesis. Methoprene inhibits the release of an execu-
evaluated for larvicidal efficacy against Ae. aegypti in tive hormone from the corpora allata early in the last
water-storage containers under field conditions in larval instar, but stimulates the glands prior to pupa-
Thailand. Each formulation was applied to 2001 clay tion. JHAs can also block embryonic development and
jars at five different dosages (0.02, 0.05, 0.1, 0.5, and may be ovicidal too. Various types of effects ranging
1 mg/l a.i.). Another experiment was also conducted from ovicidal to delayed effects during postembryonic
using three different dosages (0.1, 0.5, and 1 mg/l), life have been reported. Treating early larval instars
where half the water in each treated jar and the control will have very little effect on metamorphosis, since the
was removed and refilled weekly. A high degree of requirement for larval–larval moult is a high titer of
larvicidal efficacy (96–100% EI) was achieved with the hormone. However, if the last larval instar is treated
four dosages (0.05, 0.1, 0.5, and 1 mg/l) of both for- with juvenoids, when in the natural process of meta-
mulations (tablet and granular) for a period of 23 morphosis the juvenile hormone level dramatically
weeks posttreatment. The efficacy of the lowest dos- decreases, the result is abnormal pupation and/or
age (0.02 mg/l) of tablet and granular formulations incomplete adult formation.
lasted for 21 and 22 weeks posttreatment, respectively. One of the main reasons for juvenile hormone ana-
Under the conditions of water removal and weekly logs being effective as control agents is their chemical
refilling, a high degree of larvicidal efficacy (96–100% structure (terpenoid), which enables them to penetrate
EI) at the three dosages was obtained with the tablet the cuticle with great ease, and exert their effects on
formulation 18–21 weeks posttreatment, whereas the the target tissue, the epidermis.
efficacy of the granular formulation persisted 15–23 The ecotoxicological effects of JHAs have been
weeks posttreatment depending on the dosage. This extensively investigated. The toxicity to vertebrates is
study clearly demonstrated a high level of residual extremely low, e.g. the oral LD50 of methoprene for
activity with both formulations of diflubenzuron rats is over 34,500 mg/kg (Siddall 1976). However,
against larvae of Ae. aegypti in water-storage contain- adverse effects on nontarget organisms that receive a
ers. Considering environmental factors and water-use dose of JHA during their last larval instars could also
conditions, it is likely that dosages of 0.05–0.1 mg be expected. At levels far above the dosage used for
a.i./l are effective dosages providing long-lasting con- mosquito control, methoprene produces a short-term
trol for 3–4 months in the field. toxicity effect on the water flea, Daphnia magna, the
side-swimmer Hyalella azteca, the tadpole shrimp,
Triops longicaudatus and some other organisms (Miura
18.3.5.2 Juvenile Hormone Analogs (JHAs) and Takahashi 1975). However, high concentrations of
methoprene had no adverse effects on Dugesia doroto-
The natural juvenile hormone has two distinct bio- cephala, the planarian that feeds on mosquito larvae
chemical effects: one during the larval stage and the and which can be used as a biological-control agent.
18.3 Chemical Groups of Insecticides 469

It has therefore been proposed that integrated use of Depending on the biotic and abiotic factors of the breed-
planarians and JHA for the control of mosquitoes is ing site, the application rates range from 3.0 to 11.5 kg/
viable (Levy and Miller 1978). ha. A study by Kramer et al. (1993) demonstrated that
methoprene pellets applied at 3.4 kg/ha against Oc. dor-
In operational studies, the most commonly used meth-
salis prior to marsh inundation provided 99% con-
ods for evaluating the efficacy of JHAs are:
trol ~ 42 days, 86.4% ~ 131 days, and 66.6% control 8
(1) Introducing captured 3rd–4th instar larvae into the months after the application. Proportions of partially
JHA-treated water, collecting pupae after an inter- emerged adults increased over the course of the study.
val of time (e.g. 4 days), and daily observation of Of all the completely emerged mosquitoes from the
the adult emergence. treated region of the marsh, 66% were found dead on
(2) Collection of immature mosquitoes from the treated the water surface, compared with only 0.7% from the
site, and adult emergence and mortality evaluation. untreated area.
There are several alternative methods for recording For long-term control, methoprene briquettes are
and calculating efficacy, but Kline (1993) uses the fol- perhaps the principal choice, especially where access
lowing classification of emergence: dead pupae (DP); to the breeding site is difficult, and where the area may
dead adults (DA); and live adults (AA “active adults”). be flooded repeatedly during the season. The briquettes
From these data, the % emergence inhibition (% can be applied at or before the beginning of the mos-
E.I. = % control) may be calculated using the formula quito season; e.g. prior to flooding, while the sites are
still dry. For controlling Aedes/Ochlerotatus and
% E.I. = (DP + DA)/(DP + DA + AA) × 100 Psorophora larvae in shallow depressions (up to
50–60 cm depth), one briquette/18 m2 is recommended.
Briquettes have to be placed at a higher rate (1 per
9 m2) for control of Culex, Culiseta, Anopheles,
Methoprene: isopropyl (E,E)-(RS)-11-methoxy-
Mansonia, and Coquillettidia spp. larvae. The duration
3,7,11-trimethyldodeca-2,4-dienoate
of the efficacy depends on water temperature, water
quality, and the number of fluctuations. In continental
O and Mediterranean climates, effective suppression of
mosquitoes can be expected for ~ 4 months. Douglas
O O et al. (1994) reported that when solid, sustained-release
methoprene formulations were applied, the highest
(S)-methoprene residue detected was 6.0 mg/l. The
Methoprene, one of the most often used JHAs was syn- majority (85%) of samples contained residues of
thesized by Henrick and colleagues in 1973 (Baillie and 1.0 µg/l. Such low residues do not constitute a signifi-
Wright 1985). More than 30 years of field research has cant risk to nontarget organisms.
shown that methoprene is one of the most environmen- Effectiveness of a sustained-release sand granule
tally safe mosquito control products. It is available in formulation of methoprene was also established for
liquid, pellet, and briquette formulations that allow con- Oc. taeniorhynchus, a major nuisance in coastal areas
siderable flexibility at the operational level. Liquid of the U.S. (Kline 1993). In the field, inhibition of
methoprene formulations may be applied by standard emergence in mosquitoes exceeded 90% when these
ground equipment or aerially against the 2nd, 3rd, and granules were applied post flood at 5.6 kg/ha.
4th instar larvae typically found in floodwater breeding Granular formulations can be prepared on-site by
sites, within 4 days after flooding. In areas with dense mixing dry sand with the liquid methoprene formula-
vegetation or canopy, mixtures of liquid methoprene tion in a rotating-type mixer (concrete mixer) for
and sand may be applied with granule application equip- 5–10 min until the sand is uniformly coated. Silicon
ment. The persistence of these methoprene formulations dioxide should be added and mixed for an additional
is up to 10 days. The pellet formulation releases an 5 min. This will provide a dry mixture, which will flow
effective level of methoprene for ~ 30 days into flood- freely through standard granule application equipment.
water sites, artificial water containers, tyres, waste The typical application rate of such a formulation is
treatment ponds, man-made depressions, ­tree-holes, etc. 11–12 kg/ha.
470 18 Chemical Control

Fenoxycarb: ethyl N-[2-(4-phenoxyphenoxy) emergence. Studies with pyriproxyfen demonstrated

ethyl]carbamate very high activity against Aedes/Ochlerotatus, Culex
and Psorophora species, both in laboratory and in field
O studies, at rates as low as 0.56 g a.i./ha (Mulla et al.
1989; Schaefer et al. 1990). When pyriproxyfen was
O
N O
applied in dairy waste-water lagoons at 100 g a.i./ha in
H single and multiple applications, it resulted in control of
Culex spp. for a period of 7–68 days. The length of the
O
control period appeared to be related to water quality,
with greater residual activity in more polluted sources
Although its mode of action is like that of juvenoids, (Mulligan III and Schaefer 1990). The assumption was
fenoxycarb actually belongs to the carbamates. Axtell that the a.i. was adsorbed onto organic debris and
et al. (1980) and Dame et al. (1974) have shown that remained highly toxic to the larvae even after the water
fenoxycarb suppresses the development of Cx. tarsalis, was replenished with untreated waste-water.
Cx. pipiens, Cx. quinquefasciatus, Oc. melanimon and Recent studies demonstrate that pyriproxyfen can
Ps. columbiae. None of the fenoxycarb formulations be a powerful tool in controlling Ae. aegypti, the prin-
tested by Dorn et al. (1981) and Mulla et al. (1985) pro- cipal vector of dengue, the most important arboviral
duced harmful effects on mayfly, dragonfly, or various disease in the world today affecting an estimated 100
beetle larvae. Freshwater zooplankton exposed to the million people annually. It was demonstrated that a
treatments were also unaffected. slow-release sand granule pyriproxyfen (0.1%) formu-
Ps. columbiae was exposed to several fenoxycarb lation could be effectively used as a larvicide treat-
formulations by Weathersbee III et al. (1988). The ments at oviposition sites, called focal treatment
results showed that 0.5% fenoxycarb sand formulation (Seccacini et al. 2008). Additionally, WHO (2006) has
at a rate of 22 g a.i./ha was effective against larval pop- added pyriproxyfen to a group of larvicides accepted
ulations in rice fields. Excellent control (95%) was for potable water treatment.
achieved against larvae introduced at up to 24 h post- In general, IGRs have high levels of activity and
treatment and residual activity remained >55% for up efficacy against various species of mosquitoes in a
to 120 h posttreatment. The fenoxycarb formulation variety of habitats. Additionally, they show a good
based on corn cob also offered excellent initial control margin of safety to nontarget biota, including fish and
(95%) at the same rate (22 g a.i./ha), but the residual birds. On the basis of these attributes, IGRs provide an
activity decreased to 41% by 120 h posttreatment. additional tool for mosquito control, supplementing
OP, carbamate, pyrethroids, and microbial larvicides.

Pyriproxyfen: 4-phenoxyphenyl (RS)-2-

(2-pyridyloxy)propyl ether2-[1-(4-phenoxyphenoxy)
propan-2-yloxy]pyridine 18.3.6 Novel Insecticide Classes

O Despite the efforts of academia, the pesticide industry,

and national and international agencies, the discovery
N O and introduction of new insecticides remains an extremely
O expensive and a slow process. Although several novel
classes of insecticide have been recently developed for
agricultural use, no new classes of insecticides have been
developed for mosquito control in the last 2 decades.
Like fenoxycarb, pyriproxyfen is also structurally unre- The Vector Control Industry Group (VCIG), which rep-
lated to the natural insect JH, but its biological activity resents the major producers and marketers of vector
is the same as that of the juvenoids (Schaefer et al. control products used in the control of disease vectors,
1988). Through hormonal imbalance, pyriproxyfen sup- acknowledges that very few new products have been
press insect embryogenesis, metamorphosis, and adult developed and launched in the last 20 years in the
18.4 Management and Monitoring of Insecticide Resistance 471

p­ ublic health and vector control market. The causes are 18.4 M
 anagement and Monitoring
multiple, but two main reasons can be put forward. The of Insecticide Resistance
lack of market incentives, such as the modest public
health and vector control market sizes, the small quanti- When mosquito populations are exposed to selection
ties of products used and the financial risk inherent in pressure from insecticides, they may become resis-
developing new public health insecticides today is a tant. Resistance has been defined as “the developed
strong deterrent for the private sector to invest in research ability in a strain of insects to tolerate doses of toxi-
and development in this business area. The current cost cants that would prove lethal to the majority of indi-
of developing and obtaining registration for a new insec- viduals in a normal population of the same species”
ticide for Public Health is estimated at 100–150 million (Cremlyn 1978). These strains tend to be rare in a nor-
USD. The cost of developing a new product from an mal population, but widespread use of an insecticide
existing insecticide is estimated at 4–6 million USD. Not can reduce the normal susceptible population, thereby
least important is that the time required for development providing the resistant individuals with a competitive
of a new a.i. is 10–12 years, while for a new product it is advantage. The resistant individuals multiply in the
4–6 years. absence of intra­specific competition and, over a num-
The WHOPES was set-up in 1960 to collaborate ber of generations, quickly become the dominant propor-
with insecticide manufacturers to help identify new tion of the population. Hence, the insecticide is no
products, both from within existing classes and from longer effective and the insects are considered to be
totally novel classes. The WHO continues to encourage resistant. A population may even develop “cross-
manufacturers to submit novel compounds for routine resistance,” which means that the population is not
evaluation against mosquitoes and other pests. WHOPES only resistant to one insecticide of a particular class,
promotes and coordinates the testing and evaluation of but also to other insecticides in the same class, even
pesticides for public health. It functions through the par- when it has never been treated with the other insecti-
ticipation of representatives of governments, manufac- cides. More severe is the phenomenon of “multiple
turers of pesticides and pesticide application equipment, resistance,” where separate detoxification mechanisms
WHO Collaborating Centers and research institutions, for unrelated insecticides are present, resulting in an
as well as other WHO programmes, notably the insect population that is resistant to different classes
International Programme on Chemical Safety. of insecticides, which makes control with insecticides
In its present form, WHOPES comprises a 4-phase extremely difficult.
evaluation and testing programme, studying the safety, Since Melander (1914) first reported insecticide
efficacy, and operational acceptability of public health resistance, the number of insect species and mites
pesticides, and developing specifications for quality worldwide that have developed strains resistant to
control and international trade. one or more pesticides, has increased to at least 504
WHOPES collects, consolidates, evaluates, and dis- and continues to rise. The number of insecticide-
seminates information on the use of pesticides for public resistant arthropods of public health importance has
health, facilitates the search for alternative pesti­cides risen from 2 in 1946, to 198 in 1990 (Oppenoorth
and application methods that are safe and cost-effective. 1985; Georghiou 1990; Georghiou and Lagunes-
WHOPES attempts to develop and promote policies, Tejeda 1991).
strategies and guidelines for the selective and judicious Rodríguez et al. (2007), reports that eight Latin
application of pesticides for public health use, and assists American strains of Ae. aegypti were evaluated for
and monitors their implementation by Member States. resistance to six OPs (temephos, malathion, fenthion,
It is hoped that a better understanding of the needs pirimiphos-methyl, fenitrothion, and chlorpirifos)
of the mosquito control community, together with new and four pyrethroids (deltamethrin, lambdacyhalot-
approaches to novel insecticide discovery for exam- hrin, betacypermethrin, and cyfluthrin). In larval bio-
ple, based on a better understanding of the mosquito assays, resistance to temephos, malathion, fenthion
at the genomic level, will in time facilitate the discov- and fenitrothion was high in the majority of the
ery of new compounds with appropriate properties. In strains. However, resistance to pirimiphos-methyl
the meantime, IMM and IVM strategies should be the ranged from moderate to high in most of the strains.
mainstay for public health vector control operations. Adult bioassays showed that all the strains were
472 18 Chemical Control

resistant to DDT and to the majority of pyrethroids insecticides, have often accumulated a number of resis-
evaluated. The use of the synergists, S,S,S-tributyl tance (R)-genes and corresponding resistance mecha-
phosphorotrithioate and piperonyl butoxide showed nisms, which may lead to cross- or multiple-resistance.
that esterase and monooxygenases played an impor- Several distinct mechanisms are responsible for the
tant role in the temephos, pirimiphos-methyl, and development of insecticide resistance in insects. These
chlorpirifos resistance in some strains. Insecticide involve either the detoxification of the toxic compound
resistance in Ae. aegypti is a serious problem facing by biochemical metabolism, or a tolerance due to a
control operations, and integrated management strat- decreased sensitivity to the toxic compound at its site of
egies are recommended to help prevent or delay the action. Normally, an insecticide penetrates rapidly
temephos resistance in larvae and pyrethroids resis- through the integument, reaching the site of action. The
tance in adults. site may be a vital enzyme, nerve tissue or receptor pro-
Kim et al. (2007) also demonstrated variable resis- tein. Insecticide molecules bind to the site, and when
tance levels in the northern house mosquito Cx. pipi- they have attained threshold concentrations, they dis-
ens pallens, that have practical implications for the rupt vital processes, causing insect fatality. Resistance
management of insecticide resistance. Cx. pipiens pal- may be selected at each step of this pathway: the integ-
lens is a nuisance-causing insect in Korea, while it is ument, where reduced permeability may occur, thus
the primary vector of WNV (Bren 2003) and epidemic reducing the rate of entry of the insecticide; new or
encephalitis in some Asian countries. This mosquito more abundant metabolic enzymes may be selected,
species is dominant and common in urban areas. The causing breakdown of the insecticide more efficiently;
field-collected populations exhibited high levels of or altered target-sites may be selected to which the
resistance to cyfluthrin and deltamethrin, but low to insecticide no longer binds. Of these three types of
moderate levels of resistance were observed with bendio- mechanisms, metabolism and insensitivity at the site of
carb, chlorpyrifos, lambda-cyhalothrin, S-bioal-lethrin, action are the most important. A reduction in the rate of
and permethrin. These results indicate that careful cuticular penetration aids both types of mechanisms in
selection and judicious rotational use of these insecti- a synergistic way (Georghiou 1994). In addition to
cides is required in order to maintain continued satis- those, another form of insecticide resistance is behav-
factory control of field populations of Cx. pipiens ioural resistance, where insect behaviour becomes
pallens. modified so the insect no longer comes into sufficient
Many of the insecticides currently used in South contact with the insecticide deposit (Miller 1988).
Korea, have failed to control Cx. pipiens pallens in the
field, most probably due to resistance. Widespread
insecticide resistance has been a major obstacle in the
IMM programme in South Korea. These problems 18.4.2 Resistance Surveillance
indicate the need to establish an efficient resistance-
management strategy based on detailed information on Resistance monitoring should be an integral part of
the extent and nature of resistance. Detection of any mosquito control programme. The susceptibility
changes in field resistance can facilitate the use of of mosquitoes should be verified before the start of
alternative control measures, including use of syner- control operations, to provide baseline data for insec-
gists, rotational use of various insecticides, reduced ticide selection and choice of application technique.
insecticide application, and use of environmental con- Regular surveillance will allow early detection of
trol measures. resistance, so that resistance management strategies
can be implemented or in the case of late detection,
evidence of control failure can justify the replace-
ment of the insecticide. The operational criterion of
18.4.1 Resistance Mechanisms resistance has usually been interpreted as the survival
of 20% or more of field collected individuals tested at
Resistance mechanisms are generally dependent on sin- the currently known diagnostic concentration of the
gle genetic factors. Species that have been under contin- particular insecticide, using WHO test kits. The dia­
ued selection pressure with one or a range of different gnostic concentration of a particular insecticide is
18.4 Management and Monitoring of Insecticide Resistance 473

that which has been found to reliably cause complete changes in field resistance can facilitate the use of
mortality of strains that have never before been sub- appropriate alternative control measures.
jected to insecticides, and are therefore assumed to be Since the 1950s, California mosquito abatement
susceptible. districts have used chemical control programmes
Practical tests for detection of specific resistance with emphasis on IMM practices to reduce mosquito
mechanisms in individual insects have been developed. populations. Controlling members of the Culex
These include filter paper tests for esterases (Pasteur Pipiens Complex is important because of their pro-
and Georghiou 1989) and acetylcholinesterase (AChE) pensity to become a nuisance. In addition to being
(Dary et al. 1991), microtitre plates for esterases (Dary major pest mosquitoes, Culex Pipiens Complex mem-
et al. 1990) monooxygenases, glutathione transferase bers are vectors of Wuchereria bancrofti (Cobbald),
and others (Georghiou 1990). which causes filariasis in humans in the tropics. They
Since malaria is the leading cause of morbidity also transmit WNV and SLE viruses in USA, and Rift
and mortality in Africa, accounting for an estimated Valley Fever virus in Egypt. California populations
360 million clinical attacks (Snow et al. 2005) and of Cx pipiens complex mosquitoes developed resis-
1–2 million deaths annually (Breman et al. 2004), tance to DDT and other organochlorines soon after
malaria vector control activities are crucial. Most these chemicals were introduced. OPs replaced
commonly these rely on the use of effective insecti- organochlorines and shortly thereafter, in the early
cides, through IRS or on ITNs or through IVM, such 1960s, Isaak (1961) detected the first evidence of OP
as use of biological agents as larvicides in the breed- resistance in California Cx. p. quinquefasciatus. By
ing sites of the vectors. There are numerous cases of the 1970s, OP resistance was widespread, but despite
insecticide resistance reported for Anopheles species. this early evidence of resistance, OPs are still used
The potential development of insecticide resistance today, although pyrethroids are more widely used.
is a common threat to any insecticide-based malaria Pyrethroid tolerance in members of the Culex Pipiens
control programme. The numbers of insecticides formu- Complex has been documented in countries such as
lated for indoor residual treatment and recommended by Tunisia (Ben Cheikh et al. 1998), Cuba (Bisset et al.
WHOPES pesticide evaluation (WHO 2001a) scheme is 1991), Ivory Coast and Burkina Faso (Chandre et al.
very limited. To ensure that the insecticides used remain 1998), Saudi Arabia (Amin and Hemingway 1998),
effective, and decisions on insecticide choice are evi- French Polynesia (Pasteur et al. 1995), and China
dence-based, monitoring and evaluation of potential (Jinfu 1999). There has not been a published report of
resistance mechanisms within the targeted vector popu- pyrethroid tole­rance in North America in any mem-
lation need to be undertaken. The spread of pyrethroid ber of the Cx. pipiens complex or, in fact, in any mos-
resistance may be critical for sustainability of ITNs quito species. For surveillance purposes, in 2003
because this is currently the only insecticide group rec- McAbee et al. conducted adulticide bottle bioassays
ommended for impregnation. Two other classes of on Culex Pipiens Complex populations from various
insecticides, carbamates and OPs (Coosmans and locations in California, to test them for tolerance to
Carnevale 1995; Walker 2000) are available for conven- OP and pyrethroid compounds. It was found that the
tional malaria control programmes. Their relatively populations had a knock-down reduced resmethrin
short half-lives, sometimes requiring a sequence of 2–3 and permethrin knock-down response in the bottle
IRS per year, can make these insecticides less conve- bioassays relative to a standard susceptible Cx. pipi-
nient and more costly. ens quinquefasciatus. Selected larvae were shown to
Increasing levels of resistance to the most com- cross-resist to lambda-cyhalothrin as well as to DDT.
monly used insecticides have caused multiple treat- However, adult knock-down time following exposure
ments and excessive doses, raising serious human to permethrin, resmethrin, and pyrethrum was
health and environmental concerns in various coun- affected despite an increase in larval tolerance to
tries with extensive vector control programmes. pyrethroids. Partial and almost complete reversion to
Resistance monitoring can be an effective component susceptibility as larvae was achieved with S,S,S-
of the resistance management approach by providing tributylphosphorotrithioate and PBO, respectively,
valuable information on responses of mosquito popu- suggesting the presence of carboxylesterase and mono­
lations to currently-used insecticides. Detection of oxygenase-mediated resistance. Insensitive target-site
474 18 Chemical Control

resistance (kdr) was also detected in some mosqui- Measures in this category include the use of low
toes tested by use of an existing PCR-based diagnos- insecticide rates, infrequent applications, non-persis-
tic assay designed for Cx. pipiens mosquitoes. tent insecticides, and preservation of refugia.
Carboxylesterase-mediated resistance was supported by While management by moderation comes close to
use of newly synthesized novel pyrethroid-selective meeting environmental standards, it may not be appeal-
substrates in activity assays. Bottle bioassays gave ing where there is a need to control human disease vec-
underestimates of the levels of tolerance to pyrethroids tors, or control newly introduced pests. In these cases,
of Marin County (California) mosquitoes when com- the saturation or multiple-attack concepts may be more
pared with mortality rates in field trials using regis- appealing.
tered pyrethroid adulticides with and without PBO. Management by saturation: The term “saturation”
This study represents the first report of resistance to does not imply saturation of the environment with pes-
pyrethroids in a population of a mosquito species in ticides. It indicates saturation of the insect’s defenses
the USA. by use of sufficient insecticide to leave absolutely no
survivors. This approach has more merit during the
early stages of selection when resistance genes are
18.4.3 Resistance Management rare, and existing mainly in the heterozygous state.
Another means of suppressing the insect’s defenses
According to Georghiou (1994), factors that influence the is the use of synergists. PBO has been used for many
evolution of resistance can be classified into three catego- years as a synergist of pyrethrins in household aerosol
ries: genetic, biological, and operational. Georghiou and sprays, and more recently with pyrethroids in the con-
Taylor (1976) have quantified the influence of individ- trol of mosquitoes and houseflies. By suppressing the
ual factors and have shown that some are positively insect’s mixed-function oxidase system, which is
correlated with the development of resistance (i.e. involved in the degradation of pyrethroids, PBO effec-
gene dominance, population isolation, insecticide per- tively removes the selective advantage of this mecha-
sistence, etc.), while others are negatively correlated nism. The approach would not apply where alternative
(immigration of sensitive populations into areas where pathways of detoxication are also present (Ransinghe
resistant population exist, and the presence of untreated and Georghiou 1979).
habitats where populations without selection pressure Management by multiple-attack: The multiple-
for R-genes can develop). If the relative influence of attack strategy is based on the premise that control can
each factor could be expressed quantitatively, a reli- be achieved through the action of several indepen-
able model might be constructed to predict the risk for dently acting stresses, including insecticides, each
resistance in a given situation. That risk can then be exerting selection pressure that is below the level
reduced through appropriate modification of one or which could lead to resistance. This approach includes
more of the operational factors. the application of chemicals in mixtures or in rotation
In general, resistance management is intended to (Georghiou 1983, 1990; Roush and McKenzie 1987;
prevent or delay as much as possible, the develop- Tabashnik 1989).
ment of resistance to an insecticide, while at the same The strategy of using mixtures assumes that the
time maintaining an effective level of mosquito con- mechanisms of resistance to each member insecticide
trol. On the basis of the three categorical factors that are different and that initially resistance genes exist at
influence the development of resistance, Georghiou such low frequencies that they do not occur together
(1994) suggested the following approaches to resist­ in any single individual within a given population.
ance management: management by moderation, Any insect that may survive the exposure to one of
­management by saturation, and management by mul- the insecticides in the mixture is nonetheless killed
tiple-attack. by the other.
Management by moderation: Management by The strategy of using rotation may be applied in
moderation recognizes that susceptibility genes are a situations where resistant mosquitoes have a lower
valuable resource and it attempts to preserve them by biotic fitness than susceptible individuals, which
limiting the chemical selection pressure that is applied. results in a gradual decline in the frequency of resistant
18.4 Management and Monitoring of Insecticide Resistance 475

genes when the selecting insecticide is withdrawn, or resistance, the prior exposure of the target population
is replaced by a neutral insecticide that is not affected to insecticidal selection pressure, and the presence of a
by cross-resistance. significant fitness differential between resistant and
Alternatively, different insecticides maybe applied susceptible individuals.
in a mosaic pattern, with the size of the mosaic seg- In the field, the relative impact of single use, rota-
ments determined on the basis of insect movement and tion and mosaic strategies on the rate of onset of insect­
gene flow. The resulting mosaic of different selection icide resistance in Anopheline mosquitoes has been
pressures may effectively delay the development of tested on a large-scale project in Mexico. Following
resistance throughout the population. extensive baseline studies on resistance mechanisms
The feasibility of using two insecticides in rotation, and gene frequencies, different villages and regions
mixture, or sequentially for resistance-management, were subjected to different application regimes with
has been widely examined by means of cage experi- different classes of insecticides over a period of several
ments (Georghiou 1983; Cilek and Knapp 1993; Curtis years. At present, the data are still being analyzed, but
et al. 1993; McKenzie and Byford 1993). However, the interim results indicate that although techniques such
work has led to divergent conclusions, as the outcome as rotation or mosaic treatment do not prevent the
of each approach will depend on many factors, includ- development of resistance, they do slow the onset as
ing the appropriate choice of insecticides based on compared with repeated use of a single insecticide
their mode of action, the potential mechanisms of (WHO/IRAC 2003).
Chapter 19
Physical Control

19.1 Introduction composition of the products used is unknown.

Products include oils of varying paraffinic and aro-
matic contents, with varying carbon chain lengths,
Physical control may be defined as suppression of insects
and in some cases surfactants or other additives have
by physical or mechanical means. This contrasts with the
been included to alter the products’ properties (Mulla
use of insecticides, which kill insects by chemical or bio-
et al. 1971; Schultz et al. 1983). Effective application
chemical means, and with the use of environmental mea-
rates are, in general, relatively high, typically rang-
sures which do not kill insects directly, but prevent their
ing from 10 to 100 l/ha. Oils have been applied man-
establishment, reproduction or impact by, for example,
ually using conventional knapsack sprayers, by
eliminating their larval habitat, or preventing their access to
vehicles, and by aerial applications. The oils have a
the host, for example, by better designed housing. In prac-
range of different impacts on the mosquitoes. The
tice, there is some overlap between these various terms.
more paraffinic oils have a largely physical interac-
Physical control techniques exist for control of both
tion with the insect’s siphon, preventing effective
mosquito larvae (e.g. polystyrene beads) and adults
oxygen uptake which resulting in drowning or suffo-
(e.g. mass-trapping). Physical control may be used in
cation. Oils with a higher aromatic content, parti­
isolation, but is often seen as a component of integrated
cularly those with a higher volatility are considered
vector management (IVM). In general, mosquitoes are
to be toxic to mosquito larvae (Hagstrum and Mulla
considered unlikely to develop resistance to physical
1968), and so, are not strictly physical control tech-
control techniques.
niques. The oil layer also inhibits mosquito oviposition
on the water surface, either preventing or delaying
recolonization of the treated area for up to 9 days
19.2 P
 hysical Control of Immature (Beehler and Mulla 1996). Once applied, the oil film
Mosquitoes may gradually evaporate, and may also be degraded
by bacterial action.
Several studies have determined the impact of oil
19.2.1 Oil treatments on nontarget aquatic life. Mulla and
Darwazeh (1981) showed that bottom living inverte-
Since the construction of the Panama Canal in the nine- brates, such as mayfly, damselfly and dragonfly larvae,
teenth century, to the present day, petroleum oils have and tadpoles, were almost unaffected by treatment
frequently been used to control immature stages of mos- with mosquito oil at ca. 35 l/ha. However, diving beetle
quitoes. Along with rediscovering source reduction and larvae and adults, together with corixids and notonec-
water management in mosquito control programmes in tids were more severely affected, while ostracods were
recent years, oils have also regained attention as candi- also affected by some oils. Phytotoxic effects were
dates for the treatment of certain types of water bodies. also recognised with earlier petroleum products, but
A wide range of petroleum oils have been used as are much less common with more refined products
mosquito larvicides, although in many cases the exact (Floore et al. 1998).

N. Becker et al., Mosquitoes and Their Control, 477

DOI 10.1007/978-3-540-92874-4_19, © Springer-Verlag Berlin Heidelberg 2010
478 19 Physical Control

19.2.2 Surface Films and Polystyrene Beads oxygen content, all pupae and nearly all fourth-instar
larvae die within 1 h of an application of 0.6 ml/m2. In
When surfactants and monomolecular organic surface polluted ponds with a higher dissolved oxygen content,
films are used against mosquitoes they exert their con- an application rate of 0.8–1.0 ml/m2 is necessary for
trol by physicochemical modification of the air–water 100% mortality of pupae. First-instar to early fourth-
interface (Garrett and White 1977). Larvae and pupae instar larvae are killed only by very high doses, since
cannot penetrate the film at the water surface to obtain they can obtain sufficient dissolved oxygen through the
atmospheric oxygen, and newly emerged adults will integument, without access to atmospheric oxygen. In
drown on the treated water surface. Their effectiveness practice, the film is applied as a liquid formulation at an
in controlling mosquito larvae and pupae is attributed average application rate of 7.5 l/ha (0.75 ml/m2). To
to a reduction in water surface tension, with a subse- ensure maximum efficacy, application has to be very
quent wetting of tracheal structures resulting in anoxia, carefully timed, to coincide with the period when late
rather than chemical toxicity. Large numbers of film- fourth-instar larvae and pupae occur in the breeding
forming surface active agents were evaluated as mos- sites. Depending on environmental factors such as
quito larvicides (Mulla 1967a,b), and some of these water temperature and sunshine, the film is active for
were found to have potential for practical mosquito only 6–10 h.
control programmes. Although the organic surface film is relatively selec-
tive, it does have some adverse effects on other surface
breathing arthropods, such as water bugs (e.g.
Notonecta glauca), which are highly sensitive, and
19.2.2.1 Liparol some water beetles (e.g. hydrophilids and dytiscids).
Because of the effect on surface tension of the water,
A self-spreading biodegradable surface film called arthropods which live on the water surface, such as the
“Liparol” was developed by Schnetter and Engler striders (Gerris spp.) are also affected (Becker and
(1978). This substance is a mixture of soybean lecithin Ludwig 1981). Other aquatic organisms that live
and paraffin, with carbon chains containing between entirely within the water, such as fish, are unaffected.
12 and 14 carbon atoms.
Lecithin, as a macromolecule with hydrophilic
and hydrophobic ends, acts by reducing the surface 19.2.2.2 Monomolecular Surface Films (MSF)
tension of the water body. The hydrophilic end
spreads on the water surface, whereas the hydropho- Monomolecular surface films consist of nonionic sur-
bic end holds the paraffin film at the air-water inter- factants, that have been routinely used in other pro­
face. The mode of action is based partly on the ducts such as detergents and cosmetics for almost 30
interaction of the hydrophobic end of the lecithin years. When used as mosquito larvicides, they are
molecule with the hydrophobic layers within the applied to water and spread spontaneously and rapidly
pupal trumpet or the larval siphon. When a pupa over the surface to form an ultrathin film about one
pierces the water surface covered by the film, the molecule in thickness (monomolecular layer). Their
lecithin enters the trumpet and covers the hydropho- mode of action is physical rather than chemical in that
bic layer of the trumpet. When the pupa dives again, they lower the water surface tension and thus disrupt
the hydrophilic end of the lecithin is orientated normal development of mosquitoes. Mosquito larvae
towards the inner parts of the trumpet, so allowing and pupae normally use the water surface for long
water to enter the trumpet and killing the larva. In periods when breathing, feeding (larvae) and/or rest-
addition, the pupae and the larvae are unable to pierce ing, and the presence of the monomolecular layer kills
the water surface and remain there, due to the reduced them by inhibiting proper orientation at the water sur-
surface tension, and to the repulsion effect of the face and/or by wetting and flooding tracheal structures,
hydrophilic end of the lecithin molecule. causing anoxia.
At a rate of 0.6–1.0 ml/m2, the lecithin mixture is Monomolecular surface films for mosquito control
effective against late fourth-instar larvae, and pupae. In were developed during the 1980s, but they have yet to
polluted ponds with a clear surface and a low dissolved gain wide acceptance in mosquito control programmes.
19.2 Physical Control of Immature Mosquitoes 479

They have been sparingly used in the United States tion, is usually the cause of poor kill of larvae and
in floodwaters, brackish waters, and ponds. They have pupae. However some Culex species are adapted to
also been used in conjunction with other mosquito surviving in water with an extremely low oxygen
control agents as part of an integrated vector manage- concentration, Levy et al. (1982) found low efficacy
ment (IVM) approach. MSFs are of low toxicity, and against such species when they were treated in habi-
are appropriate for use on potable water. tats with high dissolved oxygen. The poor efficacy is
At present, two MSF products are commercially due to the ability of the larvae to use cuticular respi-
available for use as mosquito larvicides and pupicides. ration, and to store air in their tracheal system.
These products are Arosurf® MSF (ISA-2OE or However, pupae are significantly more susceptible to
66-E2) and Agnique® MMF. The use of Arosurf MSF the treatment.
(iso-stearyl alcohol 20E) as a mosquito larvicide was Quantitative studies by Hester et al. (1989) showed
first reported by Garrett (1976), while Agnique was that a single treatment of Arosurf MSF applied at a rate
evaluated in the field in the late 1990s and first reported 0.94 ml a.i./m2 in a 1:9 Arosurf to water mixture by
by Ali (2000). The two products are chemically identi- volume, did not significantly affect the exposed aquatic
cal (ethoxylated iso-stearyl alcohol) and are made vegetation. Effects of Arosurf MSF on a variety of
from renewable plant oils. Arosurf MSF is a viscous, aquatic nontarget organisms have been studied
clear liquid that may be applied to the water surface extensively.
without dilution. However, it contains significant In field situations, Mulla et al. (1983) tested Arosurf
amounts of polyethylene glycols (PEGs), and if mixed MSF at 4.67–7.0 l/ha and reported no apparent adverse
with water in a sprayer without high-shear agitation, it effects on nontarget organisms, such as mayfly naiads
has a tendency to gel, making application difficult (Callibaetis pacificus), diving beetle adults (Berosus
(Mulla et al. 1983). Agnique MMF is a more refined metalliceps), ostracods, and copepods.
product, without PEGs. Again it is typically applied However, field evaluation of the same rate of
undiluted, but if dilution with water in the sprayer is Arosurf MSF by Takahashi et al. (1984) indicated that
required, high-shear agitation is still necessary. Thus, corixids, notonectids, clam shrimp, and a species of
the main difference between Arosurf MSF and Agnique adult beetle were actually affected but all, except the
MMF is that the latter is chemically purer than the for- clam shrimp, had recovered to pre-treatment population
mer. To date, the majority of published studies have levels by 3 days after the treatment.
involved Arosurf MSF, although it is believed that the In an analysis of the available tools to control poten-
efficacy of Agnique MMF is similar, as both products tial mosquito vectors of human and animal diseases in
are chemically identical. Available information indi- New Zealand, Stark (2005) emphasizes that some
cates that the physical and chemical properties, appli- mosquito larvae have low susceptibility to monomo-
cation rates, and safety of Agnique MMF are also lecular surface films because they have little or no sur-
comparable with those of Arosurf MSF (Nayar and Ali face contact (Coquillettidia spp., Culex pilosis, Culex
2003). erraticus and Mansonia spp.). However, adults of these
Since their first use, the efficacy of monomolecular species may still be susceptible when laying eggs or
surface film larvicides has been demonstrated on many emerging to the adult stage. The same author reports
mosquito species in a wide variety of aquatic habitats that MMFs can persist in the field for up to 22 days
(Levy et al. 1981, 1982; Mulla et al. 1983; Takahashi under certain conditions, but results of most studies
et al. 1984). These studies show that Arosurf can be indicate that these products break down relatively
applied in polluted water habitats at surface dosages as quickly in the environment and are often undetectable
low as 0.33 ml/m2, and suppress more than 95% of the 48 h after application.
immature stages of Culex spp. Similar levels of control A recent study by Bashir et al. (2008) shows the
were achieved by ground and aerial applications impact of Agnique MMF applied at 0.25 ml/m2 to
against immature stages of Oc. taeniorhynchus and small pools in Sudan. One application of the product
Oc. infirmatus in salt marsh habitats in Florida. completely controlled (100%) pupae within 24 h and
Disruption of the integrity of the film over the gave 92.6% reduction of L3–L4 larvae of An. arabien-
water surface by wind, heavy rain or by high concen- sis a week after treatment. In general, the susceptibility
tration of algae and/or other emergent aquatic vegeta- of the immature stages of mosquitoes showed the
480 19 Physical Control

following ranking: pupae > instars L3–L4 > instars of the beads generally ranges between 4 and 5 mm but
L1–L2. Agnique MMF affected populations of anoph- laboratory tests have shown that smaller beads of
elines faster than culicine species. However, to obtain 2 mm give a more compact “carpet” which is less pen-
continuous mosquito control in these breeding habi- etrable by mosquitoes of all aquatic stages (Curtis and
tats, treatments need to be carried out at least every 7 Minjas 1985). A 2 cm thick layer of 2 mm beads is
days. sufficient to eliminate mosquito breeding. The beads
MMFs are especially useful in controlling late spread satisfactorily when still wet from the “cooking”
fourth-instar larvae and pupae because most of the process. There is no change in mass during the expan-
other commercially available larvicides and pupicides, sion process, so the weight of the polystyrene required
such as insect growth regulators (diflubenzuron, meth- per pit is the same whether it is assessed before or after
oprene, etc.) and stomach poisons (B.t.i. and B. spha- expansion. The relative merits of factory or on-site
ericus) have relatively reduced larvicidal or pupicidal expansion of the beads depend on the ease and cost of
effects on these stages. transport. About 1.5 tons of polystyrene has been
Monomolecular film products may be mixed with shown to be sufficient for the treatment of 3,000 venti-
other larvicides for more immediate control of all lar- lated pit latrines (500 g/pit latrine) each with a cross-
val instars (particularly fourth-instar) and pupae, and section area of approximately 1 m2. Such treatments
could also be particularly useful against strains resis- have been routinely applied in Zimbabwe, as a precau-
tant to conventional larvicides. Essentially, monomo- tion against mosquito breeding during the first months
lecular films can be used for mosquito control in areas of life of pit latrines.
where the surface films of these products are likely to The use of expanded polystyrene beads can bring
remain undisturbed (no wind action or any other inter- down the mosquito population within a short period of
ference) for sufficient time to interfere with larval and time. It does not require frequent application as with
pupal suspension at the water surface, and with adult other conventional insecticides, since the beads remain
emergence. on the water surface for a considerably longer dura-
Some disadvantages of using the monomolecular tion, and are not environmentally harmful. Even if the
films are: (a) they are nearly invisible on the water sur- water body dries out, the beads remain in place and are
face and require frequent testing for their presence by refloated when the water level rises again. They need
placing a few drops of an indicator oil on the water replacing only when lost due to flooding. They can be
surface and checking for a reaction, which is time- used to control mosquito breeding in a range of shel-
consuming, (b) they are less effective where emergent tered stagnant water habitats such as cesspools and
vegetation and floating debris are present, and (c) sus- water storage cisterns.
tained winds tend to make the films pile up in localized Many trials on the effectiveness of expanded polysty-
downwind areas. rene beads in pit latrines and other types of habitats for
the control of mosquitoes have been carried out in differ-
ent parts of the world. A dramatic reduction in the emer-
19.2.2.3 Polystyrene Beads gence of C. quinquefasciatus was observed from pit
latrines treated with expanded polystyrene beads, as com-
Mosquito larvae must penetrate the water surface to pared to untreated pit latrines (Sivagnaname et al. 2005).
breathe air. Curtis and Minjas (1985) cited the idea of The effectiveness of the layers for long-term pre-
Reiter (1978) using floating layers of nonbiodegrad- vention of mosquito emergence from treated pits was
able expanded polystyrene beads (EPB) at confined reported by Curtis and Minjas (1985). The authors car-
mosquito breeding sites: for example, wet pit latrines, ried out community-wide trials in Zanzibar and India
cesspits and flooded cellars. to control adult Culex populations and the filariasis
Unexpanded polystyrene beads contain pentane in that they transmit. In Zanzibar, a 1 cm-thick layer of
solid solution in each bead. Heating the beads to about 2-mm diameter polystyrene beads was applied to all
100°C in boiling water softens the plastic, and causes 500 wet pit latrines in a community of 12,000 people.
the pentane within the beads to expand rapidly. The treatment reduced the number of adult Culex that
Expansion to the required diameter can be achieved entered bedrooms by 98%. This was coupled with a
within five minutes with occasional stirring. The diameter single campaign of mass treatment of the community
19.4 Conclusions 481

with diethylcarbamazine (DEC). The campaign ini- carbon dioxide, water vapour, heat, and octenol as
tially reduced the prevalence of microfilarial infection attractants. The mosquitoes are typically killed either
from 49% to 10%. During the next 4 years, the contin- by desiccation within the device, or by high voltage
ued near-elimination of Culex prevented cured people grids. He describes operational use of mosquito traps
from being reinfected, and prevalence declined to 3% on an isolated island surrounded by salt-marsh, in
(Maxwell et al. 1999). Another Zanzibar community which Oc. taeniorhynchus was very abundant. Mosquito
used a DEC campaign but no mosquito control and Magnet Pro devices were placed around the island at a
showed a similar initial reduction but, in the longer rate of one device/0.44 ha. After about 2 weeks trap-
term, there was resurgence towards the original level ping, mosquito numbers were reduced by >80%, and
of prevalence. Comparable results were obtained in these results were repeated over several consecutive
a 2-year campaign using DEC and Ivermectin mass- years. Other evaluations of mass trapping have not been
treatment of two South Indian communities, with or so successful (Henderson et al. 2006). In light of the
without polystyrene bead treatment of Culex breeding potential for rapid increases in mosquito numbers, and
sites in bathroom water soakage-pits (Reuben et al. the diversity of species in many areas, many of those
2001). Again, as long as the drug treatment continued, involved in mosquito control remain skeptical about the
the results were similar in the two communities. potential and relevance of mass trapping to the majority
However, in the community that did not use polystyrene of mosquito control situations.
beads, once drug treatment was halted then filaria-
infective Culex appeared the following year. By con-
trast, in the community that used polystyrene beads to
suppress the mosquito population to a low level, no 19.3.1 O
 ther Technology: Novel
infective Culex were found. Mass drug administration Technology or New Tool
coupled with the use of polystyrene beads is now con-
sidered to be a practical approach to the suppression of There have been recent reports of the development of a
lymphatic fila­riasis. By this combination of chemother- laser device for mosquito control (Guth 2009). The
apy and vector control, suppression of the disease may be device is claimed to be able to detect individual flying
faster than either method used alone (Curtis et al. 2002). female mosquitoes and destroy them with a burst of
In several European countries, the problem of leak- laser energy. It has been proposed that the devices
ing sewer pipes in cellars leading to indoor breeding of could be mounted as a “fence” to protect residential
human-biting Culex pipiens molestus mosquitoes has areas against incoming mosquitoes.
been reported. These mosquitoes are likely to be the
main vectors of West Nile virus. Polystyrene beads
work well in flooded cellars and may have a role in the
control of this newly emerging disease (Curtis 2005). 19.4 Conclusions

Physical control encompasses a broad range of tech-

niques. From the use of oil in the early days of mos-
19.3 P
 hysical Control of Adult
quito control, through the use of mono-layers,
Mosquitoes polystyrene beads, traps, and now lasers, the technol-
ogy continues to develop. Physical control techniques
Mass trapping has been considered for control of mos- are attractive in that they tend not to be subject to the
quitoes, and in recent years has attracted more atten- same regulatory constraints as pesticides, they are
tion. Weidhaas and Haile (1978) conducted a theoretical effective against mosquitoes resistant to conventional
appraisal of the potential of trapping, and estimated that insecticides, and it is likely that mosquitoes will have
around 40% of the population would need to be trapped difficulty developing resistance to most techniques.
daily to provide effective control. Kline (2007) reviewed However, although physical control techniques have
progress and development in mass-trapping technology, attracted increased attention recently as components of
and lists a number of commercially available mosquito IVM, they remain at present, relatively restricted in
trapping devices, using various combinations of light, application.
Chapter 20
Genetic Control of Mosquitoes

20.1 Introduction that mate with indigenous females, yet produce no fer-
tile offspring. This approach is generally known as the
The history of the genetic control of mosquitoes goes Sterile Male Technique, although the most recent
back about half a century, when Knipling (1959) realized advances do not actually require sterilization of the
that the fertility of monogamous female organisms could males. A number of variants of Sterile Insect Techniques
be readily compromized as a result of mating with a ster- (SIT) have been evaluated in the field.
ile male. Since that time, the development of the science Alternatively, there is the approach of population
and technology that supports this approach to mosquito replacement. The objective is to identify genes, or create
control has accelerated greatly, in line with very rapid genetic constructs, that render mosquitoes refractory to
progress in the field of genomics in other disciplines, the selected disease (i.e. they cannot support develop-
such as healthcare and agriculture. The recent publica- ment of the pathogen). These refractory genes are linked
tion of the full genome sequence for Anopheles gambiae with a driver so that once released, the indigenous
(Holt 2002) has greatly enhanced the ability of scientists vector population is gradually replaced with a modified
to elucidate the working of mosquitoes at a molecular, one that is unable to carry disease. This approach is not
biochemical and genetic level, and to develop novel currently as close to operational use as SIT.
approaches to their management. There are yet major Genetic control is not just an alternative to conven-
challenges facing the widespread use of genetic tech- tional control techniques but offers some very specific
niques for the control of mosquito vectors of disease. advantages. The technique relies on the natural behaviour
Nonetheless, the continued global impact of vector-borne of the released mosquito to enable it to find and mate
diseases, the extent of constraints on the development with members of the indigenous population. The released
and use of more conventional control techniques such as mosquito is unconstrained by the problems that restrict
insecticides and widespread drug resistance, create a human access and as a result, the intervention is taken by
situation where investing research effort in exploring the the insect to innumerable places that a conventional tech-
potential of the technique, is considered worthwhile. nology may be unable to find or reach. This is important
The prospect of practical genetic control techniques in both rural and urban environments or where transport
appeared sufficiently attractive and achievable for the and infrastructure are poor or where political instability
establishment of a “genetic strategy to deplete or inca- or military activity prevents comprehensive access. Other
pacitate a disease-transmitting insect population” to be advantages arise from the species specificity of the tech-
adopted as one of the Grand Challenges in Global nology. Each genetic mechanism is targeted at one spe-
Health (Varmus et al. 2003). cies only and should have no impact on related mosquito
The term “genetic control” actually covers a range species or on other insects or animals. This specificity
of technologies and strategies. Currently, work on the brings with it the hope of a very precise intervention with
genetic control of mosquitoes and mosquito-borne dis- little or no environmental or public health repercussions.
eases is proceeding on two main fronts: Nonetheless, as outlined below, a responsible approach
On the one hand, there is the objective of eliminat- to the development and use of this innovative technology
ing entire populations of a particular species of mos- requires that due consideration must still be given to the
quito by mass releases of modified male mosquitoes risk of unplanned consequences.

N. Becker et al., Mosquitoes and Their Control, 483

DOI 10.1007/978-3-540-92874-4_20, © Springer-Verlag Berlin Heidelberg 2010
484 20 Genetic Control of Mosquitoes

The two main approaches to the genetic control the USA (Wyss 2000), and eventually from Central
of mosquitoes, i.e. Population Elimination, and America as far south as the Panama Canal. The suc-
Population Replacement are examined below. cess of this programme was instrumental in creating
a climate in which further research and developments
in this area could take place.
The sterile insect technique involves several sepa-
20.2 P
 opulation Elimination Via the
rate stages.
Sterile Insect Technique (SIT)

20.2.1 Introduction 20.2.2 Rearing and Sexing

The potential success of the SIT hinges around the fact

Given the need to numerically overwhelm the indige-
that female mosquitoes are monogamous, i.e. they
nous mosquito population, a mass-rearing technique
mate once only, and use the sperm stored in their sper-
needs to be developed for the target species. The tech-
matheca to fertilize each successive batch of eggs. If
nique and facility needs to provide high insect num-
that mating happens to be with a sterile male, then that
bers of uniform quality at an acceptable cost. This
female will lay only sterile eggs, and will not contri­
inevitably requires research into handling and feeding
bute to the next generation of mosquitoes. If sterilized
techniques, pathogen prevention, and automation
male mosquitoes can be released in sufficient numbers
(Dame et al. 1974).
and over a sufficiently extended period, so that they
Mass release of females together with males would
out-compete the indigenous males in terms of mating
be completely counter-productive, because the females
with the females, then the population should decline to
could enhance local disease transmission, and mate
extinction.
with the sterile males, reducing the impact on the
The perceived advantages of SIT are that it: indigenous population. Sterile male release pro-
grammes, therefore, require a stage in which males are
• Is highly specific to the target species.
separated from females.
• Works better at lower indigenous insect numbers,
For culicine species, the male and female pupae can
providing released numbers are maintained, the pop-
often be separated mechanically, on the basis of pupal
ulation declines progressively towards extinction.
size, using calibrated screens (Bellini et al. 2007). For
• Relies on the well-developed ability of the male
efficient pupal sexing using mechanical separation, the
mosquito to locate and mate with female mos­
rearing technique must be sufficiently standardized to
quitoes. This behaviour will take place even in areas
ensure a very consistent pupal size. However for
where conventional control techniques are not
anopheline mosquitoes, although there is sufficient
easily used.
sexual dimorphism with some species to allow mechan-
• Can if necessary, be “switched off,” i.e. the releases
ical separation, with most there is insufficient differ-
halted, after the programme is underway.
ence for this technique to work. Alternative techniques
Knipling (1959) realized the potential of this tech- have therefore been developed to enable separation of
nique for insect control, and practical developments the sexes with anophelines.
then took place against a number of target pests. Genetic sexing systems have been developed by
Probably the best known was against the New World exposing batches of mosquitoes to radiation followed
screwworm fly (Cochliomyia hominovorax), which by crossing and selection of the resultant mosquitoes.
was a serious pest of cattle in southern USA and This has resulted in the establishment of strains of mos-
Central America. A system for mass-rearing and ster- quitoes in which resistance to propoxur (Kaiser et al.
ilization of the screwworm pupae was developed, 1979, working on An. albimanus) or dieldrin (Lines
together with a programme of aerial distribution. The and Curtis 1985, working on An. arabiensis) has been
first field trials were carried out in the early 1950s, translocated onto the Y-chromosome and is, therefore,
and by 1959 Florida was declared free of screwworm. male-linked. Exposure of batches of mass-reared larvae
Subsequently the fly was eradicated from the rest of of these strains to the appropriate insecticide results in
20.2 Population Elimination Via the Sterile Insect Technique (SIT) 485

elimination of the females, and survival of the males. offspring. It was known that crosses between strains of
However, there is a tendency for such genetic systems the same species from different locations were sometimes
to be unstable (Coleman and Alphey 2004), so that unable to produce fertile offspring. These inter-strain
occasional purging is required to avoid the formation of fertility differences were shown to be due to maternally
resistant (and therefore surviving) females. inherited entities, and the phenomenon was termed
For An. stephensi, a transgenic strain has more cytoplasmic incompatibility. Releases of mass-reared
recently been developed in which an enhanced green mosquitoes that were incompatible with the local strain
fluorescent protein gene is expressed in male insects had a similar impact on sterilization achieved via chem-
throughout development. This has enabled the sexes to icals or radiation (Laven 1967). These maternally
be separated efficiently and automatically as early as inherited entities have since been recognised as being
the third larval instar (Catteruccia et al. 2005). Other the intracellular symbiont Wolbachia. These symbionts
genetic sexing techniques are under development for are not present in anophelines, so this technique is not
other species, including Ae. aegypti [St. aegypti]. appropriate to control of malaria vectors.
The release of insects with a dominant lethal (RIDL)
gene is a variant to SIT that is currently under consider-
ation. In this technique, a strain of mosquitoes carrying
20.2.3 Male Sterilization a repressible female-specific lethal gene is developed.
Removal of the repressor during mass-rearing enables
Sterilization of the male pupae has been achieved by a male-only mosquitoes to be produced without the need
variety of techniques: for chemosterilization or irradiation and the resulting
Chemosterilization is typically carried out by loss of fitness. The released males are not sterile, but
immersion of the pupae for a fixed period of time in a carry a female-specific lethal gene(s). Mating between
standard solution of an alkylating aziridinyl compound, the RIDL male and wild females, therefore, result in
such as thiotepa or bisazir. High levels of sterility may males only. These males would carry the RIDL genetic
be achieved, with minimal loss of fitness (Seawright construct in heterozygous form, and so would in turn,
et al. 1977). However use of large-scale chemosterili­ contribute to the elimination of females in subsequent
zation has largely ceased now, partly due to concerns generations (Alphey and Andreasen 2002).
about safety to staff working with these potentially
mutagenic chemicals.
Irradiation is now the most commonly used tech-
nique. It is typically the pupal stage that is exposed to 20.2.4 SIT in Practice
the gamma rays, but work has also been carried out on
adults. The gamma source used is typically cobalt-60 SIT has been used in practice against mosquitoes on
with a dose in the range 70–120 Gy. The exposure numbers of occasions (Benedict and Robinson 2003),
induces dominant lethal mutations in the sperm of the sometimes to explore and validate aspects of the tech-
male mosquitoes. The lower doses cause partial steril- nique and sometimes to attempt to control mosquito
ization, while higher doses induce a more complete populations. Release of the sterilized males is ideally
level of sterilization but are associated with damage to carried out at a time when the numbers of the indige-
other cells within the male mosquito, causing a nous insects are at a minimum. This may be achieved
decrease in fitness and competitiveness (Helinski and via pre-release use of conventional insect control tech-
Knols 2009). It has been suggested that when using niques, or release may be timed to coincide with a
lower radiation doses, the benefits of higher fitness natural seasonal depression in numbers.
may outweigh the drawbacks of partial sterilization Target species have included Ae. aegypti and Ae.
(Helinski et al. 2006). albopictus [St. albopicta], Cx. pipiens, Cx. tritaenio-
As an alternative to sterilization, other techniques rhynchus and Cx. quinquefasciatus, An. albimanus,
have been used or are under development to ensure the An. culicifacies and An. gambiae. Numbers of sterile
absence of female progeny: males released in individual programmes have ranged
Cytoplasmic incompatibility was one of the early from less than 10,000, up to hundreds of millions over
and successful techniques used to eliminate female a 2 year period. Examples of early successful SIT
486 20 Genetic Control of Mosquitoes

programmes include the project carried out by Patterson In practice however there is likely to be a requirement
et al. (1970), on a small (<1 km2) isolated island in the for significant releases across regions and over time to
Florida Keys. Over a 12 week release period, between ensure rapid dissemination and penetration.
8,000 and 16,000 chemosterilized male Cx. quinque- Developing refractory strains requires full elucidation
fasciatus were released per day. The initial ratio of of the molecular and genetic relationship between para-
released to indigenous mosquitoes was estimated to be site and vector. Plasmodium spp. undergo complex devel-
3:1, while towards the end of the programme, as the opment within the mosquito, going through a number of
indigenous mosquitoes had declined, the ratio had distinct stages, from gametocyte to sporozoite, passing
changed to 100:1. At the end of the release period, a through two separate mosquito cellular barriers; the
reduction of >99% of the indigenous mosquitoes had midgut and salivary gland epithelia. The parasite may be
been obtained. Lofgren et al. (1974) released over 4 vulnerable to attack at each of these stages.
million chemosterilized male An. albimanus over a 22
week period into an isolated mosquito population in a
15 km2 area of El Salvador. By the end of the pro-
gramme, complete elimination of the indigenous mos- 20.3.2 Refractoriness to Pathogens
quitoes had been obtained. Several other projects were
less successful with measurable impacts being modest 20.3.2.1 Natural Immunity-Based Mechanisms
or nonexistent. The reasons for these disappointing
outcomes were most commonly believed to be due to In recent years, there has been intensive research on the
poor male competitiveness (as a result of the mass- immune system of An. gambiae, to improve under-
rearing process and/or the effects of the sterilization standing of the endogenous mechanisms behind the
process), and to a lesser extent to immigration from natural variation in susceptibility to Plasmodium spp.
nearby untreated areas. infection. Genetic and molecular tools such as micro-
satellite markers and microarray platforms coupled
with the use of RNA interference (RNAi) have been
instrumental in helping elucidate the functioning of the
20.3 Population Replacement mosquito’s immune system.
Melanization is a well-known insect immune reac-
tion, and plays an important part in the mosquito’s rela-
20.3.1 T
 he principle of Population
tionship with Plasmodium spp. A genetically selected
Replacement strain of An. gambiae (L3-5) has been shown to melanize
the ookinetes of several Plasmodium species, including
The possibility of creating and releasing a mosquito allopatric P. falciparum, but not sympatric P. falciparum
strain that is refractory to human pathogens was first (Collins et al. 1986). This result indicates the role of
suggested by Curtis (1968b). In its simplest form, this evolution and co-adaption in the development of the
approach requires undertaking several basic steps: relationship between parasite and vector. Lysis of ooki-
netes within the midgut epithelial cells has also been
• The identification or assembly of a gene or genetic
shown to be an important naturally occurring defense
construct that confers refractoriness in the chosen
mechanism. Intensive research has shown the complex-
mosquito species to the chosen pathogen.
ity of the processes involved (Blandin et al. 2004; Osta
• The creation of a driver mechanism which will aid
et al. 2004). A number of genes involved in lysis and
the dissemination and fixing of the new refractory
melanization of Plasmodium spp. have now been identi-
genes within the target insect population.
fied, as well as agonistic genes that appear to protect the
• The linkage of refractory construct and driver.
parasite from these processes.
• The release of the new mosquito strain.
Work on mosquito resistance to dengue is also
Once the strain has been released, the dissemination underway in a range of areas. Ramos-Castanada et al.
and replacement process should be self-perpetuating, (2008) looked at the role of nitric oxide, naturally
and in theory the release of a single modified mosquito produced in midgut epithelial cells, in inhibiting repli-
could introduce the construct to an entire population. cation of dengue virus within mosquitoes. Within a
20.3 Population Replacement 487

dengue-susceptible strain of Ae. aegypti they found no occurring cecropins, has been shown to have activity
evidence of replication of dengue virus genome when against Plasmodium spp. Yoshida et al. (2001) linked
a nitric oxide donor was added to the infective blood Shiva-1 to a single-chain variable fragment (scFv)
meal. Interestingly, when a nitric oxide synthesis directed against the P. berghei Pbs21 protein. The immu-
inhibitor was added to a dengue infective blood meal notoxin was expressed in Escherichia coli that were fed
provided to An. albimanus, then dengue virus replication to A. albimanus which, when infected with P. berghei,
did take place within the anopheline. showed significantly reduced oocyte numbers.
In general, results of research to date on refractori-
ness have indicated significant challenges still ahead.
20.3.2.2 Engineered Refractory Mechanisms The efficacy of the refractory construct must be very
high, in order to have a useful impact on the epidemi-
In addition to identification and genetic selection of ology of the disease (Curtis et al. 2005). Immune
naturally occurring immunity mechanisms, a wide range responses to malaria parasites in convenient laboratory
of other refractory mechanisms have been created. models such as P. berghei, often differ extensively
Ito et al. (2002) selected a short peptide (SM1) from P. falciparum, the human pathogenic species. It is
known to bind selectively to mosquito midgut and sali- unlikely that single genes conferring refractoriness to
vary gland epithelia. A transgenic strain of An. ste- key pathogens will be identified. Instead, it is likely
phensi in which SM1 was expressed in the midgut, that multiple genes will have to be involved to bring
showed a greatly reduced ability for transmission of P. about a sufficient reduction in parasite development
berghei. Antimicrobial peptides (AMPs) that attack within the mosquito to have any useful epidemiologi-
the membrane of microorganisms causing cellular cal impact. It is likely that such a combination will be
damage are also being explored. For example, trans- associated with a fitness cost, and any improved fitness
genic over-expression of genes encoding for Cecropin of the mosquito obtained by avoiding infection is likely
A in the midgut of An. gambiae provided a significant to be outweighed by the cost of the refractory genes.
reduction in the number of developing oocysts (Kim
et al. 2004), although work with another endogenous
AMP, Defensin A, showed that it provided protection
against gram-positive bacteria but not against 20.3.3 Genetic Drivers
Plasmodium (Blandin et al. 2002).
However, Christophides (2005) has urged caution For the reasons indicated above, a means has to be
in the selection of immunity genes for use in trans- found to ensure that the refractory construct spreads
genic control strategies, as stable over-expression of through the target population faster than by classical
genes conferring nonspecific immunity may affect sus- Mendelian inheritance alone. A number of mechanisms
ceptibility to bacteria-based pesticides such as Bacillus have been proposed that may, if successful, drive the
thuringiensis, which may then render these very useful refractory construct into a wild mosquito population.
larvicides inactive.
Franz et al. (2006) used a transgenic approach to
develop a strain of Ae. aegypti that was resistant to 20.3.3.1 Transposable Elements
infection by dengue type 2 viruses. They used the nat-
ural antiviral RNAi pathway to construct an effector Transposable elements or transposons are sequences
gene that was inserted into the genome of a strain of of DNA that have the potential to move around and
Ae. aegypti using a mariner MosI transformation sys- propagate rapidly through a genome and are therefore
tem. The new strain then not only showed reduced of interest as gene drivers. Natural transposons have
viral antigen when fed an infective blood meal, but been found in An. gambiae (Arensburger et al. 2005).
also showed diminished virus transmission when com- Laboratory strains of An. stephensi, An. albimanus and
pared to control mosquitoes. An. gambiae have now all been transformed by intro-
Paratransgenic strategies have also been examined as duction of transposable elements carrying markers into
a means of establishing mosquito refractoriness to the germ line. Research continues into the potential of
pathogens. Shiva-1, a synthetic analog of naturally these structures as practical gene drivers.
488 20 Genetic Control of Mosquitoes

20.3.3.2 Meiotic Drive • The linkage between driver and refractory construct
must not be vulnerable to uncoupling through
A variety of meiotic drive mechanisms are naturally recombination. Such a change may result in the
widespread among insects and mammals. Driver genes “empty” driver, once released from its refractory
bias the normally random segregation of chromatids genetic load, spreading through the population to
during segregation to aggressively introduce their no useful effect.
inheritance into populations. Endogenous meiotic drive • The driver mechanism must be capable of being rea-
systems have been reported in Ae. aegypti and Cx. sonably easily modified in the laboratory to ensure
­pipiens. Cage scale trials have been carried out with Ae. that production of a number of different modified
aegypti, to assess the ability of a strong meiotic drive mosquito lines, compatible with local strains or even
(T37 strain) to bring about population replacement and species, is possible. Many vectors are actually
have given encouraging results (Cha et al. 2006). species complexes, different members of which may
have different relative importance as vectors in
neighboring regions, or in different seasons.
20.3.3.3 I ntracellular and Extracellular • The driver mechanism should be capable of being
Symbionts adapted to carry constructs that confer refractori-
ness to a range of different pathogens.
Intracellular symbionts such as Wolbachia can be spread • Finally, the mechanism must be sufficiently robust
through populations relatively rapidly via the mecha- to be able to maintain effective refractoriness levels
nism of cytoplasmic incompatibility. It has been sug- even when faced with repeated immigration, as will
gested that by insertion of appropriate genes or constructs happen for example around the fringes of an inter-
into the bacteria, they could become a dispersal vehicle. vention area.
The genome sequence of the strain of Wolbachia sp.
found in Cx. quinquefasciatus has very recently been James (2005) proposed the addition of two further cri-
described (Salzburg et al. 2009). Work is underway on teria to the above list, namely:
several mosquito species with encouraging results, e.g. • The drive mechanism should prevent the construct
Ae. albopictus (Sinkins 2004). Although anophelines do from moving beyond the target species.
not naturally carry Wolbachia sp., it has now been shown • The drive mechanism should not facilitate selection
that the bacterium can be successfully transferred into for pathogens strains that are resistant to the refractory
An. gambiae cell cultures (Rasgon 2006). mechanism or for more virulent pathogenic strains or
make the mosquito able to act as a vector of pathogens
for which it was previously not competent.
20.3.3.4 Driver Requirements
Coleman and Alphey (2004) additionally proposed that
Whatever the driver mechanism(s) used, Braig and the drive system should ideally be recallable, so that in
Yan (2001) have proposed seven ground rules with the event that the trait had unforeseen and harmful
which the driver mechanism must comply, in order to effects, the modified vectors could then be eliminated
be acceptable: from the population.
• The driver must be sufficiently effective to compen-
sate for the “load” (i.e. negative fitness) placed on it
by the refractory construct. 20.4 E
 thical, Legal and Social
• The driver must disseminate the construct through Implications of the Use
the natural mosquito population at an acceptable
of Genetic Techniques
speed. Interventions that take many years to have a
useful effect are unlikely to be acceptable. for Mosquito Control
• The driver must be capable of carrying a possibly
substantial genetic construct consisting of numbers Although genetic technology may appear to offer
of genes and regulatory elements that together con- major benefits to those at risk of vector-borne diseases,
fer refractoriness. a number of issues nonetheless remain to be resolved.
20.4 Ethical, Legal and Social Implications of the Use of Genetic Techniques for Mosquito Control 489

Suspicions about genetic technology go back a long ethics and legal issues around such releases will need
way. In the 1970s, a valuable and substantial interna- very careful consideration (Knols et al. 2007).
tional scientific programme was underway in India to Concerns over the immunological repercussions of a
assess the potential of a variety of genetic techniques successful genetic control programme have also been
for mosquito control. At a time of national and politi- raised. If the intervention is successful and is maintained,
cal tensions, the unit was falsely accused by some local it is likely that the immunity of the local human popula-
journalists and politicians of being a front for research tion will decline, making them vulnerable to epidemics
on biological warfare sponsored by the USA. The in the event of changes in epidemiology. Although these
response to the accusations on behalf of the unit was same general concerns have been raised in relation to
slow in forthcoming, and ultimately ineffective. At other vector control techniques, such as use of ITNs
very short notice, the entire programme was termi- (Snow and Marsh 2002), there are significant differences
nated by the Indian Government, and the research unit between genetic techniques and conventional vector
closed (Curtis 2007). At the present time, concern over control. The former tends to be very specific, creating the
the use of genetic technology is still high among some possibility that effective genetic control of the principal
sections of the international media, environmental vector may result in a population-wide loss of immunity,
organizations and the public. For example, the contro- which then allows for the possibility that a different
versy over the production and use of genetically modi- strain of the same species or a secondary vector may later
fied crop plants is widely recognised, and continues emerge to trigger an epidemic (Knols et al. 2007). Such
despite the best efforts of involved parties to address immunological aspects of large-scale vector elimi­
concerns. This debate has slowed investment in and nation programmes need to be considered carefully
development of such technology. With regard to new and the post-release situation monitored very closely.
developments in the genetic control of disease vectors,
it is clearly essential to work with stakeholders at an
early stage in order that the benefits of the work are 20.4.1 A
 bsence of Community
clearly communicated and any concerns fully Participation
addressed. Failure to be proactive in terms of involve-
ment and communication could jeopardize much of
One other potential criticism of the genetic approach to
this work. Involvement of such stakeholder groups
vector control is that it represents a move away from
may result in a broadening of the scope of the research
greater community participation (which is seen as a desir-
necessary for the successful implementation of genetic
able and important component of vector management),
control technology. Determination of the impact of
back to a more centralized and technocratic approach. On
transgenic mosquitoes on predators such as spiders or
the assumption that the genetic approach is effective, this
birds or of the potential for such mosquitoes to become
may not be entirely negative because community partici-
vectors of diseases not currently carried by mosquitoes
pation is seldom self-sustaining, and requires continual
may become critical to the continuation of such work
inputs (Coleman and Alphey 2004). In addition, genetic
(Coleman and Alphey 2004).
control measures as currently envisaged are species
The process for seeking ethical and legal approval for
specific, so even if one mosquito vector species is elimi-
large-scale trials or operational use of genetic control
nated, there may still be scope for community-based
technology will need to be examined closely. Trials on
programmes to address other problems such as other vec-
conventional technologies for vector control are typi-
tor or nuisance mosquitoes, houseflies, or rodents.
cally carried out in defined areas, involving a relatively
localized population. The process of obtaining ethical
approval for such work therefore follows conventional
20.4.2 I nternational Committee for
guidelines. By contrast, the genetic driver mechanisms
used in mosquito population replacement strategies are Genetic Control Work
intended to be self-perpetuating and to have the potential
for dissemination across contiguous populations of The issues raised above and others, emphasize the need
the vector. A local introduction of modified mosquitoes for establishment of an independent international coor-
therefore could have international implications. The dinating body for genetic technology work in vector
490 20 Genetic Control of Mosquitoes

control. The overall objective would be to establish a dures, liaise with and coordinate the work of the scien-
broad coalition of all those with an interest in the appli- tific community and countries in which genetic releases
cation of genetic technology for vector control. The may be carried out, and involve other stakeholder
body would inter alia establish standards and proce- groups (Knols et al. 2007).
Chapter 21
Personal Protection

21.1 Introduction been used successfully in several regions: China,

Thailand, Latin America, and some African countries.
Personal protection is a key component in the preven-
Over the last two decades, work on insecticide impreg-
tion of mosquito nuisance and mosquito-borne diseases.
nated bednets and curtains have grown from small
Measures may include: simply staying indoors, wear-
scale tests to the operational use of more than 36 mil-
ing clothing that minimises exposed skin, use of per-
lion long-lasting insecticidal nets (LLINs) which were
sonal repellents, or use of insecticides on bed nets.
distributed in Africa in 2006 (RBM programme). This
Insecticide treated nets (ITNs) for example play a major
was almost triple the number distributed in 2004
role in the global campaign against malaria. Even
(WHO 2008). The concept is to place a small quantity
where local or regionally organised mosquito manage-
of a fast acting insecticide of low mammalian toxicity
ment programme are already in place, individuals may
directly in the path of the host seeking mosquito.
still choose to invest in additional personal protection
Regarding the safety and acceptability of this method
measures. Research shows that in the USA, around one
of mosquito protection, it was stated by WHO that
third of the population use mosquito repellents in any
properly treated bednets should pose no hazard to
one year, while a recent study in India showed that as
those who use them. As a result of its very low mam-
many as 99% of the urban population used personal
malian acute oral toxicity, extremely low dermal toxic-
protection products in some seasons. However such
ity, very low volatility, and high efficacy, permethrin
products are used not only by residents, but are widely
has been widely used for bednet impregnation.
used by tourists visiting mosquito-infested areas, and
Treatment of nets or curtains may be considered the
by military forces deployed to mosquito-infested
most rational form of selective insecticide treatment in
areas. Given the relatively unsupervized way in which
the sense that the treated surfaces are those which blood-
these products may be used by the individual, it is essen-
seeking mosquitoes are bound to encounter and will be
tial that they are carefully developed and evaluated, and
attracted to, in their efforts to approach humans (Mouchet
that each country has a thorough approval system in
1987). According to the costs and availability of fabrics
place. Commercially available products must be prop-
(cotton, polyester, nylon) for bednets, and the very low
erly labelled in all aspects of safe handling and use.
dosages of the pyrethroids required for efficacy on nets,
The following chapter reviews some of the more
net impregnation is affordable for vector control and, if
important personal protection measures.
compared to DDT treatments to protect the same human
population, sometimes cheaper.
Since most Anopheles species bite at night, it has been
21.2 Impregnated Bednets assumed that nets must be useful against malaria.
Moreover, since the majority of malaria vectors prefer to
21.2.1 Conventional Impregnated Bednets feed on humans (anthropophily) and readily enter houses
(endophily), screening is one of the essential measure-
The use of insecticide treated bednets (ITN) for the ments (Curtis 1990). In parts of China and in most African
control of malaria and other vector-borne diseases has countries, evidence has been obtained on ITNs being
gained much interest since the early 1990s. ITNs have effective against malaria. However, it has also been

N. Becker et al., Mosquitoes and Their Control, 491

DOI 10.1007/978-3-540-92874-4_21, © Springer-Verlag Berlin Heidelberg 2010
492 21 Personal Protection

recognised that in many parts of the world, nets may not had not been re-treated within 6 months. These results
give sufficient protection to control malaria, because of indicate that ITNs are optimally effective if used every
local community participation and behaviour where the night and if permethrin is reapplied at least biannually.
bednets are used. The reasons for this are varied and may There was a clear impact of ITNs upon the indoor resting
include insufficient training or education of the residents, densities of both An. gambiae s.l. and An. funestus.
failure by the residents to repair nets or use them appro- Overall, a 71.5% reduction was recorded in the indoor
priately, nets that are inappropriate for the beds being resting densities of fed anopheline mosquitoes in inter-
used, or vectors that bite the residents before they have vention areas compared with control areas. Studies in
gone to bed or after they have risen in the morning. Burkina Faso, and coastal Kenya demonstrated reductions
Nonetheless, a degree of protection from biting and a in indoor anopheline densities by more than 80% in the
decreased malaria incidence when nets are properly used, presence of ITNs or curtains (Bögh et al. 1998; Cuzin-
has been proven in many endemic parts of the world. The Ouattara et al. 1999). The World Malaria Report 2009
impregnation of mosquito nets with deltamethrin and per- shows that more African households own an ITN: 31% in
methrin was adopted for malaria control in some prov- 2008 compared to 17% in 2006. Household ITN owner-
inces of China and parts of Africa (Curtis 1990). In most ship reached more than 50% in 13 high burden African
research studies, impregnation of nets has been done by countries that resulted also in increased ITN use in the pop-
dipping them in an emulsion made by mixing an emulsi- ulation of children under 5 years of age (24% in 2008).
fiable concentrate of the pyrethroid with water. It was also In situations when ITNs cannot provide personal
found that the amount of liquid left after dipping and protection, as in field situations and in military opera-
wringing by hand was almost the same as if the liquid was tions, when it is not practical for the personnel to carry
added until the point of saturation. mosquito nets with them, it is recommended that syn-
Recent publications have shown that a number of thetic pyrethroid treated patches should be made avail-
compounds can be employed as effective anti-mos- able to troops operating in endemic malarial areas.
quito impregnation insecticides (WHO 2002). Based on the results of testing impregnated fabrics,
ITNs or curtains have a profound impact on malaria WHO (2007) recommend that the following active ingre-
transmission in sub-Saharan Africa as shown by reduc- dients may be used to treat bednets (Table 21.1).
tion of various entomologic indices (Bögh et al. 1998;
Cuzin-Ouattara et al. 1999) and more importantly, by
decrease of morbidity and mortality in humans
21.2.2 L ong-Lasting Insecticide
(Phillips-Howard et al. 2003). Malaria transmission in
this area is intense. It is estimated that residents receive Treated Nets
up to 300 infectious bites/person/year with peaks just
after the two annual rainy seasons (Hawley WA, Until recently, all ITNs were typically treated with
unpublished data in Beier et al. 1990). pyrethroid EC formulations, either by the user, health
The effect of permethrin-treated bed nets (ITNs) on worker, or in local factories. These treated nets offered
malaria vectors was studied in western Kenya (Giming much improved protection against malaria, but there
et al. 2003). Indoor resting densities of fed An. gambiae were still limitations such as loss of active ingredient
s.l. and An. funestus in intervention houses were, com- during washing, failure by users to re-treat sufficiently
pared with control houses, 58.5% and 94.5% lower, often, poor insecticide uptake by coloured polyester
respectively. The sporozoite infection rate in An. gambiae nets, and sometimes uneven treatment of polyester
s.l. was 0.8% in intervention areas compared with 3.4% nets during manufacture.
in control areas, whereas the sporozoite infection rates in As a result, a programme to develop Long Lasting
An. funestus were not significantly different between the Insecticide Treated Nets (LLIN) was established. The
two areas. It was estimated that the overall transmission goal was to develop a process that resulted in a single
of Plasmodium falciparum in intervention areas was 90% treatment of the net during manufacture remaining
lower than in control areas. As measured by densities of active for the life of the net. Two approaches were
An. gambiae s.l., the efficacy of bed nets decreased if one eventually established; one in which the pyrethroid is
or more residents did not sleep under a net or if bed nets bound to the surface of polyester netting using a resin,
21.3 Repellents Against Mosquitoes 493

Table 21.1 Suitable insecticides for the treatment of mosquito nets or curtains (WHO 2007)
Insecticide Trade name and formulationa Doseb(mg/m2) Toxicityc oral LD50 of a.id(mg/kg of body weight)
Alphacypermethrin SC 20–40 79
Cyfluthrin Solfac 5EW 30–50 250
Deltamethrin K-Othrine 25 SC 15–25 135
Etofenprox Vectron 10 EC 200 >10,000
Lambdacyhalothrin Icon 2.5 EC Icon 2.5 CS, 10–20 56
Permethrin Imperator 50 EC Peripel 20 EC 200–500 500
a
Recommended formulations, but others may also be appropriate. SC suspension concentrate; EW oil-in-water emulsion; CS capsule
suspension; EC emulsifiable concentrate
b
Doses refer to synthetic netting. Higher doses may be needed for cotton netting
c
Toxicity is expressed as a.i. for rats. It is not necessarily equivalent to hazard
d
a.i. active ingredient

and another in which insecticide is incorporated into Previous work concentrated mainly on simple solutions
polyethylene fibers which then release the insecticide of topical repellents and the chemical treatment of
over several years. Evaluation of these LLINs has clothing to prevent blood-sucking arthropods (Rutledge
shown that efficacy against mosquitoes remains accept- et al. 1978). Current protection is based on controlled
able after 15 – 20 washes (Sreehari 2009). In practice, release personal use of controlled-release arthropod
evaluation of these nets has shown around 3 – 5 years repellent formulations, and the impregnation of fabrics
efficacy (Tami 2004, Kilian 2008). Currently WHOPES with permethrin. Repellents may be applied to the skin,
has full recommendations for LLINs containing per- clothing or in some cases, to screens to prevent or deter
methrin and deltamethrin. A number of other nets, arthropods from attacking humans.
including one containing alphacypermethrin, have The use of topical repellents may still play an impor-
interim recommendations. tant role in the protection of people in areas where no
LLINs cost around US $5, and although initially mosquito control methods are carried out. Several repel-
more expensive than local treatment of nets with an EC lents have been developed for self protection against mos-
formulation, the much longer effective life of LLINs quitoes (benzyl benzoate, butyl ethyl propanediol, dibutyl
makes them more cost effective in the long term. There phthalate, dimethyl phthalate, ethyl hexane-diol, butopy-
are currently extensive operational programmes to intro- ronoxyl, 2-chlorodiethylbenzamide, acylated 1,3 amino-
duce LLINs, primarily in Africa. Millions of LLINs propanole derivates) among which the best known is
have now been distributed in several countries, and these DEET (N,N-diethylmethyl-3-methylbenzamide). They are
programmes are being evaluated to improve distribution used mainly in situations where individual protection by
and access (Hightower 2010). other chemical control methods or by nets and vapourizing
In addition to their use in conventional bed nets, devices is not appropriate.
these long-lasting fibers have also been incorporated Repellents are available in a variety of formulations
into plastic sheeting, which can be used by displaced (liquids, lotions, solid waxes, creams, foams, impreg-
people for making temporary shelters in emergencies, nated wipe-on towelettes, and soaps) and can be dis-
such as following natural disasters or conflict. pensed from tubes, pressurized cans, roll-ons etc. When
applying a repellent, the biting habits of different
mosquitoes should be considered. For general protec-
tion against mosquitoes, all exposed parts of the body,
21.3 Repellents Against Mosquitoes such as arms, legs, and face (except the eye area) should
be treated with repellents.
21.3.1 Repellents on Skin or Clothing Impregnating clothing with a repellent provides
extra protection, and temporary protection can be
Repellents are the most common means of personal achieved with a spray-on application. For longer lasting
protection against blood seeking arthropods and for the effects, clothes should be dipped in a solution of a
prevention of arthropod-borne disease transmission. repellent and a pyrethroid. A combination of permethrin
494 21 Personal Protection

at a concentration of 0.65–1.0 g a.i./m2 and repellents at protection periods (>3 h) did not differ significantly
20 g. a.i./m2, or a total amount of 70 g repellent a.i.(s) from those of pyrethrum and citronella oil in the study
for a jacket, trousers and socks, is often used. of Rutledge and Gupta (1996).
Different authors have reported various durations of Several investigators have reported that repellents
repellent activity of several DEET formulations. Gupta can act as attractants when present at low concentra-
et al. (1987) demonstrated that a controlled-release tions, deposits or residues. Dubitskyi (1966) found that
cream formulation of 33% DEET was no more effective vapours of dimethyl phthalate, benzimine, DEET and
than the standard liquid formulation against several spe- some other compounds were attractants to An. hyrcanus,
cies of Australian mosquitoes. Annis (1990) presented a Ae. cinereus, Ae. vexans, Oc. caspius and Cx. modestus.
new extended duration repellent formulation (EDRF) of On the other hand, many materials that are normally
DEET which was significantly more effective than the thought to be attractants have been shown to be repel-
liquid formulation. Although the EDRF provided lents at high concentrations. Smith et al. (1970) reported
between 6 and 12 post-application hours significantly that lactic acid was an attractant to Ae. aegypti at concen-
greater protection than the liquid formulation, the degree trations normally present on the skin and in the breath,
of protection began to decline after 8 h. To provide pro- but repellent at a higher concentration (4 mg/cm2). Thus
tection against disease transmission, depending on the it is vital that the labels of commercial repellents should
formulation, re-application would be necessary before include instructions to wash off or re-apply the repellent
significant decline in repellency occurs, which has been when it is no longer effective.
reported to be 6–8 h post-treatment. Hoch et al. (1995) A recent laboratory study of several different repel-
reported a new extended duration topical insect/arthro- lents conducted in Thailand by Fradin and Day (2002)
pod repellent formulation of DEET which is a multi- demonstrates that DEET-based products provided
polymer sustained-release formulation and has numerous complete protection for the longest duration. Higher
advantages over available repellents including lower ­concentrations of DEET provided longer-lasting pro-
DEET concentration and extended protection time. tection. A formulation containing 23.8% DEET had a
Tests of the new formulation showed 95% or better bit- mean complete-protection time of 301.5 min. A soy-
ing protection from Ae. aegypti and An. stephensi at up bean-oil-based repellent protected against mosquito
to 6 and 8 h, respectively. However, questions have been bites for an average of 94.6 min. All other botanical
raised about its safety and effectiveness against some repellents tested in this study provided protection for
Anopheles species and its aggressiveness to paint, var- a mean duration of <20 min. Currently available non-
nish and some hard plastics. DEET repellents do not provide protection for dura-
Owing to public concerns over safety of synthetic tions similar to those of DEET-based repellents and
chemicals, interest in botanical repellents has increased cannot be relied on to provide prolonged protection in
lately and has stimulated a re-examination of the repel- environments where mosquito-borne diseases are a
lent data going back as far as 1939, when MacNay substantial threat.
published a paper on 38 botanical repellents against However, the long-term usage of DEET is not rec-
northern American mosquitoes. Re-analysis of the ommended, particularly for children, and as a result
MacNay data has been carried out by Rutledge and major chemical companies are actively involved in the
Gupta (1996), using modern statistical techniques. development of synthetic alternatives to DEET and/or
According to these authors, the data showed that pyre- improved formulations to prolong efficacy or increase
thrum extract (1:1 and 1:3 in olive oil) was one of the consumer acceptability. For this reason, when repeated
most effective repellents, providing protection from applications of a repellent are required, one of the nat-
Oc. stimulans, Ae. vexans and Oc. trichurus for about ural products, such as Qwenling should be used.
4.5 h, together with several other materials which Qwenling has been derived from the lemon eucalyptus
acted as repellents for shorter periods of time. Prior to plant in China and contains an active ingredient p-men-
the advent of synthetic repellents, pyrethrum and cit- thane-3,8-diol (PMD). Neem oil has also shown good
ronella oil were widely used in repellent lotions, repellency against Anopheles mosquitoes, and WHO
sprays, smokes and candles. Although pine tar oil, thy- (1997c) has declared it safe for use.
mol and geraniol (among others from the MacNay list) DEET microencapsulation (MC) is a recent formu-
have had comparatively little use as repellents, their lation development in which the repellent is gradually
21.3 Repellents Against Mosquitoes 495

released from a capsule. An experiment carried out on protein (CSP) of Plasmodium falciparum in 842
DEET-treated mosquito netting showed that the for- females of An. gambiae s.l. showed that CSP-positive
mulation repels, inhibits blood-feeding, and kills mos- mosquitoes were equally frequent in treated and con-
quitoes for a period of at least 6 months under trol subjects, indicating that the repellents could pro-
laboratory conditions. N’Guessan et al. (2007) suggest duce a reduction in the number of malaria infectious
that such formulations may have the potential for use bites (Costantini et al. 2004).
on nets against pyrethroid-resistant mosquitoes or on Various characteristics and individual product
clothing or bedding materials distributed in disaster advantages may lead physicians to recommend one
areas, emergencies or refugee camp situations. agent over another.
The history of insect repellents provides insight into
some of the current scientific strategies behind newer
products. Active ingredients currently available include
DEET, botanicals, citronella and, the newest agent, 21.3.2 Mosquito Coils
picaridin (Katz et al. 2008). At present, the US
Environmental Protection Agency’s registered insect At present, the main devices used for mosquito protec-
repellent ingredients approved for application to the tion are mosquito coils, electric mosquito mats and
skin include DEET, picaridin, oil of citronella, and oil liquid vapourizers, with all these methods vapourizing
of lemon eucalyptus. DEET has reigned as the most insecticides into the air using heat from combustion or
efficacious and broadly-used insect repellent for the electricity to kill the insects.
last 6 decades with a strong safety record and excellent Mosquito coils are made from a mixture of active
protection against ticks, mosquitoes, and other arthro- and inert ingredients and are most commonly used in
pods. Newer agents like picaridin and natural products Asia, Africa and the Western Pacific region. The a.i.
such as oil of lemon eucalyptus are becoming increas- usually used in mosquito coils, as well as in other simi-
ingly popular because of their low toxicity, comparable lar products, are pyrethroids (Table 21.2) because they
efficacy, and public approval. Bayrepel®, (a.i. Picaridin) provide quick knock-down action and present little
was tested in Burkina Faso against mosquito vectors to hazard in use. The a.i. in the smoke released when the coil
compare its relative efficacy and persistence profiles to is burnt, deter mosquitoes from the immediate vicinity
DEET. Collection of >49,000 mosquitoes (95% belong- of the burning coil or even from entering houses.
ing to the An. gambiae complex) showed that after an Depending on the size of the room in which the coil is
exposure of 10 h, picaridin based products produced used, and the type of a.i., mosquito biting rate can be
the highest protection against anophelines, followed by reduced by up to 80% (Chavasse and Yap 1997).
DEET. The response of aedines was more variable. Much attention has recently been directed toward
Immunoenzymatic detection of the circumsporozoite the development of non-heated formulations, such as

Table 21.2 Active ingredients suitable for personal protection in household insecticide products
Product Active ingredient Concentration range Toxicitya (oral LD50)b
Mosquito coils d-allethrin d-trans allethrin 0.1–0.30.005–0.3 500500
Transfluthrin 0.02–0.05 >5,000
Prallethrin 0.03–0.08 460
Electric vapourizer mats d-allethrin d-trans allethrin 25–60 mg/mat15–30 mg/mat 500500
Prallethrin 6–15 mg/mat 460
S-bioallethrin 15–25 mg/mat 700
Transfluthrin 6–15 mg/mat >5,000
Liquid vapourizers d-allethrin d-trans allethrin 3–61.5–6.0 500500
Prallethrin 0.6–1.5 460
S-bioallethrin 1.2–2.4 700
Transfluthrin 0.8–1.5 >5,000
a
Toxicity and hazard are not necessarily equivalent
b
Oral LD50 of active ingredient for rats (mg/kg of body weight)
496 21 Personal Protection

fan vapourizers, because of their increased safety and concentrations resulting from burning mosquito coils
ease of use, especially during outdoor activities. could substantially exceed health-based air quality
However, the insecticidal activity and/or the vapour standards or guidelines and suggested that exposure to
pressures of existing pyrethroids are unsatisfactory for the mosquito coil smoke poses both acute and chronic
use with such ambient-temperature devices. However, health risks.
some new compounds like metofluthrin could be used Before smoke-generating mosquito coils can be
both in heated and non-heated formulations. The ultimately replaced with nonsmoke mosquito control
Southern house mosquito (Cx. quinquefasciatus) is the devices, switching to less polluting products may bring
most important target for mosquito coils throughout substantial reductions in exposure and respiratory
global tropical and subtropical zones. Mosquito coils health risk.
containing 0.005% metofluthrin exhibited an efficacy The fifteen controlled trials identified in the system-
exceeding that of burning coils containing 0.2% atic review by Laurance and Croft (2004) provides
d-allethrin against this species, and its relative efficacy consistent evidence that coils inhibit nuisance mos-
is estimated to exceed 40 times that of d-allethrin. quito biting. Different insecticide classes and different
The unusual characteristic of metofluthrin is suf- strengths of the same insecticide, provide differing
ficient volatility to be bioactive at room tempera- levels of control. All this implies that there is a clear
tures. This activity is not seen in the majority of need for standardization and quality control in manu-
knock-down pyrethroids. This characteristic enables facture and sale of mosquito coils. Despite the clear
metofluthrin to be applied in non-heated formula- impact of mosquito coils on mosquito biting, there is
tions such as fan-type, paper and resin emanator. however no evidence that they reduce the risk of
Formulations were evaluated by Ujihara et al. (2008). malaria acquisition (Laurance and Croft 2004).
The fan-type formulation containing metofluthrin
showed high efficacy. Ambient vapourization devices,
where the a.i. is held in paper or resin, and is vapour-
ized without heating or electricity, are easy to use, so 21.3.3 Vapourizing Mats
there are likely to be new developments in this area
of mosquito control. To confirm the efficacy of the Electric vapourizing mats have become a common and
paper device, a field experiment was conducted in popular type of personal protection against household
Malaysia. A device containing 100 mg of metoflu- insect pests in all parts of the world.
thrin strongly inhibited biting of Cx. quinquefascia- They consist of a mat heater and vapourizing mat. The
tus. Tests using resin formulations were conducted mat is made from fiberboard impregnated with insecti-
in Vietnam. Resin formulations containing 1 g of cides (usually a pyrethroid), stabilizers, slow-releasing
metofluthrin exhibited excellent spatial repellent agents, perfumes and a colouring agent. The heater is
effects against Cx. quinquefasciatus and Ae. aegypti plugged into an ordinary household electric socket and
for at least 6 weeks. heats up to an optimum temperature of 110ºC, depend-
In the study conducted by Liu et al. (2003) a com- ing on the type of heater and accompanying mats. When
prehensive characterization of emissions was carried the mat is heated, insecticide vapour is released to pro-
out for six brands of mosquito coils commonly used in vide a low aerial concentration of insecticide. This
China and Malaysia. The pollutants characterized induces behaviour changes in flying insects through a
included fine and ultrafine particles (<2.5 µm in diam- sequence of sub-lethal effects including deterrence from
eter), polycyclic aromatic hydrocarbons (PAHs), vola- entering the room, bite inhibition and knock-down.
tile organic compounds (VOCs), and aldehydes, with Continued exposure results in death of the insect. The
high irritation or suspected carcinogenic effects. It was advantage of using mats over coils is that, with the for-
found that all particles emitted from burning mosquito mer, there is no unpleasant smoke. The disadvantages
coils were <1 µm in diameter. In general, the pollutant are that electricity is required and replacement mats are
emissions from the two tested Malaysian brands were generally more expensive than coils.
substantially higher than those from the four tested Mosquito mats are usually impregnated with either
Chinese brands. After comparing health-based stan- d-allethrin (36 mg/mat) or prallethrin (15 mg/mat)
dards and guidelines, the authors found that pollutant although other a.i. are also used (see Table 21.2).
21.3 Repellents Against Mosquitoes 497

Research by Adanan et al. (2005) shows that the efficacy 21.3.4 Liquid Vapourizers
of vapourizing mats depends on both the a.i. used and
the species tested. Using d-allethrin mats, the KT50 The principle of these products is similar to that of the
against Ae. aegypti and Cx. quinquefasciatus was 1.38 vapourizing mat. A liquid vapourizer has to be plugged
and 8.36 mins respectively. When d-allethrin and pral- into an electric socket. It consists of a heater, a wick
lethrin mats were tested against Ae. aegypti, mortalities and a bottle of liquid insecticide. The liquid, which is
of 63.3 and 90% respectively were obtained. Longevity a mixture of a pyrethroid and a solvent, is drawn up
of Ae. aegypti and Cx. quinquefasciatus species decreased through the wick, typically made from materials such
more than 80% and 45% respectively, after exposure to as carbon, ceramic or fiber. The end of the wick is
mosquito mats containing either d-allethrin or pral- positioned within the heating portion of the device,
lethrin. The percentage of blood-engorgement activity and when heated, the insecticide vapourizes from the
for Ae. aegypti and Cx. quinquefasciatus was reduced to wick. A bottle of liquid insecticide with its wick is
less than 70% and 25% respectively after a 20 min expo- usually designed to last up to 360 h, and requires
sure to a mat containing either one of the a.i. The num- replacement of the bottle every 1 or 2 months.
ber of eggs oviposited by the treated females, egg
hatchability, pupation rate and adult emergence rate Mosquito coils, vapourizing mats and liquid vapou­rizers
were not affected if the mosquitoes were still able to are as insecticide formulations, with the pyrethroids being
blood-engorge. the most widely used a.i. The a.i. are shown in Table 21.2
Much attention has recently been directed toward (WHO 1995). There is a developing market in these
the development of non-heated formulations, such as devices and many different brands are monitored and
fan vapourizers, because of their increased safety and approved by national authorities before introduction into
ease of use, especially during outdoor activities. By the a ­country. World­wide surveys have shown that consum-
introduction of metofluthrin as a novel pyrethroid cre- ers spend a considerable amount of money each year on
ated recently in Japan (2005) a worldwide development personal protection devices. However, due to the risk of
of this product has been carried out for environmental allergic reactions and peripheral nervous system distur-
health use (Ujihara et al. 2008). Metofluthrin has bances as well as the respiratory issues mentioned above
extremely high knock-down activity against mosqui- these products should not be used in rooms where chil-
toes, as well as high volatility and low mammalian tox- dren sleep. Therefore, the emphasis should be on promot-
icity. These features make the product applicable to, ing the use of safe and effective wide-scale mosquito
not only existing mosquito-controlling devices such as control programmes whenever possible, instead of rely-
mosquito mats and coils, but also to various new for- ing on individual protection, which should be considered
mulations and devices such as paper emanators, fan- only as an additional tool or as an integral part of a more
driven devices, and similar formulations. comprehensive mosquito control programme.
Chapter 22
Implementation and Integration of Mosquito Control
Measures

22.1 Introduction The most common mosquito control methods in an

IVM programme are:
The most successful approach for controlling 1. Chemical control: Residual applications of adulti­
mosquitoes is when an Integrated Mosquito Manage­ cides such as DDT, malathion, bendiocarb, per­
ment (IMM) strategy is implemented, in which all methrin, or related compounds, is the most frequently
appropriate technological and management techniques practiced method against endophilic and endophagic
are utilized, to bring about an effective decline of vector mosquitoes. Mosquitoes are repelled from
target-species populations in a cost-effective manner entering houses, or killed when they come into con­
(WHO 2004b). tact with the insecticides which are mainly sprayed
An IMM strategy could include biological, chemi­ on the interior walls of the houses or used to impreg­
cal, genetic, physical, environmental management, and nate bednets (Brown 1976; Lacey and Lacey 1990;
educational components. Lengeler and Snow 1996; D’Alessandro 2001;
With the development and successful use of insecti­ Takken 2002). Space application against resting or
cides (e.g. DDT), most control programmes following flying mosquitoes can be implemented when exo­
World War II were based on the sole use of available philic and exophagic mosquitoes such as floodwater
insecticides. However, the onset of resistance to chem­ mosquitoes occur in masses, thereby avoiding the
ical insecticides, and the increasing environmental and nuisance or vector activity by mosquitoes in a defined
public health concerns renewed the interest in compre­ area. However, space application usually protects
hensive integrated control strategies involving envi­ against mosquitoes only for a short time as the prod­
ronmentally safe measures. ucts used are not normally residual. This is particu­
A single method like larviciding (Table 22.1) may larly important when species of high migratory
provide adequate control in a certain situation. However, capacity are involved, which can easily re-invade the
the utilization of a range of control and management treated areas when the effect of the insecticide has
methods within an IVM approach may be more cost- declined. Chemicals can also be applied to mosquito
effective, cause less environmental damage, be effective breeding sites when they are accessible and defined.
for a longer period of time, and be better suited at the Conventional insecticides, used as adulticides or lar­
community level (Rafatjah 1982; Srdic et al. 1986; WHO vicides, are usually broad-spectrum control pro­ducts
1982a,b, 1983, 2004b). that can affect non-target organisms, and as a result
For this reason, the IVM concept was developed, are coming under scrutiny for both health and envi­
which incorporates the application of sound ecological ronmental reasons. Development of more environ­
principles to maintain mosquito populations below the mentally-friendly pro­ducts, such as insect growth
nuisance and health injury threshold. It is more precisely regulators (IGRs) or chitin synthesis inhibitors and
defined as follows: “Integrated vector control is the ratio­ microbial-control agents, can effectively reduce the
nal combination of all available control methods in the ecological damage to wildlife which can result from
most effective, economical, and safe manner to maintain the application of non-selective insecticides in eco­
mosquito vector populations at acceptable levels”. logically sensitive wetlands.

N. Becker et al., Mosquitoes and Their Control, 499

DOI 10.1007/978-3-540-92874-4_22, © Springer-Verlag Berlin Heidelberg 2010
500 22 Implementation and Integration of Mosquito Control Measures

Table 22.1 Insecticides suitable for mosquito larval control (WHO 2002)
Oral toxicity for rats(LD50 mg/
Insecticide Typea Dosage (a.i)b kg body weight)c
Temephos OP 56–112 g/ha 8,600
Temephos OP 1–2 mg/l drinking water 8,600
Chlorpyrifos OP 11–25 g/ha 135
Diflubenzuron GR 25–100 g/ha >4,640
Diflubenzuron GR 1–2 mg/l drinking water >4,640
Pirimiphos-methyl OP 50–500 g/ha 2,018
B. thuringiensis MI * Absent
B. sphaericus MI * Absent
a
OP organophosphate; GR insect growth regulator; MI microbial insecticide
b
a.i. active ingredient
c
Toxicity and hazard are not necessarily equivalent

2. Environmental control measures include environmen­ programmes. However, so far this technique had
tal management, such as physical reduction of breed­ very limited success in mosquito control. Several
ing sources, water management, draining or filling of techniques can be considered:
low-land areas, or vegetation management, to create a. The sterile-male release technique which is based on
conditions unfavourable for mosquito breeding. These the induction of sexual sterility in males through the
measures range from simple actions such as cleaning use of radiation or chemical sterilants, and the con­
street gutters to major redesigning of landscapes. sequent inundating of natural populations with mod­
Ditching in marshlands and other low areas to improve ified males. (Knipling 1955, 1959; Bellini 2005).
drainage is another example. The advantages of modi­ b. Cytoplasmic incompatibility between certain allo­
fying breeding sites are that these methods are simple patric mosquito populations which has been
and provide long-lasting effects. However, remodelling ascribed to the presence of a rickettsial endosym­
wetlands or water-flows can disturb delicate and valu­ biont, Wolbachia spp., in the gonads (Portaro and
able ecosystems, which in many areas has led to con­ Barr 1975; Clements 1992; Mahilum et al. 2003).
troversies. Initial costs of environmental management c. Chromosomal translocations which may cause an
may be high, but long-term cost-effectiveness has to increase in sterility of the progeny (Curtis 1968a,b;
be considered. Rai and McDonald 1971; Laven et al. 1972;
3. Physical control measures include: Hallinan et al. 1977). Recent developments in
a. The use of surface layers like monomolecular molecular genetics such as the ability to introduce
films or polystyrene beads prevents the imma­ recombinant DNA constructions into the genome
ture stages of mosquitoes from breathing at the of organisms (transformation of organisms) offer
water surface and can also reduce the deposition possibilities for genetic control. It is hoped to
of eggs on the water surface (Curtis et al. 1990; genetically engineer mosquitoes to make them
Reiter 1978; Webb and Russell 2009). refractory to infection by parasites (e.g.
b. Reduction of human/mosquito contact based on Plasmodium spp), or perhaps render them unable
community participation following educational to transmit the parasites (Alphey et al. 2002).
efforts, e.g. use of window meshed screens, elim­ 5. Biological control includes natural and applied bio­
ination of small water containers around houses, logical control. Natural biological control is the
prevention of access to water surface for females reduction of mosquitoes by naturally occurring biotic
to lay eggs. The use of bednets as a physical bar­ agents (Woodring and Davidson 1996). Applied bio­
rier could also be employed as a measure although logical control is planned human intervention by add­
insecticidal bednets are more frequently used ing biological-control agents to a breeding site
now which function as baited insecticidal traps, (augmentation). Potential biological-control agents
attracting and killing anthropophilic mosquitoes are pathogens (microbial-control agents) and preda­
(Schreck and Self 1985; MacCormack and Snow tors. Also, aquatic plants such as ferns (e.g. Azolla
1986; Takken 2002). sp.) or blue-green algae (e.g. Anabaena sp.) can have
4. Genetic control of pest species has been used suc­ a negative impact upon mosquito oviposition and the
cessfully in agricultural and veterinary pest-control survival of the developmental stages of mosquitoes.
22.2 Prerequisites for the Successful Implementation of a IVM programme 501

22.2 P
 rerequisites for the Successful 22.2.1 Entomological Research
Implementation of a IVM programme (Monitoring)
Most important for the implementation of an IVM
Precise knowledge of the relative abundance and
programme is to build or use an appropriate infrastructure
phenology of the relevant mosquito species is essential
for mosquito control. This includes a well-organised
to fulfil the requirements of an economical and eco­
personnel structure with clear responsibilities, intensive
logically successful control programme. Thus, a moni­
cooperative efforts with researchers from local institutes
toring programme for mosquitoes should be conducted
or universities, and adequate financial resources. The
to determine the species composition, abundance, and
most important aspect is the political will to reduce
phenology (population dynamics) in relation to the cli­
nuisance and vector-mosquito popu­lations. Despite the
matic conditions, as well as the spatial and temporal
fact that plenty of control tools are available, most
distribution related to migration. In different habitats,
control/management programmes fail because of an
human bait catches (HBC) should be carried out to
inadequate infrastructure.
determine the most significant anthropophilic mos­
The following steps for implementation need to be
quito species. The migration behaviour of the most rel­
taken:
evant species should be taken into account for designing
(1) Baseline collection of entomological and ecological the control strategy. For monitoring the adult mosquito
data which should include the occurrence of populations, EVS CO2 -baited traps are typically used
mosquito species with special regard to their to monitor adult female mosquito populations (see
vector-capacity and/or their nuisance potential. Chap. 4). Samples are usually taken at regular intervals
− The monitoring of the population dynamics of from late afternoon until the next morning, during the
the most important mosquito species in relation peak of flight activity. The trap-collected mosquitoes
to abiotic (e.g. climatic factors, such as rainy are counted and identified. When traps have been
and dry seasons, or temporary flooding periods) located in an isolated mass breeding site and in con­
and biotic conditions (the assessment of preda­ centric circles of 2, 5, and 10 or more km-diameter, the
tors of the mosquito immature stages which can horizontal dispersal behaviour of the emerging adults
assist in forecasting the development of mos­ can be determined in relation to wind speed, tempera­
quito populations), as well as defining the ture, or vegetation.
action thresholds for a programme. In a variety of typical breeding sites within the control
− Information on mosquito migration, biting, area, larval collections should be taken at regular inter­
and resting habits is essential to define the vals to assess the species composition and abundance.
intervention area. Usually, ten dips or more with a standard dipper are taken
− Assessment of parasitological and epidemio­ to obtain average and comparable data. The larval instars
logical data when vector species are involved are recorded and a sufficient number of larvae are taken
(e.g. infection or infectivity rates of vector to the laboratory to determine species composition.
species). Monitoring of post-treatment mosquito populations
(2) Mapping and individual numbering of each sig­ can also be used to compare different control strate­
nificant breeding site is essential when larvicides gies, such as larviciding, adulticiding, bio-control
are used. agents, environmental modifications, etc.
(3) Selection of appropriate tools and application sys­
tems/equipment to fight the target organisms.
(4) Effective dosage of a compound in use has to be 22.2.1.1 A
 ction Thresholds as a Component of
assessed to assure a cost-effective operation. Integrated Mosquito Management
(5) Design of the control strategy should be based on (IMM)
the results obtained in pilot studies.
(6) Training of the field staff. The concept of Integrated Pest Management (IPM)
(7) Governmental application formalities, and appeared originally in agriculture during the 1970s. It
(8) Intensive public relations, educational efforts and was proposed as an alternative to the routine and blanket
encouraging active community participation. application of pesticides, that was prevalent at that
502 22 Implementation and Integration of Mosquito Control Measures

time, and which was seen as responsible for generating To date, relatively few mosquito control organizations
resistance to pesticides, and for causing environmental have actively involved the public in setting standards
damage (Rabb 1972). Classical IPM has a number of (as opposed to the evaluation) for mosquito control. In
key components, such as identifying pests and under­ Italy, though, there have been considerable efforts by
standing their biology and behaviour, monitoring pest public survey to establish their tolerance of mosquito
levels, establishing a level of infestation above which biting and then relate this to light trap catches and tim­
control measures are justified, and using a mix of ing of treatment. This process has enabled mosquito
appropriate control measures to reduce pest damage. control organizations to ensure that their programmes
The IPM concept has been, subsequently, adjusted provide the level of control expected by the commu­
to suit other types of pest/vector control, including nity. In Germany, it was demonstrated that the flood­
mosquito control. In nuisance vector control, most of water mosquito Ae. vexans might be a nuisance
the core components of IPM have been readily adopted, problem in human settlements when more than 50
with the exception of defining a threshold infestation specimens were trapped in CO2-baited light traps about
level. Although the threshold concept fits agriculture 2 km away from the settlements.
well, there have been difficulties in establishing and Experience has shown that a community’s tolerance
using threshold infestation levels for nuisance pests. of mosquito bites tends to drift downward over time. In
Nonetheless, in mosquito control, as in agriculture, the the Rhine valley, for example, the level of mosquito-
fundamental need for such a threshold remains. Should biting that was considered as acceptable by the com­
nuisance mosquito control aim to reduce biting levels munity 30 years ago when the programme began is
by 75 or 95%, or to <5/night or <1/night, or ultimately now considered unacceptable. Mosquito control
to zero? Without defining such a level, mosquito con­ efforts, therefore, have to be steadily intensified over
trol may, on the one hand, be over-using insecticides time. These increased efforts are also likely to cost
(resulting in unnecessary expense, and possible envi­ proportionately more; initially reducing mosquito bites
ronmental damage), or may, on the other hand, be fail­ from 20 bites/night to 5/night is likely to be less costly
ing to provide the standard of control expected by than subsequently reducing the biting from 5 bites/
residents and visitors. Defining such tolerance or night to 1/night. Mosquito control organizations need
threshold levels should, therefore, be a central part of to recognise and plan for such changes in the future.
the planning of mosquito control programmes.
In the US, there are several examples of the use of
action thresholds for mosquito control activities. For 22.2.1.2 Threshold for Vector Mosquitoes
example, Headlee (1932) concluded from his research
in New Jersey that the human tolerance for mosquito All vector control measures require a high degree of
bites was no more than 4 bites/night. More recently, coverage of the areas to be treated if human population
Robinson and Atkins (1983) conducted a study in is to be protected. The requirements will vary depend­
Virginia on the knowledge and attitudes of residents to ing on the type of intervention concerned and the bion­
mosquitoes. Their data showed that 50% of the resi­ omics of the vector, epidemiological and ecological
dents considered that 3 or more mosquito bites/night factors. Disease incidence and human mortality rates
constituted a problem and that, in order to satisfy 50% directly describe the disease risk for a given area.
of the residents, a mosquito control agency should aim Besides these facts, parameters related to vectors are
to keep mosquito numbers below this level. By con­ known, which could be used to determine the “thresh­
trast, surveys of residents in Texas revealed that a mean old” limit for epidemic-risk in a particular area. Most
of 5.7 bites/h at night was a “no problem,” 7.7 bites/h commonly, the entomological inoculation rate (EIR)
at night was a “mild” problem, whereas 11.5 bites/h at for the determination of malaria endemicity, the infec­
night was considered a “severe” problem (John et al. tivity rate (occurrence of infective L3 larvae of the
1987). It should also be recognised that mosquito bites nematode; transmission risk for lymphatic filariasis) or
at night (e.g. Cx. pipiens) when residents are trying to the number of Aedes pupae/person or pupae/per area as
sleep, have a different “rating” as compared to bites transmission threshold for dengue are used.
outdoors during daytime or dusk (e.g. bites by Aedes/ One of the best ways to define malaria endemicity
Ochlerotatus spp.). is to determine the EIR which describe the number
22.2 Prerequisites for the Successful Implementation of a IVM programme 503

of infectious bites an individual is exposed to in a 22.2.2.1 Geographic Information Systems

given time period (typically a year). The EIR allows
a direct estimation of the transmission risk (Koella Geographic information systems (GIS) have now
1991; Killeen et al. 2000a,b). Another parameter, become very widely used by professionals in research,
named parasite prevalence (parasite ratio or PR = the government and industry for computing spatially-
percentage of individuals found with a positive blood related data.
slide), is related to the intensity of transmission and A GIS consists of an organised collection of com­
is, therefore, been used to define endemicity in clas­ puter hardware, software, and geographic data designed
sical malaria epidemiology (Macdonald 1957). The to efficiently capture, store, update, manipulate, ana­
levels of endemicity can be defined as follows: lyze, and display all forms of geographically refer­
hypoendemic: PR in 2–9 year olds: £10%; mesoen­ enced information.
demic: PR in 2–9 year olds: 11–50%; hyperendemic: Modern information technology allows the integra­
PR in 2–9 year olds: constantly >50%; holoendemic: tion of GIS with database technology, and with digital
PR in infants constantly > 75% (Metselaar and Van mobile field data collection systems supported by a
Thiel 1959). Global Positioning System (GPS).
The transmission threshold for dengue is based The ability to link information about, where things
on the number of Aedes pupae/per person or pupae/ are, with the information about what things are, pro­
per area. Risk of a dengue epidemic is considered vides the user with a better understanding of spatial
low when the number is below the threshold; risk phenomena and their relationships, which may not be
increases sharply above the threshold. Threshold apparent without such advanced techniques of query,
levels were estimated to range between ~0.5 and selection, analysis, and display.
1.5 Ae. aegypti pupae/person for a certain tempera­ Special care should be taken in designing and estab­
ture and initial seroprevalences ranging between lishing a high quality GIS to ensure that it contains all the
0% and 67%. The ratio of Ae. aegypti pupae to relevant data for a specific purpose, including both geo­
human density has been observed in limited field graphic data (where is the feature – location and geom­
studies to range between 0.3 and >60 in dengue- etry) and properties (what is it like – attribute data).
endemic areas in the Caribbean, Central America, Typical applications of GIS are:
and Southeast Asia.
−− Mapping locations of certain features;
−− Mapping quantities and densities;
−− Finding out properties of distinct areas using data­
base queries;
−− Mapping change by comparing how features change
22.2.2 Mapping of the Breeding Sites over a period of time, in order to forecast future
conditions.
Precise mapping and individual numbering of each
significant breeding site enables rapid and effective An extensive overview on GIS can be found in
communication between field staff which provides a Burrough et al. (1998).
solid basis for a successful operation when larvicides
are applied. Several other studies can be carried out
during mapping: (1) assessment of the diversity and 22.2.2.2 A
 pplication of GIS and Information
abundance of mosquito species in the control area; (2) Technology to Mosquito Control
characterization (typing) of the breeding sites
­according to their productivity (mosquito densities) GIS and related information technology can greatly
plus mosquito population dynamics; and (3) assess­ improve survey, logistics, and documentation of mos­
ment of the ecological conditions of the major breed­ quito control operations. The possible applications
ing sites, e.g. plant associations, occurrence of range from direct digital site-mapping using GPS
predators, or rare and sensitive organisms that indicate assisted mobile devices to timely aggregation of
the frequency of floods. operational reports.
504 22 Implementation and Integration of Mosquito Control Measures

A spatially referenced database containing all form of standardized thematic maps, graphics or
f­ eatures of interest is the basis for all further data col­ tables.
lection and analysis. This spatial element enables thema­
tically related features (e.g. population densities of For more detailed and up-to-date information on
certain species, flooding areas, plant associations and this fast developing technology, it is recommended to
vegetation type, zones of nuisance or disease) that can consult the webpages of commercial GIS-developers
be organised in separate layers of information, which or mosquito control agencies.
can then be analyzed and displayed in a user-defined
context.
The following is an outline of possible applications
in a mosquito control programme based on larviciding:
22.2.3 Selection of Appropriate Tools
• Analysis and query of available digital maps, aerial
photos or satellite imagery, and thematic maps (e.g. Data are collected in the implementation phase, to
hydrology, flooding zones, wetland inventories, ensure the appropriate choice of control tools, appli­
etc.) to determine potential larval habitats; cation techniques, correct formulations, and effective
• Spatial analysis to determine relationships between dosages, depending on the characteristics of the cho­
human nuisance or disease, and breeding sites (cal­ sen control product, as well as on the biotic and abi­
culation of buffer-zones, map- and database otic conditions at the application site. In the laboratory
query); and in small field tests, the effective dosages of the
• GPS-assisted field data collection and breeding site control compounds have to be evaluated. Then the
inspection (detailed habitat mapping, larval, and most suitable application techniques and formulations
pupal survey). The use of hand-held systems, that for the various habitats and target species may be
synchronize data with the main data base, allows chosen.
accurate and timely processing of results and data- The optimal use of the product requires homoge­
base updates; nous dispersal of the material in a recommended dos­
• Forecasting of time and location of appropriate age over the target area in a certain period of time.
control activities based on correlations between For instance, the volume of water used for dilution
the spatial occurrence of triggering events for lar­ depends on the type of equipment (size of the nozzle/s,
val development (e.g. water levels and flooding pressure of the system, and speed of application) to
areas, local weather data, the potential of larval obtain the desired dosage/area. The rate of emission
development sites, and the results of current sur­ in relation to the speed of application has to be cali­
vey data); brated before routine treatments, to ensure correct
• Preparation of operational maps to improve logis­ dosage during application. Depending upon the type
tics, calculate the quantities of control materials and of application, prevailing weather conditions must be
manpower required, and to calculate the duration taken into consideration to ensure accurate
and cost of treatment; application.
• Storage of historical-site profiles and related attri­ The selected equipment must be correctly adjusted
bute data on the basis of operational maps, enables and operated. Insufficient knowledge and lack of train­
future potential larval development, resulting from ing on how to use and maintain the application equip­
dynamic triggering events to be predicted; ment and on how to supervise teams can be important
• GPS-assisted operations allow the tracking and factors that lead to poor application of the mosquito
direct digital documentation of field activities (e.g. control products. On the basis of all available data, an
aerial application); intervention strategy for each individual area and situ­
• Reports and documentation of survey and control ation has to be worked out. It aims to produce a com­
activities can be assisted by user-defined database prehensive control strategy with a mosaic-like structure
and map queries, which give immediate access to that takes into account ecological, epidemiological,
information stored in the database. The results of the and sociological aspects and into which various meth­
queries can then be visualized and printed in the ods are integrated.
22.2 Prerequisites for the Successful Implementation of a IVM programme 505

22.2.4 Effective Dosage Assessment −− Assessment of the optimum effective dosage in the
field
This procedure is explained when for example micro­
Based on the results obtained in the laboratory, the
bial-control agents are used. The efficacy of a micro­
optimum effective dosage for field application can be
bial-control agent such as B. thuringiensis israelensis
determined. A series of small field tests in various lar­
(B.t.i.) is influenced by a great variety of biotic and abi­
val habitats should be conducted to determine the opti­
otic factors; the susceptibility of the target mosquito
mum effective dosage of B.t.i. formulations against
species, the stage of development, the feeding behaviour
naturally occurring larvae of the indigenous mosquito
of mosquito larvae, the density of larval mosquito pop­
species. For the field tests, concentrations of 1, 2, 4,
ulations, the temperature and quality of water, the
and even 8 times the value of the minimum effective
intensity of sunlight, and the presence of filter-feeding
dosage (LC99 value obtained in the bioassays) should
non-target organisms (Lacey and Oldacre 1983; Mulla
be used. Each concentration should be tested in tripli­
et al. 1990; Becker et al. 1992; Becker and Rettich
cate in the characteristic breeding sites, and untreated
1994). The characteristics of the formulations in use,
breeding sites should serve as control.
such as potency, settling-rate, and shelf-life, can also
In most countries, the dosage for each mosquito control
influence the effectiveness of microbial-control agents.
product is set by the national regulatory agency, not by
It is, therefore, important to understand the impact
the local mosquito control organization. The national
of these factors during routine treatment, especially, as
regulatory agency will, in turn, typically select dos­
it effects the calculation of the dosage, the selection of
ages that have been established by the manufacturer,
the right formulation for each particular environmental
sometimes in collaboration with WHOPES.
situation, and the appropriate timing for the treatment.

−− Assessment of the potency of the products and effec-

tive dosages 22.2.5 Design of the Control Strategy
Before new formulations are used in the field, their effi­
cacy is evaluated against Ae. aegypti and indigenous The control strategy for large-scale operations should
mosquito species in the laboratory and in the field. All be determined according to several considerations:
bioassays are run according to World Health Organization (1) Whether the mosquitoes are a vector or a nuisance
guidelines (WHO 1981). The potency of the formula­ species, the bionomics of the target organisms
tions (International Toxic Units = ITU) is determined by (e.g. are they endophilic or exophilic), and the
the formula given in Chap. 4. migration behaviour of the target mosquitoes. The
objective of the strategy is to keep mosquitoes
−− Assessment of the minimum effective dosage
away from human settlements and so the migra­
(LC99)
tory behaviour of the species, in question, needs to
Different instars of the indigenous mosquito species be considered. For instance, when a nuisance spe­
are collected in the field and their sensitivity is deter­ cies, such as Ae. vexans which readily migrates,
mined by bioassays. The procedure for bioassays has has to be controlled, the breeding sites which may
to be adapted to the specific needs of the study. Water occur at a distance from settlements should also be
from the larval habitat should be used instead of distilled controlled (Ae. vexans can migrate >15 km when
water to avoid any dramatic change in the living condi­ wind conditions are favourable and when popula­
tions of the larvae which might affect the evaluation of tion pressures are high). Domestic mosquitoes
the susceptibility of the tested species. In order to achieve (Cx. pipiens), which migrate not more than a few
mortality rates of between 10 and <100%, various hundred meters, can be controlled only within the
amounts of a stock solution are added to test containers. settlements and within a radius of 500 m. Snow-
Each formulation should be run at least 3 times at 5–7 melt mosquitoes, such as Oc. cantans, usually, do
different concentrations. The LC99 value determined for not migrate further than 2 km, and prefer to stay in
field-collected larvae is defined as the minimum effec­ densely vegetated areas. These mosquitoes may be
tive dosage and serves as a guideline for the assessment controlled in buffer zones of about 2 km in diameter
of the field trials. around villages.
506 22 Implementation and Integration of Mosquito Control Measures

(2) When larvicides are used, the potential mosquito the techniques for carrying-out the most appropriate
productivity of a breeding site is a criterion for the ­treatment for each situation. The teams should meet
relevance of that breeding site, because it allows regularly to exchange experiences from the field and
the assessment of the mosquito threshold for the for further training.
control.
(3) The climatic conditions (changes in water level,
length of rainy and dry seasons) influence the pop­
ulation dynamics of the mosquitoes. 22.2.7 G
 overnmental Application
(4) The population dynamics of the target organisms Requirements
determine the timing of the treatment, which will
have the greatest impact on the target organisms
Governmental approval for the use of a mosquito con­
(e.g. control of developmental stages of Culex and
trol agent is a legal requirement for a planned control
Anopheles during a dry period, when they occur in
operation. The application for approval will contain
defined and limited breeding sites).
data on the materials and formulations in use, strategy
(5) The properties of the control compound have to be
of control, dosages, application techniques, assess­
considered e.g. the residual effect of the control
ment of the threshold for the control operation, assess­
agent is relevant for the sequence of re-treatments.
ment of the mosquito density, and ecological
(6) Adaptation of the control technique to the ecologi­
considerations. This information is available in the
cal conditions is another factor to be considered,
material safety data sheets (MSDS) provided by the
such as water level and vegetation growth. According
manufacturer.
to the situation the most suitable formulation and
application equipment should be selected (e.g.
application of B.t.i. may be made manually or with
the aid of helicopters).
(7) Development of an integrated control strategy, 22.2.8 Community Participation
including predators, environmental management,
and community participation. The cooperation Mosquito control can be particularly successful
between political decision makers, public authori­ when the local population is well educated by the
ties, scientists, and the general public is of great responsible agency and are encouraged to be involved
importance for achieving success in a mosquito in the search for solutions to mosquito problems,
control programme. especially when they are related to mosquitoes
(8) The control strategy has to be orientated toward breeding within dwellings (Becker 1992).
financial and personal resources. Responsibility for the ­definition of the strategy,
planning, and the regional organization of the control
programme rests with the programme authorities,
but even at the planning stage, the expected cooperation
22.2.6 Training of Field Staff of the community must be taken into account
(Halstead et al. 1985; Yoon 1987).
A crucial component for a successful control programme The programme authorities have to evaluate how
is an adequately trained staff and equally well-trained the control strategy may be best achieved through
field teams. On the one hand, the control programme community participation to obtain a horizontally-
must be well organised and on the other, the control defined structure. The successful inter-digitation of the
team must be flexible enough to respond to each indi­ vertical (regional authorities) and the horizontal orga­
vidual situation with the most appropriate techniques nizational (community) structures through community
and at the correct time, weather conditions permitting. participation means that the people become “actors”
The field staff has to be trained in the biology and ecol­ instead of “spectators” (Diesfeld 1989). The programme
ogy of the target mosquitoes and their identification, has to enable people to contribute to the solution of
the principles of the methodology, the mode of action their mosquito problem related to their own ­settlement.
of the control agents, the application techniques, and This can be achieved by a comprehensive campaign of
22.2 Prerequisites for the Successful Implementation of a IVM programme 507

instruction dealing with the biology of the ­mosquitoes 6. The application of larvicides if none of these
and with straightforward methods of ­control available ­methods are practical (e.g. Culinex/Vectobac DT
on websites, leaflets, brochures, television, radio, daily tablets based on B.t.i. or B. sphaericus, methoprene
newspapers, circulars, posters, videos, slides, and briquets or Abate granules). There are many argu­
demonstrations. Thus, “help through self-help” can be ments in favour of introducing the use of microbial-
achieved. It is important to keep the level of motivation control agents with community participation. Most
high over a long period. People are frequently aware of striking is that they are safe for humans and the
the problem but they may take no action or there may environment, as well as simple to use (Table 22.1).
be just short-term involvement. 7. The application of adulticides, especially during
Community participation can be at its best and most epidemics, as an ultimate measure to control adults
meaningfully achieved by controlling the immature stages transmitting diseases, could be achieved with indoor
of mosquitoes breeding in or close to human settlements, residual house spraying (IRHS). The choice of the
for example, species such as Ae. aegypti, Ae. albopictus, Cx. insecticide depends on a variety of factors including
p. pipiens/quinquefasciatus or Anopheles in urban areas. regulations of the local/state/country. The recom­
The following methods can be used (see also 17.4.1.): mended products by WHO (2002) are given in
Table 22.2.
1. Source reduction by elimination of unnecessary
stagnant water bodies;
2. The weekly replacement of water in bowls and jugs
as well as cleaning of containers to remove and
destroy mosquito eggs; 22.2.9 Registration of Insecticides
3. The careful covering of water containers, e.g. with
tight-fitting lids or netting to prevent egg laying and In most countries, insecticide approval and use is regu­
larval breeding; lated by law. National regulatory agencies (e.g. the EPA
4. The release of larvivorous fish into water in the U.S.) will require substantial evidence that a par­
reservoirs; ticular pesticide is suitable for the intended use before
5. The filling of potholes with concrete or by draining allowing it to be sold. This evidence typically covers
the water to avoid the collection of stagnant water; several categories, including the ­physico-chemical

Table 22.2 Insecticides recommended for indoor residual house spraying (IRHS) (WHO 2002)
Duration of Safety class of
Insecticides Dosage (g/m2) Formulation effectivness Insecticidal action ingredient
Organochlorines
DDT 1–2 WP 6 months or Contact MH
more
Organophosphates
Malathion 2 WP 2–3 months Contact SH
Fenitrothion 2 WP 3–6 months Contact, airborne MH
Pirimiphos-methyl 1–2 WP 2–3 months or Contact, airborne SH
more
Carbamates
Bendiocarb 0.1–0.4 WP 2–6 months Contact, airborne MH
Propoxur 1–2 WP 3–6 months Contact, airborne MH
Pyrethroids
Alpha-cypermethrin 0.02–0.03 WP 4–6 months Contact MH
Cyfluthrin 0.02–0.05 WP 3–6 months Contact MH
Deltamethrin 0.01–0.025 WP 3–6 months Contact MH
Lambda-cyhalothrin 0.02–0.03 WP 3–6 months Contact MH
Etofenprox 0.1–0.3 WP 3–6 months Contact, airborne
Note: MH moderately hazardous; SH slightly hazardous; WP wettable powder
508 22 Implementation and Integration of Mosquito Control Measures

properties of the pesticide, the impact of the material on achieve high efficacy, whilst at the same time, avoiding
the user, the public, the environment, and its effective­ significant environmental impact.
ness against the target pest. These regulations apply to
• Timing and Frequency of Treatments
manufacturers, distributors, and to the end user. They
also apply to almost all pesticides, including microbial- Insecticide labels will normally provide guidance on
control agents such as B.t.i. Pesticide users in public when treatment should be applied for maximum efficacy,
sector organizations and also in the private sector, are e.g. against certain developmental stages of the insect or
all typically obliged to comply with these regulations. under certain meteorological conditions. In the interest
Within the European Community, for example, active of resistance management, there may also be restrictions
ingredients are regulated under the European Biocides on the frequency of pesticide use. All the above condi­
Directive (98/8/EC, BPD), whereas individual formula­ tions must be followed according to Label Directions.
tions are registered at the national level. The success of the application should be evaluated after
For the end-user of insecticides, the legislation typi­ the application (pre- and post-treatment evaluations).
cally puts a wide range of requirements in place, and • Pesticide Storage
these directions must be followed. The requirements
will, typically, be found on the product label and mos­ All pesticides must be stored safely and securely to
quito control staff at all levels must be familiar with the avoid any possible accident resulting from unauthor­
details of the label requirements. Most mosquito control ized access by the public or from fire or extreme
organizations train their staff carefully to ensure an weather conditions. The storage facility must also dis­
understanding of all aspects of the label requirements play the appropriate warning/caution signs.
and full compliance with the regulations in safety and • Proper Disposal of Used Insecticide Containers
handling during field applications. The label directions,
typically, specify a wide range of conditions including: To avoid possible pollution or contamination, empty con­
tainers and washings from the application equipment
• Use of Personal Protective Equipment (PPE)
should be disposed off in accordance with the local regu­
Staff involved in the mixing and application of insecti­ lations. In some cases it may be possible to use “wash­
cides are required to wear certain protective equipment, ings” as a diluent for the next batch of spray.
such as coveralls, gloves, respirators and face-shields, The MSDS can usually be obtained from the manu­
to prevent personal contamination. Such items should facturer, supplier, or the national regulatory agency.
be provided, replaced and laundered by the employer. Useful information may also be obtained from a variety
• Personal Hygiene of other sources, for example the International Programme
on Chemical Safety. Human and environmental safety
If there is direct contamination of the eyes and/or the during mosquito control activities have been well-
skin, the contaminated area must be immediately regulated in recent years and it is the responsibility of all
flushed/washed. In addition, it is a good practice to those involved in this important work to ensure that this
wash after using a product, before meals, breaks, and situation is continuously maintained.
before leaving work at the end of the day.
• Application Equipment and Dosages
Insecticide labels will normally specify the applica­ 22.2.10 Routine Treatments
tion equipment to be used, e.g. granule applicator,
ULV equipment, etc. The equipment should be main­ Any control programme basically needs certain core
tained in good working condition and calibrated at elements, such as effective management and adminis­
regular intervals for accurate delivery. Formulations tration, including appropriate facilities, a personnel
and dilutions will be explained specifically and these structure with clear responsibilities, and target-spe­
directions must be followed to the letter of the law. cific control tools which are used within an appropri­
Only through careful calibration and monitoring of ate control strategy which the local community
equipment performance, is it possible to ensure that the supports, and in which their involvement is crucial.
correct quantity of the control product is applied to The strategy has to be adapted to the specific needs of
22.2 Prerequisites for the Successful Implementation of a IVM programme 509

each particular situation during the operation, e.g. (4) The effect of the operation has to be evaluated by
selection of a suitable formulation which fits the entomological and epidemiological monitoring
­ecological conditions and the bionomics of the target- teams. Thus, failures can be quickly pin-pointed
organisms. The operation has to be guided by target and corrected to optimize the effectiveness of the
surveillance and an environmental monitoring pro­ control operation.
gramme, as well as by goal-oriented research and a (5) Staff involvement and motivation should ensure
well-structured educational programme. Intensive the success of the programme.
public relations work will encourage the involvement
and support of the general public.
Important prerequisites for successful routine
operations are: 22.2.11 Public Information Systems
(1) The planning and control operation aims at a
long-lasting operation and should be based on Appropriate information will increase public aware­
long-term programing and encouraging long- ness and acceptance of the control efforts. At regular
term, responsible personnel. Control of mosqui­ intervals, the media should be informed about the
toes needs skilled people who are familiar with actual operations and the results of control.
the local conditions for control and have a per­ Improvements in understanding the actual communi­
spective for a continuous realization of the con­ cation networks used by community participants may
trol strategy to which they feel responsible. The alleviate problems caused by communication gaps.
sustainability of a successful programme has to Carefully chosen continuing, compelling programmes
be guaranteed. with the desired “message” should be delivered to
(2) Besides the governmental aspects of the activities, people at peak viewing hours (Curtis 1990).
e.g. financial and logistic support, the problem Access to the Internet and computers can provide
should mainly be solved by utilizing local resources people with the tools and information to improve their
as this will assure a long-term operation but should knowledge about the biology of mosquitoes, mosquito-
not excuse the lack of governmental support. borne diseases, and the ongoing operations. Web-sites
(3) Clear and well-defined responsibilities have to be should contain information on the operations and
delegated to each “actor” in the programme at each actual matters of interest, e.g. descriptions of exotic
level of the operation. Usually, only limited resources and invasive species of mosquitoes. These public rela­
and time-frames are available for control operations, tions tactics might motivate the public to participate in
therefore, these actions have to be organised in the the monitoring and control. A website could be created
most effective and efficient manner. to announce press releases.
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Subject Index

A Allethrin, 460
Abate, 457, 507 Allopatric, 325, 330, 486, 500
Abdomen Alpha-cypermethrin, 460–462
adult, 19, 52, 54, 55, 56, 57, 63, 72–76 Alternative methods in mosquito control, 441
larva, 16, 18, 53, 76, 80–84 Ammonia, 10, 45
pupa, 19, 53, 85, 86, 87 Anal lobe, 85
Accessory glands, 20, 468 Anal papillae, 16, 84
Accessory seta, 85, 368 Anal vein, 72
Acetone, 21 Anautogenous, 9, 23, 24, 219, 277
Acetylcholine (ACh), 452, 458 Anepisternal cleft, 70, 71
Acetylcholinesterase (AChE), 452, 456, 458, 473 Anepisternum, 70
Aciculate seta, 77 Annuli, 64, 66
Acrostichal rows, 69, 106 Anophelism, 29, 170
Acrostichal stripe, 70 Anoxia, 478
Actellic. See Pirimiphos methyl Anteacrostichal patch, 70
Action thresholds, 501–502 Anteclypeus, 65
Active ingredient, 443–449, 451, 460, 466, 468, 492, Antenna
494–496, 508 adult, 63
Acus, 82 larva, 79
Acute pancreatitis, 36 Antennal seta, 79
Acylated aminopropanole derivates, 493 Antepalmate seta, 82
Adenosine diphosphate (ADP), 23 Anteprocoxal membrane, 70, 71
Adenosine triphosphate (ATP), 23 Anteprocoxal patch, 71
Adults Antepronotum, 67, 70
biology, 19–24 Anterior spiracular lobe, 83
keys, 91–111, 318–322, 334–340, 351–356, 369–374, Anterolateral spiracular lobe, 81
387–391 Anteromedian palatal brush, 79
morphology, 63–76 Anthropophilic, 24, 25, 30, 176, 180, 249, 323, 326, 329, 347,
preserving, 54–55 375, 500, 501
rearing, 51–52, 86, 200 Anthropophily, 24, 329, 491
sampling, 47–51, 54 Antibodies, 33, 35–39, 55
Aedeagal setae. See Leaflets of aedeagus Anticoagulant, 23, 66
Aedeagus, 73–75 Ants (Formicidae), 409
Aeration, 435 Anus, 73, 75, 83, 84
Aerenchyma, 10, 17, 19, 307, 309 Apical lobe, 73
Aerial application equipment, 449, 453 Apical seta, 85
Aerial photos, 504 Apical spine of gonostylus, 74
Aerosol dispenser, 447 Apodous, 16
Aerosol generator, 448–449, 453, 463 Appetitive flight, 21
Aerosols, 37, 446–449, 453, 459–460, 463, Application equipment, 448, 449, 453, 469, 471, 504, 506, 508
465, 474 Aquatic spider, 412
African region, 208, 443, 450, 451, 466 Arboreal species, 9
Agonistic genes, 486 Arboviruses, 30–39, 188, 196, 202, 203, 267, 277, 279, 312, 366
Airborn, 447, 453 Arculus, 72
Airport malaria, 29 Arsenic, 443
Aliphatic organophosphates, 452–454 Arthritis, 31

553
554 Subject Index

Arthropod-borne viruses (Arboviruses), 30–39, 188, 196, 202, Butopyronoxyl, 493

203, 267, 277, 279, 312, 366, 493 Butyl ethyl propanediol, 493
Artificial mating, 52
Asian bush mosquito. See Ochlerotatus japonicus japonicus
Asian rock pool mosquito. See Ochlerotatus japonicus japonicus C
Asian tiger mosquito See Aedes albopictus in Taxonomic Index Caddisflies See Trichoptera in Taxonomic Index
Aspirator, 47–49, 52, 60 California group viruses, 31, 37
Ataxia, 451 Canalisation, 438
Attractants, 22, 45, 47–50, 60, 481, 494 Canine cardiovascular dirofilariasis, 40
Attractant traps, 47 Cap, 16, 46
Augmentation, 405, 500 n-Capric acid, 45
Autogenous, 10, 19, 23, 168, 170, 215, 217, 219, 279, 290, Caput (larvae). See Head (larvae)
306, 310 Carbamates, 58, 441, 443–445, 449, 450, 452, 456, 458–459,
Autosomes, 56 470, 473, 507
Avian malaria, 333 Carbon dioxide, 10, 21, 22, 45, 47–51, 447, 481
Carbon dioxide traps, 47, 49–51, 481
Cardiac insufficiency, 40
B Carnoy’s fixative, 57
Bacteria, 25, 188, 416, 419–431, 442, 443, 487, 488 Catarrh, 39
Bait catches Catch basins, 29, 180, 435
animal bait catches, 49 CDC light traps, 50, 217, 429
Bancroftian filariasis, 279, 323, 325, 326, 332, 333, 407 Cecropins, 487
Banding patterns, 56, 57 Cemeteries, 9, 369, 434, 436, 456
Barmah Forest virus, 351, 359, 365 Centers for Disease Control (CDC), 29
Basal lobe, 73 Cephalothorax, 19, 53, 85, 86
Basimere. See Gonocoxite Cercal lobes, 85, 86
Basistyle. See Gonocoxite Cercal sclerites, 75
Bats (Chiroptera), 36, 37, 409–410, 430 Cerci, 73, 76
Baygon. See Propoxur Cervix
Bed nets, 60, 430, 434, 462, 464, 491, 492 adult, 65
Behavioural resistance, 472 larva, 79
Behavioural studies, 7, 45 Cesspools, 429, 480
Behaviour changes, 496 Chaetotaxy, 77, 84–86
Bendiocarb, 444, 445, 459, 472, 499, 507 Chemical control, 441–475, 493, 499
Benign malaria, 28 Chemical solubility, 450
Benzoylphenyl ureas. See Diflubenzuron Chemical stability, 450, 452, 459
Benzyl benzoate, 493 Chemical type or class of insecticides, 445, 446
Bifenthrin, 444, 445, 462 Chemosterilisants, 442
Bioaccumulation, 452 Chemosterilization, 485
Bioassay, 59, 425–428, 455, 471, 473, 474, 505 Chikungunya fever, 25, 31, 332, 442
Biochemical agents, Chitin synthesis inhibitors, 466, 499
Biodegradable surface film, 478 Chlorinated hydrocarbons, 441, 443, 445, 449–452
Biodegradation, 459 Chlorinated insecticides. See Chlorinated hydrocarbons
Biological control, 405–431, 468, 500 Chlorinated organics. See Chlorinated hydrocarbons
Biorational larvicides, 424 Chlorodiethylbenzamide, 493
Birds (Aves), 409 Chloroquine, 28
Biting midges, 38 Chlorpyrifos, 444–446, 448, 449, 455, 472, 500
Blackflies See Simuliidae in Taxonomic Index Cholinesterase (ChE), 452
Blood-meal Chorion, 45, 52, 171, 279
blood meal identification, 55 Chromatids, 57, 488
Botanical repellents, 494 Cibarial pump, 23
Brackish water swamps, 358, 392, 394 Cichlids (Fish), 408
Branched seta, 78, 83 Circumsporozoite protein (CSP), 495
Breeding site, 9–11, 13, 14, 16, 19, 21, 23, 24, 43–45, 47 Citronella oil, 494
Briquettes, 424, 425, 448, 469 Cladistic trees, 3
Broad-spectrum insecticides, 460 Clasper See Gonostylus
Bronchopneumonia, 39 Claspetoid, 76
Browsers, 17 Claspette filament, 75
Burning coil, 460, 495 Claspettes, 75, 76
Bursa copulatrix, 20 Claspette stem, 75
Butanone, 21 Classification of insecticides, 443–446
Subject Index 555

Claws, 71 Dimethyl phthalate, 493

Climatic, 9, 15, 24, 40, 42, 202, 248, 277, 290, 501, 506 Dipper, 43, 46, 501
Coconut growing areas, 333 Dirofilariasis. See Canine cardiovascular dirofilariasis
Comb, 82 Disease transmission, 47, 49, 315, 325, 433–436,
Comb scale, 82 464, 484, 493
Common carp. See Cyprinus carpio in Taxonomic Index Dispersal, 21–22, 219, 325, 488, 501, 504
Common guppy. See Poecilia reticulata, in Taxonomic Index Dissolved oxygen, 14, 15, 24, 262, 478, 479
Community participation, 412, 422, 427, 436, 438–439, 489, Distimere. See Gonostylus
492, 500, 501, 506–507 Dististyle. See Gonostylus
Community’s tolerance, 502 Ditching, 433, 437, 500
Compound eyes, 22, 64, 65, 79, 80, 85 Diuron, 466
Compression sprayer, 448, 449 DNA fingerprinting, 58
Conditioning, 16 Dog heartworm. See in Taxonomic Index
Contact pheromones, 20 Dormancy, 10, 24
Contact poison, 444 Dorsal arm, (inner division), 76
Copulation, 9, 20, 52, 73, 196, 219, 246, 277, 310, 415 Dorsocentral rows, 69, 70
Cork, 54 Dorsocentral stripes, 70
Corolla, 10 Double mounted method, 54
Coronal suture, 64 Dragonflies. See in Taxonomic Index
Corpora allata, 468 Drainage, 168, 174, 224, 227, 288, 375, 429, 434, 435, 437,
Costa (C), 72 438, 500
Cost effectiveness, 423, 459, 500 Draining, 433, 436, 500, 507
Coxa, 70, 71 Driver mechanism, 486, 488, 489
Coxite. See Gonocoxite Drop-net, 49
Cratal setae, 84 Dry ice, 50
Cross resistance, 455, 461, 464, 475 Dursban. See Chlorpyrifos
Cubitus, 72
Cumulative effects, 455
Cuticular penetration, 472 E
Cuticular respiration, 479 Ecdysial line, 19, 85
Cyanide, 54 Ecdysis, 467
Cyfluthrin, 444, 445, 449, 460, 462–463, 472, 493, 507 Ecdysone, 18
Cypermethrin, 444, 445, 449, 460, 461, 463 Ecological data, 501
Cytodiagnostic methods, 56–57 Economy, 32
Cytoplasmic incompatibility, 485, 488, 500 Ecotoxicological effects, 468
Cytoplasmic polyhedrosis virus, 431 Educational materials, 439
Effective dosage assessment, 505
Effector gene, 487
D Egg batches, 10, 20, 52, 195
Dancing flight, 20 Egg burster See Egg tooth
Deconditioning, 16 Egg density, 44
DEET, 466, 494 Egg-laying behaviour, 10–12, 43, 45
Deltamethrin. See K-Othrine Egg-laying substrate, 12
Dendriform seta, 78 Egg production, 23
Dengue fever (DF), 35, 436, 438, 442, 458 Egg raft, 10, 43, 45, 52, 276, 284, 298
Dengue haemorrhagic fever (DHF), 35, 36, 47, 407, 436, Eggs
438, 458 biology, 9–14, 16, 19–24
Dermal toxicity, 445, 491 key, Anopheles Maculipennis Complex, 171
Design of the control strategy, 428, 501, 505–506 rearing, 45, 52
Diapause, 10, 13–16, 24, 44, 173–175, 195, 202, 241, sampling, 43–46
262, 277, 279, 401 Egg stage, 24, 31
Diazinon, 445, 448, 455, 456 Egg tooth, 16
Dibrom, 453 Electric mosquito mats, 495
Dibutyl phthalate, 493 Electronic mosquito repellents, 47, 495–496
Dichlobenil, 467 Embryogenesis, 11, 13, 16, 195, 196, 470
Dichlorodiphenyltrichloroethane (DDT), 29, 347, Embryonic development, 10, 13, 468
430, 441–446, 450–452, 460, 461, 464, 472, Emergence inhibition (EI), 468, 469
473, 491, 499, 507 Empodium, 71
Dichlorvos (DDVP), 454 Emulsifiable concentrates (EC), 446–447, 455–457, 462,
Diflubenzuron, 445, 466–468, 480, 500 463, 492
Dilatation of the ovarial epithelium, 56 Encapsulated materials, 448
556 Subject Index

Encephalitis, 25, 31, 32, 34, 36–38, 50 F

Encephalitis virus surveillance trap (EVS), 49–51, Fan-like seta, 78, 84
429, 501 Fascicle. See Stylet bundle
Endemic malaria, 28, 30, 325, 450, 456, 492 Fat body, 19, 23, 24, 278, 419, 431
Endochorion, 11 Fatty acids, 45
Endogenous mechanisms, 486 Feeders, 17, 79, 291, 298, 408
Endogenous meiotic drive, 488 Feeding
Endophagic, 23, 342, 347, 379, 381, 430, 464, 499 adults, 22–24, 66
Endophagy, 23, 224 larvae, 17, 18, 77, 78, 426, 478, 505
Endophilic, 23, 30, 174–176, 379, 381, 430, 450, Femur, 71
458, 499, 505 Fenitrothion, 444, 445, 448, 449,
Endophily, 23, 491 454–455, 471, 507
Energy source, 23, 51 Fenoxycarb, 466, 470
Entomological research (monitoring), 501–503 Fenthion, 444, 445, 449, 455, 457, 471
Entomological studies, 43 Ficam. See Bendiocarb
Environmental control measures, 472, 500 Filariasis, 25, 39–40
Environmental impact, 422, 429–430, 437, 465, 508 Filter feeders, 17, 79
Environmental management, 427, 433–439, Fin. See Ventral brush
499, 500, 506 Fish (Osteichthyes), 406–408
Environmental manipulation, 433 Flagellomere, 64
Environmental modification, 433, 501 Flagellum, 20, 63
Environmental Protection Agency (EPA), 60, 422, 454–456, Flatworms. See in Taxonomic Index
495, 507 Flight behaviour, 21
Environmental safety, 422, 427, 508 Flight range, 9, 21, 173, 174, 176,
Enzootic vector, 36, 453 183, 224, 332, 342, 349, 357, 366, 375,
Enzyme inhibition, 452, 458 376, 378, 401
Epicranial plates, 78, 79 Flood catchment areas, 438
Epicranial suture Flooding method, 44
adult, 64 Floodwater mosquitoes
larva, 79 dispersal, 21
Epidemiological studies, 43 egg-laying behaviour, 10–12
Epidemiology, 487, 489, 503 embryonic development, 13
Epimeron, 70 hatching, 13–16, 19
Epiproct, 72, 73 hibernation, 24
Episternum, 70 larval development, 15
Epizootic, 32, 36, 400, 442 Food chain, 450, 452
Equine encephalitis viruses, 31 Food channel. See Labroepipharynx
Equipment calibration, 448, 449, 508 Formulations, 59, 424–428, 445–449, 453, 455–459,
Erythrocytes, 27, 28, 55 462, 463, 465, 468–470, 478, 493–497,
Erythrocytic schizogony, 27 504–509
Ether, 54 Frequency of treatments, 508
Ethyl acetate, 48, 54 Freshwater snails, 409
Ethyl hexanediol, 493 Fringe scales, 72
Etofenprox, 444, 445, 449, 460, 463, 493, 507 Frons, 65
European Biocides Directive, 508 Frontal setae, 79, 80
European Centre for Disease Prevention and Control Frontal sutures, 64, 65
(ECDC), 31 Frontoclypeus, 78, 79
Eurygamy, 20, 171 Fumigants, 55, 444, 446, 454
Exit trap, 48 Fungi, 278, 416–418, 442
Exophagic, 23, 178, 182, 217, 227, 306, 325, 378, 430, 499
Exophagy, 23, 167
Exophilic, 23, 167, 170, 175, 182, 224, 344, G
378, 430, 499, 505 Gametocyte, 28, 29, 486
Exophily, 23, 166, 170, 182 Gastritis, 35, 39
Extended duration repellent formulation (EDRF), 494 Genae, 65
Extended residual briquettes (XR), 448 Gene dominance, 474
External genitalia slide preparation, 55 Genetic control, 442, 483–490, 500
Exuvia, 19, 467 Genetic engineering, 424
Eyes Genetic manipulation, 29
adult, 65 Genetic mapping, 56
larva, 16, 79, 80 Genetic maps, 56
Subject Index 557

Genetic markers, 26, 57, 277 Humeral vein, 72

Genetic techniques, 442, 488–490 Humidity chamber, 54
Genetic translocation, 442 Hydras, 405, 411, 423
Genitalia, 55, 73–75, 85 Hydrophilic, 10, 478
Genital lobe, 85, 86 Hydrophobic, 10, 17, 19, 478
Genome, 31, 37, 56, 58, 325, 483, Hydrostatic organs, 77
487, 488, 500 Hypnozoites, 27
Genotype, 57 Hypopharynx, 23, 66
Geographic Information Systems (GIS), Hypopygium, 20, 73–76
503–504 Hypostigmal area, 70, 71
Glycoprotein receptors, 420 Hypostigmal patch, 71
Gnathocephalon, 63, 65 Hypostomal bridge, 65
Gonocoxal apodemes, 74
Gonocoxite, 73–75
Gonopod, 73 I
Gonostylus, 73, 74 Ice granules, 424, 425
Gonotrophic cycle, 29, 53, 55, 56, 198 Imaginal disks, 19
Grid, 84 Immune responses, 23, 37, 40, 487
Grid ditching, 437 Immunological repercussions, 489
Gut epithelium, 40 Immunotoxin, 487
Implementation, 428, 430, 451, 471, 489, 499–509
Impregnated bed nets, 462, 464, 491–493
H Impregnation, 460–462, 473, 491, 492
Haemocele, 26, 27 Incidence, 10, 28, 41, 170, 177, 198, 277, 442, 465, 492, 502
Haemolymph, 20 Indigenous malaria, 29
Haemorrhagic fever, 31, 35, 36, 310 Indigenous population, 483, 484
Halophilous species, 9 Indoor catches, 47–48
Halteres, 67, 71 Inert ingredients, 495
Hand-operated compression sprayer, 448 Infectious bites, 492, 495, 503
Harpagones. See Claspettes Influenza-like symptoms, 33, 38
Harpes. See Claspettes Information dissemination, 439
Hatching, 9, 11, 13–16, 19, 24, 44, 52 Inner clypeal setae, 78, 79
Hatching in installments, 16 Inner division of aedeagus, 76
Hatching process, 13, 15 Inoculation, 33, 405, 412, 414, 416, 502
Hatching stimulus, 44 Insect growth regulators (IGRs), 45, 59, 443, 445, 446, 457,
HBC. See Human bait catches 466–470, 480, 499
Head Insecticide
adult, 23, 54, 63–67 application techniques, 448–449, 472, 504, 506
capsule, 16, 18, 63, 64, 77, 78, 467 containers–disposal, 508
larva, 16–18, 53, 76–80 droplet size, 447, 449, 453
Heart failure, 40 formulations, 446–448, 497
Heartworm, 40, 203, 279, 333, 351, 365, 366, 394. See also label requirements, 508
Dog heartworm registration, 507–508
Hepatitis, 36 resistance, 30, 41, 431, 451, 458, 471–475
Heterocyclic organophosphates, 455–457 insecticide-treated bednets (ITNs), 28, 430, 473, 489,
Heteromorphic sex chromosomes, 56 491, 492
Heterozygous, 474, 485 Insemination, 20
Hibernating, 24, 36, 39, 215, 224, 262 Instar sensitivity, 426
Hibernating shelters, 24 Integrated biological control (IBC), 427
Hibernation, 19, 24, 167, 174–176, 179, 184, 191, 193, 248, Integrated control strategy, 506
283, 285, 286, 288, 290, 294, 296, 297, 301, 303, 306, Integrated mosquito management (IMM), xxix, xxx, 406, 408,
312, 400, 411 422, 430, 442, 460, 471–473, 501–502
Holoptic, 64 Integrated vector management (IVM), xxix, xxx, 430, 442,
Homomorphic chromosomes, 56 463, 471, 473, 477, 479, 499, 501–509
Hoofprints, 400 Integration of mosquito control measures, 499–509
Horizontal transmission, 30 Internal seta, 75
Host odour, 21, 22, 47, 48 International toxic units (ITU), 59, 423, 425,
Host-seeking, 21–22, 47, 48 427, 428, 505
House martin, 409, 410 Interocular space, 65
House mosquito, 278, 465, 472, 496 Interstrain fertility, 485
Human bait catches, 47, 501 Intervention areas, 492, 501
558 Subject Index

Intracellular symbiont, 485, 488 Lateral branched seta, 78

Intrinsic muscles, 63, 66, 71 Lateral lobes, 85
Inundation, 175, 193, 215, 231, 267, 277, 405, 406, Lateral palatal brushes, 17, 76, 79
429, 469 Lateral plate, 82
Inversions, 57, 453 Lateral stripes, 70
Invertebrate predators, 410–415 Lateral teeth. See Lateral arm
Iridescent virus, 431 Leaflets of aedeagus, 75
Irradiation, 485 Leaflets of palmate seta, 82
Isogametes, 416 Lecithin, 478
Leeches (Hirudinea), 23
Legs, 10, 20, 40, 48, 54, 63, 67, 71, 85
J Lemon eucalyptus See in Taxonomic Index
Japanese B encephalitis, 334, 367 Light trap, 46, 49, 50, 217, 430, 502
Japanese encephalitis (JE), 34, 227, 279, 333, 334, Ligula, 66
350, 437 Linkage maps. See Genetic maps
Johnston’s organ, 20, 63 Liparol, 478
Juvenile hormone, 441, 443, 466, 468–469 Liquid vapourizer, 495–497
Juvenile hormone analogs (JHAs), 466, 468–469 Longevity, 25, 29, 60, 418, 497
Juvenoids. See Juvenile hormone analogs Longevity estimation, 56
Long term control, 421, 456, 469
Long-term reduction, 434
K Lower anal setae, 81, 83
Kairomones, 48, 49, 462 Lower mesepimeral setae, 71
Karyotype, 56, 57 Lower mesepisternal setae, 71
Katepimeron, 70 Lower postpronotal patch, 71
Kerosene emulsion, 446, 454 Lucky bamboo (Dracaena sp.), 9, 203
Knock-down effect, 418, 423, 449, 460, 461 Lymphatic filariasis. See Filariasis
Knock-down resistance (kdr), 461
Knot-like dilatation. See Dilatation of the ovarial epithelium
M
MacGregor’s solution, 53
L Malaria
Labella, 23, 66 quartan, 28
Labium tertiana, 28
adult, 23, 63, 66 tropica, 28
larva, 40, 79 Malathion, 444, 446, 449, 452–453, 455, 456, 462–464, 471,
Labral brushes, 76, 141, 190, 194. See also Lateral palatal 499, 507
brushes Malayan filariasis, 279, 332
Labroepipharynx, 23, 65, 66 Malignant malaria, 28
Labro-palatum. See Labroepipharynx Malpighian tubes, 40
Labrum, 66, 79 Management and monitoring of insecticide resistance, 471–475
Labyrinth fish, 408 Management techniques, 430, 438, 499
Lacewings. See in Taxonomic Index Mandibles
Lactic acid, 21, 22, 48, 57, 494 adult, 23, 66
Lambdacyhalothrin, 446, 460, 465, 493 larva, 79
Landing rate counts. See Human bait catches Mandibular stylets, 66
Larvae Mapping of the breeding sites, 503–504
biology, 9–11, 13–19, 24 Mark-recapture, 51
key, 135–162 Mass drug administration, 481
morphology, 76–84 Mass media, 438, 439
preserving, 53 Mass rearing, 410, 411, 416, 419, 484–486
rearing, 52, 77, 484 Mating, 7, 20, 39, 52, 72, 73, 483–485
sampling, 46–47 Matronae, 20
Larval food, 17 Maxillae
Larval indices, 436, 439 adult, 23, 66
Larval siphon, 81–83 larva, 79
Larval stage, 19, 20, 24, 40, 46, 85, 413, 428, 468 Maxillary laciniae, 66
Larviciding, 444, 446, 447, 449, 499, 501, 504 Maxillary palps, 63, 66, 67, 79
Laser leveling, 433 Maxillary stylets, 23, 66
Lateral aedeagal plates, 75, 76 Mayflies. See Ephemeroptera in Taxonomic Index
Lateral arms (outer division), 76 Median caudal lobe, 85
Subject Index 559

Median keel, 85 Migration distances. See Flight range

Median membrane, 73 Minimum effective dosage, 505
Median spine, 71 Mist blower, 423, 448
Median stripe, 70 Mites, 411–412, 471
Medical importance, 25–42, 166, 168, 170, 176–178, 180, 182, Mode of action (insecticide), 451–452, 458, 460–461, 467–468,
183, 185, 186, 196, 201, 203, 211, 215, 218, 227, 229, 470, 475
242, 267, 271, 275, 277, 279, 280, 282, 296, 302, 310, Modification of breeding habitats, 500
312, 315, 323, 325, 326, 328, 330, 332, 340–346, Modification of the air-water interface, 478
347–350, 357, 359, 360, 362, 364–367, 374–379, Molecular genetics, 500
381–383, 385, 386, 394, 397, 398, 400, 401 Molecular methods, 4, 57–58
Medio-cubital vein, 72 Molting hormone, 18
Meiotic drive genes, 442, 488 Monitoring, 41, 49, 58, 429–430, 451, 471–475, 501–503, 508,
Melanization, 486 509
Mendelian inheritance, 487 Monocyclic. See Univoltine
Meningoencephalitis, 36 Monogamous, 483, 484
Mentum, 79, 277 Monomolecular surface films (MSF), 478–480
Mermithid parasites, 415 Monomorphic, 57
Meron, 70 Monophyletic, 3, 4
Merozoites, 27, 28 Mosquito
Mesepimeral patch, 71 abundance, 429, 454
Mesepimeron, 70, 71 breeder, 47, 52
Mesepisternal patch, 71 coils, 466, 495, 496
Mesepisternum, 70, 71 fish (Gambusia affinis), 405, 406
Mesh cage, 52, 60 magnet, 50, 51, 481
Mesomeron, 70 trap, 49–51, 429, 481
Mesonotum, 68 Mosquito-borne diseases, 34, 41–43, 315, 408, 442, 454, 460,
Mesopleural suture, 70 465, 491, 494
Mesopleuron, 67, 70 Mosquitocidal activity, 422
Mesosternum, 70, 71 Mosquitocidal bacteria, 419
Mesothoracic spiracles, 68, 70, 85 Mosquito-roofing, 47, 48, 323, 433, 435
Mesothorax, 67, 80, 85 Moult, 441, 466–468
Mesotrochantin, 70 Moult inhibitors, 441, 466
Metabolic disruptors, 441, 466 Mounting, 53
Metameron, 70 Mouth parts
Metamorphosis, 19, 468, 470 adult, 22, 23, 63, 66
Metanotum, 67, 69 larva, 16–18, 40, 77, 79
Metapneustic, 82 Multiple resistance, 471, 472
Metathoracic spiracles, 70, 71 Multipolymer sustained-release, 494
Metathorax, 67, 70, 80 Multivoltine, 14, 383, 392
Metepimeron, 70 Murray Valley fever, 362
Metepisternum, 70 Mutagenic, 485
Methane, 10, 45 Mutations, 485
Methoprene, 446, 457, 466, 468, 469–470, 507 Myocarditis, 36
Metofluthrin, 465–466, 496, 497 Mysids (Crustacea), 455
Microarray platforms, 486 Myxomatosis, 366
Microbial control agents, 416, 418, 422, 426–431, 499, 500,
505, 507, 508
Microbial larvicides, 59, 470 N
Microbial pathogens, 406 Naled, 446, 449, 453–454
Microclimatic factors, 16 Neck. See Cervix
Micro-encapsulated products, 448 Neem oil, 494
Microfilariae, 39, 40 Net impregnation, 462, 491
Microfilarial infection, 481 Netting, 47, 50, 52, 495, 507
Microsatellite markers, 486 Nocturnal, 39, 301, 310, 406, 410
Microvilli, 27, 420 Non-oriented dispersal, 21, 22
Midges. See Chironomidae in Taxonomic Index Nontarget organisms, 420–422, 431, 442, 468, 469, 479,
Midgut cells, 420, 424, 426 499, 505
Midgut epithelium, 26, 420 Notched organ, 17, 163
Midrib, 85, 87 Notum, 67
Migrating birds, 36 Novaluron, 466, 467
Migration, 21, 22, 30, 43, 57, 191, 193, 196, 224, 259,501, 505 Novel insecticide classes, 470–471
560 Subject Index

Nuclear polyhedrosis virus, 431 Parasporal body (PSB), 419–421, 424

Nulliparity, 56 Paratergite, 69
Nutrition, 23, 191, 426 Paratransgenic strategies, 487
Nuvan. See Dichlorvos Parity, 56, 60
Passive migration, 21
Pathogens, 25, 26, 29, 31, 36, 41, 43, 55, 56, 198,
O 315, 405, 406, 416–431, 433, 441, 442, 483, 484,
Occipital foramen, 79 486–488, 500
Occiput PCR. See Polymerase chain reaction
adult, 65 Pecten, 77, 81–83
larvae, 79 Pedicel, 20, 63
Octenol, 21, 51, 481 Pellets and briquettes, 424, 448, 469
Olfactory stimuli, 21, 48 Peptide, 487
Oocyst, 26, 27, 29, 487 Permethrin, 444, 446, 448, 449, 457, 459, 460, 462, 464–465,
Oocytes, 55, 56 472, 473, 491–493
Oogenesis, 21 Personal hygiene, 508
Ookinete, 26, 27, 486 Personal protection, 28, 60, 461, 462, 491–497
Oospores, 417, 418 Pesticide storage, 508
Operational maps, 504 Petroleum oils, 477
Optimum effective dosage, 505 Phagostimulants, 23
Oral toxicity, 445, 491, 500 Phallosome, 74
Orcein, 57 Pharate, 19
Organic phosphorous. See Organophosphates Pharyngeal pump, 23
Organochlorines. See Chlorinated hydrocarbons Phenetic clustering, 4
Organophosphates, 58, 444, 452–458, 507 Phenolic compounds, 21
Oriented host location behaviour, 21 Phenotype, 57, 176
Ornamental pools, 400 Phenyl derivate, 454, 455
Ornithophilic species, 22, 24 Pheromones, 12, 20, 468
Ornithophily, 23 Phosphoric acid esters. See Organophosphates
Osmoregulation, 84 Phosphorus esters. See Organophosphates
K-Othrine, 464, 493 Phosphorus insecticides. See Organophosphates
Outdoor resting catches, 47 Photoperiodic sensitivity, 9
Outer clypeal setae, 79 Phoxim, 456
Outer division of aedeagus, 76 Phylogenetic trees, 3
Ovarioles, 16, 55, 56 Physical colouration, 63
Overwintering, 24, 31, 38, 176, 177, 233, 238, 250, 262, 276, Physical control, 477–481, 500
359, 392, 395 Physiological stage, 21, 47, 55–56
Ovicidal effects, 468 Piercing, 17, 22, 23, 63, 66, 83, 85
Oviposition Pigment colouration, 63
attractants, 45 Pink shrimp, 455
behaviour, 12, 241, 246 Pinnate seta, 77, 78
oviposition traps (See Ovitraps) Pinning, 54
Ovipositor, 76 Piperonyl butoxide (PBO), 460, 463, 465, 474
Ovitraps, 45, 462 Pirimiphos methyl, 444, 446, 449, 456–457,
472, 500, 507
Pit latrines, 480
P Plankton net, 46
Paddles, 19, 85–87 Plasmid, 421
Palatum, 65, 79 Plesiomorphies, 3
Palmate setae, 19, 78, 82, 85 Pleurae (Pleurites), 67, 68, 70
Palpomeres, 66 Pleural regions, 72
Palpi, 63, 66, 67, 79 Pleural suture, 70
Parabasal setae, 75, Plumose antennae, 20, 63
Paraffinic oils, 477 Plumose seta. See Pinnate seta
Parameral apodemes, 74 Polyacrylamide, 57
Paramere. See Gonocoxite Polyarthritis, 35
Paraphyletic, 3 Polycyclic. See Multivoltine
Paraproct crown, 76 Polycyclic aromatic hydrocarbons (PAHs), 496
Paraprocts, 73, 75, 76 Polymerase chain reaction (PCR), 26, 58, 474
Parasites, 25–30, 40, 43, 55, 198, 208, 242, 290, 343, 405, 406, Polymorphism, 57
415–419, 442, 486, 487, 500, 503 Polyporous, 54
Subject Index 561

Polystyrene beads, 477–481, 500 Q

Polytene chromosomes, 56, 57, Quartan malaria, 28
323, 344 Qwenling, 494
Postacrostichal patch, 70
Postclypeal setae, 79
Postclypeus, 65 R
Posterolateral spiracular lobe, 81 Radial sector, 72
Postgenital plate, 76 Radio-medial vein, 72
Postnotum, 69 Radius, 72
Postocciput Rash, 31–33, 35, 36
adult, 65 Rearing mosquitoes, 51–53
larva, 79 Rearing temperature, 52, 200
Postprocoxal membrane, 70, 71 Receptors, 21, 22, 63, 420–422, 424, 426, 472
Postprocoxal patch, 71 Recombination, 488
Postpronotal setae, 69 Recycling processes, 427
Postpronotum, 67, 69–71 Refractoriness, 486–488
Postspiracular area, 70, 71 Refractory, 29, 483, 486–488, 500
Postspiracular patch, 71 Refugia, 474
Postspiracular setae, 71 Registration of insecticides, 507–508
Preala, 70, 71 Regulation, 31, 84, 196, 405, 434, 436, 439, 450, 460, 507, 508
Precratal setae, 84 Repellents, 58–61, 459, 465, 491, 493–497
Predators, 11, 12, 15, 17, 20, 36, 405–416, 427, 430, Research techniques, 43–61
437, 442, 452, 460, 489, 503, 506 Residual spraying, 430, 444
Prehensile setae, 79 Resin formulations, 465, 496
Prementum, 66 Resistance, 28, 30, 41, 58, 217, 405, 421, 424, 425, 429–431,
Prescutellar area, 70 433, 442, 443, 450–452, 454–458, 460–466, 471–475,
Prescutum, 67 477, 481, 483, 484, 486, 499, 502, 508
Preserving mosquitoes, 53–55 management, 472–475, 508
Prespiracular area, 70 mechanisms, 472, 473, 475
Prespiracular setae, 69 surveillance, 472–474
Pretarsus, 71 Resmethrin, 446, 460, 463, 473
Primary health care concept, 427 Respiratory trumpets, 19, 85, 86, 307, 401
Primordial compound eyes, 79, 80 Resting behaviour, 23, 381
Proboscis, 23, 39, 63–67 Restriction maps, 56
Procoxa, 70, 71 R-genes, 472, 474
Proctiger, 73–75, 85 Rice production, 436, 437
Progeny, 485, 500 Rift Valley fever, 37, 282, 317, 328, 362, 473
Propleuron, 70, 71 Risk assessment,
Propoxur, 444, 446, 449, 456, 458–459, Rockholes, 168, 392
484, 507 Roll Back Malaria (RBM), 28, 430
Prosternum, 70, 71 Roof gutters, 435
Protein crystal, 419, 420 Ross River virus, 31, 32, 332, 351, 359, 360, 362, 364–366, 466
Protein-electrophoresis, 57, 275 Rotenone,
Prothorax, 17, 67, 70, 80 Routine treatments, 427, 504, 505, 508–509
Public health, 29, 35, 37, 315, 422, 439,
442, 451, 453, 455, 458, 459, 462–464,
471, 483, 499 S
Public information systems, 509 Saddle seta, 81, 83
Pulvilli, 71 Saliva, 23, 26, 66
Pupae Salivary channel. See Hypopharynx
biology, 19 Salivary glands, 26, 27, 56, 57, 344, 486
morphology, 84–87 Salt marshes, 84, 217, 227, 251, 326, 365, 392, 394, 433, 437,
preserving, 53 438, 479, 481
sampling, 46–47 Saltwater method, 44
Pupal trumpet, 20, 85, 478 Sampling, 8, 43–54, 168, 315, 409, 428
Pyrethrins, 48, 446, 459, 460, 463, 474 Sandflies. See in Taxonomic Index
Pyrethroids, 58, 441, 443–445, 449–451, 456, Sanitation, 29, 39, 436
459–466, 470, 471–474, 491–496, 507 Scape, 63, 64
Pyrethrum, 459, 473, 494 Schizogonic cycle, 28
Pyrethrum flowers, 459 Schizogony, 27, 28
Pyriproxyfen, 446, 466, 470 Schizont, 27, 28
562 Subject Index

Sclerotised plate, 78, 82, 83 Striders, 20, 478

Screening, 491 Stripes, 63, 70, 71, 76
Scutal angle, 68, 69 Stylet bundle, 23
Scutal fossa, 68 Stylets, 23, 63, 65, 66
Scutellar setae, 69 Subapical lobe, 73
Scutellum, 67, 69 Subbasal tooth, 71
Scutum, 54, 63, 67–69, 85 Subcosta (Sc), 72
Selection of appropriate tools, 501, 504 Subcostal-radial vein, 72
Sensilla, 23, 66 Submedian stripes, 70
Sentinel chickens, 33 Subspiracular area, 70, 71
Sentinel rabbits, 33 Subspiracular patch, 71
Serosal cuticle, 11 Supraalar setae, 69
Serotypes, 32, 34, 35 Surface films, 478–481
Setae, 7, 17, 19, 53, 56, 63, 69–71, 73, 75–80, 82–86 Surfactants, 477, 478
Sewage systems, 434 Suspension feeders. See Filter feeders
Sewage treatment, 435 Sustained-release formulation, 494
Sexual dimorphism, 484 Swarming, 20, 50, 171, 173, 174, 219, 233, 246, 250, 277, 310
Sexual maturity, 20, 415 Sylvatic yellow fever, 382
Sibling species, 7, 8, 25, 26, 56–57, 166, 170, 171, 191, 216, Sympatric, 168, 170, 176, 218, 486
219, 220, 222, 224, 231, 240, 275, 323, 325, 347 Synapomorphies, 3
Sidepiece. See Gonocoxite Synergists, 449, 459, 463, 472, 474
Sigmoid setae, 79 Synthetic repellents, 494
Silicon dioxide, 469
Siphon, 10, 16, 17, 76, 77, 82, 83, 85
Siphonal index, 82 T
Siphonal setae, 83 Tablets, 424, 425, 429, 447–448, 468, 507
Slow release systems, 447–448 Tadpole shrimp. See Triops cancriformis in Taxonomic Index
Snow-melt mosquitoes Tarsomeres, 71
dispersal, 21 Tarsus, 71
hatching, 13, 14 Taxonomic techniques, 56–58
hibernation, 24 Technical concentrates (TC/TP), 446
larval development, 18 Temephos, 444, 446, 455, 457–458, 471, 472, 500
Socio-economic aspects, 439 Terga, 63, 73, 85
Soil samples, 16, 44 Tergal plate, 81, 82
Soluble powders (SP), 447 Tergum (Tergites), 67, 72, 73, 75, 85. See also notum
Solution concentrates (SC), 446, 447 Terminal spine. See Median spine
Source reduction, 433–436, 462, 477, 507 Tertian malaria, 28
Southern house mosquito. See Culex pipiens quinquefasciatus Thermal foggers, 448, 449
Space spraying, 444, 499 Thermal stimuli, 21
Spatial analysis, 504 Thoracic setae, 80
Spermatheca, 20, 164, 187, 484 Thorax
Spermatozoa, 20 adult, 67–72
Spicules, 79, 85 larva, 80
Spiders. See in Taxonomic Index Threshold concentration, 472
Spinosad, 419 Threshold for vector mosquitoes, 502–503
Spiracular lobes, 16, 17, 81, 83 Threshold infestation level, 502
Spiracular plate, 82, 83 Tibia, 71
Spiracular teeth, 83 Timing and frequency of treatments, 508
Sporogony, 26, 28 Toxicity by hazard, 445
Sporozoite infection rate, 492 Toxin genes, 421
Sporozoites, 26, 27, 326, 486, 492, 495 Toxin proteins, 420, 424
Springtails. See in Taxonomic Index Tracheal trunk, 17, 81, 85
Standard pint dipper, 46 Tracheoles, 56
Stellate seta, 78 Training, 28, 428, 433, 492, 501, 504, 506
Stemmata, 79, 85 Transformation, 9, 57, 433, 468, 487, 500
Stenogamy, 20, 171, 173, 277 Transgenic, 487, 489
Sterile hybrids, 442 Transgenic strain, 485, 487
Sterile insect technique (SIT), 483–486 Translocations, 57, 442, 500
Sterile males, 483–485, 500 Transmission cycle, 26, 32–34, 37
Sternum (Sternites), 67, 71–73, 85 Transovarial transmission, 30–32, 35, 36
Stomach poisons, 443, 444, 458, 480 Transposons, 487
Subject Index 563

Transverse suture, 67, 68 Vertical dispersal, 22

Traps, 21, 22, 45–51, 55, 217, 301, 387, 409, 429, 430, 436, Vertical transmission, 30
462, 481, 500–502 Viraemia, 30
Tree-holes, 9, 24, 29, 38, 43, 45, 46, 165, 179, 180, 197, 200, Virus amplification, 36
202, 204, 206–208, 214, 248, 277, 301, 305, 310–312, Visual stimuli, 21
357, 381, 436, 469 Vitellogenines, 19
Triflumuron, 466 Volatile organic compounds (VOCs), 496
Trochanter, 71 Volume median diameter (VMD), 453
Trochantin, 70
Trophozoite, 28
Trumpets. See Respiratory trumpets W
Tubercle, 68, 75, 80 Water beetles. See Coleoptera in Taxonomic Index
Tuft, 78, 83, 84 Water bugs. See Heteroptera in Taxonomic Index
Tularaemia. See Francisella tularensis in Taxonomic Index Water dispersible powders (WDP/WP), 447
Tyres, 41, 42, 469 Water fern, 437
Water hyacinth, 386, 435
Water management, 174, 430, 437, 438, 477, 500
U Water mites (Hydrachnellae), 412
Ultra-low-volume formulations (ULV), 60, 422, 434, 446–449, Water storage, 36, 41, 433–436, 458, 468
453, 454, 456, 459, 463, 464, 508 Water surface tension, 478
Ungues. See Claws Western Pacific Region, 35, 39, 443, 466, 495
Univoltine, 13, 14 West Nile fever, 36, 37
Upper anal setae, 81, 83 Wetland, 351, 434, 436–438, 499, 500, 504
Upper mesepimeral setae, 71 WHOPES. See WHO Pesticide Evaluation Scheme
Upper mesepisternal setae, 71 WHO Pesticide Evaluation Scheme, 422, 443, 444, 448, 451,
Upper postpronotal patch, 71 460, 463, 466, 471, 473, 505
Use of personal protective equipment (PPE), 508 WHO test kits, 472
Wind velocities, 21
Wing beat, 20
V Wing spots in Anopheles, 72
Vapona. See Dichlorvos Wing veins, 63, 72
Vapourizing mats, 496 Woodland species, 21
Vapourizing strips, 447, 454 Woodlice. See Isopoda in Taxonomic Index
Vector
vector-borne diseases, 25, 42, 442, 443, 451, 458, 466, 483,
488, 491 Y
vector capacity, 4, 25, 55, 501 Yellow fever, 31, 34, 47, 188, 201, 317, 382, 442
vector management, 28, 427–430, 433, 442, 443, 465, 489 Yolk synthesis, 468
Veins. See Wing veins
Venation, 72
Ventral arm of the paraproct, 76 Z
Ventral brush, 78, 84 Zoophily, 24, 49, 173, 182
Vertebrate predators, 406–410 Zoospores, 416, 417
Vertex, 65 Zygopteran nymphs, 412
Taxonomic Index

A systematics, 188, 189

Abraedes genus, 6 viruses carried by, 33, 38
Abraedes subgenus, 6 Aedes circumluteolus, 317
Abramis brama, 16 Aedes cooki, 351
Acalleomyia subgenus, 5 Aedes cretinus, 203–204
Acallyntrum subgenus, 5 identification, 97, 119, 153
Acanthocyclops vernalis, 412, 416 Aedes dahuricus, 189
Acari, 422, 423 Aedes duplex, 216
Acartomyia genus, 6 Aedes esoensis, 189, 192
Acartomyia mariae. See Ochlerotatus mariae Aedes furcifer, 317
Acartomyia phoeniciae. See Ochlerotatus phoeniciae Aedes geminus, 191–192
Acartomyia zammitii. See Ochlerotatus zammitii identification, 101, 118, 142
Actinotrix subgenus, 7 systematics, 189
Aedeomyia genus, 5, 79 Aedes genus, ix, x, xii, 187–188
Aedeomyia subgenus, 5 biology, 9
Aedeomyiini tribus, 5 dispersal and host-seeking behaviour, 21, 22
Aedes aegypti, 198–201 embryonic development, 13
control, 407, 412, 414, 425, 431, 434–436, 438, 455, hatching, 13–16
457, 458, 461, 462, 468, 470–472, 485, 487, 488, hibernation, 24
494–497, 503, 505, 507 larvae, 17, 18
identification, 97, 119, 142, 153, 321, 329, 333, 339, 351, oviposition, 11
354, 369, 371, 373, 389, 390 control, 408, 411–413, 415, 423, 426,
medical importance, xxviii, 31, 32, 34–36 428, 430, 434, 437, 439, 454, 456,
research, egg sampling, 45, 47, 55, 59 457, 465, 468–470, 502, 503
ssp. formosus, 201 identification, 91, 92, 95–106, 113, 118–128,
var. queenslandensis, 201 135, 136, 141–154, 318, 321, 334,
Aedes africanus 351–353, 370, 373, 388
medical importance, 34 medical importance, 31, 33, 35, 38–40
Aedes albocephalus, 317 morphology, 71, 73–76, 79, 82
Aedes albopictus, 9, 201–203 research
control, 414, 435, 436, 438, 439, 454, 456–458, 462, 463, egg sampling, 44
465, 485, 488, 507 rearing, 52
identification, 97, 119, 153, 154, 321, 333, 339, 351, 354, systematics, 4, 6, 7
369, 373, 387, 389, 390 See also Aedes/Ochlerotatus
medical importance, xiii, xxix, 31, 35, 41 Aedes hebrideus, 351
research, egg sampling, 45 Aedes hensilli, 351
Aedes argenteus, 201 Aedes luteocephalus, 317
Aedes bromeliae Aedes melanimon
medical importance, 34 medical importance, 37
Aedes calopus, 201 Aedes mubiensis, 189
Aedes cinereus, 189–191 Aedes/Ochlerotatus
biology biology
dispersal and host-seeking behaviour, 21, 22 dispersal and host-seeking behaviour, 21, 22
feeding, 23 egg-laying behaviour, 9
control, 494 embryonic development, 13
identification, 101, 118, 137, 142 hatching, 13, 15–16

565
566 Taxonomic Index

Aedes/Ochlerotatus (cont.) Alphavirus, 31, 208, 229

hibernation, 24 Amblyospora, 418, 419
larvae, 17 Amphibia, 32, 285, 286, 288, 298, 314, 406, 408–409, 422,
control, 408, 412, 413, 423, 426, 428, 430, | 423, 429, 430
454, 456, 457, 468–470, 502 Amphicorisa, 412
identification, 92, 95–108, 113, 118–128, 136, 141–154 Anabaena, 500
medical importance, ix, 33, 40 Anas platyrhynchos, 409
morphology, 73–75, 79 Anisopodidae systematics, 3
research Ankylorhynchus subgenus, 5
egg sampling, 44–45 Annelida, 422, 423
rearing in laboratory, 52 Annulipes Group, 209–211, 214
Aedes opok, 317 Anoedioporpa subgenus, 5
Aedes polynesiensis, 32, 351, 412 Anopheles aconitus, 333
Aedes rossicus, 193–194 Anopheles albimanus, 376–377
biology, dispersal and host-seeking behaviour, 22 identification, 370
identification, 95, 101, 114, 118, 142 medical importance, 30
systematics, 188, 189 Anopheles albitarsis
Aedes rotumae, 351 medical importance, 30
Aedes sasai systematics, 189 Anopheles algeriensis, 165–166
Aedes scutellaris, 351 identification, 93, 115, 116, 137, 138
Aedes subgenus, 6, 67, 76, 188, 321, 339, 353, 372, 389 medical importance, 29
Aedes taylori, 317 morphology, larvae, 79
Aedes vexans, 194–196 Anopheles amictus
biology medical importance, 30
dispersal and host-seeking behaviour, 21 Anopheles annulipes s.l., 351, 362
egg-laying behaviour, 10–12 Anopheles aquasalis, 377–378
embryonic development, 13 identification, 370, 371
hatching, 13–16 medical importance, 30
larvae, 17–19 Anopheles arabiensis, 325
control medical importance, 25, 30
resistance, 424 Anopheles atroparvus, 173
sensitivity to Bacillus, 426 control, 454
identification, 91, 95, 97, 98, 101, 118, 119, 136, 141, 142, identification, eggs, 171, 172
333, 387, 389 medical importance, 29
medical importance, xxvii, 32, 38 Anopheles aztecus, 177, 369
research, egg sampling, 44 Anopheles baimaii, 344
ssp. arabiensis, 196 Anopheles bancroftii
ssp. nipponii, 196 medical importance, 30
ssp. vexans, 196 Anopheles barberi, 180
Aedes vittatus, 196–198 Anopheles barianensis, 180
identification, 97, 114, 119, 142, 153, 154 Anopheles beklemishevi, 173–174
medical importance, 34 identification, eggs, 171, 172
morphology, larva, 97 Anopheles bellator, 369
Aedes yamadai systematics, 189 Anopheles bifurcatus systematics, 168
Aedimorphus genus, 6 Anopheles bwambae, 323, 326
Aedimorphus subgenus, 6, 76, 188, 194, 196 Anopheles calderoni, 374
Aedimorphus vexans. See Aedes vexans identification, 371
Aedini tribus Anopheles cinereus, 180–182
Aedinus subgenus, 5 Anopheles cinereus hispaniola
Aeshna cyanea, 411, 412 identification, 95, 117, 140
Afroculex subgenus, 5 medical importance, 29
Afrorhynchus subgenus, 5 Anopheles Claviger Complex, 82, 166, 168
Agabus spp., 413 Anopheles claviger s.s., 166–168
Aglaonotus subgenus, 6 identification, 94, 116, 138, 139
Alanstonea genus, 6 medical importance, 168
Alanstonea subgenus, 6 morphology, 85
Albuginosus genus, 6 Anopheles cracens, 344
Albuginosus subgenus, 6 Anopheles crucians, 387
Alburnus alburnus, 408 Anopheles cruzii, 369
Allimanta subgenus, 5 Anopheles culicifacies, 341–342
Alloeomyia subgenus, 6 identification, 336
Allotheobaldia subgenus, 5, 289 medical importance, 30
Taxonomic Index 567

Anopheles darlingi, 378–379 Anopheles marteri, 177–178

identification, 370 identification, 93, 116, 117, 138, 139
medical importance, 30 var. conquensis, 178
Anopheles dirus, 342–344 Anopheles martinius, 177
identification, 11, 12 Anopheles melanoon, 175
medical importance, 30 identification, eggs, 171, 172
Anopheles Dirus Complex systematics, 344 Anopheles melas, 10, 324, 326
Anopheles earlei, 177 Anopheles merus, 317, 323, 326
Anopheles elegans, 344 Anopheles messeae, 175
Anopheles farauti, 356–357 identification, eggs, 171, 172
identification, 351 Anopheles minimus, 346–347
medical importance, 30 identification, 335–337
Anopheles flavirostris, 344 medical importance, 30
identification, 337 Anopheles Minimus Complex
Anopheles fluviatilis, 344 systematics, 347
identification, 336, 337 Anopheles multicolor, 182–183
medical importance, 30 identification, 94, 95, 117, 140, 334, 336
Anopheles freeborni Anopheles nemophilous, 344
medical importance, 29 Anopheles nigerrimus, 170
Anopheles funestus, 322–323 Anopheles nuneztovari, 380–381
identification, 318, 319 identification, 370, 371
medical importance, 30, 33 Anopheles occidentalis, 177
Anopheles Gambiae Complex identification, Anopheles paeditaeniatus, 170
25, 30, 323 Anopheles petragnani, 168
Anopheles gambiae s.s., 324–325 identification, 94, 116, 139
medical importance, 25, 30, 33 morphology, pupae, 85
Anopheles genus, 164–165 Anopheles pharoensis, 326–328
biology identification, 318
hibernation, 24 medical importance, 30
larvae, 9, 17 Anopheles plumbeus, 178–180
oviposition, 10 biology, hibernation, 24
control, 408, 414, 424, 427, 428, 434, 435, 456, 457, 459, identification, 93, 94, 115, 116, 137
469, 473, 491, 494, 506, 507 medical importance, 29
identification, 91–95, 113, 115–117, 135, 137–140, 318, morphology, larvae, 79
334, 351, 352, 369, 370, 388 Anopheles pseudopictus, 170
medical importance, vi, vii, 25, 26, 33, 38–40 Anopheles pseudopunctipennis, 374–375
morphology, 63, 66, 69, 72–76, 78, 79, 85 identification, 370, 371
personal protection methods, 491, 494 Anopheles pulcherrimus, 268, 333
research, egg sampling, 43 Anopheles punctimacula, 375–376
Anopheles hilli, 30 identification, 371
Anopheles hyrcanus, 169–170 Anopheles punctipennis, 387
attitude at rest, 163 Anopheles punctulatus, 357
identification, 94, 116, 117, 139, 334 Anopheles Punctulatus Complex
personal protection methods, 494 systematics, 357
var. pseudopictus, 94, 169 Anopheles quadriannulatus s.l., 325
Anopheles hyrcanus group, 334 Anopheles quadrimaculatus, 387
Anopheles koliensis systematics, 357 medical importance, 29
Anopheles labranchiae, 174 Anopheles sacharovi, 175–176
identification, eggs, 171, 172 control, 456
Anopheles lesteri, 340 identification, 93, 171–172
identification, 334, 335 medical importance, 30
Anopheles maculatus, 345–346 Anopheles scanloni, 344
identification, 335 Anopheles sergentii, 183–185
Anopheles Maculipennis Complex identification, 94, 95, 117, 140
eggs, 52, 171, 172 medical importance, 29
identification, 93, 116, 139 Anopheles sicaulti, 177
medical importance, 29 Anopheles sinensis, 340–341
Anopheles maculipennis s.l. See Anopheles Maculipennis identification, 334, 335
Complex medical importance, 30
Anopheles maculipennis s.s., 174 Anopheles sogdianus, 178
control, 409 Anopheles stephensi, 347–348
identification, eggs, 171, 172 identification, 335, 336
568 Taxonomic Index

Anopheles subalpinus, 176–177 Bothromesostoma, 411

identification, eggs, 171, 172 Brachycera systematics, 3
medical importance, 177 Bradysia, 423
Anopheles subgenus, 5, 163–165 Bruceharrisonius genus, 6
identification, males, 115 Brugella subgenus, 5
Anopheles sundaicus, 348–349 Brugia malayi, 39, 279, 332–334, 341, 367
identification, 335, 336 Brugia timori, 39
medical importance, 30 Bufo bufo, 409, 423
Anopheles superpictus, 185–186 Bunyamwera virus, 38
identification, 94, 95, 116, 117, 138, 140 Bunyaviridae (Bunyavirus), 37–39
medical importance, 29, 30 Buvirilia subgenus, 6
Anopheles takasagoensis, 344
Anophelinae subfamily
biology, egg-laying behaviour, 10 C
morphology Cache Valley virus, 37, 39
adult, 63 Caenomyiella subgenus, 5
larvae, 81 California Encephalitis (CE) virus, 37, 196,
pupae, 86 227, 400
Antunesmyia subgenus, 5 Calla, 401
Araneae, 409 Calovo virus. See Batai virus
Argyroneta aquatica, 411, 412 Cancraedes genus, 6
Armigeres annulipalpis, 333 Cancraedes subgenus, 6
Armigeres aurolineatus, 333 Carassius carassius, 408
Armigeres flavus, 333 Carex, 230, 246, 262, 309, 401
Armigeres genus, 6, 65, 66, 83, 333, 338, 414 Carrollia subgenus, 5
Armigeres malayi, 333 Caspius Group, 209
Armigeres subalbatus, 333 Catageiomyia genus, 6
Armigeres subgenus, 6 Catatassomyia genus, 6
Austromansonia subgenus, 5, 307 Cellia subgenus
Austrotheobaldia subgenus, 5 identification, males, 180
Aves, 409 Ceratopogonidae, 3, 38, 415, 423, 453
Ayurakitia genus, 6 Chaetocruiomyia subgenus, 6
Azolla, 500 Chagasia genus, 5, 69, 76, 78, 163
Aztecaedes genus, 6 Chaoboridae
Aztecaedes subgenus, 6 morphology, pupae, 87
Chaoborus, 415, 423
Chikungunya virus, 31–33
B Chironomidae, 409, 410, 429
Babanki virus, 33 morphology, 63, 87
Bacillus sphaericus (B.s.), 59, 406, 421–422, 424–426, Chiroptera (bats), 409–410
428–430, 500, 507 Chlorohydra viridissima, 411
Bacillus thuringiensis israelensis (B.t.i.), 406, 407, 418–422, Christophersiomyia genus, 6
424–430, 480, 506, 507 Christophersiomyia subgenus, 6
Bacillus thuringiensis kurstaki, 424 Chrysanthemum, 459
Baimaia subgenus, 5, 164 Chrysoconops subgenus, 6
Barraudius subgenus, 5, 264, 265 Chytridiales, 416, 417
Batai virus, 38–39 Climacura subgenus, 5
Beauveria, 418 Cloeon dipterum, 423
Belkinius genus, 6 Cnidaria, 422, 423, 429
Belkinius subgenus, 6 Coelambus impressopunctatus, 413, 423
Belkinomyia subgenus, 5 Coelenterata, 411
Bibionomorpha systematics, 3 Coelomomyces psorophorae, 416, 417
Bifidistylus genus, 6 Coelomomyces spp., 416
Bironella genus, 5, 76, 78, 163 Coenagrion puella, 412
Bironella subgenus, 5, 67, 72 Coleoptera, 409–411, 413–414, 422, 423, 457
Blastocladiales, 416 Collembola, 409, 457
Blephariceromorpha systematics, 3 Collessius genus, 6
Bohartius subgenus, 7 Collessius subgenus, 6
Bombina bombina, 409 Colymbetes fuscus, 414
Borichinda genus, 6 Colymbetinae, 413, 414
Bothaella genus, 6 Communis Group, 209
Bothaella subgenus, 6 Conopostegus subgenus, 6
Taxonomic Index 569

Coquillettidia buxtoni, 307–308 Culex hortensis

identification, 111, 134, 162 identification, 108, 128, 129, 136, 154, 155, 166
Coquillettidia genus morphology, larvae, 82
biology Culex impudicus
egg-laying behaviour, 10 identification, 107, 131, 156
embryonic development, 13 Culex inatomii, 265
emergence, 20 Culex laticinctus, 270–271
larvae, 17 identification, 107, 130, 157
control, 428, 469 Culex martinii, 285–286
identification, 92, 111, 114, 134, 135, 162, identification, 107, 129, 131, 155
352, 353, 390 Culex mimeticus, 272–273
morphology, 82, 83, 85, 86 identification, 106, 107, 130, 154, 156, 157
Coquillettidia linealis, 351 Culex modestus, 265–267
Coquillettidia perturbans, 400–401 control, 494
identification, 387, 390 identification, 106, 107, 114, 129, 157
medical importance, 32 medical importance, 36, 38
Coquillettidia richiardii, 308–310 personal protection methods, 494
biology, hibernation, 24 Culex neavei, 317
identification, 111, 134, 135, 162 identification, 320, 329, 330
viruses carried by, 39 Culex nigripalpus, 384–385, 387
Coquillettidia subgenus, 5, 307, 469, 479 identification, 373, 374
Coquillettidia xanthogaster, 367–368 Culex perexiguus, 273–275
identification, 352 identification, 107, 108, 130, 154, 155, 158
Corethrellidae systematics, 3 Culex Pipiens Complex, 275
Corixa punctata, 412 Culex pipiens erectus, 277
Corixidae, 412 Culex pipiens pallens, 275, 277, 472
Cornetius genus, 6 Culex pipiens pipiens, 275–277
Crustacea, 405, 406, 411, 412, 422, 423 biology
Cruzmyia subgenus, 5 dispersal and host-seeking behaviour, 21–22
Ctenogoeldia subgenus, 5 egg-laying behaviour, 10, 13
Ctenopharygodon idella, 408 embryonic development, 13, 18, 19
Culex annulirostris, 365–366 hibernation, 24
identification, 351–356 larvae, 19, 21
Culex antennatus, 328 control, 409, 421, 422, 424, 426–429, 431, 436, 470,
identification, 318–322 473, 481, 485, 488, 502, 505, 507
Culex apicalis, 288 identification, 106–108, 130, 131, 135, 156, 158,
Culex argenteus. See Aedes aegypti 159, 168
Culex australicus, 275 morphology, larvae, 24
Culex bifurcatus. See Anopheles claviger sensitivity to Bacillus thuringiensis israelensis, 426
systematics, 168 viruses carried by, 277, 279, 280
Culex brumpti, 269–270 Culex pipiens pipiens biotype molestus, 277–278
identification, 107, 129, 130, 154, 155, 158 biology
Culex decens, 329 feeding, 277, 278
Culex deserticola, 282 hibernation, 280
Culex duttoni, 317 control, 429
Culex erythrothorax, 387 Culex pipiens quinquefasciatus, 278–279
Culex fasciatus. See Aedes aegypti control, 406, 422, 434, 457, 459, 465, 470, 473, 480, 485,
Culex gelidus, 334 488, 496, 507
Culex genus medical importance, xxvii, 36, 39
biology Culex pipiens torridus, 277
egg-laying behaviour, 10–12 Culex pusillus, 267–268
embryonic development, 13 identification, 107, 129, 156
hibernation, 24 control, 411, 414, 423
larvae, 16–19 Culex quasiguiarti, 329
control, 408, 414, 419, 422, 428–430, 434, 435, Culex restuans, 396–397
437, 454, 456, 457, 459, 463, 465, 469, 470, identification, 391
479–481, 506 Culex richeti, 265
identification, 106–108, 113, 128–131, 136, 154–159 Culex salinarius, 397–398
medical importance, 33, 36, 38–40 identification, 391
morphology, 106–108 Culex simpsoni, 329
research, egg sampling, 43, 45, 46 Culex sitiens, 366, 367
Culex globocoxitus, 275 identification, 319, 320, 334, 338, 353
570 Taxonomic Index

Culex subgenus, 83, 187, 268–269, 372, 390 Culiseta inornata, 387
Culex tarsalis, 398–400 Culiseta litorea, 293–294
control, 406, 411, 461, 465, 468, 470 identification, 109, 132, 133, 161, 162
identification, 390, 391 Culiseta longiareolata, 289–291
medical importance, 32 identification, 83, 108, 115, 132, 159
research, blood meal identification, 55 Culiseta melanura
Culex territans, 287–288 medical importance, 32, 454
identification, 108, 130, 131, 154–158 Culiseta morsitans, 294–296
Culex theileri, 280–282 biology,
identification, 107, 130, 156, 157 behaviour, 22
Culex torrentium, 279–280 hatching, 14
identification, 107, 108, 131, 158, 159 hibernation, 24
medical importance, 33 larvae, 19
morphology, 82 identification, 109, 114, 132, 133,
Culex tritaeniorhynchus, 349–350 159, 161, 162
control, 437 medical importance, 32, 33
identification, 319, 320, 329, 333 morphology, larvae, 79
Culex univittatus, 329–330 Culiseta ochroptera, 296–298
identification, 317, 320 identification, 109, 133, 161
Culex vishnui, 334, 457 Culiseta setivalva, 292
Culicada subgenus, 6 Culiseta subgenus, 298
Culicella subgenus biology
egg-laying behaviour, 295 embryonic development, 13
morphology, larvae, 295–296 larvae, 17
research, egg sampling, 292 oviposition, 10
Culicelsa subgenus, 6 egg sampling, 43
Culicidae, 3–5, 40, 63, 71, 87, 409, 414, 423, 429 morphology, larvae, 79, 83
Culicinae subfamily, 187–314 Culiseta subochrea, 305–306
Culicini tribus, 5 identification, 110, 134, 160
Culicinomyces, 418 morphology, pupae, 85
Culicinomyces clavisporus, 418 Culisetini tribus, 5
Culiciomyia subgenus, 5 Cyclops, 411, 412, 423
Culicoides Cymatia coleoptrata, 412
medical importance, 38 Cynolebias bellottii, 408
Culicomorpha systematics, 3, 4 Cyprinodontidae, 408
Culiseta alaskaensis, 298–300 Cyprinus carpio, 408, 423
identification, 110, 132–134, 160
Culiseta alaskaensis indica, 299
Culiseta annulata, 300–302 D
egg-laying behaviour, 167–168 Dahliana echinus. See Ochlerotatus echinus
identification, 109, 110, 134, 137, 159, 160, 167 Dahliana geniculata. See Ochlerotatus
morphology, pupae, 85 geniculatus
Culiseta bergrothi, 302–303 Dahliana genus, 6
identification, 109, 110, 132, 160 Dahliana gilcolladoi.
Culiseta dyary, 296 See Ochlerotatus gilcolladoi
Culiseta fumipennis, 291–292 Danielsia genus, 6
identification, 109, 114, 133, 161 Daphnia magna, 423, 426, 468
morphology, larvae, 83 Davismyia subgenus, 5
Culiseta genus Decamyia subgenus, 5
biology Deinocerites genus, 5, 64
egg-laying behaviour, 10 medical importance, 33
hibernation, 24 Deinocerites subgenus, 5
control, 436, 469 Delichon urbica, 409, 410
identification, 91, 108–110, 115, 132–134, 136, 159–162 Dendromyia subgenus, 5
medical importance, 33, 38, 39 Dendroskusea genus, 6
morphology, 69, 71–73, 79, 82, 83 Dengue virus, 31, 34–36, 203,
research, egg sampling, 45 486, 487
Culiseta glaphyroptera, 303–305 Deuteromycetes, 416
identification, 108–110, 115, 133, 160 Dipetalonema, 40
Culiseta impatiens, 464 Diceromyia furcifer. See Aedes furcifer
Culiseta incidens, 387 Diceromyia genus, 6, 317
Taxonomic Index 571

Diceromyia subgenus, 6, 317 Georgecraigius fluviatilis.

Diceromyia taylori. See Aedes taylori See Ochlerotatus fluviatilis
Diptera Georgecraigius genus, 6, 369
biological control with, 409, 410, 414–416, 418, 422, 431, Georgecraigius subgenus, 6
457, 462 Geoskusea genus, 6
systematics, 3 Geoskusea subgenus, 6
Dirofilaria immitis, 40, 203, 279, 333, 394 Gerridae, 413
Dirofilaria repens, 40 Gerris, 411, 413, 478
Dixidae Gerris lacustris, 411, 413
morphology, 78, 87 Gilesia subgenus, 6
Dobrotworskyius genus, 6 Gilesius genus, 6
Dodecamyia subgenus, 5 Gobio gobio, 408
Dolichopodidae, 415 Grabhamia subgenus, 7
Downsiomyia genus, 6, 333 Guignotus pusillus, 411, 414, 423
Downsiomyia nivea. See Ochlerotatus niveus Gymnometopa genus, 6, 369
Dracaena, 9, 41, 203 Gymnometopa mediovittata.
Dugesia dorotocephala, 468 See Ochlerotatus
Dytiscidae, 413 mediovittatus
Dytiscus circumflexus, 413 Gymnometopa subgenus, 6
Dytiscus marginalis, 413 Gyrinidae, 414

E H
Eastern Equine Encephalomyelitis virus, 32 Haemagogus genus, 6, 34, 63, 67, 371,
Edwardsaedes genus, 6 372, 381–382
Edwardsaedes subgenus, 6 medical importance, vi, 34
Eichhornia crassipes, 332, 386 Haemagogus janthinomys,
Elpeytonius genus, 6 381–382
Empididae, 415 identification, 372
Empihals subgenus, 6 Haemagogus subgenus, 6
Entomophthora culicis, 418 Halaedes genus, 6
Entomophtorales, 416, 418 Halaedes subgenus, 6
Ephemeroptera, 73, 410, 422, 423, 457 Hantavirus, 37
Eptesicus, 410 Harbachius subgenus, 7
Eretmapodites genus, 6, 414 Heizmannia genus, 6
Etorleptiomyia subgenus, 5 Heizmannia subgenus, 6
Eucalyptus citriodora, 494, 495 Helochares obscurus, 414
Eumelanomyia subgenus, 5 Heteraspidion subgenus, 7
Exallomyia subgenus, 5 Heteroptera, 410–414, 422, 423
Heterorhabditis, 415
Himalaius genus, 6
F Hodgesia genus, 5, 83, 307
Ficalbia genus, 5 Hodgesiini tribus, 5
Ficalbiini tribus, 5 Hopkinsius genus, 6
Finlaya genus, 6 Hopkinsius subgenus, 6
Finlaya subgenus, 113, 205, 354 Horsfallius subgenus, 6
morphology, larvae, 79 Howardina genus, 6
Flaviviridae, 31, 34 Howardina subgenus, 6
Flavivirus, 31, 34, 208, 215 Huaedes genus, 6
Formicidae, 409 Huaedes subgenus, 6
Francisella tularensis, 208, 218, 227 Huangmyia subgenus, 7
Fredwardsius genus, 6, 188, 196–198 Hulecoeteomyia genus, 6
Fredwardsius subgenus, 6, 188, 196–198 Hulecoeteomyia japonica. See Ochlerotatus
Fredwardsius vittatus. See Aedes vittatus japonicus japonicus
Hyalella azteca, 468
Hydra, 411, 412, 423
G Hydrocorisa, 412
Galindomyia, 5, 64 Hydrometra stagnorum, 413
Gambusia affinis, 405, 406, 435 Hydrometridae, 413
Gasterosteus acyleatus, 408 Hydrophilidae, 414
Gastropoda, 409 Hydrophilus caraboides, 411, 414, 423
572 Taxonomic Index

Hydroporinae, 413 Limatus genus, 5, 71

Hydroporus palustris, 413, 423 Limnephilus, 414
Hygrotus inaequalis, 413, 423 Lispe, 415
Hyla arborea, 409 Lophoceraomyia subgenus, 5
Hyphydrus ovatus, 413 Lophopodomyia subgenus, 5, 164
Hystatamyia subgenus, 5 Lorrainea genus, 6
Lorrainea subgenus, 6
Luccophilus, 411, 414
I Lugenidium giganteum, 417, 418
Ilyocoris cimicoides, 412, 423 Luius genus, 6
Indusius genus, 6 Lutzia genus, 5, 83, 264, 307
Indusius subgenus, 6 Lutzia subgenus, 5
Ingramia subgenus, 5 morphology, larvae, 83
Inkoo virus, 37 Lymnaea (Galba) palustris, 423
Insulalutzia subgenus, 5 Lynchiella subgenus, 5
Intrudens Group, 209
Iridescent virus, 431
Isoaedes genus, 6 M
Isoaedes subgenus, 6 Macleaya genus, 6
Isopoda, 409 Macleaya subgenus, 6
Isostomyia genus, 5 Macropodus chinensis, 408
Macropodus opercularis, 408
Maillotia subgenus, 5, 265, 282
J Malaya genus
Jamestown Canyon virus, 37, 38 morphology, adult, 63, 67
Janthinosoma subgenus, 7, 395 Mansonella, 40
Japanese encephalitis virus, 34, 227, Mansonia africana, 317, 330
279, 333, 350 identification, 321, 322
Jarnellius genus, 6 Mansonia annulata, 333
Jihlienius genus, 6 Mansonia genus
Johnbelkinia genus, 5 biology, pupae, 17, 19
Juncus, 401 medical importance, 33, 39
Juppius subgenus, 6 Mansonia indiana, 333
Mansonia subgenus, 372
Mansonia titillans, 385–386
K identification, 372
Kenknightia genus, 6 Mansonia uniformis, 330–332, 333
Kenknightia subgenus, 6 identification, 321, 322, 339, 353
Kerteszia subgenus, 5, 164 medical importance, 32
Kimia genus, 5 Mansoniini tribus, 4, 5, 187
Kitzmilleria subgenus, 5 Mansonioides subgenus, 5, 330
Kompia genus, 6 Maorigoeldia genus, 5
Kompia subgenus, 6 Mastigomycotina, 416
Kyzylagach virus, 33 Mattinglyia subgenus, 6
Megacyclops viridus, 412
Melanoconion subgenus, 5
L Menolepis subgenus, 5
La Crosse Encephalitis virus, 37–38 Mermitbidae, 415
Lagenidium giganteum, 417, 418 Mesocyclops aspericornis, 412
Lasiosiphon subgenus, 5 Mesostoma ehrenbergii, 411
Lednice virus, 37, 39 Metalutzia subgenus, 5
Leicesteria subgenus, 6 Metarhizium, 418
Lepidokeneon subgenus, 6 Micraedes subgenus, 5
Lepiothauma subgenus, 5 Microculex subgenus, 5
Leptosomatomyia genus, 6 Microsporidia, 418, 419
Leptosomatomyia subgenus, 6 Mimomyia genus, 5
Lepus americanus, 39 morphology, larvae, 83
Leucaspius delineatus, 408 Mimomyia subgenus, 5
Levua genus, 6 Mochlonyx culiciformis, 414, 415
Levua subgenus, 6 Mochlonyx genus
Lewnielsenius genus, 6 larva morphology, 77–78
Taxonomic Index 573

Mollusca, 422, 423 See also Aedes/Ochlerotatus

Molpemyia genus, 6 Ochlerotatus albifasciatus, 369, 382–383
Molpemyia subgenus, 6 identification, 373
Mucidus genus, 6, 66 medical importance, 32
Mucidus subgenus, 6, 354 Ochlerotatus aloponotum, 228
Mukwaya subgenus, 7 Ochlerotatus alternans, 357–358
Murray Valley encephalitis virus, 364 identification, 354
Musca domestica, 415 Ochlerotatus annulipes, 209–211
Muscidae, 415 identification, 100, 114, 127, 128, 144, 151, 152
Myotis, 409 Ochlerotatus atlanticus, 387
Myxoma virus, 25, 218 Ochlerotatus bancroftianus, 351
Ochlerotatus behningi, 211–212
identification, 99, 124, 127, 128, 150
N Ochlerotatus beklemishevi, 229
Natrix natrix, 37 Ochlerotatus berlandi, 212–214
Naucoridae, 412–413 identification, 95, 96, 123, 141
Nematocera, 3, 63, 73, 421, 423 Ochlerotatus bicristatus, 257
Nematoda (Nematodes), 25, 39, 415–416, 442, 502 Ochlerotatus caballus, 317
Neobironella subgenus, 5, 163 Ochlerotatus campestris, 227
Neoculex subgenus, 5, 265, 272, 283–284 Ochlerotatus camptorhynchus, 360
Neomacleaya subgenus, 7 identification, 355
Neomelaniconion circumluteolum. Ochlerotatus canadensis canadensis, 387
See Aedes circumluteolus medical importance, 32
Neomelaniconion genus, 6 Ochlerotatus cantans, 214–215
Neomelaniconion subgenus, 6 biology
Neotheobaldia subgenus, 5 feeding, 23
Nepa cinerea, 413 hatching, 13, 14
Nepidae, 413 larvae, 18, 23
Nicaromyia subgenus, 5 control, 505
Nosema, 419 identification, 95, 98, 100, 126, 151, 152
Noterinae, 413 medical importance, 36, 38
Nothoskusea subgenus, 6 Ochlerotatus caspius, 216–218
Notonecta glauca, 413, 423, 478 biology, egg-laying behaviour, 11
Notonecta undulata, 413 control, 494
Notonecta unifasciata, 413 identification, 95, 96, 121–123, 137,
Notonectidae, 413 144–146
Nunezia subgenus, 5 morphology, larvae, 84
Nymphea, 401 Ochlerotatus Caspius Complex, 216
Nymphomyiidae, 3 Ochlerotatus cataphylla, 218–219
Nyssorhynchus subgenus, 5, 75, 164, 370 identification, 101, 103, 123–125, 143–145
morphology, larvae, 83
Ochlerotatus churchillensis, 219
O Ochlerotatus coluzzii, xi, 209, 223, 224
Ochlerotatus genus, ix, x, xii, 204–205, 333, 369 Ochlerotatus communis, 220–221, 333, 387
biology, 9 biology
dispersal and host-seeking behaviour, 21, 22 dispersal and host-seeking behaviour, 21
embryonic development, 13 hatching, 14
hatching, 13, 15, 16 identification, 104, 105, 118, 124, 125, 145, 146
hibernation, 24 medical importance, xxvii, 39
larvae, 17 Ochlerotatus Communis Complex, 219
oviposition, 11 Ochlerotatus cyprius, 221–222
control, 408, 412, 413, 423, 426, 428, 430, 436, identification, 98, 126, 127, 141
454, 456, 457, 468–470, 502 Ochlerotatus detritus, 223–224, 317
identification, 92, 95–106, 113, 118–128, 136,141–154, identification, 101, 102, 125, 127, 136, 145
318, 321, 339, 354, 372,373, 388, 389 Ochlerotatus Detritus Complex, 222
medical importance, 33, 34, 38–40 Ochlerotatus diantaeus, 224–226
morphology, 71, 72–76, 79, 82–84 identification, 104, 121, 122, 141
research Ochlerotatus dorsalis, 226–228, 333, 387
egg sampling, 44 control, 469
rearing, 52 identification, 96, 122, 123, 146
systematics, 4, 6, 7 systematic status, 218, 227–228
574 Taxonomic Index

Ochlerotatus eatoni, 206 Ochlerotatus provocans, 257

Ochlerotatus echinus, 205–206 Ochlerotatus pulcritarsis, 248–249
identification, 102, 120, 152, 153 identification, 95, 123, 152
Ochlerotatus euedes, 228–229 morphology, larvae, 79
identification, 100, 101, 128, 141, 149, 150 Ochlerotatus pullatus, 249–250
medical importance, 34 identification, 103, 104, 121, 146–148
Ochlerotatus excrucians, 229–231, 333 Ochlerotatus punctodes, 250–251
identification, 99, 128, 149–151 identification, 105, 124, 143, 144
systematics, 229, 231 morphology, larvae, 83
Ochlerotatus Excrucians Complex, 228 Ochlerotatus punctor, 251–253, 333, 387
Ochlerotatus fitchii, 333 identification, 103, 105, 124, 142–144
Ochlerotatus flavescens, 231–233 medical importance, xxvii, 38
identification, 98, 127, 151 Ochlerotatus quasirusticus, 258–259
medical importance, 38 identification, 102, 121, 143
Ochlerotatus fluviatilis, 369 Ochlerotatus refiki, 259–261
Ochlerotatus geniculatus, 206–208 identification, 102, 120, 121, 142, 143
identification, 91, 101, 102, 120, 142, 152, 153 Ochlerotatus riparius, 253–254
morphology, larvae, 79 identification, 99, 100, 114, 126, 141, 148, 149
systematics, 206 Ochlerotatus rusticus, 261–263
Ochlerotatus hexodontus, 233–234, 333, 387 biology
identification, 105, 106, 124, 141, 144 dispersal and host-seeking behaviour, 21, 22
medical importance, xxvii hatching, 13, 14, 24
Ochlerotatus hungaricus, 234–236 hibernation, 24
identification, 106, 122, 147, 148 larvae, 19, 24
Ochlerotatus impiger, 236–237, 333, 387 identification, 101, 102, 120, 142, 143
identification, 103, 122–124, 147 Ochlerotatus sagax, 362–363
Ochlerotatus increpitus, 387 identification, 354, 355
Ochlerotatus infirmatus Ochlerotatus scapularis, 383–384
medical importance, 38 identification, 373
Ochlerotatus intrudens, 237–238 Ochlerotatus sierrensis, 387
identification, 104, 120–122, 144, 145 Ochlerotatus sollicitans, 369, 391–392
Ochlerotatus japonicus japonicus, xxix, 9, 46 identification, 389, 390
medical importance, 41, 42 medical importance, 32
Ochlerotatus krymmontanus, xi, 257 Ochlerotatus sticticus, 255–256, 333, 387
Ochlerotatus lepidonotus, 257–258 identification, 105, 106, 125, 126,
identification, 102, 121, 143 146, 148
Ochlerotatus leucomelas, 238–240 medical importance, 38
identification, 103, 124, 125, 146 Ochlerotatus stimulans, 387, 494
Ochlerotatus mariae, 240–242 Ochlerotatus subdiversus, 263–264
identification, 96, 123, 148, 149 identification, 102, 121, 143
morphology, larvae, 82 Ochlerotatus subgenus, 4, 6, 17, 45,
Ochlerotatus Mariae Complex, 240 208–209, 354
Ochlerotatus mediovittatus, 369 Ochlerotatus surcoufi, 209, 228, 231
Ochlerotatus melanimon, 227, 387, 470 identification, 101, 128, 150, 151
Ochlerotatus mercurator, 242–243 Ochlerotatus taeniorhynchus, 393–394
identification, 99, 113, 126, 127, 148, 150, 151 identification, 390
Ochlerotatus nevadensis, 219 medical importance, 33
Ochlerotatus nigrinus, 243–244 Ochlerotatus tahoensis, 219
identification, 106, 126, 147, 149 medical importance, 38
Ochlerotatus nigripes, 245–246, 333, 387 Ochlerotatus theobaldi, 363–364
identification, 103, 118, 120, 123, 124, 143 identification, 355
Ochlerotatus nigromaculis, 387 Ochlerotatus togoi, 333
Ochlerotatus niveus, 333 Ochlerotatus trichurus, 494
Ochlerotatus normanensis, 360–362 Ochlerotatus triseriatus, 387
identification, 355, 356 medical importance, 38
Ochlerotatus notoscriptus, 351, 358–359 blood meal identification, 55
identification, 354 Ochlerotatus trivittatus, 387
control, 435 medical importance, 37, 38, 278
Ochlerotatus phoeniciae, 240 Ochlerotatus vigilax, 333, 364–365
Ochlerotatus pionips, 246–248, 333 biology, 9
identification, 105, 106, 125, 146, 147 identification, 354–356
Taxonomic Index 575

medical importance, 32 Plasmodium vivax, 25, 28–30, 180, 378

control, 437 Plea leachi, 413, 423
Ochlerotatus vittiger, 351 Pleidae, 413
Ochlerotatus zammitii, 242 Plodia interpunctella, 424
identification, 123, 149 Podura aquatica, 457
Ockelbo virus, 33, 277, 280, 296 Poecilia reticulata, 406, 407
Oculeomyia subgenus, 5 Polylepidomyia subgenus, 5
Odonata, 412, 422, 423, 457 Polyleptiomyia genus, 7
Onchocercidae, 40 Potamogeton, 327
Onirion, 5 Prosopolepis subgenus, 5
O’Nyong-Nyong virus, 33 Protoculex subgenus, 6
Opifex, 6 Protomacleaya subgenus, 6
Orechromis hornorum, 408 Pseudarmigeres genus, 7
Orechromis mossambia, 408 Pseudarmigeres subgenus, 6
Orthopodomyia genus, 310 Pseudoficalbia subgenus, 5
biology, egg-laying behaviour, 9 Pseudoskusea subgenus, 6
embryonic development, 13 Psorophora columbiae, 394–395
Orthopodomyia pulcripalpis, 310–312 identification, 388
biology, 9, 24 control, 406, 470
habitat, 9 Psorophora ferox, 369, 395–396
hibernation, 24 identification, 371, 388
identification, 92, 115, 136 Psorophora genus
morphology, larvae, 82, 83 biology, larvae, 18
Orthopodomyiini tribus, 5 control, 412, 414, 469, 470
Oryzias latipes, 408 medical importance, vi, 33, 39
Osteichthyes, 406–408 morphology, 69, 71, 75, 76
Psorophora subgenus, 7
Psychodidae, 421–423
P Ptychopteromorpha, 3
Paecilomyces, 418 Punctor Group, 209
Paraedes genus, 6
Paraedes subgenus, 6
Parathelohania, 419 R
Pardomyia subgenus, 6 Rachionotomyia subgenus, 5
Passeriformes, 33, 36, 202 Rachisoura subgenus, 5
Patmarksia genus, 6 Rampamyia genus, 7
Pelobates fuscus, 409 Rampamyia notoscripta.
Petermattinglyius genus, 6 See Ochlerotatus notoscriptus
Petermattinglyius subgenus, 6 Rana, 288, 409, 423
Peytonulus subgenus, 5 Ranatra linearis, 413
Phagomyia genus, 7 Rhantus, 413, 423
Phenacomyia subgenus, 5 Rhinoskusea genus, 7
Phlebovirus, 31, 37 Rhinoskusea subgenus, 6
Pholeomyia subgenus, 6 Rhynchotaenia subgenus, 5, 307
Phoniomyia subgenus, 5 Romanomermis, 415, 416
Phragmites, 12, 166, 262, 309, Ross River virus, 31, 32, 332, 351, 359,
314, 401 360, 362, 364–366, 466
Phryganea, 414 Rotatoria, 422, 423
Phytotelmatomyia subgenus, 5 Runchomyia genus, 5
Piona nodata, 412 Runchomyia subgenus, 5
Pisces, 422, 423 Rusticoidus subgenus, 6, 83, 205, 256–257
Pistia, 327, 386 Rutilus rutilus, 408
Pistia stratiotes, 330, 332, 386
Planipennia, 410
Plasmodium, 25–29, 242, 343, 379, 418, 442, 486, 487, 500. S
See also Malaria (subject index) Sabethes genus, 5, 63, 67, 84
Plasmodium falciparum, 25, 28–30, 166, 180, Sabethes subgenus, 5
486, 487, 492, 495 Sabethini tribus, 5
Plasmodium malariae, 25, 28, 30 Sabethinus subgenus, 5
Plasmodium ovale, 25, 28, 30 Sabethoides subgenus, 5
576 Taxonomic Index

Saccharopolyspora spinosa, 419 Tipulomorpha, 3

Sagittaria, 401 Tipuloidea systematics, 3
Sallumia genus, 7 Togaviridae (Alphavirus), 31–34
Scardinus erythrophthalamus, 408 Tolypocladium, 418
Sciaridae, 422, 423 Topomyia genus, 5
Scutomyia genus, 7 Topomyia subgenus, 5
Scutomyia subgenus, 6 Toxorhynchites genus, 5, 18, 65, 66, 69,
Semliki Forest virus, 33–34 76, 83,315, 414
Shannoniana, 5 Toxorhynchites subgenus, 5
Sigara striata, 412, 423 Toxorhynchitinae subfamily, 3, 4
Simuliidae, 3, 7, 423, 429 Toxorhynchitini tribus, 5
Simulium damnosum, 423, 424 Tricholeptomyia subgenus, 5
Simulium vittatum, 431 Trichoprosopon, 5
Sindbis virus, 31, 33, 282, 317, 330, 333, 438 Trichoptera, 410, 414, 422, 423
Sirivanakarnius subgenus, 5 Triops cancriformis, 412, 468
Skusea genus, 7 Triops longicaudatus, 412, 468
Skusea subgenus, 6 Tripteroides genus, 5
Snowshoe Hare virus, 37, 38 Tripteroides subgenus, 5
Spercheidae, 414 Triturus, 408, 409, 423
Spilonympha subgenus, 5 Trivittatus virus, 37, 38
Stegomyia aegypti. See Aedes aegypti Tubifera, 423
Stegomyia africana. See Aedes africanus Turbellaria, 411, 422, 423
Stegomyia albopicta. See Aedes albopictus Typha, 230, 294, 308, 309, 374, 401
Stegomyia cooki. See Aedes cooki
Stegomyia cretina. See Aedes cretinus
Stegomyia fasciata. See Aedes aegypti U
Stegomyia genus, 7 Udaya genus, 7
Stegomyia hebridea. See Aedes hebrideus Uranotaenia genus, 5, 312–313
Stegomyia hensilli. See Aedes hensilli biology
Stegomyia luteocephala. See Aedes luteocephalus egg-laying behaviour, 10
Stegomyia opok. See Aedes opok embryonic development, 13
Stegomyia polynesiensis. See Aedes polynesiensis hibernation, 24
Stegomyia rotumae. See Aedes rotumae research, egg sampling, 43
Stegomyia scutellaris. See Aedes scutellaris Uranotaenia subgenus, 5
Stegomyia subgenus, 6, 7, 188, 194, 196, 198 Uranotaenia unguiculata, 313–314
identification, 321, 339, 353, 372, 389 identification, 91, 114, 115, 136, 137
morphology, 76, 82 morphology, 80, 82, 83
medical importance, 31, 32, 35 Uranotaeniini tribus, 5
Steinernema, 415 Urodela, 408
Steinernematidae, 415
Stethomyia subgenus, 5, 164
St. Louis encephalitis virus, 31, 34, 37, 227, 279, 385, V
400, 463 Vansomerenis genus, 7
Suaymyia subgenus, 5 Vavraia, 419
Syrphidae, 409, 423 Venezuelan Equine Encephalomyelitis virus, 32–33,
386, 394
Verrallina funerea, 351
T Verrallina genus, 7
Tahyna virus, 37, 38, 196, 211, 215, 218, 267, 302 Verrallina subgenus, 7
Tanakaius genus, 7 Verticillium, 418
Tanakaius togoi. See Ochlerotatus togoi
Tanichthys albonubes, 408
Tewarius genus, 7 W
Thaumaleidae systematics, 3 Western Equine Encephalomyelitis virus, 32, 196, 227, 279,
Theobaldia genus, 288 369, 383, 397, 400
Theomyia subgenus, 5 West Nile virus, 31, 34, 36–37, 41, 218, 267, 275,
Tilapia zilli, 408 277–279, 282, 310, 317, 328, 330, 333,
Tinca tinca, 408 385, 387, 397, 398, 400, 401, 421, 428,
Tinolestes subgenus, 5 438, 454, 463, 472, 473, 481
Tipulidae, 63, 409, 422, 423 Whataroa virus, 33
Taxonomic Index 577

Wolbachia, 485, 488, 500 Y

Woodius subgenus, 6 Yamada subgenus, 6
Wuchereria bancrofti, 39, 332, 333, 344, 346, Yellow Fever virus, 31, 34, 201, 317
347, 357, 366, 473
Wyeomyia genus, 5, 67, 84
Wyeomyia subgenus, 5 Z
Zavortinkius genus, 7
Zavortinkius subgenus, 6
X Zeugnomyia genus, 7
Xenopelopia, 423 Zinzala subgenus, 5
Xyele subgenus, 7 Zoromorphus subgenus, 7