00Integrated pest prelim.

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Integrated Pest Management

Potential, Constraints and Challenges

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Integrated Pest Management

Potential, Constraints and Challenges

Edited by

Opender Koul

Insect Biopesticide Research Centre

Jalandhar, India

G.S. Dhaliwal

Department of Entomology
Punjab Agricultural University
Ludhiana, India

and

G.W. Cuperus

Department of Entomology and Plant Pathology

Oklahoma State University, Stillwater, Oklahoma, USA

CABI Publishing
00Integrated pest prelim.QXD 14/4/04 2:24 pm Page iv

CABI Publishing is a division of CAB International

CABI Publishing CABI Publishing
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A catalogue record for this book is available from the British Library,
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Library of Congress Cataloging-in-Publication Data

Integrated pest management: potential, constraints, and challenges/
edited by Opender Koul, G.S. Dhaliwal, G.W. Cuperus.
p. cm.
Includes bibliograpical references and index.
ISBN 0-85199-686-8 (alk. paper)
1. Pests--Integrated control. I. Koul, Opender. II. Dhaliwal, G.S.
III Cuperus, Gerrit W. IV. Title.
SB950.I4577 2004
632’.9--dc22

2003015419

ISBN 0 85199 686 8

Typeset by Columns Design Ltd, Reading

Printed and bound in the UK by Biddles, King’s Lynn
00Integrated pest prelim.QXD 14/4/04 2:24 pm Page v

Contents

About the Editors vii

Contributors ix
Preface xi

1. Integrated Pest Management: Retrospect and Prospect 1

G.S. Dhaliwal, Opender Koul and Ramesh Arora

2. Cultural Practices: Springboard to IPM 21

Waheed I. Bajwa and Marcos Kogan

3. The Relevance of Modelling in Successful Implementation of IPM 39

David E. Legg

4. Manipulation of Tritrophic Interactions for IPM 55

Robert H.J. Verkerk

5. Behaviour-modifying Chemicals: Prospects and Constraints in IPM 73

Larry J. Gut , Lukasz L. Stelinski, Donald R. Thomson and James R. Miller

6. Transgenic Insecticidal Cultivars in IPM: Challenges and Opportunities 123

Julio S. Bernal, Jarrad Prasifka, M. Sétamou and K.M. Heinz

7. Plant Resistance Against Pests: Issues and Strategies 147

C. Michael Smith

8. The Pesticide Paradox in IPM: Risk–Benefit Analysis 169

Paul Guillebeau

9. Manipulation of Host Finding and Acceptance Behaviours in Insects: 185

Importance to IPM
Richard S. Cowles

10. IPM in Forestry: Potential and Challenges 205

Imre S. Otvos

v
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vi Contents

11. Consumer Response to IPM: Potential and Challenges 255

Craig S. Hollingsworth and William M. Coli
12. The Essential Role of IPM in Promoting Sustainability of Agricultural 265
Production Systems for Future Generations
G.W. Cuperus, R.C. Berberet and R.T. Noyes
13. Opportunities and Challenges for IPM in Developing Countries 281
David Bergvinson
Index 313
00Integrated pest prelim.QXD 14/4/04 2:24 pm Page vii

About the Editors

Opender Koul, Fellow of the National Academy of Agricultural Sciences and the Indian
Academy of Entomology, is an insect toxicologist/physiologist/chemical ecologist and cur-
rently the Director of the Insect Biopesticide Research Centre, Jalandhar, India. After obtain-
ing his PhD in 1975 he joined the Regional Research Laboratory (CSIR), Jammu and then
became Senior Group Leader of Entomology at Malti-Chem Research Centre, Vadodara,
India (1980–1988). He has been a visiting scientist at the University of Kanazawa, Japan
(1985–1986), the University of British Columbia, Canada (1988–1992), and the Institute of
Plant Protection, Poznan, Poland (2001). His extensive research experience concerns
insect–plant interactions, spanning toxicological, physiological and agricultural aspects.
Honoured with an Indian National Science Academy (INSA) medal and the Kothari Scientific
Research Institute award, he has authored over 140 research papers and articles and is the
author/editor of the books Insecticides of Natural Origin, Phytochemical Biopesticides, Microbial
Biopesticides and Predators and Parasitoids. He has also been an informal consultant to the
Board of Science and Technology for International Development (BOSTID), the National
Research Council (NRC) of the USA and at the International Centre for Insect Physiology and
Ecology (ICIPE), Nairobi.

G.S. Dhaliwal, a Fellow of the National Environmental Science Academy (NESA), Society of
Plant Protection Sciences and Society of Pesticide Sciences, India, is Professor of Ecology in the
Department of Entomology at the Punjab Agricultural University, Ludhiana, India. Having
completed his PhD in Entomology at the Indian Agricultural Research Institute (IARI), New
Delhi, in 1972, he was awarded the Gurprasad Pradhan Gold Medal and became a postdoc-
toral fellow at the International Rice Research Institute, Manila, for 2 years. He has
authored/edited more than 30 books on different aspects of pest management and the envi-
ronment. Honoured with the Best Scientist Award of NESA, he is the founding President of
the Indian Society for the Advancement of Insect Science and the Society of Biopesticide
Sciences, India, and President of the Indian Ecological Society as well as Vice-President of the
Indian Society of Allelopathy and the Society of Pesticide Science, India. He is a member of the
World Food Prize Nominating Academy, The World Food Prize Foundation, Des Moines,
Iowa.

Gerrit W. Cuperus, was a Regent’s Professor and Integrated Pest Management Coordinator
at Oklahoma State University for over 20 years. Dr Cuperus obtained his PhD in 1982, joined

vii
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viii About the Editors

the Department of Entomology at Oklahoma State University and has since been involved in
national IPM programmes of the USA aiming at an interdisciplinary focus to solve manage-
ment issues. Dr Cuperus has chaired and served in different capacities in various national
committees on food safety and pest management. He has made specific contributions in
extension/research and has won distinguished service awards from the US Department of
Agriculture (USDA). His research efforts, focused on stored-product pest management, have
helped to build the Stored Product Research and Education Center (SPREC) at Oklahoma
State University. He has authored over 60 research papers and articles and is an editor of
Successful Implementation of IPM for Agriculture Crops (1992) and Stored Product Management
(1995).
00Integrated pest prelim.QXD 14/4/04 2:24 pm Page ix

Contributors

Ramesh Arora, Department of Entomology, Punjab Agricultural University, Ludhiana 141 004,
India
Waheed I. Bajwa, Department of Entomology and Integrated Plant Protection Center, Oregon State
University, Corvallis, OR 97331, USA
R.C. Berberet, Department of Entomology and Plant Pathology, Oklahoma State University,
Stillwater, OK 74078, USA
David Bergvinson, International Maize and Wheat Improvement Center (CIMMYT), El Batán,
Mexico CP 56130, Mexico
Julio S. Bernal, Department of Entomology, Biological Control Laboratory, Texas A&M University,
College Station, TX 77843–2475, USA
William M. Coli, Department of Entomology, University of Massachusetts, Amherst, MA 01003,
USA
Richard S. Cowles, Connecticut Agricultural Experiment Station, Valley Laboratory, PO Box 248,
Windsor, CT 06095, USA
G.W. Cuperus, Department of Entomology and Plant Pathology, Oklahoma State University,
Stillwater, OK 74078, USA
G.S. Dhaliwal, Department of Entomology, Punjab Agricultural University, Ludhiana 141 004,
India
Paul Guillebeau, Department of Entomology, University of Georgia Cooperative Extension Service,
Athens, GA 30602, USA
Larry J. Gut, Department of Entomology, Michigan State University, East Lansing, MI 48824, USA
K.M. Heinz, Department of Entomology, Biological Control Laboratory, Texas A&M University,
College Station, TX 77843–2475, USA
Craig S. Hollingsworth, Department of Entomology, University of Massachusetts, Amherst, MA
01003, USA
Marcos Kogan, Department of Entomology and Integrated Plant Protection Center, Oregon State
University, Corvallis, OR 97331, USA
Opender Koul, Insect Biopesticide Research Centre, 30 Parkash Nagar, Jalandhar 144 003, India
David E. Legg, Department of Renewable Resources, University of Wyoming, Laramie, WY 82071,
USA
James R. Miller, Department of Entomology, Michigan State University, East Lansing, MI 48824,
USA

ix
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x Contributors

R.T. Noyes, Department of Biosystems and Agricultural Engineering, Oklahoma State University,
Stillwater, OK 74078, USA
Imre S. Otvos, Natural Resources Canada, Canadian Forest Service, Pacific Forestry Centre, 506
West Burnside Road, Victoria, BC, V8Z 1M5, Canada
Jarrad Prasifka, Department of Entomology, Biological Control Laboratory, Texas A&M University,
College Station, TX 77843–2475, USA
M. Sétamou, Department of Entomology, Biological Control Laboratory, Texas A&M University,
College Station, TX 77843–2475, USA
C. Michael Smith, Department of Entomology, Kansas State University, Manhattan, KS
66506–4004, USA
Lukasz L. Stelinski, Department of Entomology, Michigan State University, East Lansing, MI
48824, USA
Donald R. Thomson, DJS Consulting Services, LLC, 3015 SW 109 Street, Seattle, WA 98146, USA
Robert H.J. Verkerk, Department of Biological Sciences, Imperial College London, Silwood Park,
Ascot, Berkshire SL5 7PY, UK
00Integrated pest prelim.QXD 14/4/04 2:24 pm Page xi

Preface

The concept of integrated pest management (IPM) excelled during the mid-1970s when envi-
ronmental, health and production problems associated with dependence on large-scale use of
synthetic organic pesticides came into the limelight. Following some large-scale successes
with IPM based on biological control systems, improved profitability and pesticide reduction
IPM has moved from a peripheral to the central stage of pest suppression. Today it is consid-
ered to be the springboard to sustainable crop management. Over the years more than 70 def-
initions of IPM (including related terms) have been proposed. Although some new terms
such as ‘biointensive IPM’ and ‘ecologically based pest management’ have been suggested,
the essence of all the definitions is the promotion of compatibility of management tactics to
ensure economic and ecological sustainability. There have been many success stories, particu-
larly in the developed world, and many bottlenecks, more so in developing countries. The
availability of modern tools and transgenic crop-protection technology has opened new
opportunities and challenges. All these issues form the focus of the book, where they have
been discussed by world authorities in their respective areas of specialization.
With the growing interest in IPM, opportunities and challenges have come to the fore and
it is necessary to understand the potential in such programmes. To begin with, the book out-
lines the historical perspective of IPM in the first chapter and sets the stage for the discussion
on potential, constraints and challenges involved in IPM. It covers the era of traditional
approaches, from ancient times to 1938, the era of pesticides, from 1939 to 1975 and the cur-
rent era of IPM, from 1976 onward. The significance of the ‘farmer first’ concept in IPM
development and implementation is stressed. The potential of different management tactics
in future IPM programmes has been discussed in various chapters, such as cultural practices,
the relevance of modelling in the successful implementation of IPM, the manipulation of
tritrophic interactions for the systems and the role of behaviour-modifying chemicals.
There are several challenges and opportunities for transgenic insecticidal cultivars, which
have been discussed in Chapter 6, and the role of Bacillus thuringiensis (Bt) insect-resistant
transgenes, molecular markers, cloning and sequencing plant resistance genes in host-plant
resistance to pests has been highlighted in Chapter 7. The risk–benefit analysis of different
groups of pesticides (i.e. insecticides, fungicides and weedicides) with respect to biological
controls is an important component of IPM implementation. An effort has been made to
make pesticides more compatible with IPM by improving pesticide selectivity via manipulat-
ing various spray parameters such as placement, timing and formulations, or through official
policies and regulations and these are comprehensively discussed.
xi
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xii Preface

Chapter 9 focuses on the manipulation of host finding and acceptance behaviours to shift
highly mobile and discriminating insect populations to plants or traps outside the valued
crops. Potential tools for implementing the ‘push–pull strategy’ have been explained and sev-
eral models have been proposed to demonstrate the application of behavioural manipulation
in trap crops. The consumer response to IPM has been discussed in Chapter 11 and the vari-
ous constraints and bottlenecks have been highlighted.
The forest ecosystem is much more complex, resilient and longer term than that of agricul-
ture, and the threshold level of damage caused by insects or pathogens is much higher in
forestry than what most consumers are willing to accept on or in their fruits or vegetables.
Therefore, IPM has an important role to play in silviculture pest management and this has
been discussed comprehensively in Chapter 10.
The role of IPM in sustaining productivity in future has been discussed in Chapter 12. The
contribution of IPM in meeting economic, environmental and social mandates has been elab-
orated. The role of diagnostic tools, weather forecasting, transgenic plants, biological control
and chemical pesticides in future IPM programmes has been highlighted and the strategies to
meet the challenges of pest adaptation have been outlined. The need for improved informa-
tion transfer among all groups involved in the development, implementation and application
of IPM has been stressed. Finally, it is essential to know the status of IPM in developed versus
developing countries. Therefore, the potentials and the constraints between the two worlds
have been compared extensively in the last chapter of this book.
We received a tremendous response and support from all the authors for preparing their
chapters in tune with the theme of the book, for which we express our gratitude to them. We
are also thankful to Tim Hardwick at CABI Publishing for his cooperation and help at vari-
ous stages in the preparation of this volume. Through this IPM book we also want to pay
homage to Prof. Bill Brown, who could not complete his chapter for this volume due to his
untimely demise in January 2003. Prof. Brown, worked in Nigeria, Thailand, South Korea and
Bolivia after becoming a Professor of Plant Pathology and Cooperative Extension IPM
Coordinator at Colorado State University. He had a passion for teaching plant pathology and
the philosophy of IPM.
We hope the book will prove useful to all those interested in promoting the cause of IPM
in formal and informal applications in both developed and developing countries, so that sus-
tainability in the agricultural system and environmental protection for future generations is
achieved.
Opender Koul
G.S. Dhaliwal
Gerrit W. Cuperus
01IntpestManCh1.QXD 14/4/04 2:24 pm Page 1

1 Integrated Pest Management: Retrospect

and Prospect

G.S. Dhaliwal,1 Opender Koul2 and Ramesh Arora1

1Department of Entomology, Punjab Agricultural University, Ludhiana 141 004, India;
2Insect Biopesticide Research Centre, Jalandhar 144 003, India
E-mail: [email protected]; [email protected]

Introduction stantially slower than the average popula-

tion growth rate of 1.6% in the developing
In the history of the world, no century can world (Hinrichsen and Robey, 2000). Since
match the population growth of the one that humans started practising agriculture about
has just come to a close. We entered the 20th 10,000 years ago, the increased need for food
century with fewer than 2 billion people and that resulted from increasing population or
left it with more than 6 billion. At the current rising living standards was met by bringing
pace, when the population increases by a greater area of land under cultivation.
about 78 million per year, the global popula- However, during the last century, larger
tion is projected to rise to over 8 billion by needs for food were mostly met by increas-
2025 (Hinrichsen and Robey, 2000). Thus, the ing productivity per unit of land. This trend
population may grow even more in the 21st is likely to continue as the populations
century, but in a very different way. The new increase and the land is required for pur-
century’s growth will occur almost exclu- poses other than agriculture (FAO, 2001).
sively in the developing countries – among Food production per unit of land is lim-
people with limited financial resources. The ited by many factors, including fertilizer,
developed countries, which almost doubled water, genetic potential of the crop and the
their population in the 20th century, will organisms that feed on or compete with food
grow slowly or not at all. Over half of the plants. These organisms that interfere signifi-
world population growth will occur in Asia cantly with the productivity or quality of
and one-third will be in Africa. The world plants considered useful for humans are
farmers will thus need to produce enough called pests. Broadly speaking, a pest is any
food for the expanding population (Dhaliwal organism that is in competition with humans
and Arora, 2001). for some resource. In agriculture, pests occur
The future of world food supply is closely in many groups of organisms, including
linked with the pattern of population plants, arthropods (insects, mites), fungi,
growth. In many countries over the past two bacteria, nematodes, viruses, viroids,
decades, growth in food supply has lagged mycoplasma-like organisms, rodents, birds
behind population growth. Worldwide, the and other vertebrates. Food plants of the
grain harvest increased by 1% annually world are damaged by 10,000 species of
between 1990 and 1997, a rate of growth sub- insects, 30,000 species of weeds, 100,000 dis-

© CAB International 2004. Integrated Pest Management: Potential, Constraints and Challenges
(eds O. Koul, G.S. Dhaliwal and G.W. Cuperus) 1
01IntpestManCh1.QXD 14/4/04 2:24 pm Page 2

2 G.S. Dhaliwal et al.

eases (caused by fungi, viruses, bacteria and damaging insects/insect-infested plants, etc.,
other microorganisms) and 1000 species of developed by farmers through experience
nematodes (Hall, 1995). were among the oldest methods developed
The global losses due to various categories by humans to minimize the damage caused
of pests vary with the crop, the geographical by insect pests (Smith et al., 1976). These
location and the weather. Total yield losses were followed by the use of plant products
from different pests of all crops have been from neem, chrysanthemum, rotenone,
estimated to be US$500 billion worldwide. tobacco and several other lesser-known
Despite the plant-protection measures plants in different parts of the world. The
adopted to protect the principal crops, 42.1% Chinese were probably the pioneers in the
of attainable production is lost as result of use of botanical pesticides as well as biologi-
attack by pests. However, if no control mea- cal control methods for the management of
sures were used to protect crops, the figure insect pests of stored grains and field crops
would be 69.8%. Animal pests account for (Dhaliwal and Arora, 1994a).
15.6% loss of production, pathogens 13.3% However, systematized work on many
and weeds 13.2% (Oerke et al., 1994). important tactics of pest control, including the
use of resistant varieties, biological control
agents and botanical and inorganic insecti-
Evolution of Management Tactics cides, was done in the USA from the end of
the 18th to the end of the 19th century.
During ancient times, humans had to live Remarkable success was achieved in the man-
with and tolerate the ravages of crop pests, agement of grape phylloxera, caused by
but they gradually learned to improve their Viteus vitifoliae (Fitch), by the grafting of
condition through trial-and-error experi- European grapevine scions to resistant North
ences. Over the centuries, farmers developed American rootstocks during the 1880s. At
a number of mechanical, cultural, physical around the same time, cottony cushion scale,
and biological control measures to minimize Icerya purchasi Maskell, which was causing
the damage caused by phytophagous insects. havoc in the citrus industry in California,
Synthetic organic insecticides developed USA, was successfully controlled by release of
during the mid-20th century provided spec- the vedalia beetle, Rodolia cardinalis (Mulsant),
tacular control of these pests and resulted in imported from Australia (DeBach, 1964).
the abandonment of traditional pest-control A number of synthetic inorganic insecti-
practices. Thus, the evolution of the concept cides containing arsenic, mercury, tin and
of pest management spans a period of more copper were also developed towards the end
than a century (Table 1.1). Many components of the 19th and the beginning of the 20th cen-
of pest management were developed in the tury. With the development of these insecti-
late 19th and early 20th centuries. Rapidly cides, the focus of research in pest control
developing technologies and changing soci- slowly shifted from ecological and cultural
etal values had their impact on pest-control control to chemical control, even before the
tactics also. The history of agricultural pest development of synthetic organic insecti-
control thus has three distinct phases, cides (Perkins, 1980).
namely, the era of traditional approaches, the
era of pesticides and the era of integrated
pest management (IPM) (Metcalf, 1980; Era of pesticides (1939–1975)
Dhaliwal et al., 1998).
The synthetic inorganic insecticides were
broad-spectrum biocides and were highly
Era of traditional approaches (ancient–1938) toxic to all living organisms. These were fol-
lowed in due course by the synthetic organic
Cultural and mechanical practices, such as insecticides, such as alkyl thiocyanates,
crop rotation, field sanitation, deep plough- lethane, etc. The era of pesticides, however,
ing, flooding, collection and destruction of began with the discovery of the insecticidal
01IntpestManCh1.QXD 14/4/04 2:24 pm Page 3

IPM: Retrospect and Prospect 3

Table 1.1. Landmarks in the history of agricultural pest management (modified after Dhaliwal et al.,
1998).

Period Landmark(s)

Ancient The Chinese used wood-ash for the control of insect pests in enclosed spaces and botanical
insecticides for seed treatment. They also used ants for biological control of stored grain as
well as foliage-feeding insects. In India, neem leaves were placed in grain bins to keep away
troublesome pests. In the Middle and Near East, powder of chrysanthemum flowers was used
as an insecticide
1762 The myna (a bird) from India was imported for the control of locusts in Mauritius
1782 ‘Underhill’ variety of wheat reported resistant to Hessian fly in the USA
1831 ‘Winter Majetin’ variety of apple reported resistant to woolly apple in the USA
1855 A. Fitch reported the role of ladybird beetles, green lacewings and other predacious insects in
the control of insect pests of crops
1858 Pyrethrum first used for insect control in the USA
1889 Biological control of cottony cushion scale on citrus in the USA by use of the vedalia beetle
imported from Australia
1890 Control of grape phylloxera in Europe by grafting of European grapevine scions to resistant
North American rootstocks
1923 Multiple-component suppression techniques involving the use of resistant varieties, sanitation
practices and need-based application of insecticides developed for the control of boll-weevil in
the USA
1939 ● Insecticidal properties of DDT reported by Paul Muller in Switzerland
● Bacillus thuringiensis Berliner first used as a microbial insecticide
1941 Insecticidal activity of hexachlorocyclohexane (HCH) discovered in France
1946 Parathion, the first organophosphatic insecticide developed
1948 ‘Doom’ based on Bacillus popilliae Dutky and Baciilus lentimorbus registered in the USA for the
control of Japanese beetle larvae on turf
1951 ● R.H. Painter published his classic book Insect Resistance in Crop Plants
● Introduction of first carbamate insecticide, isolan
1959 ● Concept of integrated control involving integration of chemical and biological control
introduced
● Concept of economic injury level and economic threshold developed by V.M. Stern and
co-workers
1962 Publication of the book Silent Spring, by Rachel Carson, which dramatized the impact of the
misuse and overuse of pesticides on the environment
1964 Publication of the book Biological Control of Insect Pests and Weeds, by Paul DeBach, which
established biological control as a separate discipline in entomology
1975 ● Elcar (Helicoverpa nucleopolyhedrovirus (NPV)) registered for the control of boll-worm and
tobacco budworm on cotton
● First insect growth regulator (Methoprene) registered for commercial use in USA
● Publication of the book Introduction to Insect Pest Management by R.L. Metcalf and W.H.
Luckmann, which was the first comprehensive treatise on IPM and established the concept
on a firm footing
1980 The interest in botanical pesticides revived and the First International Conference on Neem
was held at Rottach-Egern, Germany
1987 Development of first transgenic plant, reported by M. Vaeck and co-workers of Belgian biotech-
nology company, Plant Genetic System, by transferring B. thuringiensis -endotoxin gene to
tobacco for the control of Manduca sexta (Johannsen)
1989 An IPM Task Force was established to garner international support for the development and
implementation of IPM programmes. A team of consultants appointed by the Task Force
reviewed the status of IPM and made recommendations. The Task Force was later reconsti-
tuted as the Integrated Pest Management Working Group (IPWG) in 1990
1992 ● Concept of environmental economic injury levels proposed by L.P. Pedigo and L.G. Higley
● Dr Edward F. Knipling and Dr Raymond C. Bushland were awarded the World Food Prize
for developing sterile-insect technique
Continued
01IntpestManCh1.QXD 14/4/04 2:24 pm Page 4

4 G.S. Dhaliwal et al.

Table 1.1. Continued.

Period Landmark(s)

● United Nations Conference on Environment and Development (Rio de Janeiro, Argentina)

assigned a pivotal role to IPM in the agricultural programmes and policies envisaged as
part of its Agenda 21
1994 A Task Force consisting of FAO, the World Bank, UNDP and UNEP co-sponsored the estab-
lishment of the Global IPM Facility with the Secretariat located at FAO, Rome
1995 Dr Hans R. Herren was awarded the World Food Prize for developing and implementing the
world’s largest biological control project for cassava mealy bug, which had almost destroyed
the entire cassava crop of Africa
1996 Insect-resistant transgenic (Bt) cotton, maize and potato were commercialized in the USA
1997 Dr Ray F. Smith and Dr Perry L. Adkisson were awarded the World Food Prize for their
pioneering work in the development and implementation of the IPM concept
2002 Bt cotton approved for commercialization in India

DDT, dichlorodiphenyltrichloroethane; FAO, Food and Agriculture Organization; UNDP, United Nations
Development Programme; UNEP, United Nations Environment Programme; Bt, Bacillus thuringiensis.

properties of 2,2-bis(p-chlorophenyl)-1,1, agrochemical use (Meerman et al., 1997).

1-trichloroethane (DDT) by Paul Muller in Nearly three-quarters of the documented
1939. The impact of DDT on pest control is deaths take place in the Third World, even
perhaps unmatched by any other synthetic though it consumes only 15% of the global
substance and Muller was awarded a Nobel pesticide output. In addition, long-term tera-
Prize for this work in 1948. togenic, carcinogenic and mutagenic effects
DDT was soon followed by a number of of pesticides are well documented. In a land-
other insecticides, such as hexachlorocyclo- mark report, the National Resource Defence
hexane (HCH), chlordane, aldrin, dieldrin, Council (NDRC) of the USA reported that
heptachlor (organochlorine group), para- one out of every 3400 children between 1
thion, toxaphene, schradan, O-ethyl and 5 years of age could one day get cancer
O-4(nitrophenyl) phenyl phosphonothionate because of the pesticides they consumed as
(EPN) (organophosphorus group) and young children (NDRC, 1989).
allethrin (synthetic pyrethroid), during the Only a small amount (< 1%) of the pesti-
1950s and a large number of other popularly cide applied to a crop reaches target pests
used organophosphates and carbamates in and the remaining (> 99%) enters different
the ensuing decade. components of the environment to contami-
Due to their efficacy, convenience, flexibil- nate soil, water, air, food, feed, forage and
ity and economy, these pesticides played a other commodities. Nearly 100% of the
major role in increasing crop production. The human population has been found to contain
success of high-yielding varieties of wheat some residues of pesticides, such as DDT
and rice, which ushered in the ‘green revolu- and HCH (Dhaliwal and Arora, 2001). In
tion’, was partially due to the protective developing countries, such as India, a large
umbrella of pesticides (Pradhan, 1983). The proportion of market samples of nearly all
spectacular success of these pesticides types of food commodities have been found
masked their limitations. The intensive and to contain pesticide residues above the legal
extensive use, misuse and abuse of pesticides maximum residue limits (MRLs). In addition
during the ensuing decades caused wide- to human beings, the whole range of living
spread damage to the environment. The organisms, including natural enemies, polli-
most serious effects of pesticides are those on nators, domestic and wild animals, birds,
human health and life. It has been reported fish and other aquatic organisms and even
that at least 3 million, and perhaps as many soil fauna are affected by the use of insecti-
as 25 million, agricultural workers are poi- cides in agriculture (Dhaliwal and Singh,
soned each year by pesticides, and some 2000). In addition, pest problems in some
20,000 deaths can be directly attributed to crops increased following the continuous
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IPM: Retrospect and Prospect 5

application of pesticides. This, in turn, fur- Environment and Development, held in Rio de
ther increased the consumption of pesticides, Janeiro, Brazil, in 1992, which assigned a central
resulting in the phenomenon of the pesticide role for IPM in agriculture as part of Agenda 21.
treadmill (Altieri, 1995). The combined The Facility will serve as a coordination, con-
impact of all these problems, together with sulting, advising and promoting agency for the
the rising cost of pesticides, provided the advancement of IPM worldwide (Kogan, 1998).
necessary feedback for limiting the use of the Major efforts in implementing IPM in irri-
chemical control strategy and led to the gated rice have been carried out in Asia by the
development of the IPM concept. FAO through the Inter-Country Programme
for the Development and Application of
Integrated Pest Control in Rice in South-east
Asia. This programme remains one of the best
Era of IPM (1976 onwards)
examples of IPM implementation in the tropi-
cal region. It involves purposeful, direct
Although many IPM programmes were initi-
efforts to change farmers’ practices, in con-
ated in the late 1960s and early 1970s in sev-
trast to some more indirect routes of IPM
eral parts of the world, it was only in the late
technology diffusion in many industrialized,
1970s that IPM gained momentum. The first
temperate environments. The programme
major IPM project in the USA, commonly
itself has evolved into its present transna-
called the Huffaker project, spanned
tional form from a relatively small project
1972–1978 and covered six crops, i.e. lucerne,
supported by Australia in the late 1970s, fol-
citrus, cotton, pines, pome and stone fruits,
lowing the large-scale pest outbreaks in sev-
and soybean. This was followed by another
eral South-east Asian countries (NRI, 1992).
large-scale IPM project called the Consortium
The first phase of the FAO programme
for Integrated Pest Management (CIPM)
(1980–1986) focused on developing and test-
(1979–1985), which focused on lucerne, apple,
ing the technical aspects of the IPM concept
cotton and soybean. The average adoption of
in its seven participating countries, namely,
IPM for four crops was claimed to be about
Bangladesh, India, Malaysia, the Philippines,
66% over 5.76 million ha (Frisbie and
Sri Lanka and Thailand. More recently, the
Adkisson, 1985a,b). In 1993, the US govern-
project has been directed towards enhancing
ment set up the National IPM Initiative and
farmers’ adoption of IPM. Australia, The
submitted that implementing IPM practices
Netherlands and the Arab Gulf fund have
on 75% of the nation’s crop area by 2000 was
supported the programme. One significant
a national goal (Sorenson, 1994). In a recent
accomplishment of the programme has been
accounting of the progress by the US
to cause policy changes within several gov-
Department of Agriculture (USDA) in achiev-
ernments, in the form of official support of
ing this goal, it has been estimated that some
IPM as the means for national plant protec-
level of IPM has been implemented on about
tion in the Philippines, Indonesia, India, Sri
70% of the US crop acreage (Baron, 2002).
Lanka and Malaysia (NRI, 1992).
National IPM programmes were launched
A case study of the National IPM
in the late 1980s and early 1990s in several
Programme in Indonesia as a part of the
developing countries. The most outstanding
success has been the Food and Agriculture regional programme during 1989–1991 pro-
Organization (FAO) IPM programme for rice in vides an interesting scenario. Following
South-east Asia. By the end of 1995, 35,000 research findings showing the relation
trainers and 1.2 million farmers had been between brown planthopper outbreaks and
exposed to IPM through this programme (FAO, high pesticide use, the Indonesian govern-
1995). A recent development at FAO in support ment banned the use of 57 broad-spectrum
of IPM is the establishment of the Global IPM pesticides and declared IPM as the national
Facility, co-sponsored by the United Nations pest-control strategy. These measures,
Development Programme (UNDP), the United together with the gradual abolition of the
Nations Environment Programme (UNEP) and high subsidies on pesticides, created a
the World Bank. The concept is in response to favourable climate for the large-scale imple-
the United Nations Conference on mentation of IPM (Fig. 1.1).
01IntpestManCh1.QXD 14/4/04 2:24 pm Page 6

6 G.S. Dhaliwal et al.

60 31 In spite of this, IPM farmers obtained higher

yields than non-IPM farmers, which, in addi-
tion to lower pest-control expenditure,

Milled rice production (millions of tonnes)

resulted in higher returns from the crop.
Pesticide production (× 1000 tonnes)

50
Additionally, there were fewer variations in
85% 28
fields among IPM farmers than among non-
IPM farmers, indicating less risky farm man-
40 agement under the IPM regime. Timeliness
75% and adequacy of various cultivation and
25 pest-control practices, resulting from better
monitoring and decision-making skills, seem
30
to be most important in this respect (van de
55% Fliert, 1998).
22 During the second phase of the National
20 40% IPM Programme (1994/95), 310,550 farmers
Rice participated in rice IPM field schools. IPM
Pesticide
Pesticides subsidy farmers applied pesticides, on average, 1.25
0%
times while non-IPM farmers made an aver-
10 19
1984 1986 1988 1990 age of 3.62 applications during the season.
Similarly, IPM farmers used fewer formula-
Fig. 1.1. Impact of pesticide subsidy on rice tions (cocktails) per spray event, with an
production in Indonesia (after FAO, 1990). average of 2.6 for IPM farmers versus 7.2 for
non-IPM farmers.
To assess the impact of IPM on pest con- China, which has been experimenting
trol and yield, the latter were compared with with IPM for the control of rice pests since
those of non-IPM farmers (van de Fliert, the early 1980s, was also invited to join the
1993). IPM farmers really decreased their fre- FAO project in 1989. During 1989/90 alone,
quency of pesticide sprays during and after nearly 160,000 farmers from over 2000 vil-
the training to a level consistently lower than lages received IPM training. Compared with
that of non-IPM farmers (Table 1.2). untrained farmers, IPM-trained farmers
Consequently, IPM farmers’ expenditure on saved roughly a third of the pesticides in rice
insect chemical control decreased. The num- cultivation and still obtained a 7% higher
ber of farmers not applying pesticides was yield. It was estimated that the investment in
also significantly higher among IPM farmers. IPM training generated a return of more than

Table 1.2. Insect pest-control practices, expenditures and yields of IPM and non-IPM farmers in two
villages in Central Java, before, during and after IPM training (from van de Fliert, 1993).

After two
Before training During training After one season seasons

Parameter IPMF NIPMF IPMF NIPMF IPMF NIPMF IPMF NIPMF

Frequency of spray 1.4 1.5 0.7 1.5 0.8 1.3 0.3 0.8
applications (no./season)
Frequency of granular 0.4 0.3 0.7 0.9 0.7 0.8 0.6 0.7
applications (no./season)
Farmers not using 26 31 41 19 46 24 50 43
pesticides (%)
Average insect control 32 22 18 31 18 21 9 19
cost (Rs 1000/ha)
Average yield (t/ha) 5.38 5.11 5.77 4.64 3.70 3.11 6.38 5.68

IPMF, IPM farmers; NIPMF, non-IPM farmers.

01IntpestManCh1.QXD 14/4/04 2:24 pm Page 7

IPM: Retrospect and Prospect 7

400%. Encouraged by these results, the pesticides and satisfactory control of insect
Ministry of Agriculture has set up a National pests was being provided by fish and natu-
Steering Committee for the comprehensive rally occurring parasitoids and predators
prevention and control of diseases and insect (Table 1.3).
pests to protect the nation’s rice crop and Farmers cultivating fish in their rice fields
increase profits. The Committee conducts totally eliminated the use of pesticides even
IPM tests, gives demonstrations and makes without training in IPM. However, only 20%
appraisals (Quinghua, 1995). of the farmers could cultivate fish, mainly
In the Philippines, a National IPM due to lack of adequate water, the poor
Programme was launched in 1993 and a total water-holding capacity of the soil and the
of 40,024 farmers were trained during risk of flooding. Those farmers who could
1993–1995, among whom 36,024 are rice farm- not cultivate fish still reduced their pesticide
ers. Of 1632 farmers’ field schools (FFSs), 1470 use by 76% with IPM training. By harvest
were devoted to rice farmers. The increase in time, some farmers were able to harvest
rice yield obtained by IPM farmers varied quantities of fish worth as much as their rice.
from 4.7 to 62%. The expenditure on pesticide These results underline the need for under-
use (15% of total cost) was almost eliminated taking an IPM programme as part of overall
in the case of IPM farmers (Kenmore, 1997). rural development programmes (Kamp et al.,
In Vietnam, during 1992–1995, 5941 FFSs 1993).
were organized in 3095 villages (out of 9274 During 1995, farmers at IPM schools
villages in the country), with a total of applied an average of 0.19 spray/season as
173,650 farmers trained. The number of compared with 1.65 sprays/season during
insecticide applications by IPM farmers was the pretraining period. The average yield
reduced by 80–90% and, in some agroecologi- increased by 17% from 3.76 t/ha during the
cal regions, there was almost no use of insec- pretraining period to 4.4 t/ha after IPM
ticides. IPM fields produced 150–460 kg/ha training. The average number of pests per
more rice than non-IPM fields. One study of ten rice hills decreased from 20 to 11 and the
over 1300 villages in Vietnam showed a 4% number of natural enemies increased from
yield increase in rice and over 20% increase 18 to 31.
in profits (Kenmore, 1997). In India, FFSs were organized at locations
In Bangladesh, the Cooperative for covering all the major rice growing areas of
American Relief to Everywhere (CARE)- the country during 1994/95. Pesticide use in
Bangladesh began introducing IPM activities IPM fields decreased by 50–100% as com-
into an ongoing rice irrigation project in the pared with non-IPM areas. There was an
late 1980s. Most of the farmers that CARE increase in yield between 6.2 to 42.1% in IPM
worked with were very small, owning less fields as compared with non-IPM areas
than half an acre of land. The farmers were (Rajak et al., 1997).
trained in rice–fish culture and IPM. A sur- The success of the rice programme per-
vey among the farmers trained in rice–fish suaded FAO to launch similar IPM
culture and IPM revealed that, during Intercountry Programmes for vegetables
1992/93, virtually all of them stopped using (1996) and cotton (1999). Moreover, in the

Table 1.3. Effect of training in rice–fish culture and IPM on pesticide use by rice growers during 1992/93,
Rangpur, Bangladesh (from Kamp et al., 1993).

Parameter Group I Group II Group III Group IV

Number of farmers 121 58 972 60

Type of training Rice–fish Rice–fish IPM only Nil
culture only culture and
IPM
Reduction in pesticide use (%) 100 100 76 –
Increase in rice yield (%) 6 13 10 –
01IntpestManCh1.QXD 14/4/04 2:24 pm Page 8

8 G.S. Dhaliwal et al.

individual countries, FFS activities were integrated control was first conceived by
started in a range of other crops, sometimes Hoskins et al. (1939) when they said:
with external donor support, sometimes Biological and chemical control are considered
without. The Asian model of FFS IPM train- as supplementing to one another or as the two
ing has been applied in other continents as edges of the same sword … nature’s own
well, albeit with adjustments for different balance provides the major part of the
cropping and socio-economic conditions protection that is required for the successful
(Eveleens, 2002). pursuit of agriculture … insecticides should be
used so as to interfere with natural control of
pests as little as possible.
Origin of IPM Concept The credit for using the term ‘integrated
control’ for the first time goes to
The basic tactics of IPM were proposed and Michelbacher and Bacon (1952), who, while
used to protect crop plants against the rav- working on the control of codling moth,
ages of pests long before the term was Cydia pomonella (Linnaeus), stressed ‘the
coined. Most discussions of IPM include the importance of considering the entire, ento-
concept of economic threshold, implying mological picture in developing a treatment
that whatever cost one applies to the pest for any particular pest … All effort was
control techniques should be returned from directed towards developing an effective
the production of the crop (McNeal, 1988). integrated control program of the important
Another concept is that of team effort, where pests of walnut.’ Subsequently, Smith and
IPM strives to bring together as many disci- Allen (1954) stated that ‘integrated control …
plines and areas of interest as possible. The will utilize all the resources of ecology and
concern over pesticides as a main source of give us the most permanent, satisfactory and
pest control is that it makes one totally reliant economical insect control that is possible’.
on such technology and, if that technology Following this was a series of papers that
starts to fail, the only way out is a new established integrated control as a new trend
replacement that promises an improvement in entomology (Kogan, 1998).
over the old one, even if the transfer may also Stern et al. (1959) were the first to define
cause difficulties. Thus, in the absence of integrated control as ‘applied pest control,
modern synthetic pesticides, crop protection which combines and integrates biological and
specialists during the late 19th and early 20th chemical control’. This definition remained in
centuries relied on pest biology and cultural place through the late 1950s and early 1960s,
practices to propose multitactical approaches, but began to change soon in the early 1960s as
which could be considered as precursors of the concept of pest management gained
modern IPM systems. To be precise, the con- acceptance among crop protection specialists.
cept of technology packages assembled in
IPM can help us to avoid some of the pitfalls
inherent in reliance on a single technology Pest management
(McNeal, 1988).
The idea of managing insect-pest popula-
tions was proposed by Geier and Clark
Integrated control (1961), who called this concept ‘protective
population management’, which was later
According to McNeal (1988), one of the activ- shortened to ‘pest management’ (Geier,
ities most responsible for the genesis of IPM 1966). By the mid-1970s, integrated control
was the work done in cotton entomology in and pest management coexisted essentially
Arkansas in the 1920s. This research was as synonyms. However, a synthesis of the
overshadowed in the late 1940s as pesticides two expressions had already become avail-
came along, but the work continued into the able when Smith and van den Bosch (1967)
1950s with the cotton scouting programme in wrote: ‘The determination of insect numbers
Arkansas. However, apparently the idea of is broadly under the influence of the total
01IntpestManCh1.QXD 14/4/04 2:24 pm Page 9

IPM: Retrospect and Prospect 9

agroecosystem and a background role of the pest management’ (EBPM), emphasizing that
principal elements is essential to integrated it was:
pest population management’.
● safe for farmers and consumers;
● cost-effective and easy to adopt and inte-
grate with other crop protection practices;
Integrated pest management ● durable and without adverse environ-
mental and safety consequences; and
It was, however, in 1972 that the term ‘inte- ● used with ecosystems as the ecological
grated pest management’ was accepted by focus.
the scientific community, after the publica-
tion of a report under the above title by the All these goals have been well taken care
Council on Environmental Quality (CEQ, of by the concept of IPM.
1972). In creating this synthesis between Thus IPM is here to stay and to provide
integrated control and pest management, no suitable solutions to future pest problems.
obvious attempts seemed to have been made Recently, Benbrook (2002) proposed a new
to advance a new paradigm. Much of the term: the IPM continuum. According to the
debate had already taken place during the author, IPM systems exist in almost limitless
1960s and by then there was substantial variety along an IPM continuum. It includes
agreement on the following issues (Kogan, four major zones/levels: no, low, medium
1998): and high or biointensive IPM. Farmers in the
‘non-IPM’ zone manage pests with routine
● ‘Integration’ means the harmonious use pesticide applications. Low-end IPM
of multiple methods to control single depends on basic field sanitation, scouting
pests as well as the impacts of multiple and pesticide applications linked to thresh-
pests. olds. Medium-level IPM shifts a portion of
● ‘Pests’ are any organisms detrimental to the control burden to largely preventive
humans, including invertebrate and ver- measures and requires farmers to bypass
tebrate animals, pathogens and weeds. most applications of pesticides because of
● ‘Management’ refers to a set of decision the greater degree of reliance on beneficial
rules based on ecological principles and organisms. High-level IPM systems manage
economic and social considerations. The pests largely through multitactic prevention-
backbone for the management of pests in based interventions. Biointensive IPM (or
an agricultural system is the concept of Bio IPM) lessens pest pressure through man-
economic injury level (EIL). agement of ecological and biological
● ‘IPM’ is a multidisciplinary endeavour. processes and interactions.

Alternative paradigms Defining IPM

Although the success of IPM has been Since the first definition of integrated control
accepted worldwide, some new terms have (Stern et al., 1959), more than 65 definitions
been proposed to lay emphasis on particular of integrated control, pest management or
strategies. Frisbie and Smith (1991) proposed IPM have been proposed. A broader defini-
‘biologically intensive IPM’ or ‘biointensive tion was adopted by FAO Panel of Experts
IPM’, which would rely on host-plant resis- (FAO, 1967):
tance, biological control and cultural control.
Integrated pest control is a pest management
In fact, the utilization of biological control
system that, in the context of associated
and other non-chemical methods has been environment and population dynamics of the
amply stressed in all IPM programmes. pest species, utilizes all suitable techniques and
Recently, a special committee of the National methods in as compatible a manner as possible
Research Council’s Board of Agriculture and maintains pest populations at levels below
(NRC, 1996) proposed ‘ecologically based those causing economic injury.
01IntpestManCh1.QXD 14/4/04 2:24 pm Page 10

10 G.S. Dhaliwal et al.

It is not simply the juxtaposition or superim- IPM is systematic approach to crop pro-
position of two control techniques but the tection that uses increased information and
integration of all suitable management tech- improved decision-making paradigms to
niques with the natural regulating and limit- reduce purchased inputs and improve eco-
ing elements of the environment. According nomic, social and environment conditions on
to the National Academy of Sciences, IPM the farm and in society (Allen and Rajotte,
refers to an ecological approach in pest man- 1990). IPM is a comprehensive approach to
agement in which all available necessary pest control that uses combined means to
techniques are consolidated in a unified pro- reduce the status of pests to tolerable levels
gramme, so that pest populations can be while maintaining a quality environment
managed in such a manner that economic (Pedigo, 1991). IPM is also defined as the
damage is avoided and adverse side effects intelligent selection and use of pest-control
are minimized (NAS, 1969). tactics that will ensure favourable economic,
Most other contemporary definitions per- ecological and sociological consequences
petuate the perception of an entomological (Luckman and Metcalf, 1994).
bias in IPM because of the emphasis on pest IPM is a dynamic and constantly evolv-
populations and EIs, of which the former is ing approach to crop protection in which all
not always applicable to plant pathogens and the suitable management tactics and avail-
the latter is usually attached to the notion of able surveillance and forecasting informa-
an action threshold that is often incompatible tion are utilized to develop a holistic
with pathogen epidemiology or many weed- management programme as part of a sus-
management systems. Smith (1978) defined tainable crop production technology
IPM as a multidisciplinary ecological (Dhaliwal and Arora, 2001). Here it needs to
approach to the management of pest popula- be emphasized that the aim of future IPM
tions, which utilizes a variety of control tactics programmes should not be restricted merely
compatibly in a single coordinated pest-man- to the efficient use of pesticides and product
agement system. In its operation, integrated substitution (biorationals and botanicals in
pest control is a multitactical approach that place of conventional insecticides) within an
encourages the fullest use of natural mortality agricultural system that remains essentially
factors, complemented, when necessary, by unchanged (Table 1.4). Rather, these pro-
artificial means of pest management. In other grammes should aim at fundamental struc-
words, IPM seeks to integrate multidiscipli- tural changes through a better
nary methodologies to develop pest-manage- understanding of ecological processes and
ment strategies that are practical, effective, synergy between crops (van Veldhuizen and
economical and protective of both public Hiemstra, 1993).
health and the environment (Smith et al., Kogan (1998) carried out numerical analy-
1976). IPM has also been defined as a pest ses of various definitions spanning the last
population management system that utilizes 35 years and found that most of the authors
all suitable techniques in a compatible manner depended on the following issues to capture
to reduce pest populations and maintain them the essence of the IPM concept:
at levels below those causing economic injury
● The appropriate selection of pest-control
(Frisbie and Adkisson, 1985a,b). Dr Ray F.
methods, used singly or in combination.
Smith and Dr Perry Adkisson were awarded
● The economic benefits to growers and to
the 1997 World Food Prize for their pioneering
society.
work in the development and implementation
● The decision rules that guide the selection
of the IPM concept. However, in 1998, USDA
of the control action.
came up with a definition that IPM is a sus-
● The need to consider impacts of multiple
tainable approach that combines the use of
pests.
prevention, avoidance, monitoring and sup-
pression strategies in a way that minimizes Taking into consideration all the above
economic, health and environmental risks points and the current thought, Kogan (1998)
(www.reeusda.gov/nipmn). put forward his definition:
Table 1.4. Approaches to insect pest management: retrospect and prospect (from Dhaliwal and Arora, 1994b).

Pest management system

No. Parameter Traditional Industrial Present IPM IPM in sustainable agriculture

1 Goal Reduce losses due to pests Eliminate or reduce Reduce costs of production Multiple-ecological, economic and social
pest species
2 Diversity High Low Low or medium High
3 Ecosystem stability Uncertain Highly unstable Unstable Striving towards stability and equilibrium
4 Spatial scale Single farm Single farm Single farm or small region Biogeographical regions
defined by pests
5 Time scale Long term Immediate Single season Long-term steady-state oscillatory
dynamics
6 Target Single pest or closely related Single pest Several pests around a Fauna and flora of a cultivated area and
01IntpestManCh1.QXD 14/4/04 2:24 pm Page 11

groups of pests crop and their natural linkages with non-cultivated ecosystem
enemies
7 Criteria for intervention Past experience Calendar date or Economic threshold Multiple criteria
presence of pest
8 Principal method Cultural and mechanical Pesticides Resistant varieties, cultural Agroecosystem design to minimize pest
measures practices, monitoring, outbreaks and mixed strategies,
product substitution, including group action on an area-wide
insecticide resistance basis to complement pest controls
management and multiple aimed at individual fields
IPM: Retrospect and Prospect

interventions
9 Research goal Nil due to absence of Improved pesticides More kinds of interventions Minimize need for intervention
organized effort
10 Extension technique Nil Transfer of technology TOT Complementarity between TOT and
(TOT) farmer-first (FF) mode
11 Effect on environmental Usually negligible Highly detrimental Moderately detrimental Negligible
quality
11
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12 G.S. Dhaliwal et al.

IPM is a decision support system for the numbers or damage), specify an effective-
selection and use of pest control tactics, singly ness target that is appropriate, given the
or harmoniously coordinated into a experimental data and information at
management strategy, based on cost/benefit hand (e.g. a 50% reduction in pest popula-
analyses that take into account the interests of
tion).
and impacts on producers, society and the
environment.
● Multiply the cost of each practice times
the effectiveness target and then divide
that product by the actual level of effec-
tiveness achieved by the practice. This
Decision Making Systems
gives a set of relative cost-effectiveness
figures.
Pest management is a combination of
● Compare the cost-effectiveness of alterna-
processes that include decision making, tak-
tive practices. The practice that has associ-
ing action against a pest and obtaining the
ated with it the lowest cost to achieve the
information to be used in reaching these deci-
effectiveness target is the most cost-
sions (Ruesink and Onstad, 1994). In assess-
effective practice.
ing, evaluating and choosing a particular
pest-control option, farmers are likely to take
three major factors into account (Fig. 1.2):
Implementation
● Farmers’ perception of the problem and
of potential solutions is the most impor- Although IPM has been accepted in principle
tant factor. Here, the farmer’s ability to as the most attractive option for the protec-
identify pests, his/her assessment of tion of agricultural crops from the ravages of
likely and potential pest losses and insect and non-insect pests, implementation
his/her opinion regarding the efficacy of at the farmers’ level has as yet been rather
different control options will affect the limited. Some of the important constraints to
decision process. wider adoption of IPM and suggested mea-
● The way in which control options are sures to overcome them are discussed in this
assessed will depend on the farmers’ section.
objectives. Subsistence farmers may opt
for a guaranteed food supply, while com-
mercial farmers are more concerned with Constraints in IPM implementation
profit.
● The number of options that a farmer can The Consultant Group of the IPM Task Force
feasibly use will depend on the con- has conducted an in-depth study of the con-
straints set by the resources available. straints on the implementation of IPM in
developing countries, which can be catego-
Various alternative pest-control options
rized into the following five main groups
could be evaluated for their cost-effectiveness
(NRI, 1992; Alam, 2000).
(Reichelderfer et al., 1984):
● Determine from experimental results both
Institutional constraints
the per hectare cost and a measure of
effect of each alternative practice. If effec- IPM requires an interdisciplinary, multi-
tiveness can be measured in terms of out- functional approach to solving pest prob-
put (yield and/or crop quality), use lems. Fragmentation between disciplines,
partial budgeting or other analytical tech- between research, extension and implemen-
niques to evaluate alternatives. If effec- tation and between institutes leads to a lack
tiveness cannot be measured in these of institutional integration. Secondly, both
terms, proceed with determination of the national programmes of developing
cost-effectiveness. countries and the donor agencies have
● Using the same units in which effective- lacked a policy commitment to IPM in the
ness is measured (e.g. reduction in pest context of national economic planning and
01IntpestManCh1.QXD 14/4/04 2:24 pm Page 13

IPM: Retrospect and Prospect 13

Farmer’s perception Farmer’s

of pest problem and resources
its control

Farmer’s
needs and Assessment of options, Pest-control
objectives feasibility and options
appropriateness

Evaluation and comparison

among appropriate options

Action arising from choice of

option

Outcome of action

Fig. 1.2. The process of decision making in IPM (after Reichelderfer et al., 1984).

agricultural development. This has resulted individual control techniques are well
in a low priority for IPM from national pro- known, little knowledge is available on
grammes and donors alike. Thirdly, the tra- using them in an integrated fashion under
ditional top-down research in many cases farm conditions. The lack of training materi-
does not address the real needs of farmers, als, curricula and experienced teachers on
who eventually are the end-users and who the principles and practice of IPM is another
elect to adopt or reject the technology based major constraint. In many cases, the field
on its appropriateness. Institutional barriers level extension workers are not sufficiently
to research scientists in national programmes trained in IPM to instil confidence in the
conducting on-farm research in developing farmers.
countries are real and need to be addressed.
Sociological constraints
Informational constraints
The conditioning of most farmers and farm-
The lack of IPM information that could be level extension workers by the pesticide
used by farmers and extension workers is a industry has created a situation where chem-
major constraint in implementation. In a icals are presented as highly effective and
recent study regarding the implementation simple to apply. This acts as a major con-
of IPM in Haryana, India, it was found that straint in IPM implementation. There appears
more than three-quarters of the farmers were to be a direct conflict between the industry’s
not even aware of the concept of IPM. Even objective of more sales and the IPM message
those who were aware of the concept of rational pesticide use in the eyes of farm-
reported that they lacked the skills necessary ers. There is a need for private industry and
to practise IPM (Alam, 2000). While the public-sector extension agencies to work in a
01IntpestManCh1.QXD 14/4/04 2:24 pm Page 14

14 G.S. Dhaliwal et al.

more complementary manner. A majority of Farmers’ participation

the farmers in a recent study in Haryana,
It would not be an exaggeration to say that
India, expressed their lack of faith in IPM.
the dawn of civilization started with farmer
They considered IPM practices to be risky as
innovation. Ever since that day, farmers have
compared with the use of chemical pesticides
improved ways of growing crops through
(Alam, 2000).
successive innovations. Prior to the emer-
gence of crop-protection sciences and even
Economic constraints before the broad outlines of the biology of
A major constraint, even if IPM is adopted in pests were understood, farmers evolved
principle, is the funding for research, exten- many cultural, mechanical and physical con-
sion and farmer training needed for an accel- trol practices for the protection of their crops
erated programme. IPM must be viewed as from insects and non-insect pests (Smith et
an investment and, as with other forms of al., 1976). Farmers’ innovations were the only
investment, requires an outlay. Starting with source of improvements in crop production
the Huffaker project, the US Environmental and protection technology until formal
Protection Agency (USEPA) and USDA have research by on-station scientists started com-
financed a number of IPM programmes, plementing it during the late 18th and 19th
resulting in substantial progress in the devel- centuries (Haverskort et al., 1991).
opment and implementation of IPM. In the Unfortunately, with the advent of modern
long run, IPM programmes may become self- high-tech agriculture, comprising of high-
generating due to savings on resource inputs yielding varieties (HYVs), fertilizers and pes-
for production. A majority of the farmers pur- ticides, farmers have been completely
chase pesticides on credit and depend on displaced from the research and develop-
shopkeepers and pesticide dealers for infor- ment process. Instead, this role has been
mation about pest-control methods. usurped by private industry and govern-
ment agencies. The technology generated by
farm scientists is being transferred through
Political constraints extension agencies to farmers. The new tech-
The relatively low status of plant-protection nology package has created a number of eco-
workers in the administrative hierarchy is a logical and environmental problems. The
constraint to general improvement in plant alternative path of sustainable agriculture
protection. Associated with the above is the requires farmers’ participation at every step
moral and financial standing of these work- of the research and development process in
ers. The continuance of pesticide subsidies order to draw on their understanding of the
by the government for political reasons and local conditions and constraints, their innov-
their tie-up with the government-provided ativeness and their skills at making the best
credit for crop production act as a major con- possible use of limited resources.
straint to farmers’ acceptance of IPM. Placing the farmer at the centre of the
Various vested interests associated with the development process is wholly consistent
pesticide trade also act as a political con- with the IPM goal of making the farmer a
straint on the implementation of IPM confident manager and decision maker, free
(Jiggins, 1996). from dependence on a constant stream of
pest-control instructions from outside. The
role of researchers, extension workers and
Strategies for IPM implementation non-governmental organizations (NGOs) is
to act as consultants, facilitators and collabo-
Acceleration of IPM implementation in rators, stimulating and empowering the
developing countries requires farmers’ par- farmers to analyse their own situation, to
ticipation, increased government support, an experiment and to make constructive
improved institutional infrastructure and a choices. A number of terms have been pro-
favourable environment. posed for the new approach. These include:
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IPM: Retrospect and Prospect 15

‘farmer first and last’, ‘farmer participatory with the objectives of IPM are relatively
research’, ‘farmer first’, ‘approach develop- greater than the costs to developed coun-
ment’, ‘people-centred technology develop- tries. National policies to promote IPM
ment’ (PCTD) and ‘participatory technology require close regulation at all stages related
development’ (PTD) as well as the old term to the importation and/or manufacture, dis-
‘sustainable agriculture’ (Chambers et al., tribution, use and disposal of pesticides. In
1991; Haverskort et al., 1991). PTD serves to the case of pesticides that do not meet pre-
improve the experimental capacity of farm- scribed standards for safety, persistence, etc.,
ers and helps in the development of locally import and manufacturing bans should be
adapted improved technologies. enacted. At a minimum, the conditions laid
The approach has been used for imple- out by the FAO Code of Conduct on the
mentation of IPM programmes in Indonesia Regulation, Distribution and Use of Pesticides
(Matteson et al., 1994). In this method, farm- should be adopted. Pesticide subsidies need
ers are divided into small groups to monitor to be eliminated in order to make IPM an
the crop and then each group analyses the attractive alternative. The funds thus saved
field situation by identifying the key factors. may be utilized for the implementation of
Group members then decide whether any IPM. Funds may also be diverted from some
action is required. At a combined meeting, of the current research programmes to IPM-
each group presents and defends its sum- oriented plant-protection programmes.
mary to the other trainees. The trainer facili- Additional monetary resources may be gen-
tates by asking leading questions or adding erated through cooperation with bilateral/
technical information if necessary. This multilateral agencies willing to support such
process allows farmers to integrate and prac- programmes (NRI, 1992).
tise their skills and knowledge and gives
trainers an opportunity to evaluate the
Legislative measures
trainees’ ability. Thousands of farmers have
been trained utilizing this approach and it is IPM is an information system and its adop-
being tried on a pilot scale. A survey among tion reduces pest-control costs. The alterna-
these farmers during the first post-training tive to IPM is the indiscriminate use of
season revealed that they really decreased broad-spectrum synthetic organic pesticides.
their frequency of pesticide sprays to a level Unfortunately, while pesticide manufactur-
consistently lower than that of non-IPM ers and users (farmers) derive the full bene-
farmers. The percentage of farmers not fits from the use of these chemicals, they
applying pesticides was also significantly pass on the environmental and ecological
higher among the trained farmers. In spite of costs of their use to the society as a whole. If
lower pest-control expenditures, these farm- they are made to bear the full cost of the use
ers obtained higher yields than the non-IPM of these toxicants, they may find IPM a more
farmers. This programme has been extended economical and attractive alternative. This
to several other Asian countries and the evi- could be achieved by enforcing suitable leg-
dent advantages of the approach are a islative measures.
marked reduction in the use of pesticides, Secondly, the success of an IPM pro-
with measurable benefits to the environment gramme in any geographical region depends
(APO, 1996; Heinrichs, 1998; Ooi, 2000). upon its implementation by all the farmers
in the area. Ideally, farmers may voluntarily
adopt an IPM programme but some farmers
Government support
may hold out. Such farmers, called ‘spoiler
Both the national programmes of developing holdouts’, may impair the success of a pro-
countries and the donor agencies must have gramme by failing to adopt a necessary prac-
a policy commitment to IPM in the context of tice, thus causing damage to adjacent areas.
national economic planning and agricultural This is especially important in the case of
development. The costs to developing coun- mobile pests. In addition, some farmers may
tries of not bringing their policies in line free-ride and thus shift the costs of imple-
01IntpestManCh1.QXD 14/4/04 2:24 pm Page 16

16 G.S. Dhaliwal et al.

menting and managing a programme to a Improved awareness

group of participating farmers. To overcome
Increased education and awareness regard-
‘spoiler holdouts’ and ‘free riders’, it may be
ing the objectives, techniques and impact of
necessary to impose a programme upon an
IPM programmes are required at all levels
unwilling minority through suitable legisla-
including policy makers, planners, farmers,
tive measures (Tarlock, 1980).
consumers and the general public. The
importance and benefits of pesticides are
Improved institutional infrastructure being overemphasized by a multibillion-
dollar industry utilizing the services of not
IPM cannot be implemented unless there is a
only their salesmen but also agricultural sci-
basic infrastructure for plant protection in a
entists, administrators and planners. There is
country. There is a need to develop and sup-
not yet a strong market in IPM information.
port national programme capabilities for on-
Policy makers and planners need to be con-
farm testing and technology extrapolation.
vinced that without IPM current agricultural
At the international level, the establishment
production systems are not sustainable.
of an IPM working group to coordinate and
Similarly, much important information that
monitor the funding of IPM projects is
might induce a farmer to adopt IPM is not
bound to provide an impetus to the imple-
immediately observable and is therefore not
mentation of IPM.
sought by the farmer. A manufacturer has no
IPM is predominantly a knowledge tech-
incentive to recommend a programme that
nology, the use of which requires training of
uses less pesticide or even selective pesti-
the many groups involved. There is currently
cides that kill a limited range of pests
little training material for most of these
(Tarlock, 1980).
groups, including farmers, extension person-
Consumer groups and the general public
nel and researchers. If IPM is to become the
may also be able to support the implementa-
major approach for pest management in the
tion of IPM programmes by demanding
developing world, this deficiency must be
residue-free commodities. There is now a
remedied urgently (NRI, 1992). Another
distinct market for organically produced
aspect requiring greater attention is coordina-
food and other products. For example, there
tion of effort within and between countries
is a major programme at Cornell University,
(which is especially important with mobile
USA, for pesticide-reduced produce. NGOs
insect species, such as the brown planthop-
and consumer groups need to be strength-
per), between national research, training and
ened in developing countries, so that there is
implementation institutes/programmes, and
a public-oriented movement for implementa-
among international development agencies.
tion of IPM.
Lack of a reliable database has also ham-
pered the progress of IPM programmes. A
reliable source of accurate information on the
status of crops and pests in farmers’ fields is Future Outlook
necessary for many IPM activities. Most of
the successful IPM programmes in both Initially, IPM programmes evolved as a result
developed and developing countries have a of the pest problems caused by repeated and
reasonably accurate system of monitoring excessive use of pesticides and increasing
and evaluating various biological and envi- cases of pest resistance to these chemicals. It
ronmental parameters in the agroecosystem. is only during the past few years that the eco-
A reliable database on crop yield and pest nomic and social aspects of IPM have also
losses is required for planning and resource received increasing attention (Fig. 1.3). It is
allocation at the national and international now being increasingly recognized that mod-
level. Systems analysis has been used as a ern agriculture cannot sustain the present
problem-diagnosis tool for IPM in devel- productivity levels with the exclusive use of
oped-country cropping systems and may be pesticides. Increasing pest problems and dis-
used in developing countries as well. ruptions in agroecosystems can only be cor-
01IntpestManCh1.QXD 14/4/04 2:24 pm Page 17

IPM: Retrospect and Prospect 17

There needs to be a paradigm shift in the

pest-management approach from managing
components or individual organisms to an
Natural control
approach that examines processes, flows and
interactions between populations of plants
and populations of pest, beneficial and
Ecological Economic innocuous organisms (Dent, 1995; Hall, 1995;
sustainability sustainability
NRC, 1996; Kogan, 1998). There is a need for
a better understanding of factors that affect
IPM
ecosystem stability, the population dynamics
of pests and the ability of populations to
Social
stability recover from stress. Technologies generated
Farmers’ Modern
practices approaches for the control of one group of pests, such as
insects, diseases, weeds or nematodes, must
be integrated in a crop-production system.
There is a need to integrate the traditional
practices of farmers with the advanced bio-
Fig. 1.3. Role of IPM in ecosystem stability (after
logical technologies now available in order
Dhaliwal and Heinrichs,1998)
to develop a profitable, safe and sustainable
rected by use the of holistic pest-management approach to pest management. It must be
programmes. If the environmental and social remembered that the success of any IPM pro-
costs of pesticide use are taken into account, gramme will depend upon the effective
IPM appears to be a more attractive alterna- transfer of technology to farmers. Therefore,
tive with lower economic costs. The IPM pro- the quick transfer, synthesis and simplifica-
grammes do not endanger non-target tion of information among farmers, suppliers
organisms, nor do they pollute the soil, water of agricultural inputs and public agencies
and air. IPM builds upon indigenous farming would speed up the successful development
knowledge, treating traditional cultivation and implementation of IPM. Finally, the
practices as components of location-specific challenge to develop new technology, new
IPM practices. This is especially important management skills and new concepts of inte-
for farmers in developing countries, where gration for pest management must be met so
traditional agricultural systems are based on that we may protect our environment and
indigenous farming practices. The incorpora- provide a continuous supply of safe and
tion of IPM into these practices helps the nutritious food for the rapidly expanding
farmers to modernize while maintaining world population.
their cultural roots.

References

Alam, G. (2000) A Study of Biopesticides and Biofertilizers in Haryana, India. Gatekeeper Series No. 93,
International Institute of Environment and Development, London.
Allen, W.A. and Rajotte, E.G. (1990) The changing role of extension entomology in the IPM era. Annual
Review of Entomology 25, 379–397.
Altieri, M.A. (1995) Escaping the treadmill. Ceres 27, 15–23.
APO (1996) Integrated Pest Management in Asia and the Pacific. Asian Productivity Organization, Tokyo, 170
pp.
Baron, J.J. (2002) The role of reduced risk crop protection chemicals on the success of IPM in the US. In:
International IPM Conference Exploring New Frontiers in Integrated Pest Management, 24–26 March,
2002, Toronto, Ontario, Canada, pp. 60–62.
Benbrook, C.M. (2002) Measuring IPM adoption and the IPM continuum. In: International IPM Conference
Exploring New Frontiers in Integrated Pest Management, 24–26 March, 2002, Toronto, Ontario, Canada,
pp. 48–50.
CEQ (1972) Integrated Pest Management. Council on Environmental Quality, Washington, DC, 41 pp.
01IntpestManCh1.QXD 14/4/04 2:24 pm Page 18

18 G.S. Dhaliwal et al.

Chambers, R., Pacey, A. and Thrupp, L.A. (eds) (1991) Farmer First: Farmer Innovation and Agricultural
Research. Intermediate Technology Publications, London.
DeBach, P. (1964) Biological Control of Insect Pests and Weeds. Chapman & Hall, London.
Dent, D. (1995) Integrated Pest Management. Chapman & Hall, London, 356 pp.
Dhaliwal, G.S. and Arora, R. (eds) (1994a) Trends in Agricultural Insect Pest Management. Commonwealth
Publishers, New Delhi, 547 pp.
Dhaliwal, G.S. and Arora, R. (1994b) Components of insect pest management: a critique. In: Dhaliwal,
G.S. and Arora, R. (eds) Trends in Agricultural Insect Pest Management. Commonwealth Publishers,
New Delhi, pp. 1–55.
Dhaliwal, G.S. and Arora, R. (2001) Integrated Pest Management: Concepts and Approaches. Kalyani
Publishers, New Delhi, 427 pp.
Dhaliwal, G.S. and Heinrichs, E.A. (eds) (1998) Critical Issues in Insect Pest Management. Commonwealth
Publishers, New Delhi, 287 pp.
Dhaliwal, G.S. and Singh, B. (2000) Pesticides and Environment. Commonwealth Publishers, New Delhi,
439 pp.
Dhaliwal, G.S., Arora, R. and Heinrichs, E.A. (1998) Insect pest management: from traditional to sustain-
able approach. In: Dhaliwal, G.S. and Heinrichs, E.A. (eds) Critical Issues in Insect Pest Management.
Commonwealth Publishers, New Delhi, pp. 1–25.
Eveleens, K.G. (2002) International IPM implementation and adoption: the Asian experience. In:
International IPM Conference Exploring New Frontiers in integrated Pest Management, 24–26 March,
2002, Toronto, Canada, pp. 75–77.
FAO (1967) Report of the First Session of the FAO Panel of Experts on Integrated Pest Control. Food and
Agriculture Organization of the United Nations, Rome.
FAO (1990) Mid-term Review of FAO Intercountry Program for the Development and Application of Integrated
Pest Control in Rice in South and South-East Asia. Mission Report, Food and Agriculture Organization,
Rome.
FAO (1995) Intercountry Programme for the Development and Application of Integrated Pest Control in Rice in
South and South-East Asia. FAO Plant Protection Service, Rome, Italy.
FAO (2001) World Review of the State of Food and Agriculture. Food and Agriculture Organization of the United
Nations, Rome, Italy, 295 pp.
Frisbie, R.E. and Adkisson, P.C. (1985a) Integrated Pest Management on Major Agricultural Systems. Texas
A&M University, College Station, Texas.
Frisbie, R.E. and Adkisson, P.L. (1985b) IPM: definitions and current status in US agriculture. In: Hoy,
M.A. and Herzog, D.C. (eds) Biological Control in Agricultural IPM Systems. Academic Press,
Orlando, Florida, pp. 41–51.
Frisbie, R.E. and Smith, J.W. Jr (1991) Biologically intensive integrated pest management: the future. In:
Menn, J.J. and Steinhauer, A.L. (eds) Progress and Perspectives for the 21st Century. Entomological
Society of America, Lanham, Maryland, pp. 151–164.
Geier, P.W. (1966) Management of insect pests. Annual Review of Entomology 11, 471–490.
Geier, P.W. and Clark, L.R. (1961) An ecological approach to pest control. In: Proceedings of the Eighth
Technical Meeting, 1960, Warsaw, Poland. International Union for Conservation of Nature and Natural
Resources, Warsaw, pp. 10–18.
Hall, R. (1995) Challenges and prospects of integrated pest management. In: Reuveni, R. (ed.) Novel
Approaches to Integrated Pest Management. Lewis Publishers, Boca Raton, Florida, pp. 1–19.
Haverskort, B., van der Kamp, J. and Waters-Bayer, A. (1991) Joining Farmers Experiments – Experiences in
Participatory Technology Development. Intermediate Technology Publications, London.
Heinrichs, E.A. (1998) IPM in the 21st century: challenges and opportunities. In: Dhaliwal, G.S. and
Heinrichs, E.A. (eds) Critical Issues in Insect Pest Management. Commonwealth Publishers, New
Delhi, pp. 267–276.
Hinrichsen, D. and Robey, B. (2000) Population and the Environment: the Global Challenge. Population
Reports, Series M, No. 5, Johns Hopkins University School of Public Health, Baltimore, Maryland,
31 pp.
Hoskins, W.M., Borden, A.D. and Michellbacher, A.E. (1939) Recommendations for a more discriminating
use of insecticides. In: Proceedings of the 6th Pacific Science Congress, Vol. 5, pp. 119–123.
Jiggins, J. (1996) Women and the re-making of civil society. Forest Trees and People Newsletter 30, 18–22.
Kamp, K., Gregory, R. and Chowhan, G. (1993) Fish cutting pesticide use. LEISA 9, 22–23.
Kenmore, P. (1997) A perspective on IPM. LEISA 13, 8–9.
01IntpestManCh1.QXD 14/4/04 2:24 pm Page 19

IPM: Retrospect and Prospect 19

Kogan, M. (1998) Integrated pest management: historical perspectives and contemporary developments.
Annual Review of Entomology 43, 243–270.
Luckman, W.H. and Metcalf, R.L. (1994) The pest management concept. In: Metcalf, R.L. and Luckman,
W.H. (eds) Introduction to Insect Pest Management. John Wiley & Sons, New York, pp. 1–34.
McNeal, C.D. Jr (1988) Integrated pest management. In: Pesticides: Risks, Management, Alternatives. Virginia
Water Resources Research Center, Blacksburg, Virginia, pp. 9–12.
Matteson, P.C., Gallagher, K.D. and Kenmore, P.E. (1994) Extension of integrated pest management for
planthoppers in Asian irrigated rice: empowering the user. In: Denno, R.F. and Perfect, T.J. (eds)
Planthoppers: Their Ecology and Management. Chapman & Hall, London, pp. 656–685.
Meerman, F., Bruinsma, W., Vanhuis, A. and Terweel, P. (1997) Integrated pest management: smallholders
fight back with IPM. LEISA 13, 4–5.
Metcalf, R.L. (1980) Changing role of insecticides in crop protection. Annual Review of Entomology 25,
215–226.
Michelbacher, A.E. and Bacon, O.G. (1952) Walnut insect and spider mite control in Northern California.
Journal of Economic Entomology 45, 1020–1027.
NAS (1969) Principles of Plant and Animal Pest Control, Vol. 3. Insect Management and Control. National Academy
of Sciences, Washington, DC.
NDRC (1989) Intolerable Risk: Pesticides in Our Children’s Food. Natural Resource Defense Council,
Washington, DC.
NRC (1996) Ecologically Based Pest Management: New Solutions for a New Century. National Academy Press,
Washington, DC, 144 pp.
NRI (1992) Integrated Pest Management in Developing Countries: Experience and Prospects. National
Resources Institute, Chatham, UK.
Oerke, E.-C., Dehne, H.-W., Schonbeack, F. and Weber, A. (1994) Crop Production and Crop Protection.
Elsevier Science, Amsterdam, 808 pp.
Ooi, P.A.C. (2000) Present status of IPM in the Asian region. In: Farmer-led Integrated Pest Management.
Asian Productivity Organization, Tokyo, pp. 21–29.
Pedigo, L.P. (1991) Entomology and Pest Management. Macmillan, New York.
Perkins, J.H. (1980) The quest for innovation in agricultural entomology. In: Pimentel, D. and Perkins,
J.H. (eds) Pest Control: Cultural and Environmental Aspects. AAAS Selected Symposium 43, Westview
Press, Boulder, Colorado, pp. 23–80.
Pradhan, S. (1983) Agricultural Entomology and Pest Control. Indian Council of Agricultural Research, New
Delhi.
Quinghua, Z. (1995) Careful control: IPM in China. Ceres 27, 12–13.
Rajak, R.L., Diurakar, M.C. and Mishra, M.P. (1997) National IPM programme in India. Pesticides
Information 23, 23–26.
Reichelderfer, K.H., Carlson, G.A. and Norton, G.A. (1984) Economic Guidelines for Crop Pest Control. FAO
Plant Production and Protection Paper 58, Food and Agriculture Organization of the United
Nations, Rome.
Ruesink, W.G. and Onstad, D.W. (1994) Systems analysis and modelling in pest management. In: Metcalf,
R.L. and Luckman, W.H. (eds) Introduction to Insect Pest Management. John Wiley & Sons, New York,
pp. 393–420.
Smith, R.F. (1978) History and complexity of integrated pest management. In: Smith, E.H. and Pimetel, D.
(eds) Pest Control Strategies. Academic Press, New York, pp. 41–53.
Smith, R.F. and Allen, W.W. (1954) Insect control and the balance of nature. Scientific American 190, 38–92.
Smith, R.F. and van den Bosch, R. (1967) Integrated control. In: Kilgore, W.W. and Doutt, R.L. (eds) Pest
Control: Biological, Physical and Selected Chemical Methods. Academic Press, New York, pp. 295–340.
Smith, R.F., Apple, J.L. and Bottrell, D.G. (1976) The origins of integrated pest management concepts for
agricultural crops. In: Apple, J.L. and Smith, R.F. (eds) Integrated Pest Management. Plenum Press,
New York, pp. 1–16.
Sorenson, A.A. (1994) Proceedings Integrated Pest Management Forum, Arlington, Virginia. American
Farmland Trust, Dekalb, Illinois.
Stern, V.M., Smith, R.F., van den Bosch, R. and Hagen, K.S. (1959) The integration of chemical and biolog-
ical control of the spotted lucerne aphid. 1. The integrated control concept. Hilgardia 29, 81–101.
Tarlock, A.D. (1980) Legal aspects of integrated pest management. In: Pimentel, D. and Perkins, J.H. (eds)
Pest Control: Cultural and Environmental Aspects. AAAS Selected Symposium 43, Westview Press,
Boulder, Colorado, pp. 217–236.
01IntpestManCh1.QXD 14/4/04 2:24 pm Page 20

20 G.S. Dhaliwal et al.

Van de Fliert, E. (1993) Integrated Pest Mangement: Farmers’ Field Schools Generate Sustainable Practices.
Wageningen Agricultural University, Wageningen, The Netherlands.
Van de Fliert, E. (1998) Integrated pest management: springboard to sustainable agriculture. In: Dhaliwal,
G.S. and Heinrichs, E.A. (eds) Critical Issues in Insect Pest Management. Commonwealth Publishers,
New Delhi, pp. 250–266.
Van Veldhuizen, L. and Hiemstra, W. (1993) Cutting back: cure or prevent. ILEIA Newsletter 9, 3–4.
02IntpestManCh2.QXD 14/4/04 2:24 pm Page 21

2 Cultural Practices: Springboard to IPM

Waheed I. Bajwa and Marcos Kogan

Department of Entomology and Integrated Plant Protection Center,
Oregon State University, Corvallis, OR 97331, USA
E-mail: [email protected]; [email protected]

Introduction economically grown under tropical or sub-

tropical conditions, and the reverse is true
Each agricultural region of the world grows for tropical tree crops, such as citrus, coffee,
a set of crops, the basic elements of agro- pawpaw, cocoa and coconuts. Average
ecosystems, and uses unique technological annual temperatures and photoperiods are
procedures that in combination constitute the key climatic factors. Where irrigation is
the typical cropping system of the region. not feasible, precipitation is another climatic
Cropping systems evolved under the pres- determinant of cropping-systems evolution.
sure of the region’s prevalent agroecological Not far behind the climatic and edaphic con-
conditions and the sociocultural and eco- ditions in shaping the nature of regional
nomic characteristics of its human popula- cropping systems are the pest complexes that
tion. Cropping systems range from attack the otherwise regionally adapted
extremely monotonous, such as the huge crops. Throughout the evolution of cropping
small-grain monocropping systems in the systems, the presence of weeds, plant
traditional bread baskets of the world, to the pathogens and arthropod pests has led to the
highly diversified mixed or intercropping adoption of procedures that in the aggregate
systems that prevail in many subsistence are defined as cultural controls. Cultural
agricultural production systems in the less controls, therefore, represent a fundamental
developed countries of Central and South integrated pest management (IPM) tactic
America, Africa and Asia. In the hierarchy of even if the adoption of the practices, as
environmental forces that shape a regional driven by biotic factors of the environment,
cropping system, climate and soil must be at may remain unrecognized by growers. One
the top. Soil fertility and texture have shaped of the dilemmas in maximizing the efficiency
the nature of cropping systems throughout of cultural controls in IPM, however, is that
history, but current knowledge and availabil- seldom, if ever, are cropping systems opti-
ity of adequate amendments have allowed mized to cope with pest problems. Usually
farmers to correct soil deficiencies in many economic determinants take absolute prece-
parts of the world. Climate, however, is not dence over all other factors. For a long time,
amenable to large-scale correction; therefore, maize-growers in the Midwestern USA knew
crop mixes available for local production that they could reduce the impact of root-
systems are usually limited by climatic fac- worm, Diabrotica spp., attacks if they rotated
tors. For instance, apples, pears, cherries and maize with soybean. Continuous planting of
other temperate-zone fruits cannot be maize, however, was more profitable for a
© CAB International 2004. Integrated Pest Management: Potential, Constraints and Challenges
(eds O. Koul, G.S. Dhaliwal and G.W. Cuperus) 21
02IntpestManCh2.QXD 14/4/04 2:24 pm Page 22

22 W.I. Bajwa and M. Kogan

large segment of the grower population that essentially all pests. Cultural control, when
raised pigs or dairy cattle. The economic well planned and integrated into an IPM sys-
consideration often prevailed over the IPM tem, can provide economic control of many
consideration. insect pests, plant pathogens and weeds and
The main focus of cultural controls in IPM greatly reduce reliance on pesticides.
is to explore and enhance synergies of eco- The ecology of the crop, including the
logical processes that limit pest invasion and surrounding vegetation, determines the
population growth in an agroecosystem. IPM potential for the proliferation of pests and
systems are generally developed and imple- the complement of the pests’ natural ene-
mented in a stepwise manner and the first mies. In an optimal cropping system, pro-
step requires the full understanding of the ducers strive to provide the best conditions
cropping system that is targeted for manage- for crop plants to express their yield poten-
ment. Cultural-control approaches that best tial and to create adverse conditions for the
fit the nature of the cropping system form potential pests and the most favourable con-
the foundation upon which the other IPM ditions for the pest’s natural enemies to
tactics will be implemented. Use of cultural flourish. Many stages in crop husbandry
practices for pest control is one of the oldest may provide such enhancements, and each
and most effective pest-management tactics. of these stages should be considered in
Cultural-control tactics are agronomic prac- designing and implementing an IPM pro-
tices primarily aimed at the prevention and gramme. It is possible often to identify
reduction of pest outbreaks by increasing underlying weaknesses in the ecosystem and
pest mortality or reducing its rates of in the prevailing agronomic practices that
increase, dispersal and overall damage have allowed organisms to reach pest status.
potential. At present, most successful IPM Identification of these weaknesses requires a
programmes for major annual and perennial thorough knowledge of the bionomics,
crops are based on a combination of cultural behaviour and ecology of the pest in relation
control and biological control, coupled with to the crop and its surroundings. Such
moderate use of chemical pesticides. knowledge is essential for developing alter-
Under the label ‘cultural control’ are native cultural practices that limit the poten-
included cropping-systems practices related tial of an organism to reach pest status. If
to the crop ecology with an impact on crop/ these practices are cost-effective and can be
pest interactions and practices that have a integrated easily with other production prac-
physical or mechanical nature. Practices tices, they are usually readily adopted by
related to crop ecology include crop rota- growers. In many parts of the world, good
tions, row spacing (for row crops), planting cultural-control methods have become stable
dates (for annual crops), inter- and mixed farming practices that serve multiple pur-
cropping, strip cropping and cover cropping, poses and help maintain agroecosystem sus-
among others. Practices that have an effect on tainability.
the pests because of direct physical or Agronomic practices may have a positive,
mechanical impact include ploughing, disc- negative or neutral impact on a pest and its
harrowing, cultivating, burning, flooding and natural enemies. Analysis of these impacts
pruning, among others. So cultural controls provides a basis for the development of
operate either through physical forces that cultural-control programmes. Cultural-control
suppress or limit pest-population growth or practices fall into three main categories: pre-
by promoting conditions within the agro- vention, avoidance and suppression (Table
ecosystem that are detrimental to the pest but 2.1). Individually or together, these practices
favourable to its natural enemies. Therefore, improve the ability of a crop to withstand
conserving pests’ natural enemies and pro- pest attack, make the crop less suitable for
moting their effectiveness are essential parts the pest or make it more suitable for natural
of cultural-control programmes. The appro- enemies. Some of the practices involve many
priate use of cultural-control practices can aspects of crop management, such as the use
reduce the damage potential to crops of of pest-free seed, good sanitation and the
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Cultural Practices 23

Table 2.1. Use of various cultural control practices for different categories of pests.

Cultural control strategy/tactics Insects Weeds Diseases Nematodes

Prevention/avoidance
Clean seed and planting material X X X X
Selection of well-adapted cultivars X X X
(including pest-resistant cultivars)
Optimal crop nutrition X X X X
Optimal water management (timing and X X X X
proper amount of irrigation)
General sanitation of farm equipment X X X X
(cleaning of cultivating and harvesting
equipment)
Soil tillage X X X X
Crop rotation X X X X
Selection of planting and harvesting dates X X X X
Trap crops X
Suppression
Adjustment of seeding rates and optimal X X X
row spacing (optimal plant density and
fast canopy closure)
Cultivation or hand hoeing (mainly for weed X
suppression)
Habitat management for natural-enemy X X X
enhancement (hedgerows, alternative
crops, cover crops, mulches)
Crop diversification/mixed cropping X X
Soil tillage (reduction of seasonal carry-over) X X
Destruction of alternative hosts and X X X
volunteer-crop plants

destruction of plant residue to limit the strategy and thus are highly desirable for the
spread of pests; provision of optimum grow- management of all pests. Variety selection is
ing conditions to minimize stress on the a key cultural practice and selection of resis-
crop; tillage practices that disrupt the insect’s tant varieties is a major IPM tactic. Most
life cycle and destroy crop residue; early or texts on IPM, however, deal with host-plant
late planting and harvest dates to promote resistance as a separate tactic, not under cul-
phenological asynchronies between the crop tural controls.
and the pests; and crop rotations that include
non-susceptible crops. In addition, several
specific practices fall under the concept of
Characteristics of Cultural-control
habitat management, where practices are
Practices
implemented to render the crop environment
less favourable for the pests or more
The following features characterize cultural-
favourable for the pests’ natural enemies.
control practices within an IPM context:
Intercropping, mixed cropping, hedge-vege-
tation management, trap cropping, cover ● Cultural-control methods are simple
cropping and certain other methods help modifications or adaptations of regular
divert pests from the main crop and promote farm operations. The added cost of their
the activities of beneficials (Landis et al., incorporation into pest-management sys-
2000). These practices are generally compati- tems is minimal in most cases. They are
ble among themselves and with other pest- often the only control measures economi-
control tactics within a comprehensive IPM cally feasible for low-value crops.
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24 W.I. Bajwa and M. Kogan

● Cultural-control practices generally pro- life cycle, pest–crop interactions or the

duce no, or negligible, undesirable eco- ‘flaws’ in agronomic practice that have
logical consequences. allowed organisms to reach pest status.
● Cultural control is primarily aimed at the ● An area-wide deployment of cultural-
prevention and reduction of pest out- control practices is essential for the effec-
breaks. Its effectiveness is dependent on tiveness of the practice in IPM. If
long-term, careful planning. The objective deployed in only a small area, a mobile
is either to reduce pest numbers below arthropod pest would merely move from
economic injury levels or to keep pests at surrounding areas; effective use of some
a level that allows natural or biological of these practices requires cooperation
control to take effect. among farmers within communities.
● Results of cultural practices as applied to ● Cultural-control methods are often pest-,
arthropods are often difficult to quantify, crop- and region-specific. Care should be
primarily because ecological relationships exercised in transferring tactics to a
within crop systems are poorly under- region with markedly different agroeco-
stood and because baseline data on pest logical conditions.
abundance in the absence of cultural con-
trols are not available. The effects of phys-
ical methods for weed control and crop Cultural Practices and Sustainable IPM
rotations for disease control are often Systems
dramatic and very well documented.
● Cultural-control tactics are an effective Optimizing plant health and the biological
means of pest control. They do not result diversity of the farm system is the founda-
in total elimination of the pest, thus tion of effective cultural controls. Healthy
allowing for conservation of beneficial and vigorous crops are inherently tolerant
insects. In the USA biological control of of pests or their effects. Decreased biodiver-
musk thistle is an excellent example (Kok, sity tends to result in unstable agroecosys-
2001). tems prone to recurrent pest outbreaks,
● Most cultural practices indirectly affect reduced soil health and gradually declining
arthropod pests. They are relatively slow productivity. Systems high in biodiversity
acting and thus cannot resolve a pest out- tend to be more dynamically stable. Such
break. They are important, however, in systems provide more checks and balances
minimizing pest damage by preventing to component species, thus helping prevent
pest build-up, rather than relieving an any given species from overwhelming the
already existing pest problem. system. Most cultural-control tactics lower
● Cultural-control methods make cropping pest numbers in an ecosystem, and some
systems less friendly to the establishment may affect the carrying capacity of the
and proliferation of pest populations. ecosystem. These impacts tend to accumu-
While they are designed to have positive late over time to produce sustained sup-
effects on farm ecology and pest manage- pression of pest populations, keeping them
ment, negative impacts may also result below economic injury levels (Fig. 2.1).
due to variations in weather, changes in Cultural-control practices, therefore, must
crop management or perturbations in be a continuous component of an IPM pro-
agroecosystems. gramme so as to have a positive impact on
● Timing is critical to the success of many all other practices by reducing overall levels
cultural controls; accordingly, the imple- of pest populations (MacHardy, 2000).
mentation of cultural-control tactics Cultural controls tend to favour natural bio-
requires thorough knowledge of pest logical control directly by providing shelter
ecology and its interaction with the crop- and nectar for predators and parasitoids or
ping system. In designing cultural con- indirectly by reducing insecticide use. It is
trol, special attention is given to the level and integration of both cultural
recognizing the ‘weak link’ in the pest’s and biological control that determine the
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Cultural Practices 25

Effect of cultural-practice changes on EIL Cultural-control Practices

Table 2.1 lists the major cultural practices

Pest population

most commonly recommended for the con-

trol of weeds, plant pathogens and arthro-
EIL pods. These are discussed in some detail in
the following sections. Comprehensive
reviews of the major cultural-control meth-
ods are available in the literature. Variety
selection and preference for adapted culti-
vars that incorporate resistance to arthro-
Time
pods and diseases are key components of the
Fig. 2.1. Hypothetical effect of a change in cultural decision-making process in crop manage-
practices that lowers the general equilibrium ment. Host-plant resistance, however, is such
position of a pest population, thus maintaining the an important component of IPM systems
population below the economic injury level (EIL). that it deserves special treatment in most
texts. Detailed discussions of both traditional
and genetically engineered plant resistance
nature and amount of other control actions are offered in Chapters 6 and 7.
to be taken at the farm level.

Sanitation
Cultural-control Practices and
Contemporary Production Systems Sanitation involves removing and destroying
overwintering sites, breeding refuges of
The introduction of the concept of IPM in the arthropod pests and substrates for pathogen
late 1960s shifted the emphasis in pest con- inoculum. Sanitation also prevents new pests
trol from a single-tactic, chemically based to from becoming established on the farm. This
a multitactic, ecologically based or bio- cultural-control method has been particu-
intensive system (Frisbie and Smith, 1991). larly useful for horticultural and tree-fruit
Since the early days of IPM, cultural controls crops. Fruit, twig and branch as well as root-
have been considered a first line of defence crop pests can be affected by carefully con-
in many pest-management systems. Cultural ceived sanitation procedures. The most
practices alone may not give completely sat- common means of field sanitation is destruc-
isfactory pest control but, within an IPM sys- tion of crop residues by shredding and
tem, they provide the matrix upon which ploughing, separately or in combination.
other IPM tactics are deployed and often This process not only kills some pests
help reduce dependency on chemical pesti- directly but also speeds up natural rotting of
cides (MacHardy, 2000). Ecologically based the residues thus removing them as food or
production systems, including organic farm- shelter source.
ing (Brumfield and Ogier, 2000), total-habitat Removing crop residues can reduce the
management (Prokopy, 1994; Kogan and carry-over of pests from one season to the
Bajwa, 2001) and integrated fruit and crop next. After harvest, destroying the stubble of
production (Sansavini, 1997), take maximum cotton, maize and sugarcane is an important
advantage of farming practices that promote measure in the control of cotton bollworm,
plant health and pests’ natural controls and boll-weevil and pink bollworm in cotton,
allow crops to escape or tolerate pest injury. various corn borers and sugarcane borers
Cultural control is a cornerstone for most (All, 1999). The practice of grazing by live-
biointensive IPM programmes, where each stock of cotton fields after last picking is
component complements and often aug- effective in reducing hibernating loads of
ments the effects of others (ecological syner- pink bollworm and American bollworm in
gism) (Fig. 2.2). many regions (Bajwa, 1988). In the USA,
02IntpestManCh2.QXD 5/5/04 2:30 pm Page 26

26 W.I. Bajwa and M. Kogan

Chemointensive crop protection

0 100

Chemical
control
High
(non-
selective)

Negative environmental impacts

Biorational Moderate
Control tactics

Biological/
natural
control Low

Cultural
control/ Negligible
plant
resistance

100 50 25 6.25 0

Biointensive crop protection (IPM)

Fig. 2.2. Graphic representation of two opposing strategies of pest control. Triangle at left: biointensive pest
control system (= IPM). These systems are integrative, stable and environmentally benign, with little reliance
on broad-spectrum pesticides. The contribution of each control tactic to the stability of the system is
represented as a proportion of the area of the triangle sector (or trapezoid) corresponding to that tactic. The
various tactics complement and often potentiate each other (ecological synergism). Triangle at the right:
chemointensive pest-control systems, on the other hand, are unstable (the ecological base is weak); control
methods other than pesticides are not emphasized or their effects are masked by the antagonistic effects of
chemical pesticides.

sheep grazing wheat stubble during the peach borer, Synanthedon exitiosa (Say), and
autumn and autumn/spring gave an effec- the lesser peach borer, Synanthedon pictipes
tive control of wheat-stem sawfly, Cephus (Grote and Robinson) (Cox and Atkins,
cinctus Norton (Hatfield et al., 1999). In rice, 1964). Collecting and using dropped fruit or
destroying stubble and off-season sprouts else destroying them reduces the popula-
reduces populations of the leafhopper, tions of some important direct pests, such as
Nephotettix impicticeps Ishihara, and the plum curculio, Conotrachelus nenuphar
whitebacked planthopper, Sogatella furcifera (Herbst) (All, 1999), the codling moth, Cydia
(Horvath) (Bajwa, 1988). In sugarcane and pomonella (Linnaeus) (Prokopy, 2001), the
maize, destruction of cane trash and maize false codling moth, Cryptophlebia leucotreta
stalks in the winter significantly reduces the (Meyrick), and many species of fruit flies
hibernating loads of several stem borers (Bajwa, 1989; Stoll, 2000).
(Capinera, 2001). Other sanitation techniques include using
Removal of fallen fruit from orchards and pest-free seeds or transplants and decontam-
destruction of tree prunings are useful in inating equipment, animals and other
reducing insect pests and plant-disease sources of food and shelter. Insects in cut-
agents that overwinter in these materials. tings or roots used in the vegetative propa-
Destruction of prunings can control the gation of crops can initiate infestations.
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Cultural Practices 27

Seeding equipment should be clean and free borers, Tryporyza incertulas (Walker) and
of pests. Ideally, all farm machines should be Chilo suppressalis (Walker); and cotton boll-
cleaned before going from one field to worms, Pectinophora gossypiella (Saunders)
another. Such procedures are essential to pre- and Earias insulana (Boisduval) (Bajwa, 1988).
vent the spread of soil-inhabiting pests, such In the case of the European corn borer, the
as the grape phylloxera in vineyards of ploughing of stubble may result in a 90%
California and Oregon, in the USA (Hellman reduction of hibernating larvae (Horn, 1988).
and Watson, 2000). In the tropics, the use of Shallow autumn tillage may provide up to
clean planting material reduces banana wee- 90% sawfly control (Steffey et al., 1992). If
vil, Cosmopolites sordidus (Germar), infesta- only spring tillage operations are performed,
tion by up to 80% (Stoll, 2000). approximately 25% of larvae may be
destroyed, depending upon the tillage
implements used (Steffey et al., 1992).
Soil tillage Reduced- or conservation-tillage practices
may increase soil surface residues. These
While tillage may be a part of field sanita- residues may have an impact on populations
tion, it can be an effective direct means of of certain pests. The presence of such
pest control by itself. Tilling the soil destroys residues repels the colonizing of a field by
life-cycle stages that occur in the soil or in greenbugs, Schizaphis graminum (Rondani) in
crop residues. It destroys pests by mechani- wheat and sorghum (Burton et al., 1987), but
cal action, starvation through debris destruc- attracts black cutworms in maize (Steffey et
tion, desiccation and exposure to predators al., 1992). Greenbugs prefer fields with more
or adverse environmental conditions. Tillage bare ground visible, while black cutworm
may modify the soil microclimate, which prefers crop residue for oviposition. Reduced-
will influence pest behaviour and plant tillage systems may have higher soil mois-
growth. Often tillage timing and depth are ture and be slower to warm up in the spring,
the major considerations for the manage- thus reducing crop growth. This may add to
ment of soil-inhabiting animal pests and crit- damage from soil pests (wireworms, white
ical factors in weed management. Timing is grubs and other seed and seedling pests) by
usually determined when pests are in an increasing their feeding time on young
immobile stage (pupation or dormancy), and plants (Steffey et al., 1992).
depth is recommended by the location of this Biological control agents are often
stage in soil. Generally, tillage may be con- affected by tillage practices. Discing or har-
ducted in the autumn or early winter and in rowing has fewer negative impacts on the
the spring before planting. parasitoid population than does ploughing
Soil-inhabiting pests such as rootworms, (Herzog and Funderburk, 1986). Parasitoids
white grubs, wireworms and the overwinter- of the cereal leaf beetle, Oulema melanopus
ing larvae and pupae of Lepidoptera and (Linnaeus), can be severely affected by
Coleoptera may be exposed to desiccation or tillage operations, which has little effect on
bird predation by ploughing. The pests that the pest (Pedigo, 2002). Reduced-tillage sys-
feed on stubble after harvest may starve if tems may increase populations of various
the ground is tilled (Speight et al., 1999). predatory arthropods by increasing popula-
Deep ploughing after harvest buries infested tions of their prey, such as other insects,
plant parts and stubble and destroys the lar- mites and organisms that feed on decaying
vae of pests such as army worm, Pseudaletia organic matter. Increased levels of predatory
unipunctata (Harworth) (Capinera, 2001); insects and predation on black cutworms,
wheat-stem sawfly, C. cinctus; maize ear- Agrotis ipsilon (Hufnagel), and maize ear-
worm, Helicoverpa zea (Boddie); European worm, H. zea, have been observed in
corn borer, Ostrinia nubilalis (Hübner); soy- reduced-tillage systems (Stinner and House,
bean stem borer, Dectes texanus LeConte; 1990).
grape berry moth, Endopiza viteana Clemens Tillage is not always advantageous and
(Herzog and Funderburk, 1986); rice stem can actually aggravate some pest problems.
02IntpestManCh2.QXD 14/4/04 2:24 pm Page 28

28 W.I. Bajwa and M. Kogan

For example, in some areas the soil surface (Lidell and Schuster, 1990); potato tuber-
tends to form a crust; keeping this crust worm, Phthorimaea operculella (Zeller); potato
intact can inhibit weed germination and/or aphid, Macrosiphum euphorbiae (Thomas)
prevent the penetration of soil-inhabiting (Capinera, 2001); cutworms, Agrotis spp.
pests (Norris et al., 2003). Serious side effects (van den Berg et al., 1998); and the wheat curl
of tillage are loss of organic matter, espe- mite, Eriophyes tosichella (Keifer) (Buntin et
cially in warm soils, and accelerated loss of al., 1991).
soil to wind and water erosion if the soil is
left bare for an extended period.
Maintaining and improving plant health

Management of alternative hosts The primary goal of agricultural production

is to maximize the yield of high-quality pro-
Eliminating plants that can serve as alterna- duce. Healthy plants are essential for opti-
tive hosts when the crop is not present can mal agricultural production. Stressed plants,
suppress overwintering populations and including those with nutritionally induced
reduce the growth rate of many pest popula- low vigour, are often more susceptible to
tions. Vegetation serving as the alternative pest attack (Stoll, 1988). Vigorous plants are
host may occur within the crop field and/or better able to tolerate pests, as well as pro-
in surrounding areas. Whiteflies use many ducing high yields. In most crops, yield
broad-leaved weeds as alternative hosts losses to a given degree of pest injury vary
when suitable crops are not present (Norris considerably depending on the vigour of the
et al., 2003). Johnson grass is an excellent host plants. However, there are documented
of sorghum midge (Pedigo, 2002). Significant instances of modern fertilizers and irrigation
reductions of these pests have been reported increasing vulnerability to certain pests (dis-
where weed destruction by burning and cussed below). Excessive nutrients (particu-
other means was used. Many vegetable larly nitrogen) and relative nutrient balance
pests, such as squash- and stinkbugs, over- (ratios of nutrients) in soils affect the pest
winter in crop debris and plant cover at the response to plants. Imbalances in the soil can
edge of plantings. Elimination of these hiber- make a plant more attractive to insect pests,
nating habitats can significantly reduce infes- less able to recover from pest damage or
tations in squash, beans, cabbage and other more susceptible to secondary infections by
vegetables (Capinera, 2001). Destruction of plant pathogens (Daane et al., 1995; Phelan,
alternative hosts may also require careful 1997).
scrutiny as it may eliminate an important Cultural practices, such as proper irriga-
habitat for beneficial insects. tion and drainage, fertilization, row spacing
Volunteer plants of a crop that remain in and weed control, significantly influence the
parts of a field after harvest may be a poten- vigour of the crop and consequently the
tial source of pest carry-over. These plants amount of pest damage. Undernourished
may harbour a large number of insect pests plants, because of their pale or yellowish
at times when pest presence would other- appearance, are often more attractive to colo-
wise be impossible. The destruction of these nizing aphids (Ferro, 1996). In some
volunteer plants is particularly important instances, however, the vigorous growth of
when crop rotation is practised to eliminate plants may attract or enhance the develop-
pests. For example, volunteer maize in soy- ment of many pest species. For example,
bean fields should be removed to prevent leafhoppers and Spodoptera littoralis
maize rootworm adults, Diabrotica spp., from (Boisduval) have been most abundant on rice
laying eggs and producing larvae that would fertilized with high rates of nitrogen (Stoll,
colonize maize the following season 2000). Excessive nitrogen may increase the
(Goodwin, 1985). Destruction of volunteer incidence of Tetranychus mites (Stoll, 2000),
plants is also recommended for the suppres- fungal diseases and sucking insects (Flint
sion of other pests, such as Hessian fly and Gouveia, 2001) on an array of crops.
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Cultural Practices 29

Succulent cotton growth attracts higher pop- pressed by frequent overhead irrigation of
ulations of the cotton aphid, Aphis gossypii potatoes, head cabbage (McHugh and Foster,
(Glover), cotton fleahopper, Pseudatamoscelis 1995) and apple trees (Knight, 1998), respec-
seriatus (Reuter), and cotton bollworm, H. zea tively. In California, sprinkler irrigation has
(Herzog and Funderburk, 1986). Increasing been observed to suppress spider mites
levels of soil fertility delay crop maturity in (Flint and Gouveia, 2001). Flooding is fre-
cotton, thereby reducing the potential for quently used to reduce populations of sugar-
escape from pest injury (Anon., 1996). cane (Cherry, 1987; Deren et al., 1993) and
Increases in soil fertility of wheat result in vegetable pests (Capinera, 2001). Paddy rice
increased wheat-stem sawfly injury due to in the Orient has a complex biota (Kiritani,
the preference of ovipositing females for 2000). The biological impact of flooding in
large succulent wheat plants (Morrill and the rice paddy is a critical factor in the eco-
Kushnak, 1996). nomic production of rice in vast regions of
Good soils can improve yields and pro- the world. Nevertheless, effective use of this
duce robust crops that are less vulnerable to technique depends on factors such as flood
pests. Soils used for years of continuous susceptibility and the stage of the pest
farming often require heavy fertilizer appli- species, the duration of flooding, water tem-
cation to produce high yields. Soil quality perature and, perhaps more importantly, the
can be maintained and enhanced in many availability and cost of water.
ways, including incorporation of animal
waste (manure), living plants or plant debris
(compost). The addition of organic matter to Timing of planting and harvest (disrupting
soil is known to result in the suppression of a crop–pest phenological synchrony)
wide range of soil-borne plant pathogens
(Cook and Baker, 1983). Application of Plant phenology can be manipulated to dis-
manure to maize fields increases the preda- rupt synchronization with the phenology of
tory efficiency of mesostigmatid mites on the major pests. It is sometimes possible to
maize rootworm larvae (Allee and Davis, alter the timing of crop development by
1996). modifying regular cultural practices and
Water management can be used to grow thus to effect a substantial reduction in dam-
more vigorous plants and thereby reduce age. This can be achieved by modifying
losses. Excessive irrigation or frequent irriga- planting time, by either delaying or advanc-
tions may favour the spread and develop- ing planting dates. In some cases, early-
ment of many diseases and should be planted crops are less likely to suffer from
avoided. Cotton is severely stressed by inad- pest outbreaks as they become well estab-
equate irrigation, but excessive water may lished before pests appear. They are either
result in overly lush plants with higher less palatable to herbivores or tolerant of
insect densities and increased vulnerability higher pest densities without suffering much
to pest damage (Horn, 1988). Winter irriga- effect on yield. Early harvest often produces
tion may reduce populations of overwinter- phenological asynchronies capable of dis-
ing pink bollworms by up to 50–70% rupting a pest’s life cycle, allowing harvest
(Bariola, 1983; Beasley, 1992). Cotton boll- of the crop before the damaging state occurs.
worms are attracted to succulent, rank-grow- Planting early-maturing varieties often
ing cotton plants; therefore, keeping water, allows fields to escape infestations by late-
fertilizer and plant density at recommended season pests.
levels is important in order to avoid rank Early-planted maize is far less susceptible
growth (Anon., 1999). Sprinkler irrigation to maize earworm and stem borer, Diatraea
has been effective in suppressing certain grandiosella Dyar, damage than late-planted
foliage-feeding insects by a washing and crops. The female D. grandiosella tends to lay
drowning action. The diamondback moth, fewer eggs on more mature plants and the
Plutella xylostella (Linnaeus), and codling plants have already passed their critical
moth, C. pomonella, are effectively sup- growth stage before significant numbers of
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30 W.I. Bajwa and M. Kogan

larvae begin to feed (Herzog and planting the crop after the spring migration
Funderburk, 1986). In addition, early- of the beet leafhopper, a vector for the dis-
planted maize can be harvested before many ease (Norris et al., 2003).
fully grown pre-diapause larvae have gir- Sometimes, it is possible to reduce pest
dled the mature plants and caused yield populations or their damage by adjusting
losses through lodging of the plants (Roth et harvest time. As a general rule, crops should
al., 1995). The early planting of maize in East be harvested at the earliest possible date.
Africa is known to reduce problems with Early harvesting of sorghum removes a large
both maize leafhopper, Cicadulina mbila proportion of stem-borer populations; there-
(Naude), and stalk borer, Papaipema nebris fore, the crop should generally be harvested
(Guenee) (Bajwa and Schaefers, 1998). The immediately after it attains physiological
practice is so effective that no additional con- maturity (Omolo and Reddy, 1983). In
trol measures are generally needed. Earlier- lucerne, damage from the potato leafhopper,
planted tomatoes in the western USA are far Empoasca fabae (Harris) and lucerne weevil,
less likely to be infested by the tomato fruit- Hypera postica (Gyllenhal), can be minimized
worm, H. zea, than those planted later in the by early clipping at the early bloom or late
season (Anon., 1998). Early-season varieties bud stage (Steffy et al., 1994). The lack of
of cotton avoid most boll-weevil and boll- food, and hot, dry conditions after harvest
worm populations, and early-maturing soy- can cause considerable mortality to the
bean cultivars sufficiently evade bean-leaf leafhopper and weevil larvae. Early planting
beetles compared with standard varieties reduces the loss of yield from maize ears that
(Horn, 1988). Early-planted groundnuts drop early because of European corn-borer
avoid aphid damage in tropical Africa tunnelling. However, early-harvested maize
(Bajwa and Schaefers, 1998). Early planting usually has a higher moisture content and
of rice reduces or eliminates many insect- must be dried before it is stored. Early sweet
related problems (Speight et al., 1999). This potato planting and harvesting is useful in
effect may not be a general rule for all pests white-fringed beetle, Naupactus spp., man-
and ecological situations. Early rice trans- agement programmes. These pests cause
planting in South Korea may increase popu- damage to roots late in the season, therefore,
lations of striped rice borer, C. suppressalis harvesting the crop before larvae reach suffi-
(Ma and Lee, 1996). cient size to cause serious feeding damage
Late planting of soybean interferes with reduces the proportion of damaged and
the colonization patterns of the soybean unmarketable roots at harvest (Zehnder et
thrips that are vectors of the bud-blight virus al., 1998).
(Kogan et al., 1999). Late planting of wheat
has been used for a long time to manage
Hessian flies. Adult Hessian flies have a very Crop rotation (increasing and maintaining
short lifespan (3–4 days) and oviposition temporal diversity)
occurs over a limited span of time during
early autumn. If planting is delayed so that Crop rotation means growing different crops
most of the flies have died before the wheat in succession in the same field. It is espe-
emerges, damaging infestations may be cially effective against host-specific pests.
avoided. In regions where Hessian flies are a Crop rotation drastically changes the envi-
problem, fly-free dates have been established ronment, both above and below ground,
to guide autumn planting of wheat, based on usually to the disadvantage of pests of the
the seasonal occurrence of the adults previous crop. The same crop grown year
(Dufour, 2001). In situations in which after year on the same field will inevitably
migrant rather than resident populations are build up populations of organisms that feed
the major source of infestation, crop planting on that plant or have a life cycle similar to
should be delayed until any major pest that of the crop. It is important that the crops
migration is over. Damage to sugarbeets by in a rotation system are genetically distant
curly-top virus can be avoided or reduced by (belonging to different plant families) so that
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Cultural Practices 31

they do not have common pests. The focus is therefore provide an excellent control, both
on either selecting rotations detrimental to effective and economical. Rotating potatoes
certain pest species or avoiding rotations with lucerne reduces wireworm damage,
known to favour the pests. Crop rotation and rotating oats and maize reduces maize
works by disrupting normal life cycles of rootworm damage. Maize rootworms,
pests by placing them in a non-host habitat Diabrotica longicornis Say and Diabrotica vir-
(crop). It reduces pest pressure on all crops gifera Le Conte, in the Midwestern USA have
in the rotation by breaking the pest repro- been effectively controlled by a 2-year rota-
ductive cycles. This practice seldom has any tion of maize with soybeans. Unfortunately,
economic or ecological disadvantage; there- this tactic has been compromised in some
fore, it is widely used even when crop dam- areas where the rootworms have developed
age is anticipated to be minimal (Herzog and strains that can diapause for more than 1
Funderburk, 1986). Crop rotation is generally year (Levine and Oloumi-Sadeghi, 1991).
compatible with biological controls and Crop rotation may impose some limita-
forms the basis for IPM systems for many tions. Some crops used in rotation are of
crops. Most common rotations include grass, such low value that they contribute little to
legume and root crops. A leguminous crop in farm income. Also, an incorrect choice of
rotation generally replenishes plant nutri- crop sequence in a rotation can result in an
ents, particularly nitrogen, thereby reducing elevated insect problem. For example, wire-
the rates of needed chemical fertilizers. Also, worms are more severe in potatoes following
rotation reduces the chance of pesticide red clover or sweet clover (Norris et al.,
build-up in the environment, thus decreas- 2003).
ing the threat of pest resistance to pesticides
(Reeves, 1994). Rotations that increase
organic matter improve the environment for Interplanting or multiple cropping systems
biological activity, which will increase the (maintaining and improving spatial diversity)
breakdown of pesticides.
Crop rotation is one of the oldest and Multiple cropping or polyculture is typical of
most important measures for the control of traditional farming systems in most develop-
pests that overwinter in the soil as eggs or ing countries. At present, there is insufficient
partially grown larvae. It has been success- experimental evidence that multiple crop-
fully used against many soil pests, including ping has a positive effect for pest manage-
arthropods, plant-parasitic nematodes, fun- ment, although Altieri (1987, 1991, 1994),
gal pathogens and bacterial pathogens. It is Wratten and van Emden (1995), Landis et al.
most effective against arthropod pests with a (2000) and others provide abundant observa-
restricted plant-host range, long generation tional evidence that the inherent increase in
cycle (1 year or longer) and limited dispersal biodiversity of multiple cropping systems
capability. Host selectivity may occur increases the quality and quantity of the nat-
through either ovipositional or feeding ural enemy fauna. The advantage of multiple
behaviour. cropping systems for IPM is postulated on
Numerous species of major soil pests are the principle of habitat diversification.
successfully controlled by crop rotation. For Monocultures inherently lack biodiversity as
example, the white-fringed weevil complex they are simplified and unstable agroecosys-
has limited dispersal capacity as the adult is tems, frequently prone to recurrent pest out-
unable to fly (Zehnder, 1997). These species breaks that demand constant human
are highly prolific on legumes; however, intervention. Systems high in biodiversity
grasses, including maize, are in some way tend to be more ‘dynamically stable’ because
nutritionally deficient for supporting their the variety of organisms provides more
feeding (Ferro, 1996). These pests cause no or checks and balances on each other, thus help-
low damage to grasses, but leguminous ing prevent one species (i.e. pest species)
crops, soybean and groundnuts may suffer from overwhelming the system. In IPM, bio-
heavy losses. A soybean/maize rotation can diversity may create stability (but not
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32 W.I. Bajwa and M. Kogan

always) within a crop season if employed as For example, a scheme of alternating six-row
an area-wide approach. When applied to sin- blocks of soybean and maize or alternating
gle fields, the approach may fail due to strips of lucerne and cotton or lucerne and
movement of pest organisms from adjacent maize may reduce pest problems. Strip crop-
fields. Monocultures open the way to pest ping may result in a more balanced insect
infestations by providing concentrated population with an increase in beneficial
resources and uniform physical conditions insects.
that promote pest invasions (Altieri, 1987). In An example is interplanting strips of
these environments, the abundance and lucerne in cotton for the control of lygus
effectiveness of natural enemies are reduced bugs, which prefer and will concentrate in
because of inadequate alternative sources of the strips of uncut lucerne, leaving the cotton
food, shelter, breeding sites and other envi- undamaged (Godfrey and Leigh, 1994). The
ronmental factors. Increasing crop diversity, lucerne may be harvested later as a forage
on the other hand, may be used to augment crop.
predator and parasitoid populations or to In mixed-crop stands, it may be more dif-
impair herbivores’ ability to find and utilize ficult for pests to locate their host by either
their host plants. In multiple cropping sys- physical (visual clues) or chemical means
tems certain plants may deter pests and (plant odours from non-host plants confuse
reduce food supply for pests, while attract- feeding stimuli) (Bajwa and Shaefers, 1998).
ing and increasing an abundance of natural For example, thrips and whiteflies are
enemies. Pest levels are thus expected to be attracted to green plants with a brown (soil)
lower in polycultures. background, avoiding areas with full vegeta-
Spatial arrangements used in multiple tion cover, such as a main crop and a cover
cropping are variations of row intercropping crop between rows (Sullivan, 2001). Some
and strip cropping. Row intercropping is a intercrops have a spatial arrangement that
system in which two or more crops are produces the full vegetation cover that
simultaneously planted in rows across a sin- would be unfavourable for thrips and white-
gle field. The use of this practice as a strategy flies. Other insects recognize their host plant
for weed control should be approached care- by smell. Onions planted with carrots mask
fully. Intercropping may result in reduced the smell of carrots from carrot flies
yields of the main crop if competition for (Sullivan, 2001).
water or nutrients occurs. On the positive Besides the potential IPM benefits, multi-
side, infestations of armyworm, Spodoptera ple cropping may also protect farmers
frugipereda (J.E. Smith), in maize and against the risks of crop failure; if one crop
Empoasca spp. (leafhoppers) and Diabrotica within the system fails, the other may sur-
spp. (leaf beetles) in beans can be greatly vive and compensate in yield to some extent,
reduced by interplanting the two crops allowing the farmer an acceptable harvest.
(Altieri, 1987). Intercropping of soybean and Despite all its potential benefits, much more
maize increases the rate of parasitism by research is needed on the complex interac-
Trichogramma spp. (Altieri et al., 1981). In tions between various paired crops and their
Africa, intercropping of cereal crops (mainly pest/predator complexes before the method
maize and sorghum) with the non-host will be widely accepted to replace large-scale
molasses grass, Melinis minutiflora (Beauv.), monocultures. A major drawback of multiple
reduces infestation by stem borers, Busseola cropping is the difficulty in mechanized
fusca Fuller and Chilo partellus (Swinhoe), in planting, cultivating and harvesting.
the main crop and also increases larval para-
sitism by Cotesia sesamiae (Cameron) (Khan et
al., 1997). Trap crops
Strip cropping is the practice of growing
two or more crops in different strips (usually Trap cropping is the practice of attracting
four or more rows per strip) across a field pests to small plantings in or around a main
wide enough for independent cultivation. crop or to an early planting of a crop on a
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Cultural Practices 33

small area. Trap crops are generally more the southern USA and Hawaii, melon fields
favourable hosts for the target pest than the with small plantings of squash on the
main crop. If a trap crop is maintained in a perimeter typically do not require insecti-
vigorous state, the pest may never leave the cides. The practice reduces production costs
trap crop. If the pest population builds up for the main crop, conserves natural enemies
and begins to leave, the trap crop can be and decreases the risk of secondary pest out-
mowed or sprayed to prevent damage to the breaks. In this case, the squash trap crop
main crop. This action does not affect the enhances sustainability for the producer as a
activities of beneficial species in the main value-added crop. Sales of squash offset
crop. In many instances, trap crops can also costs of the seed and pesticide and still pro-
serve as refugia or additional reservoirs for vide additional income (Suszkiw, 1997).
beneficial predators and parasitoids in the
event that the adjacent crop field is treated.
Trap crops or trap plants have been in use Non-crop vegetation manipulation
against many insect pests, nematodes and
plant pathogens. In beans, trap cropping can Vegetation manipulation in agroecosystems
considerably reduce damage to Mexican and their surroundings is an important prac-
bean beetle, Epilachna varivestis (Mulsant), tice used to enhance beneficial arthropods in
and the bean leaf beetle, Cerotoma trifurcata agricultural crops. For example, an orchard
(Forster). Early-maturing varieties can be ground cover, if properly maintained, pro-
planted 2 weeks prior to the main soybean motes the build-up of natural enemies of cer-
crop. The adult beetles are attracted to these tain pests (USDA, 1998). Recently, several
early-maturing trap crops and are then studies have demonstrated the potential for
destroyed by cultivation or sprayed with an establishing flowering plants in or around
insecticide (Newsom and Herzog, 1977). farm fields to attract natural enemies and
Early-planted potatoes may act as a trap crop enhance biological control in the adjacent
for Colorado potato beetles emerging in the field (Altieri and Nicholls, 2000). In Europe,
spring (Hokkanen, 1991). Since the early windbreaks and hedgerows have been used
potatoes are the only food source available, to encourage the build-up of natural enemies.
the beetles will assemble on these plants, Flowering strips on uncultivated field mar-
where they can be controlled more easily. In gins can encourage the build-up of syrphid
Finland, mixed stands of trap plants fly and parasitoid populations, but plant age
(Chinese cabbage, oilseed and turnip rape, and composition appear to be important
sunflower and marigold) near the main cau- (Altieri and Nicholls, 2000). Unfortunately,
liflower plantings have been used for trap- the effectiveness of this practice is generally
ping the rape-blossom beetle, Meligethes limited to areas of the crop close to the flow-
viridescens (Fabricius). This beetle often rav- ering strips (Alford, 2000). Modifying the
ages up to one-third of the whole harvest. As wild vegetation surrounding crop fields and
the beetle is highly mobile, several strips of orchards may favour a natural balance
trap plants are grown in the anticipated between pest arthropods and their enemies
direction of infestation. Appropriately timed (Rieux et al., 1999). The technique is still in its
insecticide applications for trap cropping early stages of development, but research in
control the beetle and prevent its spread to progress should help ascertain the role of the
the cauliflower plants. The technique has local flora and promising new plant introduc-
proved to increase by approximately 20% the tions in and around agricultural fields. This
marketable yield of the crop (Hokkanen, research should help to clarify both the
1991). While some of these techniques still potential of the non-crop vegetation benefit
rely on insecticidal control, the area treated is as sources of natural enemies and the risk of
greatly reduced (Hokkanen, 1991). harbouring phytophagous arthropods shared
A possible limitation of trap cropping is with the crops.
the expense of producing and destroying a Cover crops are non-crop plant species
crop that brings no income. Nevertheless, in grown either concurrently with the host crop
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34 W.I. Bajwa and M. Kogan

(usually perennial plants) or in rotation with spider species and can reduce considerable
annual crops; they are generally not har- damage to vegetable crops by insect pests
vested. Examples include the establishment (Reichert and Bishop, 1990). Living mulches
of pure or mixed stands of legumes and cere- of various clovers reduce insect-pest damage
als to protect the soil against erosion. This to vegetables and orchard crops (Bugg et al.,
technique ameliorates soil structure, 1990) by providing essential resources for
enhances soil fertility and may help suppress natural enemies. In some cases, mulching
certain weeds, arthropod pests and patho- may provide a favourable environment for
gens. Cover crops affect the ecology of slugs and snails, which can be particularly
orchards and vineyards by improving soil damaging at the seedling stage.
biology and fertility and by increasing bio-
logical control of insect pests by harbouring
predators and parasitoids (Altieri and Conclusions
Nicholls, 2000). Cover crops attract and pro-
vide a nectar source for beneficial insects, Pest managers, in general, must learn to
spiders and mites. adjust the use of cultural controls to the fea-
tures and properties of extant cropping sys-
tems. Powerful ecological, economic, cultural
Miscellaneous cultural-control practices and social pressures have shaped the pre-
dominant cropping systems in most parts of
Increased plant density may sometimes be the world. For example, as a consequence of
useful, but can add to production costs. the 1973 oil crisis, Brazil launched a vigorous
Damage to seedlings by soil pests, such as campaign to promote the use of sugarcane-
cutworms, can sometimes be compensated derived ethanol as a petrol substitute.
for by higher seeding rates. Reducing row Government subsidies and other incentives
spacing causes the canopy to close early and led growers in the state of São Paulo to
improves conditions for predator coloniza- replace a diverse agriculture that included
tion in many crops. Narrow row spacing in some of the staples for low-income popula-
soybean decreases ovipositional preference tions, such as rice and beans, with sugarcane
of maize earworm moths as they prefer to plantations. In some areas, huge new
oviposit in open-canopy fields. In contrast, monocrops became established almost
damage to maize by larvae of the Diabrotica overnight, covering millions of hectares. As
undecimpunctata Mannerheim borer expected, pest problems were aggravated
decreases as plant density increases or when and treated with an array of broad-spectrum
broad-leaved weeds are present rather than pesticides. Industry and government gave
bare soil (Speight et al., 1999). Planting of little or no consideration to the resulting pest
wheat at high densities and in narrow rows impacts of this shift of cropping systems
decreases moisture in stems, stem diameter until after the fact.
and plant height. The wheat sawfly, C. cinc- Thus, pest pressure is but one of the eco-
tus, prefers larger, more succulent plants for logical forces that have influenced the evolu-
oviposition, and damage to wheat decreases tion of cropping systems as they exist at
as seeding density increases and row spacing present. Among the agricultural pests,
decreases (Herzog and Funderburk, 1986). weeds, more than either arthropod pests or
Mulches – natural or synthetic soil cover- pathogens, have influenced the development
ings – are useful for the suppression of of cropping systems. Row spacing is
weeds, insect pests and some plant diseases. adjusted for ease of cultivation. Vegetation
A mulch can reduce the spread of soil-borne management to enhance the natural enemies
plant pathogens by preventing their trans- of arthropod pests and the use of cover crops
mission through soil splash. Winged aphids are often disregarded by growers for fear
are repelled by reflective mulches (silver- or that these techniques may make weed con-
aluminium-coloured). Hay and straw mulches trol more difficult. Certain rotations and bet-
are more habitable than bare ground to some ter selection of regional crops could
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Cultural Practices 35

potentially improve overall regional crop times; thus the early-planted fields in a
health, but economic and cultural constraints region already acted as trap crops (Newsom
often take these options away from the pest et al., 1980).
manager. As a result, successful use of We do not presume to have offered an
cultural-control methods must take into exhaustive discussion of cultural pest-control
account the nature of the dominant cropping practices in this chapter. There is a vast liter-
system. Experiments conducted in isolated ature on the subject (Herzog and
soybean fields in Louisiana showed that Funderburk, 1986; Speight et al., 1999; Landis
early planting of a border row of soybean, et al., 2000; Norris et al., 2003) and the crop-
prior to planting of the bulk of the field, specific literature offers the pest manager the
could be beneficial for the control of the best key to the prevalent practices in each
bean-leaf beetle. A strip of about 10% of the region. This literature should be the first to
total field area was planted. It attracted the be studied if one is to develop an IPM sys-
colonizing beetles in large numbers. The tem with a strong foundation on cultural-
strip was sprayed with an insecticide, thus control tactics. The effectiveness of cultural
eliminating most of the colonizing popula- controls often rests on the complex interrela-
tion. When the rest of the field was planted, tionships among many of these practices and
it remained uninfested for most of the with other IPM tactics, particularly biological
remainder of the season. The technique control. Nearly every operation carried out
resulted in a 90% reduction in insecticide in the field will have some effect, either good
use. Despite the positive result of this trap- or bad, on current or potential pest prob-
cropping experiment, the technique was not lems. Understanding these relationships and
adopted by growers, who objected to mov- acting to promote the positive ones are
ing twice to the same field the huge planters essential steps in the success of IPM pro-
used in the industry. In addition, growers grammes that aim at optimizing the role of
within a region tend to plant at different cultural-control methods.

References

Alford, D.V. (2000) Pest and Disease Management Handbook. Blackwell Science, Oxford, 615 pp.
All, J.N. (1999) Cultural approaches to management arthropod pests. In: Ruberson, J.R. (ed.) Handbook of
Pest Management. Marcel Dekker, New York, pp. 395–416.
Allee, L.L. and Davis, P.M. (1996) Effect of manure and corn hybrid on survival of western corn root-
worm (Coleoptera: Chrysomelidae). Environmental Entomology 25, 801–809.
Altieri, M.A. (1987) Agroecology: the Scientific Basis of Alternative Agriculture. Westview Press, Boulder,
Colorado, 227 pp.
Altieri, M.A. (1991) How best can we use biodiversity in agroecosystems. Outlook on Agriculture 20,
15–23.
Altieri, M.A. (1994) Biodiversity and Pest Management in Agroecosystems. Food Products Press, New York,
185 pp.
Altieri, M. and Nicholls, C.I. (2000) Applying agroecological concepts to the development of ecologically
based pest management strategies. In: National Research Council (ed.) Professional Societies and
Ecologically Based Pest Management. National Academy Press, Washington, DC, pp. 14–19.
Altieri, M.A., Lewis, W.J., Nordlund, D.A., Gueldner, R.C. and Todd, J.W. (1981) Chemical interactions
between plants and Trichogramma wasps in Georgia soybean fields. Protection Ecology 3, 259–263.
Anon. (1996) Integrated Pest Management for Cotton in the Western Region of the United States. Publication
3305, University of California, Oakland, California, 164 pp.
Anon. (1998) Integrated Pest Management for Tomatoes, 4th edn. Publication 3274, University of California,
Oakland, California, 118 pp.
Anon. (1999) Integrated Pest Management for Apples and Pears. Publication 3340, University of California,
Oakland, California, 232 pp.
Bajwa, W.I. (1988) Pest Management of Major Field Crops. Agricultural Development Bank Pakistan,
Islamabad, 60 pp.
02IntpestManCh2.QXD 14/4/04 2:24 pm Page 36

36 W.I. Bajwa and M. Kogan

Bajwa, W.I. (1989) Citrus Pest Management. Agricultural Development Bank Pakistan, Islamabad, 10 pp.
Bajwa, W.I. and Schaefers, G. (1998) Indigenous Crop Protection Practices in Sub-Saharan East Africa, their
Status and Significance Relative to Small Farmer IPM Programs in Developing Countries. Available at:
http://ippc.orst.edu/ipmafrica/
Bariola, L.A. (1983) Survival and emergence of overwintered pink bollworm moths (Lepidoptera:
Gelechiidae). Environmental Entomology 12, 1877–1881.
Beasley, C.A. (1992) Winter irrigation reduces spring emergence of pink bollworm moths. In: Proceedings
Beltwide Cotton Production Research Conference, Vol. 2. National Cotton Council of America, Memphis,
Tennessee, pp. 943–944.
Brumfield, R.G. and Ogier, J.P. (2000) A review of organic horticulture and agriculture in the US. In:
Proceedings of the XIVth International Symposium on Horticultural Economics. Acta Horticulturae, No.
536, St Peter Port, Guernsey, UK, pp. 21–28.
Bugg, R.L., Phatak, S.C. and Dutcher, J.D. (1990) Insects associated with cool-season cover crops in south-
ern Georgia: implications for pest control in truck-farm and pecan agroecosystems. Biological
Agriculture and Horticulture 7, 17–45.
Buntin, G.D., Cunfer, B.M. and Bridges, D.C. (1991) Impact of volunteer wheat on wheat insects in a
wheat soybean double crop system. Journal of Entomological Science 26, 401–407.
Burton, R.L., Jones, O.R., Burd, J.D., Wicks, G.A. and Krenzer, E.G. Jr (1987) Damage by greenbug
(Homoptera: Aphididae) to grain sorghum as affected by tillage, surface residues, and canopy.
Journal of Economic Entomology 80, 792–798.
Capinera, J.L. (2001) Handbook of Vegetable Pests. Academic Press, New York, 728 pp.
Cherry, R.H. (1987) The effect of flooding on insect populations. Bulletin of Agricultural Experiment Stations
(University of Florida) 870, 27–34.
Cook, R.J. and Baker, K.F. (1983) The Nature of Practice of Biological Control of Plant Pathogens. American
Phytopathological Society, St Paul, Minnesota, 539 pp.
Cox, G.W. and Atkins, M.D. (1964) Agricultural Ecology: an Analysis of World Food Production Systems. W.H.
Freeman, San Francisco, California, 721 pp.
Daane, K.M., Dlott, J.W., Johnson, R.S., Ramirez, H.T., Michailides, T.J., Yokota, G.Y., Crisosto, C.H. and
Morgan, D.P. (1995) Excess nitrogen raises nectarine susceptibility to diseases and insects. California
Agriculture 49, 13–18.
Deren, C.W., Cherry, R.H. and Snyder, G.H. (1993) Effect of flooding on selected sugarcane clones and
soil insect pests. Journal American Society of Sugar Cane Technologists 13, 22–27.
Dufour, R. (2001) Biointensive Integrated Pest Management. Appropriate Technology Transfer for Rural
Areas (ATTRA), Fayetteville, Arkansas, 52 pp.
Ferro, D.N. (1996) Cultural control. In: Radcliffe, E.B. and Hutchison, W.D. (eds) Radcliffe’s IPM World
Textbook. University of Minnesota, St Paul, Minnesota. Available at: http://ipmworld.umn.edu
Flint, M.L. and Gouveia, P. (2001) IPM in Practice – Principles and Methods of Integrated Pest Management.
Publication 3418, University of California, Oakland, California, 296 pp.
Frisbie, R.E. and Smith, J.W. Jr (1991) Biologically intensive integrated pest management: the future. In:
Menn, J.J. and Steinhauer, A.L. (eds) Progress and Perspectives for the 21st Century. Entomological
Society of America, Lanham, Maryland, pp. 151–164.
Godfrey, L.D. and Leigh, T.F. (1994) Alfalfa harvest strategy effect on lygus bug (Hemiptera: Miridae) and
insect predator population density: implications for use as trap crop in cotton. Environmental
Entomology 23, 1106–1118.
Goodwin, D. (1985) The ecology of two species of corn rootworm (Coleoptera: Chrysomelidae) on volun-
teer corn in soybean fields in northern Illinois. Bulletin of the Ecological Society of America 66, 179–183.
Hatfield, P.G., Blodgett, S.L., Johnson, G.D., Denke, P.M., Kott, R.W. and Carroll, M.W. (1999) Sheep graz-
ing to control wheat stem sawfly, a preliminary study. Sheep and Goat Research Journal 15, 159–160.
Hellman, E. and Watson, B. (2000) Reducing the risk of Phylloxera infestation. Northwest Berry and
Grape Information Network. Electronic publication. Available at: http://berrygrape.orst.edu/
fruitgrowing/grapes/phylrisk.htm
Herzog, D.C. and Funderburk, J.E. (1986) Ecological bases for habitat management and pest cultural con-
trol. In: Kogan, M. (ed.) Ecological Theory and Integrated Pest Management Practice. John Wiley & Sons,
New York, pp. 217–250.
Hokkanen, H.M.T. (1991) Trap cropping in pest management. Annual Review of Entomology 36, 119–138.
Horn, D.J. (1988) Ecological Approach to Pest Management. Guilford Press, New York, 285 pp.
02IntpestManCh2.QXD 14/4/04 2:24 pm Page 37

Cultural Practices 37

Khan, Z.R., Ampong-Nyarko, K., Chiliswa, P., Hassanali, A., Kimani, S., Lwande, W. and Overholt, C.M.
(1997) Intercropping increases parasitism of pests. Nature 388, 631–632.
Kiritani, K. (2000) Integrated biodiversity management in paddy fields: shift of paradigm from IPM
toward IBP. IPM Reviews 5, 175–183.
Knight, A.L. (1998) Management of codling moth (Lepidoptera: Tortricidae) in apple with overhead
watering. Journal of Economic Entomology 91, 209–216.
Kogan, M. and Bajwa, W.I. (2001) IPM in the next century: how might things change? Proceedings of
Oregon Horticultural Society 92, 51–70.
Kogan, M., Croft, B.A. and Sutherst, R.F. (1999) Applications of ecology for integrated pest management.
In: Huffaker, C.B. and Gutierrez, A.P. (eds) Ecological Entomology. John Wiley & Sons, New York,
pp. 681–736.
Kok, L.T. (2001) Classical biological control of nodding and plumeless thistles. Biological Control: Theory
and Applications in Pest Management 21, 206–213.
Landis, D.A., Wratten, S.D. and Gurr, G.M. (2000) Habitat management to conserve natural enemies of
arthropod pests in agriculture. Annual Review of Entomology 45, 175–201.
Levine, E. and Oloumi-Sadeghi, H. (1991) Management of diabroticite rootworms in corn. Annual Review
of Entomology 36, 229–255.
Lidell, M.C. and Schuster, M.F. (1990) Distribution of the Hessian fly and its control in Texas.
Southwestern Entomologist 15, 133–145.
Ma, K.C. and Lee, S.C. (1996) Occurrence of major rice insect pests at different transplanting times and
fertilizer levels in paddy field. Korean Journal of Applied Entomology 35, 132–136.
MacHardy, W.E. (2000) Current status of IPM in apple orchards. Crop Protection 19, 801–806.
McHugh, J.J. Jr and Foster, R.E. (1995) Reduction of diamondback moth (Lepidoptera: Plutellidae) infes-
tation in head cabbage by overhead irrigation. Journal of Economic Entomology 88, 162–168.
Morrill, W.L. and Kushnak, G.D. (1996) Wheat stem sawfly (Hymenoptera: Cephidae) adaptation to win-
ter wheat. Environmental Entomology 25, 1128–1132.
Newsom, L.D. and Herzog, D.C. (1977) Trap crops for control of soybean pests. Louisiana Agriculture 20,
14–15.
Newsom, L.D., Kogan, M., Miner, F.D., Rabb, R.L., Tunnipseed, S.G. and Whitecomb, W.H. (1980)
General accomplishments toward better pest control in soybean. In: Huffaker, C.B. (ed.) New
Technology of Pest Control. Wiley, New York, pp. 51–98.
Norris, R.F., Caswell-Chen, E.P. and Kogan, M. (2003) Concepts in Integrated Pest Management. Prentice
Hall, Upper Saddle River, New Jersey, 586 pp.
Omolo, E.O. and Reddy, S. (1983) An overview of cultural component of an integrated pest management
systems in sorghum. In: Africa: Seminar on the Use and Handling of Agricultural and Other Pest Control
Chemicals. Environment Liaison Centre in support of African NGO’s Environment
Network/Pesticide Action Network, Duduville, Nairobi, Kenya, pp. 100–103.
Pedigo, L.P. (2002) Entomology and Pest Management. Prentice Hall, Upper Saddle River, New Jersey, 742
pp.
Phelan, L. (1997) Soil management history and the role of plant mineral balance as a determinant of
maize susceptibility to the European corn borer. Biological Agriculture and Horticulture 15, 25–34.
Prokopy, R. (1994) Integration in orchard pest and habitat management: a review. Agriculture, Ecosystems
and Environment 50, 1–10.
Prokopy, R. (2001) Twenty years of apple production under an ecological approach to pest management.
Fruit Notes 66, 3–10.
Reeves, D.W. (1994) Cover crops and rotations. In: Hatfield, J.L. and Stewart, B.A. (eds) Crops Residue
Management. Lewis Publishers, Ann Arbor, Michigan, pp. 127–172.
Reichert, S.E. and Bishop, L. (1990) Prey control by an assemblage of generalist predators: spiders in gar-
den test systems. Ecology 71, 1441–1450.
Rieux, R., Simon, S. and Defrance, H. (1999) Role of hedgerows and ground cover management on
arthropod populations in pear orchards. Agriculture, Ecosystems and Environment 73, 119–127.
Roth, G.W., Calvin, D.D. and Lueloff, S.M. (1995) Tillage, nitrogen timing, and planting date effects on
western corn rootworm injury to corn. Journal of Agronomy 87, 189–193.
Sansavini, S. (1997) Integrated fruit production in Europe: research and strategies for a sustainable indus-
try. Scientia Horticulturae 68, 25–36.
Speight, M.R., Hunter, M.D. and Watt, A.D. (1999) Ecology of Insects – Concepts and Applications. Blackwell
Science, London, 350 pp.
02IntpestManCh2.QXD 14/4/04 2:24 pm Page 38

38 W.I. Bajwa and M. Kogan

Steffey, K., Gray, M. and Weinzierl, R. (1992) Insect management. In: Conservation Tillage Systems and
Management. Midwest Plan Services, Iowa State University, Ames, Iowa, pp. 67–74.
Steffey, K.L., Armbrust, E.J. and Onstad, D.W. (1994) Management of insects in lucerne. In: Metcalf, R.L.
and Luckmann, W.H. (eds) Introduction to Insect Pest Management, 3rd edn. John Wiley & Sons, New
York, pp. 469–506.
Stinner, B.R. and House, G.J. (1990) Arthropods and other invertebrates in conservation-tillage agricul-
ture. Annual Review of Entomology 35, 299–318.
Stoll, G. (1988) Principles of preventive crop protection. In: Stoll, G. (ed.) Natural Crop Protection in the
Tropics. Margraf Verlag, Weikersheim, pp. 14–23.
Stoll, G. (2000) Natural Crop Protection in the Tropics. Margraf Verlag, Weikersheim, 376 pp.
Sullivan, P. (2001) Intercropping Principles and Practices: Agronomy Systems Guide. Appropriate Technology
Transfer for Rural Areas (ATTRA), Fayetteville, Arkansas, 16 pp.
Suszkiw, J. (1997) Melon growers’ next battle cry against insect pests could be squash ’em. Agricultural
Research 45, 16–17.
USDA (1998) Managing Cover Crops Profitably. Publication SX1005, Sustainable Agriculture Network,
Washington, DC, 212 pp.
van den Berg, J., Nur, A.F. and Polaszek, A. (1998) Cultural control. In: Polaszek, A. (ed.) African Cereal
Stem Borers: Economic Importance, Taxonomy, Natural Enemies and Control. CAB International,
Wallingford, UK, pp. 333–347.
Wratten, S.D. and van Emden, H.F. (1995) Habitat management for enhanced activity of natural enemies
of insect pests. In: Glen, D.M., Greaves, M.P. and Anderson, H.M. (eds) Proceedings of the 13th Long
Ashton International Symposium on Arable Ecosystems for the 21st Century. Bristol, UK, p. 329.
Zehnder, G.W. (1997) Population dynamics of whitefringed beetle (Coleoptera: Chrysomelidae) in sweet
potato in Alabama. Environmental Entomology 26, 727–735.
Zehnder, G.W., Briggs, T.H. and Pittsi, J.A. (1998) Management of whitefringed beetle (Coleoptera:
Curculionidae) grub damage to sweet potato with adulticide treatments. Journal of Economic
Entomology 91, 708–714.
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3 The Relevance of Modelling in Successful

Implementation of IPM

David E. Legg
Department of Renewable Resources, University of Wyoming
Laramie, WY 82071, USA
E-mail: [email protected]

Introduction is also an important part of the agroecosys-

tem (see Chapter 4, this volume). Behaviour-
Integrated pest management (IPM) has modifying chemicals, as well as
evolved from its beginning as a concept of non-behaviour-modifying pesticides, have
integrated control (Stern et al., 1959) to a also played important roles in IPM. In addi-
complex study of the agroecosystem. This tion, the behaviours of some pests can some-
change was both natural and necessary times be used against them in a carefully
because conventional agroecosystems are crafted IPM programme. Finally, we must
typically dominated by one crop or animal never forget that humans are an integral part
species (host) and thus are not diverse. of the agroecosystem, and it can be argued
Ecosystems with limited diversity are vul- that the ‘consumer’ is a powerful, driving
nerable to the rapid colonization of the host force in determining the composition of IPM
by some biological organisms, and some- programmes (see Chapter 11, this volume).
times it can result in host depredation. It goes without saying that humans both
Consequently, the task of many IPM practi- craft agroecosystems and study the interac-
tioners is to increase the diversity of an tions between pests, their hosts, their natural
agroecosystem as well as to increase the enemies and the environment. From such
diversity of the pest-management tools that studies, IPM specialists obtain the informa-
are used in that system; this will make them tion upon which agroecosystem changes are
more stable and less dependent on pesticide based. Also from these studies, ‘tools’ are
usage. To this end, IPM very much encom- developed to describe, analyse and even
passes and makes use of the cultural-control mimic parts of those systems. When those
tactics and practices that were identified in tools have been developed to a sufficient
Chapter 2. It also embraces the practice of degree, they may then be used to predict
using biopesticides. Host-plant resistance what will happen in the future; predictions
has always been a key element in many IPM of the future are referred to as forecasts.
programmes and transgenic techniques pre- The tools I am referring to are models. For
sent many exciting opportunities for increas- decades, models have been an integral part
ing the diversity of the agroecosystem. of IPM. For instance, the use of models has
Biological control, particularly when viewed helped pest managers decide how the agro-
from a perspective of tritrophic interactions, ecosystem should be changed to favour
© CAB International 2004. Integrated Pest Management: Potential, Constraints and Challenges
(eds O. Koul, G.S. Dhaliwal and G.W. Cuperus) 39
03IntpestManCh3.QXD 14/4/04 2:24 pm Page 40

40 D.E. Legg

economy and conservation and not to favour What differentiates the former use of the
pests. Moreover, the use of models has word model from the latter? In the former,
allowed scientists to conduct simulated the focus is on an idealized representation of
experiments when the conduct of those reality. In the latter, the focus is on an actual
experiments would not have been possible. representation of reality. In IPM, we use
Further, models have been used whenever models as actual representations of reality.
scientists wanted to explore as well as under- Models represent or mimic reality in sev-
stand the complexities of agroecosystems. eral ways and, accordingly, there are several
In this chapter, I will define and discuss definitions as to what constitutes a model.
two basic terms: models and systems. I will Smith (1974) indicates that a model is a
then discuss the systems approach to model- description of general ideas that include as
ling, which will be followed by discussions little detail as possible. Jeffers (1978) defines
on various classification schemes of systems, a model as any formal expression of the rela-
the modelling process, the implementation tionships between defined symbols. Teng
of models and the identification of some (1981, 1987) defines a model as any represen-
commonly used models in IPM. Then I will tation of a system in some form other than
discuss the teaching of some aspects of mod- the original. Manetsch and Park (1982)
elling to students in the classroom and to define a model as an abstract representation
IPM practioners in the field. Finally, I will of a real-world system that behaves like the
address the future of modelling in IPM. real-world system in certain respects.
Further, these authors indicate that a ‘good’
model represents the important aspects of
Two Basic Terms the system for problem solving and mini-
mizes ‘behaviour’ that is insignificant to the
There are two basic terms that need to be problem. Clearly, most definitions of models
understood; the ‘models’ and the ‘systems’. In indicate that they represent something called
some circumstances, a ‘model’ represents an systems and depend, therefore, on the defini-
idealized situation or person. For example, tion of those systems.
the clothing and garment industry has the A ‘system’, as defined by Miller and Miller
fashion model, who demonstrates the most (1984), is something that has a set of charac-
beautiful way in which clothing may be worn. teristics common to all systems and lacking
Estate agents have the model home, which in things that are not systems. Further, these
represents a well-designed and richly deco- authors indicate that a system has parts
rated dwelling. Society has the model citizen, called units or components, which are inter-
who is a person that everyone should strive to dependent and interact with one another.
emulate. Then there is the model athlete, who Focusing on living organisms, Teng (1987)
is a person that excels beyond all others at indicates that a system cannot be properly
his/her sport while also being a good person. understood or managed based on knowledge
Happily, not all usage of the term model of some of its components. He also states that
is of this sort. Architects and engineers often the components of a system interact with
construct likenesses of whatever they are try- each other and are influenced in that interac-
ing to build, and these constructs are called tion by external factors. Further, Teng (1987)
models. In addition, we can purchase minia- indicates that the whole of the system is more
ture pieces of cars, aeroplanes, ships and the than the sum of its parts. Manetsch and Park
like and then assemble them; these too are (1982) define a system as a set of intercon-
called models. If the dimensions of such nected elements organized towards a goal or
models are proportionally smaller versions set of goals separate from the environment,
of what is to be constructed, then they are and are determined by factors completely
said to be models of scale (e.g. 1 mm = 1 m). independent of or external to the system.
Models of scale have been used for centuries, Teng (1987) correctly points out that the sys-
particularly when constructing buildings tems approach to problem solving differs
and bridges. from systems analysis, which is the analysis
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Modelling in Successful Implementation of IPM 41

of system structure and behaviour, as well as model that would mimic the relations
from system control, which is the manipula- between fields within a farm. So where does
tion of input, system design, which is either a system begin and where does it end, and
the structuring of non-existing systems or the how can it be specified? The use of some-
restructuring of existing systems, and system thing called the systems approach to model-
synthesis, which is a major rebuilding of sys- ling may facilitate the answering of these
tems through modelling. questions.
From these definitions, it can be deduced
that any specified system is composed of com-
ponents, which are relevant and necessary to The Systems Approach to Modelling
the system’s function. Components of a sys-
tem necessarily depend on one another, and The systems approach, as defined by Teng
together they function to achieve the goal of (1987), is actually a problem-solving philoso-
the system. One example of a system would phy and methodology that are useful for
be a wheat (Triticum aestivum L.) production guiding the generation of knowledge to sup-
system, which has the following components: port pest management and for synthesizing
crop, pests, soil, economics, environment, information into useful forms for delivery.
humans and pest and soil management. The systems approach occurs in steps. As
Each component of a system can be subdi- outlined by Jeffers (1978, 1984), these begin
vided. For example, the crop component of with recognizing the ‘problem’. Then the
the aforementioned system could be divided problem is rigorously defined. Next, the
into low-, mid- and high-latitude varieties. goals and objectives of the problem-solving
Moreover, varieties within a latitude could be effort are explicitly stated. Then two or more
divided into plants, with each plant being potential solutions are generated to solve the
divided into leaves, roots, stems and flowers. problem. These are then employed in the
Each leaf, for example, could then be divided modelling process (more on that later). After
into cells, and each cell could be divided into modelling, the outcomes are carefully evalu-
molecules. Each molecule could be divided ated, with potential courses of action being
into atoms, and each atom could be divided assessed. Finally, the course of action that
into subatomic particles. These are examples shows the greatest promise for achieving the
of how a system could be specified at any stated goals is taken (taking action). Placed
number of increasing levels of resolution and into the context of a wheat production sys-
decreasing levels of scale. However, I could tem, let us use the example of the pest
also have specified that system at any number Diuraphis noxia (Mordvilko) being acciden-
of decreasing levels of resolution and increas- tally introduced into the western wheat-
ing scale, by mimicking the relations between growing areas of the USA. For many years
fields within farms, farms within regions, after its introduction, this pest caused hun-
regions within continents or continents within dreds of millions of dollars (US) of damage
the planet. Clearly, then, the specification of a (Legg and Archer, 1998). Initially, there were
system is a matter of resolution. few alternatives to the use of insecticides, so
As was mentioned earlier, models are insecticides were relied upon to keep D.
developed to mimic systems. However, noxia from causing significant economic
models can also be developed to mimic sys- losses (Legg and Archer, 1998). Therefore,
tem subcomponents. These are often referred one problem of immediate concern was that
to as submodels (e.g. Gelovani, 1984). Here, I D. noxia was destroying a significant portion
simply note that the use of the terms model of the US wheat crop and insecticides were
and submodel is somewhat subjective as a being heavily used for its control. A step
model that mimics one system may be a sub- towards solving this problem was to develop
model in another system. For example, if a methods whereby the severity of D. noxia
model represented or ‘mimicked’ the rela- infestations could be gauged, relative to the
tions between plants in a field, that model cost of insecticide application, so that pro-
could also be a submodel of a more inclusive ducers could assess whether such applica-
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42 D.E. Legg

tions would be economically viable. concrete systems are ‘phenomena’ of the

Accomplishing this goal would reduce much physical world. Concrete systems can be
of the uncertainty surrounding D. noxia subdivided into subsystems; Miller and
infestations and, in doing so, would reduce Miller give 19, four of which are the non-
the number of insecticide applications. living, living, ecological and earth subsys-
To satisfy this goal, three objectives were tems. Abstracted systems are actions that are
identified: (i) to establish the relationship abstracted from the behaviour of organisms.
between wheat yield and level of D. noxia Conceptual systems, on the other hand, are
infestation; (ii) to establish a method systems of ideas that are expressed in sym-
whereby the population dynamics of D. bolic form.
noxia could be mimicked; and (iii) to estab- The Bawden et al. classification scheme
lish methods whereby D. noxia infestations distinguishes the ‘soft’ from the ‘hard’ sys-
could be quickly and reliably estimated. For tems. Soft systems are those for which the
the sake of simplicity, I will refer to these as goals are not clearly recognizable and the
the wheat response–D. noxia infestation sys- outcomes are ambiguous and uncertain.
tem, the D. noxia population-dynamics sys- However, hard systems are those that have
tem and the D. noxia population-estimation clear goals and for which their outcomes are
system. Once these were identified, experi- predictable. Finally, the Teng classification
ments were designed and conducted to pro- system is even more fundamental than the
vide the necessary data for creating the Bawden et al. system in that Teng divides the
models that mimicked each system. These world into systems and non-systems.
models were then evaluated, courses of
action were formulated and those that pro-
vided the best promise for satisfying the Classification Schemes for Models
stated goals were implemented (Legg et al.,
1993; Legg and Archer, 1998). To summarize Up to now, I have avoided using terms that
the generalized concepts of models and sys- serve to classify models. This was deliberate,
tems, it is sufficient to say that models repre- as there are many such classification schemes
sent systems, whereas systems are composed being used. One scheme, put forward by
of objects that are united by their interactions Richardson (1984), identifies 12 generalized
to perform identifiable functions (Teng, types of models. Other classification schemes
1987). can be found in Jeffers (1978) and elsewhere
(Manetsch and Park, 1982; Logan, 1994;
Hess, 1996; Gutierrez, 2002). An important
Classification Schemes for Systems addition to these was put forward by Peck
(2000), when he distinguished statistical
Some scientists, it seems, cannot resist the from process models, the former being used
temptation to group different kinds of sys- to give a ‘probabilistic interpretation of the
tems into categories. This is natural and data’ without describing the underlying
serves to qualitatively describe systems of processes that drive the system, while the
interest. In the literature, three such classifi- latter attempt to describe the permanent
cation schemes are documented and will be underlying biological processes that drive
referred to as the Miller and Miller (1984), the system. Yet another classification scheme,
Bawden et al. (1984), and Teng (1987) which originated with Smith (1974), distin-
schemes. The Miller and Miller classification guished the practical (tactical) from the theo-
scheme identifies three classes of systems. retical (strategic) models. These serve to
These are the concrete, the abstracted and identify just two of the many purposes for
the conceptual systems. Concrete systems which modelling is undertaken (Hess, 1996).
represent non-random accumulation of mat- Other such purposes include crop growth,
ter and energy in a region in physical space- pest-population dynamics, sampling and
time, organized into interacting, interrelated sequential sampling. Also, models that
subsystems and components. In other words, describe or predict the change of something
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Modelling in Successful Implementation of IPM 43

over space may be referred to as landscape and the longevity of one’s life. Modelling by
or spatial models. Finally, some models are perfecting the paradigm mimics systems
simply referred to by the name of the person through the use of rules; such models are
or persons who either developed or popular- essential to many knowledge-based systems
ized them. Two examples are the Nachman (Stone et al., 1986; Plant and Stone, 1991). Life
(Nachman, 1981) and Taylor’s power law models are a collection of methods whose
models (Taylor, 1961). Here, I briefly describe commonality resides in the fact that they
the Richardson and Jeffers schemes for class- mimic human life processes; life models are
ifying models, as they include most model necessary because it would be unethical,
types identified in the other schemes that are immoral and illegal to conduct certain exper-
currently in use. iments on humans. Caricature models are
models that represent systems through the
use of metaphors, similes, effigies and the
Richardson classification system like. Computer models mimic systems
through the incorporation of rules and math-
The Richardson system of model classifica- ematical equations that express relationships
tion includes the sample, symbolism, simpli- between variables within systems. Computer
fication, analogy, scale forecast, paradigm models greatly facilitate the conduct of
perfection, life, caricature, computer, holism repetitive, complicated tasks. Also, they
and design models. Modelling by sample swiftly locate pieces of information that may
involves selecting a representative number be ‘buried’ in a great deal of literature.
of ‘individuals’ from a specified population, Modelling by holism represents a ‘turning
assessing those individuals and inferring away’ from the standard, reduction-driven
that assessment to the population at large; systems approach to modelling and making
modelling by sample is an essential part of use of philosophies and methods that have
statistics. Modelling by symbolism involves heretofore not been used (more on that later).
the use of symbols to express and represent Modelling by design ensures that the
the relations and states of variables in a sys- processes and schemas are constructed so
tem; this type of modelling is primarily that they will serve their intended purpose
found in mathematics, studies in logic and (i.e. will address the stated goals and objec-
decision making. Modelling by simplifica- tives of the problem-solving venture).
tion involves the development of schemas of
systems that are difficult or impossible to
otherwise envision; it serves to simplify sys- Jeffers classification systems
tems to the extent that just the basics are
modelled. Modelling by analogy is a tangible Jeffers (1978) actually put forward three sys-
representation of something that can be seen. tems for classifying models. The first is
Modelling by analogy requires (and pro- based on a dichotomy of simulation and ana-
vides) more detail than does modelling by lytic models. Simulation models are those
simplification. An example of modelling by that can be specified by a routine of arith-
analogy is a map of roads or streets. metic operations (Jeffers, 1978), while simu-
Modelling by scale is producing a represen- lation modelling involves the operation over
tative of some real-world entity, which time of a mathematical model that represents
resembles that entity in detail such that each the structure and dynamics of a system.
part of the model is proportionally the cor- Simulation modelling is often conducted for
rect size in relation to every other part of the the purpose of observing the system’s behav-
model; as mentioned before, architects and iour under controlled or experimental condi-
engineers have used these models. tions (Berryman and Pienaar, 1974).
Forecasting models will predict events that Simulation models perform many tasks,
happen in the future. Examples include the some of which are to solve differential equa-
times of sun- and moonrise (and set), the tions, repeatedly apply transition matrices or
high and low temperatures for future dates, repeatedly use random or pseudorandom
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44 D.E. Legg

number algorithms (Jeffers, 1978). Simu- the other hand, are models that mimic sys-
lation models are very important in that they tems through the use of symbolic logic. Such
are used to conduct ‘experiments’ under con- models are capable of expressing ideas and
ditions for which experiments could other- relations of great complexity while simulta-
wise not be done. To simulate experiments, neously retaining simplicity (Jeffers, 1978).
however, modellers must make assumptions Also, mathematical models are unambigu-
about how the system works because not all ous. However, mathematical models must
components are included in the model and continually be checked for the presence of
therefore the model is incomplete. As simu- contradictions (Jacobsen, 1984).
lations often involve the repetitive solution Mathematical models are often divided
of mathematical equations, as well as the into two groups: deterministic and stochas-
handling of many individuals in specified tic (Jeffers, 1978; Peck, 2000). Deterministic
populations, a computer is often needed to models make use of the branch of mathe-
conduct them (e.g. Dowd et al., 1984; matics that was developed when mathemat-
Nachapong et al., 1989; Culin et al., 1990; ics were first applied to physical problems
Berry et al., 1991; Follett et al., 1993; Flinn and and then to engineering problems (Jeffers,
Hagstrum, 1995; Legg, 2000; Legg et al., 2000, 1978; Logan, 1994). Sometimes deterministic
2002; Arthur et al., 2001). There are, however, models are composed of differential and dif-
some tasks that can be simulated without a ference equations (Jeffers, 1978); however,
computer (e.g. Penman and Chapman, 1982). deterministic models can be represented by
Analytic models are those for which explicit almost any kind of equation (Peck, 2000).
formulae are derived for predicted values or For example, if a 22% infestation of D. noxia
distributions (Jeffers, 1978). Also, analytic occurred on winter wheat in Wyoming,
models allow modellers to conduct in-depth USA, then application of the deterministic
explorations of model ‘behaviour’ (Peck, model:
2000). Analytic models tend to be less com-
Yield loss = EY × (0.5 × per cent
plex than are simulation models, though not
infestation/100) (1)
all are necessarily simple. Typical analytic
models are those used to describe gravity would determine the yield to be reduced by
(Peck, 2000) or those used in analysis of vari- 47.08 l/ha (prediction), where Yield loss is the
ance (ANOVA), regression and multivariate predicted yield loss (expressed in the same
analyses, as well as those that make use of units as EY), EY is the expected yield that
the theoretical probability distributions of would occur if D. noxia were not infesting
statistical applications (Jeffers, 1978). that field (say, 428 l/ha), and per cent infesta-
The second of Jeffers’ systems for classify- tion is the per cent of wheat tillers that are
ing models is based on a fundamental infested with at least 1.0 D. noxia (Legg et al.,
dichotomy between word models and math- 1993). A graphical representation of this
ematical models. Word models are purely model may be seen in Fig. 3.1.
verbal descriptions of events, processes and It has long been known that many mea-
relations. Often they are used to define the surements taken by scientists do not repre-
scope and depth of a problem. If systems are sent the actual or true values of, say,
extremely simple, word models will perform population means. Rather, they come from
well in mimicking them. However, if sys- distributions of measures that are taken on
tems are not very simple, word models fail each of those populations (Salsburg, 2001).
to mimic them. This is so because it requires For these measures, deterministic models
a great number of words to describe the cannot exactly determine or predict the true
complex relationships that occur in some values because the predictions will deviate
systems, as well as their feedbacks. In addi- from the true values by random amounts. In
tion, it is unfortunate that some words have such cases, the application of stochastic
more than one meaning; such ambiguity, models may be more appropriate in the
when it occurs, makes word models unten- modelling process. Stochastic models resem-
able (Jeffers, 1978). Mathematical models, on ble deterministic models to an extent, but
03IntpestManCh3.QXD 14/4/04 2:24 pm Page 45

Modelling in Successful Implementation of IPM 45

250
Yield loss = EY × (0.5 × per cent infestation/100)

200
Yield loss (l/ha)

150

100

50

0
0 20 40 60 80 100
Per cent Diuraphis noxia infestation

Fig. 3.1. Graphical representation of a deterministic model, which provides the exact yield losses that will
occur at given levels of Diuraphis noxia infestation on winter wheat.

they also contain symbols, terms or algo- these are referred to as multiple linear
rithms that represent the deviations of pre- regression models.
dicted from measured values. Moreover, the The errors (ξij) of linear statistical models
behaviour of these deviations can be and the errors (ξi) of regression models are
explained, to an extent, through probability known to have a mean of 0.0 and are used to
distributions. For example, one stochastic calculate variance (σ2), which describes the
model that is used when testing for equality ‘spread’ of the errors about the mean. Also,
of ‘treatments’ in a one-way ANOVA is as the ξij and ξi are assumed to conform to a
follows: specific probability distribution – in this case,
the normal distribution (Snedecor and
Yij = µ + τi + ξij [2]
Cochran, 1967). Use of stochastic models in
where Yij is a measure of the ith treatment the form of linear statistical models and
and jth replicate, µ is the grand average of regression models have been very important
the experiment, τi is the ith treatment effect in the successful implementation of IPM as
(i.e. the ith treatment average minus the their use has helped researchers to analyse
grand average), and ξij is the departure of the results of experiments (e.g. Legg et al.,
each measured Yij from its predicted value 1987), describe ecological relationships (e.g.
(i.e. µ + τi). These types of models are Legg and Chiang, 1984) and make predic-
referred to as linear statistical models tions in IPM settings (Plant and Stone, 1991).
(Cochran and Cox, 1957). Another stochastic Stochastic functions can be added to
model that is used when testing for relations almost any deterministic model. For exam-
between one dependent variable (Y) and one ple, if I wished to represent equation 1 as a
independent variable (X) is as follows: stochastic model, I would first research
which distribution describes the pattern of ξ
Yi = β0 + β1Xi + ξi [3]
(errors) about the predicted values, and then
where β0 and β1 are the true y intercept and establish whether that distribution holds
slope (Weisberg, 1980). These are sometimes true for all values of expected yield in the
referred to as regression models. Regression absence of D. noxia (i.e. EY), as well as for all
models can have more than one independent values of per cent infestation that would be
variable, as well as more than one slope, and encountered. Next I would establish whether
03IntpestManCh3.QXD 5/5/04 2:06 pm Page 46

46 D.E. Legg

0.010

Probability of departures occurring

0.008
Predicted

0.006

0.004

0.002

0.000
–150 –100 –50 0 50 100 150
Departures of measured losses from predicted (l/ha)

Fig. 3.2. Simulated probability distribution for the departures of measured yield losses (winter wheat) from
predicted yield losses due to infestation of the insect Diuraphis noxia.

both the spread of the errors and the value taken from a normal distribution with a
for s2 were constant over all combinations of mean of 0.0 and a s2 of 1849, to each pre-
EY and per cent infestation that would be dicted value (Press et al., 1986). Using these
encountered. Once those steps were com- simulated measures, I was then able to gen-
pleted, I would then construct a stochastic erate a graphical representation of model 4,
representation of Equation 1: where the predicted values (i.e. the ‘line’
from Equation 1) fails to equal each and
Yield lossi = EY ¥ (0.5 ¥ per cent every observed measure (dots) by some ran-
infestation/100) + xi [4]
dom amount (Fig. 3.3). As stochastic models
where the ‘spread’ of the xi is described by a are most useful when inadequate informa-
specific distribution with a constant value tion exists for determining the outcome of
for s2. If the spread of xi is described by the each and every measure, the outcome of the
normal distribution and the value for s2 is modelling effort should be expressed as the
constant at, say, 1849, then, for any value of chance of being within stated ‘low’ and
per cent infestation, the probabilities of ‘high’ values. For example, it is 90% certain
obtaining certain values for yield losses that yield loss will be from 93 to 121 l/ha
would be as shown in Fig. 3.2. Note that the when per cent infestation is 50.
probabilities of yield losses are greatest for The third of Jeffers’ systems for classify-
values of per cent infestation that are at or ing models involves what he terms ‘families
near the ‘predicted value’ and decline in a of models.’ These include the dynamic mod-
predictable manner as departures of mea- els, matrix models, multivariate models and
sured yield losses (abscissa) increase (Fig. optimization models. As pointed out by
3.2). The stochastic model, as represented by Jeffers (1978), these are not mutually exclu-
Equation 4, could be used for all kinds of sive as, for example, a dynamic model may
purposes, one of which is to simulate a also be a matrix model. The dynamic models
graphical representation of that model. This are those that emphasize change in the vari-
was done by calculating the predicted yield ables of a system with respect to one another.
losses for each per cent infestation, begin- They have the advantage of being very flexi-
ning with 0.0 and ending with 100, in incre- ble and can make use of many mathematical
ments of 1.0, and then adding a random xi, equations to describe the change in specific
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Modelling in Successful Implementation of IPM 47

300
Yield loss = EY × (0.5 × per cent infestation/100)
250

200
Yield loss (l/ha)

150

100

50

0
0 20 40 60 80 100
Per cent Diuraphis noxia infestation

Fig. 3.3. Simulated distribution of observed yield losses (dots) about predicted levels of yield losses (line)
due to infestation of the insect Diuraphis noxia on winter wheat.

parts of the system, relative to its other parts, marize information, they simplify proce-
at any point in time. The disadvantage of dures for solving complex problems and
dynamic models is that they do not usually they can be placed into computer programs
contain equations for all system components, that conduct repetitive and sometimes com-
as the description of most systems is incom- plex mathematical procedures. One disad-
plete. Dynamic models must therefore oper- vantage of using matrix models is that they
ate on the condition of making several make use of a special notation commonly
assumptions. After a dynamic model is used with linear algebra, so they can be con-
developed it can then be used to explore the fusing to non-mathematically oriented IPM
system either for further understanding or practitioners. Another disadvantage to the
for simulation. Examples of dynamic models use of matrix models is that some computer
include testing the effectiveness of pesticides programming skill may be needed to con-
(Schaalje, 1990), the growth of winter wheat struct and maintain them. One type of
in the Western Great Plains of the USA matrix model is that of Lewis (1942) and
(McMaster and Smika, 1988) and the popula- Leslie (1945). Another is that of the Markov
tion dynamics of the Douglas-fir tussock chain, which has been used to predict the
moth, Oryzia pseudotsugata (McDunnough) probability of grasshopper outbreaks in
(Berryman, 1991). Wyoming (Zimmerman, 1999). Multivariate
Matrix models use a mathematical tech- models describe the pattern of relationships
nique that is often referred to as linear alge- between several variables at the same time.
bra. The use of matrix models involves the These may be most useful for investigating
manipulation of values that are expressed in ecological relationships in IPM. Some time-
table-like entities, referred to as matrices, honoured multivariate techniques that have
and row- and column-like entities referred to been used are principal component analysis,
as vectors. These can be subjected to all sorts cluster analysis, discriminant analysis and
of mathematical operations and manipula- canonical analysis. Optimization models are
tions, and they most often mimic the popula- often used in operations research to search
tion dynamics of biological organisms. The for a mathematical maximum or minimum,
advantages of using matrix models lie in the whichever is optimal. For IPM, practitioners
fact that they are elegant in how they sum- often wish to maximize the return on a pest-
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48 D.E. Legg

management investment, so the application how complex or how simple does the model
of optimization models may be found in the need to be to satisfy its stated purpose?
calculation of some economic thresholds. After these questions are answered, it is
This is by no means a trivial task, as many always good to conduct a thorough review of
variables are often used, with many different the literature and find out, from a historical
values being tried for each, to find the ‘opti- perspective, what is known about the system
mum’. Obviously, intensive computer pro- of interest. Next, capture your ideas on how
gramming is involved with the use of the model should be structured in a concep-
optimization models. One example of using tual diagram. For this, I typically use flow
an optimization model in IPM involved soy- charts, as I am comfortable with writing com-
bean pest management (Hutchins et al., puter programs. However, just about any
1986). Another involved rangeland IPM with system of ‘boxes’ and arrows will be suffi-
respect to grasshopper infestations (Davis et cient to show the variables and their relations
al., 1992). to one another. After constructing a concep-
tual diagram, collect some data through
either a series of designed experiments or
The Modelling Process observational studies, or both; then use these
data to construct the ‘equations’ that mimic
the system. Note that this step ‘assumes’ that
Modelling can be thought of as involving
mathematical models are to be constructed to
two phases. Phase I is the conception of the
mimic the system. This is not necessarily so,
model, the construction of the model and the
as for some problems, constructing an ele-
validation and verification of the model.
gant word model or perhaps a knowledge-
Phase II is the implementation of the model.
based system may prove satisfactory. Next, a
detailed system is constructed for computer
modelling. Here again, it is assumed that the
Phase I
identified system is sufficiently complicated
for detailed analyses, as well as simulations,
The first phase often progresses in a stepwise to be needed. Next, the constructed model is
manner. To that end, both Jeffers (1978) and translated into a computer language for its
Teng (1987) have identified some of the steps use. Again, it is assumed that the model is
in the process, which include: (i) defining mathematical in nature, is very complex, or
and bounding the system that is to be mod- both, and should be embedded in a computer
elled; (ii) evaluating the historical and cur- program for ease of use. However, if the
rent knowledge about the system; (iii) model is not of a mathematical nature, it may
developing an initial conceptual (system) be represented by a knowledge-based sys-
model; (iv) collecting data and constructing tem. Further, if the model is non-mathemati-
equations to describe the system; (v) struc- cal and is simple in its depth or breadth, a
turing a detailed system model for computer decision table or decision tree may be suffi-
modelling; (vi) translating the model into a cient. Sensitivity analyses are then conducted
selected language for computer perfor- on the model by varying the values for cer-
mance; (vii) sensitivity analyses with verifi- tain parameters in the equations, as well as
cation and validation of the model; and (viii) the values for certain variables, to see if small
model experimentation. Defining and changes in those parameters or variables
bounding the system to be modelled is induce small or large changes in the model’s
extremely important and, arguably, may be performance. In a parallel effort, the model
the most important step in the process. The must be tested in the ‘real world’ to see if it
objectives of this step should include the will perform at an acceptable level on inde-
identification of how resolute the modelling pendent sets of data. Finally, once the model
process should be in order to address the has been so analysed, ‘verified’, and ‘vali-
stated problem, as well as the breadth of dated’, it can be used to perform experiments
scale that should be considered for develop- to see how the system will behave under new
ing and applying the model. In other words, sets of conditions.
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Modelling in Successful Implementation of IPM 49

This first phase to modelling, as challeng- ‘user’ will not implement a model unless the
ing as it may seem, can be conducted if you model also serves some political interests
have some training in and experience with (Kraemer, 1984).
modelling and if you possess a measure of
‘modelling intuition.’ In addition, having an
open mind (as to which types of models to Some Commonly Used Models in IPM
use), as well as using some creativity, can
also help in the modelling process (Jeffers, As was mentioned earlier, some of the most
1978). However, it is the second phase of commonly used models in IPM are the linear
modelling that has turned out to be some- statistical models of ANOVA as well as
what of a challenge. the regression models. Other commonly
used models include crop-growth and crop-
loss models, economic-threshold and injury-
level models, sampling models and
Phase II phenology models. Crop-growth and crop-
loss models are commonly used in IPM.
Model implementation involves three gen- Many crop-growth models are process models
eral steps: (i) introduction; (ii) adaptation; that attempt to function on the physiological
and (iii) incorporation by a specific agency, level (Pace and MacKenzie, 1987; Gutierrez,
company or groups of individuals (user) 2002). Most mimic plant growth by dividing
(Kraemer, 1984). To date, much more atten- the plant into its fundamental components,
tion has been given to the process of model such as leaf, stem and root biomass accumu-
development than has been given to the lation, as well as photosynthesis and respira-
process of model implementation. As stated tion. Some crop-growth models can be used
by Kraemer (1984), ‘Some posit that this mis- for crop-loss assessment, through simula-
placed attention has resulted in a generally tion. However, most crop-loss assessment is
low level of model use and model success’. conducted through the use of regression
Model introduction refers to a period during models (e.g. Sah and MacKenzie, 1987;
which the model is considered for adoption. Shane and Teng, 1987; Walker, 1987; Mesbah
During this step, some early initial testing et al., 1994). Economic-threshold models are
may be conducted and the results, along deterministic in nature and either contain or
with the introductory information that was are linked to population-dynamics models
presented with the model, are used to make (Chiang, 1979, 1983; Pedigo et al., 1986); eco-
the decision on model adoption. Model nomic injury-level models are also determin-
adaptation refers to the period after model istic in nature but do not contain the
introduction during which broader support population-dynamics link. Economic-thresh-
for the model is developed and plans are old models can also take the form of opti-
made for instructing and training practition- mization models. Many examples exist in the
ers on its use as well as the interpretation of literature of using the deterministic form of
its output. During model adaptation, the economic-threshold and economic injury-
model begins to be widely used. Model level models in IPM (e.g. Legg et al., 1993).
incorporation is the step at which the model Examples also exist for using optimization
is no longer a new entity but, rather, models when calculating economic thresh-
becomes a routine part of the user’s oper- olds in IPM (e.g. Davis et al., 1992).
ation. Research has shown that the success- Sampling models are particularly well
ful implementation of a model is influenced used in IPM. The acts of sampling and sam-
by at least three factors: (i) the inherent tech- ple inspection for assessing the abundance
nical characteristics of the model itself; (ii) and presence of pests can take several forms
the social setting in which the model is used; (Legg and Archer, 1998). However, the sam-
and (iii) the uses and impacts of the model as pling models serve to assist researchers and
experienced by the user (Kraemer, 1984). IPM practitioners in either the efficient esti-
Interestingly, it has been hypothesized that a mation of pest-population abundance or in
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50 D.E. Legg

the rapid classification of a pest population practitioners outside the classroom. I will
relative to an economic (or action) threshold. refer to the former as ‘teaching’ and the latter
The former are often referred to as precision- as ‘extension’ or ‘outreach’. First, I will
based sequential sampling models, as they address teaching.
serve to guide researchers (mostly) in deter- Teaching students about modelling actu-
mining how many samples are needed to ally has two perspectives: developing mod-
estimate a population average with a certain els and using models. Regarding the former,
predetermined level of precision (Hutchison, courses must be offered so that some stu-
1994); precision is a measure of the consis- dents will learn how to develop models. In
tency of the estimates of the average (Legg these courses, students learn how to use the
and Moon, 1994). The latter are often modelling process and how to apply some
referred to as classification-based sequential modelling techniques. It has been my experi-
sampling models, as they serve to quickly ence that most students who enrol in these
classify infestations as being ‘high’ or ‘low’ courses are agriculturalists, biologists or nat-
relative to a threshold value, thus requiring ural resource scientists who also have some
less sampling effort to make a pest-manage- quantitative skills. Consequently, the teach-
ment decision (Binns, 1994). ing of ‘modelling’ must be done from a con-
Finally, phenology models serve to pre- ceptual perspective using each of the
dict, mostly in real time, the phenological following techniques: verbal, visual, activity-
development of pest populations. These are oriented and mathematically oriented meth-
most useful for predicting the dates of first ods. The use of verbal methods requires that
or peak emergence or the emergence of a sec- I, as the instructor, use words to describe
ond generation of a pest. Almost all phenol- what is being done, why it is done and how
ogy models are driven by ambient it is done. For me, this requires careful
temperature, as plant-pathogenic organisms, thought and effort as such verbal descrip-
weeds and pestiferous insects are poikilo- tions are far longer and, in some cases, less
therms (Legg et al., 2002). However, some elegant than using mathematical descrip-
phenology models are driven by both tem- tions of the same. Nevertheless, verbal
perature and moisture (e.g. Legg and Brewer, descriptions must be incorporated into each
1995). Phenology models can be developed of the lectures as some students are very
either in the laboratory or in the field (Legg good listeners and learn primarily through
et al., 1998b). If they are developed in the lab- verbal descriptions. Visual methods are
oratory, the parameters may be meaningful extremely useful for some students as they
in a biological sense. However, care must be are ‘visually oriented’ and will understand
taken to ensure that the model output, when the concept or process only when a chart,
used for IPM purposes, reflects pest develop- graph or some other visual is used. Activity-
ment in the field. If they are developed in the oriented students are usually befuddled by
field, however, the parameters may not be either the verbal descriptions or the visual
biologically meaningful but they may pro- depictions I provide until I either work
vide acceptable predictions (Legg et al., through an example or assign them a special
1998a). project to be completed outside class (home-
work). Finally, there are some mathemati-
cally oriented students who are comfortable
Education and Modelling: Some Lessons with and learn through the symbolic lan-
Learned guage of mathematics. For these, I provide
explanations of processes and techniques
Teaching people how to develop and use using such tools as manipulated equations
models is important for producing the next (all kinds), integrals and algebra.
generation of modellers and ensuring that Teaching students how to use models is
models will be used by IPM practitioners. necessarily different from teaching students
Here, I distinguish between teaching stu- how to develop models. This is so because
dents in the classroom and educating IPM these students are agriculturalists, biologists
03IntpestManCh3.QXD 14/4/04 2:24 pm Page 51

Modelling in Successful Implementation of IPM 51

or natural resource scientists who have few solve agricultural problems because much of
quantitative skills. Instead, I teach these stu- the present understanding of these systems
dents a little about developing models but a is qualitative and is based on experience
lot about using models. Also, these students (Plant and Stone, 1991). Such knowledge is
need to be taught to interpret the results or not easily quantifiable, which makes it diffi-
‘output’ from models, as well as to ‘experi- cult to construct mathematical models. In his
ment’ with them by posing ‘what if ’ scenar- 1994 article, Logan eloquently expressed
ios and rerunning the models for each how the ‘infatuation’ that IPM researchers
scenario. and practitioners had with complex, mathe-
Finally, extending models to IPM practi- matical simulation models waned during the
tioners necessarily differs from teaching, as 1980s, due in part to the unrealistic expecta-
practitioners do not enrol in courses and tions that were put forward by the propo-
therefore cannot be forced to use models for nents of those models, the lack of the
the conduct of pest management. Instead, I models’ ‘predictive power’ and the environ-
have learned that the development and ment in which some models were put
implementation phases of modelling must be together. In the general modelling literature,
conducted with regular input from the peo- Richardson (1984) has summarized the
ple who will use those models. These people essence of some papers by calling for a more
include representatives from producer inclusive approach to systems definitions
groups, some university personnel and, per- and analysis, one that he termed ‘holism’.
haps, some government officials. Also, the Further, Richardson (1984) articulated the
administrator from the modeller’s unit may perception that dynamic models (and mod-
be important as that individual provides ellers) are in the process of a ‘shift of para-
resources for maintaining the models. digm’ away from the classic application of
Anyway, these individuals must work with reductionism, or Cartesian disassembly of
the modellers because they have an interest systems, to a more inclusive approach to
in developing and maintaining the models modelling those systems. In the IPM litera-
as well as the computer programs in ture, this shift appears to be headed towards
which they reside. This kind of ‘partnership’ something called a ‘whole-system’, within
is essential for developing products that which agriculture is viewed as an ecosystem
are useful to and will be used by IPM that involves habitat management, crop
practitioners. attributes and multitrophic interactions as
some of the principles that will guide deci-
sion making and promote agricultural sus-
The Future of Modelling in IPM tainability (Rains et al., 2002). Modelling
changes in the landscape, using the science
Given the importance of modelling and sys- of geographical information systems, also
tems analysis in IPM, both should play appear likely. Access to models and the
important future roles. However, the types of weather data that are needed to run the
models that may be used and the approach models will be increasingly made avail-
to designing and implementing those mod- able on the Worldwide Web (e.g.
els may be different from the types of models http://okmesonet.ocs.ou.edu/) (Brock et al.,
that are currently being used and the 1995). Finally, there are the knowledge-based
approaches that are currently being systems. These are computer programs that
employed by modellers. Plant and Stone solve complex problems within some
(1991) have pointed out that traditional sys- defined area of knowledge (knowledge
tems-level problems have been solved using domain). Knowledge-based systems differ
systems analysis, along with mathematical from traditional mathematical models in that
models, which were central to the IPM pro- they are designed to mimic the human rea-
jects of the 1970s and 1980s. More recently, soning processes, which rely on logic, beliefs,
however, some emphasis has been placed on generalized rules, opinion, and experience;
the use of qualitative methods (or models) to these are typically not quantifiable (Plant
03IntpestManCh3.QXD 14/4/04 2:24 pm Page 52

52 D.E. Legg

and Stone, 1991). Relatively new in their attention by teams of experts, programmers,
development, knowledge-based systems are and ‘knowledge engineers’ to keep them cur-
extremely flexible and inexpensive to con- rent and valid.
struct. They do, however, require constant

References

Arthur, F.H., Throne, J.E., Maier, D.E. and Montross, M.D. (2001) Impact of aeration on maize weevil
(Coleoptera: Curculionidae) populations in corn stored in the northern United States: simulation
studies. American Entomologist 47, 104–110.
Bawden, R.J., Macadam, R.D., Packham, R.J. and Valentine, I. (1984) Systems thinking and practices in
the education of agriculturalists. Agricultural Systems 13, 205–225.
Berry, J.S., Holtzer, T.O. and Norman, J.M. (1991) Experiments using a simulation model of the banks
grass mite (Acari: Tetranychidae) and the predatory mite Neoseiulus fallacies (Acari: Phytoseiidae) in
a corn microenvironment. Environmental Entomology 20, 1074–1078.
Berryman, A.A. (1991) Population theory: an essential ingredient in pest prediction, management, and
policy-making. American Entomologist 37, 138–142.
Berryman, A.A. and Pienaar, L.V. (1974) Simulation: a powerful method of investigating the dynamics and
management of insect populations. Environmental Entomology 3, 199–207.
Binns, M.R. (1994) Sequential sampling for classifying pest status. In: Pedigo, L.P. and Buntin, G.D. (eds)
Handbook of Sampling Methods for Arthropods in Agriculture. CRC Press, Boca Raton, Florida,
pp. 137–174.
Brock, F.V., Crawford, K.C., Elliott, R.L., Cuperus, G.W., Stadler, S.J., Johnson, H.L. and Eilts, M.D. (1995)
The Oklahoma mesonet: a technical overview. Journal of Atmospheric and Oceanic Technology 12, 5–19.
Chiang, H.C. (1979) A general model of the economic threshold level of pest populations. Food and
Agricultural Organization of the United Nations Plant Protection Bulletin 27, 71–73.
Chiang, H.C. (1983) Factors to be considered in refining a general model of economic threshold.
Entomophaga 27, 99–103.
Cochran, W.G. and Cox, G.M. (1957) Experimental Designs, 2nd edn. John Wiley Press, New York, 611 pp.
Culin, J., Brown, S., Rogers, J., Scarborough, D., Swift, A., Cotterill, B. and Kovach, J. (1990) A simulation
model examining boll weevil dispersal: historical and current situations. Environmental Entomology
19, 195–208.
Davis, R.M., Skold, M.D., Berry, J.S. and Kemp, W.P. (1992) The economic threshold for grasshopper con-
trol on public rangelands. Journal of Agricultural and Resource Economics 17, 56–65.
Dowd, P.F., Sparks, T.C. and Mitchell, F.L. (1984) A microcomputer simulation program for demonstrat-
ing the development of insecticide resistance. American Entomologist 30, 37–41.
Flinn, P.W. and Hagstrum, D.W. (1995) Simulation model of Cephalonomia waterstoni (Hymenoptera:
Bethylidae) parasitizing the rusty grain beetle (Coleoptera: Cucujidae). Environmental Entomology 24,
1608–1615.
Follett, P.A., Kennedy, G.A. and Gould, F. (1993) REPO: a simulation model that explores the Colorado
potato beetle (Coleoptera: Chrysomelidae) adaptation to insecticides. Environmental Entomology 22,
283–296.
Gelovani, V.A. (1984) An interactive modelling system as a tool for analyzing complex socio-economic
problems. In: Richardson, J. (ed.) Models of Reality Shaping Thought and Action. Lomond Press, Mt
Airy, Maryland, pp. 75–86.
Gutierrez, A.P. (2002) Modeling pest management. In: Pimentel, D. (ed.) Encyclopedia of Pest Management.
Marcel Dekker, New York, pp. 500–503.
Hess, G.R. (1996) To analyse or to simulate, is that the question? American Entomologist 42, 14–16.
Hutchins, S.H., Higley, L.G., Pedigo, L.P. and Calkins, P.H. (1986) Linear programming model to opti-
mize management decisions with multiple pests: an integrated soybean pest management example.
Bulletin of the Entomological Society of America 32, 96–102.
Hutchison, W.D. (1994) Sequential sampling to determine population density. In: Pedigo, L.P. and Buntin,
G.D. (eds) Handbook of Sampling Methods for Arthropods in Agriculture. CRC Press, Boca Raton,
Florida, pp. 207–243.
Jacobsen, E. (1984) On logic, axioms, theorems, paradoxes and proofs. In: Richardson, J. (ed.) Models of
Reality Shaping Thought and Action. Lomond Press, Mt Airy, Maryland, pp. 71–73.
03IntpestManCh3.QXD 14/4/04 2:24 pm Page 53

Modelling in Successful Implementation of IPM 53

Jeffers, J.N.R. (1978) An Introduction to Systems Analysis, with Ecological Applications. Edward Arnold Press,
London, 198 pp.
Jeffers, J.N.R. (1984) The development of models in urban and regional planning. In: Richardson, J. (ed.)
Models of Reality Shaping Thought and Action. Lomond Press, Mt Airy, Maryland, pp. 87–99.
Kraemer, K.L. (1984) The politics of model implementation. In: Richardson, J. (ed.) Models of Reality
Shaping Thought and Action. Lomond Press, Mt Airy, Maryland, pp. 131–160.
Legg, D.E. (2000) Tables of computer-simulated errors for binomial sequential sampling plans. In:
Pandalai, S.G. (ed.) Recent Research Developments in Entomology, Vol IV. Research Signpost Press,
Trivandrum, pp. 95–106.
Legg, D.E. and Archer, T.L. (1998) Sampling methods, economic injury levels, and economic thresholds
for the Russian wheat aphid (Homoptera: Aphididae). In: Quisenberry, S.S. and Peairs, F.B. (eds)
Response Model for an Introduced Pest – the Russian Wheat Aphid. Thomas Say Publications in
Entomology, Proceedings, Entomological Society of America, Lanham, Maryland, pp. 313–336.
Legg, D.E. and Brewer, M.J. (1995) Relating within-season Russian wheat aphid (Homoptera: Aphididae)
population growth in dryland winter wheat to heat units and rainfall. Journal of the Kansas
Entomological Society 68, 149–158.
Legg, D.E. and Chiang, H.C. (1984) European corn borer (Lepidoptera: Pyralidae) infestations: predicting
second generation egg masses from blacklight trap captures and relating their abundance to several
corn crop characters. Journal of Economic Entomology 77, 1432–1438.
Legg, D.E. and Moon, R.D. (1994) Bias and variability in statistical estimates. In: Pedigo, L.P. and Buntin,
G.D. (eds) Handbook of Sampling Methods for Arthropods in Agriculture. CRC Press, Boca Raton,
Florida, pp. 55–69.
Legg, D.E., Barney, R.J., Tipping, P.W. and Rodriguez, J.G. (1987) Preferred grain quantity and insect den-
sity for maize weevil (Coleoptera: Curculionidae) interaction studies. Journal of Economic
Entomology, 80, 388–393.
Legg, D.E., Wangberg, J.K. and Kumar, R. (1993) Decision support software for implementation of
Russian wheat aphid economic injury levels and thresholds. Journal of Agricultural Entomology 10,
205–213.
Legg, D.E., Van Vleet, S.M., Lloyd, J.E. and Zimmerman, K.M. (1998a) Calculating lower developmental
thresholds of insects from field studies. Recent Research Developments in Entomology 2, 163–172.
Legg, D.E., Struttmann, J.M., Van Vleet, S.M. and Lloyd, J.E. (1998b) Bias and variability in lower
developmental thresholds estimated from field studies. Journal of Economic Entomology 91,
891–898.
Legg, D.E., Van Vleet, S.M. and Lloyd, J.E. (2000) Simulated predictions of insect phenological events
made by using mean and median functional lower developmental thresholds. Journal of Economic
Entomology 93, 658–661.
Legg, D.E., Van Vleet, S.M., Ragsdale, D.W., Hansen, R.W., Chen, B.M., Skinner, L. and Lloyd, J.E. (2002)
Required number of location-years for estimating functional lower developmental thresholds and
required thermal summations of insects: first emergence of adult Aphthona nigriscutis Foudras as an
example. International Journal of Pest Management 48, 147–154.
Leslie, P.H. (1945) On the use of matrices in certain population mathematics. Biometrika 33, 183–212.
Lewis, E.G. (1942) On the generation and growth of a population. Sankhya 6, 93–96.
Logan, J.A. (1994) In defence of big ugly models. American Entomologist 40, 202–207.
McMaster, G.S. and Smika, D.E. (1988) Estimation and evaluation of winter wheat phenology in the cen-
tral great plains. Agricultural and Forest Meteorology 43, 1–18.
Manetsch, T.J. and Park, G.L. (1982) System Analysis and Simulation with Application to Economic and Social
Systems, Vol. I, 4th edn. Engineering Library, Michigan State University, East Lansing, Michigan, 52
pp.
Mesbah, A., Miller, S.D., Fornstrom, K.G. and Legg, D.E. (1994) Kochia (Kochia scoparia) and green foxtail
(Setaria viridis) interference in sugarbeets. Weed Technology 8, 754–759.
Miller, G.G. and Miller, J.L. (1984) The earth as a system. In: Richardson, J. (ed.) Models of Reality Shaping
Thought and Action. Lomond Press, Mt Airy, Maryland, pp. 19–49.
Nachapong, M., Legg, D.E., Kittiboonya, S. and Wangboonkong, S. (1989) Validation of computer-simu-
lated presence-absence sequential sampling plans for the cotton bollworm (Heliothis armigera)
(Hübner) in cotton. Thai Journal of Agricultural Science 22, 293–302.
Nachman, G. (1981) A mathematical model of the functional relationship between density and spatial
distribution of a population. Journal of Animal Ecology 50, 453–460.
03IntpestManCh3.QXD 14/4/04 2:24 pm Page 54

54 D.E. Legg

Pace, M.E. and MacKenzie, D.R. (1987) Modeling of crop growth and yield for loss assessment. In: Teng,
P.S. (ed.) Crop Loss Assessment and Pest Management. American Phytopathological Society Press, St
Paul, Minnesota, pp. 30–36.
Peck, S.L. (2000) A tutorial for understanding ecological modelling papers for the nonmodeler. American
Entomologist 46, 40–49.
Pedigo, L.P., Hutchins, S.H. and Higley, L.G. (1986) Economic injury levels in theory and practice. Annual
Review of Entomology 31, 341–368.
Penman, D.R. and Chapman, R.B. (1982) Design of a field-sampling simulator. Bulletin of the Entomological
Society of America 28, 143–145.
Plant, R.E. and Stone, N.D. (1991) Knowledge-based Systems in Agriculture. McGraw-Hill Press, New York,
364 pp.
Press, W.H., Flannery, B.P., Teukolsky, S.A. and Vetterling, W.T. (1986) Numerical Recipes. Cambridge
University Press, New York, 203 pp.
Rains, G.C., Olson, D.M., Lewis, J.W. and Tumlinson, J.H. (2002) Systems management. In: Pimentel, D.
(ed.) Encyclopedia of Pest Management. Marcel Dekker, New York, pp. 826–828.
Richardson, J.G. (1984) A primer of model systems. In: Richardson, J. (ed.) Models of Reality Shaping
Thought and Action. Lomond Press, Mt Airy, Maryland, pp. 3–18.
Sah, D.N. and MacKenzie, D.R. (1987) Methods of generating different levels of disease epidemics in loss
experiments. In: Teng, P.S. (ed.) Crop Loss Assessment and Pest Management. American
Phytopathological Society Press, St Paul, Minnesota, pp. 90–96.
Salsburg, D. (2001) The Lady Tasting Tea. Freeman Press, New York, 24 pp.
Schaalje, G.B. (1990) Dynamic models of pesticide effectiveness. Environmental Entomology 19, 440–447.
Shane, W.W. and Teng, P.S. (1987) Generating the database for disease-loss modelling. In: Teng, P.S. (ed.)
Crop Loss Assessment and Pest Management. American Phytopathological Society Press, St Paul,
Minnesota, pp. 82–89.
Smith, M.J. (1974) Models in Ecology. Cambridge University Press, London, 145 pp.
Snedecor, G.W. and Cochran, W.G. (1967) Statistical Methods, 6th edn. Iowa State University Press, Ames,
Iowa, 593 pp.
Stern, V.M., Smith, R.F., Van Den Bosch, R. and Hagen, K.S. (1959) The integrated control concept.
Hilgardia 29, 81–101.
Stone, N.D., Coulson, R.N., Frisbie, R.E. and Loh, D.K. (1986) Expert systems in entomology: three
approaches to problem solving. American Entomologist 32, 161–166.
Taylor, L.R. (1961) Aggregation, variance and the mean. Nature 189, 732–735.
Teng, P.S. (1981) Validation of computer models of plant disease epidemics: a review of philosophy and
methodology. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz 88, 49–63.
Teng, P.S. (1987) The systems approach to pest management. In: Teng, P.S. (ed.) Crop Loss Assessment and
Pest Management. American Phytopathological Society Press, St Paul, Minnesota, pp. 160–167.
Walker, P.T. (1987) Quantifying the relationship between insect populations, damage, yield, and eco-
nomic thresholds. In: Teng, P.S. (ed.) Crop Loss Assessment and Pest Management. American
Phytopathological Society Press, St Paul, Minnesota, pp.114–125.
Weisberg, S. (1980) Applied Linear Regression. John Wiley Press, New York, 283 pp.
Zimmerman, K.M. (1999) A spatial model for markov chain analysis of grasshopper population dynam-
ics in Wyoming. MS thesis, University of Wyoming, Laramie, Wyoming, 91 pp.
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4 Manipulation of Tritrophic Interactions

for IPM

Robert H.J. Verkerk

Department of Biological Sciences, Imperial College London,
Silwood Park, Ascot, Berkshire, SL5 7PY, UK
E-mail: [email protected]

Introduction NATURAL ENEMY Fourth trophic level

Until recently, there has been a tendency by

those involved in integrated pest manage- NATURAL ENEMY
ment (IPM) or integrated crop management Third trophic level
Extrinsic
(ICM) (Meerman et al., 1996; Denyer, 2000) to plant
resistance
be principally concerned with effects on her-
bivores or interactions between just two HERBIVORE Second trophic level
trophic levels. However, interest in the Intrinsic
plant
importance of interactions between the three resistance
or four trophic levels that characterize most PLANT First trophic level
natural systems and agroecosystems has
been increasing rapidly during the last two Fig. 4.1. Simplified multitrophic interactions in
decades. natural and agroecosystems (adapted from Price,
1986).
Historically, the chemical-control expo-
nent has rarely been concerned about host-
plant effects, and has been interested the abundance of and damage caused by
primarily in chemical impacts on herbivores herbivorous pests
(the second trophic level; Fig. 4.1) and Following from this, the plant-resistance
sometimes side effects on natural enemies specialist has tended to have little interest in
(third trophic level; Fig. 4.1). Understanding interactions between the first, second and
of interactions between the levels has not third trophic levels, while the biological con-
been prioritized (Thomas, 1999). Most host- trol specialist, in turn, has given only passing
plant resistance specialists are concerned attention to interactions between the first and
mainly with ways in which resistance fac- third trophic levels. In the case of some nat-
tors within or on the plant (first trophic ural systems and many fewer crop-based sys-
level; Fig. 4.1) affect the development of tems, interactions between the third and
herbivores, while the biological control spe- fourth trophic levels have been well studied
cialist tends to concentrate on ways in (e.g. parasitoid–hyperparasitoid interactions).
which predators, parasitoids or pathogens It is interesting that many traditional cul-
(third trophic level; Fig. 4.1) are able to limit tural practices – one of the less-studied

© CAB International 2004. Integrated Pest Management: Potential, Constraints and Challenges
(eds O. Koul, G.S. Dhaliwal and G.W. Cuperus) 55
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56 R.H.J. Verkerk

aspects of pest-management science – exert across different trophic levels in order to

their effects through complex multitrophic develop more sustainable approaches to pest
interactions, but it is exactly this complexity management. Some of the most relevant
that makes such systems difficult to assess approaches are discussed in this chapter and
experimentally or validate conclusively are supported with examples. The chapter
across a broad range of environments. restricts itself to consideration of tritrophic
The reality is that agroecosystems, espe- aspects of arthropod pest management as
cially perennial ones, which are not subject to arthropods have, to date been much better
intensive pesticide regimes, like natural sys- studied in this regard than pathogens.
tems, contain much more than simple
tritrophic interactions. They support food-web
interactions of varying complexity across mul- Identifying Areas for Manipulation
titrophic levels (Berryman et al., 1995; Janssen
et al., 1998; Letourneau and Andow, 1999). There are a number of key areas where
Modelling approaches, using empirical data manipulation of crop–pest–natural-enemy
where these are available, are contributing interactions could provide substantial bene-
substantially to the understanding of interac- fits in pest-management systems. The signifi-
tions in agroecosystems (Gutierrez, 1996). cant and growing evidence from
Research on tritrophic interactions relating fundamental research in certain areas, e.g.
to arthropod herbivores has expanded allelochemically mediated interactions, hold
rapidly since the late 1970s (e.g. Bergman and substantial promise with regard to the devel-
Tingey, 1979; Price et al., 1980; Strong et al., opment of novel IPM or ICM techniques, but
1984; Boethel and Eikenbary, 1986; Price, practical methods have yet to be developed
1986; Duffey and Bloem, 1987; Barbosa, 1988; for wide-scale application. In other areas,
Gutierrez et al., 1988; Nordlund et al., 1988; techniques involving tritrophic interactions
Whitman, 1988; Smith, 1989; Price et al., 1990; are already practised. Although these areas
Fritz, 1992; Hare, 1992; Vet and Dicke, 1992; are considered discretely under different
Steinberg et al., 1993; Godfray, 1994; Mattiacci headings, it is important to appreciate the
et al., 1994, 1995; Dicke et al., 1998; Du et al., considerable overlap between different tech-
1998; Redman and Scriber, 2000; Walker and niques or approaches. Some of the conflicts
Jones, 2001). However, as implied above, or paradoxes that may be inherent in certain
there have been relatively few empirical forms of manipulation, are also outlined.
studies on crop-based systems (van Emden,
1987, 1995; van Emden and Wratten, 1991;
Hare, 1992; Shimoda et al., 1997) and rigorous Manipulation of host-plant quality
field studies have only been conducted in the
last few years (Eigenbrode et al., 1995; For many years, there was a widely held
Camara, 1997; Fritz et al., 1997; Karban and view that host-plant resistance should be
EnglishLoeb, 1997; Nwanze et al., 1998; seen as an integral component of IPM pro-
Hufbauer and Via, 1999; Theodoratus and grammes, but it has been demonstrated that
Bowers, 1999; Lill and Marquis, 2001; Chen host-plant resistance is by no means always
and Welter, 2002; Thaler, 2002). compatible with biological control (van
Studies in the tritrophic area are taking on Emden, 1991, 1995; Hare, 1992; Thomas and
a new significance as less pesticide-depen- Waage, 1994). Hare (1992), for example, cited
dent, more ecologically based approaches to 16 studies where interactions between resis-
the management of pests are being demanded tant crop varieties and natural enemies (par-
(Poppy, 1997; Bottrell et al., 1998; Verkerk et al., asitoids) were studied and the outcomes
1998). As knowledge of interactions across show a spectrum of interactions, ranging
multitrophic systems both in nature and in from synergistic, to additive, to none appar-
agroecosystems expands, researchers and ent through to disruptive or antagonistic.
pest-management practitioners are beginning Negative interactions can occur because of
to find ways of manipulating interactions the presence of secondary chemicals that are
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Manipulation of Tritrophic Interactions 57

ingested or sequestered by natural enemies resistance–natural-enemy interactions. The

feeding on hosts present on resistant or par- authors emphasize that many of the interac-
tially resistant plants (Godfray, 1994). tions that occur in field systems are poorly
Specific toxic components in partially resis- understood and that combining natural ene-
tant soy bean plants can be particularly mies and plant resistance may slow the
problematic in this regard (Orr and Boethel, adaptation of some insect pests, while it may
1985). van Emden (1995) suggests that nega- speed up adaptations of others.
tive interactions between potentially toxic Feeny (1976) and others (e.g. Moran and
secondary plant compounds and natural Hamilton, 1980; Price et al., 1980; Leather,
enemies are less likely in the case of natural 1985) proposed that sublethal defences (e.g.
enemies using phloem-feeding insects, such ‘digestibility reducers’) in plants increase
as aphids, as prey compared with chewing herbivore exposure to natural enemies: the
insects because, when present, these com- slower the growth, the higher the mortality.
pounds are quite often at low concentrations This aside, several studies have shown that
or absent in the phloem (Ryan et al., 1990). natural enemies foraging on leaf surfaces
van Emden (1995) cites a number of stud- dislodge potential (aphid) prey to a greater
ies showing that partial plant resistance or extent on partially resistant compared with
environmental variables (e.g. reduced nitro- susceptible host plants. Gowling and van
gen fertilization of plants) can not only Emden (1994) showed this for Metopolophium
reduce aphid size and fecundity but may dirhodum (Walker) and the parasitoid A.
also substantially reduce (by c. 30%) the rhopalosiphi (on partially resistant and sus-
weight and fecundity of female parasitoids, ceptible cultivars of wheat) in the
Aphidius rhopalosiphi De Stefani Perez, emerg- glasshouse, as well as for Brevicoryne brassi-
ing from the aphids. Also of potential con- cae (Linnaeus) on Brussels sprouts in the
cern to the biological control practitioner field, where hover flies (Diptera: Syrphidae)
were the effects of plant resistance on sex were the main predatory group.
ratio (10% fewer females on a partially resis- However, field studies on galling sawflies
tant compared with a susceptible wheat vari- of willow showed the opposite phenomenon,
ety) and parasitoid emergence success from i.e. that parasitism was greater in faster-
aphid mummies (c. 20% reduction). A subse- growing larvae, implying that sublethal
quent study has shown that linear furano- plant defences remain a paradox (Clancy
coumarins (secondary plant metabolites) in and Price, 1987). Faster-growing larvae of the
celery plants selectively and adversely affect pyralid moth Omphalocerca munroei that fed
the polyembryonic encyrtid parasitoid, on young leaves of their host plants (Asimina
Copidosoma floridanum, while not affecting its spp.) were also observed to be more vulnera-
larval noctuid host, Trichoplusia ni (Hübner) ble to predators than their slower-growing
(Reitz and Trumble, 1996). Negative interac- counterparts that fed on the preferred, older
tions may also be caused by physical (or leaves of the same host plants (Damman,
chemical) factors such leaf toughness, cuticle 1987). The latter studies support the view of
thickness, trichomes (glandular and non- Schultz (1983) that bigger individuals are a
glandular), galls and plant architecture more profitable resource for predators.
(Price, 1986). However, galling sawflies and the pyralid
In terms of positive interactions that can moth (a gregarious shelter-builder) both live
be manipulated, van Emden and Wearing in relatively protected but highly apparent
(1965) were the first to suggest that partial environments (i.e. vulnerable to discovery by
plant resistance, in combination with natural their enemies) and may not be ideal systems
enemies, may give economic levels of control to test the slow growth/higher mortality
for some agricultural insect pests. However, hypothesis (Leather and Walsh, 1993). To
since this time, a considerable body of work examine this hypothesis, the latter authors
has accumulated regarding mechanisms that infested ‘poor’- and ‘good’-quality hosts
both support and oppose this notion. Bottrell (Pinus contorta of two different origins) with
et al. (1998) provide a useful review of plant- the pine beauty moth, whose larvae are more
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58 R.H.J. Verkerk

exposed on foliage. They found that larvae Elkinton, 2000). When larvae fed on old
reared on the ‘good’ host, in the absence of leaves, i.e. larvae released long before bud-
predators, were heavier and more numerous burst, the adult fecundity of the moth
than those reared in a similar manner on the declined owing to the low quality of the host
‘poor’ host. However, with populations suf- plant. However, where the leaves were old,
fering predation, it was found that these the dispersal rate (by ‘ballooning’) was
heavier individuals had been the ones greater than from young leaves and, since
favoured by the predators. This result sug- dispersal reduces herbivore density, natural-
gests that the bigger and healthier the host, enemy-induced density-dependent mortality
the greater the reward for the predator (see was also lower (Hunter and Elkinton, 2000).
Schultz, 1983), and that poor nutritional sta- This shows that first and third trophic-level-
tus may be a liability to the plant in these cir- mediated effects may counteract each other
cumstances rather than an asset. in relation to herbivore survival or abun-
Host-plant quality may affect the influ- dance.
ence of pathogens of insect pests. Differential Finally, host-plant quality can have
susceptibility to a nuclear polyhedrosis virus important implications for omnivores. This
(NPV) was found for two pests, beet army- has been well studied in the case of western
worm, Spodoptera exigua (Hübner), and flower thrips, Frankliniella occidentalis
maize earworm, Helicoverpa zea (Boddie), fed (Pergande), which eats both animal prey
on different host plants. Beet armyworm was (mite eggs) and host-plant foliage. According
most susceptible to the virus on tomato, least to foraging theory, omnivores balance their
susceptible on cotton and intermediate on diet as a result of food quality, nutritional
cole-wort, while maize earworm was most need and the availability of alternative
susceptible on maize, least on cotton and foods. Although it has been shown that
intermediate on bean (Farrar and Ridgway, reducing plant quality can cause omnivores
2000). The greenhouse whitefly, Trialeurodes to shift towards relatively more predation
vaporariorum (Westwood) was found to be than herbivory (Agrawal et al., 1999), it was
considerably more susceptible to the fungal later shown that where plant resistance has
pathogens Beauveria bassiana and been induced by herbivory (induced plant
Paecilomyces fumosoroseus when reared on resistance), reduced prey density and quality
cucumber compared with tomato may antagonize this shift towards increased
(Poprawski et al., 2000). predation (Agrawal and Klein, 2000).
Host-plant variation has been shown to
contribute substantially to the toxicity of
endotoxins of the bacterial pathogen Bacillus Allelochemicals
thuringiensis (Bt). More than fivefold differ-
ences in toxicity of Bt subsp. aizawai were Allelochemicals are those chemicals that
found to diamondback moth, Plutella mediate interspecific interactions and are
xylostella (Linnaeus), larvae when exposed to distinguished from pheromones, which
treated leaves of susceptible and partially mediate intraspecific interactions. They have
resistant common cabbage (Brassica oleracea been shown to be among the most important
var. capitata) (Verkerk and Wright, 1996a), factors controlling the sequence of natural-
while a more than tenfold variation in toxic- enemy host-searching and selection behav-
ity of Bt subsp. kurstaki was shown to larvae iours, and this has been particularly well
of gypsy moth, Lymantria dispar (Linnaeus), studied in the case of parasitoids (Vinson,
when exposed on a range of different host 1984; Lewis and Martin, 1990; Turlings and
plants (Farrar et al., 1996). Tumlinson, 1991; Whitman and Eller, 1992;
There have been few studies looking at Tumlinson et al., 1993).
population-level effects of variable plant The induction of plant defence through
phenology. In one such study, the timing of the release of allelochemicals as a response to
egg hatch of the gypsy moth, L. dispar was herbivory has been amply demonstrated
manipulated in the field (Hunter and (e.g. Whitman and Eller, 1992; Steinberg et
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Manipulation of Tritrophic Interactions 59

al., 1993; Takabayashi et al., 1994; Mattiacci et areas of allelochemical manipulation, draw-
al., 1995; Du et al., 1996, 1998; Dicke et al., ing heavily on research on herbivorous and
1998; van Poecke et al., 2001). Such allelo- predatory mite systems. These authors cite
chemicals are often referred to as syn- work relating to: enhancement of searching
omones, given that both the plant (emitter) efficiency or triggering specific search modes
and the natural enemy (receiver) benefit in natural enemies; increasing host accept-
from the chemical communication. It has ability to natural enemies in mass rearing;
been shown that the allelochemicals released using the response to an allelochemical as a
following herbivory not only influence spe- criterion in the selection of natural enemies
cialist and/or generalist natural enemies but in control programmes; ensuring quality
can also affect the behaviour of the herbivore control of mass-reared natural enemies; and
and, through plant–plant communication, breeding of plant cultivars that have high
can make adjacent plants more attractive to emission rates of natural-enemy-attracting
natural enemies. The plant emissions can be synomones.
herbivore-specific. De Moraes et al. (1998) Aphid parasitoids may be ‘conditioned’
showed that tobacco, cotton and maize during their larval stage to the specific host-
plants each released distinct blends of plant variety on which the parasitoid’s host
volatiles when they were exposed to her- is reared (Braimah and van Emden, 1994;
bivory by two closely related Lepidoptera van Emden, 1995). This is potentially of con-
larvae, Heliothis virescens (Fabricius) and H. siderable relevance to biological control since
zea. In chemical/behavioural assays, these the introduction of a crop variety with resis-
authors demonstrated that the specialist par- tance based on an allelochemical may actu-
asitoid Cardiochiles nigriceps Viereck was able ally deter parasitoids and the existence of
to discriminate between these blends, being host-plant conditioning could offset the use-
attracted specifically to its own host, H. fulness of weed-based reservoirs of
virescens. polyphagous parasitoids (van Emden, 1995).
Despite recent progress and an abun- This phenomenon may also cause subopti-
dance of research in the area of allelochemi- mal parasitism following introduction of an
cally mediated tritrophic interactions, there exotic parasitoid where mass rearing has
have yet to be significant advances in the occurred on a host-plant variety different
applied area, so there are few examples of from that constituting the target crop.
synomones being used practically as an IPM The rapidly growing body of work on
technique. Lewis and Nordlund (1984) allelochemicals demonstrates that the use of
demonstrated the potential of synomone- natural-enemy-attracting chemicals pro-
mediated attraction of natural enemies by duced by plants may hold substantial
applying synomone-containing extracts from promise for enhancement of biological con-
maize and tomato. Parasitism by Telenomus trol. This is most likely either through aug-
remus Nixon of autumn armyworm, mentation (field application of synomones)
Spodoptera frugiperda (J.E. Smith) was or by breeding of plants with elevated emis-
increased twofold on plants treated with sion rates of synomones (see Genetic manip-
extracts, compared with the untreated ulation section below).
plants. Limited field studies by Altieri et al.
(1981) found that application of a water-
based extract from an Amaranthus sp. signifi- Crop diversification
cantly increased parasitism of H. zea eggs by
naturally occurring Trichogramma spp. in var- The diversification of crop and neighbouring
ious crops, including soybean, cowpea, environments is widely regarded as benefit-
tomato and cotton. ing biological control and sustainable agri-
The prospects for manipulating predator– culture systems. It is based on the premise
prey interactions via the first (plant) trophic that habitats that are structurally, biologi-
level have yet to be fully realized. Dicke et al. cally or temporally diverse provide greater
(1990) provide a useful synthesis on specific levels of habitat diversity, which in turn
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60 R.H.J. Verkerk

diversifies the available prey, so increasing tial and habitat differences, polycultures may
the abundance of natural enemies (Root, give rise to changes in movement rate which
1973). can only be detected through season-long
There are many ways in which diversifi- studies. For example, initial colonization by
cation of the crop environment can be under- a eulophid parasitoid of the Mexican bean
taken; most practical attempts rely on beetle, Epilachna varivestis Mulsant, was
polycultures (multiple cropping) or the use found to be greater in monoculture than in
of refugia. Despite the theoretical benefits of more diverse (intercropped) plots (Coll and
crop diversification, results from studies Bottrell, 1996). But, because emigration from
attempting to verify the benefits or otherwise the monocultural plots occurred sooner,
of such practices have been mixed (Sheehan, tenure time for the parasitoid in the inter-
1986) and demonstrate the importance of cropped plots was greater as the latter pro-
understanding the nature of multitrophic vided a more favourable habitat.
interactions. One of the best-known practical Intercropping may increase the effects of
examples of the benefits of mixed cropping natural enemies because one of the inter-
was the rediversification of the cotton agro- cropped plants provides allelochemical
ecosystem in the Cañete Valley in Peru, after attraction or a nectar source for natural ene-
massive bollworm outbreaks followed the mies or because the intercrop improves con-
abandonment of mixed cropping in the 1950s ditions (e.g. moisture, shelter) for
(Doutt and Smith, 1971). However, it should ground-dwelling predators (van Emden,
be borne in mind that some of these benefits 1989). Read et al. (1970) suggested that plant-
occurred as a result of the cessation of highly ing cole-worts near beet might enhance bio-
intensive insecticide application regimes. logical control of beet pests because
Chen and Welter (2002) tested the hypoth- cole-worts attract braconid parasitoids, e.g.
esis that herbivores are more abundant in Diaeretiella rapae M’Intosh, to the general
agroecosystems compared with more diverse area.
natural habitats, and studied the dynamics Field studies in Mexico showed that para-
of the sunflower moth, Homoeosoma electellum sitism of the pyralid Diaphania hyalinata was
(Hulst) and its natural enemies in agricul- greater in tricultures (squash, maize,
tural and native sunflower habitats. The legumes) than in monocultures of squash
authors showed clearly that sunflower (Letourneau, 1987), providing partial sup-
moths were consistently more abundant in port for the ‘enemies hypothesis’ (Root,
the agricultural habitats (with domesticated 1973), which dictates that natural enemies
sunflowers) compared with the native ones should be more abundant in diverse rather
(containing wild ancestors of the domesti- than in simple habitats. However, the author
cated varieties). Additionally, parasitism also found that parasitoid attack rates were
rates of the herbivore were between six and elevated in maize monocultures and that
ten times higher in the native compared with predator abundance was not enhanced in the
the agricultural habitats. tricultures, some predator species being
One of the likely reasons for mixed results actually more abundant in the monocultures.
from studies investigating the effects of crop The author concluded that particular vegeta-
diversification on natural enemies is the tional associations can enhance natural-
presence of confounding factors (Barbosa enemy activity, although the role of
and Wratten, 1998). Also, the results will single-species effects can be obscured by a
inevitably be limited by the specific parame- focus on diversity and these enhancement
ters measured. effects do not apply to all natural enemies
(Letourneau, 1987).
Polycultures
Refugia and non-crop plants
Gold et al. (1989) showed that the density of
plants in a polyculture may confound the Knowledge that uncultivated land can sup-
influence of plant diversity. Apart from spa- port a diverse range of natural enemies,
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Manipulation of Tritrophic Interactions 61

which can help to control pests on agricul- predators in turn migrated into the cotton
tural crops, has long been known. However, and were on average twice as abundant in
in many industrialized countries, the mecha- cotton with lucerne strips compared with
nization of agriculture, as well as the avail- cotton without the strips (Mensah, 1999).
ability of high-yielding crop varieties and Wild brassicas (e.g. Barbarea vulgaris and
synthetic pesticides, has meant that pest- Brassica kaber) planted in the vicinity of culti-
management programmes have often failed vated brassicas provide floral nectar reserves
to emphasize the importance of natural- for parasitoids of the diamondback moth, P.
enemy refugia. In Britain, for example, xylostella, so improving the potential for bio-
hedgerows and uncultivated field margins logical control (Idris and Grafius, 1996). Such
were destroyed as a result of these modern non-crop plants can sometimes provide a
technologies and only recently have there dual function in pest management, acting
been attempts to reverse this trend in the both as refuge sites for natural enemies and
wake of increasing awareness of the prob- as trap crops for the pest. However, there is
lems associated with large-scale monocul- also the possibility that some plants known
tures and over-reliance on pesticides (van to favour natural enemies will also attract
Emden, 1990). pests to the vicinity.
Within the crop, natural-enemy refugia Border-planting of Phacelia tanacetifolia
can take the form of unsprayed crop areas, (Hydrophyllaceae) as a floral (pollen)
protected plant parts of the crop itself, non- resource has also been shown to be effective
crop plants that favour natural enemies or in increasing the abundance of aphid-eating
alternative hosts, which in turn encourage hover flies, the larvae of which are often key
economically unimportant arthropods that natural enemies of aphids (White et al., 1995).
provide an alternative food source for nat- Adult female hover flies generally need to
ural enemies. Outside the crop, uncultivated consume pollen before they can lay fertile
field margins, hedgerows, ‘conservation eggs so it is important that such floral
headlands’ and ‘live fences’ have all been reserves are present close to the crop.
used, at least in part, to provide refugia for The common farming practice of using
natural enemies, which can subsequently plum trees as parasitoid refugia has been
move into the crop environment. shown to improve biological control of the
The effective use of refugia generally western grape leafhopper, Erythroneura ele-
requires a thorough knowledge of crop– gantula Osborn in vineyards in the western
pest–natural-enemy interactions. Spatial USA (Murphy et al., 1996). Almost twice the
scales are particularly important (Murdoch abundance of the egg parasite Anagrus epos
and Briggs, 1996). It is often not sufficient Girault was found in vineyards with plum
simply to leave uncultivated sections within tree refugia compared with those without,
or outside the crop. The floral composition of the trees acting both as overwintering sites
refuges, their location and their dimensions and as wind-breaks, which aid parasitoid
should be carefully considered in relation to flight and dispersal (Murphy et al., 1996).
the specific crop–pest–natural-enemy situa- Protected parts of certain crops that are
tion in question. relatively free from the disturbances associ-
There are many examples in the literature ated with agronomic practices can also pro-
indicating the effectiveness of natural-enemy vide important refugia for natural enemies.
refugia across a wide range of agroecosys- For example, the areas beneath the plucking
tems. Some examples are considered below. surface of tea plants are well known as a
The planting of lucerne (Medicago sativa) refuge for a range of natural enemies of
strips in cotton fields in Australia has been important tea pests. Research has shown that
shown to increase the abundance of impor- domatia, which are small, sometimes elabo-
tant predators (Mensah, 1999). Predatory rate pits or shelters at the junctures of veins
beetles, bugs and lacewings were five- to on the lower surface of leaves of some
sevenfold more abundant in the lucerne plants, are inhabited primarily by predatory
strips than in the cotton crop itself and these rather than herbivorous arthropods. A group
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62 R.H.J. Verkerk

of researchers has shown that, by adding shown that in some situations resource avail-
artificial domatia to cotton plants, fruit pro- ability can override the importance of nat-
duction could be increased by 30%, com- ural enemies, and this has potential
pared with control plants (Agrawal and applications for pest management in agricul-
Karban, 1997). This increase was caused by ture.
enhanced predation of herbivorous mites by The most common method of manipulat-
predatory ones that were able to harbour in ing bottom-up processes in the field is by
the artificial domatia (Agrawal and Karban, altering the fertilization regime. Differences
1997). in nutritional status of the host plant will
Some natural enemies overwinter within have different effects on herbivores com-
plant parts so the removal of stubble, fruits pared with natural enemies, and under some
or other crop litter may be counterproduc- conditions the growth rate of natural enemy
tive as these plant parts act as refugia for the populations may not be able to ‘keep up’
natural enemies. For example, in Australia, with pest populations. Walde (1995) tested
several species of predatory mite, this hypothesis in a mite system and found
Typhlodromus spp., have been shown to over- that the growth rate of a phytophagous mite,
winter in the calyx cavities of apple fruits, so Panonychus ulmi (Koch), in apple trees was
that early-season phytophagous mite control non-linear in relation to increased addition
can be improved if apples are left on the of NKP fertilizer; the density increased and
ground through winter (Gurr et al., 1997). then decreased with the increasing N content
of the leaves. Two key predatory mite
species in this system were unable to com-
Resource availability pensate for the increased growth rate of the
phytophagous mite, but the populations of
Population ecologists are actively debating the latter were none the less maintained
the relative importance of bottom-up beneath the economic threshold.
(resource-driven) and top-down (natural- Apart from affecting growth rates, fertil-
enemy-driven) processes in the regulation of ization may affect sex ratios of natural ene-
herbivores (Walker and Jones, 2001; Denno et mies. In studies of interactions between
al., 2002). cole-worts, diamondback moth and its ich-
Walker and Jones (2001) argue that the neumonid parasitoid, Diadegma insularis
absence of empirical data and the desire by (Cresson), sex ratios of parasitoids emerging
researchers to favour one of these processes from hosts on plants treated with high levels
to the exclusion of the other have greatly of nitrogen were found to be consistently
hampered the understanding of the interac- female-biased compared with those of para-
tions between these processes. Very little sitoids emerging from unfertilized plants,
work of this type has been conducted in rela- where sex ratios were male-biased with the
tion to agricultural systems, but models implication of lower potential parasitism
using limited empirical data are increasingly (Fox et al., 1990).
being used to elucidate the importance of A comprehensive study of the effects of
these processes (Gutierrez, 1996). nitrogen treatment of cole-worts greens on
Denno et al. (2002) investigated the rela- the vulnerability of the cabbage white butter-
tive effects of bottom-up and top-down fly, Pieris rapae (Linnaeus), to natural enemies
processes in both laboratory mesocosms and showed that its larvae grew more slowly
the field, using a non-agricultural Spartina under low-nitrogen conditions and were
grassland system. They found that changes more susceptible to ground-dwelling preda-
in plant nutrition and structure had complex tors (Loader and Damman, 1991). This sup-
effects on natural-enemy and herbivore ported the slow growth/high mortality
abundance and that these effects were not hypotheses of Feeny (1976) and Moran and
necessarily paralleled under laboratory and Hamilton (1980) (see above). Interestingly,
field conditions because of more complex however, Loader and Damman (1991) found
interactions in the field. However, it was that emergence of pupal parasites, e.g.
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Manipulation of Tritrophic Interactions 63

Pteromalus spp., was greater on high-nitro- enhance parasitism of the diamondback

gen plants, larvae on the low-nitrogen plants moth, P. xylostella (Verkerk, 1995), led to the
frequently dying as a result of stress-induced testing of low (sublethal) concentrations of
bacterial infection, so preventing complete neem seed kernel extract (from Azadirachta
development of the parasitoids. indica), on a host plant highly susceptible to P.
xylostella. This botanical treatment was
shown to enhance parasitism success by
Crop background Diadegma semiclausum Hellen in the labora-
tory, although a dose fivefold greater than
Visual cues can influence host selection by this parasitism-enhancing dose led to a dras-
both herbivores and natural enemies. tically reduced rate of pupal emergence so
Accordingly, crop background can have an effectively inhibiting parasitism (Verkerk and
influence on long-range searching. A number Wright, 1994). Verkerk and Wright (1994)
of insect pests and natural enemies have suggested that observed increases in the rates
been shown to be differentially attracted to of parasitoid pupation when hosts were
particular crop backgrounds. For example, maintained either on partially resistant host
cabbage aphid, B. brassicae, abundance was plants or susceptible plants treated with
greater on Brussels sprout plants where they neem could be caused by stress-induced
contrasted with a bare background com- impairment of the host’s immune system.
pared with when the background consisted This phenomenon has previously been
of a ‘carpet’ of weeds, cut regularly to avoid shown to occur in other host–parasitoid sys-
excessive competition with the crop (Smith, tems when the hosts were subjected to nutri-
1969). Smith (1969) and others (e.g. Kennedy tional stress (see Godfray, 1994).
et al., 1961; van Emden, 1965) showed that Low doses of a neem extract and
aphids were more strongly attracted to the azadirachtin (a primary active ingredient of
crop when it contrasted with the bare back- neem) on plants have been shown to reduce
ground, but that relative attraction between the fecundity of several aphid species
different groups of natural enemies (Lowery and Isman, 1994; Koul, 2003). It has
(Coccinelidae, Cecidomyiidae, Chrysopidae, also been suggested that sublethal doses of
Anthocoridae and Syrphidae) varied signifi- azadirachtin may make a significant contri-
cantly (Smith, 1969). Smith (1969) suggested bution to the control of the peach–potato
that aphid abundance could have been aphid, Myzus persicae (Sulzer), while having
affected by differential attraction of natural little or no adverse impact on parasitism by
enemies, with anthocorid predators being Aphidius matricariae Haliday (Sugden, 1994;
most strikingly enhanced in the weedy habi- Mordue et al., 1996). Laboratory studies
tats. Van Emden (1989) noted that certain showed that azadirachtin could enhance the
species of hover fly lay more eggs on aphid- toxicity of gypsy moth, L. dispar, NPV to its
infested crops when the ground is covered, host, the combined effects of the insecticide
but warned that other syrphid species prefer and NPV being greater than either product
crops surrounded by bare soil. applied on its own (Cook et al., 1996).
In an IPM programme targeting the
glasshouse whitefly, T. vaporariorum, conven-
Exogenous interactions tional insecticides were used at one-third
rates in conjunction with a mycoinsecticide
The application of exogenous substances, (B. bassiana: Boveral®) and the encyrtid para-
such as botanical extracts, may have differen- sitoid, Encarsia formosa (Dirlbek et al., 1992).
tial effects on pests and natural enemies that The selection of appropriate insecticides (at
can be exploited as a biorational method in reduced rates), careful timing and integra-
IPM. Although such substances do not neces- tion of all three control methods gave opti-
sarily affect interactions across three trophic mum whitefly control on certain lines (e.g.
levels, this possibility exists. The appreciation Transvaal daisy) where one method alone
that partial host-plant resistance could was found to be inadequate.
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64 R.H.J. Verkerk

Although not tritrophic in nature, icity when bound to the soil, there is a real
Chilcutt and Tabashnik (1997) investigated possibility of non-target impacts, although
the effects of ditrophic (within-host) interac- the effects may be indirect and difficult to
tions between different phenotypes of P. evaluate. Some fauna (e.g. earthworms and
xylostella, its endolarval braconid parasitoid some non-target herbivores) are not directly
Cotesia plutellae Kurdyumov and Bt. The out- affected by the toxins, but the toxins may be
come of the interaction was dependent on ingested subsequently by susceptible inver-
the host phenotype (Bt-resistant or Bt- tebrates (Groot and Dicke, 2002).
susceptible). In susceptible hosts the para- The potential risk of insects developing
sitoid did not affect performance of the resistance to toxins in such transgenic crops
pathogen, in moderately resistant hosts the has been recognized by many researchers
interaction was symmetrical and competi- (e.g. Strong et al., 1990; Menken et al., 1992;
tive, while highly resistant hosts were not Daly et al., 1994), while others have argued
susceptible to the pathogen, which created a that the risk may be smaller than that of the
refugium from competition for the parasitoid use of the same toxic principles in sprays
(Chilcutt and Tabashnik, 1997). These studies (e.g. Roush, 1994). Transgenic crops such as
demonstrate the considerable scope for inte- cotton have also been known to trigger sec-
gration of chemical and biological control ondary pest outbreaks (e.g. Heteroptera:
within a multitrophic context (see also Miridae: see Fitt et al., 1994; Hardee and
Wright and Verkerk, 1995). Bryan, 1997), which may need to be con-
trolled with conventional insecticide sprays.
These insecticides have the potential to harm
Genetic manipulation natural enemies. Strong et al. (1990) argued
that transgenic techniques need to be refined
To date, most of the work on genetic manip- so that toxins are only expressed in a subset
ulation for pest-management purposes, of crucial tissues and at specific developmen-
through either plant breeding or genetic tal stages and they should also be integrated
engineering, has involved host plants. This into an ecological framework if they are to be
has been mainly through the development of effective and contribute to biocontrol. Van
transgenic crops containing endotoxins from Emden and Wratten (1991) warned that
Bt (Brar and Khush, 1993; Daly et al., 1994; modern gene-transfer techniques aimed at
Tabashnik, 1994; Metz et al., 1995). Virtually creating resistant crop varieties are more
no work has been carried out on breeding likely than traditional plant-breeding meth-
programmes or genetic engineering that ods to use an allelochemical mechanism of
affects natural enemies, despite the recog- resistance (antibiosis), which might be dam-
nized key importance of natural enemies in aging to natural enemies and other non-
pest management (Groot and Dicke, 2002). target organisms.
Genetic manipulation of insects (pests and Genetic manipulation of crop plants to
natural enemies) for pest management is in enhance nutrient uptake has been considered
its infancy but it is thought that it will and could be compatible with IPM/ICM sys-
become increasingly important as non- tems (Johansen et al., 1995). The potential
pesticidal approaches gain increasing favour also exists for creating genetically engi-
in IPM (DeVault et al., 1996). neered plants that emit increased amounts of
As transgenic crops become more widely natural-enemy-attracting volatiles (syn-
adopted, concerns about their potential omones), although such plants are yet to be
natural-enemy and non-target impacts, as available commercially.
well as the likelihood of their inducing resis-
tance to toxic principles, are increasing. In a
review by Groot and Dicke (2002), the possi- Tritrophic Models
ble effects of insect-resistant transgenic and
non-transgenic crops on food webs are con- The intrinsic complexity of multitrophic
sidered. Because Bt toxins maintain their tox- interactions in agroecosystems and the diffi-
04IntpestManCh4.QXD 14/4/04 2:24 pm Page 65

Manipulation of Tritrophic Interactions 65

culty of generating meaningful empirical supply–demand relations. The model

data from the field have meant that model- demonstrates the importance of plant-level
ling approaches have been used to facilitate effects on higher trophic levels. Such models
the understanding of mechanisms and can be very valuable tools in understanding
processes. Simulation models of crop–pest– agroecosystems, which can in turn facilitate
natural-enemy systems used to date (e.g. better management of biological- or cultural-
Gutierrez, 1996) are based on detailed field control programmes in IPM.
and laboratory data. The models integrate
the biology and physiology of consumers,
which in turn affect resource acquisition and
allocation and hence population birth and Conclusions
death rates. Resource availability (i.e. bot-
tom-up effects) define the underlying base Improving the understanding of multitrophic
dynamics of each species, while natural ene- systems is critical to the development of sus-
mies provide the top-down or regulatory tainable, less pesticide-dependent or pesti-
effects (Gutierrez, 1996). cide-free pest-management systems (Bottrell
Simulation models have been used to et al., 1998). This is because control tech-
assist in the tactical evaluation of various niques, or target pests, cannot be regarded in
biological control and plant-resistance inter- isolation – manipulation of any single factor
actions (e.g. Gutierrez et al., 1984, 1988, 1994) will tend to have knock-on effects on differ-
and simple analytical models (e.g. Hassell, ent trophic levels. From a commercial point
1978) have been used to make very general of view, the areas with greatest potential are
population-dynamics predictions. However, likely to be allelochemical and genetic manip-
there have been very few studies that have ulations. However, it should be recognized
examined tritrophic interactions using bio- that at present the biological control market is
logically realistic but quantitative popula- estimated to be in the region of only US$75
tion-dynamics models (see Gutierrez et al., million (Waage, 1997), compared with the
1993). The relatively recent application of US$32 billion global agricultural-chemical
age-structured models written as a series of market (Warrior, 2000).
delay-differential equations (Nisbet and Thomas (1999) reasons that increasing our
Gurney, 1983) has promoted a middle basic understanding of how individual pest-
approach between tactical and strategic pre- control technologies act and interact will
dictive modelling, which may lead to a bet- reveal new opportunities for improving pest
ter understanding of pest–natural-enemy control. There is a great
interactions under field conditions. Such need to break away from the existing single-
models have been termed ‘models of inter- technology, pesticide-dominated paradigm
mediate complexity’ (e.g. Godfray and and to adopt a more ecological approach
Waage, 1991; Briggs and Godfray, 1995) and built around a fundamental understanding of
can be applied to tritrophic systems (Thomas population biology at the local farm level and
and Waage, 1994), although to date these the true integration of renewable technolo-
models have been largely concerned with gies such as host plant resistance and natural
biological control, which are available to even
second and third trophic-level interactions
the most resource-poor farmers.
(Gutierrez et al., 1994).
(Thomas, 1999)
A complex, metapopulation tritrophic
model of the African cassava system was As the popularity of organic agriculture
developed recently by Gutierrez et al. (1999). increases and pesticide-related problems
The model is based on a single-patch age- (e.g. residues, resistance, side effects) con-
structured population-dynamics model, tak- tinue to mount, there will be an ever
ing into account key plants and animals in greater requirement for effective and rea-
the system. It also accounts for movement sonably predictable natural control systems
rates of animals between patches, these (see Verkerk and Wright, 1996b). A study of
being dependent on species-specific 18 commercial tomato farms in California,
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66 R.H.J. Verkerk

half certified organic production systems, tinct approach to biological and/or cultural
half conventionally managed and using control, is likely to be prioritized increas-
synthetic pesticides, showed clearly the ingly by both researchers and those respon-
viability of organic systems (Letourneau sible for the development and practical
and Goldstein, 2001). Benefits of the implementation of pest-management pro-
organic systems included greater natural- grammes. This process will be facilitated as
enemy diversity and abundance of func- improvements in the understanding of
tional guilds. crop–pest–natural-enemy evolution and
In the interest of agricultural sustain- interactions are achieved (Bottrell et al.,
ability, tritrophic manipulation, as a dis- 1998).

References

Agrawal, A.A. and Karban, R. (1997) Domatia mediate plant–arthropod mutualism. Nature 387, 562–563.
Agrawal, A.A. and Klein, C.N. (2000) What omnivores eat: direct effects of induced plant resistance on
herbivores and indirect consequences for diet selection by omnivores. Journal of Animal Ecology 69,
525–535.
Agrawal, A.A., Kobayashi, C. and Thaler, J.S. (1999) Influence of prey availability and induced host-plant
resistance on omnivory by western flower thrips. Ecology 80, 518–523.
Altieri, M.A., Lewis, W.J., Nordlund, D.A., Gueldner, R.C. and Todd, J.W. (1981) Chemical interactions
between plants and Trichogramma wasps in Georgia soybean fields. Protection Ecology 3, 259–263.
Barbosa, P. (1988) Natural enemies and herbivore plant interactions: Influence of plant allelochemicals
and host specificity. In: Barbosa, P. and Letourneau, D.K. (eds) Novel Aspects of Insect–Plant
Allelochemicals and Host Specificity. John Wiley & Sons, New York, pp. 201–229.
Barbosa, P. and Wratten, S.D. (1998) Influence of plants on invertebrate predators: implications to conser-
vation biological control. In: Barbosa, P. (ed.) Conservation Biological Control. Academic Press, San
Diego, California, pp. 83–100.
Bergman, J.M. and Tingey, W.M. (1979) Aspects of interactions between plant genotypes and biological
control. Bulletin of the Entomological Society of America 25, 275–279.
Berryman, A.A., Michalski, J., Gutierrez, A.P. and Arditi, R. (1995) Logistic theory of food web dynamics.
Ecology 76, 336–343.
Boethel, D.J. and Eikenbary, R.D. (1986) Interactions of Plant Resistance and Parasitoids and Predators of
Insects. Wiley & Sons, Chichester, UK, 224 pp.
Bottrell, D.G., Barbosa, P. and Gould, F. (1998) Manipulating natural enemies by plant variety selection and
modification: a realistic strategy? Annual Review of Entomology 43, 347–367.
Braimah, H. and van Emden, H.F. (1994) The role of the plant in host acceptance by the parasitoid
Aphidius rhopalosiphi (Hymenoptera: Braconidae). Bulletin of Entomological Research 84, 303–306.
Brar, D.S. and Khush, G.S. (1993) Application of biotechnology in integrated pest management. Journal of
Insect Science 6, 7–14.
Briggs, C.J. and Godfray, H.C.J. (1995) The dynamics of insect–pathogen interactions in stage-structured
populations. American Naturalist 145, 855–887.
Camara, M.D. (1997) Predator responses to sequestered plant toxins in buckeye caterpillars: are tritrophic
interactions locally variable? Journal of Chemical Ecology 23, 2093–2106.
Chen, Y.H. and Welter, S.C. (2002) Abundance of a native moth Homoeosoma electellum (Lepidoptera:
Pyralidae) and activity of indigenous parasitoids in native and agricultural sunflower habitats.
Environmental Entomology 31, 626–636.
Chilcutt, C.F. and Tabashnik, B.E. (1997) Host-mediated competition between the pathogen Bacillus
thuringiensis and the parasitoid Cotesia plutellae of the diamondback moth (Lepidoptera: Plutellidae).
Environmental Entomology 26, 38–45.
Clancy, K.M. and Price, P.W. (1987) Rapid herbivore growth enhances enemy attack: sublethal plant
defences remain a paradox. Ecology 68, 733–737.
Coll, M. and Bottrell, D.G. (1996) Movement of an insect parasitoid in simple and diverse plant assem-
blages. Ecological Entomology 21, 141–149.
04IntpestManCh4.QXD 14/4/04 2:24 pm Page 67

Manipulation of Tritrophic Interactions 67

Cook, S.P., Webb, R.E. and Thorpe, K.W. (1996) Potential enhancement of the gypsy moth (Lepidoptera:
Lymantriidae) nuclear polyhedrosis virus with the triterpene azadirachtin. Environmental
Entomology 25, 1209–1214.
Daly, J.C., Hokkanen, H.M.T. and Deacon, J. (1994) Ecology and resistance management for Bacillus
thuringiensis transgenic plants. Biocontrol Science and Technology 4, 563–571.
Damman, H. (1987) Leaf quality and enemy avoidance by the larvae of a pyralid moth. Ecology 68, 88–97.
De Moraes, C.M., Lewis, W.J., Pare, P.W., Alborn, H.T. and Tumlinson, J.H. (1998) Herbivore-infested
plants selectively attract parasitoids. Nature 393, 570–573.
Denno, R.F., Gratton, C., Peterson, M.A., Langellotto, G.A., Finke, D.L. and Huberty, A.F. (2002) Bottom-up
forces mediate natural-enemy impact in a phytophagous insect community. Ecology 83, 1443–1458.
Denyer, R. (2000) Integrated crop management: introduction. Pest Management Science 56, 945–946.
DeVault, J.D., Hughes, K.J., Johnson, O.A. and Narang, S.K. (1996) Biotechnology and new integrated
pest management approaches. Bio-technology 14, 46–49.
Dicke, M., Sabelis, M.W., Takabayashi, J., Bruin, J. and Posthumus, M.A. (1990) Plant strategies of manip-
ulating predator-prey interactions through allelochemicals: prospects for application in pest control.
Journal of Chemical Ecology 16, 3091–3118.
Dicke, M., Takabayashi, J., Posthumus, M.A., Schutte, C. and Krips, O.E. (1998) Plant-phytoseiid interac-
tions mediated by herbivore-induced plant volatiles: variation in production of cues and in
responses of predatory mites. Experimental and Applied Acarology 22, 311–333.
Dirlbek, J., Dirlbekova, O. and Jedlicka, M. (1992) The combined use of mycoinsecticide, parasitoid and
chemical stressor in the control of greenhouse whitefly (Trialeurodes vaporariorum Westwood).
Ochrana Rostlin 28, 71–77.
Doutt, R.L. and Smith, R.F. (1971) The pesticide syndrome – diagnosis and suggested prophylaxis. In:
Huffaker, C.B. (ed.) Biological Control. Plenum Press, New York, pp. 3–15.
Du, Y.J., Poppy, G.M. and Powell, W. (1996) Relative importance of semiochemicals from first and second
trophic levels in host foraging behaviour of Aphidius ervi. Journal of Chemical Ecology 22, 1591–1605.
Du, Y.J., Poppy, G.M., Powell, W., Pickett, J.A., Wadhams, L.J. and Woodcock, C.M. (1998) Identification
of semiochemicals released during aphid feeding that attract parasitoid Aphidius ervi. Journal of
Chemical Ecology 24, 1355–1368.
Duffey, S.S. and Bloem, K.A. (1987) Plant defence-herbivore-parasite interactions and biological control.
In: Kogan, M. (ed.) Ecological Theory and Integrated Pest Management Practice. Wiley & Sons, New
York, pp. 135–184.
Eigenbrode, S.D., Moodie, S. and Castagnola, T. (1995) Predators mediate host plant resistance to a phy-
tophagous pest in cabbage with glossy leaf wax. Entomologia Experimentalis et Applicata 77, 335–342.
Farrar, R.R. and Ridgway, R.L. (2000) Host plant effects on the activity of selected nuclear polyhedrosis
viruses against the corn earworm and beet armyworm (Lepidoptera : Noctuidae). Environmental
Entomology 29, 108–119.
Farrar, R.R., Martin, P.A.W. and Ridgway, R.L. (1996) Host plant effects on activity of Bacillus thuringiensis
against gypsy moth (Lepidoptera: Lymantriidae) larvae. Environmental Entomology 25, 1215–1223.
Feeny, P. (1976) Plant apparency and chemical defence. In: Wallace, J.W. and Mansell, R.L. (eds)
Biochemical Interaction between Plants and Insects. Plenum Press, New York, pp. 1–40.
Fitt, G.P., Mares, C.L. and Llewellyn, D.J. (1994) Field-evaluation and potential ecological impact of trans-
genic cottons (Gossypium hirsutum) in Australia. Biocontrol Science and Technology 4, 535–548.
Fox, L.R., Letourneau, D.K., Eisenbach, J. and van Nouhuys, S. (1990) Parasitism rates and sex ratios of a
parasitoid wasp: effects of herbivore and plant quality. Oecologia 83, 414–419.
Fritz, R.S. (1992) Community structure and species interactions of phytophagous insects on resistant and
susceptible host plants. In: Fritz, R.S. and Simms, E.L. (eds) Plant Resistance to Herbivores and
Pathogens: Ecology, Evolution and Genetics. University of Chicago Press, Chicago, Illinois, pp. 240–277.
Fritz, R.S., McDonough, S.E. and Rhoads, A.G. (1997) Effects of plant hybridization on herbivore-
parasitoid interactions. Oecologia 110, 360–367.
Godfray, H.C.J. and Waage, J.K. (1991) Predictive modelling in biological control: the mango mealy bug
(Rastrococcus invadens) and its parasitoids. Journal of Applied Ecology 28, 434–453.
Godfray, H.J.H. (1994) Parasitoids – Behavioural and Evolutionary Ecology. Princeton University Press,
Princeton, New Jersey, 473 pp.
Gold, C.S., Altieri, M.A. and Bellotti, A.C. (1989) The effects of intercropping and mixed varieties of
predators and parasitoids of cassava whiteflies (Hemiptera: Aleyrodidae). Bulletin of Entomological
Research 79, 115–121.
04IntpestManCh4.QXD 14/4/04 2:24 pm Page 68

68 R.H.J. Verkerk

Gowling, G.R. and van Emden, H.F. (1994) Falling aphids enhance impact of biological control by para-
sitoids on partially aphid-resistant plant varieties. Annals of Applied Biology 125, 233–242.
Groot, A.T. and Dicke, M. (2002) Insect-resistant transgenic plants in a multi-trophic context. Plant Journal
31, 387–406.
Gurr, G.M., Thwaite, W.G., Valentine, B.J. and Nicol, H.I. (1997) Factors affecting the presence of
Typhlodromus spp. (Acarina: Phytoseiidae) in the calyx cavities of apple fruits and implications for
integrated pest management. Experimental and Applied Acarology 21, 357–364.
Gutierrez, A.P. (1996) Applied Population Ecology: a Supply–Demand Approach. John Wiley & Sons, New
York, 300 pp.
Gutierrez, A.P., Baumgaertner, J.V. and Summers, C.G. (1984) Multitrophic models of predator prey ener-
getics. I. Age-specific energetics models – pea aphid Acrythosiphon pisum (Harris) (Homoptera:
Aphidae) as an example. Canadian Entomologist 116, 924–932.
Gutierrez, A.P., Wermelinger, B., Schulthess, F., Baumaertner, J.V., Herren, H.R., Elliss, C.K. and Yaninek,
J.S. (1988) Analysis of biological control of cassava pests in Africa. I. Simulation of carbon, nitrogen
and water dynamics in cassava. Journal of Applied Ecology 25, 901–920.
Gutierrez, A.P., Neuenschwander, P. and van Alphen, J.J.M. (1993) Factors affecting biological control of
cassava mealybug by exotic parasitoids: a ratio-dependent supply–demand driven model. Journal of
Applied Ecology 30, 706–721.
Gutierrez, A.P., Mills, N.J., Schreiber, S.J. and Ellis, C.K. (1994) A physiologically based tritrophic perspec-
tive on bottom-up–top-down regulation of populations. Ecology 75, 2227–2242.
Gutierrez, A.P., Yaninek, J.S., Neuenschwander, P. and Ellis, C.K. (1999) A physiologically-based
tritrophic metapopulation model of the African cassava food web. Ecological Modelling 123, 225–242.
Hardee, D.D. and Bryan, W.W. (1997) Influence of Bacillus thuringiensis-transgenic and nectarless cotton
on insect populations with special emphasis on the tarnished plant bug (Heteroptera: Miridae).
Journal of Economic Entomology 90, 663–668.
Hare, D.J. (1992) Effects of plant variation on herbivore–enemy interactions. In: Fritz, R.S. and Simms,
E.L. (eds) Plant Resistance to Herbivores and Pathogens. University of Chicago Press, Chicago, Illinois,
pp. 278–298.
Hassell, M.P. (1978) The Dynamics of Arthropod Predator–Prey Systems. Princeton University Press,
Princeton, New Jersey, 237 pp.
Hufbauer, R.A. and Via, S. (1999) Evolution of an aphid–parasitoid interaction: variation in resistance to
parasitism among aphid populations specialized on different plants. Evolution 53, 1435–1445.
Hunter, A.F. and Elkinton, J.S. (2000) Effects of synchrony with host plant on populations of a spring-
feeding lepidopteran. Ecology 81, 1248–1261.
Idris, A.B. and Grafius, E. (1996) Effects of wild and cultivated host plants on oviposition, survival, and
development of diamondback moth (Lepidoptera: Plutellidae) and its parasitoid Diadegma insulare
(Hymenoptera: Ichneumonidae). Environmental Entomology 25, 825–833.
Janssen, A., Pallini, A., Venzon, M. and Sabelis, M.W. (1998) Behaviour and indirect interactions in food
webs of plant-inhabiting arthropods. Experimental and Applied Acarology 22, 497–521.
Johansen, C., Lee, K.K., Sharma, K.K., Subbarao, G.V. and Kueneman, E.A. (1995) Genetic manipulation
of crop plants to enhance integrated nutrient management in cropping systems. 1. Phosphorus. In:
Proceedings of an FAO–ICRISAT Expert Consultancy Workshop, Patancheru, India, 15–18 March 1994.
International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Patancheru, India, 177
pp.
Karban, R. and EnglishLoeb, G. (1997) Tachinid parasitoids affect host plant choice by caterpillars to
increase caterpillar survival. Ecology 78, 603–611.
Kennedy, J.S., Booth, C.O. and Kershaw, W.J.S. (1961) Host finding by aphids in the field. III. Visual
attraction. Annals of Applied Biology 49, 1.
Koul, O. (2003) Variable efficacy of neem-based formulations and azadirachtin to aphids and their nat-
ural enemies. In: Koul, O., Dhaliwal, G.S., Marwaha, S.S. and Arora, J.K. (eds) Biopesticides and Pest
Management, Vol. 1. Campus Books International, New Delhi, pp. 64–74.
Leather, S.R. (1985) Oviposition preferences in relation to larval growth rates and survival in the pine
beauty moth, Panolis flammea. Ecological Entomology 10, 213–217.
Leather, S.R. and Walsh, P.J. (1993) Sub-lethal plant defences: the paradox remains. Oecologia 93, 153–155.
Letourneau, D.K. (1987) The enemies hypothesis: tritrophic interactions and vegetational diversity in
tropical agroecosystems. Ecology 68, 1616–1622.
Letourneau, D.K. and Andow, D.A. (1999) Natural-enemy food webs. Ecological Applications 9, 363–364.
04IntpestManCh4.QXD 14/4/04 2:24 pm Page 69

Manipulation of Tritrophic Interactions 69

Letourneau, D.K. and Goldstein, B. (2001) Pest damage and arthropod community structure in organic
vs. conventional tomato production in California. Journal of Applied Ecology 38, 557–570.
Lewis, W.J. and Martin, W.R. (1990) Semiochemicals for use with parasitoids: status and future. Journal of
Chemical Ecology 16, 3067–3089.
Lewis, W.J. and Nordlund, D.A. (1984) Semiochemicals influencing fall armyworm parasitoid behavior:
implications for behavioral manipulation. Florida Entomologist 67, 343–349.
Lill, J.T. and Marquis, R.J. (2001) The effects of leaf quality on herbivore performance and attack from nat-
ural enemies. Oecologia 126, 418–428.
Loader, C. and Damman, H. (1991) Nitrogen content of food plants and vulnerability of Pieris rapae to natural
enemies. Ecology 72, 1586–1590.
Lowery, D.T. and Isman, M.B. (1994) Insect growth-regulating effects of a neem extract and azadirachtin
on aphids. Entomologia Experimentalis et Applicata 72, 77–84.
Mattiacci, L., Dicke, M. and Posthumus, M.A. (1994) Induction of parasitoid attracting synomone in
Brussels sprouts plants by feeding of Pieris brassicae larvae – role of mechanical damage and herbi-
vore elicitor. Journal of Chemical Ecology 20, 2229–2247.
Mattiacci, L., Dicke, M. and Posthumus, M.A. (1995) Beta-glucosidase – an elicitor of herbivore-induced
plant odor that attracts host-searching parasitic wasps. Proceedings of the National Academy of Sciences
of the USA 92, 2036–2040.
Meerman, F., van den Ven, G.W.J., van Keulen, H. and Breman, H. (1996) Integrated crop management: an
approach to sustainable agricultural development. International Journal of Pest Management 42, 13–24.
Menken, S.B.J., Visser, J.H. and Harrewijn, P. (1992) Proceedings of the 8th International Symposium on
Insect–Plant Relationships. Series Entomologica Vol. 49, Kluwer Academic Publishers, Dordrecht, The
Netherlands, 424 pp.
Mensah, R.K. (1999) Habitat diversity: implications for the conservation and use of predatory insects of
Helicoverpa spp. in cotton systems in Australia. International Journal of Pest Management 45, 91–100.
Metz, T.D., Roush, R.T., Tang, J.D., Shelton, A.M. and Earle, E.D. (1995) Transgenic broccoli expressing a
Bacillus thuringiensis insecticidal crystal protein – implications for pest resistance management
strategies. Molecular Breeding 1, 309–317.
Moran, N. and Hamilton, W.D. (1980) Low nutritive quality as defence against herbivores. Journal of
Theoretical Biology 86, 247–254.
Mordue, A.J., Nisbet, A.J., Nasiruddin, M. and Walker, E. (1996) Differential thresholds of azadirachtin
for feeding deterrence and toxicity in locusts and an aphid. Entomologia Experimentalis et Applicata
80, 69–72.
Murdoch, W.W. and Briggs, C.J. (1996) Theory for biological control: recent developments. Ecology 77,
2001–2013.
Murphy, B.C., Rosenheim, J.A. and Granett, J. (1996) Habitat diversification for improving biological con-
trol: abundance of Anagrus epos (Hymenoptera: Mymaridae) in grape vineyards. Environmental
Entomology 25, 495–504.
Nisbet, R.M. and Gurney, W.S.C. (1983) The systematic formulation of population models for insects with
dynamically varying instar duration. Theoretical Population Biology 23, 114–135.
Nordlund, D.A., Lewis, W.J. and Altieri, M.A. (1988) Influences of plant produced allelochemicals on the
host–prey selection behaviour of entomophagous insects. In: Barbosa, P. and Letourneau, D.K. (eds)
Novel Aspects of Insect–Plant Interactions. John Wiley & Sons, New York, pp. 65–95.
Nwanze, K.F., Reddy, Y.V.R., Nwilene, F.E., Kausalya, K.G. and Reddy, D.D.R. (1998) Tritrophic interac-
tions in sorghum, midge (Stenodiplosis sorghicola) and its parasitoid (Aprostocetus spp.). Crop
Protection 17, 165–169.
Orr, D.B. and Boethel, D.J. (1985) Comparative development of Copidosoma truncatellum (Hymenoptera:
Encyrtidae) and its host, Pseudoplusia includens (Lepidoptera: Noctuidae), on resistant and suscepti-
ble soybean genotypes. Environmental Entomology 14, 612–616.
Poppy, G.M. (1997) Tritrophic interactions: improving ecological understanding and biological control?
Endeavour 21, 61–65.
Poprawski, T.J., Greenberg, S.M. and Ciomperlik, M.A. (2000) Effect of host plant on Beauveria bassiana
and Paecilomyces fumosoroseus-induced mortality of Trialeurodes vaporariorum (Homoptera :
Aleyrodidae). Environmental Entomology 29, 1048–1053.
Price, P.W. (1986) Ecological aspects of host plant resistance and biological control: interactions among
three trophic levels. In: Boethel, D.J. and Eikenbary, R.D. (eds) Interactions of Plant Resistance and
Parasitoids and Predators of Insects. Ellis Horwood, Chichester, UK, pp. 11–30.
04IntpestManCh4.QXD 14/4/04 2:24 pm Page 70

70 R.H.J. Verkerk

Price, P.W., Bouton, C.E., Gross, P., McPheron, B.A., Thompson, J.N. and Weis, A.E. (1980) Interactions
among three trophic levels: influence of plants on interactions between insect herbivores and nat-
ural enemies. Annual Review of Ecology and Systematics 11, 41–65.
Price, P.W., Cobb, N., Craig, T.P, Fernandes, G.W., Tami, J.K., Mopper, S. and Preszler, R.W. (1990) Insect
herbivore population dynamics on trees and shrubs: new approaches relevant to latent and eruptive
species and life table development. In: Bernays, E.A. (ed.) Insect–Plant Interactions, Vol. 2. CRC Press,
Boca Raton, Florida, pp. 2–38.
Read, D.P., Feeny, P.P. and Root, R.B. (1970) Habitat selection by the aphid parasite Diaeretiella rapae
(Hymenoptera: Braconidae) and hyperparasite Charips brassicae (Hymenoptera: Cynipidae).
Canadian Entomologist 102, 1567–1578.
Redman, A.M. and Scriber, J.M. (2000) Competition between the gypsy moth, Lymantria dispar, and the
northern tiger swallowtail, Papilio canadensis: interactions mediated by host plant chemistry,
pathogens, and parasitoids. Oecologia 125, 218–228.
Reitz, S.R. and Trumble, J.T. (1996) Tritrophic interactions among linear furanocoumarins, the herbivore
Trichoplusia ni (Lepidoptera: Noctuidae), and the polyembryonic parasitoid Copidosoma floridanum
(Hymenoptera: Enccyrtidae). Environmental Entomology 25, 1391–1397.
Root, R.B. (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna
of collards (Brassica oleracea). Ecological Monographs 43, 95–124.
Roush, R.T. (1994) Managing pests and their resistance to Bacillus thuringiensis – can transgenic crops be
better than sprays? Biocontrol Science and Technology 4, 501–516.
Ryan, J.D., Morgham, P.E., Richardson, R.C., Johnson, R.C., Mort, A.J. and Eikenbary, R.D. (1990)
Greenbug and wheat: a model system for the study of phytotoxic Homoptera. In: Campbell, R.K.
and Eikenbary, R.D. (eds) Aphid–Plant Genotype Interactions. Elsevier, Amsterdam, pp. 171–186
Schultz, J.C. (1983) Impact of variable plant defensive chemistry on susceptibility of insects to natural
enemies. American Chemical Society Symposium Series 208, 37–54.
Sheehan, W. (1986) Response by specialist and generalist natural enemies to agroecosystem diversifica-
tion: a selective review. Environmental Entomology 15, 456–461.
Shimoda, T., Takabayashi, J., Ashihara, W. and Takafuji, A. (1997) Response of predatory insect Scolothrips
takahashii toward herbivore-induced plant volatiles under laboratory and field conditions. Journal of
Chemical Ecology 23, 2033–2048.
Smith, C.M. (1989) Plant Resistance to Insects: a Fundamental Approach. John Wiley & Sons, New York, 286 pp.
Smith, J.G. (1969) Some effects of crop background on populations of aphids and their natural enemies
on brussels sprouts. Annals of Applied Biology 63, 326–330.
Steinberg, S., Dicke, M. and Vet, L.E.M. (1993) Relative importance of infochemicals from 1st and 2nd
trophic level in long-range host location by the larval parasitoid Cotesia glomerata. Journal of Chemical
Ecology 19, 47–59.
Strong, D.R., Lawton, J.H. and Southwood, T.R.E. (1984) Insects on Plants. Blackwell Scientific
Publications, Oxford, 313 pp.
Strong, D.R., Baker, R.R. and Dunn, P.E. (1990) Interface of natural enemy and environment. UCLA
Symposia on Molecular and Cellular Biology 112, 57–64.
Sugden, M.R. (1994) The effects of azadirachtin on Myzus persicae and its hymenopterous parasitoid
Aphidius matricariae. MSc thesis, University of Aberdeen, UK.
Tabashnik, B.E. (1994) Evolution of resistance to Bacillus thuringiensis. Annual Review of Entomology 39,
47–79.
Takabayashi, J., Dicke, M. and Posthumus, M.A. (1994) Volatile herbivore-induced terpenoids in plant
mite interactions – variation caused by biotic and abiotic factors. Journal of Chemical Ecology 20,
1329–1354.
Thaler, J.S. (2002) Effect of jasmonate-induced plant responses on the natural enemies of herbivores.
Journal of Animal Ecology 71, 141–150.
Theodoratus, D.H. and Bowers, M.D. (1999) Effects of sequestered iridoid glycosides on prey choice of
the prairie wolf spider, Lycosa carolinensis. Journal of Chemical Ecology, 25, 283–295.
Thomas, M.B. (1999) Ecological approaches and the development of ‘truly integrated’ pest manage-
ment. Proceedings of the National Academy of Sciences of the USA 96, 5944–5951.
Thomas, M.B. and Waage, J.K. (1994) Integration of Biological Control and Host Plant Resistance Breeding.
CAB International, Wallingford, UK, 139 pp.
Tumlinson, J.H., Turlings, T.C.J. and Lewis, W.J. (1993) Semiochemically mediated foraging behavior in
beneficial parasitic insects. Archives of Insect Biochemistry and Physiology 22, 385–391.
04IntpestManCh4.QXD 14/4/04 2:24 pm Page 71

Manipulation of Tritrophic Interactions 71

Turlings, T.C.J. and Tumlinson, J.H. (1991) Do parasitoids use herbivore-induced plant chemical defenses
to locate hosts? Florida Entomologist 74, 42–50.
van Emden, H.F. (1965) The effect of uncultivated land on the distribution of cabbage aphid (Brevicoryne
brassicae) on an adjacent crop. Journal of Applied Ecology 2, 171.
van Emden, H.F. (1987) Cultural methods: the plant. In: Burn, A.J., Coaker, T.H. and Jepson, P.C. (eds)
Integrated Pest Management. Academic Press, London, pp. 27–68.
van Emden, H.F. (1989) Pest Control, 2nd edn. Edward Arnold, London, 117 pp.
van Emden, H.F. (1990) Plant diversity and natural enemy efficiency in agroecosystems. In: Mackauer,
M., Ehler, L.E. and Roland J. (eds) Critical Issues in Biological Control. Intercept, Andover, UK,
pp. 63–80.
van Emden, H.F. (1991) The role of host plant resistance in insect pest mis-management. Bulletin of
Entomological Research 81, 123–126.
van Emden, H.F. (1995) Host plant–Aphidophaga interactions. Agriculture, Ecosystems and Environment
52, 3–11.
van Emden, H.F. and Wearing, C.H. (1965) The role of the host plant in delaying economic damage levels
in crops. Annals of Applied Biology 56, 323–324.
van Emden, H.F. and Wratten, S.D. (1991) Tri-trophic interactions involving plants in the biological con-
trol of aphids. In: Peters, D.C., Webster, J.A. and Chouber, C.S. (eds) Aphid–Plant Interactions:
Populations to Molecules. Agricultural Research Service, USDA Oklahoma State University, Stillwater,
Oklahoma, pp. 29–43.
van Poecke, R.M.P., Posthumus, M.A. and Dicke, M. (2001) Herbivore-induced volatile production by
Arabidopsis thaliana leads to attraction of the parasitoid Cotesia rubecula: chemical, behavioral, and
gene-expression analysis. Journal of Chemical Ecology 27, 1911–1928.
Verkerk, R.H.J. (1995) Studies on interactions between diamondback moth, host plants, endolarval para-
sitoids and selective toxicants. PhD thesis, University of London, UK, 244 pp.
Verkerk, R.H.J. and Wright, D.J. (1994) The potential for induced extrinsic host plant resistance in IRM
strategies targeting the diamondback moth. In: Proceedings – Brighton Crop Protection Conference:
Pests and Diseases – 1994. British Crop Protection Council, Farnham, UK, pp. 457–462.
Verkerk, R.H.J. and Wright, D.J. (1996a) The effects of host plant-selective insecticide interactions on larvae
of Plutella xylostella (Lepidoptera: Yponomeutidae) in the laboratory. Pesticide Science 44, 171–181.
Verkerk, R.H.J. and Wright, D.J. (1996b) Multitrophic interactions and management of the diamondback
moth. Bulletin of Entomological Research 86, 205–216.
Verkerk, R.H.J., Leather, S.R. and Wright, D.J. (1998) The potential for manipulating crop pest-natural
enemy interactions for improved insect pest management. Bulletin of Entomological Research 88,
493–501.
Vet, L.E.M. and Dicke, M. (1992) Ecology of infochemical use by natural enemies in a tritrophic context.
Annual Review of Entomology 37, 141–172.
Vinson, S.B. (1984) How parasitoid locate their hosts: a case of insect espionage. In: Lewis, T. (ed.) Insect
Communications. Academic Press, London, pp. 325–348.
Waage, J. (1997) What does biotechnology bring to integrated pest management? Biotechnology and
Development Monitor 32, 19–21.
Walde, S.J. (1995) How quality of host-plant affects a predator-prey interaction in biological control.
Ecology 76, 1206–1219.
Walker, M. and Jones, T.H. (2001) Relative roles of top-down and bottom-up forces in terrestrial tritrophic
plant-insect herbivore-natural enemy systems. Oikos 93, 177–187.
Warrior, P. (2000) Living systems as natural crop-protection agents. Journal of Pest Management Science 56,
681–687.
White, A.J., Wratten, S.D., Berry, N.A. and Weigmann, U. (1995) Habitat manipulation to enhance biologi-
cal control of Brassica pests by hover flies (Diptera: Syrphidae). Journal of Economic Entomology 88,
1171–1176.
Whitman, D.W. (1988) Allelochemical interactions among plants, herbivores and predators. In: Barbosa,
P. and Letourneau, D.K. (eds) Novel Aspects of Insect-Plant Interactions. John Wiley & Sons, New York,
pp. 11–64.
Whitman, D.W. and Eller, F.J. (1992) Orientation of Microplitis croceipes (Hymenoptera: Braconidae) to
green leaf volatiles: dose–response curves. Journal of Chemical Ecology 18, 1743–1753.
Wright, D.J. and Verkerk, R.H.J. (1995) Integration of chemical and biological control systems for arthro-
pods: evaluation in a multitrophic context. Pesticide Science 44, 207–218.
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5 Behaviour-modifying Chemicals:
Prospects and Constraints in IPM

Larry J. Gut,1 Lukasz L. Stelinski,1 Donald R. Thomson2 and

James R. Miller1
1Department of Entomology, Michigan State University, East Lansing, Michigan, USA;
2DJS Consulting, Seattle, Washington, USA

Introduction Since the early 1970s, considerable progress

in understanding insect behaviour and com-
Many organisms rely on chemical messages plementary advances in analytical chemistry
to communicate with each other or to find have led to the identification of thousands of
suitable hosts. Insects and other arthropods pheromones and other semiochemicals
appear to be especially dependent on chemi- (Mayer and McLaughlin, 1991; Hardie and
cal stimuli for survival and reproduction. Minks, 1999). Not surprisingly, a wide array of
Essential insect behaviours that may be stim- uses for semiochemicals has been tested over
ulated or inhibited by olfactory information the past few decades and many practical
include mating, feeding and oviposition. applications have become integral compo-
Chemical messages that trigger various nents in pest-management programmes
behavioural responses are collectively (Metcalf and Metcalf, 1992; Jones, 1998; Knight
referred to as semiochemicals. The term and Weissling, 1999; Suckling and Karg, 2000).
pheromone is used to describe compounds Applied scientists have long recognized
that operate intraspecifically (Karlson and the potential of using behaviourally active
Lüscher, 1959), while allelochemical is the compounds to trap insects (Lanier, 1990).
general term for an interspecific effector Monitoring the activity of insects with
(Whittaker and Feeney, 1971). Pheromones pheromone- or kairomone-baited traps is
are categorized according to function, now a standard practice in the majority of
including sex pheromones, aggregation pest-management systems. The information
pheromones, alarm pheromones, trail gathered can be used to time insecticide
pheromones and host-marking pheromones. applications or for determining the need to
Allelochemicals are classified based on the treat. Trapping is also widely used to detect
advantage of the message to the receiver or the presence of pests in quarantine or survey
sender. Alomones benefit the sender, programmes.
kairomones give advantage to the receiver The realization that behaviours critical to
and synomones benefit both parties. insect survival were strongly influenced by
Examples of these kinds of semiochemicals semiochemicals rapidly led to proposals for
include floral compounds that are attractive using these agents as practical tools for pest
to pollinators and plant-produced feeding or suppression (Wood et al., 1970; Shorey and
oviposition deterrents or stimulants. McKelvey, 1977). For example, some early
© CAB International 2004. Integrated Pest Management: Potential, Constraints and Challenges
(eds O. Koul, G.S. Dhaliwal and G.W. Cuperus) 73
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74 L.J. Gut et al.

pioneers proposed the tactic of broadcasting tactics based on semiochemicals have pro-
insect sex-attractant pheromones for direct gressed considerably since the earliest
control through communication disruption attempts at direct control. New regulations
(Gaston et al., 1967; Mitchell et al., 1974; governing the use of pesticides, increasing
Shorey et al., 1974). In addition to recogniz- environmental concerns and the regular
ing the strengths offered by semiochemical- occurrence of resistance to chemical controls
based controls, the early innovators also have provided a strong impetus for the
appreciated the weaknesses of behavioural adoption of novel technologies, including
controls (Knipling, 1979; Ritter, 1979; behavioural controls. In addition, growing
Mitchell, 1981). These inherent strengths and numbers of producers have recognized that
weaknesses are well worth reviewing. the weaknesses of behavioural controls are
As rendered by Miller and Cowles (1990), to some extent counterbalanced by the
damage to a crop can be approximated by the advantage of negligible environmental
expression: damage ∝ D  A  S  T, where impact and increased compatibility with bio-
D is the density of pest in a crop, A is the logical and cultural methods of control.
acceptability of the crop to the pest, S is the Although the majority of successful uses
suitability of the crop to the pest and T is the of semiochemicals are for monitoring pest
time of the interaction. Generally, as more of activity, there is an increasing number of
these parameters are reduced by a control tac- examples of direct control with pheromones
tic, the outcome for crop damage reduction and other behaviour-modifying compounds.
improves. For example, a great strength of The various approaches in which semio-
insecticides lies in the dramatic reduction in chemicals are used in pest management are
pest density, crop suitability and time of the listed in Table 5.1. Monitoring the activity of
interaction. The lack of a negative effect on insects using pheromone- or kairomone-
acceptability is actually advantageous in this baited traps is an integral part of many pest-
case because ingestion of the toxic substance is management programs. Trapping is often the
desired. Behavioural controls often do not kill most efficient method of detecting the
the target pest. In this case, they do not presence of a species or measuring its sea-
directly reduce pest density or the time of
pest–crop interactions, unless the mode of
Table 5.1. Practical uses of semiochemicals in
action is repellence. Thus, while insecticides
pest management (adapted from Knight and
can prove effective during their short lifespan Weissling, 1999).
on the crop, behavioural controls must remain
effective for longer durations, usually Monitoring
throughout the lifetime of the pest. 1. Detect the presence of a species
Additionally, behavioural controls can some- 2. Measure seasonal activity and provide decision
times lose their effect over time due to changes support
in physiological and behavioural thresholds 3. Evaluate the effectiveness of mating disruption
resulting from, for example, increased hunger 4. Assess levels of insecticide resistance
or build-up of eggs (Miller and Cowles, 1990). Direct control
The effectiveness of controls involving antibio- 1. Mass deployment of attractant-baited traps
sis is generally independent of pest density. In 2. Application of attract-and-kill formulations or
contrast, the efficacy of behavioural controls devices
can be density-dependent. Under such condi- 3. Pheromone-mediated mating disruption
tions, behavioural-control measures become 4. Manipulation of natural enemies using
more suited for management of pest popula- allelochemicals
tions that are below the outbreak threshold 5. Pheromone-based interference with host
rather than for suppression (sensu Knipling, location or acceptance
6. Plant allomone-based deterrence of feeding or
1979) after an outbreak has occurred.
oviposition
Despite some fundamental limitations, 7. Application of pheromones to enhance
the development and implementation of pollination
pest-management strategies and control
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Behaviour–modifying Chemicals 75

sonal activity. This kind of information is development and widespread commercial

helpful in making economically sound man- use of attractant-baited traps for monitoring
agement decisions. Attractant-baited lures and trapping insect pests in many agricul-
also form the basis for two direct control tural production systems, government detec-
measures: mass trapping and attract-and- tion and quarantine programmes, and
kill. Both strategies require a high level of consumer-protection efforts. Unlike other
attraction to the lure. Another set of direct sampling methods that may be very time
controls using pheromones or kairomones is consuming and require technical expertise,
based on interfering with an insect’s natural semiochemical-based monitoring is efficient
behavioural response to these compounds. and easy to use. In addition, the approach is
The most developed tactic is termed mating effective over a range of pest densities and
disruption. This approach entails releasing often provides the most practical means of
large amounts of synthetic sex pheromone monitoring adult activity.
into the atmosphere of a crop in an effort to
interfere with mate-finding, thereby control-
Detect the presence of a species
ling the pest by curtailing the reproductive
phase of its life cycle. Semiochemical-baited traps provide a rela-
Our chapter is not intended to be a com- tively simple and reliable means of detecting
prehensive review of the possible uses of pest infestations. They are one of the pri-
behaviour-modifying chemicals in pest man- mary tools employed in quarantine surveys
agement, nor will it attempt to identify all of to determine the presence of a species and
the constraints to successful deployment of prevent its establishment and spread
the various approaches. Several treatises cov- (Johnson and Schall, 1989; Schwalbe and
ering these subjects have been published over Mastro, 1990). Traps are routinely deployed
the past 25 years (Shorey and McKelvey, 1977; around airports and harbours to detect
Mitchell, 1981; Nordlund et al., 1981; potential introductions of exotic pests at
Kydonieus and Beroza, 1982; Jutsum and these high-risk sites. In a similar manner,
Gordon, 1989; Ridgway et al., 1990; Cardé and large numbers of traps are used in regional
Minks, 1995, 1997; Jones, 1998). In keeping survey programmes to determine the distri-
with the intent of this book, we present an bution of specific pests and to provide the
overview of the potential role of semiochemi- information needed for preventing spread to
cals in pest management and provide some new areas (Schwalbe and Mastro, 1990). The
examples of successes. The core of the chap- use of attractant-baited traps to demonstrate
ter, however, is a discussion of the constraints pest-free production zones is of increasing
and future prospects for mating disruption. importance. The process often requires
We have emphasized this approach over oth- implementing a defined monitoring pro-
ers largely for practical reasons. A review of gramme to allow for the export of an agricul-
the literature quickly reveals that mating dis- tural commodity to a specific country
ruption is the most highly developed and (Riherd et al., 1994). The monitoring proto-
widely adopted semiochemical-based control cols can be quite demanding, often specify-
tactic. In addition, over the past 5–10 years ing the kind of trapping system, the density
our personal efforts have focused on the prac- of traps and a specific treatment regimen if a
tical and commercial use of various mating single individual is detected.
disruption technologies in plant protection.
Measure seasonal activity and provide
decision support
Monitoring
Monitoring with attractant-baited traps is an
Applications of trapping systems important component of pest-management
programmes. The combination of pheromone
The production of synthetic copies of numer- traps and degree-day models can provide a
ous kinds of semiochemicals has led to the reliable method for monitoring adult activity,
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76 L.J. Gut et al.

predicting egg hatch and timing insecticide Table 5.2. Comparison of a degree-day model
sprays (Welch et al., 1981; Riedl et al., 1986; with a calendar approach for timing the first
Knight and Croft, 1991). The precision of this insecticide spray for control of hatching codling-
method of timing sprays has been well docu- moth larvae (based on Beers et al., 1993).
mented for codling moth, a key pest of pome
Accuracy in timing sprays (days)a
fruits throughout the world (Beers et al.,
1993). The phenology model for this pest is Year Model Calendar
based on accumulating degree-days (base
1979 0 3
10°C) beginning on the day the first moth is 1980 0 4
captured in a pheromone trap, provided 1981 2 13
moths are captured on two successive trap- 1982 0 2
ping dates. This start of sustained moth cap- 1983 1 8
ture is referred to as biofix. The first spray is 1984 0 18
applied at 121 degree-days (°C) post-biofix, 1985 1 1
which coincides with the start of egg hatch. 1986 0 13
In 6 of 10 years in the state of Washington, 1987 2 2
USA, this model predicted the start of egg 1993 0 6
hatch on the same day that it was first a Positive numbers indicate predicted timing was

observed in the field (Table 5.2) and there too early, negative numbers indicate predicted
was never a discrepancy of more than 2 days timing was too late.
between the predicted and observed event.
Prior to the development of the degree-day
approach, the first spray for codling moth in 2000). In some cases, captures in one year
Washington State was timed on a calendar can be used to predict events in a subsequent
basis. The emergence of moths from over- year. McBrien et al. (1994) demonstrated a
wintering sites was anticipated at full bloom correlation between catches of male mullein
on ‘Delicious’ apples and the first treatment bug, Campylomma verbasci (Herrich-Schaffer),
was applied 21 days after this event. Based in the autumn and the density of nymphs the
on this approach, treatments were often following spring in apple orchards. There
applied before egg hatch. In 7 of 10 years the has been developed for the eastern spruce
predicted start of egg hatch occurred at least budworm, Choristoneura fumiferana
3 days prior to observed hatch in the field (Clemens), an early-warning system that
and, moreover, predictions were over 13 uses male captures in pheromone traps to
days early on three occasions (Table 5.2). The predict a severe outbreak of this pest several
use of a degree-day model rather than a cal- years in advance (Sanders, 1988). Basing
endar approach to time insecticide applica- management decisions on adult catches
tions will become increasingly crucial in the rather than taking a preventive or calendar-
coming years because many new insecticide based approach is a key step in many efforts
chemistries, such as insect growth regula- to reduce insecticide inputs. The approach
tors, require precise timing as they are pri- typically entails intervening with a spray
marily active against specific instars or life only if catches exceed a predetermined level.
stages. The decision can be based on a single weekly
Semiochemical-based monitoring systems catch, consecutive catches or cumulative
can also be used to assess population trends catches over an extended period time, such
and determine the need to treat. Quantitative as a generation. Sticky-coated red spheres
relationships between adult captures and baited with synthetic apple volatiles can be
counts of larval stages or signs of larval feed- used to monitor apple maggot activity and
ing, such as faeces or damage, have been to alert growers as to the need for a spray
found for pests of tree fruits (McBrien et al., (Stanley et al., 1987; Agnello et al., 1990). An
1994; Bradley et al., 1998), annual crops (Van action threshold of eight flies per trap
Steenwyk et al., 1983) and forests (Sanders, allowed for a 70% reduction in sprays and
1988; Evenden et al., 1995; Morewood et al., acceptable levels of control. Reducing the
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Behaviour–modifying Chemicals 77

threshold to five flies per trap resulted in 0.6 be improved by increasing the amount of
fewer sprays, but the conservative threshold codlemone in the lure. Moth catch in dis-
was more likely to be adopted by apple rupted orchards increased considerably
growers. Treatment thresholds for codling when traps were baited with 10 or 20 mg of
moth based on moth captures in pheromone pheromone. Others have subsequently con-
traps have been developed for most pome firmed a significantly greater sensitivity of
fruit producing regions of the world (Riedl et 10 mg- compared with 1 mg-baited traps in
al., 1986; Wall, 1989). disrupted orchards (Barrett, 1995; Judd et al.,
1996). A further increase in moth captures in
orchards treated with mating-disruption dis-
Evaluate the effectiveness of mating disruption
pensers can be achieved by placing traps in
An increasingly important use of attractant- the upper canopy (Barrett, 1995). Although
baited traps is to measure the efficacy of the high-load pheromone trap is a useful tool
mating-disruption formulations. Capture of for monitoring codling-moth activity in dis-
zero (complete shutdown) or very few moths rupted orchards, when used alone it is not a
in a pheromone-baited trap has been used to reliable method for assessing the effective-
indicate successful disruption of the target ness of the pheromone treatment. Trapping
pest. The rationale behind this measure of should be used in conjunction with visual
mating-disruption effectiveness is that, if inspection of fruit for codling-moth damage.
male moths were incapable of finding a lure The biggest concern with using pheromone
releasing synthetic pheromone, they were traps to measure the effectiveness of mating
also unable to find a female moth releasing disruption, regardless of the lure load, is the
natural pheromone. Unfortunately, it is not regular occurrence of ‘false negatives’
uncommon to record low moth catches in (Knight, 1995). This refers to a situation
traps and still have less than adequate pest where low or no catches are recorded and
control in pheromone-treated plots (refer to yet fruit injury occurs in the block.
several chapters in Ridgway et al., 1990). In
some cases, it is possible to greatly inhibit
Assess levels of insecticide resistance
catches in pheromone traps but still detect
substantial numbers of mated females (Rice A dramatic rise in resistance to insecticides
and Kirsch, 1990; Atanassov et al., 2002) or over the past decade (Norris et al., 2003) has
actual mating (Suckling and Shaw, 1992). In brought about an acute need to have simple
the former situation where mated females and reliable methods for monitoring its
are found in treated plots, it is possible that a severity and distribution. Pheromone-trap
portion of these females immigrated from bioassays are one of the more widely
adjacent plots not treated with pheromone. adopted methods for assessing the suscepti-
There have been two approaches to bility of lepidopteran pests to insecticides.
improving the usefulness of pheromone- The basic approach was developed by Riedl
baited traps as monitoring tools in et al. (1985) to test codling-moth susceptibil-
pheromone-treated plots. Cardé and Elkinton ity to azinphosmethyl. It has since been
(1984) suggested that a lure with an emission modified and used to evaluate the tolerance
rate closer to the natural rate would seem to of other pests to various insecticides
be the most suitable for measuring the effi- (Suckling et al., 1985; Haynes et al., 1987;
cacy of a disruption treatment. Charmillot Knight and Hull, 1989; Varela et al., 1997;
(1990) took a different approach, opting to Shearer and Usmani, 2001). The bioassay
use lures with very high release rates as a entails collecting large numbers of males in
means of following changes in adult popula- traps and testing for expression of resistance
tion densities in spite of air permeation with by topical application of insecticides or
pheromone. In a series of experiments over through incorporation of insecticide into the
the course of 2 years, he showed that, for glue. The major advantage of pheromone-
codling moth, the sensitivity of pheromone trap bioassays over most other methods of
traps in pheromone-treated orchards could assessing resistance is that many individuals
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78 L.J. Gut et al.

can be tested without incurring the costs in tems as quantitative decision tools is due in
time and money associated with rearing part to the substantial effect that trap design,
large numbers of larvae. The simplicity of attractiveness of delivery device, trap mainte-
the trap bioassay does not come without nance programme, and placement in the crop
trade-offs. Dose–mortality responses may be have on the performance of the system.
strongly affected by a number of factors, Various trap designs and means of dispens-
including whether the toxicant was deliv- ing attractants have been developed for mon-
ered topically or through the adhesive itoring insects (Cardé and Elkinton, 1984;
(Knight and Hull, 1989; Shearer and Riedl, Wall, 1989; Jones, 1998). The majority of trap
1994). The technique may overestimate the types employ a sticky surface to capture
impact of resistance in the field because only attracted insects. Other trap designs rely on a
males are captured and assayed. Sex-related flight barrier, often combined with a knock-
differences in the tolerance to organophos- down insecticide or a liquid trapping medium
phorous and carbamate insecticides have to retain attracted insects. Attractants are com-
been discovered for populations of Oriental monly formulated in reservoirs made of vari-
fruit moth in the USA, with females more ous materials, including rubber, polyethylene,
susceptible than males (deLame et al., 2001; polyvinyl chloride and hollow fibres.
Shearer and Usmani, 2001). A major limita- The probability of insects finding a trap is
tion of the approach is that it cannot be used highly dependent on the attractiveness of the
to monitor for resistance to materials whose lure and the placement of the trap. Traps
primary mode of action requires ingestion. may be placed within or outside the crop, on
Unfortunately, this includes most of the the edge or interior of the plot, high or low
newer insecticide chemistries, such as insect in the canopy or on different sides of a tree.
growth regulators and neonicotinoids. The location of the trap with respect to these
parameters can have a substantial impact on
moth catch. For example, differences in cap-
Performance of trapping systems tures due to vertical positioning of traps
within the crop canopy have been docu-
The development and commercialization of mented in both annual and perennial crops.
pheromone- or kairomone-based monitoring Riedl et al. (1979) demonstrated that catches
systems has greatly enhanced society’s ability of male codling moth varied substantially
to monitor and manage insect pests. As a depending on trap placement in the tree
means of estimating population density or canopy (Fig. 5.1). Higher catches were
predicting crop damage, however, the strategy recorded in the upper compared with lower
has proved to be of more limited utility. Morse canopy positions. Very few moths were cap-
and Kulman (1985) found no significant rela- tured above or below the canopy. Simandl
tionship between catches of the yellow- and Anderbrant (1995) documented a similar
headed spruce sawfly, Pikonema alaskensis, and outcome for the sawfly, Neodiprion sertifer
the degree of defoliation inflicted by this pest. (Geoffroy). Pheromone traps installed in the
A lack of correlation between moth catches crowns of conifers (> 9 m) caught up to 15
and egg numbers has been reported for sev- times as many males as did traps suspended
eral vegetable pests; examples are Helicoverpa at 2.5 m. Derrick et al. (1992) found that traps
zea (Boddie) on tomato (Campbell et al., placed within maize fields at ear level (1.5 m)
1992) and field maize (Latheef et al., 1991). captured greater numbers of European corn
A trap will sample only a portion of the borer, Ostrinia nubilalis (Hübner), than traps
pest population in an area. For a trap to accu- hung in the field at canopy height (3.0 m).
rately reflect the true population density and Trap design and maintenance will influ-
thus the potential for crop loss, the trap’s ence the likelihood of capturing an insect
attractiveness should remain constant, as after it finds the trap. The effectiveness of
should the proportion of the individuals from many trap designs depends on maintaining
the population that are captured. The inade- the integrity of trap shape and the quality of
quacy of attractant-baited monitoring sys- the adhesive surface throughout the season.
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Behaviour–modifying Chemicals 79

4 m canopy
height
40

Proportion caught (%)

30

20

10

0
0.5 1.4 2.3 3.2 4.1
Trap elevation (m)

Fig. 5.1. The influence of canopy position on codling-moth captures in pheromone traps (from Riedl et al.,
1979).

Traps that depend on a sticky surface to cap- ing range. Using this approach, they were
ture insects can lose their ability to retain able to restrict the sampling of Cydia molesta
new arrivals if the surface becomes covered (Busck) to the immediate vicinity of the trap
with debris or target and non-target insects. by lowering the dose. Faccioli et al. (1993)
The efficiency of trapping for codling moth found that reducing the pheromone dosage
declined as catches exceeded 20–30 moths in in traps for the polyphagous pest
traps with a 185 cm2 sticky surface, while Argyrotaenia ljungiana (Thunberg) enhanced
catches of 50–60 moths unacceptably the correlation of moth catch to larval infes-
reduced the performance of traps with a tation. The major reason for the improved
360 cm2 sticky surface (Riedl et al., 1986). precision was a decrease in the number of
Under conditions of moderate or high pest ‘false positives’ or cases of high catch with
pressure, traps can quickly become saturated little or no concurring infestation. There are
with moths and diminish the likelihood of other possibilities for mitigating the effects of
accurately measuring pest density by moth sampling large numbers of individuals from
captures. outside the crop on the usefulness of trap-
ping information. The simplest approach for
highly polyphagous pests would be to avoid
placing traps close to the perimeter of a plot
Future prospects
as a large portion of the area monitored by
the trap would be outside its boundaries.
Drawing range of lures
However, placing traps in the interior still
A crucial problem with using pheromone- may not sufficiently limit the active space. A
baited traps to measure pest density and pre- significant number of insects may move con-
dict damage is that insects may be attracted siderable distances prior to attraction, effec-
from distances well beyond the boundaries tively increasing the area of influence of a
of the crop. Using the mark-and-recapture trap (Wall and Perry, 1987). Knight and Hull
technique, Thayer (2002) demonstrated that (1988) found that a better correlation
male oblique-banded leaf-rollers could be between pheromone-induced catches of
captured in pheromone traps at distances of tufted apple-bud moth, Platynota idaeusalis
up to 440 m from the release point. The (Walker), and damage could be obtained if
active space of a trap baited with 1 mg of predictions were based on captures early in
pheromone was calculated to be 152,000 m2 the flight, presumably before substantial
or nearly 15 ha. Baker and Roelofs (1981) rec- movement by the moths, rather than over
ognized the problems associated with a large the entire flight period. Another promising
active space and proposed modifying the approach is to bait traps with a lure that
dose of the attractant to optimize the draw- attracts both males and females.
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80 L.J. Gut et al.

Monitoring males and females (Light et al., 2001; Alan Knight, Washington,
USA, 2002, personal communication).
The use of a food bait or specific kairomone
Additional research on cultivar effects and
that attracts both sexes offers some distinct
the range of attraction is crucial to the devel-
advantages over a sex-pheromone lure that
opment of a reliable pear ester-based moni-
attracts males only. Capture of females is
toring system for codling moth.
more directly linked to oviposition and the
potential for larval damage. Because females
in many species do not disperse great dis- Commercial implementation of monitoring
tances, catch of females may more accurately programmes
reflect pest densities in the block that is
Perhaps the greatest factor limiting the use-
being monitored.
fulness of attractant-baited traps is the incon-
The attraction to host volatiles should not
gruence between the monitoring programme
be greatly impeded or suppressed by
that is developed and tested through experi-
pheromone-based mating disruption, offer-
mentation and the system that is actually
ing the possibility of a means of monitoring
implemented in the field. Researchers focus
pest density in disrupted plots. Traps baited
with a brown sugar and terpinyl acetate on developing a tool and set of monitoring
solution have been used to monitor Oriental guidelines that are scientifically sound but
fruit moth activity in pheromone-treated often impractical. For example, treatment
pome and stone-fruit orchards (Sexton and thresholds for codling moth in apple or pear
Il’ichev, 2000; Il’ichev and Sexton, 2002; were largely developed based on a trapping
Il’ichev et al., 2002). These food traps are not density of one trap per hectare because this
specific to Oriental fruit moth, but they do was determined to be the active space of a
capture females and males of this species and trap. For an integrated pest management
provide a more reliable measure of pest pres- (IPM) practitioner, the economically ‘practi-
sure than pheromone-baited traps. More cal space’ is closer to one trap per 4 ha. A
recently, ethyl-(2E,4Z)-2,4-decadienoate (DA), consultant is typically paid a set fee based on
a volatile present in the odour of ripe Bartlett the size of the block monitored and must
pears, has been identified as a compound carefully consider the time involved in
that is attractive to both sexes of codling inspecting and maintaining traps in deciding
moth (Light et al., 2001). This pear ester is a how many to deploy. From the researcher’s
stable compound that can be readily synthe- perspective, a consultant or other IPM practi-
sized and loaded into a rubber septum to tioner often ignores critical aspects of trap
make a lure for monitoring both sexes of placement or maintenance. In fruit orchards
codling moth. Comparisons of DA and in the USA, codling-moth traps are routinely
pheromone lures to monitor the activity of placed at ‘truck-window’ height, as well as
codling moth have been carried out for the on the very edge of a block. This certainly
past few years, most extensively in the west- facilitates inspecting the trap but is counter-
ern USA. Trials by a team of scientists (Light productive because very few moths will be
et al., 2001) indicated that DA lure-baited caught. The typical justification for placing
traps provided good resolution of moth traps in less than optimum positions is that
flight patterns for both sexes in conventional the best monitoring system is the one that
and especially mating-disrupted orchards. provides the most reliable estimate of the
A number of factors may influence the population, not necessarily the catch of the
performance of traps baited with the DA lure greatest number of insects. However, it is
and should be considered when using this essential to have at least adequate numbers
trapping system. The crop or cultivar in upon which to base a decision. Moreover,
which traps are placed influences moth catch there is likely to be no relationship between
in traps baited with the pear ester. Higher information garnered from a poorly run
catches with this kairomone lure were trapping programme and thresholds or other
recorded in walnut and in some late-season information that has been generated through
apples than in pear or in early-season apples more carefully conducted experiments.
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Behaviour–modifying Chemicals 81

The bottom line is that the best monitoring trapping, attract-and-kill and other practical
programme will develop through an aware- applications of this pest-management
ness and consideration of the concerns and approach have been reviewed comprehen-
limitations expressed by the researcher and sively (Bakke and Lie, 1989; Lanier, 1990;
the practitioner, especially the cost of the pro- Jones, 1998). Here we summarize the con-
gramme. For example, effective monitoring straints, provide examples of some successes
of codling moth can be achieved by placing and offer some challenges for the future.
traps at mid-canopy height, and at a density
of one trap every 4–6 ha on farms with large
uniform plantings without a history of local- Mass trapping
ized infestations. A tighter spacing of traps is
required on farms with small plantings or a The aim of mass trapping is to prevent crop
suspected uneven distribution of codling- damage by capturing a substantial propor-
moth pressure or in mating-disrupted blocks. tion of a pest population prior to mating,
Finally, in pheromone-treated orchards, con- oviposition or feeding. Success with this
sultants are urged to place traps high in the method requires the combination of a very
canopy. attractive lure and a highly efficient trap.
Although examples of mass trapping for pest
control are fairly plentiful (see Table 5.3 for
Attraction–annihilation examples), most efforts have not been suc-
cessful from the standpoint of commercial
Attraction–annihilation is probably the earliest adoption.
use of attractants for pest control. Many early
efforts were discouraging or, when effective
Constraints
control was demonstrated, practical deficien-
cies often inhibited the commercial adoption The commercial viability of mass trapping is
of the control system. The principles of attrac- limited by a number of practical and biologi-
tion–annihilation and the potential of mass cal requirements. Of foremost importance

Table 5.3. Some promising applications of attraction–annihilation for insect pest management.

Approach Pest References

Mass trapping
Attractants and water-based funnel traps Carpophilus beetles James et al., 1996
Attractant-baited traps Japanese beetle Wawrzynski and Ascerno, 1998
Sex pheromone-baited traps Chinese tortrix Zhang et al., 2002
Attractant-baited multisurface traps Cigarette beetle Buchelos and Levinson, 1993
Pheromone-based mass trapping Ambrosia beetles Borden, 1990
Inhibitor combined with mass trapping Mountain pine beetle Lindgren and Borden, 1993
Sex pheromone-based mass trapping Beet armyworm Park and Goh, 1992
Attract-and-kill
Pesticide-treated spheres Apple maggot fly Prokopy et al., 2000;
Stelinski et al., 2001
Pesticide-treated spheres Blueberry maggot fly Ayyappathe et al., 2000;
Stelinski and Liburd, 2001
Pheromone bait spray Olive fly Jones, 1998
Sex-pheromone-based attracticide Codling moth Charmillot et al., 2000
Sex-pheromone-based attracticide Light-brown apple moth Suckling and Brockerhoff, 1999
Autodissemination
Pheromone trap and fungus Diamondback moth Furlong et al., 1995
Attractant trap and fungus Japanese beetle Klein and Lacey, 1999
Pheromone trap and baculovirus Tobacco budworm Jackson et al., 1992
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82 L.J. Gut et al.

are the costs of substantial numbers of traps some pest damage in exchange for a per-
and the expenses for the material and labour ceived reduced exposure to insecticides. In
needed to maintain them. The technique is parks and city plantings, 80–90% rather than
more useful for the control of low-density 100% control may be acceptable. Male
than high-density populations. Traps can removal using sex-pheromone traps was
quickly become saturated with insects at demonstrated to be an effective means of
high densities. If the attractant is a sex controlling Chinese tortrix, Cydia trasias, on
pheromone, mass trapping will require street-planted Chinese scholar trees (Zhang
many traps to be effective against high-den- et al., 2002). Four years of mass trapping with
sity populations because of competition with a sex and floral lure reduced a small pocket
calling females (Knipling, 1979). The kind of Japanese beetles in a city park by 97%
and potency of the attractant influence the (Wawrzynski and Ascerno, 1998).
outcome of a mass trapping programme. The The prospects for mass trapping are
chances for success are improved if both enhanced if population densities are low or
males and females are attracted to the trap. If if the technique is carried out in an area
only males are trapped, it is essential that where immigration by the pest from outside
they be captured before mating. In most the treated area is limited. The success of the
insect species, males can mate more than above-mentioned efforts in urban or park
once; thus a very high proportion of individ- settings was, in part, due to the isolation of
uals needs to be removed from the popula- the sites and the relatively low pest densities.
tion to obtain the high reduction in female Attempts to control Japanese beetle in other
fecundity required for control (Roelofs et al., settings or where population densities were
1970). Therefore, optimizing the lure is criti- high have proved ineffective (Klein, 1981;
cal to the success of mass trapping. Synthetic Gordon and Potter, 1985, 1986). Food ware-
lures must compete well with natural attrac- houses and other enclosed situations provide
tive sources. The lure must be potent enough a high level of isolation, which should
to draw in insects from a considerable dis- enhance the prospects for mass trapping
tance without impeding progress once they (Suckling and Karg, 2000). Control of
are close to the source. Trap density is based Mediterranean flour moths, Ephestia
on both economic considerations and the kuehniella Zeller, in flour mills was achieved
attractiveness of the lure. The spacing of through the mass deployment of
traps should be such that competition pheromone-baited funnel traps combined
between traps occurs, but just to a level that with careful cleaning of the rooms and
does not reduce the total kill (Lanier, 1990). machinery (Trematerra and Battaini, 1987).
Finally, as pointed out in the monitoring sec- Perhaps the most successful use of this
tion, the ability to attract and retain very tactic has been for the control of some species
high numbers of individuals will be affected of forest beetles. Semiochemicals play a major
by trap design, placement and maintenance. role in the process of host colonization by
bark beetles. Intensive trapping of bark bee-
tles for pest control is facilitated by their high
Prospects
dependence on aggregation pheromones that
The success of a mass-trapping programme are attractive to both sexes as they mass
is directly related to the desired outcome. A attack a host. Mass trapping combined with
very high percentage of the individuals in other control measures, such as sanitation
the population must be removed if the toler- cutting, were used to control populations of
ance for damage is very low. Pests that cause the conifer bark beetle, Ips typographus
direct damage to a crop and have tolerances (Linnaeus), in Norway and Sweden (Bakke
near zero are probably not the best choices and Lie, 1989). One of the most effective uses
for this control tactic. Better opportunities for of mass trapping has been for control of
mass trapping are in situations where there ambrosia beetles in timber-processing facili-
is some flexibility in the desired outcome, ties in British Columbia (Borden, 1990). In
such as where the public is willing to tolerate this case, the programme probably benefited
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Behaviour–modifying Chemicals 83

from the trapping area being somewhat iso- Greece through various attract-and-kill
lated from beetle populations in the forest strategies. His review illustrates well the
(Schlyter and Birgersson, 1999). Control of process of developing this approach for fruit-
some forest beetles may be enhanced by use fly control. Protein/insecticide-bait sprays
of deterrents to ‘push’ the target beetles away have been used for control of this pest in
from a host, combined with attractant-baited most Mediterranean olive-growing areas for
traps or trap trees to ‘pull’ them away a number of years. A major concern with this
(Borden, 1997). Aggregation and anti-aggre- tactic is that the bait is highly attractive and
gation pheromones were successfully used in toxic to natural enemies. To overcome the
this push–pull manner against the mountain detrimental effects on natural enemies, a sys-
pine beetle, Dendroctonus ponderosae Hopkins tem was developed based on the use of target
(Lindgren and Borden, 1993). traps baited with either a food-attractant or a
sex-pheromone dispenser. This target-device
method of controlling B. oleae was effective at
Attract-and-kill reducing fruit infestation, especially when
applied on an area-wide basis. In addition,
As a control tactic, attract-and-kill is similar the effectiveness of the device allowed for a
to mass trapping in that an attractant-based reduction in the use of bait sprays and an
system is used to eliminate a substantial pro- accompanying increase in natural-enemy
portion of a pest population and thereby pre- populations. The most recent development
vent unacceptable levels of crop damage. for fruit-fly control has been a microencapsu-
The major difference is that the attract-and- lated sprayable formulation comprised of the
kill approach relies on a toxicant, rather than sex pheromone of this species, 1,7-dioxaspiro,
a trap, to remove individuals that respond to and an insecticide (either malathion or
the synthetic attractant. In many ways this dimethoate). Interestingly, the pheromone-
technique suffers from the same constraints bait spray has provided significant reduc-
as outlined for mass trapping, including tions in fruit infestation, while attempts to
population density, attractiveness of the lure use the pheromone as a mating disruptant
and efficiency of the method of killing. A only have failed because the approach pro-
major advantage of the attract-and-kill duces substantial immigrations of male and
approach is that the problem of trap satura- female olive flies into the treated area.
tion can be eliminated. This may improve Concerted efforts to develop lure-baited
the effectiveness of control in high-density trapping systems for control of Rhagoletis
situations. The issues of trap maintenance fruit flies are ongoing in the eastern and
and the high cost of the control programme Mid-western USA. Some early success was
can also be mitigated to some extent, espe- achieved using sticky-coated red spheres for
cially if the system relies on attracting the direct control of Rhagoletis pomonella (Walsh)
insect to a plant surface that has been treated (Duan and Prokopy, 1995). A major impedi-
with an insecticide rather than to some kind ment to commercial adoption of this control
of target device (Jones, 1998). system was the high level of maintenance
Attract-and-kill formulations have been required to ensure trap effectiveness. Recent
developed for control of various beetles, efforts, therefore, have focused on develop-
moths and especially flies (see examples in ing a system that relies on a small dose of
Table 5.3). Some of the earliest and most toxicant, rather than a sticky material, to kill
widely tested applications of attractants in alighting flies. Biodegradable or wooden
combination with insecticides have been for spheres laced with a low dose of imidaclo-
control of tephritid fruit flies (Jones, 1998). prid show promise for control of R. pomonella
They have largely evolved from attempts to in apple and Rhagoletis mendax Curran in
mass trap these insects, which often failed blueberry (Hu et al., 1998; Liburd et al., 1999;
because of the problem of trap saturation. Ayyappathe et al., 2000; Prokopy et al., 2000;
Jones (1998) has summarized efforts to con- Stelinski and Liburd, 2001; Stelinski et al.
trol the olive fly, Bactrocera oleae Gmelin, in 2001). Pesticide-treated spheres rely on a
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84 L.J. Gut et al.

combination of attractants, a feeding stimu- has been tested for control of this pest, using
lant and a toxicant to lure and kill the target the fungal pathogen Metarhizium anisopliae
pest. Sphere shape and colour and fruit- (Klein and Lacey, 1999). High levels of mor-
volatile or food-based lures are the major tality were recorded for beetles emerging
attractants. The insecticide is incorporated from the trapping device. In addition, it was
into the latex paint used to colour the demonstrated that contaminated beetles
spheres, which aids in maintaining the resid- could pass the fungus to untreated beetles in
ual activity of the toxicant. Sucrose is used as quantities sufficient to kill a high proportion
a feeding stimulant, which coerces flies to of the population.
ingest lethal doses of toxicant. Placement of A number of deficiencies will have to be
biodegradable spheres baited with an attrac- overcome to make the autodissemination
tive component of host odour, butyl hexa- approach a commercially viable option.
noate, on perimeter trees of commercial Some innovation will be required to design
apple blocks were nearly as effective as effective transfer stations. For example, Vega
insecticide sprays at intercepting apple mag- et al. (1995) invented an autoinoculating
got flies and preventing fruit injury (Prokopy device that induces sap beetles to pick up
et al., 2000). whatever microorganism is loaded into it.
The pathogens that are placed in delivery
stations should also be readily transferred
Autodissemination between individuals. Suckling and Karg
(2000) pointed out that fungi might be the
Autodissemination is an innovative and best candidates as they are transferred
promising control technique that combines between adults and larvae, and do not
an attractive lure with an entomopathogen. require consumption or copulation to
Suckling and Karg (2000) recently proposed become pathogenic. Once an appropriate
the term ‘lure and infect’ to describe this pathogen is selected, a formulation must be
approach and provided a good summary of developed that protects the organism from
its limitations and unique advantages. environmental degradation. A major con-
Individuals that arrive at the source are not straint with these systems, as with mass-
killed, but rather are inoculated with the trapping strategies, is likely to be the ability
pathogen and hopefully magnify the treat- to make them cost-effective as many bait sta-
ment by spreading the disease to other indi- tions may need to be deployed for the
viduals. The host specificity of the pathogens approach to be effective. Finally, a general
means that the method will be highly com- public concern over the production of
patible with biological control. pathogens and their release into the environ-
The approach has been attempted using a ment may limit the development and accep-
variety of disease organisms (Table 5.3). Shapas tance of this technique.
et al. (1977) substantially suppressed popula-
tions of a stored-product pest, Trogoderma
glabrum (Herbst), using a combination of its Mating Disruption
pheromone and spores of a pathogenic proto-
zoan, Mattesia trogodermae. Autodissemination The most successful approach using semio-
of a baculovirus for management of tobacco chemicals for pest control over the last few
bud-worm has been tested by Jackson et al. decades has been the release of large
(1992). The effectiveness of a pheromone trap amounts of synthetic pheromone into a crop
designed to deliver conidia of a fungal in an effort to prevent or delay mating. The
pathogen has been explored for control of the potential to control insects through mating
diamondback moth, Plutella xylostella disruption was first demonstrated for
(Linnaeus) (Furlong et al., 1995). A fungus is Trichoplusia ni (Hübner) over 30 years ago
also being developed for use against Japanese (Gaston et al., 1967). Similar efforts with other
beetle. A Trece Catch Can Japanese-beetle trap moth species confirmed that dispensing large
modified to serve as an inoculation chamber quantities of pheromone into a crop could
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Behaviour–modifying Chemicals 85

disrupt mate location, thereby controlling the such as the development of new techniques
pest by interfering with the fertilization of for identification and synthesis of
eggs (Mitchell et al., 1974; Shorey et al., 1974; pheromones and devices for releasing the
Taschenberg et al., 1974; Rothschild, 1975). pheromone over an extended period of time.
There has been considerable progress in Often overlooked was the strong involve-
the application of formulated pheromone for ment of government agencies, both in
direct pest control since the first promising research and in technology transfer.
trials. Through the combined efforts of Companies developing mating-disruption
researchers, private entrepreneurs, extension products typically had very small research
personnel and others, mating disruption has budgets, with support provided primarily as
become an accepted control option for a donations of product to government
number of lepidopteran pests of fruits, veg- researchers to conduct efficacy trials.
etables and forests (Ridgway et al., 1990; Government agencies have played a particu-
Cardé and Minks, 1995, 1997). A listing of larly important educational role in area-wide
commercial formulations currently regis- projects and deserve a great deal of the credit
tered for use in North America and the esti- for providing technical expertise and demon-
mated total area treated in 2002 (Table 5.4) strating the benefits of mating disruption
provides strong testimony to the success of (Staten et al., 1997; Calkins et al., 2000;
this approach. Il’ichev et al., 2002). Finally, changes in regu-
A number of developments had to occur latory requirements were made that acceler-
in order to make mating disruption an effec- ated the registration process (Thomson et al.,
tive and economically viable control tactic. 1998).
Continual advances in understanding the Although substantial inroads into com-
many biological characteristics, behavioural mercial markets have been made since the
and otherwise, that influence the outcome of early 1980s, disruptants and other semio-
a mating-disruption programme were cer- chemical products continue to hold a rather
tainly instrumental in paving the way. Some small share of the total pest-control market.
advances were more technical in nature, Jones and Casagrande (2000) placed the

Table 5.4. Commercial disruption formulations registered for use in North America and estimated area
treated in 2002.

Number of Per cent Current

formulations of total market
Reservoir- Hectares hectares value
Crop Pest type Other treated planted ($US)

Almond Peach-twig borer 2 1 200 < 0.1 30,000

Apple Codling moth 6 4 45,000 18.0 13,750,000
Leaf-roller 2 1 1,600 0.6 200,000
Oriental fruit moth 2 2 400 0.1 40,000
Cotton Pink bollworm 2 2 8,900 0.2 562,000
Cranberry Black-headed fireworm 1 2 200 1.5 25,000
Sparganothis fruitworm 1 100 0.7 12,500
Grape Grape berry moth 2 1 300 0.1 18,750
Omnivorous leaf-roller 1 1 500 0.1 31,250
Peach Oriental fruit moth 4 3 17,800 26.2 1,780,000
Peach-twig borer 2 1 600 0.9 90,000
Pear Codling moth 6 4 8,000 28.6 2,200,000
Tomato Tomato pinworm 2 2 10,000 5.6 72,000
Walnut Codling moth 1 3 1,200 1.5 330,000
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86 L.J. Gut et al.

worldwide sales of semiochemical products at of mating disruption is dependent upon

about US$70–80 million or about 1% of the population density, the ecological setting of
agrochemical market. More recently, the the treated area, and specific traits of the tar-
world pheromone market for mating-disrup- get species. Key biological traits include host
tion products was estimated to be $80 million specificity, dispersal capacity, number of gen-
(K. Ogawa, Japan, 2002, personal communica- erations and adult lifespan, fecundity, char-
tion). A limited understanding of what is acteristics of pheromone emission by the
required to achieve success, technical defi- female and other aspects of mating behav-
ciencies and tightening profit margins in agri- iour.
culture are the principal factors that have Experience teaches us that the effective-
slowed the rate of adoption of mating disrup- ness of mating disruption is compromised in
tion. situations where mated females invade from
Even some of the failures have been use- outside the treated area. Treatment with
ful for identifying patterns that will improve pheromone alone provides no protection
our ability to select pest species, production against immigrating females, which can
systems and specific sites that will maximize readily deposit fertile eggs. Immigration of
the chance for the success of mating disrup- gravid females is believed to be a key
tion from the outset. The discussion that fol- process that contributes to the development
lows is an attempt to identify and synthesize of border infestations (Tatsuki, 1990; Il’ichev
the patterns that have emerged since the first et al., 2002). It follows that a high dispersal
disruption field trials were conducted some capacity and a wide host range are life-
40 years ago. history traits that tend to reduce the suitabil-
To a large extent, the potential for the suc- ity of a species for mating disruption.
cess of mating disruption is determined by Furthermore, the impact of these traits
the following set of biological parameters: should be most pronounced where the area
treated with disruptant is adjacent to
● Biology/ecology of the target species.
untreated areas that harbour hosts for the
● Male sensitivity to the pheromone (physi-
target pest.
ological).
As with other semiochemical-based con-
● Chemical characteristics of the pheromone.
trol tactics, there is often a strong interaction
● Influence of the physical environment.
between population density and the effec-
It is how this suite of features plays out for a tiveness of mating disruption. In many
specific pest, commodity or site that deter- instances, high-density populations are more
mines the suitability of mating disruption for difficult to control with this technique than
that particular situation. Once the decision is less dense populations. For example, the best
made to implement a mating-disruption pro- disruption of codling moth has been
gramme, its commercial success depends on achieved where pest pressure is low, while
a set of operational parameters that provide attempts to control high-pressure popula-
for effective delivery of the active ingredient. tions have been problematic at best (Trimble,
Practical considerations, such as cost, ease of 1995; Gut and Brunner, 1998; Vickers et al.,
application and the reliability of a scouting 1998). In an effort to mitigate the effects of
programme will determine the extent to population density, growers typically apply
which users will embrace this technique. one or more companion insecticide sprays to
reduce pest pressure.
It is worth noting that, for some pest
Pest biology and ecology species, mating disruption is equally effec-
tive over a range of population densities.
A number of biological and ecological attrib- Field trials to determine the effectiveness of
utes are likely to influence the suitability of a disruption for control of peach-tree borer,
pest species as a candidate for control by Synanthedon exitosa (Say), were conducted in
mating disruption (Rothschild, 1981; Cardé peach orchards in Georgia, USA, using
and Minks, 1995; Sanders, 1997). The success Hercon vinyl laminated dispensers loaded
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Behaviour–modifying Chemicals 87

with 43 mg of the main component of the proteins (Klein, 1987). Finally, the binding
pheromone for this species, (Z),(Z)-3,13- protein complexes travel from the pores to
octadecadienyl acetate (Snow, 1990). receptors on the dendritic membranes of the
Excellent control was achieved under either odour neurons. After activation of the den-
moderate or heavy population pressure. dritic receptor, pheromone molecules must
Damage was recorded in the high-density be rapidly removed in order for the moth to
area in the first year of the trial, but no mat- detect further stimuli. This is thought to be
ing was recorded on mating tables, and lar- achieved by enzymatic degradation of the
val infestation was attributed to infiltration pheromone molecules (Vogt and Riddiford,
of mated females from outside the treated 1986; Rybczynski et al., 1989). The rapid ter-
area. After 2 years, it was impossible to con- mination of the pheromone signal by
duct further trials in these peach blocks degrading enzymes is required for the high
because the population had essentially been quantitative and temporal resolution of the
eliminated. We will return to this apparent odour signal (Stengl et al., 1992).
disparity in the effect of density on mating The electric potential generated across
disruption, as we believe it is of critical moth antennae after stimulation with their
importance in identifying promising targets pheromone was successfully measured by
for this technique. Schneider (1956, 1962) using the electroan-
tennogram (EAG) technique. An EAG mea-
sures the depolarization of receptor potentials
Male response to pheromone summed across the antennal olfactory neu-
rones over the length of the antenna. EAGs
The male’s response to pheromone is per- have been an effective means of identifying
haps the most important biological charac- the sensitivity of moths to odorants, quantify-
teristic determining the outcome of a ing dose–response relationships and measur-
mating-disruption programme. ing adaptation effects at the peripheral level
of odour detection. Other researchers began
to perform extracellular recordings from sin-
Perception
gle sensilla and thus demonstrated the speci-
The most important and specialized mate- ficity of populations of sensilla to odorants in
detection organs in moths are the antennae. various insect taxa (Den Otter, 1977; Dickens,
These comb-like or hairy, rod-shaped struc- 1979; Fonta and Masson, 1987; Almaas and
tures are adapted to sift odorant molecules Mustaparta, 1990).
from the air, which are then perceived by Moth pheromones are commonly com-
specifically tuned receptor cells. These olfac- prised of complex blends of components
tory receptor neurones elicit receptor poten- (Tamaki, 1979; O’Connell, 1981). Although
tials in response to species-specific the major components of such blends often
pheromone components which manifest in elicit some behavioural responses typical of
specific patterns of action potentials that con- males responding to calling females, usually
vey information about both odorant quantity the full complement and correct ratio of com-
and quality to the moth’s brain (Kaissling, ponents are required to induce the complex
1986). Usually, just a few receptor neu- sequence of male sexual behaviours (Linn et
rones are situated within hair-like, odour- al., 1984). Such sensitivity to specific blend
perceiving structures, called sensilla, covering ratios is believed to function as a mechanism
the external surfaces of moth antennae. for maintaining species isolation (Linn and
Pheromone molecules adsorb on to the sur- Roelofs, 1983). It is thought that numerous
face of sensilla and diffuse into the interior types of narrowly tuned receptor neurones are
sensillum through minute pores sprinkled specialized for detecting each separate
over the exterior sensillar shaft. Once inside pheromone component; this is known as the
the sensillum lymph, the hydrophobic component hypothesis (O’Connell, 1972; Den
pheromone molecules are dissolved through Otter, 1977; Akers and O’Connell, 1988;
the association with pheromone-binding Almaas et al., 1991). However, there is also
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88 L.J. Gut et al.

evidence that separate components of a multi- The first two mechanisms result from
component pheromone blend may interact prolonged exposure to high and/or constant
with common receptor binding sites; the blend concentrations of pheromone delivered by
hypothesis (O’Connell, 1985; Christensen et synthetic dispensing systems. Under the
al., 1989). Receptors having a very high affin- third mechanism, it is assumed that male
ity for pheromonal compounds are said to be moths are unable to distinguish between
‘tuned’ to that odour stimulus. Such ‘tuning’ female-produced pheromone plumes and the
is based on molecular shape, length of the background concentration of pheromone
carbon chain and position of double bonds emanating from dispensers. Finally, the
and functional groups (Todd and Baker, fourth model postulates that males may
1997). follow the pheromone plumes generated by
point sources of synthetic dispensers. Real
females are thought to be out-competed by
Orientation
false plumes. Different combinations of the
A female-produced pheromone plume is a above mechanisms may be important in
filamentous structure of varying internal practical mating-disruption programmes
concentration detected by males as a series based on crop canopy structure, wind speed,
of stimulus pulses of varying duration and pheromone chemistry, the pheromone
concentration (Murlis et al., 1992). The delivery system and the insect species.
intensity at which pheromone molecules are Permeation of agricultural habitats with
detected by the antennae determines the synthetic pheromones presumably exposes
rate of action potentials generated. This the target pest moths within those localities
information is passed to higher processing to unnaturally high and/or constant doses of
centres in the brain that control the rate of pheromone. Given this presumption, many
casting and counterturning behaviour, flight investigations have examined the effects of
speed and orientation up the pheromone short and prolonged exposures of moths to
plume by the moth (Baker et al., 1985). This their species-specific synthetic pheromones
plume-following behaviour brings males and geometric isomers (Bartell and Roelofs,
within close proximity of the calling female. 1973; Bartell and Lawrence, 1976a,b; Linn
At this point, the high pheromone concen- and Roelofs, 1981; Sanders, 1985). Bartell and
tration, along with visual cues, arrests Lawrence (1976a,b) differentiated between
flight. The male and female may then two possible effects of prolonged pheromone
undergo courtship behaviours (Baker and exposure: they called the effect operating at
Cardé, 1979) and then mate. The disruption the peripheral level ‘adaptation’ and the
of any or the entire above-described plume effect operating at the level of the CNS
following and courtship behaviours is ‘habituation’. Many experiments directed at
referred to as mating disruption or establishing whether adaptation or habitua-
pheromone confusion. tion validly explains mating disruption have
not adequately differentiated between these
two mechanisms, effectively lumping
Mechanisms for disruption
peripheral and central effects together
The most popular explanatory models for (Rumbo and Vickers, 1997; Sanders, 1997).
disruption of pheromone-based communica- Numerous basic investigations have
tion are: (i) sensory adaptation at the periph- shown that exposing male moths to their
eral level affecting olfactory receptors; (ii) pheromone decreases subsequent stereo-
habituation affecting processing of and nor- typed behavioural responses, such as wing
mal responsiveness to olfactory information fanning and rapid walking. In addition, pre-
reaching the central nervous system (CNS); exposed male moths were less successful in
(iii) camouflage of female-produced plumes; orienting towards pheromone point sources,
and (iv) false-trail-following of synthetic as measured by mark–release–recapture and
pheromone plumes by male moths wind-tunnel studies (Rumbo and Vickers,
(Rothschild, 1981; Bartell, 1982; Cardé, 1990). 1997; Daly and Figueredo, 2000). Such studies
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 89

Behaviour–modifying Chemicals 89

provide evidence that either habituation in Recent studies with vertebrate olfactory
the CNS or adaptation of the peripheral sen- receptor neurones distinguish three different
sory apparatus had affected subsequent male forms of adaptation based on their different
behaviours. At least one study (Kuenen and onset and recovery time courses and their
Baker, 1981) demonstrated that pheromone pharmacological properties (Zufall and
exposure of male T. ni disrupted normal ori- Leinders-Zufall, 2000). The two short-lived
entation responses of males with no corre- variants have onset times on the order of
sponding effect on the olfactory receptor 100 ms and 4 s and corresponding recovery
neurones as measured by EAGs. These times of 10 s and 1.5 min, respectively. The
results implicate habituation of the CNS as third type of adaptation is characterized as
opposed to adaptation of the peripheral ‘long-lasting’; onset occurs after an exposure
receptors on the antennae as the cause of the of 25 s and subsequent recovery takes place
subsequent aberrant male behaviours. after 6 min. In addition, research has shown
Furthermore, a later study demonstrated that that these three types of adaptation are
male C. molesta exhibited days-long habitua- mediated by separate molecular mechanisms
tion after exposure to their pheromone (Zufall and Leinders-Zufall, 2000).
(Figueredo and Baker, 1992). Similarly, wind- There is also evidence for a distinction
tunnel and field experiments on Heliothis between long-lasting and short-lived variants
virescens (Fabricius) implicated CNS habitua- of peripheral adaptation in insects. Kuenen
tion lasting up to 96 h as the major mecha- and Baker (1981) documented a short-lived
nism for decreasing male moth response to form of pheromonal adaptation in T. ni, using
female pheromone and as the underlying EAGs. In this case full receptor-cell recovery
means for pheromone-based mating disrup- occurred within 1 min of exposure. In con-
tion of this species (Daly and Figueredo, trast, Schmitz et al. (1997) recorded a longer-
2000). lasting antennal adaptation in Lobesia botrana
Bartell and Lawrence (1976b) suggested Denis and Schiffermüller, using EAGs, and
that male moth exposures to pulsed observed that receptor recovery took place
pheromonal stimuli would more effectively after 5 min. Stelinski et al. (2003a) have
reduce normal sexual responses compared recently documented a ‘long-lasting’ form of
with constant stimulation, because peri- peripheral adaptation in Choristoneura
pheral adaptation would be circumvented, rosaceana (Harris), along with no such corre-
allowing for greater central habituation. sponding adaptation in Argyrotaenia veluti-
Kuenen and Baker (1981) obtained data sup- nana (Walker). Exposure to high doses of
porting this hypothesis for T. ni by showing pheromone for 60 min reduced sensory
that pulsed rather than constant pre-expo- responsiveness of C. rosaceana by up to 60%,
sure resulted in greater disorientation of sub- while identical exposure of A. velutinana
sequent sexual responses. Also, they yielded no long-lasting peripheral sensory
demonstrated decreased EAG amplitudes adaptation (Fig. 5.2). Neither species adapted
with concurrent exposure, indicating that after only 5 min of exposure to pheromone.
receptor adaptation was occurring. The EAG responses of C. rosaceana were low-
Therefore, this study implicated receptor ered by 55–58% following exposure to
adaptation in the antennae as an impediment pheromone for 15 min and made a linear
for CNS habituation. In other words, a recovery to 70–100% of the pre-exposure
pheromone-exposed antenna becomes response within 12.5 min at a rate of
adapted and thus fires fewer action poten- 3–4%/min (Stelinski et al., 2003a). By per-
tials in response to later pheromonal stimu- forming recordings from single antennal neu-
lation. In this sense, an adapted antenna can rones, Baker et al. (1989) showed that male
be considered as a filtering mechanism of the Agrotis segetum (Denis and Schiffermüller)
sensory information that would otherwise olfactory receptor neurones adapted when
flood the CNS, perhaps preventing habitua- they were exposed to high pheromone con-
tion and the associated reduction of normal centrations known to cause in-flight arrest-
sexual behavioural responses. ment of progress toward the source. Using
 90

5 7

6
4
5
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 90

3
4

2 3

EAG response (mV)

EAG response (mV)

L.J. Gut et al.

1
2mg 1 2mg
200µg 200µg
0 0
Before 2µg Before 2µg
exposure 1 min after Cartridge exposure 1 min after Cartridge
exposure 60 min after Blank exposure 60 min after Blank
exposure 1 min after 60 min after dosage exposure 1 min after 60 min after dosage
sham sham
sham exposure sham
exposure exposure exposure

Time of measurement Time of measurement

Fig. 5.2. Peripheral response of Choristoneura rosaceana (left) and Argyrotaenia velutinana (right) to the main component of their pheromonal blend and traces of its
geometric isomer (Z11–14Ac and E11–14Ac, respectively) as measured by EAGs following 60 min exposure to high pheromone concentrations (adapted from
Stelinski et al., 2003a).
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Behaviour–modifying Chemicals 91

the same technique, they also showed that air and adsorption on to solid surfaces.
antennal neurones from H. virescens failed to Collectively, differences in these physico-
adapt regardless of concentration. Baker et al. chemical properties can translate into highly
(1989), proposed that, given the low emission disparate residence times of semiochemicals
rate of (Z)-11–16:Ald from the rubber septa in the environment and the need for tailoring
employed in their study, it was unlikely that application technologies to suit the particu-
H. virescens neurones were challenged to the lar molecular specimen being used to manip-
same degree as those of A. segetum had been ulate a pest insect.
by the more volatile pheromone of that
species. Alternatively, we suggest that A. sege-
Vapour pressures
tum and H. virescens may differ in their sus-
ceptibility to peripheral sensory adaptation, The pressure attained at equilibrium by the
as was observed with C. rosaceana and A. volume of pure vapour that builds up over a
velutinana. Given these data and the fact that pure liquid or solid in a closed vessel is
chemical signalling pathways are conserved known as vapour pressure (VP). This prop-
among insects and vertebrates (Fein, 1986), it erty is expressed in pressure units, e.g.
is possible that different molecular mecha- mmHg. VP is an equilibrial measure – the
nisms and signal-transduction pathways may net value of the propensities of molecules to
be involved in different forms of insect odour evaporate, as well as to condense.
adaptation; these mechanisms may differ Compounds with high VPs evaporate
across insect taxa. rapidly, while those with low VPs evaporate
slowly. Moreover, VP varies exponentially
with molecular weight. Therefore, plots of
Chemical characteristics of the pheromone molecular weights of compounds in a partic-
ular class (e.g. alcohols) against log10 of VP
Moth sex-attractant pheromones are com- yield straight lines (Fig. 5.3).
prised of blends of straight-chain hydrocar- Several notable conclusions arise from
bons, alcohols, aldehydes and acetates, Fig. 5.3. First, VPs vary dramatically with
varying in chain length from c. C10 to C20 molecular weight. Small organic molecules
and in number and isomeric configuration of with low polarity, e.g. methyl acetate
internal double bonds (Tamaki, 1979; (C3H6O2, MW = 74) or hexane (C6H14, MW =
O’Connell, 1981; Chapman, 1998). All are 86) have VPs higher than 100 mmHg. In con-
lipids – soluble in organic solvents rather trast, only modestly larger molecules of simi-
than water. In pure form, most are oils at lar polarity, e.g. pentyl acetate (C7H14O2,
room temperature. Moreover, it is correctly MW = 130) or decane (C10H22, MW = 142)
understood that these agents of long- have dramatically lower VPs, < 10 mmHg.
distance sexual communication operate as Back-calculations from the regression equa-
volatiles. As such, sex pheromones are invisi- tions given in Fig. 5.3 reveal a consistent
ble when they travel through air; yet their threefold decrease in VP for each additional
powerful effects on moth behaviours provide –CH2– unit added to any compound in a
convincing evidence that atmospheric trans- given molecular series. Secondly, adding a
fer of information is occurring. particular functional group to a straight-
Given their many similarities in the visi- chain hydrocarbon base may strongly influ-
ble liquid state, it is understandable that per- ence VP while adding another may not. For
sons working with pheromones can get example, adding an –OH moiety to the cor-
lulled into envisioning that the behaviours of responding hydrocarbon decreases VP by
all these chemicals in the environment are nearly 100-fold, as derived from the differ-
similar. However, as the next sections will ence in y intercepts of the regression equa-
document, such a conclusion is a risky over- tions (Fig. 5.3). Only c. 4% of this change can
generalization. Differences in molecular be explained by increasing the molecular
weight and functional group can profoundly weight by 16 (one oxygen atom), leaving
influence rates of evaporation, dispersion in some 96% of the effect attributable to altered
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92 L.J. Gut et al.

chemical characteristics – most probably pounds like those in Fig. 5.3. However, some
increased polarity due to the prevalent predictions can be deduced from an under-
hydrogen bonding of alcohols (Morrison and standing of physicochemical properties as to
Boyd, 1974). An even greater effect would be how VP measures would translate into open
expected from organic acids. In contrast, evaporation measures. At ordinary field tem-
nearly all of the effect of adding an acetate peratures, small compounds (MW < 100)
moiety to a hydrocarbon base is explained have a much higher propensity to evaporate
by increasing molecular weight, as evi- than to condense (see following section). The
denced by acetate data adherence to the converse is true for large compounds (MW >
hydrocarbon line (Fig. 5.3) when regressed 200) at similar temperatures; condensation is
against molecular weight. VP data for alde- much more favoured than evaporation. It
hydes fall between the lines for alcohols and follows that removing condensation effects
acetates (Fig. 5.3), consistent with their from equilibrial VP measures will raise the
known intermediate polarity. rate of evaporation for large compounds pro-
The evaporation rate of pheromones mea- portionately more than for small com-
sured in flowing open air at field-relevant pounds. Thus, in a plot with the log of the
temperatures is probably a parameter of evaporation rate in open air on the y axis
greater direct relevance to applied chemical against molecular weight on the x axis, the
ecologists than is VP. Under these condi- slope of the resultant line would be expected
tions, evaporation apart from condensation to be smaller than the threefold reduction for
would be the main effect measured. VP values seen with the addition of each
Unfortunately, such data are not readily –CH2– (Fig. 5.3). In other words, the effect of
available even for standard reference com- molecular weight would be less severe on

4
methyl acetate = hydrocarbons
1:Ac pentyl acetate = acetates
2 (100) 5:Ac = aldehydes
Log vapour pressure (mm Hg)

peach-twig
(10) borer = alcohols
0 (1) ethanol 10:Ac
2:OH OFM
(0.1) 12:Ac leaf-roller
moths
–2 (0.01) hexanol 14:Ac
6:OH peach-tree
borers
–4 10:OH 18:Ac
codlemone
12:OH
–6
bombykol
16:OH tomato
–8 hornworm
16:Ald
–10
20 40 60 80 20 40 60 80 20 40 60 80 20 40 60 80
0 100 200 300 400
Molecular weight

Fig. 5.3. Vapour pressures for straight-chain hydrocarbons, acetates, aldehydes and alcohols at 25ºC
as a function of molecular weight. Data points were obtained from manufacturers’ MSDS sheets via
website (http://hazard.com/msds/gn). Estimates of vapour pressures for the selection of moth sex
pheromones shown by arrows were extrapolated using the dashed lines. For the solid lines, regression
equations were: (alcohols) log VP  0.034  MW  3.31; R2  0.99. Not being statistically
distinguishable, data for the hydrocarbons and acetates were combined: log VP  0.030  MW 
4.50; R2 = 0.96.
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Behaviour–modifying Chemicals 93

evaporation rate in free moving air than it is evaporation than for equilibrial VP. For
for equilibrial VP. example, the difference in evaporation rates
Although not originally done for this for 12:Ac vs. 18:Ac was less than two orders
purpose, we have produced some data on of magnitude, rather than the nearly three
the relative rates of evaporation of orders of magnitude predicted for VP. The
pheromonal compounds in open moving air 2.4-fold decrease in evaporation rate for
as a function of molecular weight. In one sit- each additional carbon compares well to the
uation, the rates of evaporation of several 2.7-fold decrease in evaporation rate per
milligrams of the pheromones of Oriental additional carbon recorded by McDonough
fruit moth (12:Ac) and peach-tree borer et al. (1989) for acetates evaporating from
(18:Ac) loaded on to filter-paper discs were rubber septa. Clearly, molecular weight still
compared in a wind tunnel operating at c. has a dramatic effect on pheromone
30°C and a wind speed of 2 m/s. In another longevity in the open air and explains the
situation, an ethanolic solution of long-chain relationship across data points of Fig. 5.4
primary alcohols was sprayed on to apple quite well. Half of the 12:Ac and 14:OH
trees under typical Michigan midsummer samples disappeared in less than 7 and 3 h,
field conditions and the disappearance of respectively. Over half of the 12:OH sample
the compounds from leaves was measured had evaporated in the first hour after appli-
over days by gas–liquid chromatography cation. Thus, the longevity at the site of
(GLC). release of pheromonal compounds smaller
The resultant data are co-plotted in Fig. than this is fleeting under summertime field
5.4 as time for disappearance of half the conditions.
sample of applied compound against mol- On the other hand, the longevity of the
ecular weight. Although these data should larger moth sex pheromones was appreci-
be considered preliminary, the outcome able. It took 10 days for half of the sample of
supports the above prediction of a less 18:Ac to evaporate at c. 30°C. Corresponding
severe molecular weight effect for free values for C18 and C16 alcohols were 4 days

30

10
Time for half-disappearance

18:Ac
18:OH
3
(days)

1 16:OH

0.3
12:Ac
14:OH
0.1

12:OH
0.03
20 40 60 80 20 40 60 80 20 40 60 80 20 40 60 80
0 100 200 300 400
Molecular weight

Fig. 5.4. Relative evaporation rates of differently sized straight-chain alcohols or acetates in moving air or
under Michigan summertime conditions. Comparisons within a compound type (same functional group) are
reliable; comparisons across compound types should be considered preliminary, as test conditions were not
identical.
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94 L.J. Gut et al.

and 1 day, respectively, measures thought molecule and that surface. If the forces of
(by interpolation using Fig. 5.4) likely to cohesion to various sites along the molecule
correspond to those for C16 and C14 collectively exceed some energetic threshold,
acetates. the molecule becomes ‘adsorbed’ and begins
These large differences in VP and evapo- to skid about on the surface of the solid in
ration rates across the spectrum of moth sex- two- rather than three-dimensional space, as
pheromonal chemicals argues that the was the case in air. The temperature of
challenges in formulating them for use in this surface establishes the probability that
pest control will likewise vary widely. For this ‘captured’ molecule will, by chance, at
example, formulating pheromone to success- some point in time, receive a sufficient ener-
fully meter it out for 1 month above a dis- getic boost to tear it from this surface and
ruption threshold should be much easier for again thrust it into the vapour state (re-
peach-tree borers than for codling moth. For evaporation). The process of molecules
peach-tree borer pheromone, the release pro- travelling through space, sometimes in the
file (rate over time) without additives natu- vapour state while at other times adsorbed
rally lies much closer to the desired on to or permeating into surfaces, is known
straight-line profile (representing constant as ‘partitioning’. Significant partitioning
release) than is true for the pheromone of occurs for all moth sex-pheromone mol-
codling moth or peach-twig borer, whose ecules at normal field temperatures, pro-
release profiles are naturally severely con- vided the pheromone molecules are released
cave. Whether or not the underlying reasons into an environment in which contacts with
were understood, this pattern of achieving solid surfaces are probable.
greater success in formulating large vs. small We used the technique of gas–solid chro-
pheromones is widely experienced by those matography to quantify the degree to
manufacturing and testing pheromone for- which moth sex pheromones of various
mulations used as lures for traps and espe- molecular weights and functional groups
cially as devices for mating disruption. partition between air and various types of
solid surfaces at 25oC. Standard gas chro-
matography (GC) measures and equations
Adsorption of pheromones on surfaces –
were used to generate partitioning coeffi-
condensation and partitioning
cients (Cps), which express the ratio of the
Another common misconception concerning compound on a solid surface over that in
the behaviour of volatile chemicals is that, the adjacent gaseous phase. For example, a
once they do evaporate, it is difficult for Cp of 1.0 means there was one pheromone
them to be retrieved from the vapour state – molecule on the solid for every molecule in
i.e. achieve condensation. However, conden- the gas immediately over that solid. A Cp of
sation is another physicochemical property 10 indicates ten times more pheromone
that is highly influenced by the molecular molecules on the surface than in the vapour
weight and the functional group of given immediately over it, etc. Perhaps a more
molecules (Miller, 2004). It turns out that it is intuitive way to view this phenomenon is
remarkably easy for pheromonal compounds that Cp values equate to compound ‘sticki-
larger than molecular weight 200 to adsorb ness’; the higher the Cp value, the more
on to solid surfaces at ordinary environmen- sticky is the compound when contacting a
tal temperatures. The requirements are sim- solid.
ply: (i) a short time (probably only seconds Figure 5.5 reveals the Cp values for vari-
or less) to pass after evaporation and during ous straight-chain pheromonal compounds
which large molecules in the vapour state travelling through a 2 m long × 2 mm inside
distribute some of their atypically high diameter (i.d.) glass tube at 25°C with a
energy in collisions with the small gaseous nitrogen flow rate of 20 ml/min.
molecules comprising air; and (ii) collision Hydrocarbons were the least sticky.
with a surface sufficiently large to allow Nevertheless, even hydrocarbons with car-
multiple sites of contact between pheromone bon numbers of 13, 14 and 15 partitioned
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 95

Behaviour–modifying Chemicals 95

5
= hydrocarbons peach-tree borer (18:Ac)
= acetates
4 = epoxide gypsy moth (19:epx)
o = aldehyde leaf-rollers (14:Ac)
= alcohols
Log partitioning coefficient

(1000) (14:OH)
3 (12:Ald)
(stickiness)

codling-moth (12:OH)
2 (100)
o
(20:HC)
1 (10)
(12:Ac) Oriental fruit moth;
grape-berry moth
0 (1.0)
(10:Ac) peach-twig borer

–1 (0.1)
(10:HC)

–2
0 50 100 150 200 250 300 350

Molecular weight

Fig. 5.5. Partitioning coefficients of straight-chain hydrocarbons and selected pheromonal compounds
when moving through a narrow-bore glass tube as influenced by functional group. All data points were
measured by Miller (2004); those indicated only by an arrow are extrapolated estimates.

sufficiently to be completely resolved from pheromone molecules vary immensely, as

one another while traversing this column; visually illustrated in Fig. 5.6. For example,
they emerged in 5, 9 and 16 min, respec- the Cp of 18:Ac is 100 times larger than that
tively. As was true for VP, stickiness of 12:Ac. If the font size for the 18:Ac were
increased by a consistent threefold for every adjusted to fit on the page of Fig. 5.6, the
additional –CH2– added to the hydrocarbons printing for 12:Ac would be illegible.
as well as their oxygenated derivatives. The Hopefully, such contrasts drive home the
preference of the C20 hydrocarbon was conclusion that pheromones can differ
nearly 300-fold higher for the glass surface greatly in their physicochemical behaviour
than for the gas immediately over it. when chain lengths vary by seemingly just a
Moreover, hydrocarbon stickiness was stable few carbons.
and independent of the tube composition – Compared with the glass tube, Cps for the
glass, silylanized glass, stainless steel or oxygenated pheromonal compounds were
Teflon. This argues that the condensation even higher for a stainless-steel tube but
effect is driven mainly by molecular energet- lower for a Teflon tube. It is well established
ics and is not explained only by specialized that the lipid pheromones under considera-
binding sites on the solid surface. tion are strongly retained, even at elevated
Oxygenation of the hydrocarbons further temperatures, when moving through GC
increased Cp as compared with just raising columns with a thin film of wax used as the
the molecular weight. Adding ester, epoxide, stationary phase. Thus, surfaces at normal
aldehyde and hydroxy oxygens increased Cp environmental temperatures, such as plant
by 1.5-, 1.5-, 10-, and 30-fold, respectively, leaves and insect cuticle, which are coated
over the corresponding hydrocarbon for the with waxes, would be expected to have a
glass-tube system (Fig. 5.5). Relative to one strong affinity for pheromonal compounds,
another, the Cps for various familiar leading to strong adsorption and high Cps.
 96
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 96

L.J. Gut et al.

Fig. 5.6. Relative magnitude of partitioning coefficients of representative moth sex pheromone molecules as depicted by font size. Data derived from Fig. 5.5.
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 97

Behaviour–modifying Chemicals 97

Possible consequences of pheromone stickiness to the stationary phase.

partitioning effects in the field and Pheromone build-up over time will be
evidence from the literature inversely correlated with wind velocity and
temperature. Hopefully, an understanding of
Based on the above data, the fates of
these fundamental chemical principles and
pheromones deployed in crops to achieve
the reference data provided above will assist
mating disruption can be expected to vary as
pest managers in making implementation
a function of compound molecular weight
decisions for pheromone disruption in the
and functional group. As covered in a previ-
face of limited data on the expected behav-
ous section, pheromone evaporation rates
iours of the particular pheromone compo-
from dispensers vary widely with molecular
nents in the field.
weight. After the given molecules have evap-
Evidence that pheromone partitions on to
orated, the degree to which they partition on
foliage under field conditions is documented
to foliage as they are dispersed by wind
in the literature. However, the range of
again depends on the molecular properties
chemical structures for which it is character-
under discussion, as well as such factors as:
ized is, as yet, severely limited. The early
temperature, wind velocity and foliage den-
evidence of this partitioning phenomenon by
sity. Substantial pheromone ‘haloes’ could
moth sex pheromones arose from observa-
build up around a dispenser of a large
tions that foliage near calling female moths
pheromone, such as the doubly unsaturated
or pheromone-baited traps continued to be
18:Ac of peach-tree borers.
attractive after the calling female had
This effect will be especially large if
departed or the trap was removed (Wall et
foliage is dense, wind velocities are low, tem- al., 1981; Wall and Perry, 1983; Noldus et al.,
peratures are not excessive and compounds 1991). Upon development of the field EAG
do not quickly degrade chemically. Relative measurement technique, Karg et al. (1990),
to 18:Ac, dispensers of smaller pheromones, working with the European grapevine moth
such as codlemone ((E),(E)-8,10-12:OH), and its doubly unsaturated 12:Ac
under the same conducive environmental pheromone, demonstrated that pheromone
conditions are much less likely to build up concentration in the air of disruption plots
sizeable haloes, because of much reduced and the structure of the pheromone cloud in
stickiness once evaporated and greatly treated vineyards were highly dependent on
increased evaporation rates after incidents of the density of vegetation in the target area.
adsorption. An additional factor hindering Dense foliage was found to be conducive to
codlemone build-up in the crop is the insta- pheromone build-up. Two possible reasons
bility of its conjugated diene system, which were given for this effect. First, dense foliage
is susceptible to oxidation and polymeriza- reduces wind velocity, thus reducing dilu-
tion when exposed to sunlight and oxygen tion of the pheromone emanating at a
(Millar, 1995). roughly constant rate from the hand-applied
The picture we wish to paint here for polyethylene dispensers used in these tests.
pheromone-based disruption is that the Secondly, Karg et al. (1990) concluded that
movement of pheromones through crop pheromone was adsorbing on to the grape
foliage can be viewed as occurring roughly leaves and being re-released over time.
by a process of inefficient chromatography, Proposed positive effects for disruption were
where the wind is the mobile phase, the the wider and more homogeneous dispersal
foliage is the column packing, the waxes on of pheromone throughout the crop.
the leaves are the stationary phase and Working with colleagues in New Zealand,
pheromone is constantly being injected into Karg et al. (1994) found that leaves placed
the system. In such a system, pheromone downwind of a rope releasing (E)-11-14:Ac
build-up over time will be positively corre- became maximally loaded with the
lated with the density of the packing, the pheromone of the light-brown apple moth in
molecular weight of the pheromone and its just 3 min, as measured by EAG. Such leaves
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 98

98 L.J. Gut et al.

were then shown to release EAG-detectable remains an open question. Of course, the
levels of pheromone for at least 24 h. plume of pheromone vapour coming directly
Moreover, leaves having ample opportunity from the dispenser is thought to play a key
to adsorb pheromone were slightly but sig- role in the success of mating disruption, con-
nificantly attractive to male moths for more sistent with conventional interpretations
than 24 h when used as lures in traps. (Cardé and Minks, 1995; Sanders, 1997). The
Indeed, a halo of pheromone was found build-up of haloes around dispensers would
around rope dispensers that had aged in the definitely enlarge plumes and increase cov-
field for some days. However, for this 14:Ac, erage by pheromones. It would probably
its radius was measurable only within about also expand the area within the crop where
15 cm of the source. resting moths are exposed to adsorbed
This team (Suckling et al., 1996) went on pheromone, as suggested by Karg et al.
to find that shut-down of trap catches con- (1994) and Karg and Sauer (1997). The possi-
tinued for a day or two after pheromone ble long-lasting effects of such prolonged
dispensers were removed from disruption exposure deserve increased attention.
plots. This disruption ‘ghost effect’ was
rightly attributed to the build-up of a so-
called ‘buffer’ of pheromone thought to
have travelled away from the dispensers Influence of the physical environment
and yet remaining in the crop in concentra-
tions that remained disruptive. This sev- It is well understood that environmental fac-
eral-day ‘ghost effect’ for the C-14 acetates tors have a major impact on the field stability
of Epiphyas postvittana (Walker) corre- and longevity of mating-disruption formula-
sponds well with our estimate from Fig. 5.4 tions (Weatherston, 1990). Exposure to ultravi-
of approximately a 1-day interval for the olet (UV) radiation and heat can degrade
half-disappearance of a 14:Ac. pheromones through oxidative decomposi-
Important questions remain to be tion, isomerization of double bonds and other
answered with respect to these partitioning chemical processes. Mating disruption may
effects. Field studies should be extended to be easier to accomplish in a full-canopied
larger pheromones, which would probably crop because the pheromone is less exposed
produce larger haloes, as predicted by the to UV. Temperature also has a major influence
data in Fig. 5.5. Attention should also be on the rate of pheromone emission. High tem-
directed towards whether the pheromone peratures increase the pheromone release rate.
adsorbed on or absorbed into leaves remains This may be beneficial in the short term, but
there or is metabolized. The unexplained ultimately it may result in reduced longevity
rapid disappearance of 14:Ac topically of a disruptant. Thus, disruption formulations
applied to apple leaves (Suckling et al., 1996) may require a higher pheromone-loading rate
provides some contradictory evidence to the in hot, compared with cool production
simple notion that foliage would be an inert regions. It is also possible that cool tempera-
buffer for pheromone. This outcome is consis- tures during critical periods can reduce
tent with the unpublished preliminary obser- pheromone emission rates below the levels
vation by J.R. Miller that more than 60% of needed for disruption (Howell, 1992). Rainfall
the 30 µg of 14C-labelled (Z)-11–14:Ac released can adversely affect sprayable formulations
into a closed vessel was taken up by apple by washing off a portion of the capsules or
leaves and was no longer extractable from the beads (Waldstein and Gut, 2003b).
leaf surface after several days. Nevertheless, The distribution of pheromone is influ-
multiple lines of evidence now support the enced by several physical factors, including
reality and potential importance of this parti- wind, field or orchard topography and shape
tioning phenomenon within crops. and canopy structure (Karg et al., 1990;
The degree to which pheromone Färbert et al., 1997). The best opportunity for
adsorbed some distance from a dispenser disruption is where physical conditions allow
contributes to disruption of communication for the uniform distribution of pheromone.
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Behaviour–modifying Chemicals 99

Thus, sites that are relatively calm and flat are Mainly for economical reasons, the highest
better candidates for mating disruption than recommended deployment rates are usually in
sites that experience frequent high winds or the range of 500–1000 dispensers per hectare.
have steep slopes (Gut and Brunner, 1996). In Two kinds of formulations have been
addition, orchards with large numbers of developed that allow the pheromone to be
missing trees or uneven canopies are consid- sprayed on the crop either by ground or by
ered poor candidates for mating disruption. air. Pheromone can be formulated into plastic
flakes or chopped fibres designed to release
pheromone at about the same rate as a calling
virgin female (Brooks, 1980; Swenson and
Operational factors that determine the level Weatherston, 1989). Female-equivalent formu-
of success lations are sprayed on to a crop using custom-
designed equipment, often with a sticker
In practice, the success of mating disruption added so that the particles will adhere to
depends on the cost-effective delivery of an foliage. A similar approach is to disperse
appropriate blend, amount and spatial dis- pheromone in microcapsules or beads
tribution of pheromone for an extended (Balken, 1980; Hall et al., 1982). The individual
period of time. Suckling and Karg (2000) particles in these formulations are small
identified several operational factors that enough to be applied through conventional
affect pheromone delivery and thus the effi- spray equipment, but as a consequence,
cacy of mating disruption. Of crucial impor- pheromone is released at very low rates,
below those of individual calling females
tance is the type of formulation. To a great
(Sanders, 1997). Doane (1999) has recently
extent, the choice of formulation defines the
provided a good overview of the current sta-
other operational factors. Delivery systems
tus of microencapsulated pheromone formu-
vary in the rate and consistency of
lations. This technology has proved to be
pheromone release. They also differ in their
efficacious against several pests, especially the
ability to limit the impacts of temperature pink bollworm and tomato pinworm.
and UV radiation on rates of emission and A recently developed approach to formu-
pheromone stability. The effectiveness of lating and releasing insect sex attractants is
mating disruption further depends on appli- through the use of aerosol-emitting devices,
cation parameters, such as the timing and such as ‘puffers’ (Shorey et al., 1996),
distribution of the pheromone treatment. ‘misters’ (Mafra-Neto and Baker, 1996) or
Ultimately, commercial success hinges on ‘microsprayers’ (Isaacs et al., 1999). Aerosol
providing economically viable mating- emitters are deployed at densities of only
disruption formulations. two to five per hectare, but each unit
releases several milligrams of pheromone at
least every 15–30 min. These super-low den-
Types of formulations sity devices control the release of
pheromone mechanically to provide a con-
At present, pheromone-based mating disrup- stant predetermined release rate and a sta-
tion is largely achieved through the manual ble environment for the large volume of
application of reservoir-type release devices pheromone prior to its release. Aerosol
(Cardé and Minks, 1995; see also Table 5.4). emitters deployed at low densities have
Pheromone is enclosed in plastic or dispersed been tested for the disruption of insect pests
in synthetic polymers and slowly diffuses in field crops (Shorey et al., 1996; Baker et
from these reservoirs over a period of several al., 1997), tree crops (Shorey and Gerber,
months. Pheromone is dispensed at rates of 1996a,b; Shorey et al., 1996), stored products
up to several micrograms per hour, which is at (Mafra-Neto and Baker, 1996) and cranberry
least 100-fold greater than the release rate of bogs (Baker et al., 1997). Success has varied
pheromone from a calling female (Sanders, widely; the consistently best outcomes were
1997). Reservoir dispensers are hand-applied obtained with larger rather than smaller
at a rate of at least 250 sources per hectare. MW pheromones.
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100 L.J. Gut et al.

Application parameters after implementing an area-wide disruption

programme in Australia (Il’ichev et al., 2002).
The success of mating disruption depends on
Large-canopied crops present special chal-
achieving an even distribution of sufficient
lenges for achieving an effective distribution
quantities of pheromone. The most widely
of pheromone. The positioning of hand-
used pheromone formulations, including
applied dispensers within the canopy of tree
polyethylene tubes, laminates and plastic
crops can dramatically affect the efficacy of
membranes or ampullae, are typically
mating disruption. Weisling and Knight
deployed at rates of 250–1000 units per
(1995) demonstrated that significant mating
hectare. The total pheromone load varies by
of codling moth occurred when dispensers
formulation and target species and can range
were placed in the middle, rather than in the
from 20 to 2000 g/ha in season-long disrup-
upper portion of apple-tree canopies; the best
tion programmes. The amount of pheromone
control of codling moth with mating disrup-
delivered per unit area by sprayable formula-
tion has been achieved when dispensers are
tions and aerosol devices has largely been set
placed in the upper third of the tree canopy.
by successes achieved using given numbers
Determining the most effective pattern of
of reservoir dispensers. Microencapsulated
pheromone distribution has been largely
formulations are typically applied at rates of
guided by trial and error, with two primary
20–100 g of pheromone per hectare and aim
deployment strategies being adopted: (i) a
to release pheromone over a period of 3–4
uniform distribution; or (ii) a distribution
weeks. Multiple applications are required to
that provides for higher concentrations along
achieve season-long inhibition of mate loca-
the edge rather than in the plot interior.
tion. Aerosol emitters may be programmed
Hand-application of reservoir dispensers in a
to release over 700 mg of pheromone per day
predetermined pattern distributes the
and may emit this large volume of active
pheromone load uniformly within the
ingredient for over 120 days. At this rate, the
treated area. The recommended application
total pheromone load provided by five units
rate always specifies a minimum number of
per hectare would be over 400 g.
dispensers needed to achieve suppression.
Crop damage in pheromone-treated
The conventional thinking has been that suf-
plantings is often greater on the borders than
ficient numbers of dispensers are needed to
in the interior (Knight, 1995; Gut and
provide enough false trails to compete with
Brunner, 1998). Two processes are thought to
females. Thus, higher application rates are
contribute to the development of border
needed when population pressure is higher.
infestations. Mated females emigrate from
Alternatively, we suggest that enough dis-
adjacent plantings that are not treated with
pensers are needed to ‘charge’ or impregnate
pheromone. In addition, pheromone concen-
the area around the dispenser with suffi-
trations may be lower on the borders than in
ciently high amounts of pheromone. In this
the interior (Ogawa, 1990; Karg and Sauer,
view, applying too few dispensers increases
1995; Sauer and Karg, 1998), thus increasing
the chances of creating areas with inade-
the likelihood of males locating females and
quate pheromone coverage.
mating on the borders. Among the tactics
In principle, sprayable formulations
used to protect borders is the application of
should provide a highly uniform distribu-
extra pheromone near the edge of the plant-
ing or the extension of the pheromone treat- Good choice Best choice Poor choice
ment into adjacent plantings, if possible.
Maximizing the amount of field or orchard
interior relative to edge is the best protection
against border damage (Fig. 5.7). Long, nar-
row plots are especially poor choices for
mating disruption. The best approach for
limiting edge effects is area-wide treatment Area-wide
with pheromone. Hot spots and edge infesta- Fig. 5.7. Selection of appropriate plots for control
tions of Oriental fruit moth were eliminated with pheromones.
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 101

Behaviour–modifying Chemicals 101

tion of pheromone. However, this assumes considerably depending on several factors,

that capsules or fibres readily stick to plant including wind conditions, plant canopy
surfaces. Waldstein and Gut (2003a) found structure and chemical properties, such as rel-
considerable variation in the propensity of ative molecular mass, inherent to the specific
microcapsules to stick to various plant sur- pheromone released. A grid of pheromone-
faces. Apple wood is a better substrate than baited traps has been used to map the appar-
fruit, which is superior to leaves. Sticking ent distribution of pheromone in 0.8 ha apple
agents are often added to sprayable formula- plots treated with an aerosol device, the
tions to improve adhesion. Even with the Microsprayer (Gut and Garcia-Salazar, 2001,
addition of stickers, a high percentage of unpublished data). Examples of the patterns
microcapsules may be lost following as little that were observed for C. pomonella and A.
as 10 cm of rain (Waldstein and Gut, 2003b). velutinana after the Microsprayers had been
Wind is the primary means for dispersing running for 2 days are presented in Fig. 5.8.
pheromone that is emitted from aerosol Patterns of moth captures indicated that
devices. Pheromone distribution is also pheromone coverage was poor or absent in
accomplished secondarily through a process the areas upwind from the unit. Interestingly,
of adsorption on to plant surfaces and subse- a ‘ghost’ plume (sensu Suckling et al., 1996) of
quent release back into the environment pheromone was observed for several days
(Suckling et al., 1996; refer also to our earlier after the units were turned off, supporting the
discussion of chemical characteristics of the role of secondary release of adsorbed
pheromone). Each unit is required to disperse pheromone from foliage as an important
pheromone over an area of at least 0.5 ha. means of maintaining adequate pheromone
Whether this can be achieved is questionable. levels throughout the treated area (Gut and
The rate and extent of dispersion may vary Garcia-Salazar, 2001, unpublished data).

Fig. 5.8. Spatial mapping of moth captures using a grid of 30 pheromone-baited traps in 0.8-ha apple plots.
Numbers are total catches per day in a single trap. Captures of Cydia promonella males in a plot not treated
with pheromone (top left). Captures of Cydia pomonella males in a plot treated with a single aerosol device,
the MSU Microsprayer, (rectangular symbol) emitting the major component of the pheromone of this species,
(E) (E) 8, 10–12 : OH (bottom left). Captures of Argyrotaenia velutinana males in a plot treated with a single
aerosol device, the MSU Microsprayer, emitting the major components of the pheromone of this species,
Z11–14OAc and E11–14OAc in a 96 : 4 ratio (right panel). Arrows indicate the prevailing wind direction.
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 102

102 L.J. Gut et al.

Comparison of delivery systems mating disruption, Epstein et al. (2002) devel-

oped a model for evaluating the economics
Rather than predicting that any particular
of pheromone-based management pro-
formulation of pheromones will out-compete
grammes. The model factored in not only
and displace all others, we envision that each
input costs, but how those inputs affected
may find a niche within pest control.
fruit quality, the quantity of fruit harvested
Microencapsulated pheromones may be the
and the price received for that fruit. An
most convenient and quick to apply, but each
approach known as ranging analysis, in the
application lasts for periods considerably
economic literature, was used. Ranging
shorter than hand- or aerosol-applied mat-
analysis takes into account variation in yield
erials last. This weakness may be circum- and price, with price varying depending on
vented through the application of very low whether fruit was destined for the fresh or
rates of pheromone at frequent intervals. processing market. Direct comparisons of the
Widely spaced devices appear to be particu- economics of mating-disruption-based man-
larly effective for pests that use large agement programmes versus insecticide-
pheromone compounds, which have a high only programmes demonstrated that in
propensity for sticking to foliage upon wind many cases the pheromone programmes
dispersal. Moreover, such devices provide were as inexpensive as or cheaper than the
the option of releasing a mixture of conventional programmes. The use of
pheromones of several pests simultaneously. sprayable pheromone to enhance control of
Hand-applied pheromone formulations offer leaf-rollers was the most economical mating-
the advantages of longevity and a greater disruption program, yielding increased prof-
guarantee of uniform pheromone dispersal its of US$20/acre when the yield was
throughout the crop. However, they are average and 75% of the fruit was of fresh-
more labour-intensive to apply than other market grade. The major impetus for con-
techniques. This is especially true if dis- ducting the economic analysis was to
pensers must be applied in the upper canopy determine whether initial input costs could
of tall trees, which is currently the recom- lead to future profits through decreased
mended application protocol for disruption insecticide use and a larger harvest of high-
of some fruit pests (Gut and Brunner, 1996). quality fruit. The model demonstrated the
In addition, the rate of release is greatly economic benefit of eliminating some insecti-
affected by environmental conditions, partic- cide applications for secondary pests if fewer
ularly temperature. There may be consider- sprays were used to control primary pests.
able variation in emission rate and field Presenting this information to growers was
longevity among formulations or within for- crucial to the recruitment process and
mulations between years or in different enabled the project to expand from 500 to
growing regions (Thomson et al., 1998). 8000 acres over a 3-year period.
Difficulties in measuring the efficacy of
mating-disruption formulations in small
Economic considerations plots has led to an overwhelming reliance on
conducting such trials in large commercial
Many growers are apprehensive about using plantings. The major drawbacks of on-farm
mating-disruption products because the input experiments have been that untreated con-
costs are high compared with most alterna- trols are usually not available and that a high
tives. These include the cost of the product level of replication cannot be accomplished.
and additional expenses to apply reservoir- Furthermore, plots often vary substantially
type dispensers and intensively monitor pest relative to initial pest densities and pesticide
populations, as well as other indirect costs inputs throughout the season. Obtaining
associated with using an approach that only meaningful results from on-farm trials is
controls specifically targeted species. indeed challenging. One approach, however,
In an attempt to address questions con- has provided a very effective means of
cerning the high input costs associated with demonstrating the economic viability of
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Behaviour–modifying Chemicals 103

mating-disruption programmes. The general cluded that not all species would prove to be
experimental design is to overlay a susceptible to this technique. As a caveat to
pheromone treatment on a portion of a large this statement, we would add that not all pest
block that is being treated with insecticides. species susceptible to mating disruption may
As long as the entire block receives the same be equally controlled. For some species, such
sprays, differences in fruit injury can be cred- as peach-tree borer, red-banded leaf-roller
ited to the added benefit of the disruption and Oriental fruit moth, treatment with
treatment. Gut et al. (1999) reported a three- pheromone alone is often sufficient to miti-
to sixfold reduction in leaf-roller damage gate crop damage. Other pests, such as the
when mating disruption was overlaid on an codling moth and certain leaf-rollers, appear
insecticide programme. The growing reliance to be more difficult to control using only mat-
on mating disruption for control of codling ing disruption. Providing a framework that
moth can be attributed, in part, to the discov- identifies certain pest species as more
ery by fruit growers that substantially better amenable to mating disruption than others
levels of control can be achieved by using should improve the likelihood of success. It
pheromones in conjunction with a full- would also minimize the considerable time
season insecticide programme than by rely- and money spent on field trials that from the
ing on insecticides alone. outset are unlikely to be successful – or are
likely to fail. Taking a very practical
approach, we have examined many of the
Towards increased success and adoption successes and failures of mating disruption
and propose that the following set of criteria
The fact that producers rely on the deploy- can be used for rating species from easy to
ment of pheromones for pest control on difficult to control using mating disruption:
150,000 to 200,000 ha worldwide (D.
● Extent to which moth captures in traps
Thomson, unpublished data) justifies contin-
are inhibited.
ued efforts to develop and implement man-
● Number of dispensers necessary per unit
agement programmes based on the use of
area to achieve control.
these behaviour-modifying chemicals. But
● Pheromone dispensed per unit area to
what can be done to accelerate the successful
achieve control.
use of mating disruption and minimize fail-
● Extent to which the outcome is density-
ures? There is general agreement among sci-
dependent.
entists working with this technique that a
better understanding of the mechanisms Complete or nearly complete trap shut-
underlying disruption, coupled with a good down is consistently achieved for some
working knowledge of the biology, behav- species, while for others it occurs rarely, if at
iour and mating system of target pests, is all. The leaf-rollers A. velutinana and C.
needed to improve success. Although we rosaceana are representative of the two
agree, in principle, with the above goal, we extremes. The effectiveness of an aerosol
also believe that practical solutions are delivery system, the MSU Microsprayer, for
needed to facilitate the successful adoption controlling these two species was evaluated
of mating disruption. Despite examples of in replicated trials in orchards in Michigan,
marginal efficacy in field trials and insuffi- USA. Microsprayers were placed in 0.8 ha
cient knowledge of how to improve perfor- apple blocks at densities of five units per
mance, we believe that many new products hectare. Each unit was programmed to
will be introduced into the market-place release a total of 410 mg of a 96 : 4 blend of
over the next decade. (Z)-11–14:OAc : (E)-11–14:OAc per day. Moth
catches in pheromone-baited traps were
recorded weekly for each species in the
Target species selection
Microsprayer-treated plots and in nearby
In reviewing the status of mating disruption plots not treated with pheromone. The
of moth pests, Cardé and Minks (1995) con- pheromone treatment provided a very high
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 104

104 L.J. Gut et al.

level of inhibition of moth captures for A. tion rate of c. 250 dispensers per hectare (one
velutinana, averaging 99.7% across four repli- per tree), with each device releasing c. 0.3 mg
cates (Fig. 5.9, top). In contrast, an average of of pheromone per day, provides levels of
85% inhibition was recorded for C. rosaceana inhibition of moth catches in traps usually in
in the same plots (Fig. 5.9, bottom). Similar excess of 97%. In addition, the level of disori-
reductions in moth catches for these species entation to traps and decrease in larval den-
have been recorded following the deploy- sities appears to be independent of pest
ment of hand-applied devices or microen- pressure (Snow, 1990). Similar levels of dis-
capsulated sprayable formulations releasing orientation to traps and population suppres-
the same quantities and blend of active sion are readily achieved for the Oriental
ingredients. Additional examples of species fruit moth, C. molesta (Rice and Kirsch, 1990;
that are effectively inhibited from orienting Vickers, 1990). In contrast, the oblique-
to pheromone-baited traps through the banded leaf-roller, C. rosaceana, exemplifies a
deployment of a disruptant, include the species that is ‘difficult’ to control using this
tomato pinworm (Jenkins et al., 1990), lesser technique. An application rate of 1000 dis-
peach-tree borer (Snow, 1990) and Oriental pensers per hectare, with each device loaded
fruit moth (Rice and Kirsch, 1990). with 80–160 g of pheromone, provides levels
Determining the amount of pheromone of trap inhibition in the range of 85–92%.
needed to interfere with mate location in the Doubling or tripling the rate of deployment
field has proved difficult. There have been a does not significantly improve the level of
few examples where pheromone concentra- inhibition of moth captures (Lawson et al.,
tions required for disruption in the field have 1996). Also, the level of disorientation to traps
been estimated (Rothschild, 1975; Koch et al., and suppression of the larval population
2002), but these have largely served as broad appears to be highly related to population
guidelines. The resultant limit in our under- density, with commercially acceptable
standing of the required airborne pheromone impacts only observed under low pest pres-
concentration needed to achieve communica- sure (Novak et al., 1978; Reissig et al., 1978;
tion disruption has led to the use of a trial- Roelofs and Novak, 1981; Deland et al., 1994;
and-error approach in determining effective Agnello et al., 1996; Lawson et al., 1996;
application rates. This has typically involved Knight, 1997). The codling moth, C. pomonella,
direct comparisons of various rates in small- is another example of a pest that appears to
and large-plot field trials. Based on this be relatively difficult to control through com-
empirical approach, application rates rang- munication disruption. Deployment of 500
ing from 250 to 1000 dispensers per hectare dispensers per hectare is only sufficient if pest
have been established for polyethylene densities are low. At higher densities, applica-
tubes, ampullae and other hand-applied dis- tion rates up to 1000 devices per hectare and
pensers. The number of devices deployed companion insecticide sprays are needed to
depends on the target species and may also achieve commercially acceptable control.
vary in accordance with anticipated levels of If indeed some species are highly
pest pressure. The pheromone loading rate amenable to disruption and others are not,
in the dispensers is often tuned to the then what are the factors that allow the more
requirements for communication disruption resilient species to operate in environments
of a particular species. Other considerations permeated with synthetic pheromone? We
include the cost of the active ingredient and have documented in a previous section
the length of time a formulation must release (Male response to pheromone) that there are
pheromone. For example, a higher loading fundamental differences in the capacities of
rate is required for season-long disruption of species to become adapted and/or habitu-
multiple-generation pests with extended ated when exposed to high doses of syn-
periods of activity. thetic pheromone. In addition, we know that
The peach-tree borer, Synanthedon exitosa species differ in their dispersal and repro-
(Say), is an example of a species that is ‘easy’ ductive capabilities. Finally, we have pro-
to disrupt using pheromone. A low applica- vided evidence in an earlier section
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Behaviour–modifying Chemicals 105

(Chemical characteristics of the pheromone) an advantage to moth species such as

that pheromones vary considerably with C. rosaceana relative to species such as A.
respect to rates of evaporation, dispersion in velutinana, which do not appear to exhibit a
air and adsorption on to solid surfaces. physiological capacity for a long-lasting form
Collectively, differences in these physico- of adaptation (Stelinski et al., 2003a). For
chemical properties can have profound example, perhaps moths under long-lasting
effects on the longevity and movement of adaptation might sufficiently subdue their
pheromones in the environment. It is these overt sexual responses so as to preclude
basic differences in the properties of moths exhaustion and cause them to depart from
and their pheromones that make some extraordinarily high-concentration pheromone
species highly susceptible to mating disrup- sites where the likelihood of mate-finding is
tion, while others are capable of averting the low. If they then happen to arrive in a loca-
effects of this control technique (Fig. 5.9). tion of low or no pheromone, disadaptation
Certain lepidopteran species appear to be would occur within a short interval (10–15
good ‘adapters’ in that they are physiologi- min) and their ability to discriminate and ori-
cally capable of decreasing their sensitivity to ent to a natural pheromone plume would be
pheromone for an extended period of time restored, provided the possible effects of CNS
following pheromone exposure. We speculate habituation were shielded (Bartell and
that, under pheromone mating-disruption Lawrence, 1976b; Kuenen and Baker, 1981).
regimes, long-lasting adaptation may confer Evenden et al. (2000) subjected male C.
Mean moths per trap per week ± SE

35

30 Pheromone
Control
25

20

15

10

0
Jun Jul Aug Sep
Mean moths per trap per week ± SE

4.5
4.0 Pheromone
3.5 Control
3.0
2.5
2.0
1.5
1.0
0.5
0.0
Jun Jul Aug Sep

Fig. 5.9. Inhibition of Argyrotaenia velutinana (upper) and Choristoneura rosaceana (lower) male catches in
pheromone-baited traps following deployment of a disruption treatment. An aerosol delivery system, the
MSU Microsprayer, was placed in 0.8-ha apple plots at densities of five units per hectare. Each unit was
programmed to release a total of 400 mg of a 96 : 4 blend of the main component of their pheromonal
blend and traces of its geometric isomer (Z-11–14Ac and E11–14Ac). SE, standard error.
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 106

106 L.J. Gut et al.

rosaceana to 1 h of constant pheromone expo- even greater opportunity for target moths to
sure and then tested their behavioural be exposed to extraordinarily high concen-
response to a pheromone source in a wind- trations of pheromone as the pheromone
tunnel 10–30 min after the exposure treat- solution emitted in an aerosol spray falls on
ments. Constant pre-exposure did not alter to foliage and droplets of pure pheromone
the proportion of males orienting upwind to accumulate over time on the source tree.
pheromone plumes in the wind-tunnel. The Moreover, large and highly concentrated
conclusion was that habituation probably plumes are thought to waft great distances
plays a minor role as a mechanism of mating downwind of the source trees. However, it
disruption in this species. Evenden et al. remains to be determined whether moths
(2000) chose to assay their pheromone- exhibit the behavioural capacity for ‘dosing’
exposed C. rosaceana 10–30 min after treat- themselves with enough pheromone in the
ment in order to avoid the effects of antennal field for physiological phenomena such as
adaptation. Our results showed that olfactory long-lasting adaptation to be relevant under
receptor neurones of C. rosaceana disadapt mating disruption.
within 12.5 min after constant pre-exposure Implementing a pheromone-based man-
to pheromone. Therefore, the combined agement programme for a pest that has been
results of our study and that of Evenden et al. identified as easy to disrupt improves the
(2000) suggest that ‘long-lasting’ adaptation chances for success, but it certainly does not
may shield C. rosaceana from CNS habitua- ensure that control will be achieved or that it
tion, explaining why this species could suc- will be economical. The success of mating
cessfully orient to pheromone point sources disruption in the field or orchard depends on
shortly after constant exposure to cost-effective delivery of the active ingredi-
pheromone. Alternatively, both adaptation ent. Achieving this requires addressing the
and habituation might occur, but recovery many factors or conditions, other than the
from both might be rapid. moth and its pheromone, that have an impact
Currently, hand-applied rope dispensers on a mating disruption programme. We pro-
are the dominant method of dispensing pose that, in practice, it is this set of condi-
pheromone for mating disruption of moth tions that determines the level of difficulty in
pests in orchards (Nagata, 1989; Agnello et meeting requirements for successful disrup-
al., 1996; Knight et al., 1998; Knight and tion of a particular pest species (Fig. 5.10).
Turner, 1999). The release rate for ropes mar- Operational requirements for successful mat-
keted for leaf-roller moths averages c. ing disruption broadly include technical con-
11 ng/s (Knight et al., 1998; Knight and siderations, such as pheromone-delivery
Turner, 1999). Moths within the treated crop strategies, crop-management considerations
could perceive the applied pheromone in and characteristics of the site, including
several ways, including: (i) as a ‘cloud’ of initial pest density. Growers, consultants,
pheromone resulting from a coalescence of extension personnel and others with a very
plumes emanating from the many dis- applied viewpoint emphasize the need for
pensers; (ii) as a localized plume downwind disruption formulations that are economical
of a nearly dispenser; or (iii) a moth could relative to other control tactics, easy to use
even be attracted on to a dispenser. In our and compatible with current IPM pro-
field tests, C. rosaceana did exhibit long- grammes. From a technical standpoint, the
lasting adaptation upon exposure to delivery system that is selected must release
pheromone ropes, but only when held the appropriate blend and amount of
within a few centimetres of the dispenser pheromone. It must also provide for an ade-
(Stelinski et al., 2003b). Nevertheless, these quate distribution of the active ingredient
results demonstrate that this phenomenon over an extended period of time.
can occur under field conditions. Use of low- Perhaps the most crucial management
density, high-release dispensers, such as decision is the selection of an appropriate area
puffers (Shorey and Gerber, 1996a,b) or to be treated in terms of size and pest pres-
microsprayers (Isaacs et al., 1999), offers an sure. The likelihood of failure certainly
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 107

Behaviour–modifying Chemicals 107

GPTB
RBLR TPW OFM CM PLR OBLR

Easy Difficult

Ease of disruption

Conditions A Conditions B Conditions C

e.g. low pest density e.g. moderate pest density e.g. high pest density

Low High

Level of difficulty in meeting requirements for successful disruption

Fig. 5.10. Conceptualization of differences in the susceptibility of various species to mating disruption
based on fundamental properties of the moths and their pheromones (upper). Species are red-banded leaf-
roller (RBLR), greater peach-tree borer (GPTB), tomato pinworm (TPW), Oriental fruit moth (OFM), codling
moth (CM), pandemis leaf-roller (PLR) and oblique-banded leaf-roller (OBLR). Conceptualization of
differences in the level of difficulty of disrupting a particular species based on all of the factors other than
the moth and its pheromone, such as physical characteristics of the site or starting pest density (lower).

increases if site selection does not minimize where fairly low doses impede the approach
opportunities for immigration by mated of males to a pheromone source (Cardé et al.,
females. In addition, the best successes for 1975; Baker and Roelofs, 1981). Yet, since
many species will be achieved where pest these early observations, considerable atten-
pressure is not too high. Operational require- tion has been focused on some species that
ments for successful disruption can vary have proved to be difficult candidates for dis-
depending on anticipated pest pressure. For ruption. The apparent driving force for these
example, a relatively low application rate of efforts is the importance of the pest economi-
500 dispensers per acre is sufficient for com- cally. We propose that it may not be necessary
munication disruption and control of codling to carry out detailed sets of experiments to
moth if pest pressure is low. The level of diffi- determine the disruption capacity (high to
culty in meeting the requirements for success- low) among pest species. As a starting-point,
ful disruption in this case is low (Fig. 5.10, the simplest measure may be, as was sug-
conditions A). Control of codling moth can gested over 25 years ago, the dose response of
also be achieved under moderate pest pres- a species for orienting to various loading rates
sure, but a full rate of 1000 dispensers per acre of pheromone lures. Some species, such as the
needs to be applied. Control of this pest is dif- Oriental fruit moth and tomato pinworm, are
ficult to achieve where initial pest pressure is attracted to a narrow range of concentrations.
high, as even high application rates of at least A single hollow fibre attracted significantly
1000 dispensers per hectare cannot prevent more tomato pinworm moths than five or
mating. The difficulty in meeting the require- more fibre lures (Wyman, 1979). For Oriental
ments for disruption of codling moth in these fruit moth, high doses caused arrestment of
cases is moderate and high, respectively (Fig. upwind progress of males as they approached
5.10, conditions B and C). the source (Cardé et al., 1975; Baker and
Traditionally, little attention has been Roelofs, 1981). A similar response was
focused on selecting appropriate targets prior observed for spruce budworm, C. fumiferana,
to the development of a mating-disruption and Oriental fruit moth orienting to high-dose
formulation. As pointed out by Doane (1999), lures in wind tunnels (Sanders and Lucuik,
there were suggestions over 20 years ago that 1996). All of these species, which are maxi-
habituation may be easier to elicit in species mally attracted to low-dose lures, also appear
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 108

108 L.J. Gut et al.

to have a low capacity to avert communica-

Mean no. of moths per trap per week

tion disruption. In contrast, other species that 6
exhibit high levels of attraction to a compara-
tively wider range of pheromone loadings 5
appear to be more difficult to disrupt. 4
Included in this second group is C. rosaceana, 3
which is readily captured in traps baited with
2
a wide range of dosages (Fig. 5.11).
1

Area-wide approach 0
0× 1/10× 1× 10× 30×
The best successes with mating disruption
Relative lure dosage
have been achieved where large, contiguous
areas have been treated with pheromone.
Fig. 5.11. Effect of lure dosage on captures of
Excellent control of Oriental fruit moth was Choristoneura rosaceana in pheromone-baited traps
obtained following implementation of area- (L. Stelinski, 2002, unpublished data).
wide disruption programmes in 1100 ha of
apples and pears in Australia (Il’ichev et al.,
2002) and 1200 ha of mixed stone fruits in the low levels following implementation of an
Tulbagh valley in South Africa (Barnes and area-wide approach (Fig. 5.12). In addition,
Blomefield, 1997). The US Department of direct comparisons with conventional pro-
Agriculture (USDA) sponsored the Codling grammes outside the project area revealed
Moth Area-wide Management Program dramatic reductions in the number of insecti-
(CAMP), adopting an IPM approach that cides applied for codling-moth control in
relied on mating disruption technology and CAMP orchards. Similar levels of success
judicious and timely applications of insecti- have been achieved through government-
cides for management of codling moth in supported projects to control pink bollworm
pome fruit in the western USA (Calkins et al., with pheromones in vast areas of cotton in
2000; Brunner et al., 2001). The number of the south-western USA (Staten et al., 1997)
CAMP sites and their size increased from an and Egypt (Jones and Casagrande, 2000).
initial five sites totalling 1260 ha in 1995 to
over a dozen sites totalling approximately Season-long versus targeted use of
4000 ha by 1999. The results of this project pheromones
were impressive, with pest densities, as mea-
sured by moth captures in pheromone traps Commercial development of disruption
and fruit injury at harvest, declining to very products has largely been geared towards

Mean fruit injury (%) Mean moths per trap per Mean OP applications per
season season

0.8 1994 60 6
0.7 1995 50 5
0.6 1996
1997 40 4
0.5
0.4 30 3
0.3 20 2
0.2
0.1 10 1
0.0 0 0
Area 1 Area 2 Area 1 Area 2 Area 1 Area 2

Fig. 5.12. Summary of results for two locations that were part of the Codling Moth Area-wide Management
Program, USA, during the year prior to using mating disruption (1994) and the first 3 years of area-wide
disruption (adapted from Calkins et al., 2000; Brunner et al., 2001). OP, organophosphorus insecticide.
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 109

Behaviour–modifying Chemicals 109

providing season-long control of a pest pop- vantages to their use in pest management.
ulation. The first application of pheromone is Mating-disruption technologies are non-
typically applied at or prior to the start of toxic to natural enemies. As a result, greater
adult flight for the targeted pest. Additional reliance on these highly selective tactics for
treatments are made if the residual activity pest control will increase the potential for
of the pheromone product does not cover the biological control of secondary pests. On the
entire flight period. Although certain disrup- other hand, the use of pheromone-based
tion products have achieved great success technology and the subsequent reduction in
season-long, there are some critical limita- insecticides for a primary pest frequently
tions to this approach. Season-long control of result in outbreaks of other pests (Ridgway
some multivoltine species may require main- et al., 1990; Thomson et al., 1998). Growers
taining pheromone in the crop for over 180 are keenly aware of the potential risks and
days. This may be economically prohibitive added costs associated with secondary-pest
or technically infeasible. outbreaks.
Targeted use of pheromones is an alterna- The need to control several pest species is
tive approach that could provide new oppor- a major factor limiting the acceptance of dis-
tunities for some mating-disruption ruption technologies in some crop-production
formulations. This strategy entails targeted systems. For example, over a dozen lepi-
use of a disruption formulation to affect a key dopteran species can reach damaging levels
period of adult activity. Sprayable pheromone in eastern apple-production systems (Epstein
formulations offer the greatest opportunity for and Gut, 2000). Included in this mix is a
incorporation into pest-management pro- complex of leaf-rollers that have overlapping
grammes in such a selective manner. We can activity periods and cause similar damage.
envision microcapsules serving as a means for Pfeiffer et al. (1993) tested the viability of
delivering a variety of insect pheromones. mating disruption for a complex of four tort-
Perhaps they could be used in an ‘off-the- ricids using various generic blends. All for-
shelf ’ approach, much like that adopted for mulations proved ineffective for one or more
lures used to attract pests to traps and monitor species, presumably because they were not
their activity. Suppliers of monitoring tools sufficiently similar to the natural blend. It
often rely on a single delivery device, such as may be worth revisiting this approach as
a red septum, as the basis for a large product new technologies are developed. For exam-
line. A key advantage of using pheromones in ple, newly developed polyethylene twin-
a targeted manner is that expensive mating- tube dispensers offer the possibility of
disruption products can be applied on an as- emitting two generic blends, one from each
needed basis. This is in contrast to the tube, while applying only one device for
preventive basis of using pheromones dictated both pheromone blends.
by the season-long approach, with the disrup- A few hand-applied dispensers contain-
tion product typically applied prior to start of ing the attractive blends for two or three
flight and often prior to any knowledge of species with very different pheromone com-
pest density. In this situation, a grower must ponents are either already commercially
make an up-front investment in an expensive available or will soon be on the market. In
and, to some extent, risky technology. large-plot field trials conducted over the past
Microencapsulated formulations have recently 2 years, multispecies formulations for
been registered for suppression of Oriental codling moth and Oriental fruit moth or for
fruit moth. These may be especially useful in these two species and oblique-banded leaf-
crops such as apple, where this pest is gener- roller have performed as well as the single-
ally only a problem late in the season. species products currently in commercial use
(L.J. Gut, 2002, unpublished data). A concern
with multiple-species reservoir-type dis-
Multispecies disruption
pensers is that the pheromones may interact
The extreme specificity of sex pheromones in ways that reduce the efficacy of disruption
means there will be advantages and disad- against one or more target species. For
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 110

110 L.J. Gut et al.

example, Snow (1990) reported that release expensive active ingredients are not wasted,
of only pure (E,Z)-3,13-octadecadenyl acetate contrary to when multispecies hand-applied
(EZA) shut down captures of lesser peach- dispensers are used.
tree borer, while various blends, excluding
pure EZA, significantly reduced captures of
Implementation and demonstration
greater peach-tree borer. Successful disrup-
programmes: a key to success
tion of lesser and greater peach-tree borer
required that the specific blends most attrac- A major determinant of the success of mat-
tive to each species were provided in sepa- ing disruption for pest control is the extent to
rate dispensers deployed on opposite sides which growers will adopt these technologies,
of trees. Other problems that need to be which are generally information-intensive,
addressed include the application timing risky and expensive in comparison with con-
and chemical interactions that affect the ventional remedies. The best means of gain-
longevity of pheromone release. The spring ing acceptance for these sophisticated and
emergence of Oriental fruit moth occurs c. 2 less-certain pest-control methods is to
weeks before that of codling moth and c. 6 demonstrate, on farm, that they are effica-
weeks prior to oblique-banded leaf-roller. A cious and economical. Investment in demon-
multispecies dispenser containing the stration and implementation projects has
pheromones of all three of these pests would been the key to widespread adoption of
have to be applied either prior to or after, the pheromone technologies in most cases where
beginning of flight for at least one species. In it has occurred. The rate of adoption of
addition, blending codlemone and (Z)- codling-moth mating disruption in
11–14:OAc in the same tube accelerates the Washington, USA, as estimated by Brunner
release of codlemone, apparently because the et al. (2001) and J.F. Brunner (unpublished
acetate is a good solvent for the alcohol. data), is illustrated in Fig. 5.13. Isomate-C®
Sprayable formulations are now being was registered in 1991 as the first mating-
tested or used commercially for a number of disruption product for codling-moth control
insect pests. It is possible that future pest- in the USA. On-farm trials were immediately
control programmes in tree-fruit crops may implemented by USDA and Washington
include sprayable products for codling moth, State University researchers and comprised a
oblique-banded and red-banded leaf-rollers, large percentage of the acreage treated with
tufted apple bud-moth and Oriental fruit pheromone in the first year. Parallel 3-year
moth. The advantage of this approach is that studies that followed the transition of apple-
each spray can be timed to coincide with the orchard management with conventional or
start of flight for each pest. This may organic pest-control programmes to a
improve efficacy and be more economical, as pheromone-based management programme

40,000 50%
35,000 40%
Total hectares treated

30,000
25,000
20,000
15,000
10,000
5000
0
1990 1992 1994 1996 1998 2000 2002

Fig. 5.13. Use of codling-moth mating-disruption products in Washington, USA (adapted from Brunner et
al., 2001).
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Behaviour–modifying Chemicals 111

provided the foundation for educating grow- believe this process is central to increased
ers about the risks and benefits of this novel adoption of mating disruption.
technology (Knight, 1995; Gut and Brunner,
1998). The number of growers trying the
technique gradually increased and, in most Concluding Remarks
cases, they achieved satisfactory control.
Where failures did occur they were usually Substantial progress in developing semio-
associated with smaller plot sizes, especially chemical-based pest-management products
where neighbouring orchards served as a that are commercially viable has certainly
source of immigrating mated females. The been made over the past 10 years, with
USDA-sponsored CAMP was initiated in mating-disruption formulations leading the
1995 to address the issue of border effects way. We have no doubt that this trend will
and the need for improved monitoring and, continue over the next decade. Two factors,
in general, to facilitate greater adoption of one practical and the other biological, appear
mating disruption. The apple acreage under to provide the greatest impediment to the
mating disruption in Washington increased adoption of direct controls based on the use
dramatically over a period of 5 years, reach- of behaviour-modifying chemicals. Mass
ing a peak in 2000 at 37,000 ha, or 50% of trapping, attack-and-kill and mating disrup-
state’s total apple acreage. Perhaps the great- tion are expensive techniques compared
est achievement of this project was that the with insecticidal control. It is hoped that the
growers have continued coordinated efforts direct costs of the active ingredients will fall
over large areas since the USDA terminated in the future. Meanwhile, the research com-
their role in the area-wide programme in munity, farmers and others involved in com-
1999. mercial production systems must work
This 10-year transition to the large-scale, together to develop cost-effective ways of
sustained use of mating disruption has been using semiochemicals.
replicated in other production systems and As recognized early on by Knipling (1979)
in other parts of the world. The basic and others, pest density is a very crucial lim-
approach has been to establish a partnership iting factor to pest control using semiochemi-
between government or other public enter- cals. Two approaches that have successfully
prises and producers. These demonstration mitigated the problem of controlling high-
sites serve as the catalyst and educational density populations are area-wide pro-
foundation for new sites in subsequent grammes and the use of companion
years, culminating in a large, coordinated insecticide sprays. In the second approach,
effort between farmers and others involved insecticides are used either to reduce initial
in the production system. To be successful on population densities or as a supplement to
an area-wide scale, the project must engage the semiochemical-based tactic.
the infrastructure that is already in place in Wyatt (1997) proposed that, to make the
making management decisions. Critical par- task of developing mating disruption for
ticipants include, among others, farmers, various pests manageable, we should search
suppliers of control products, consultants for patterns and good predictors of success.
and university extension and research per- We have proposed a set of criteria for pre-
sonnel. A robust implementation programme dicting the success of mating disruption for a
involves educational programmes, including particular species or for the same species
hands-on training, economic analysis, docu- under varying conditions. Now, the chal-
mentation of programme efficacy, regular lenge for us and hopefully also for others is
communication between the participants to explore the usefulness of this scheme.
and, often, some kind of financial incentive. There is a heightened need for both good
To be successful, it must be an evolving monitoring tools and alternatives to pesti-
process that develops and incorporates new cides. As we mentioned at the outset, new
control and monitoring technologies to over- regulations governing the use of pesticides
come problems that are certain to arise. We and the regular occurrence of resistance to
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 112

112 L.J. Gut et al.

chemical controls provide a strong impetus tal impact and increased compatibility with
for the adoption of behavioural controls. In biological and cultural methods of control. It
addition, behavioural controls have the is truly an exciting time to be working with
added advantages of negligible environmen- semiochemicals.

References

Agnello, A.M., Spangler, S.M. and Reissig, W.H. (1990) Development and evaluation of a more efficient
monitoring system for apple maggot (Diptera: Tephritidae). Journal of Economic Entomology 83,
539–546.
Agnello, A.M., Reissig, W.H., Spangler, S.M., Charlton, R.E. and Kain, D.P. (1996) Trap response and fruit
damage by obliquebanded leafroller (Lepidoptera: Torticidae) in pheromone-treated apple orchards
in New York. Enviromental Entomology 25, 268–282.
Akers, R.P. and O’Connell, R.J. (1988) The contribution of olfactory receptor neurones to the perception of
pheromone component ratios in male redbanded leafroller moths. Journal of Comparative Physiology
163, 641–650.
Almaas, T.J. and Mustaparta, H. (1990) Pheromone reception in tobacco moth, Heliothis virescens. Journal
of Chemical Ecology 16, 1331–1347.
Almaas, T.J., Christensen, T.A. and Mustaparta, H. (1991) Antennal receptor neurons encode several fea-
tures of intra- and interspecific odorants in the male corn earworm moth Helicoverpa zea. Journal of
Comparative Physiology 169, 249–258.
Atanassov, A., Shearer, P.W., Hamilton, G. and Polk, D. (2002) Development and implementation of a
reduced risk peach arthropod management program in New Jersey. Journal of Economic Entomology
95, 803–812.
Ayyappathe, R., Poloavarapa, S. and McGuire, M. (2000) Effectiveness of thiomethoxam-coated spheres
against blueberry maggot flies (Diptera: Tephritidae). Journal of Economic Entomology 93, 1473–1479.
Baker, T.C. and Cardé, R.T. (1979) Courtship behavior of the Oriental fruit moth (Grapholitha molesta):
experimental analysis and consideration of the role of sexual selection in the evolution of courtship
pheromones in the Lepidoptera. Annals of the Entomological Society of America 72, 173–188.
Baker, T.C. and Roelofs, W.L. (1981) Initiation and termination of Oriental fruit moth male response to
pheromone concentrations in the field. Environmental Entomology 10, 211–218.
Baker, T.C., Willis, M.A., Haynes, K.F. and Phelan, P.L. (1985) A pulsed cloud of sex pheromone elicits
upwind flight in male moths. Physiological Entomology 10, 257–265.
Baker, T.C., Hansson, B.S., Löfstedt, C. and Löfqvist, J. (1989) Adaptation of male moth antennal neurons
in a pheromone plume is associated with cessation of pheromone-mediated flight. Chemical Senses
14, 439–448.
Baker, T.C., Dittl, T. and Mafra-Neto, A. (1997) Disruption of sex pheromone communication in the black-
headed fireworm in Wisconsin cranberry marshes by using MSTRS devices. Journal of Agricultural
Entomology 14, 449–457.
Bakke, A. and Lie, R. (1989) Mass trapping. In: Jutsum, A.R. and Gordon, R.F.S. (eds) Insect Pheromones in
Plant Protection. Wiley, Chichester, UK, pp. 67–87.
Balken, J.A. (1980) Microencapsulation using coacervation/phase separation techniques. In: Kydonius,
A.E. (ed.) Controlled Release Technologies: Methods and Applications, Vol. II. CRC Press, Boca Raton,
Florida, pp. 83–105.
Barnes, B.N. and Blomefield, T.L. (1997) Goading growers towards mating disruption: the South African
experience with Grapholita molesta and Cydia pomonella (Lepidoptera: Tortricidae). IOBC WPRS
Bulletin 20, 45–56.
Barrett, B.A. (1995) Effect of synthetic pheromone permeation on captures of male codling moth
(Lepidoptera: Tortricidae) in pheromone and virgin female moth-baited traps at different tree
heights in small orchard blocks. Environmental Entomology 24, 1201–1206.
Bartell, R.J. (1982) Mechanisms of communication disruption by pheromone in the control of
Lepidoptera: a review. Physiological Entomology 7, 353–364.
Bartell, R.J. and Lawrence, L.A. (1976a) Reduction in responsiveness of Epiphyyas postvittana
(Lepidoptera) to sex pheromone following pulsed pheromonal exposure. Physiological Entomology 2,
1–6.
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 113

Behaviour–modifying Chemicals 113

Bartell, R.J. and Lawrence, L.A. (1976b) Reduction in responsiveness of male light-brown apple moths,
Epiphyas postvittana, to sex pheromone following pulsed pre-exposure to pheromone components.
Physiological Entomology 2, 89–95.
Bartell, R.J. and Roelofs, W.L. (1973) Inhibition of sexual response in males of the moth Argyrotaenia
velutinana by brief exposures to synthetic pheromone or its geometrical isomer. Journal of Insect
Physiology 19, 655–661.
Beers, E.H., Brunner, J.F., Willet, M.J. and Warner, G.M. (1993) Orchard Pest Management: a Resource for the
Pacific Northwest. Good Fruit Grower, Yakima, Washington, 276 pp.
Borden, J.H. (1990) Use of semiochemicals to manage coniferous tree pests in Western Canada. In:
Ridgway, R.L., Silverstein, R.M. and Inscoe, M.N. (eds) Behavior-modifying Chemicals for Insect
Management. Marcel Dekker, New York, pp. 281–315.
Borden, J.H. (1997) Disruption of semiochemical-mediated aggregation in bark beetles. In: Cardé, R.T.
and Minks, A.K. (eds) Insect Pheromone Research, New Directions. Chapman & Hall, New York,
pp. 421–438.
Bradley, S.I., Walker, J.T.S., Wearing, C.H., Shaw, P.W. and Hodson, A.J. (1998) The use of pheromone
traps for leafroller action thresholds in pipfruit. Proceedings of the New Zealand Plant Protection
Conference 51, 173–178.
Brooks, T.W. (1980) Controlled vapor release from hollow fibers: theory and applications with insect
pheromones. In: Kydonius, A.E. (ed.) Controlled Release Technologies: Methods and Applications, Vol II.
CRC Press, Boca Raton, Florida, pp. 165–193.
Brunner, J., Welter, S., Calkins, C., Hilton, R., Beers, E., Dunley, J., Unruh, T., Knight, A., VanSteenwyk, R.
and Van Buskirk, P. (2001) Mating disruption of codling moth: a perspective from the Western
United States. IOBC WPRS Bulletin 25, 207–215.
Buchelos, C.T. and Levinson, A.R. (1993) Efficacy of multisurface traps and Lasiotraps with and without
pheromone addition, for monitoring and mass-trapping of Lasioderma serricorne F. (Col., Anobiidae)
in insecticide-free tobacco stores. Journal of Applied Entomology 116, 440–448.
Calkins, C.O., Knight, A.L., Richardson, G. and Bloem, K.A. (2000) Area-wide population suppression of
codling moth. In: Tan, K.-H. (ed.) Area-wide Control of Fruit Flies and Other Insect Pests. Peneritg
Universiti Sains Malaysia, Pulau Pinang, pp. 215–219.
Campbell, C.D., Walgenbach, J.F. and Kennedy, G.G. (1992) Comparison of black light and pheromone
traps for monitoring Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) in tomato. Journal of
Agricultural Entomology 9, 17–24.
Cardé, R.T. (1990) Principles of mating disruption. In: Ridgeway, R.L., Silverstein, R.M. and Inscoe, M.N.
(eds) Behavior-modifying Chemicals for Pest Management: Applications of Pheromones and Other
Attractants. Marcel Dekker, New York, pp. 47–71.
Cardé, R.T. and Elkinton, J.S. (1984) Field trapping with attractants: methods and interpretation. In:
Hummel, H.E. and Miller, T.A. (eds) Techniques in Pheromone Research. Springer-Verlag, New York,
pp. 111–129.
Cardé, R.T. and Minks, A.K. (1995) Control of moth pests by mating disruption: successes and con-
straints. Annual Review of Entomology 40, 559–585.
Cardé, R.T. and Minks, A.K. (eds) (1997) Insect Pheromone Research, New Directions. Chapman & Hall, New
York, 684 pp.
Cardé, R.T., Baker, T.C. and Roelofs, W.L. (1975) Ethological function of components of a sex attractant
system for Oriental fruit moth males, Grapholita molesta (Lepidoptera: Tortricidae). Journal of
Chemical Ecology 1, 475–491.
Chapman, R.F. (1998) The Insects: Structure and Function. Cambridge University Press, Cambridge, UK,
770 pp.
Charmillot, P.-J. (1990) Mating disruption technique to control codling moth in western Switzerland. In:
Ridgway, R.L., Silverstein, R.M. and Inscoe, M.N. (eds) Behavior-modifying Chemicals for Insect
Management. Marcel Dekker, New York, pp. 165–182.
Charmillot, P.-J., Hofer, D. and Pasquier, D. (2000) Attract and kill: a new control of the codling moth
Cydia pomonella. Entomologia Experimentalis et Applicata 94, 211–216.
Christensen, T.A., Mustaparta, H. and Hildebrand, J.G. (1989) Discrimination of sex pheromone blends in
the olfactory system of the moth. Chemical Senses 14, 463–477.
Daly, K.C. and Figueredo, A.J. (2000) Habituation of sexual response in male Heliothis moths. Physiological
Entomology 25, 180–191.
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 114

114 L.J. Gut et al.

deLame, F.M., Hong, J.J., Shearer, P.W. and Brattsten, L.B. (2001) Sex-related differences in the tolerance of
Oriental fruit moth, Grapholita molesta, to organophosphate insecticides. Pest Management Science 57,
827–832.
Deland, J.-P., Judd, G.J.R. and Roitberg, B.D. (1994) Disruption of pheromone communication in three
sympatric leafroller (Lepidoptera: Tortricidae) pests of apple in British Columbia. Environmental
Entomology 23, 1084–1090.
Den Otter, C.J. (1977) Single sensillum responses in the male moth Adoxophyes orana (F.v.R.) to female sex
pheromone components and their geometrical isomers. Journal of Comparative Physiology 121, 205–222.
Derrick, M.E., Van Duyn, J.W., Sorenson, C.E. and Kennedy, G.C. (1992) Effect of pheromone trap place-
ment on capture of male European corn borer (Lepidoptera: Pyralidae) in three North Carolina
crops. Environmental Entomology 21, 240–246.
Dickens, J.C. (1979) Electrophysiological investigations of olfaction in bark beetles. Mitteilungen der
Schweizerishce Entomologische Gesellschaft 52, 203–216.
Doane, C.D. (1999) Controlled-release devices for pheromones. In: Scher, H.B. (ed.) Controlled-release
Delivery Systems for Pesticides. Marcel Dekker, New York, pp. 295–317.
Duan, J.J. and Prokopy, R.J. (1995) Development of pesticide-treated spheres for controlling apple maggot
flies (Diptera: Tephritidae): pesticides and residue extending agents. Journal of Economic Entomology
88, 117–126.
Epstein, D. and Gut, L. (2000) A Pocket Guide for IPM Scouting in Michigan Apples. Extension Bulletin E-
2720, Michigan State University, East Lansing, Michigan, 72 pp.
Epstein, D., Waldstein, D. and Edson, C. (2002) Michigan Apple Integrated Pest Management Implementation
Project. Final Narrative Report. East Lansing, Michigan, 99 pp.
Evenden, M.L., Borden, J.H. and Van Sickle, G.A. (1995) Predictive capabilities of a pheromone-based
monitoring system for western hemlock looper (Lepidoptera: Geometridae). Environmental
Entomology 24, 933–943.
Evenden, M.L., Judd, G.J.R. and Borden, J.H. (2000) Investigations of mechanisms of pheromone commu-
nication disruption of Choristoneura rosaceana (Harris) in a wind tunnel. Journal of Insect Behavior 13,
499–510.
Faccioli, G., Antropoli, A. and Pasqualini, E. (1993) Relationship between males caught with low
pheromone doses and larval infestation of Argyrotainia pulchellana. Entomologia Experimentalis et
Applicata 68, 165–170.
Färbert, P., Koch, U.T., Färbert, A. and Staten, R.T. (1997) Measuring pheromone concentrations in cotton
fields with the EAG method. In: Cardé, R.T. and Minks, A.K. (eds) Insect Pheromone Research, New
Directions. Chapman & Hall, New York, pp. 347–358.
Fein, A. (1986) Excitation and adaptation of Limulus photoreceptors by light and inositol 1,4,5-triphos-
phate. Trends in Neuroscience 9, 110–114.
Figueredo, A.J. and Baker, T.C. (1992) Reduction of the response to sex pheromone in the Oriental fruit
moth, Grapholita molesta (Lepidoptera: Torticidae) following successive pheromonal exposures.
Journal of Insect Behavior 5, 347–361.
Fonta, C. and Masson, C. (1987) Structural and functional studies of the peripheral olfactory nervous sys-
tem of male and female bumble bees (Bombus hypnorum and B. terrestris). Chemical Senses 12, 53–69.
Furlong, M.J., Pell, J.K., Choo, O.P. and Rahman, S.A. (1995) Field and laboratory evaluation of a sex
pheromone trap for the autodissemination of a fungal entomopathogen Zoophthora radicans
(Entomophthorales) by the diamondback moth Plutella xylostella (Lepidoptera: Yponomeutidae).
Bulletin of Entomological Research 85, 331–337.
Gaston, L.K., Shorey, H.H. and Sario, S.A. (1967) Insect population control by the use of sex pheromones
to inhibit orientation between the sexes. Nature 213, 1155.
Gordon, F.C. and Potter, D.A. (1985) Efficiency of Japanese beetle (Coleoptera: Scarabaeidae) traps in
reducing defoliation of plants in the urban landscape and effect on larval density in turf. Journal of
Economic Entomology 78, 774–778.
Gordon, F.C. and Potter, D.A. (1986) Japanese beetle (Coleoptera: Scarabaeidae) traps: evaluation of sin-
gle and multiple arrangements for reducing defoliation in urban landscapes. Journal of Economic
Entomology 79, 1381–1384.
Gut, L. and Brunner, J. (1996) Implementing Codling Moth Mating Disruption in Washington Pome Fruit
Orchards. Tree Fruit Research and Extension Center Information Series 1, Washington State
University, Wenatchee, Washington, 8 pp.
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 115

Behaviour–modifying Chemicals 115

Gut, L. and Brunner, J. (1998) Pheromone-based management of codling moth (Lepidoptera: Tortricidae)
in Washington apple orchards. Journal of Agricultural Entomology 15, 387–405.
Gut, L.J., Wise, J., Isaacs, R. and McGhee, P. (1999) Obliquebanded leafroller control tactics and manage-
ment strategies: 1998 update. Proceedings of the Michigan State Horticulture Society 128, 97–106.
Hall, D.R., Nesbitt, B.F., Marrs, G.J., Green, A.StJ., Campion, D.G. and Critchley, B.R. (1982) Development
of microencapsulated pheromone formulations. In: Leonhardt, B.A. and Beroza, M. (eds) Insect
Pheromone Technology: Chemistry and Applications. ACS Symposium Series Number 190. American
Chemical Society, Washington, DC, pp. 131–143.
Hardie, J. and Minks, A.K. (eds) (1999) Pheromones of Non-lepidopteran Insects Associated with Agricultural
Plants. CAB International, Wallingford, UK, 466 pp.
Haynes, K.F., Miller, T.A., Staten, R.T., Li, W.G. and Baker, T.C. (1987) Pheromone trap for monitoring
insecticide resistance in the pink bollworm moth (Lepidoptera: Gelechiidae), new tool for resistance
management. Environmental Entomology 16, 84–89.
Howell, J.F. (1992) Control of codling moth (Cydia pomonella) using pheromone to disrupt mating
(Lepidoptera: Tortricidae). In: Proceedings XIX International Congress of Entomology. Beijing, p. 202.
Hu, X.P., Shasha, B.S., McGuire, M.R. and Prokopy, R.J. (1998) Controlled release of sugar and toxicant
from a novel device for controlling pest insects. Journal of Controlled Release 50, 257–265.
Il’ichev, A. and Sexton, S.B. (2002) Reduced application rates of mating disruption for effective control of
Oriental fruit moth Grapholita molesta (Busck) (Lepidoptera: Tortricidae) on pears. General and
Applied Entomology 31, 47–51.
Il’ichev, A.L., Gut, L.J., Hossain, M.S., Williams, D.G. and Jerie, P.H. (2002) Area-wide approach for
improved control of Oriental fruit moth, Grapholita molesta (Busck) (Lepidoptera: Tortricidae) by
mating disruption. General and Applied Entomology 31, 7–15.
Isaacs, R., Ulczynscki, M., Wright, B., Gut, L.J. and Miller, J.R. (1999) Performance of a microsprayer
specifically designed for pheromone-mediated control of insect pests. Journal of Economic Entomology
92, 1157–1164.
Jackson, D.M., Brown, G.C., Nordin, G.L. and Johnson, D.W. (1992) Autodissemination of a baculovirus
for management of tobacco budworms (Lepidoptera: Noctuidae) on tobacco. Journal of Economic
Entomology 85, 710–719.
James, D.G., Bartelt, R.J. and Moore, C.J. (1996) Mass-trapping of Carpophilus spp. (Coleoptera:
Nitidulidae) in stone fruit orchards using synthetic aggregation pheromones and a coattractant:
development of a strategy for population suppression. Journal of Chemical Ecology 22, 1541–1556.
Jenkins, J.W., Doane, C.C., Schuster, D.J., McLaughlin, J.R. and Jimenez, M.J. (1990) Development and
commercial application of sex pheromone for control of the tomato pinworm. In: Ridgway, R.L.,
Silverstein, R.M. and Inscoe, M.N. (eds) Behavior-modifying Chemicals for Insect Management. Marcel
Dekker, New York, pp. 269–280.
Johnson, R.L. and Schall, R.A. (1989) Early detection of new pests. In: Kahn, R.P. (ed.) Plant Protection and
Quarantine, Vol. III. CRC Press, Boca Raton, Florida, pp. 105–116.
Jones, O.T. (1998) Practical applications of pheromones and other semiochemicals. In: House, P.E.,
Stevens, I.D.R. and Jones, O.T. (eds) Insect Pheromones and Their Use in Pest Management. Chapman &
Hall, London, pp. 261–355.
Jones, O.T. and Casagrande, E.D. (2000) The use of semichemical-based devices and formulations in area-
wide programmes: a commercial perspective. In: Tan, K.-H. (ed.) Area-wide Control of Fruit Flies and
Other Insect Pests. Peneritg Universiti Sains Malaysia, Pulau Pinang, pp. 285–293.
Judd, G.J.R., Gardiner, M.G.T. and Thomson, D.R. (1996) Commercial treals of pheromone-mediated mat-
ing disruption with Isomate-C® to control codling moth in British Columbia apple and pear
orchards. Journal of the Entomological Society of British Columbia 92, 23–34.
Jutsum, A.R. and Gordon, R.F.S. (eds) (1989) Insect Pheromones in Plant Protection. Wiley, Chichester, UK,
369 pp.
Kaissling, K.-E. (1986) Chemo-electrical transduction in insect olfactory receptors. Annual Review of
Neuroscience 9, 121–145.
Karg, G. and Sauer, A.E. (1995) Spatial distribution of pheromones in fields treated for mating disruption
of the European grape vine moth Lobesia botrana measured with electroantennograms. Journal of
Chemical Ecology 21, 1299–1314.
Karg, G. and Sauer, A.E. (1997) Seasonal variation of pheromone concentration in mating disruption tri-
als against European grape vine moth, Lobesia botrana (Lepidoptera: Tortricidae) measured by EAG.
Journal of Chemical Ecology 23, 487–501.
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 116

116 L.J. Gut et al.

Karg, G., Sauer, A.E. and Koch, U.T. (1990) The influence of plants on the development of pheromone
atmospheres measured by EAG method. In: Elsner, N. and Roth G. (eds) Brain-Perception-Cognition,
Proceedings of the 18th Gottingen Neurobiology Conference. Thieme Verlag, Stuttgart, p. 301.
Karg, G., Suckling, D.M. and Bradley, S.J. (1994) Adsorption and release of pheromone of Epiphyas postvit-
tana (Lepidoptera: Tortricidae) by apple leaves. Journal of Chemical Ecology 20, 1825–1841.
Karlson, P. and Lüscher, M. (1959) ‘Pheromones’: a new term for a class of biologically active substances.
Nature 183, 55–56.
Klein, M.G. and Lacey, L.A. (1999) An attractive trap for autodissemination of entomopathogenic fungi
into populations of Japanese beetle, Popillia japonica (Coleoptera: Scarabaeidae). Biocontrol Science
and Technology 9, 151–158.
Klein, M.O. (1981) Mass trapping for suppression of Japanese beetles. In: Mitchell, E.R. (ed.) Management
of Insect Pests with Semiochemicals. Plenum Press, New York, pp. 183–190.
Klein, U. (1987) Sensillum-lymph proteins from antennal olfactory hairs of the moth Antheraea polyphe-
mus (Saturniidae): Insect Biochemistry 8, 1193–1204.
Knight, A.L. (1995) The impact of codling moth (Lepidoptera: Tortricidae) mating disruption on apple
pest management in Yakima Valley, Washington. Journal of the Entomological Society of British
Columbia 92, 29–38.
Knight, A.L. (1997) Mating disruption of leafrollers in Washington’s apple orchards. La Difesa delle Piante
20, 73–77.
Knight, A.L. and Croft, B.A. (1991) Modelling and prediction technology. In: van der Geest, L.P.S. and
Evenhuis, H.H. (eds) Tortricid Pests: Their Biology, Natural Enemies and Control. World Crop Pests
Volume 5. Elsevier, Amsterdam, pp. 301–312.
Knight, A.L. and Hull, L.A. (1988) Area-wide population dynamics of Platynota idaeusalis (Lepidoptera:
Tortricidae) in Southcentral Pennsylvania pome and stone fruits. Environmental Entomology 17,
1000–1008.
Knight, A.L. and Hull, L.A. (1989) Use of sex pheromone traps to monitor azinphosmethyl resistance in
tufted apple bud moth (Lepidoptera: Tortricidae). Journal of Economic Entomology 82, 1019–1026.
Knight, A.L. and Turner, J.E. (1999) Mating disruption of Pandemis spp. (Lepidoptera: Torticidae).
Environmental Entomology 28, 81–87.
Knight, A.L. and Weissling, T.J. (1999) Behavior-modifying chemicals in management of arthropod pests.
In: Ruberson, J.R. (ed.) Handbook of Pest Management. Marcel Dekker, New York, pp. 521–545.
Knight, A.L., Thomson, D.R. and Cockfield, S.D. (1998) Developing mating disruption of obliquebanded
leafroller (Lepidoptera: Tortricidae) in Washington State. Environmental Entomology 27, 1080–1088.
Knipling, E.F. (1979) The Basic Principles of Insect Populations Suppression and Management. Agriculture
Handbook 512, USDA, Washington, DC, 659 pp.
Koch, U.T., Cardé, A.M. and Cardé, R.T. (2002) Calibration of an EAG system to measure airborne con-
centration of pheromone formulated for mating disruption of the pink bollworm moth, Pectinophora
gossypiella (Saunders) (Lep., Gelechiidae). Journal of Applied Entomology 126, 431–435.
Koutek, B., Hoskovec, M., Vrkocova, P., Konecny, K. and Feltl, L. (1994) Gas chromatographic determina-
tion of vapor pressures of pheromone-like compounds II. Alcohols. Journal of Chromatography 679,
307–317.
Koutek, B., Hoskovec, M., Vrkocova, P., Konecny, K., Feltl, L. and Vrkoc, J. (1996) Gas chromatographic
determination of vapor pressures of pheromone-like compounds III. Aldehydes. Journal of
Chromatography 719, 391–400.
Koutek, B., Hoskovec, M., Vrkocova, P. and Feltl, L. (1997) Gas chromatographic determination of vapor
pressures of pheromone-like compounds IV. Acetates, a reinvestigation. Journal of Chromatography
759, 93–109.
Kuenen, L.P.S. and Baker, T.C. (1981) Habituation versus sensory adaptation as the cause of reduced
attraction following pulsed and constant sex pheromone pre-exposure in Trichoplusia ni. Journal of
Insect Physiology 27, 721–726.
Kydonieus, A.F. and Beroza, M. (1982) Insect Suppression with Controlled Release Pheromone Systems, Vols 1
and 2. CRC Press, Boca Raton, Florida.
Lanier, G.N. (1990) Principles of attraction–annihilation. In: Ridgway, R.L., Silverstein, R.M. and Inscoe,
M.N. (eds) Behavior-modifying Chemicals for Insect Management. Marcel Dekker, New York,
pp. 25–45.
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 117

Behaviour–modifying Chemicals 117

Latheef, M.A., Witz, J.A. and Lopez, J.D. Jr (1991) Relationships among pheromone trap catches of male
corn earworm moths (Lepidoptera: Noctuidae), egg numbers, and phenology in corn. Canadian
Entomologist 123, 271–281.
Lawson, D.S., Reissig, W.H., Agnello, A.M., Nyrop, J.P. and Roelofs, W.L. (1996) Interference with the
mate-finding communication system of the obliquebanded leafroller (Lepidoptera: Tortricidae)
using synthetic sex pheromones. Environmental Entomology 25, 895–905.
Liburd, O.E., Gut, L.J., Stelinski, L.L., Whalon, M.E., McGuire, M.R., Wise, J.C., Willett, J.L., Hu, X.P. and
Prokopy, R.J. (1999) Mortality of Rhagoletis species encountering pesticide-treated spheres (Diptera:
Tephritidae). Journal of Economic Entomology 92, 1151–1156.
Light, D.M., Knight, A.K., Henrick, C.A., Rajapaska, D., Lingren, B., Dickens, J.C., Reynolds, K.M.,
Buttery, R.G., Merrill, G., Roitman, J. and Campbell, B.C. (2001) A pear-derived kairomone with
pheromonal potency that attracts male and female codling moth, Cydia pomonella (L.).
Naturwissenschaften 88, 333–338.
Lindgren, B.S. and Borden, J.H. (1993) Displacement and aggregation of mountain pine beetles,
Dendroctonus ponderosae (Coleoptera: Scolytidae) in response to their antiaggregation and aggrega-
tion pheromones. Canadian Journal of Forest Research 23, 286–290.
Linn, C.E. Jr and Roelofs, W.L. (1981) Modification of sex pheromone blend discrimination in male
Oriental fruit moths by pre-exposure to (E)-8-dodecenyl acetate. Physiological Entomology 6, 421–429.
Linn, C.E. Jr and Roelofs, W.L. (1983) Effect on varying proportions of the alcohol component on sex
pheromone blend discrimination in male Oriental fruit moths. Physiological Entomology 8, 291–306.
Linn, C.E., Bjostad, L.B., Du, J.W. and Roelofs, W.L. (1984) Redundancy in a chemical signal: behavioral
responses of male Trichoplusia ni to a 6-component sex pheromone blend. Journal of Chemical Ecology
10, 1635–1658.
Mafra-Neto, A. and Baker, T.C. (1996) Timed, metered sprays of pheromone disrupt mating of Cauda
cautella (Lepidoptera: Pyralidae). Journal of Agricultural Entomology 13, 149–168.
Mayer, M.S. and McLaughlin, J.R. (1991) Handbook of Insect Pheromones and Sex Attractants. CRC Press,
Boca Raton, Florida, 1083 pp.
McBrien, H., Judd, G.J.R. and Borden, J.H. (1994) Campylomma verbasci (Heteroptera: Miridae):
pheromone-based seasonal flight patterns and prediction of nymphal densities in apple orchards.
Journal of Economic Entomology 23, 1224–1229.
McDonough, L.M., Brown, D.F. and Aller, W.C. (1989) Insect sex pheromones – effect of temperature on
evaporation rates of acetates from rubber septa. Journal of Chemical Ecology 15, 779–790.
Metcalf, R.L. and Metcalf, E.R. (1992) Plant Kairomones in Insect Ecology and Control. Chapman & Hall,
New York, 168 pp.
Millar, J.G. (1995) Degradation and stabilization of E8,E10-dodecadienol, the major component of the sex
pheromone of the codling moth (Lepidoptera: Tortricidae). Journal of Economic Entomology 88,
1425–1432.
Miller, J.R. (2004) Adsorptive interactions of insect pheromone-like compounds with inorganic solid sur-
faces: quantifying partitioning coefficients by gas–solid chromatography. Journal of Chemical Ecology
(in review).
Miller, J.R. and Cowles, R.S. (1990) Stimulo-deterrent diversion: a concept and its possible application to
onion maggot control. Journal of Chemical Ecology 16, 3197–3212.
Mitchell, E.R. (ed.) (1981) Management of Insect Pests with Semiochemicals. Plenum, New York, 514 pp.
Mitchell, E.R., Copeland, W.W., Sparks, A.N. and Sekul, A.A. (1974) Fall armyworm: disruption of
pheromone communication with synthetic acetates. Environmental Entomology 3, 778–780.
Morewood, P., Gries, G., Liska, Kapitola, P., Häußler, D., Möller, K. and Bogenshutz, H. (2000) Towards
pheromone-based monitoring in nun moth, Lymantria monacha (L.) (Lep., Lymantriidae) popula-
tions. Journal of Applied Entomology 124, 77–85.
Morrison, R.J. and Boyd, R.N. (1974) Organic Chemistry, 3rd edn. Allin and Bacon, Boston, Massachusetts.
Morse, B.W. and Kulman, H.M. (1985) Monitoring damage by yellowheaded spruce sawflies with sawfly
and parasitoid pheromones. Environmental Entomology 14, 131–133.
Murlis, J., Elkinton, J.S. and Cardé, R.T. (1992) Odor plumes and how insects use them. Annual Review of
Entomology 37, 505–532.
Nagata, K. (1989) Revue: pest control by mating disruption in Japan. Japanese Pesticide Information 54, 3–6.
Noldus, L.P.J., Potting, R.P.J. and Barendrengt, H.E. (1991) Moth sex pheromone adsorption to leaf sur-
faces: bridges in time for chemical spies. Physiological Entomology 6, 71–86.
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 118

118 L.J. Gut et al.

Nordlund, D.A., Jones, R.L. and Lewis, W.J. (1981) Semiochemicals: Their Role in Pest Control. John Wiley &
Sons, New York, 306 pp.
Norris, R.F., Caswell-Chen, E.P. and Kogan, M. (2003) Concepts in Integrated Pest Management. Prentice
Hall, Upper Saddle River, New Jersey, 586 pp.
Novak, M.A., Reissig, W.H. and Roelofs, W.L. (1978) Orientation disruption of Argyrotaenia velutinana
and Choristoneura rosaceana (Lepidoptera: Tortricidae) male moths. Journal of the New York
Entomological Society 4, 311–315.
O’Connell, R.J. (1972) Response of olfactory receptors to the sex attractant, its synergist and inhibitor in the
redbanded leaf roller, Argyrotaenia velutinana. In: Schneider, D. (ed.) International Symposium Olfaction
Taste IV, Wissenschaftliche Verlagsgesellschaft, Stuttgart, pp. 180–186.
O’Connell, R.J. (1981) The encoding of behaviorally important odorants by insect chemosensory neurons.
In: Norris, D.M. (ed.) Perception of Behavioral Chemicals. Elsevier/North-Holland Biomedical Press,
New York, pp. 133–163
O’Connell, R.J. (1985) Responses to pheromone blends in insect olfactory neurons. Journal of Comparative
Physioliology 156, 747–761.
Ogawa, K. (1990) Commercial development: mating disruption of tea tortrix moths. In: Ridgway, R.L.,
Silverstein, R.M. and Inscoe, M.N. (eds) Behavior-modifying Chemicals for Insect Management. Marcel
Dekker, New York, pp. 547–551.
Park, J.D. and Goh, H.G. (1992) Control of beet armyworm, Spodoptera exigua Hubner (Lepidoptera:
Noctuidae), using synthetic sex pheromone. I. Control by mass trapping in Allium fistulosum field.
Korean Journal of Applied Entomology 31, 45–49.
Pfeiffer, D.G., Kaakeh, W., Killian, J.C., Lachance, M.W. and Kirsch, P. (1993) Mating disruption to control
damage by leafrollers in Virginia apple orchards. Entomologia Experimentalis et Applicata 67, 47–56.
Prokopy, R.J., Wright, S.E., Black, J.L., Hu, X.P. and McGuire, M.R. (2000) Attracticidal spheres for control-
ling apple maggot flies: commercial-orchard trials. Entomologia Experimentalis et Applicata 97,
293–299.
Reissig, W.H., Novak, M. and Roelofs, W.L. (1978) Orientation disruption of Argyrotaenia velutinana and
Choristoneura rosaceana male moths. Environmental Entomolology 7, 631–635.
Rice, R.E. and Kirsch, P. (1990) Mating disruption of Oriental fruit moth in the United States. In: Ridgway,
R.L., Silverstein, R.M. and Inscoe, M.N. (eds) Behavior-modifying Chemicals for Insect Management.
Marcel Dekker, New York, pp. 193–211.
Ridgway, R.L., Silverstein, R.M. and Inscoe, M.N. (eds) (1990) Behavior-modifying Chemicals for Insect
Management. Marcel Dekker, New York, 761 pp.
Riedl, H., Hoying, S.A., Barnett, W.W. and Detar, J.E. (1979) Relationship of within-tree placement of the
pheromone trap to codling moth catches. Environmental Entomology 8, 765–769.
Riedl, H., Seaman, A. and Henrie, F. (1985) Monitoring susceptibility to azinphosmethyl in field popula-
tions of the codling moth (Lepidoptera: Tortricidae) with pheromone traps. Journal of Economic
Entomology 78, 692–699.
Riedl, H., Howell, J.F., McNally, P.S. and Westigard, P.H. (1986) Codling Moth Management, Use and
Standardization of Pheromone Trapping Systems. Bulletin 1918, University of California, Berkeley,
California, 23 pp.
Riherd, C., Nguyen, R. and Brazzel, J.R. (1994) Pest free areas. In: Sharpe, J.L. and Hallman, G.J. (eds)
Quarantine Treatments for Pests of Food Plants. Westview Press, Boulder, Colorado, pp. 213–223.
Ritter, F.J. (eds) (1979) Chemical Ecology: Odour Communication in Animals. Elsevier/North-Holland,
Amsterdam, 427 pp.
Roelofs, W.H. and Novak, M. (1981) Small-plot disorientation tests for screening potential mating disrup-
tants. In: Mitchell, E.R. (ed.) Management of Insect Pests with Semiochemicals: Concepts and Practice.
Plenum, New York, pp. 229–242.
Roelofs, W.L., Glass, E.H., Tette, J. and Comeau, A. (1970) Sex pheromone trapping for red-banded leaf
roller control: theoretical and actual. Journal of Economic Entomology 63, 1162–1167.
Rothschild, G.H.L. (1975) Control of Oriental fruit moth (Cydia molesta [Busck][Lepidoptera, Tortricidae])
with synthetic female pheromone. Bulletin of Entomological Research 65, 473–490.
Rothschild, G.H.L. (1981) Mating disruption of lepidopterous pests: current status and future prospects.
In: Mitchell, E.R. (ed.) Management of Insect Pests with Semiochemicals: Concepts and Practice. Plenum
Press, New York, pp. 207–228.
Rumbo, E.R. and Vickers, R.A. (1997) Prolonged adaptation as possible mating disruption mechanism in
Oriental fruit moth, Cydia (=Grapholita) molesta. Journal of Chemical Ecology 23, 445–457.
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 119

Behaviour–modifying Chemicals 119

Rybczynski, R., Reagan, J. and Lerner, M.R. (1989) A pheromone-degrading aldehyde oxidase in the
antennae of the moth Manduca sexta. Journal of Neuroscience 9, 1341–1353.
Sanders, C.J. (1985) Disruption of spruce budworm, Choristoneura fumiferana (Lepidoptera: Tortricidae),
mating in a wind tunnel by synthetic pheromone: role of habituation. Canadian Entomologist 117,
391–393.
Sanders, C.J. (1988) Monitoring spruce budworm population density with sex pheromone traps. Canadian
Entomologist 120, 175–183.
Sanders, C.J. (1997) Mechanisms of mating disruption in moths. In: Cardé, R.T. and Minks, A.K. (eds)
Insect Pheromone Research, New Directions. Chapman & Hall, New York, pp. 333–346.
Sanders, C.J. and Lucuik, G.S. (1996) Disruption of male Oriental fruit moth to calling females in a wind
tunnel by different concentrations of synthetic pheromone. Journal of Chemical Ecology 22, 1971–1986.
Sauer, A.E. and Karg, G. (1998) Variables affecting the pheromone concentration in vineyards treated for
mating disruption of grape vine moth. Journal of Chemical Ecology 24, 289–302.
Schlyter, F. and Birgersson, G.A. (1999) Forest beetles. In: Hardie, J. and Minks, A.K. (eds) Pheromones of
Non-lepidopteran Insects Associated with Agricultural Plants. CAB International, Wallingford, UK,
pp. 113–148.
Schmitz, V., Renou, M., Roehrich, R., Stockel, J. and Lecharpentier, P. (1997) Disruption mechanisms in
the European grape moth Lobesia botrana Den & Schiff. III. Sensory adaptation and habituation.
Journal of Chemical Ecology 23, 83–95.
Schneider, D. (1956) Electrophysical investigation on the antennal receptors of the silk moth during
chemical and mechanical stimulation. Experientia 13, 89–91.
Schneider, D. (1962) Electrophysical investigation on the olfactory specificity of sexual attracting sub-
stance in different species of moths. Journal of Insect Physiology 8, 15–30.
Schwalbe, C.P. and Mastro, V. (1990) Use of pheromones and attractants by government agencies in the
United States. In: Ridgway, R.L., Silverstein, R.M. and Inscoe, M.N. (eds) Behavior-Modifying
Chemicals for Insect Management. Marcel Dekker, New York, pp. 619–630.
Sexton, S.B. and Il’ichev, A. (2000) Pheromone mating disruption with reference to Oriental fruit moth
Grapholita molesta (Busck) (Lepidoptera: Tortricidae): literature review. General and Applied
Entomology 29, 63–68.
Shapas, T.J., Burkholder, W.E. and Boush, G.M. (1977) Population suppression of Trigoderma glabrum by
using pheromone luring for protozoan pathogen dissemination. Journal of Economic Entomology 70,
469–474.
Shearer, P.W. and Riedl, H. (1994) Comparison of pheromone trap bioassays for monitoring insecticide
resistance in Phyllonorycter elmaella (Lepidoptera: Gracillariidae). Journal of Economic Entomology 87,
1450–1454.
Shearer, P.W. and Usmani, K.A. (2001) Sex-related response to organophosphorous and carbamate insec-
ticides in adult Oriental fruit moth, Grapholita molesta. Pest Management Science 57, 822–826.
Shorey, H.H. and Gerber, R.G. (1996a) Use of puffers for disruption of sex pheromone communication
among navel orangeworm moths (Lepidoptera:Pyralidae) in almonds, pistachios, and walnuts.
Environmental Entomology 25, 1154–1157.
Shorey, H.H. and Gerber, R.G. (1996b) Use of puffers for disruption of sex pheromone communication of
codling moths (Lepidoptera: Tortricidae) in walnut orchards. Environmental Entomology 25,
1398–1400.
Shorey, H.H. and McKelvey, J.J. (1977) Chemical Control of Insect Behavior. John Wiley & Sons, New York,
414 pp.
Shorey, H.H., Kaae, R.S. and Gaston, L.K. (1974) Sex pheromones of Lepidoptera: development of a
method for pheromonal control of Pectinophora gossypiella in cotton. Journal of Economic Entomology
67, 347.
Shorey, H.H., Sisk, C.B. and Gerber, R.G. (1996) Widely separated pheromone release sites for disruption
of sex pheromone communication in two species of Lepidoptera. Environmental Entomology 25,
446–451.
Simandl, J. and Anderbrant, O. (1995) Spatial distribution of flying Neodiprion sertifer (Hymenoptera,
Diprionidae) males in a mature Pinus sylvestris stand as determined by pheromone trap catch.
Scandinavian Journal of Forest Research 10, 51–55.
Snow, J.W. (1990) Peachtree borer and lesser peachtree borer control in the United States. In: Ridgway,
R.L., Silverstein, R.M. and Inscoe, M.N. (eds) Behavior-modifying Chemicals for Insect Management.
Marcel Dekker, New York, pp. 241–253.
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 120

120 L.J. Gut et al.

Stanley, B.H., Reissig, W.H., Roelofs, W.L., Schwarz, M.R. and Shoemaker, C.A. (1987) Timing treatments
for apple maggot (Diptera: Tephritidae) control using sticky sphere traps baited with synthetic
apple volatiles. Journal of Economic Entomology 80, 1057–1063.
Staten, R.T., El-Lissy, O. and Antilla, L. (1997) Successful area-wide program to control pink bollworm by
mating disruption. In: Cardé, R.T. and Minks, A.K. (eds) Insect Pheromone Research, New Directions.
Chapman & Hall, New York, pp. 383–396.
Stelinski, L.L. and Liburd, O.E. (2001) Evaluation of various deployment strategies of imidacloprid-
treated spheres in highland blueberries for control of Rhagoletis mendax (Diptera: Tephritidae).
Journal of Economic Entomology 94, 905–910.
Stelinski, L.L., Liburd, O.E., Wright, S., Prokopy, R.J., Behle, R. and McGuire, M.R. (2001) Comparison of
neonicotinoid insecticides for use with biodegradable and wooden spheres for control of Rhagoletis
species (Diptera: Tephritidae). Journal of Economic Entomology 94, 1142–1150.
Stelinski, L.L., Miller, J.R. and Gut, L.J. (2003a) Presence of long-lasting peripheral adaptation in the
obliquebanded leafroller, Choristoneura rosaceana and absence of such adaptation in the redbanded
leafroller, Argyrotaenia velutinana. Journal of Chemical Ecology 29, 405–423.
Stelinski, L.L., Gut, L.J. and Miller, J.R. (2003b) Concentration of air-borne pheromone required for long-
lasting peripheral adaptation in the obliquebanded leafroller, Choristoneura rosaceana. Physiological
Entomology 29, 97–107.
Stengl, M., Hatt, H. and Breer, H. (1992) Peripheral processes in insect olfaction. Annual Review of
Physiology 54, 665–681.
Suckling, D.M. and Brockerhoff, E.G. (1999) Control of light brown apple moth (Lepidoptera: Tortricidae)
using an attracticide. Journal of Economic Entomology 92, 367–372.
Suckling, D.M. and Karg, G. (2000) Pheromones and other semiochemicals. In: Rechcigl, J. and Rechcigl,
N. (eds) Biological and Biotechnological Control of Insect Pests. CRC Press, Boca Raton, Florida,
pp. 63–99.
Suckling, D.M. and Shaw, P.W. (1992) Conditions that favor mating disruption of Epiphyas postvittana
(Lepidoptera: Tortricidae): Environmental Entomology 21, 949–956.
Suckling, D.M., Penman, D.R., Chapman, R.B. and Wearing, C.H. (1985) Pheromone use in insecticide
resistance surveys of the light brown apple moth Epiphyas postvittana. Journal of Economic Entomology
78, 204–206.
Suckling, D.M., Karg, G. and Bradley, S.J. (1996) Apple foliage enhances mating disruption of lightbrown
apple moth. Journal of Chemical Ecology 22, 325–341.
Swenson, D.W. and Weatherston, I. (1989) Hollow-fiber controlled-release systems. In: Jutsum, A.R. and
Gordon, R.F.S. (eds) Insect Pheromones in Plant Protection. Wiley, Chichester, UK, pp. 173–197.
Tamaki, Y. (1979) Multi-component sex pheromone of Lepidoptera with special reference to Adoxophyes
sp. In: Ritter, F.J. (ed.) Chemical Ecology: Odour Communication in Animals. Elsevier/North-Holland,
Amsterdam, pp. 169–180.
Taschenberg, E.F., Cardé, R.T. and Roelofs, W.L. (1974) Sex pheromone mass trapping and mating disrup-
tion for control of redbanded leafroller and grape berry moths in vineyards. Environmental
Entomology 3, 239–242.
Tatsuki, S. (1990) Application of the sex pheromone of the rice stem borer moth, Chilo suppressalis. In:
Ridgway, R.L., Silverstein, R.M. and Inscoe, M.N. (eds) Behavior-modifying Chemicals for Insect
Management. Marcel Dekker, New York, pp. 387–406.
Thayer, G.R. (2002) The sampling range of pheromone traps baited with lures of different strengths for
monitoring obliquebanded leafroller, Choristoneura rosaceana Harris (Lepidoptera: Tortricidae). MS
thesis, Washington State University, Pullman, Washington, 55 pp.
Thomson, D.R., Gut, L.J. and Jenkins, J.W. (1998) Pheromones for insect control. In: Hall, F.R. and Menn,
J.J. (eds) Methods in Biotechnology, Vol. 5: Biopesticides: Use and Delivery. Humana Press, Totowa, New
Jersey, pp. 385–412.
Todd, J.L. and Baker, T.C. (1997) The cutting edge of insect olfaction. American Entomologist 43, 174–182.
Trematerra, P. and Battaini, F. (1987) Control of Ephestia kuehniella Zeller by mass-trapping. Journal of
Applied Entomology 104, 336–340.
Trimble, R.M. (1995) Mating disruption for control of codling moth Cydia pomonella (L.) (Lepidoptera:
Tortricidae), in organic apple production in Southwestern Ontario. Canadian Entomologist 127,
493–505.
Van Steenwyk, R.A., Oatman, E.R. and Wyman, J.A. (1983) Density treatment level for tomato pinworm
(Lepidoptera: Gelechiidae) based on pheromone trap catches. Journal of Economic Entomology 76,
440–445.
05IntpestManCh5.QXD 14/4/04 2:24 pm Page 121

Behaviour–modifying Chemicals 121

Varela, L.G., Shearer, P.W., Jones, V.P., Riedl, H. and Welter, S.C. (1997) Monitoring of insecticide resis-
tance in Phyllonorycter mespilella (Lepidoptera: Gracillariidae) in four western states. Journal of
Economic Entomology 90, 252–260.
Vega, F.E., Dowd, P.F. and Bartelt, R.J. (1995) Dissemination of microbial agents using an autoinoculating
device and several insect species as vectors. Biological Control 5, 545–552.
Vickers, R.A. (1990) Oriental fruit moth in Australia and Canada. In: Ridgway, R.L., Silverstein, R.M. and
Inscoe, M.N. (eds) Behavior-modifying Chemicals for Insect Management. Marcel Dekker, New York,
pp. 183–192.
Vickers, R.A., Thwaite, W.G., Williams, D.G. and Nicholas, A.H. (1998) Control of codling moth in small
plots by mating disruption: alone and with limited insecticide. Entomologia Experimentalis et
Applicata 86, 229–239.
Vogt, R.G. and Riddiford, L.M. (1986) Pheromone reception: a kinetic equilibrium. In: Payne, T.L., Birch,
M.C. and Kennedy, C.E.J. (eds) Mechanisms in Insect Olfaction. Clarendon Press, Oxford, pp. 201–208.
Waldstein, D.W. and Gut, L.J. (2003a) Comparison of microcapsule density with various apple tissues
and formulations of Oriental fruit moth (Lepidoptera: Tortricidae) sprayable pheromone. Journal of
Economic Entomology 96, 58–63.
Waldstein, D.W. and Gut, L.J. (2003b) Effects of rain and sunlight on Oriental fruit moth (Lepidoptera:
Tortricidae) microcapsules applied to apple foliage. Pest Management Science (in review).
Wall, C. (1989) Monitoring and spray timing. In: Jutsum, A.R. and Gordon, R.F.S. (eds) Insect Pheromones
in Plant Protection. Wiley, Chichester, UK, pp. 39–66.
Wall, C. and Perry, J.N. (1983) Further observations on the responses of male pea moth, Cydia nigricana, to
vegetation previously exposed to sex-attractant. Entomologia Experimentalis et Applicata 33, 112–116.
Wall, C. and Perry, J.N. (1987) Range of action of moth sex-attractant sources. Entomologia Experimentalis
et Applicata 44, 5–14.
Wall, C., Sturgeon, D.M., Greenway, A.R. and Perry, J.N. (1981) Contamination of vegetation with syn-
thetic sex attractant released from traps for the pea moth, Cydia nigricana. Entomologia Experimentalis
et Applicata 30, 111–115.
Wawrzynski, R.P. and Ascerno, M.E. (1998) Mass trapping for Japanese beetle (Coleoptera: Scaraaeidae)
suppression in isolated areas. Journal of Arboriculture 24, 303–307.
Weatherston, I. (1990) Principles of design of controlled-release formulations. In: Ridgway, R.L.,
Silverstein, R.M. and Inscoe, M.N. (eds) Behavior-modifying Chemicals for Insect Management. Marcel
Dekker, New York, pp. 93–112.
Weisling, T.J. and Knight, A.K. (1995) Vertical distribution of codling moth adults in pheromone-treated
and untreated plots. Entomologia Experimentalis et Applicata 77, 271–275.
Welch, S.M., Croft, B.A. and Michels, M.F. (1981) Validation of pest management models. Environmental
Entomology 10, 425–432.
Whittaker, R.H. and Feeney, P. (1971) Allelochemicals: chemical interactions between species. Science 171,
757–770.
Wood, D.L., Silverstein, R.M. and Nakajima, M. (1970) Control of Insect Behavior by Natural Products.
Academic Press, New York, 345 pp.
Wyatt, T.D. (1997) Putting pheromones to work: paths forward for direct control. In: Cardé, R.T. and
Minks, A.K. (eds) Insect Pheromone Research, New Directions. Chapman & Hall, New York,
pp. 445–459.
Wyman, J.A. (1979) Effect of trap design and sex attractant release on tomato pinworm catches. Journal of
Economic Entomology 72, 865–868.
Zhang, G.-F., Meng, S.-Z., Han, Y. and Sheng, C.-F. (2002) Chinese tortrix Cydia trasisas (Lepidoptera:
Olethreutidae): suppression on street-planting trees by mass trapping with sex pheromone traps.
Environmental Entomology 31, 602–607.
Zufall, F. and Leinders-Zufall, T. (2000) The cellular and molecular basis of odor adaptation. Chemical
Senses 25, 473–481.
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6
Transgenic Insecticidal Cultivars in
Integrated Pest Management: Challenges and
Opportunities

Julio S. Bernal, Jarrad Prasifka, M. Sétamou and K.M. Heinz

Department of Entomology, Biological Control Laboratory, Texas A&M University,
College Station, TX 77843-2475, USA
E-mail: [email protected]

Introduction is lost annually to insect pests in the USA

(Pimentel et al., 1993). However, perhaps
Transgenic insect-resistant cultivars were more significant than the extent of losses is
first developed in the mid-1980s and were the failure, despite ample research invest-
commercially available starting in the mid- ments, to make any substantial progress
1990s (Hilder et al., 1987; Vaeck et al., 1987). towards reducing these losses. Losses due to
Transgenic potato cultivars expressing a insect pests in the first half of the 20th cen-
toxic protein derived from the bacterium tury were on average ~9%, while losses in
Bacillus thuringiensis Berliner (hereafter Bt) the latter half were ~13% (Pimentel et al.,
were available to farmers in 1995, while 1993). Moreover, while losses did not
maize and cotton varieties also expressing Bt decrease, insecticide use increased tenfold in
toxins were available 1 year later. All three the period ~1950–1990, although losses dur-
commercial introductions were made in the ing this period were offset by widespread
USA, but currently a number of transgenic planting of high-yielding varieties and
cultivars are planted in different countries greater use of fertilizer and other inputs
worldwide (e.g. cotton in Australia and (Pimentel et al., 1993). A suite of problems
Mexico). Thus far, development of insect- associated with widespread and heavy pesti-
resistant cultivars has followed two broad cide use are now well known and have been
approaches. One approach seeks to develop discussed at length elsewhere (e.g. Perkins,
transgenic cultivars by incorporating genes 1982; Regev, 1984; Repetto, 1985; McConnell
of plant origin that express proteins that and Hruska, 1993; NRC, 1993; Bottrell and
interfere with protein and sugar metabolism, Weil, 1995; Lichtenberg and Zimmerman,
whereas the other seeks to incorporate genes 1999; Porter et al., 1999). Increasing concern
of bacterial origin, largely from Bt, which are over such problems is one of the principal
acutely toxic to insects (Hilder et al., 1987; factors driving the development of inte-
Vaeck et al., 1987). Crop losses due to insect grated pest management (IPM) strategies for
pests account for a substantial portion of many crops worldwide.
total crop losses worldwide. One estimate A formal concept of IPM was first articu-
indicates that c. 13% of total crop production lated in the late 1950s (Stern et al., 1959). This
© CAB International 2004. Integrated Pest Management: Potential, Constraints and Challenges
(eds O. Koul, G.S. Dhaliwal and G.W. Cuperus) 123
06IntpestManCh6.QXD 14/4/04 2:25 pm Page 124

124 J.S. Bernal et al.

first conception was reductionistic in that malathion sprays against boll-weevil,

emphasis was largely restricted to integra- Anthonomus grandis grandis Boheman, in
tion of chemical- and biological control tac- southern US cotton), and infrequently takes
tics. Subsequent definitions expanded the into account natural-enemy populations.
concept to include the use of all available Insecticidal transgenic cultivars, as a form
tactics in a harmonious manner so that pest of plant resistance, are attractive novel tactics
populations are maintained below levels and may play central roles in IPM strategies.
causing economic injury (FAO, 1967; Smith A number of reasons make transgenic culti-
and van den Bosch, 1967), while others vars attractive tactical components of IPM
emphasized natural mortality factors, such strategies, particularly in relation to the use
as natural enemies, climate and crop man- of insecticides: (i) plants are protected
agement (Board on Agriculture, 1989). The throughout the growing season; (ii) pests are
discussion presented in this chapter is based treated at their most susceptible stage; (iii)
on a concept of IPM in which biological con- protection is independent of weather; (iv)
trol and plant resistance are fundamental pests protected from natural enemies and
components. insecticides by living within plant tissues are
The goal of IPM remains unchanged: exposed to the insecticidal effect of plants;
maintain pest populations below levels at (v) only insects feeding on the crop are
which they cause economic injury, while directly affected; (vi) the insecticidal factor is
maintaining productive, societal and envi- confined to plant tissues and therefore does
ronmental impacts at acceptable levels. not leach into the environment; and (vii) the
Moreover, the IPM concept adhered to herein insecticidal factor is biodegradable and
includes an agroecosystem-level focus. The therefore does not accumulate in the envi-
different crops within an agroecosystem ronment (Gatehouse et al., 1991). However,
share pest and natural-enemy populations, so several of these advantages may also be dis-
pest-management tactics implemented advantages. For instance, pest-management
within one crop are likely to have impacts decisions are made prior to planting and
across crops and across seasons. Thus, thus without knowledge of subsequent pest-
regional crop management (i.e. distribution population levels. Subeconomic pest popula-
in space and time) is also an important com- tions are targeted along with economic
ponent of IPM. Crop-specific IPM strategies populations. Such preemptive management
should take into account the potential tactics may have a significant impact on the
impacts of production practices, including sustainability of transgenic cultivars, a situa-
pest-management practices, on pest and nat- tion aggravated by extensive and continuous
ural-enemy populations of neighbouring and planting. Additional significant impacts are
subsequent crops, as well as effects of prior likely if the resistance factor of a transgenic
crops. IPM with an agroecosystem-level cultivar is also an important and valuable
focus is similar to area-wide pest manage- insecticide, as in the case of Bt. Other impor-
ment (Chandler and Faust, 1998) in that pests tant and likely impacts concern non-target,
are managed across large geographical areas, secondary pests of transgenic crops.
the boundaries of which are defined by pest- Typically, populations of secondary-pest
colonization and dispersal capabilities. species are maintained below economic lev-
However, the strategies differ in that area- els by the action of natural-enemy popula-
wide pest management typically focuses on tions. It is conceivable that transgenic crop
single or a few key pests, such as pink boll- plants might impair natural enemies of sec-
worm, Pectinophora gossypiella (Saunders), in ondary pests to the extent that biological
California, codling moth, Cydia pomonella control is relaxed and these pests become
(Linnaeus) in north-western USA and maize economically important.
rootworms, Diabrotica spp., in various US Commercially available transgenic crop
states. It frequently relies on single or a few cultivars, such as Bt-expressing cotton, maize
management tactics (e.g. baculovirus sprays and potatoes, are now widely grown in the
against Helicoverpa and Heliothis and USA and to a lesser extent worldwide.
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Transgenic Insecticidal Cultivars 125

Recent reports indicate that areas planted in genic cultivars express semi-active Bt toxins,
the USA exceed 7.0 million ha for maize, 1.4 whereas cultivars expressing insecticidal
million ha for cotton and 20 thousand ha for plant proteins are not currently available
potatoes and that they are likely to increase outside of research laboratories.
in each case (Gianessi and Carpenter, 1999;
NRC, 2000). Worldwide, the total area proba-
bly exceeds 35 million ha for these crops Cultivars expressing Bacillus thuringiensis
(ISAAA, 2002). Moreover, novel transgenic endotoxin genes
cultivars are being developed for numerous
crops worldwide and evaluated for introduc- Bt is a ubiquitous soil bacterium that was first
tion in the near term into many countries isolated and described in the early 1900s
(McLaren, 2000). The evident widespread (Federici, 1999). Commercial products based
planting of transgenic cultivars and projec- on Bt toxins and consisting of sporulated,
tions for greater areas, particularly in the lysed cells of fermented isolates have been
USA, indicate that these cultivars are quickly used for many years (Dulmage, 1981;
becoming mainstream IPM tactics. Thus, it is Federici, 1999). The insecticidal activity of Bt
imperative that the compatibility of trans- depends on intracellular, insecticidal crystal
genic cultivars with biological control and proteins produced by the bacterium during
regional crop management, both fundamen- sporulation, which accumulate as parasporal
tal tactics of IPM strategies, is evaluated. The bodies adjacent to spores. The mode of action
goals of this chapter are to identify chal- depends on a complex process, in which, fol-
lenges and opportunities pertinent to wide- lowing ingestion by susceptible insects,
scale adoption of transgenic crop cultivars as parasporal bodies are solubilized in the alka-
an IPM tactic and to suggest lines of research line environment (pH 8–10) of the midgut,
that it is critical to address prior to wide- thereby releasing large protoxin molecules
spread acceptance. Emphasis is placed upon (130–140 kDa), which are then reduced
likely interactions of transgenic crop culti- through proteolytic cleavage to smaller
vars with biological control and impacts on (~55–70 kDa), active toxins (Gill et al., 1992;
pest population levels at the agroecosystem Cannon, 1996; Schnepf et al., 1998). Activated
level. toxins paralyse and kill insects by destroying
the mid-gut epithelium through lysis of
epithelial cells, which allows movement of
Types of Transgenic Plants Currently gut contents into haemolymph, leading to an
Available or Being Developed for Pest increase in haemolymph pH (Gill et al., 1992;
Management Cannon, 1996; Schnepf et al., 1998; Federici,
1999). Transgenic crop cultivars express semi-
Development of insect-resistant transgenic activated Bt toxins (~69 kDa); thus, toxic
crop cultivars has thus far focused on two activity does not require solubilization in the
distinct approaches: (i) integration of bacter- insect mid-gut and requires relatively little
ial genes encoding for production of toxic protoxin-to-toxin conversion (Perlak et al.,
proteins, especially from Bt; and (ii) integra- 1990; Koziel et al., 1993). The abridged mode
tion of plant genes encoding for production of action of Bt expressed in transgenic crop
of enzyme inhibitors and sugar-binding cultivars has significant implications for the
lectins. Both approaches were pioneered in selectivity of these cultivars because both sol-
the mid-1980s and thus have developed in ubilization and protoxin–toxin conversion are
parallel (Hilder et al., 1987; Vaeck et al., 1987). important for the specificity of Bt activity
However, the first approach, based in partic- (Visser et al., 1993; Cannon, 1996). For exam-
ular on integration of δ-endotoxin genes ple, it is feasible that insects unable to solubi-
derived from various subspecies of Bt, has lize parasporal bodies may have appropriate
undoubtedly received more attention and receptors in the mid-gut epithelium for semi-
thus enjoyed greater progress. To date, all active Bt toxins expressed in transgenic
commercially available insect-resistant trans- plants (Hilbeck et al., 2000).
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126 J.S. Bernal et al.

Cultivars expressing plant-derived enzyme allow the possibility of combining (pyramid-

inhibitors and lectins ing) genes that are active at various target
sites within a pest insect or against various
Transgenic crop cultivars expressing plant pests. However, levels of protection pro-
genes are a valuable alternative to cultivars vided by genes of plant origin are typically
expressing Bt toxins. One significant advan- lower than those provided by genes express-
tage of using plant genes as a source of crop ing Bt toxins. Frequently, effects on target
resistance is their broad spectrum of activity insects are sublethal, including reductions in
across several orders, including sap-sucking feeding, weight gain, developmental rates
insect pests, such as Homoptera (Gatehouse and fecundity (Gatehouse and Gatehouse,
and Gatehouse, 1998). Indeed, plant genes 1998; Legaspi et al., 2004). Yet transgenic cul-
expressing chemical products responsible for tivars with sublethal or chronic effects on
plant resistance to insects are probably avail- target pests may be more attractive compo-
able against all pest species because they nents of IPM strategies than cultivars with
presumably evolved in response to her- acute toxic effects because they are more
bivory by insects. Thus far, a number of eco- likely to be compatible or act synergistically
nomically important crop plants, such as with biological control, as discussed below.
tobacco, potato, tomato, rice, sugarcane,
oilseed rape, among others, have been genet-
ically transformed to express various genes Role of Transgenic Plants in Pest
of plant origin (Gatehouse and Gatehouse, Management
1998; Legaspi et al., 2004). In many of these
cases, significant effects of the plant genes Insect resistance via transgenes is a form of
were evident on target-pest mortality rates plant resistance against insect pests. How-
and/or developmental and reproductive ever, unlike insect-resistant cultivars devel-
parameters (Gatehouse and Gatehouse, 1998; oped via conventional breeding methods,
Legaspi et al., 2004). commercially available transgenic cultivars,
Numerous plant chemical defensive com- all of which express Bt toxins: (i) are acutely
pounds have been identified to date, and toxic against their target pests; and (ii) were
these compounds are the bases for develop- developed largely by private enterprises and
ing transgenic cultivars expressing plant remain within the commercial realm. The
genes. The number of compounds identified acute toxicity of commercially available
to date potentially provides an unending transgenic cultivars has two significant impli-
array of opportunities for developing trans- cations for IPM. First, these cultivars exert
genic crop cultivars effective against virtu- strong selection pressures on target-pest pop-
ally any pest species. However, many plant ulations, which consequently are expected to
defensive compounds are products involv- rapidly evolve resistance in the absence of
ing multiple enzyme pathways and genes, effective resistance management strategies.
and hence transfer and expression of these Secondly, the acute toxicity of transgenic cul-
products in crop plants is beyond current tivars in many cases translates into signifi-
capabilities (Gatehouse and Gatehouse, cant indirect effects on upper-trophic-level
1998). None the less, a number of defensive consumers, such as natural enemies, and
compounds are protein products of single such effects will probably affect naturally
genes and these have been transferred occurring biological control. Both implica-
successfully to various crops. Largely, plant tions are further discussed below. Private
transformation involving plant genes has development of commercial transgenic culti-
focused on: (i) protease inhibitors; (ii) vars has meant that publicly supported IPM
α-amylase inhibitors; and (iii) lectins researchers are largely excluded from evalu-
(Gatehouse and Gatehouse, 1998). The var- ating these cultivars prior to their wide-
ied modes of action and levels of specificity spread deployment. At present, participation
of these gene products increase the potential in research on transgenic cultivars by IPM
target-pest range of transgenic cultivars and researchers remains largely restricted to eval-
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Transgenic Insecticidal Cultivars 127

uating their effectiveness against target pests toxins for chemical defence will rapidly lead
and developing resistance management to the evolution of resistant herbivore popu-
strategies intended to delay the evolution of lations. Thus, apparency theory predicts that
resistant pest populations. The top-down apparent plants will rely on digestibility
manner in which commercially available reducers for chemical defence. In contrast,
transgenic cultivars were deployed and their unapparent or rare plants will be colonized
rapid adoption by farmers left IPM by fewer insect herbivores, will not support
researchers with little time to adequately high and continuous insect populations and
integrate these cultivars into existing pest- will thus exert relatively low selection pres-
management strategies. Thus, transgenic cul- sure on herbivore populations. These plants
tivars are rapidly becoming stand-alone are predicted to rely on toxins for chemical
control tactics against their target pests. defence. However, all commercially available
Many of the potential ecological and environ- transgenic cultivars express toxins and are
mental problems that have been identified to acutely toxic to target pest species. The pre-
date associated with transgenic cultivars, and diction of apparency theory is clear in this
which remain to be addressed, are a direct case, and current widespread and deep con-
result of the top-down and rapid deployment cern over the sustainability of commercial
of these cultivars. Moreover, because trans- transgenic cultivars due to the evolution of
genic cultivars thus far have been entirely resistance in pest populations points to its
appropriated by private industry, external high likelihood. In short, the strategy of
costs such as potentially negative environ- developing transgenic cultivars that express
mental and pest-management impacts, will toxins is not evolutionarily sustainable.
probably tend to be neglected. A number of Because crop species are akin to apparent
these problems are discussed below. plants, one evolutionarily sustainable
Crop-plant resistance against insects approach is to develop crop cultivars that rely
involves either physical (e.g. pubescence) or on digestibility reducers (e.g. plant-derived
chemical (e.g. DIMBOA) defences. In gen- enzyme inhibitors and lectins). Moreover,
eral, transgenic cultivars rely on chemically digestibility reducers are more likely than tox-
based antibiosis as their plant resistance ins to be compatible with biological control
mechanism. Resistant plants expressing (see below). If a long-term objective of devel-
antibiosis produce significant negative phys- oping IPM strategies for specific crops is to
iological effects (e.g. slow development, rely more on biological control and plant resis-
reduced growth and fertility, death of young tance and less on non-biological alternatives,
individuals, etc.) on susceptible herbivores then emphasis should be placed on develop-
feeding on their tissues. ‘Apparency theory’ ing transgenic cultivars that act synergistically
(Feeny, 1976; Rhoades and Cates, 1976) pro- or at least additively with biological control.
vides a useful framework for discussing This requires greater interaction during culti-
plant resistance to insects and the types of var development between plant breeders and
transgenic cultivars that may be most useful biological control researchers than currently
in agriculture. Chemical defences involved occurs. One promising approach is to develop
in antibiosis can be broadly categorized as antibiosis-expressing transgenic cultivars that
toxins (qualitative defences) or digestibility reduce yield losses while rendering pests more
reducers (quantitative defences), and susceptible to parasitism and predation by
apparency theory predicts that plants should natural enemies. For example, plant resistance
rely on either type of chemical defence, via digestibility reducers that decrease the
depending on the probability of herbivore amount of feeding and prolong the develop-
colonization (Feeny, 1976; Rhoades and mental period of pests may act synergistically
Cates, 1976). Apparent plants, such as crop with biological control by increasing the
species, will predictably be colonized by length of time during which pests are suscep-
large numbers of insect herbivores over evo- tible to parasitism and predation. Examples
lutionary time and, because insects repro- are documented in which longer developmen-
duce at a greater rate than plants, reliance on tal times in herbivores led to increased para-
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128 J.S. Bernal et al.

sitism or predation rates and more effective remedial control measures, such as insecti-
biological control (Price et al., 1980; Haggstrom cide applications. The evolutionary goal
and Larsson, 1995; Luck et al., 1995; Benrey should be to deploy transgenic cultivars that
and Denno, 1997; Devine et al., 2000). will not rapidly select for resistant pest pop-
Moreover, existing cultivars that are known to ulations and consequently will be sustain-
produce alternative foods (e.g. floral nectar, able in the medium to long term with nil or
extrafloral nectar, pollen) at high levels or of minimal intervention. The economic goal
high quality or that support (and tolerate) sub- should be to deploy transgenic cultivars that
stantial populations of alternative hosts or do not significantly add to production costs
prey may be targeted for transformation to and therefore have a cost : benefit ratio that is
express digestibility reducers active against largely independent of market and yield
target pests. Numerous studies have demon- fluctuations. Transgenic cultivars should be a
strated the importance of the availability of viable alternative for farmers in marginal as
alternative food sources or hosts/prey in well as high-yielding areas. In sum, a long-
maintaining natural-enemy populations at term goal of developing transgenic cultivars
levels that effect biological control of target should be to facilitate transition to ecologi-
pests (Hagen, 1986; Jervis et al., 1993; Bottrell et cally based IPM strategies for major crops
al., 1998; Ferro and McNiel, 1998; Thompson worldwide, while maintaining the economic
and Hagen, 1999). An alternative approach is and evolutionary sustainability of the culti-
to develop transgenic cultivars that rely on vars. However, the context in which com-
antixenosis as a resistance mechanism. mercial transgenic cultivars are developed
Resistant plants expressing antixenosis are and deployed may not be compatible with
refractory to colonizing herbivores and hence such a goal. It remains to be seen whether
frequently lead to increased levels of activity future development of transgenic cultivars
and movement of susceptible herbivores on will be dictated by market opportunities and
and between plants. Examples are docu- technological limitations (e.g. single-gene
mented in which greater herbivore movement transformations), rather than the needs of
led to greater parasitism rates, and such incre- farmers and interest in the long-term sus-
ments may lead to improved biological control tainability of agricultural production.
(Pair et al., 1986; Annis and O’Keefe, 1987). Developing and deploying transgenic culti-
Other plant traits not directly targeted against vars simply because the necessary technol-
insect pests but that may interact positively ogy is now available is not justifiable if a
with biological control if transferred to crop long-term goal of IPM research is to develop
cultivars are discussed by Hoy et al. (1998). strategies that contribute to agricultural sus-
Some examples include improved tolerance to tainability. Farmers’ needs should be consid-
diseases, which would raise the threshold ered prior to transgenic-cultivar development,
level for insect vectors, and altered plant archi- and the likely ecological, environmental and
tecture and leaf surfaces, which may affect the socio-economic impacts closely examined to
exposure of pests to natural enemies. the extent that current science allows so that
The development and deployment of scientifically informed decisions supersede
transgenic cultivars should be pursued those based on commercial interests.
within a context of ecological, evolutionary
and economic considerations. Ideally, trans-
genic cultivars should be developed as tacti- Challenges and Opportunities in
cal components of IPM strategies and their Deploying Transgenic Cultivars as
compatibility with biological control tactics Tactical Components of IPM Systems
should be considered a priority during
development. The ecological goal should be Interactions of transgenic crop cultivars with
to promote a transition to true ecologically IPM tactics
based pest management, which maintains
populations of potential pests at low levels, As discussed in this chapter, IPM has its
and in so doing, obviates the need to apply foundations in biological control and plant
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Transgenic Insecticidal Cultivars 129

resistance, and benefits from regional crop enemies and herbivores are likely to be most
management that has an impact on levels of affected by widespread deployment of trans-
pest and natural-enemy populations within genic crops. Such impacts may be negative,
crops. Because transgenic crop cultivars are a and thus pose challenges to be redressed, or
form of plant resistance, it is likely that they positive, and thus offer opportunities to be
will increasingly occupy central roles within exploited. Redressing any challenges and
IPM strategies, a trend that is rapidly becom- taking advantage of any opportunities are
ing evident in the case of Bt-transgenic culti- crucial if transgenic cultivars are to be ade-
vars in the USA. In consequence, it is quately integrated into IPM strategies.
important that potential impacts, whether
positive or negative, of transgenic crop culti-
vars on herbivore (including non-target Biological control
species) and natural-enemy populations at
the agroecosystem level are identified and Natural enemies important in biological con-
measured. trol include parasitoids, predators, and
The levels of pest populations found in pathogens. Of these, parasitoids are perhaps
crops are influenced by movement of pest- the most important as they are responsible
and natural-enemy populations between for most documented examples of biological
crops and seasons within agroecosystems. control. For example, c. three-quarters of
Thus, pest levels and biological control are 1193 species of predators and parasitoids
likely to be affected by deployment of trans- included in a world review of biological
genic crop cultivars, particularly if these cul- control programmes were parasitoids
tivars affect a wide range of herbivores and (Gordh et al., 1999). Predators are widely
are widely planted within agroecosystems. recognized as important mortality factors,
Thus far, a number of studies have docu- particularly in ephemeral crops (Kogan et al.,
mented the occurrence of significant nega- 1999), even if their impact on pest popula-
tive effects of transgenic cultivars on tions is frequently unappreciated or underes-
non-target insects, while others have shown timated. Moreover, the importance of
negligible, non-existent, or positive effects predation for pest management is well estab-
(Bell et al., 1999; Birch et al., 1999; Losey et al., lished in several crops for which transgenic
1999; Schuler et al., 1999; Hilbeck et al., 2000; cultivars are commercially available (e.g. cot-
Jesse and Obrycki, 2000; Wraight et al., 2000; ton: Hagen et al., 1976; González and Wilson,
Sétamou et al., 2002a,c). The magnitude and 1982). Pathogens are not widely relied upon
direction of potential effects of transgenic for insect-pest management, although in
crops on IPM strategies will depend on the many cases they are believed to be important
degree to which herbivore and natural- short-term regulators of insect populations
enemy populations are affected. Transgenic (Federici, 1999). Indeed, only one pathogen,
cultivars that have sublethal effects on herbi- Bt, is widely used for pest management.
vores and natural enemies will have a differ- Thus, the discussion that follows focuses
ent impact on their populations from that of largely on likely and known impacts of
cultivars that have lethal effects. At the same transgenic cultivars on parasitoids and bio-
time, transgenic cultivars that have negligi- logical control by natural enemies other than
ble effects on natural enemies will probably pathogens.
have positive impacts on IPM strategies. Parasitoids, mostly in the order
Because transgenic crop cultivars are a Hymenoptera, have larvae that typically
form of plant resistance, a tactic that occu- consume and kill single hosts, while adults
pies a central role in modern IPM strategies, are free-living or only secondarily carnivo-
they will interact with other cornerstone IPM rous, feeding on host-derived haemolymph.
tactics. Frequently, IPM strategies rely on The biology of parasitoid larvae and their
biological control and are affected by relationships with hosts have two important
regional crop management. Thus, biological implications for the suite of potential
control and transient populations of natural impacts of transgenic cultivars on biological
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130 J.S. Bernal et al.

control. First, parasitoid larvae are typically

Larvae
unable to search for a new host if the avail- Individuals
able host is unsuitable. Secondly, parasitoids
are frequently capable of exploiting only a Adults
Potential
small number of closely related species as effects on
hosts. Thus, it is likely that, if a transgenic parasitoids
Negative
cultivar affects a parasitoid’s main host, all
alternative host species will be similarly
affected. In consequence, parasitoid females Populations – Synergistic
searching for hosts within a transgenic crop biological control
are likely to encounter only hosts that are
Additive
susceptible to the transgenic cultivar, and
their offspring are restricted to developing
on these hosts. The likely effects of trans- Fig. 6.1. Levels at which transgenic insecticidal crop
genic crop cultivars on parasitoids are sum- cultivars may have an impact on parasitoids and
some likely directions of impacts.
marized in Fig. 6.1. The potential effects of
transgenic cultivars on parasitoids are
divided into individual- and population- (Fig. 6.2). For example a direct positive effect
level effects. At the individual level, the on parasitoid larvae was evident in a recent
likely effects are further divided into those study in which it was suggested that the
affecting parasitoid larvae and adults. At the immune-defence reactions of hosts were
population level, the likely effects are those compromised by feeding on artificial diet
relating to impacts on biological control as a containing 2% of the lectin Galanthus nivalis
population-level process. Specifically, the agglutinin (GNA) (Bell et al., 1999; Fig. 6.2).
effects are divided into negative (e.g. impacts Broods of the gregarious parasitoid Eulophus
of wide-scale depletion of host populations), pennicornis (Nees) developing on tomato
synergistic (e.g. greater parasitism levels due moth larvae, Lacanobia oleracea (Linnaeus) fed
to weakened host immune responses) and an artificial diet containing 2% GNA were
additive effects (e.g. parasitism of individu- more than twice as large (21 adult para-
als surviving the effects of transgenic plants). sitoids per host) as broods developing on
Each of these likely effects of transgenic cul- hosts fed a diet without GNA (nine adult
tivars on parasitoids and biological control parasitoids per host) (Bell et al., 1999).
by parasitoids is briefly discussed below. However, a similar effect was not evident
when hosts were fed transgenic potato
leaves expressing GNA at 0.8%. In contrast,
Individual-level effects
direct negative impacts on parasitoid larvae
The most direct and obvious effect of trans- are evident in studies showing decreased
genic crop cultivars on parasitoid larvae survival of parasitoids developing on hosts
occurs in hosts susceptible to the transgenic feeding on transgenic plant tissues due to
cultivar and is the result of the acute toxicity exposure to toxins (Fig. 6.2). For example, a
of the cultivar to the host (Fig. 6.2). In this recent study showed that egg–adult sur-
case, parasitoid eggs or larvae are unable to vivorship was c. 90% in parasitoids develop-
complete their development due to prema- ing on hosts fed non-transgenic maize tissue,
ture death of their host. Such effects on para- while it was c. 40% in those whose hosts
sitoids are likely to be less important in were intoxicated after feeding on transgenic
transgenic cultivars that are not acutely toxic maize tissue (Bernal et al., 2002). Similar
to the targeted pests such as cultivars effects on survivorship are evident in preda-
expressing enzyme inhibitors and lectins or tors fed prey intoxicated after feeding on
toxins at low doses. transgenic maize tissue versus those fed
The effects on parasitoid larvae via hosts healthy prey (Hilbeck et al., 1998).
tolerant of the transgenic cultivar are less Indirect effects of transgenic cultivars on
obvious and can be either direct or indirect parasitoid larvae are probably common as
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Transgenic Insecticidal Cultivars 131

Susceptible Parasitoid death/

host failure to develop
Impaired
Positive immune
response
Larvae
Direct

Exposure
Tolerant Negative to toxin
host

Altered
Indirect host
quality

Fig. 6.2. Likely impacts of transgene products on parasitoid larvae developing on/in hosts feeding on
transgenic insecticidal crop cultivars.

they derive from effects on a herbivore’s The effects on parasitoid adults will thus be
quality as a host. For instance, both target determined by the susceptibility of the devel-
and non-target pests of transgenic cultivars oping larvae to the transgenic cultivar as
are frequently sublethally affected by these mediated by the host, or the effects on larvae
cultivars, and negative effects, such as lower of developing on hosts of altered quality. In
weight and nutritional quality, will probably addition, transgenic cultivars may affect para-
affect developing parasitoid larvae (Fig. 6.2). sitoid adults independently of effects on their
A number of studies have shown that hosts larvae by interfering with different compo-
fed transgenic plant tissue weighed less than nents of the host-finding process, and these
hosts fed non-transgenic plant tissue, and effects may be mediated by the transgenic cul-
that these differences in weight resulted in tivar itself or by hosts feeding on transgenic
smaller, less fit parasitoids, smaller para- plants (Fig. 6.3). For example, plants are
sitoid broods and a lower ratio of female off- known to emit volatiles that attract natural
spring (Adamczyk et al., 1998; Lynch et al., enemies, particularly when they are under
1999; Couty et al., 2001; Sétamou et al., attack by herbivores (Turlings and Benrey,
2002a,b). In contrast, differences in suscepti- 1998; Venzon et al., 1999; Pels and Sabelis,
bility between target and non-target pests of 2000). It is conceivable that volatiles emitted
transgenic cultivars may result in indirect by transgenic cultivars are qualitatively differ-
positive effects such as improved quality as a ent from those emitted by non-transgenic cul-
host in the latter pests (Fig. 6.2). For exam- tivars. One recent study failed to find
ple, non-target pests may have greater toler- differences between herbivore-damaged
ance than target pests, and may benefit (e.g. transgenic and non-transgenic oil-seed rape
increased weight gain) from feeding on plants in their attractiveness to the parasitoid
transgenic cultivars that express low levels Cotesia plutellae (Kurdyumov) (Schuler et al.,
of insecticidal proteins or toxins (De Leo et 1999). However, the results of another study
al., 1998; Sétamou et al., 2002b). Any benefits showed that when given a choice, sugarcane
for parasitoid larvae of feeding on borer, Diatraea saccharalis (Fabricius), and
improved-quality hosts, however, will Mexican rice borer, Eoreuma loftini (Dyar),
depend on their susceptibility to insecticidal adults prefer non-transgenic over transgenic
proteins, which may accumulate in their GNA-expressing sugarcane for oviposition,
host’s gut and haemolymph (Fitches and suggesting that differences exist between the
Gatehouse, 1998; Bell et al., 1999). sugarcane cultivars in their attractiveness to
Transgenic cultivars may affect parasitoid these herbivores (Bernal and Sétamou, 2003).
adults via effects on larvae that develop on It is conceivable that these differences may
tolerant hosts, as discussed above (Fig. 6.2). also extend to adult parasitoids searching for
06IntpestManCh6.QXD 14/4/04 2:25 pm Page 132

132 J.S. Bernal et al.

Plant- Interfere with host habitat location,

mediated synomone production and threshold,
alternative food sources

Kairomones e.g. faeces,

Adults honeydew

Synomones e.g. elicitors

Host-
mediated

Less defence,
Behaviour more movement,
less noise

Fig. 6.3. Likely impacts of transgenic insecticidal crop cultivars on parasitoid adults as mediated by the
transgenic plant or by hosts feeding on transgenic plants.

sugarcane borer or Mexican rice borer hosts in herbivore chemical cues, products or elici-
infesting sugarcane plants. tors between herbivores feeding on trans-
In addition to direct effects, transgenic genic versus non-transgenic cultivars, or in
cultivars may also affect parasitoid adults the attractiveness of these cultivars to para-
indirectly via their hosts (Fig. 6.3). Currently, sitoids searching for hosts. In contrast, avail-
all transgenic cultivars are active on their tar- able data suggest that transgenic cultivars
get pest’s gut or digestive processes. may affect parasitoid adults via alterations in
Parasitoids in general are known to rely on the behaviour of their hosts (Fig. 6.3). The
chemical cues (kairomones) from their hosts positive effect of increased herbivore move-
(e.g. pheromones) or host products (e.g. ment on parasitism rates (Pair et al., 1986;
frass, honeydew) during the host-searching Annis and O’Keefe, 1987) was discussed
process. It is conceivable that chemical cues above, and it is likely that pests intoxicated
emanating from host products, such as frass or weakened after feeding on transgenic cul-
or honeydew, may be altered in herbivores tivars may be less able to defend themselves
feeding on transgenic cultivars. For example, against natural-enemy attack. Some studies
females of the parasitoid Cotesia marginiven- show that host aggression against parasitoid
tris (Cresson) were more attracted to frass of adults can result in high levels of parasitoid
fall armyworm, Spodoptera frugiperda (J.E. mortality during host handling (Potting et
Smith) that had fed on non-transgenic versus al., 1999). In contrast, natural enemies that
transgenic maize tissue (Bernal et al., unpub- rely on airborne or substrate-borne vibratory
lished data). Also, the lectin GNA was found or visual cues for locating hosts or prey may
in similar to higher concentrations in the be less successful if hosts/prey show
honeydew relative to the diet of rice brown decreased activity levels when feeding on
planthopper, Nilaparvata lugens (Stal) transgenic cultivars. For example, Mexican
between 24 and 72 h after feeding on a GNA rice borer, a stem-boring pest, is less active
diet (Powell et al., 1998). Similarly, produc- and produces less noise inside artificial tun-
tion of herbivore-induced chemical cues nels and consequently is parasitized less fre-
(synomones) by plants is dependent on elici- quently when feeding on diet containing
tors from herbivores, and these elicitors are GNA versus diet free of GNA (Tomov et al.,
associated with herbivore feeding (Turlings 2003).
and Benrey, 1998). It is plausible that the
chemical composition of these elicitors is
Population-level effects
altered in herbivores feeding on transgenic
cultivars. However, few data are currently Finally, transgenic cultivars may affect para-
available that address potential differences sitoids at the population level, and conse-
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Transgenic Insecticidal Cultivars 133

quently may have an impact on the degrees mies are able to exploit only a narrow range
of biological control they achieve (Fig. 6.4). of host/prey instars or sizes. Comparable dif-
The effects at the population level may be ferences in parasitism rates, albeit not signifi-
evident at the agroecosystem level if trans- cant, were reported in a study involving
genic cultivars eliminate host populations to tobacco budworm, maize earworm,
the extent that parasitoid populations are Helicoverpa zea (Boddie), and transgenic
unable to persist locally (negative direct) or tobacco (Warren et al., 1992). Similar synergis-
suffer in terms of their quality (negative indi- tic interactions are plausible if transgenic cul-
rect), or they will be extensions of effects on tivars have other sublethal effects, such as
parasitoid larvae and adults at the individual weakening a host’s immune system or
level, as discussed above (synergistic or addi- impairing its ability to defend itself from par-
tive) (Fig. 6.4). Agroecosystem-level effects on asitoids, as discussed above.
natural-enemy populations and biological A significant interaction may be lacking
control are further discussed below. between transgenic cultivars and biological
Synergistic effects of transgenic cultivars on control in the field, with any effects merely
biological control will arise when pest mor- being additive (Fig. 6.4). Additivity between
tality due to plant resistance and natural ene- transgenic cultivars and biological control
mies within transgenic fields is greater than through parasitism or predation of pest indi-
the expected sum of the mortality from both viduals surviving after feeding on transgenic
these factors. However, synergism with bio- plants has significant implications for the
logical control is more likely in transgenic evolution of resistance in pest populations to
cultivars that are sublethal to the targeted transgenic cultivars, because surviving indi-
pest. For example, greater than expected par- viduals are likely to be genetically resistant
asitism of tobacco budworm, Heliothis to the antibiotic effects of these cultivars. For
virescens (Fabricius), by the parasitoid example, genetic models show that natural
Campoletis sonorensis (Cameron) was evident enemies may double to quadruple the num-
in transgenic tobacco expressing a low level bers of generations necessary for the evolu-
of Bt endotoxin relative to non-transgenic tion of resistance to transgenic cultivars in
tobacco (Johnson and Gould, 1992). In this pest populations (Johnson and Gould, 1992;
case, the greater parasitism was attributed to Arpaia et al., 1997). However, more compre-
longer developmental times for tobacco bud- hensive models indicate that natural enemies
worm larvae and the ensuing longer window may increase, decrease or not affect the rate
of opportunity for parasitism, which should of resistance evolution in pest populations
be increasingly important where natural ene- (Gould et al., 1991).

Depletion of
Direct host
populations
Negative
Reduction of
quality in
Indirect host
Populations –
biological population
control

Extended ‘window’,
Synergistic weak immune system
and defensive reactions

Parasitism of
Additive surviving individuals

Fig. 6.4. Likely impacts of transgenic insecticidal crop cultivars, and their direction, on parasitoid
populations and biological control.
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134 J.S. Bernal et al.

Other important interactions between 1981; Honêk, 1982; Vorley and Wratten, 1987;
transgenic cultivars and biological control Brazzle et al., 1997; Kennedy and Storer,
are likely to occur via secondary pests, which 2000). Indeed, interconnections of both pest
typically are not targeted during transgenic and natural-enemy populations in common
cultivar development. In this case, the most transgenic crops to other crops in regional
obvious effects will derive from two likely production systems are well established.
effects of transgenic cultivars. First, sec- Common pests of agroecosystems in
ondary pests may be sublethally affected by North Carolina are unquestionably linked.
transgenic cultivars due to greater tolerance The European corn borer, Ostrinia nubilalis
of the insecticidal toxins or proteins (Hübner), colonizes potatoes and wheat
expressed by these cultivars relative to target (Anderson et al., 1984; Umeozor et al., 1986;
(primary) pests. In this case, the expected Jones, 1994) before infesting maize and cot-
effects would be similar to those discussed ton (Savinelli et al., 1986, 1988; Umeozor et
above for sublethally affected primary (i.e. al., 1986). Maize earworm, H. zea, popula-
target) pests, as well as the agroecosystem- tions initially develop in maize and later col-
level effects discussed below. Secondly, a onize cotton and soybean crops in the area
positive interaction between transgenic culti- (Neunzig, 1963, 1969), while two-spotted spi-
vars and biological control may occur if der mites, Tetranychus urticae (Koch), from
deployment of these cultivars results in maize become pests in nearby groundnuts
reduced usage of broad-spectrum insecti- (Brandenburg and Kennedy, 1982; Margolies
cides against primary pests, which may lead and Kennedy, 1985).
to improved biological control of secondary A similar relationship exists for natural
pests through conservation of natural enemies in Texas cropping systems.
enemies. A number of examples in which Parasitoids such as Trichogramma pretiosum
Bt-transgenic potato cultivars support Riley, C. sonorensis (Cameron) and Microplitis
greater and more diverse natural-enemy croceipes (Cresson) all parasitize maize ear-
communities are discussed by Hoy et al. worm or tobacco budworm, H. virescens in
(1998). However, it will be important that several crops, including lucerne, maize and
applications of broad-spectrum insecticides potatoes early in the season and lucerne,
are indeed reduced if transgenic cultivars are maize, cotton and grain sorghum later in the
to enhance conservation biological control of season (Puterka et al., 1985). Predators,
secondary pests. Currently, some studies including spiders, convergent lady bird,
indicate that lesser amounts of insecticides Hippodamia convergens Guérin-Méneville, and
are applied in transgenic crops, such as Bt minute pirate bugs, Orius tristicolor (White)
maize and cotton, whereas others fail to find and Orius insidiosis (Say), move between cot-
significant reductions in the use of broad- ton and grain sorghum throughout their
spectrum insecticides (Fernández-Cornejo coincident cultivation, apparently respond-
and McBride, 2000). ing to local prey abundances (Prasifka et al.,
1999). Maize and grain sorghum also appear
to provide the H. convergens colonists that
Effects on agroecosystems later reproduce and sustain ladybird popula-
tions in cotton (J. Prasifka and K.M. Heinz,
Beyond effects on individuals and popula- unpublished data).
tions lies the issue of how deployment of Many other examples support the asser-
transgenic cultivars may alter the agro- tion that pest and natural-enemy popula-
ecosystem outside single transgenic field tions interact across landscapes and seasons,
boundaries. Both contemporaneous and suggesting that interactions between trans-
sequential crops affect neighbouring fields, genic and non-transgenic crops are likely.
in part because the arthropod faunas of However, because current research on the
annual crops are often produced by immi- effects of transgenic cultivars is performed
gration from nearby crops (Kieckhefer and on a much smaller scale, agroecosystem
Miller, 1967; Poston and Pedigo, 1975; Ives, effects must be predicted on the bases of lim-
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Transgenic Insecticidal Cultivars 135

ited studies, whose results vary widely (see levels of both pests and natural enemies exist
previous section). In the absence of a clear within transgenic fields, the natural process
indication of what can be expected at the of arthropod colonization of nearby crops
individual-field level, possible detrimental will be disrupted and natural biological con-
and beneficial impacts from the spread of trol compromised. For example, pests may
transgenic insecticidal cultivars are consid- colonize from a weedy host, and a transgenic
ered in turn. crop that traditionally supplied natural ene-
mies will probably fail to control the pest,
requiring remedial insecticide treatments.
Challenges to IPM in agroecosystems
Even if the natural-enemy-to-pest ratio
Transgenic cultivars are typically highly remains the same, reduced abundance of
effective against target pests, suggesting that colonists favours pests. Herbivorous pests
natural-enemy populations using these pests colonize crops in advance of the arrival of
as prey or hosts will also suffer great numeri- natural enemies (Price, 1976), allowing them
cal declines. The results of this across agro- to exploit abundant resources unchecked.
ecosystems (space and time) could have at Predators and parasitoids arrive later and
least three unwelcome effects, including: (i) ideally halt the exponential growth of pest
target-pest resurgences or secondary-pest populations, but they typically operate as
outbreaks in non-transgenic cultivars when density-dependant mortality factors. This
large areas of transgenic cultivars are concur- argument overlooks the most obvious prob-
rently grown; (ii) pest epidemics in other lem, that some pests will be unaffected by
non-transgenic crops; and (iii) chronic transgenic insecticidal cultivars, while key
secondary-pest outbreaks in transgenic crops natural-enemy numbers are reduced.
through effects on natural-enemy and pest If the effects of transgenic insecticidal cul-
populations. tivars commonly include those proposed
The potential for pest problems in non- above, then by extension, there will probably
transgenic fields of the same crop is based on be problems throughout the agroecosystem,
the connectivity between fields. Typically, including chronic secondary pest problems
extensive plantings of one annual crop har- in the transgenic cultivars themselves.
bour small, non-independent components of Predator and parasitoid populations are not
mobile pest and natural-enemy metapopula- only linked spatially (among crops), but are
tions (Settle et al., 1996; Kennedy and Storer, related temporally (over seasons), with a
2000). Insecticide treatments in one area may cycle of natural-enemy colonization repeat-
decimate natural enemies there, but mobile ing annually (Wissinger, 1997). The combina-
predators and parasitoids can repopulate tion of pest outbreaks and insecticide
treated fields from nearby untreated ones treatments outside transgenic fields and the
(Wratten and Thomas, 1990). In contrast, recurrent natural-enemy sink caused by
transgenic fields in which high pest and transgenic cultivars could reduce the avail-
natural-enemy mortality occurs represent able natural-enemy pool each year until an
sinks from which little or no recolonization entirely new pest complex emerges, as has
can be expected. Because of the cost:benefit occurred in the past due to overuse of con-
guessing game that can be required to plant ventional insecticides.
transgenic cultivars (Rice and Pilcher, 1998),
some non-transgenic fields will be planted in
Opportunities for IPM in agroecosystems
addition to required refuge plantings. If
insecticides are applied to non-transgenic While the potential for misuse and unin-
fields, insufficient natural enemies may tended side effects of widespread plantings
recolonize these fields, causing pest popula- of transgenic crops unquestionably exists,
tions to significantly increase. transgenic cultivars potentially represent a
Pest epidemics in other crops might also tremendous advance in crop protection. In
result from reduced abundance or diversity the best case, transgenic cultivars offer not
of natural enemies in transgenic fields. If low only a novel tool for managing target pests,
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136 J.S. Bernal et al.

but also a chance to incorporate biological crop cultivars can have unanticipated man-
controls into IPM to an unprecedented level. agement benefits against non-target pests.
Among the possible benefits to agroecosys- Depending on the levels of toxicity against
tems are: (i) a reduction of pest outbreaks these pests, other primary or secondary pests
through conservation of natural enemies; (ii) could be reduced in status or completely
successful area-wide management of mobile, eliminated. For example, Bt cotton cultivars
polyphagous crop pests; and (iii) incidental developed against bollworm, tobacco bud-
control of various susceptible, non-target worm and pink bollworm also showed a lar-
pests. val mortality of > 85% against cabbage
Apart from control of target pests, the looper, Trichoplusia ni (Hübner), salt-marsh
effect most often touted by proponents of caterpillar, Estigmene acrea (Drury), cotton
transgenic insecticidal cultivars is conserva- leaf perforator, Bucculatrix thurberiella Busck,
tion of natural enemies. Insecticidal toxins, and European corn borer. Minor insecticidal
such as those produced by Bt-transgenic cul- effects were also shown against beet army-
tivars, are relatively specific and may reduce worm and fall armyworm, with larval mor-
the overall need for broad-spectrum insecti- tality of 20–25% (Wilson et al., 1992, 1994;
cide applications. With this reduction in Bradley, 1995; Moore et al., 1999).
insecticide applications, predator and para-
sitoid (particularly generalists and those not
dependent on the target pests of transgenic Potential Role in Developing-country
cultivars) populations should increase and Agriculture
be better able to prevent pest outbreaks,
especially of pesticide-induced secondary Developing-country agriculture is character-
pests. When the natural-enemy faunas of ized by a mosaic of production systems,
multiple crops are intimately linked, the ranging from high-input agriculture that
presence of one widely grown transgenic seeks maximum economic returns to subsis-
cultivar could have benefits across the agro- tence agriculture that seeks maximum yields
ecosystem by providing greater numbers of with minimal variance. The former is typical
colonizing natural enemies for other crops. of export and plantation crops (e.g. cotton,
Transgenic cultivars also provide a bananas, tomatoes), whereas the latter is typ-
unique potential to manage mobile, ical of staple crops (e.g. maize, potatoes,
polyphagous pests on an area-wide basis. rice). The focus of this section is on subsis-
Extensive use of transgenic cultivars is tence agriculture, but cotton is included
advantageous for this application because because transgenic cotton cultivars are cur-
extensive plantings can exert continuous rently available and because cotton cultiva-
pressure over both space and time. Area- tion is frequently viewed as a source of
wide control of European corn borer through foreign currency in developing countries and
increased areas planted to Bt cultivars has figures prominently in agricultural develop-
been proposed (Rice and Pilcher, 1998), but ment projects (Murray, 1994).
only potential benefits to maize were consid- Several characteristics of subsistence agri-
ered. However, if few non-crop hosts were culture should be highlighted prior to dis-
available, one or more transgenic crops cussing the potential role of transgenic crop
could eliminate this and other polyphagous cultivars within pest-management strategies.
pests as problems in entire multiple-crop First, capital available to subsistence farmers
agroecosystems. In cases where non-target for investing in crop production in general
pest populations are also reduced by trans- and pest management in particular is limited.
genic cultivars, improved control and Thus, the IPM tactics most readily accessible
reduced outbreaks in other susceptible crops to subsistence farmers are those that do not
(e.g. due to reduced maize earworm move- entail direct economic expenditures.
ment between maize and cotton) could also Biological control by natural-enemy conser-
be realized. vation and plant resistance (exclusive of com-
As alluded to above, the use of transgenic mercial transgenic crops) are both free of cost
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Transgenic Insecticidal Cultivars 137

and fundamental tactics of IPM strategies avoided prima facie. IPM systems that are
and should form the bases of IPM systems in proactive should be developed by seeking
subsistence agriculture. Secondly, subsistence positive interactions between transgenic cul-
agriculture is, by definition, not typically a tivars and biological control. Examples of
major source of income, and subsistence plant resistance mechanisms likely to result
farmers must engage in other activities to in positive interactions between transgenic
procure expendable income (e.g. day labour). cultivars and biological control were dis-
Thus, pest-management tactics that require cussed above. Positive interactions between
minimal time investments will be more transgenic cultivars and biological control
appropriate than and favoured over tactics will contribute to maintaining pest popula-
requiring greater time investments. For tions at low levels, which should minimize
example, the opportunity costs associated the need for remedial control tactics such as
with monitoring pest populations as a basis insecticide applications.
for insecticide applications will detract from Transgenic cultivars have the potential to
the appeal of insecticide-based IPM strategies generate significant benefits for developing-
even when insecticides are a tenable alterna- country agriculture. Among the main benefits
tive. Again, plant resistance and biological lies the potential for reducing pesticide use in
control are especially appropriate because cash crops, such as cotton, which are notori-
they require minimal to nil time investments ous for their reliance on insecticidal control of
by farmers. Moreover, IPM strategies centred major pests. For example, reductions in the
upon insecticidal control tactics may not be numbers of insecticide applications to cotton
appropriate in the context of subsistence have been documented where Bt cotton is
farming. Insecticide use within IPM systems planted in the USA, and similar reductions
is based on the concepts of economic thresh- can be expected in developing countries (ERS-
old and economic injury levels. These con- USDA, 1999; but see Fernández-Cornejo and
cepts are based on the difference between the McBride, 2000). Moreover, transgenic culti-
costs of intervention (i.e. insecticide applica- vars may allow recultivation of crops in areas
tion) and non-intervention (i.e. yield loss due where they were discontinued due to severe
to pests), and may not be useful in the con- pest-management problems. For example,
text of subsistence agriculture because losses cotton production was largely discontinued in
associated with non-intervention are typi- north-eastern Mexico by 1970 and Central
cally not quantified in economic units. America by 1990 following upsets of sec-
It is clear that plant resistance and biolog- ondary pests, including species of Heliothis,
ical control are particularly appropriate tac- Spodoptera and Trichoplusia, and the inability
tics for pest management in subsistence to manage these pests economically based on
agriculture and that they should form the unilateral use of insecticides (DeBach and
bases of IPM strategies in that context. Thus, Rosen, 1991; Murray, 1994). Bt-transgenic cot-
transgenic cultivars have a great potential to ton may significantly contribute to expanding
play significant roles in developing-country cotton production in those and other areas
agriculture. However, it will be crucial that where lepidopteran pests are major factors
the interactions between transgenic cultivars limiting cotton production (e.g. Africa; Silvie
and biological control are closely examined et al., 2001). However, it is uncertain whether
prior to cultivar deployment. Specifically, mere transfer of Bt-transgenic cultivars from
breeding efforts should seek to develop culti- developed to developing countries will lead
vars that interact positively (i.e. synergisti- to substantial benefits in the latter unless
cally) with biological control. This requires locally important pests are targeted and
greater than current degrees of interaction locally adapted crop varieties are trans-
between plant breeders and biological formed. Pest complexes and their susceptibil-
control researchers. Cultivars that have addi- ity to Bt toxins, as well as desirable agronomic
tive interactions with biological control characters, probably differ between most
should be left as second alternatives, while regions.
those with negative interactions should be Transgenic cultivars expressing plant-
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138 J.S. Bernal et al.

derived enzyme inhibitors and lectins are crops is heavily dependent on the use of
particularly promising alternatives to Bt- broad-spectrum insecticides, which has led
transgenic cultivars in developing countries. to serious environmental, ecological and
Unlike Bt-transgenic cultivars, those express- human health problems (McConnell and
ing enzyme inhibitors and lectins are largely Hruska, 1993; Murray, 1994; Thrupp, 1995;
being developed by national and interna- Nicholls and Altieri, 1997). A promising
tional public research institutions and uni- alternative to broad-spectrum insecticides is
versities and thus are more likely to remain the use of Bt-based insecticides, which have
outside the commercial realm. For example, been increasingly employed against cotton
numerous lectin-expressing transgenic crop pests in Central America, starting in the
lines are currently in various stages of devel- 1980s (Murray, 1994). Resistance to Bt toxins
opment and evaluation (Gatehouse et al., could rapidly evolve if Bt-cotton cultivars
1991; Legaspi et al., 2004). Moreover, trans- are widely deployed and planted in Central
genic lines of staple crops of major impor- America, precluding further use of Bt-based
tance in developing countries, such as insecticides in non-traditional export crops
potatoes and rice, are in various stages of and guaranteeing in the short term a contin-
development and numerous genes express- ued heavy dependence on broad-spectrum
ing activity against pests of these crops have insecticides for pest control.
been isolated and are currently being evalu- A number of likely obstacles must be
ated (Gatehouse et al., 1998; Shu et al., 2000; overcome for widespread and sustainable
Machuka, 2001; Legaspi et al., 2004). As dis- use of transgenic cultivars in developing
cussed above, transgenic cultivars express- countries, and these are particularly impor-
ing plant-derived genes are more likely than tant in the case of existing Bt-transgenic culti-
Bt-expressing cultivars to act synergistically vars. One obstacle is the low adoption rate of
with biological control, thus potentially commercial seed varieties in many develop-
decreasing the need for remedial control tac- ing countries. For example, the areas planted
tics, such as insecticide applications. with improved hybrid maize seed in Mexico
Along with the likely benefits derived and Central America are currently below 20%
from deployment of transgenic cultivars in of the total areas planted to maize (Morris
developing countries are potentially impor- and López-Pereira, 1999). Similarly, it
tant disadvantages. A few are briefly dis- remains to be seen whether resistance man-
cussed here in reference to commercially agement programmes, based on non-trans-
available Bt-expressing cultivars. One major genic refuge crops and designed for
concern associated with Bt-transgenic culti- developed-country agriculture, will be
vars in countries where they are available appropriate for developing-country agricul-
commercially is the development of resistant ture. A pervasive feature of subsistence agri-
pest populations (Gould, 1998), and this con- culture is the relatively small size of land
cern should be greater in developing coun- allocations per farmer. It is uncertain whether
tries. In the absence of adequate knowledge land-limited subsistence farmers will be will-
and regulation, transgenic cultivars could ing to set aside a portion of their crop as a
become a transitional technology, available non-transgenic refuge susceptible to high lev-
only as long as resistance development can els of pest damage. Moreover, resistance-
be postponed, which could ultimately lead management programmes require active
to higher levels of pesticide use (Hubbell and industry, government and farmer participa-
Welsh, 1998). For instance, recent develop- tion to be effective. Past failures, despite
ment projects in Central America emphasize strong national and international interests, in
the production of non-traditional export maintaining regional IPM programmes in
crops, such as fruits, vegetables and cut various crops in developing countries caution
flowers (Thrupp, 1995; Nicholls and Altieri, against placing too much confidence in the
1997), while cotton remains an attractive and long-term viability of regional resistance-
potentially important source of foreign management programmes (Holl et al., 1990;
income (Murray, 1994). Production of these Murray, 1994; Thrupp, 1995; Nicholls and
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Transgenic Insecticidal Cultivars 139

Altieri, 1997). Finally, other potential prob- transgenic cultivars should be designed to
lems associated with the deployment of act synergistically with other IPM tactics,
transgenic cultivars in developing countries especially biological control.
relate to the unknown consequences of Some of the major challenges facing trans-
potential gene flow between crops and wild genic-cultivar development in the future
relatives and within crops, and intellectual- stem from the need for developing cultivars
and genetic-property issues. These issues that are compatible with biological control
have been discussed elsewhere and are not and consequently are more likely to be sus-
addressed here (e.g. Shand, 1991; De Souza tainable bases for IPM strategies. A first chal-
Silva, 1995; Bhat, 1999; Ellstrand et al., 1999; lenge will be to develop a sound
King and Eyzaguirre, 1999). Major staple understanding of the interactions between
crops, such as maize, rice, cowpeas and pota- transgenic plants, herbivores and natural
toes, have their centres of origin and genetic enemies, particularly parasitoids and preda-
diversity in developing countries, and there- tors. Moreover, interactions should be stud-
fore it is essential that these issues are ied at the individual, population and
addressed in advance of transgenic-cultivar community levels. This should facilitate the
deployment rather than in retrospect. development of transgenic cultivars that act
synergistically with biological control and
thus are compatible with IPM. A second
Conclusions challenge will be to better understand the
effects of transgenic cultivars on the move-
Transgenic insecticidal cultivars are a novel ment and colonization patterns of herbivore
form of host-plant resistance and, as such, and natural-enemy populations across entire
may play major roles in future IPM strategies agroecosystems. This will facilitate the
in many crops worldwide, in both developed development of regional crop-management
and developing countries. Transgenic culti- strategies that include transgenic cultivars
vars are novel because foreign genes confer and contribute to regional pest-management
their resistance, but host-plant resistance is a efforts by managing the movement and colo-
long-standing and fundamental IPM tactic. nization patterns of pest and natural-enemy
They may play major roles in future IPM populations. Finally, a third challenge will be
strategies because, unlike traditionally bred to develop and deploy transgenic cultivars
insect-resistant cultivars, they rely on genes against major pests of crops that have little
and gene products transferred between commercial potential, such as pests of staple
species, which substantially broadens the crops in developing countries and of low-
opportunities for developing new transgenic value crops in developed countries. One
cultivars. The development of new trans- model which if emulated may prove useful
genic cultivars effective against specific pests is that followed to develop -carotene-rich,
appears limited only by our ability to dis- ‘golden’ rice through joint public and philan-
cover and successfully transfer genes thropic funding, which allowed scientists to
between species. As discussed above, genes develop a (non-insecticidal) transgenic culti-
conferring resistance against all major pests var with little commercial potential in devel-
are probably available because insects as a oping countries (Ye et al., 2000).
group are major herbivores and plants have In conclusion, transgenic cultivars, in gen-
evolved diverse chemical defences against eral, are a valuable tool in our arsenal of
herbivory by insects. However, because of pest-management technologies and therefore
their tremendous promise, it is imperative it is imperative that they are used according
that transgenic cultivars are designed to be to established IPM principles. However,
sustainable. Transgenic cultivars should be recent experiences with commercial Bt culti-
developed within an IPM context, rather vars suggest that basic IPM principles are
than as stand-alone technologies against tar- ignored following deployment of these culti-
get pests because of a number of potential vars: Bt toxins are used prophylactically as a
problems, discussed above. Specifically, first resort, with no regard to established
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140 J.S. Bernal et al.

pest threshold levels, and the control of key in general with biological control, and there-
pests relies on a single tactic. This disregard fore IPM, to be addressed during the devel-
for IPM principles has serious implications opment process so transgenic cultivars are
for the sustainability of these cultivars and designed to be sustainable. Increasing our
for IPM strategies that depend on Bt toxins. understanding of the interactions between
Tacit acceptance that Bt cultivars are being transgenic cultivars and herbivore and
used in a manner that is unsustainable is natural-enemy populations is necessary and
implicit in our deep preoccupation with Bt- urgent in order to develop transgenic culti-
resistance management. It will be imperative vars that play central roles, along with bio-
for the compatibility of transgenic cultivars logical control, within IPM strategies.

References

Adamczyk, J.J., Holloway, J.W., Church, G.E., Leonard, B.R. and Graves, J.B. (1998) Larval survival and
development of the fall armyworm (Lepidoptera: Noctuidae) on normal and transgenic cotton
expressing the Bacillus thuringiensis CryIA(c) δ-endotoxin. Journal of Economic Entomology 91,
539–545.
Anderson, T.E., Kennedy, G.G. and Stinner, R.E. (1984) Distribution of the European corn borer, Ostrinia
nubilalis (Hübner) (Lepidoptera: Pyralidae), as related to oviposition preference of the spring-
colonizing generation in eastern North Carolina. Environmental Entomology 13, 248–251.
Annis, B. and O’Keefe, L.E. (1987) Influence of pea genotype on parasitization of the pea weevil, Bruchus
pisorum (Coleoptera: Bruchidae) by Eupteromalus leguminis (Hymenoptera: Pteromalidae).
Environmental Entomology 16, 653–655.
Arpaia, S., Gould, F. and Kennedy, G.G. (1997) Potential impact of Coleomegilla maculata predation on
adaptation of Leptinotarsa decemlineata to Bt-transgenic potatoes. Entomologia Experimentalis et
Applicata 82, 91–100.
Bell, H.A., Fitches, E.C., Down, R.E., Marris, G.C., Edwards, J.P., Gatehouse, J.A. and Gatehouse, A.M.R.
(1999) The effect of snowdrop lectin (GNA) delivered via artificial diet and transgenic plants on
Eulophus pennicornis (Hymenoptera: Eulophidae), a parasitoid of the tomato moth Lacanobia oleracea
(Lepidoptera: Noctuidae). Journal of Insect Physiology 45, 983–991.
Benrey, B. and Denno, R.F. (1997) The slow growth-high mortality hypothesis: a test using the cabbage
butterfly. Ecology 78, 987–999.
Bernal, J.S. and Sétamou, M. (2003) Fortuitous antixenosis in transgenic sugarcane: antibiosis-expressing
cultivar deters oviposition by herbivore pests. Environmental Entomology 32, 886–894.
Bernal, J.S., Griset, J.G. and Gillogly, P.O. (2002) Impacts of developing on Bt maize-intoxicated hosts on
fitness parameters of a stemborer parasitoid. Journal of Entomological Science 37, 27–40.
Bhat, M.G. (1999) On biodiversity access, intellectual property rights, and conservation. Ecological
Economics 29, 391–403.
Birch, A.N.E., Geoghegan, I.E., Majerus, M.E.N., McNicol, J.W., Hackett, C., Gatehouse, A.M.R. and
Gatehouse, J.A. (1999) Tri-trophic interactions involving pest aphids, predatory 2-spot ladybirds and
transgenic potatoes expressing snowdrop lectin for aphid resistance. Molecular Breeding 5, 75–83.
Board on Agriculture (1989) Alternative Agriculture. National Academy of Sciences, Washington, DC.
Bottrell, D.G. and Weil, R.R. (1995) Protecting crops and the environment: striving for durability. In: Juo,
A.S.R. and Freed, R.D. (eds) Agriculture and the Environment: Bridging Food Production and
Environmental Protection in Developing Countries. American Society of Agronomy, Madison,
Wisconsin, pp. 55–73.
Bottrell, D.G., Barbosa, P. and Gould, F. (1998) Manipulating natural enemies by plant variety selection
and modification: a realistic strategy? Annual Review of Entomology 43, 347–367.
Bradley, J.R. (1995) Expectations for transgenic Bt cotton: are they realistic? In: Herber, D.J. and Richter,
D.A. (eds) Proceedings of the Beltwide Cotton Conference. National Cotton Council of America,
Memphis, Tennessee, pp. 763–765.
Brandenburg, R.L. and Kennedy, G.G. (1982) Intercrop relationships and spider mite dispersal in a
corn/peanut agro-ecosystem. Entomologia Experimentalis et Applicata 32, 269–276.
Brazzle, J.R., Heinz, K.M. and Parrella, M.P. (1997) Multivariate approach to identifying patterns of
Bemisia argentifolii (Homoptera: Aleyrodidae) infesting cotton. Environmental Entomology 26,
995–1003.
06IntpestManCh6.QXD 14/4/04 2:25 pm Page 141

Transgenic Insecticidal Cultivars 141

Cannon, R.J.C. (1996) Bacillus thuringiensis use in agriculture: a molecular perspective. Biological Reviews
71, 561–636.
Chandler, L.D. and Faust, R.M. (1998) Overview of area wide management of insects. Journal of
Agricultural Entomology 15, 319–325.
Couty, A., de la Viña, G., Clark, S.J., Kaiser, L., Pham-Delegue, M.-H. and Poppy, G.M. (2001) Direct and
indirect sublethal effects of Galanthus nivalis agglutinin (GNA) on the development of a potato-
aphid parasitoid, Aphelinus abdominalis (Hymenoptera: Aphelinidae). Journal of Insect Physiology 47,
553–561.
DeBach, P. and Rosen, D. (1991) Biological Control by Natural Enemies. Cambridge University Press,
Cambridge.
De Leo, F., Bonadé-Bottino, M.A., Ceci, L.R., Gallerani, R. and Jouanin, L. (1998) Opposite effects on
Spodoptera littoralis larvae of high expression level of a trypsin proteinase inhibitor in transgenic
plants. Plant Physiolology 118, 997–1004.
De Souza Silva, J. (1995) Plant intellectual property rights: the rise of nature as commodity. In: Peritore,
N.P. and Galve-Peritore, A.K. (eds) Biotechnology in Latin America: Politics, Impacts, and Risks. SR
Books, Wilmington, North Dakota, pp. 57–67.
Devine, G.J., Wright, D.J. and Denholm, I. (2000) A parasitic wasp (Eretmocerus mundus Mercet) can
exploit chemically induced delays in the development rates of its whitefly host (Bemisia tabaci
Genn.). Biological Control 19, 64–75.
Dulmage, H.T. (1981) Insecticidal activity of isolates of Bacillus thuringiensis and their potential for pest
control. In: Burgess, H.D. (ed.) Microbial Control of Pests and Plant Diseases 1970–1980. Academic
Press, London, pp. 193–223.
Ellstrand, N.C., Prentice, H.C. and Hancock, J.F. (1999) Gene flow and introgression from domesticated
plants into their wild relatives. Annual Review of Ecology and Systematics 30, 539–563.
ERS-USDA (1999) Genetically Engineered Crops for Pest Management. Available at http://www.econ.
ag.gov/whatsnew/issues/biotech/
FAO (1967) Report of the First Session of the FAO Panel of Experts on Integrated Pest Control. FAO, Rome.
Federici, B.A. (1999) Bacillus thuringiensis in biological control. In: Bellows, T.S. and Fisher, T.W. (eds)
Handbook of Biological Control. Academic Press, San Diego, California, pp. 575–593.
Feeny, P. (1976) Plant apparency and chemical defence. In: Wallace, J.W. and Mansell, R.L. (eds) Recent
Advances in Phytochemistry, Vol. 10, Biochemical Interaction Between Plants and Insects. Plenum Press,
New York, pp. 1–40.
Fernández-Cornejo, J. and McBride, W.D. (2000) Genetically Engineered Crops for Pest Management in US
Agriculture: Farm-level Effects. Agricultural Economic Report No. 786, Economic Research Service, US
Department of Agriculture, Washington, DC.
Ferro, D.N. and McNiel, J.N. (1998) Habitat enhancement and conservation of natural enemies of insects.
In: Barbosa, P. (ed.) Conservation Biological Control. Academic Press, San Diego, California,
pp. 123–132.
Fitches, E. and Gatehouse, J.A. (1998) A comparison of the short and long term effects of insecticidal
lectins on the activities of soluble and brush border enzymes of tomato moth larvae (Lacanobia oler-
acea). Journal of Insect Physiology 44, 1213–1224.
Gatehouse, A.M.R. and Gatehouse, J.A. (1998) Identifying proteins with insecticidal activity: use of
encoding genes to produce insect-resistant transgenic crops. Pesticide Science 52, 165–175.
Gatehouse, A.M.R., Boulter, D. and Hilder, V.A. (1991) Novel insect resistance using protease inhibitor
genes. In: Dennis, E.S. and Llewellyn, D.J. (eds) Molecular Approaches to Crop Improvement. Springer-
Verlag, Vienna, pp. 63–77.
Gianessi, L.P. and Carpenter, J.E. (1999) Agricultural Biotechnology: Insect Control Benefits. National Center
for Food and Agricultural Policy. Available at: http://www.bio.org/food&ag/bioins01.html
Gill, S.S., Cowles, E.A. and Pietrantonio, P. (1992) The mode of action of Bacillus thuringiensis endotoxins.
Annual Review of Entomology 37, 615–636.
González, D. and Wilson, L.T. (1982) A food-web approach to economic thresholds: a sequence of
pests/predaceous arthropods on California cotton. Entomophaga 27, 31–43.
Gordh, G., Legner, E.F. and Caltagirone, L.E. (1999) Biology of parasitic Hymenoptera. In: Bellows, T.S.
and Fisher, T.W. (eds) Handbook of Biological Control. Academic Press, San Diego, California,
pp. 355–381.
Gould, F. (1998) Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology.
Annual Review of Entomology 43, 701–726.
06IntpestManCh6.QXD 14/4/04 2:25 pm Page 142

142 J.S. Bernal et al.

Gould, F., Kennedy, G.G. and Johnson, M.T. (1991) Effects of natural enemies on the rate of herbivore
adaptation to resistant plants. Entomologia Experimentalis et Applicata 58, 1–14.
Hagen, K.S. (1986) Ecosystem analysis: plant cultivars (HPR), entomophagous species and food supple-
ments. In: Boethel, D. and Eikenbary, R.D. (eds) Interactions of Plant Resistance and Parasitoids and
Predators of Insects. Ellis Horwood, New York, pp. 151–198.
Hagen, K.S., Bombosch, S. and McMurtry, J.A. (1976) The biology and impact of predators. In: Huffaker,
C.B. and Messenger, P.S. (eds) Theory and Practice of Biological Control. Academic Press, New York,
pp. 93–142.
Haggstrom, H. and Larsson, S. (1995) Slow larval growth on a suboptimal willow results in high preda-
tion mortality in the leaf beetle Galerucella lineola. Oecologia 104, 308–315.
Hilbeck, A., Baumgartner, M., Fried, P.M. and Bigler, F. (1998) Effects of transgenic Bacillus thuringiensis
corn-fed prey on mortality and development time of immature Chrysoperla carnea (Neuroptera:
Chrysopidae). Environmental Entomology 27, 480–487.
Hilbeck, A., Meier, M.S. and Raps, A. (2000) Review on Non-target Organisms and Bt-plants. Report to
Greenpeace International, Amsterdam. Ecostrat, Zurich.
Hilder, V.A., Gatehouse, A.M.R., Sheerman, S.E., Barker, F. and Boulter, D. (1987) A novel mechanism of
insect resistance engineered into tobacco. Nature 330, 160–163.
Holl, K., Daily, G. and Ehrlich, P.R. (1990) Integrated pest management in Latin America. Environmental
Conservation 17, 341–350.
Honêk, A. (1982) The distribution of overwintered Coccinella septempunctata L. (Col., Coccinellidae) adults
in agricultural crops. Zeitschrift für Angewandte Entomologie 94, 311–319.
Hoy, C.W., Feldman, J., Gould, F., Kennedy, G.G., Reed, G. and Wyman, J.A. (1998) Naturally occurring
biological controls in genetically engineered crops. In: Barbosa, P. (ed.) Conservation Biological
Control. Academic Press, San Diego, California, pp. 185–205.
Hubbell, B.J. and Welsh, R. (1998) Transgenic crops: engineering a more sustainable agriculture?
Agriculture and Human Values 15, 43–56.
ISAAA (International Service for the Acquisition of Agri-biotech Applications) (2002) Global GM Crop
Area Continues to Grow and Exceeds 50 Million Hectares for First Time in 2001. Available at:
http://www.isaaa.org/press%20release/Global%20Area_Jan2002.htm
Ives, P.M. (1981) Estimation of coccinellid numbers and movement in the field. Canadian Entomologist 113,
981–997.
Jervis, M.A., Kidd, N.A.C., Fitton, M.G., Huddleston, T. and Dawah, H.A. (1993) Flower-visiting by
hymenopteran parasitoids. Journal of Natural History 27, 67–105.
Jesse, L.C.H. and Obrycki, J.J. (2000) Field deposition of Bt transgenic corn pollen: lethal effects on the
monarch butterfly. Oecologia 125, 241–248.
Johnson, M.T. and Gould, F. (1992) Interaction of genetically engineered host plant resistance and natural
enemies of Heliothis virescens (Lepidoptera: Noctuidae) in tobacco. Environmental Entomology 21,
586–597.
Jones, K.D. (1994) Aspects of the biology and biological control of the European corn borer in North
Carolina. PhD thesis, North Carolina State University, Raleigh, North Carolina 127 pp.
Kennedy, G.G. and Storer, N.P. (2000) Life systems of polyphagous arthropod pests in temporally unsta-
ble cropping systems. Annual Review of Entomology 45, 467–493.
Kieckhefer, R.W. and Miller, E.L. (1967) Trends of populations of aphid predators on South Dakota cereal
crops – 1963–1965. Annals of the Entomological Society of America 60, 516–518.
King, A.B. and Eyzaguirre, P.B. (1999) Intellectual property rights and agricultural biodiversity: literature
addressing the suitability of IPR for the protection of indigenous resources. Agriculture and Human
Values 16, 41–49.
Kogan, M., Gerling, D. and Maddox, J.V. (1999) Enhancement of biological control in annual agricultural
environments. In: Bellows, T.S. and Fisher, T.W. (eds) Handbook of Biological Control. Academic Press,
San Diego, California, pp. 789–818.
Koziel, M.G., Carozzi, N.B., Currier, T.C., Warren, G.W. and Evola, S.V. (1993) The insecticidal crystal pro-
teins of Bacillus thuringiensis: past, present and future uses. In: Tombs, M.P. (ed.) Biotechnology and
Genetic Engineering Reviews, Vol. II. Intercept Press, Andover, Massachusetts, pp. 171–228.
Legaspi, J.C., Legaspi, B.C., Bernal, J.S. and Sétamou, M. (2004) Insect resistant transgenic crops express-
ing plant lectins. In: Koul, O. and Dhaliwal, G.S. (eds) Transgenic Crop Protection: Concepts and
Strategies. Science Publishers, New Hampshire.
Lichtenberg, E. and Zimmerman, R. (1999) Adverse health experiences, environmental attitudes, and pes-
ticide usage behavior of farm operators. Risk Analysis 19, 283–294.
06IntpestManCh6.QXD 14/4/04 2:25 pm Page 143

Transgenic Insecticidal Cultivars 143

Losey, J.E., Rayor, L.S. and Carter, M.E. (1999) Transgenic pollen harms monarch larvae. Nature 399, 214.
Luck, R.F., Tauber, M.J. and Tauber, C.A. (1995) The contributions of biological control to population and
evolutionary ecology. In: Nechols, J.R., Andres, L.A., Beardsley, J.W., Goeden, R.D. and Jackson,
C.G. (eds) Biological Control in the Western United States, Accomplishments and Benefits of Regional
Research Project W-84, 1964–1989. Division of Agriculture and Natural Resources, University of
California, Oakland, California, pp. 25–45.
Lynch, R.E., Wiseman, B.R., Plaisted, D. and Warnick, D. (1999) Evaluation of transgenic sweet corn
hybrids expressing CryIA(b) toxin for resistance to corn earworm and fall armyworm (Lepidoptera:
Noctuidae). Journal of Economic Entomology 92, 246–252.
Machuka, J. (2001) Agricultural biotechnology for Africa: African scientists and farmers must feed their
own people. Plant Physiology 126, 16–19.
Margolies, D.C. and Kennedy, G.G. (1985) Movement of the twospotted spider mite, Tetranychus urticae,
among hosts in a corn–peanut agroecosystem. Entomologia Experimentalis et Applicata 36, 193–196.
McConnell, R. and Hruska, A. (1993) An epidemic of pesticide poisoning in Nicaragua: implications for
prevention in developing countries. American Journal of Public Health 83, 1559–1562.
McLaren, J.S. (2000) The importance of genomics to the future of crop production. Pest Management
Science 56, 573–579.
Moore, C.C., Benedict, J.H., Fuchs, T.W., Friesen, R.D. and Payne, C. (1999) Bt Cotton Technology in Texas: a
Practical View. Bulletin B-6107, Texas Agricultural Extension Service, College Station, Texas.
Morris, M.L. and López-Pereira, M.A. (1999) Impacts of Maize Breeding Research in Latin America
1966–1997. CIMMYT, Mexico.
Murray, D.L. (1994) Cultivating Crisis: the Human Cost of Pesticides in Latin America. University of Texas
Press, Austin, Texas.
Neunzig, H.H. (1963) Wild host plants of the corn earworm and the tobacco budworm in eastern North
Carolina. Journal of Economic Entomology 56, 135–139.
Neunzig, H.H. (1969) The Biology of the Tobacco Budworm and the Corn Earworm in North Carolina with
Particular Reference to Tobacco as a Host. Technical Bulletin 196, North Carolina Agricultural
Experiment Station, Raleigh, North Carolina.
Nicholls, C.I. and Altieri, M.A. (1997) Conventional agricultural development models and the persistence
of the pesticide treadmill in Latin America. International Journal of Sustainable Development and World
Ecology 4, 93–111.
NRC (Committee on Pesticides in the Diets of Infants and Children) (1993) Pesticides in the Diets of Infants
and Children. National Academy Press, Washington, DC.
NRC (Committee on Genetically Modified Pest-protected Plants) (2000) Genetically Modified Pest-protected
Plants: Science and Regulation. National Academy Press, Washington, DC.
Pair, S.D., Wiseman, B.R. and Sparks, A.N. (1986) Influence of four corn cultivars on fall armyworm
(Lepidoptera: Noctuidae) establishment and parasitization. Florida Entomologist 69, 566–570.
Pels, B. and Sabelis, M.W. (2000) Do herbivore-induced plant volatiles influence predator migration and
local dynamics of herbivorous and predatory mites? Experimental and Applied Acarology 24, 427–440.
Perkins, J.H. (1982) Insects, Experts, and the Insecticide Crisis: the Quest for New Pest Management Strategies.
Plenum Press, New York.
Perlak, F.J., Deaton, R.W., Armstrong, T.A., Fuchs, R.L., Sims, S.R., Greenplate, J.T. and Fischoff, D.A.
(1990) Insect resistant cotton plants. Bio/Technology 8, 939–943.
Pimentel, D., McLaughlin, L., Zepp, A., Lakitan, B., Kraus, T., Kleinman, P., Vancini, F., Roach, W.J.,
Graap, E., Keeton, W.S. and Selig, G. (1993) Environmental and economic effects of reducing pesti-
cide use in agriculture. Agriculture, Ecosystems and Environment 46, 273–288.
Porter, W.P., Jaeger, J.W. and Carlson, I.H. (1999) Endocrine, immune, and behavioral effects of aldicarb
(carbamate), atrazine (triazine), and nitrate (fertilizer) mixtures at groundwater concentrations.
Toxicology and Industrial Health 15, 133–150.
Poston, F.L. and Pedigo, L.P. (1975) Migration of plant bugs and the potato leafhopper in a
soybean–alfalfa complex. Environmental Entomology 4, 8–10.
Potting, R.P.J., Vermeulen, N.E. and Conlong, D.E. (1999) Active defence of herbivorous hosts against
parasitism: adult parasitoid mortality risk involved in attacking a concealed stemboring host.
Entomologia Experimentalis et Applicata 91, 143–148.
Powell, K.S., Spence, J., Bharathi, M., Gatehouse, J.A. and Gatehouse, A.M.R. (1998)
Immunohistochemical and developmental studies to elucidate the mechanism of action of the
snowdrop lectin on the rice brown planthopper, Nilaparvata lugens (Stal). Journal of Insect Physiology
44, 529–539.
06IntpestManCh6.QXD 14/4/04 2:25 pm Page 144

144 J.S. Bernal et al.

Prasifka, J.R., Krauter, P.C., Heinz, K.M., Sansone, C.G. and Minzenmayer, R.R. (1999) Predator conserva-
tion in cotton: using grain sorghum as a source for insect predators. Biological Control 16, 223–229.
Price, P.W. (1976) Colonization of crops by arthropods: non-equilibrium communities in soybean fields.
Environmental Entomology 5, 605–611.
Price, P.W., Bouton, C.E., Gross, P., McPheron, B.A., Thompson, J.N. and Weiss, J.E. (1980) Interactions
among three trophic levels: influence of plants on interactions between insect herbivores and nat-
ural enemies. Annual Review of Ecology and Systematics 11, 41–65.
Puterka, G.J., Slosser, J.E. and Price, J.R. (1985) Parasites of Heliothis spp. (Lepidoptera: Noctuidae): para-
sitism and seasonal occurrence for host crops in the Texas Rolling Plains. Environmental Entomology
14, 441–446.
Regev, U. (1984) An economic analysis of man’s addiction to pesticides. In: Conway, G.R. (ed.) Pest and
Pathogen Control: Strategic, Tactical, and Policy Models. John Wiley & Sons, New York, pp. 441–453.
Repetto, R. (1985) Paying the Price: Pesticide Subsidies in Developing Countries. World Resources Institute,
Washington, DC.
Rhoades, D.F. and Cates, R.G. (1976) Towards a general theory of plant antiherbivore chemistry. In:
Wallace, J.W. and Mansell, R.L. (eds) Recent Advances in Phytochemistry, Vol. 10, Biochemical
Interaction Between Plants and Insects. Plenum Press, New York, pp. 168–213.
Rice, M.E. and Pilcher, C.D. (1998) Potential benefits and limitations of transgenic Bt corn for manage-
ment of the European corn borer (Lepidoptera: Crambidae). American Entomologist 44, 75–78.
Savinelli, C.E., Bacheler, J.S. and Bradley, J.R. Jr (1986) Nature and distribution of European corn borer
(Lepidoptera: Pyralidae) larval feeding damage to cotton in North Carolina. Environmental
Entomology 15, 399–402.
Savinelli, C.E., Bacheler, J.S. and Bradley, J.R. Jr (1988) Ovipositional preferences of the European corn
borer (Lepidoptera: Pyralidae) for field corn and cotton under field cage conditions in North
Carolina. Environmental Entomology 17, 688–690.
Schnepf, E., Crickmore, N., Van Rie, J., Lereclus, D., Baum, J. and Feitelson, J. (1998) Bacillus thuringiensis
and its pesticidal proteins. Microbiology and Molecular Biology Reviews 62, 775–806.
Schuler, T.H., Poppy, G.M., Kerry, B.R. and Denholm, I. (1999) Potential side effects of insect-resistant
transgenic plants on arthropod natural enemies. Trends in Biotechnology 17, 210–216.
Sétamou, M., Bernal, J.S., Legaspi, J.C. and Mirkov, T.E. (2002a) Effects of snowdrop lectin (GNA)
expressed in transgenic sugarcane on fitness of Cotesia flavipes (Cameron), a parasitoid of the non-
target pest Diatraea saccharalis F. Annals of the Entomological Society of America 95, 75–83.
Sétamou, M., Bernal, J.S., Legaspi, J.C., Mirkov, T.E. and Legaspi, B.C. Jr (2002b) Evaluation of lectin-
expressing transgenic sugarcane against stalkborers (Lepidoptera: Pyralidae): effects on life history
parameters and damage. Journal of Economic Entomology 95, 469–477.
Sétamou, M., Bernal, J.S., Legaspi, J.C. and Mirkov, T.E. (2002c) Parasitism and location of sugarcane
borer hosts by Cotesia flavipes (Cameron) (Hymenoptera: Braconidae) on transgenic and conven-
tional sugarcane. Environmental Entomology 31, 1219–1225.
Settle, W.H., Ariawan, H., Astuti, E.T., Cahyana, W., Hakim, A.L., Hindayana, D., Lestari, A.S. and
Sartanto, P. (1996) Managing tropical rice pests through conservation of generalist natural enemies
and alternative prey. Ecology 77, 1975–1988.
Shand, H. (1991) There is a conflict between intellectual property rights and the rights of farmers in
developing countries. Journal of Agricultural and Environmental Ethics 4, 131–142.
Shu, Q., Ye, G., Cui, H., Cheng, X., Xiang, Y., Wu, D., Gao, M., Xia, Y., Hu, C., Sardana, R. and Altosaar, I.
(2000) Transgenic rice plants with a synthetic cry1Ab gene from Bacillus thuringiensis were highly
resistant to eight lepidopteran rice pest species. Entomologia Experimentalis et Applicata 6, 433–439.
Silvie, P., Deguine, J.P., Nibouche, S., Michel, B. and Vaissayre, M. (2001) Potential of threshold-based
interventions for cotton pest control by small farmers in West Africa. Crop Protection 20, 297–301.
Smith, R.F. and van den Bosch, R. (1967) Integrated control. In: Kilgore, W.W. and Doutt, R.L (eds) Pest
Control: Biological, Physical, and Selected Chemical Methods. Academic Press, New York, pp. 295–340.
Stern, V.M., Smith, R.F., van den Bosch, R. and Hagen, K.S. (1959) The integrated control concept.
Hilgardia 29, 81–101.
Thompson, S.N. and Hagen, K.S. (1999) Nutrition of entomophagous insects and other arthropods. In:
Bellows, T.S. and Fisher, T.W. (eds) Handbook of Biological Control. Academic Press, San Diego,
California, pp. 594–692.
Thrupp, L.A. (1995) Bittersweet Harvests for Global Supermarkets: Challenges in Latin America’s Agricultural
Export Boom. World Resources Institute, Washington, DC.
06IntpestManCh6.QXD 14/4/04 2:25 pm Page 145

Transgenic Insecticidal Cultivars 145

Tomov, B.W., Bernal, J.S. and Vinson, S.B. (2003) Impacts of transgenic sugarcane expressing GNA lectin
on parasitism of Mexican rice borer by Parallorhogas pyvalophagus (Marsh) (Hymenoptera:
Braconidae). Environmental Entomology 32, 866–872.
Turlings, T.C.J. and Benrey, B. (1998) Effects of plant metabolites on the behaviour and development of
parasitic wasps. Ecoscience 5, 321–333.
Umeozor, O.C., Van Duyn, J.W., Bradley, J.R. Jr and Kennedy, G.G. (1986) Intercrop effects on the distrib-
ution of populations of the European corn borer, Ostrinia nubilalis, in maize. Entomologia
Experimentalis et Applicata 40, 293–296.
Vaeck, M., Reynaerts, A., Höfte, H., Jansens, S., De Beuckeleer, M., Dean, C., Zabeau, M., Monatgu, M.V.
and Leemans, J. (1987) Transgenic plants protected from insect attack. Nature 328, 33–37.
Venzon, M., Janssen, A. and Sabelis, M.W. (1999) Attraction of a generalist predator towards herbivore-
infested plants. Entomologia Experimentalis et Applicata 93, 305–314.
Visser, B., Bosch, D. and Honée, G. (1993) Domain function studies of Bacillus thuringiensis crystal pro-
teins: a genetic approach. In: Entwistle, P.F., Cory, J.S., Bailey, M.J. and Higgs, S. (eds) Bacillus
thuringiensis, an Environmental Biopesticide: Theory and Practice. John Wiley & Sons, Chichester, UK,
pp. 71–88.
Vorley, V.T. and Wratten, S.D. (1987) Migration of parasitoids (Hymenoptera: Braconidae) of cereal
aphids (Hemiptera: Aphididae) between grassland, early-sown cereals and late-sown cereals in
southern England. Bulletin of Entomological Research 77, 555–568.
Warren, G.W., Carozzi, N.B., Desai, N. and Koziel, M.G. (1992) Field evaluation of transgenic tobacco
containing a Bacillus thuringiensis insecticidal protein gene. Journal of Economic Entomology 85,
1651–1659.
Wilson, F.D., Flint, H.M., Deaton, W.R., Fischhoff, D.A., Perlak, F.J., Armstrong, T.A., Fuchs, R.L.,
Berberich, S.A., Parks, N.J. and Stapp, B.R. (1992) Resistance of cotton lines containing a Bacillus
thuringiensis toxin to pink bollworm (Lepidoptera: Gelechiidae) and other insects. Journal of
Economic Entomology 85, 1516–1521.
Wilson, F.D., Flint, H.M., Deaton, W.R. and Buehler, R.E. (1994) Yield, yield components, and fiber prop-
erties of insect-resistant cotton lines containing a Bacillus thuringiensis toxic gene. Crop Science 34,
38–41.
Wissinger, S.A. (1997) Cyclic colonization in predictably ephemeral habitats: a template for biological
control in annual crop systems. Biological Control 10, 4–15.
Wraight, C.L., Zangerl, A.R., Carroll, M.J. and Berenbaum, M.R. (2000) Absence of toxicity of Bacillus
thuringiensis pollen to black swallowtails under field conditions. Proceedings of the National Academy
of Science USA 97, 7700–7703.
Wratten, S.D. and Thomas, C.F.G. (1990) Farm-scale spatial dynamics of predators and parasitoids in
agricultural landscapes. In: Bunce, R.G.H. and Howard, C.G. (eds) Species Dispersal in Agricultural
Habitats. Belhaven Press, London, pp. 219–237.
Ye, X.D., Al-Babili, S., Kloti, A., Zhang, J., Lucca, P., Beyer, P. and Potrykus, I. (2000) Engineering the
provitamin A (beta-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science
287, 303–305.
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7 Plant Resistance against Pests: Issues

and Strategies

C. Michael Smith
Department of Entomology, Kansas State University, Manhattan,
KS 66506–4004, USA
E-Mail: [email protected]

Introduction ment. In the USA, insect-resistant sorghum

cultivars increase producer profits by several
The production of crop plants with heritable hundred million dollars each year
arthropod-resistant traits has been recognized (Eddleman et al., 1999). The use of Bacillus
for more than 100 years as a sound approach thuringiensis (Bt) transgenic maize hybrids
to crop protection (Painter, 1951; Smith, 1999). (see below and Fig. 7.1) currently increases
Today, hundreds of arthopod-resistant crop US maize producer profits by approximately
cultivars are grown globally, representing the 7% per year. In Morocco, Hessian-fly-
products of many successful cooperative resistant bread wheats have been shown to
research efforts between entomologists and provide a 9:1 return on investment of
plant breeders. These efforts have signifi- research (Azzam et al., 1997). The economic
cantly improved world food production, value of genetic resistance in wheat to all
helped to alleviate hunger, improved the major worldwide arthropod pests amounts
nutrition of many populations and trans- to more than US$250 million/year (Smith et
formed many food-importing nations into al., 1999). The multiple insect-resistant rice
food exporters. Numerous authors have cultivar IR36 provided approximately US$1
chronicled the development of plant resis- billion of additional annual income to rice
tance as a science and as a valuable tool in producers and processors in Asia for over 20
integrated pest management (IPM) (Snelling, years (Khush and Brar, 1991). The returns on
1941; Painter, 1951; Chesnokov, 1953; Russell, resistant-cultivar research compared with
1978; Lara, 1979; Panda, 1979; Maxwell and insecticides range from 100:1 to 10:1, making
Jennings, 1980; Smith, 1989; Dhaliwal and them a valuable component of crop produc-
Dilawari, 1993; Smith et al., 1994; Panda and tion and greatly improving the competitive-
Khush, 1995; Dhaliwal and Singh, 2004). ness of crop producers in many countries.
Insect resistant-cultivars also provide sub-
stantial environmental benefits and con-
Benefits of Resistance tribute to reduced crop insecticide use and
insecticide residues, thus improving the
Insect-resistant cultivars are highly cost- food, health and safety of consumers. The
effective components of IPM systems, and production of insect-resistant cultivars also
many examples demonstrate how they pro- helps to protect groundwater from pesticide
vide substantial returns on economic invest- contamination.
© CAB International 2004. Integrated Pest Management: Potential, Constraints and Challenges
(eds O. Koul, G.S. Dhaliwal and G.W. Cuperus) 147
07IntpestManCh7.QXD 14/4/04 2:25 pm Page 148

148 C.M. Smith

70
1996
60
Percentage of hectares grown
1997

50 1998

1999
40
2000
30 2001

20

10

0
Cotton Maize

Fig. 7.1. Percentage of cotton and maize cultivars produced in the USA from 1996 to 2001 containing
Bacillus thuringiensis delta endotoxins (from James, 2000; Anon., 2001).

Issues and Strategies: Recent and Future (Thomas), and three Meloidogyne spp. nema-
todes, is the only insect-resistance gene to be
There were three predominant scientific sequenced (Milligan et al., 1998).
issues that affected the thoughts and actions Bioinformatic computational tools to analyse,
of plant-resistance scientists in the decade of interpret and utilize huge amounts of data
the 1990s. These issues were the develop- being generated by genomics research on
ment and deployment of the first transgenic several major crop plants have already pro-
insect-resistant cultivars, the discovery of the vided genetic maps, physical maps and
first molecular markers linked to plant genes expressed sequence tag (EST) complementary
for arthropod resistance and the first cloning DNA (cDNA) libraries of several major crop-
and sequencing of a plant gene expressing plant genomes. Future insect-resistance gene
insect resistance. cloning and sequence determination will
Transgenes from the bacterium, Bt, which probably proceed by ‘data-mining’ the
encode δ-endotoxin insecticidal proteins, genomic information from plant resistance-
were expressed in the first commercial trans- gene analogues (RGAs), defence response
genic cotton, maize and potato cultivars. (DR) genes and EST libraries.
Although controversial, Bt crops are cur- Each of these issues has been researched,
rently marketed and produced in Australia, debated and implemented to varying
Canada, China, India, South Africa and the degrees. In the following sections, informa-
USA. There is a trend towards Bt crops tion is presented to demonstrate how each
becoming more prevalent in global agricul- issue has become or potentially will become
ture. Many other proteins toxic to arthropods a strategy used by many plant-resistance
have been identified and transgenes encod- practitioners in the 21st century.
ing several of these inhibitors have been
used to transform plants expressing insect
resistance. Transgenic Insect Resistance
Molecular markers have been used to map
conventional insect-resistance genes in sev- A major change occurred in the development
eral crops (Yencho et al., 2000). Nevertheless, of insect-resistant varieties near the end of
the Meu-1.2 gene of wild tomato, Lycopersicon the 20th century, when Agrobacterium trans-
peruvianum, which expresses resistance to the formation systems and biolistic projectile
potato aphid, Macrosiphum euphorbiae devices were used to transfer genes encoding
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Plant Resistance against Pests 149

insecticidal crystal (cry) toxins from the soil Initial experiments by Losey et al. (1999)
bacterium Bt into the genome of naïve plant indicated that Bt maize pollen applied at
cells. Transformed plants resulting from cell very high concentrations to leaves of the
and tissue culture were grown to maturity milkweed plant was toxic to larvae of the
and produced transgenic seed. When trans- monarch butterfly, Danaus plexippus
genic plant foliage is fed upon by pest (Linnaeus), feeding on milkweed. Wraight et
insects, ingested crystals are solubilized in al. (2000) reported no mortality of the larvae
the alkaline gut environment, where active of black swallowtail, Papilio polyxenes
toxic fragment(s) are released by insect Fabricius, on food plants located at varying
digestion, and these fragments bind to spe- distances from field plantings of Bt maize, no
cific receptors on the midgut cells of suscep- matter how close the larval food plants were
tible larvae, causing colloid osmotic lysis of to the pollen-shedding Bt maize plants.
those cells, resulting in insect death. Subsequent studies by Sears et al. (2001) and
Numerous other proteins toxic to insects Stanley-Horn et al. (2002) concluded that the
have also been identified and expressed in risk from Bt maize to monarchs is not signifi-
transgenic plants (see reviews by Sharma et cant. One Bt maize cultivar on only 2% of the
al., 2000; Oppert, 2001; Lawrence and annual US crop hectarage was shown to be
Koundal, 2002). These include the carbohy- toxic to monarch larvae and has been elimi-
drate-binding proteins lectins; proteinase nated from production. Pimentel and Raven
inhibitors from maize, potato, rice and (2000) classified the effects of Bt pollen on
tomato; proteinase inhibitors from insects; the food plants of several non-target US but-
chymotrypsin and trypsin inhibitors from terfly species as relatively insignificant, in
cowpea and sweet potato; and α-amylase comparison with maize pesticide applica-
inhibitors from common bean. Transgenes tions and butterfly abiotic mortality factors,
encoding several of these inhibitors have such as habitat destruction. Several studies
been transferred into various crop plants, have shown that Bt maize has limited effects
including bean, cotton, potato and rice. on beneficial arthropods in maize agro-
Despite these impressive accomplishments, ecosystems (Johnson and Gould, 1992;
the general usefulness of transgenic plants Pilcher et al., 1997; Al-Deeb et al., 2001).
containing non-Bt toxic proteins in plant pro- By 1999, the American Phytopathological
tection remains to be implemented. Society proclaimed that threats to human
Many transgenic Bt crop plants have been health were reduced by Bt maize production
developed (see review by Huang et al., 1999), because of reduced incidence of potentially
but only cotton, maize and potato cultivars dangerous mycotoxins (APS, 1999).
with transgenes expressing resistance to Nevertheless, differences in media coverage
Coleoptera and Lepidoptera have been pro- of transgenic crops, European public percep-
duced and marketed. These crops are essen- tions of transgenic crops and greater
tially insecticidal plants, which has European cultural sensitivities about trans-
complicated their deployment. Bt crop-plant genic crops than those of the US public
production and use have met with strong brought out strong European concerns about
opposition by environmentalists, primarily transgenic crops (Gaskell et al., 1999). The
in Europe and the USA. The marketing of concerns resulted in the US government
the first Bt cultivars in 1994 launched an developing an independent scientific
intense scientific debate on how much Bt is approval process for Bt crops and other
sufficient for effectiveness without selecting genetically modified organisms. Public
for pest population resistance to Bt. By 1998, activism peaked between 1999 and 2001,
Bt maize production had increased to when US government and private agricul-
approximately 20% of the US crop and the tural research facilities valued at more than
first Bt educational publications were pub- US$4 million were destroyed by bioterrorists
lished to provide a scientific basis for the in California, Hawaii, Maine, Michigan,
debate (Rissler and Mellon, 1996; Wayland et Minnesota, New York, Oregon, Washington
al., 1998). and Wisconsin. In addition, greenhouse and
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150 C.M. Smith

field experiments involving genetically mod- the deployment of Bt cotton cultivars con-
ified rape, flowers, fruits, maize, oats, tributed to reducing the need for insecticide
onions, trees and wheat were destroyed sprays. Similar results have been reported
(Service, 2001). for bollworm control in South Africa, where
Consumer support for transgenic food Bt cotton use shifted from 7% in the 1997/98
crops in the USA is strong despite these growing season to 90% in the 2001/02 grow-
bioterrorism events. A consumer survey con- ing season on both small and large farms
ducted in August 2002 indicated that 71% of (Kirsten and Gouse, 2002). The primary ben-
the US population favoured purchasing pro- efits have been increased yields from
duce that had been enhanced through improved bollworm control and related
biotechnology, in order for it to be protected decreased production costs from greatly
from insect damage and require fewer pesti- reduced insecticide usage. Sachs et al. (1996)
cide applications (IFIC, 2002). Nevertheless, transformed a high-terpenoid-content cotton
the majority of European countries continue cultivar with the CryIA(b) protein for
to oppose the use of Bt (and other genetically increased resistance to the tobacco bud-
modified) crops. Exceptions are occurring in worm, Heliothis virescens (Fabricius).
several European countries, such as the However, no such conventional gene–
Czech Republic, where Bt maize was field- transgene combinations have been marketed
tested in 2002. commercially.
Improved governmental decision-making Insecticide use against one US insect pest
processes, better genetically modified food of maize, the European corn borer, Ostrinia
risk/benefit communication, an increasing nubilalis (Hubner), has dropped by approxi-
volume of research data and an endorsement mately 30% since after the commercialization
by the United Nations Food and Agriculture of Bt maize in North America. Bt maize has
Organization (FAO) have led to increased proved to be a particularly effective means of
production of Bt cotton and maize in coun- borer control, because larvae feed inside
tries other than the USA, including maize stalks and are impossible to kill by
Argentina, China, India and South Africa conventional foliar insecticide-spray applica-
(see below). In spite of these successes, the tions (Rice and Pilcher, 1998). In contrast,
FAO has voiced concerns that the majority of demand for Bt potatoes resistant to the
transgenic crops focus on reducing chemical Colorado potato beetle, Leptinotarsa decemlin-
inputs and labour costs in large corporate eata (Say), peaked in 1995, when growers
farms of developed countries, and not on planted them on 22,260 ha in North America.
increasing food supplies for the populations By 2000 that hectarage had declined by 50%,
of underdeveloped countries. To date, there and in 2001 sales of Bt potato seed ceased in
has been little corporate or public investment the USA and Canada, primarily because
in important food crops of the semi-arid food-processing companies were concerned
tropics, such as sorghum, millet, pigeon pea, about consumer food preferences and reluc-
chickpea or groundnut. tantly chose not to market transgenic foods.
Over the past several years, farm trials in The successes of Bt maize and cotton
India show Bt cotton yield increases of globally in both developed and several
approximately 60% more than those of con- developing countries, as well as the lack of
ventional non-Bt cultivars (Qaim and success of Bt potatoes, point to the critical
Zilberman, 2003). In 2001, more than a quar- importance of risk communication in devel-
ter of the maize produced in the USA, and oping consumer and producer understand-
over half of the cotton produced was from ing of new technologies. Abbott et al. (2001)
planting of Bt cultivars (Anon., 2001; Fig. have shown that the media coverage of the
7.1). Data from a 10-year study conducted by development and use of Bt maize has fol-
Carrière et al. (2003) in Arizona indicate that lowed a predictable pattern similar to that of
production of Bt cotton significantly sup- many other risk issues. The pattern is one in
pressed populations of the pink bollworm, which scientific developments are initially
Pectinophora gossypiella Saunders, and that communicated by the media to the public in
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Plant Resistance against Pests 151

a positive way, albeit at low levels, and to demonstrate how certain perceived risks
research and industry sources are stressed, are in fact not significant.
without perceptions of public advocacy The history of the scientific development
groups. A ‘triggering event’, in the case of Bt of Bt-crop technology is much less compli-
maize the initial Losey et al. (1999) data, cated, although at some points involving
caused a dramatic increase in media cover- controversy. Before the development of Bt
age. These events allow increased inclusion transformants, numerous studies deter-
of information from advocacy groups, who mined that insects became resistant to the cry
elect (in the case of Bt) to exploit negative toxin gene after prolonged exposure to a
scientific data, both real and perceived. A high dose of Bt (Huang et al., 1999), in the
trend to report ‘for and against’ information same manner that insect biotypes develop
rather than scientific truth follows, deluging resistance to high doses of conventional pes-
the public with conflicting information in a ticides or high levels of conventional gene
short period of time. Public attention to these expression (Llewellyn et al., 1994). Insect bio-
sources then declines as other issues come types are well documented in the interac-
forward or new information is publicized. tions between genes of the gall midge,
The current US–European dichotomy over Orseolia oryzae (Wood-Mason), and brown
the acceptance of biotechnology illustrates planthopper, Nilaparvata lugens (Stal), and
this point well, with the perceived benefits of rice (Tanaka, 1999; Pani and Sahu, 2000) and
Bt crops allowing US consumer acceptance the Hessian fly and wheat (Ratcliffe and
and the perceived detriments continuing Hatchett, 1997). Biotype occurrence is influ-
European rejection of them. enced by the genetic plasticity of the pest
Future transgenic-technology education insect, its ecological fitness, the number of
and risk communication efforts may benefit resistance genes expressed, the resistance
from integrating the educational capabilities category expressed, the fraction of the crop
of different agencies involved in food pro- cultivated in an insect-resistant cultivar and
duction, processing and distribution. Such the overall efficacy of the IPM programme
initiatives are illustrated by the development used to control the pest.
of the International Food Information Some of these same concepts have been
Council- and the US Environmental used to develop Bt crop-plant deployment
Protection Agency (EPA)-led development of strategies. In order to obtain their maximum
Bt integrated risk-management programmes longevity, Bt insect-resistant transgenes in
(see below). maize and cotton are deployed with non-Bt
In order for transgenic-crop risk-assess- plant ‘refuges’ that enable the survival of
ment training to be effective, however, edu- pest moths from susceptible larvae to mate
cators may consider using hazard analysis with moths produced from larvae resistant
critical control point (HACCP) principles, to Bt. Shifting the mortality of larvae het-
described by Cuperus et al. (1991) for use in erozygous for resistance from 50 to 95% pro-
food-safety education. HACCP principles vides a tenfold delay in time before the
have been used extensively to reduce development of resistance (Gould, 1998). A
microbiological contamination in the food- refuge portion of the crop was not commer-
processing industry. The HACCP approach cially or sociologically acceptable at first,
assesses hazards and risks associated with but the US EPA coordinated industry and
growing, harvesting, processing, manufac- academic research efforts to establish a
turing, marketing and distribution of food mechanism to prevent the development of
products and determines critical control resistance to Bt by key maize insect pests.
points (CCPs) (a point where loss of control In 2001, these efforts led to the creation of
may result in an unacceptable health risk). an insect resistance management (IRM) com-
For a given CCP, critical limits are identified, pliance assurance programme to promote
monitoring procedures are established and grower compliance and preserve the effec-
corrective actions are taken if necessary. tiveness of Bt maize. Manufacturers sponsor
Application of HACCP principles may serve an annual survey of Bt maize growers, con-
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152 C.M. Smith

Table 7.1. Comparisons of conventional and transgenic resistance in crop plants (from Daly and
Wellings, 1996).

Criteria Conventional Transgenic

Resistance category Antibiosis, antixenosis, tolerance Antibiosis

Mechanism(s) Chemical and physical Chemical
Efficacy Moderate High
Expression Constitutive and induced Constitutive
Management Optional Required
Sociology Simple Complex
Stability High High
Technology transfer Moderate Fast

ducted by an independent third party, and cal mechanisms have been identified to
growers not in compliance with IRM require- explain resistance (Smith, 1989). Transgenic
ments over 2 consecutive years are denied resistance is expressed solely as antibiosis,
additional access to Bt-maize seed. Bt-crop due to a digestive toxin. While conventional
producers must plant at least a 20% non-Bt resistance may have both constitutive and
maize refuge, except in certain cotton-grow- induced components, transgenic resistance is
ing areas, where at least a 50% non-Bt maize fully constitutive. Both types of resistance
refuge is required. Refuge-planting options genes have high stability and, although
include blocks within fields, strips across transgenes have been part of IPM systems
fields or separate fields. Bt-maize fields must for less than 10 years, the transfer of trans-
be planted within 0.8 km of a refuge. The genic technology has occurred very quickly.
IRM programmes are a first ever type of The major difference in the two types of
government–industry-regulated IPM tecnol- resistance genes is the management (IRM)
ogy. As such, US crop-management pro- plan for transgenes. Although the initial IRM
grammes relying on transgenic technology schemes for Bt maize are functional, we do
have entered a new era in crop production. not know if they will continue to be effective.
The IRM programmes are an overall success, Bt maize with resistance to the western
although some producers have failed to meet maize rootworm, Diabrotica virgifera
the minimum requirements for non-Bt refuge LeConte, a far more damaging pest than the
plantings. In an initial 2000 survey, 29% of European corn borer, has recently been
producers were not in compliance, but since approved by the US EPA (Knight, 2003). A
that time participation has improved. In 2001 20% refuge similar to that for European corn
only 13% of the producers surveyed were borer has been adopted for initial production
not in compliance and in 2002 14% were purposes, but an advisory panel had recom-
non-compliant (Byrne et al., 2003). The con- mended a much larger 50% refuge to suffi-
tinued (and improved) successes of these ciently dilute Bt virulence alleles in
producer–regulatory–industry partnerships surviving maize rootworm larvae. European
will depend on a combination of good sci- corn borer-resistant Bt-maize cultivars pro-
ence, communication and common sense in duce high doses of toxin, but the rootworm-
making decisions about Bt-crop cultivar resistant maize cultivars cause only 50%
selection and refuge composition. rootworm larval mortality. This reduced
Daly and Wellings (1996) contrasted maize rootworm Bt efficiency and decreased
aspects of conventional and transgenic plant refuge size may lead to a different outcome
resistance to insects (Table 7.1). Conventional for maize rootworm-resistant Bt maize from
plant resistance genes are expressed as that currently developing for Bt cultivars
antibiosis or antixenosis effects on insects resistant to lepidopterous larvae. If the
and tolerance of the resistant cultivar to an Lepidoptera IRM schemes (and others) con-
insect pest. Many biochemical and biophysi- tinue to function successfully, they may
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Plant Resistance against Pests 153

serve as workable models for the deploy- occurs between the resistance gene and the
ment of conventional plant resistance genes marker during meiosis, and the gene and
that are expressed as high levels of antibiosis marker are always linked together from one
(insect mortality), in order to delay the generation to another. They may be incom-
development of resistant biotypes. pletely linked and crossing over may occur
between the gene and the marker during
meiosis. They may have no linkage, because
Molecular Marker-assisted Selection of the gene and the marker are located on dif-
Plant Genes for Insect Resistance ferent chromosomes or are far apart on the
same chromosome. Estimates of the recombi-
The tagging and mapping of plant genes for nation between the resistance gene and a
insect resistance has accelerated tremen- linked marker are measured as the recombi-
dously since the mid-1990s. This progress nation frequency (RF). RF values are mea-
has been facilitated by the construction of sured among segregating F2 plants or F2:3
high-density genetic maps of barley, maize, families by matching the phenotype and
rye, soybean and wheat (Cregan et al., 1999; genotype of each progeny and subjecting the
Hernández et al., 2001; Korzun et al., 2001; paired data to MAPMAKER (Lander et al., 1987),
Boyko et al., 2002; Sharopova et al., 2002). an interactive computer package for calculat-
Yencho et al. (2000) reviewed molecular ing genetic distance and constructing
markers in many of these same crops linked genetic-linkage maps. The linkage between
to genes expressing resistance to several QTLs and marker loci is determined by the
major insect pests. In the premolecular age of way distribution patterns for the resistance
plant resistance to insects, phenotypic evalu- character(s) are linked with the segregation
ations determined the initial identity of a of the resistance gene and the molecular
source of resistance or progeny from crosses marker at each locus.
made between resistant and susceptible par-
ents. The marker-assisted selection (MAS) of
plants based on genotype, before the pheno- Why molecular markers?
typic trait for resistance is expressed, is now
being used in many plant-improvement pro- Many practitioners ask ‘Why use molecular
grammes. markers?’, given the additional time and
Demonstrating that a molecular marker is labour required to define a molecular marker
linked to a plant resistance gene, however, linked to an insect resistance gene. The
involves identifying a phenotypic source of answer lies in the fact that there are several
resistance, isolating DNA from resistant and advantages to adopting this technology.
susceptible parent plants, hybridizing or Restriction fragment length polymorphism
amplifying DNA of resistant and susceptible (RFLP) markers and microsatellite or simple-
plants with molecular markers from known sequence repeat (SSR) markers (see below)
chromosome locations to identify those that behave in a codominant manner to detect
differentially hybridize or amplify DNA in a heterozygotes in segregating populations of
polymorphic (informative) pattern via gel progeny from crosses between resistant and
electrophoresis, and genotypically screening susceptible parents. In contrast, morphologi-
individual plants from segregating popula- cal markers behave in a dominant/recessive
tions for linkage to putative molecular mark- manner and do not detect heterozygotes
ers. Molecular markers have been identified (Staub et al., 1996). In general, the allelic vari-
that are linked both to single major genes for ation detected by molecular markers in nat-
resistance and to groups of loci controlling ural plant populations is considerably
the expression of quantitative resistance, greater than that detected by morphological
known as quantitative trait loci (QTLs). markers. Molecular markers are unaffected
Linkages of a resistance gene and a mole- by environment and thus phenotype-neutral,
cular marker may vary greatly. They may be while several examples exist to indicate that
completely linked, where no crossing over morphological markers are highly affected
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154 C.M. Smith

by environmental variations (see review by commercialization of PCR resulted in the

Smith, 1999). Finally, morphological markers thermal cycler, in which PCR primers of
may interact epistatically and molecular known chromosome location are reacted
markers do not, which greatly increases the with template DNA, and the amplification
number screened in a single population. products are electrophoresed to identify
primers (markers) yielding polymorphisms.
Compared with RFLP hybridization, PCR
Types of molecular markers reactions are much faster (2–3 h) and non-
radioactive. However, compared with many
Several types of molecular markers have RFLP genomic maps, there are fewer PCR
been used to determine the locations of primers.
insect-resistance genes. They include RFLP Several types of PCR primers identify
markers, mentioned previously, sequence- insect-resistance genes in plants. RAPD PCR
tagged site (STS) markers, random ampli- primers are short random DNA sequences
fied polymorphic DNA (RAPD) markers, that alone do not reveal heterozygotes and
amplified fragment length polymorphism chromosome-linkage information per se.
(AFLP) markers and SSRs or microsatellite However, RAPD-generated DNA polymor-
markers. RFLP markers detect differences phic bands can be end-sequenced to de-
between genotype DNA when restriction sign location-specific sequence-characterized
enzymes cut genomic DNA at specific amplified regions (SCARs). SCARs have
nucleotide sequences (binding sites) to yield been used to identify and map genes for
variable-size fragments of DNA base pairs. resistance to the rice gall midge, O. oryzae
The digested DNA is electrophoresed and (Sardesai et al., 2001), and the brown plant-
transferred to a nylon membrane via hopper, N. lugens (Renganayaki et al., 2002).
Southern blotting, and the membrane is AFLPs are based on the selective PCR
probed with a 32P–labelled dinucleotide amplification of restriction enzyme-digested
sequence of known chromosome location. DNA fragments, as in RFLP analysis (Vos et
The membrane-bound DNA is denatured by al., 1995). However, the DNA bands gener-
heat, allowing probe sequences to bind with ated in each amplification contain DNA
complementary sites in the restriction markers of random origin, which result in
digest and providing information about the many more amplified DNA bands. AFLP
putative location of the resistant gene. RFLP markers have been used successfully to iden-
probes allow very fine mapping of loci tify insect-resistance genes in apple, rice and
linked to resistance genes, since initially wheat (Murai et al., 2001; Cevik and King,
they were more numerous in some crop 2002; Weng and Lazar, 2002).
genomes than other types of molecular SSR or microsatellite primers are tandem
markers. Disadvantages of RFLP linkage arrays of 2–5 base repeat units (particularly
analysis include the time required to com- dinucleotide repeats), which have been
plete (7–10 days) and the use of radioactive found to be widely distributed in eukaryotic
isotopes. RFLP analysis has been used to DNA. Microsatellite primers have proved to
map insect-resistance gene loci in barley, be very useful in crops where they have been
cowpea, mung bean, sorghum, rice and developed, such as maize, soybean and
wheat (Moreira et al., 1999; Smith, 1999; wheat. As a result of a rapidly expanding
Huang et al., 2001; Katsar et al., 2002; Xu et library of microsatellite markers, SSRs are
al., 2002). being used with increasing frequency to
DNA analysis was revolutionized with identify and map genes for insect resistance
the discovery of the polymerase chain reac- in wheat (Liu et al., 2001, 2002; Miller et al.,
tion (PCR) technique (Mullis, 1990). PCR 2001). STS markers – PCR markers
allows the in vitro enzymatic amplification of sequenced from ends of RFLP sequences –
specific DNA sequences present between have been used to map genes for insect resis-
two convergent oligonucleotide primers tance in barley (Nieto-Lopez and Blake,
hybridizing to opposite DNA strands. The 1994) and rice (Katiyar et al., 2001).
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Plant Resistance against Pests 155

MAS of plants is accelerating the accuracy of QTL analysis makes conventional selec-
and rate at which a resistance gene can be tion more cost effective.
tracked in the development of arthropod-
resistant cultivars. There are few compar-
isons of the efficiency of MAS of resistant Cloning and Sequencing Plant Resistance
plants with phenotypic selection. MAS of Genes
genes for Russian wheat aphid, Diuraphis
noxia Mordvilko, resistance in wheat and The examples described above demonstrate
cereal cyst nematode, Heterodera avenae Woll. how plant resistance to insects is mediated
resistance in barley can be accomplished by constitutive gene effects. As mentioned
approximately 30 times faster for approxi- previously however, the only insect-resis-
mately 75% more cheaply per evaluation tance gene identified to date is the Meu1.2
compared to plant phenotypes (Kretshmer et gene from wild tomato, L. peruvianum, which
al., 1997; C.M. Smith and X.E. Liu, unpub- confers resistance to the potato aphid, M.
lished). A US MAS genotyping centre for euphorbiae (Kaloshian et al., 1995, 1997; Rossi
barley and wheat is developing QTLs linked et al., 1998; Vos et al., 1998) and to three
to resistance for fusarium head blight, species of the root-knot nematode,
caused by Fusarium graminearum Schwabe Meloidogyne spp. (Roberts and Thomason,
(teleomorph Gibberella zeae (Schwein.)), in 1986). Meu1.2 is a member of the nucleotide-
order to genotype plants in breeding popula- binding site–leucine-rich region (NBS–LRR)
tions (Van Sanford et al., 2001). family of disease- and nematode-resistance
QTL analysis has successfully identified genes (Milligan et al., 1998). The LRR region
loci containing insect-resistance genes in of Meu1.2 functions to signal localized cell
maize (Cardinal et al., 2001; Jampatong et al., death and programmed cell death (Hwang et
2002), rice (Huang et al., 1997, 2001; Xu et al., al., 2000; Wang et al., 2001). Similarities in the
2002), soybean (Rector et al., 1998, 2000), sequence and function of other pest-
tomato (Moreira et al., 1999) and wheat resistance genes are beginning to show pat-
(Castro et al., 2001). Narvel et al. (2001) used terns. RGA sequences (see below) from barley
SSR markers to assess US soybean breeding map to loci in regions involved in resistance
lines and cultivars developed over a 30-year to the maize leaf aphid, Rhopalosiphum maidis
period using conventional phenotypic selec- (Fitch). These same sequences are similar to
tion for resistance to foliar feeding by sev- the wheat NBS-LRR Cre3 gene for resistance
eral Lepidoptera. Although some resistance to the cereal cyst nematode, H. avenae
has been transferred, very few minor resis- (Lagudah et al., 1997). Other NBS–LRR-
tance QTLs have been transferred. MAS has related sequences have also been mapped to
been used to develop near-isogenic soybean regions controlling resistance to the melon
lines with multiple insect-resistant QTLs, aphid, Aphis gossypii Glover (Brotman et al.,
suggesting that the use of MAS in soybean is 2002).
justified. Extensive research comparing the
use of conventional selection of phenotypic
resistance in maize to feeding damage by Functional genomics
the southwestern corn borer, Diatraea
grandiosella Dyar, to QTL mapping of During the past decade, the genomes of
resistance-gene loci suggests that QTL-MAS Arabidopsis and rice were sequenced, open-
and conventional selection methods are ing huge opportunities for in-depth studies
equivalent in their ability to improve the of the molecular bases of plant resistance.
level of resistance (Willcox et al., 2002). The sequencing of extremely large genomes
Although the cost of MAS alone is approxi- such as wheat, however, remains well in the
mately one-tenth the cost of conventional future. In the interim, plant resistance
selection, the accurate identification of QTL researchers are data-mining information
position and the cost of generating these ini- about Arabidopsis and rice gene sequence,
tial data as the first step in the MAS process function, and expression, in order to provide
07IntpestManCh7.QXD 14/4/04 2:25 pm Page 156

156 C.M. Smith

new information about the biochemical and knowledge of the chromosome locations and
physiological pathways involved in the genome organizations of RGAs in wheat and
resistance of other plants to insects. other crops will be of great value in candi-
RGAs are conserved amino acid motifs date resistance-gene analyses.
(such as NBS and LRR motifs) derived from The genomes of cereal crops, such as bar-
sequence comparisons of predominant ley, maize, rice, rye, sorghum and wheat, are
classes of insect-, disease-, and nematode- highly conserved, i.e. the arrangement of
resistance genes. RGAs have been isolated in many of the genes in a region of a chromo-
Arabidopsis, barley, lettuce, maize, rice, soy- some of one species is similar to that of a
bean and wheat (Seah et al., 1998; Shen et al., chromosome region of another plant species
1998; Speulman et al., 1998; Leister et al., in DNA sequence (Ahn et al., 1993; Paterson
1999; Mago et al., 1999; Tada, 1999; Graham et et al., 1995; Boyko et al., 1999). Resistance-
al., 2000). Many cereal-crop RGAs map to gene maps in barley, sorghum, rice and
orthologous positions in different cereal wheat demonstrate the synteny among loci
species. The fact that Meu-1.2 and Mi are of these crops linked to genes expressing
active against two organisms as distantly resistance to several species of pest aphids
related as aphids and nematodes supports and planthoppers (Fig. 7.2). The exploitation
the hypothesis that RGAs can also be used to of such conserved gene order to identify
clone or design genes for insect resistance in pest-resistance loci of interest will greatly
crops. Map positions of RGAs in the Triticeae stimulate efforts to clone insect-resistance
indicate that these genes occur in clusters genes in cereals and other crops as functional
and are more closely linked physically than genomics becomes more of a reality in agri-
those in other regions with similar genetic cultural research. For example, using synte-
distances (Feuillet and Keller, 1999; Li et al., nous areas of barley, rice and wheat
1999; Boyko et al., 2002). For this reason, chromosomes where resistance genes have

Ssg 69
Gb 610 Dn 1, 2, 5, 6, 8, x7,8
Dn 47 Gby2
Ssg 1, 2, 96 Gb3,5
QBph513 QBph1
QBph1113

Grh11
Ssg 86

Dn 98 Dn 29
Gb 312
Gb 54
Gb x14
Gb z14
QBph113
Triticeae Triticeae
Homoeologous Group 1 Homoeologous Group 7

Fig. 7.2. Map positions of Heteroptera-resistance gene loci in barley, rice, sorghum and wheat on Triticeae
homoeologous chromosome groups 1 and 7 (relative loci positions for illustration only, not ordered). Gb,
greenbug, Schizaphis graminum (Rondani), resistance gene in wheat; Dn, Russian wheat aphid, Diuraphis
noxia (Mordvilko), resistance gene in wheat; Ssg, greenbug-resistance gene in sorghum; QBph, main effect
brown planthopper, Nilapartava lugens (Stal), resistance QTL in rice; Grh, green rice leafhopper, Nephotettix
cincticeps (Uhler), resistance gene in rice. 1Alam and Cohen, 1998; 2 Boyko et al., 2002; 3Castro et al.,
2001; 4 Dubcovsky et al., 1998; 5 Moharramipour et al., 1998; 6 Katsar et al., 2002; 7 Liu et al., 2002; 8 Liu et
al., 2001; 9 Miller et al., 2001; 10 C.M. Smith and S. Starkey, unpublished; 11 Tamura et al., 1999; 12 Weng
and Lazar, 2002; 13 Xu et al., 2002; 14 L. Zhu, C.M. Smith, E. Boyko and S. Starkey, unpublished.
07IntpestManCh7.QXD 14/4/04 2:25 pm Page 157

Plant Resistance against Pests 157

been mapped, specific candidate rice bacter- 7.3), were expressed at significantly
ial artificial chromosome (BAC) contiguous increased levels.
segments can be subjected to in silico analy- Complementary DNA libraries can also
ses to identify sequences similar to those of be probed with molecular markers of known
known resistance genes. genome function and location, in order to
determine the degree of involvement of the
expressed gene(s) in resistance. Finally,
Expressed plant resistance genes unique cDNAs can be used to probe oligonu-
cleotide microarrays (gene chips) as a means
Plants use both constitutive and induced of determining resistance-gene function
defences to protect themselves from insect based on mRNA expression levels.
attack. From a plant-breeding standpoint, Commercial oligonucleotide microarrays
plant resistance genes are viewed as consti- now allow rapid screening of plant cDNAs
tutively active (always transcribed) in order expressing potential resistance, with over
to identify them in breeding programmes. 14,000 expressed Arabidopsis thaliana
With the advent of cDNA technologies, how- sequences. Reymond et al. (2000) constructed
ever, information about plant genes a small-scale microarray of 150 ESTs impli-
expressed in reaction to disease and insect cated in Arabidopsis defence to demonstrate
attack has exploded, with more than 3000 differences in genes activated by Pieris rapae
articles published since 1995 (see reviews of (Linneaus) feeding, mechanical wounding,
Walling, 2000; Kessler and Baldwin, 2001; and water stress. Several hundred thousand
Heil and Bostock, 2002). When plant tissues cereal cDNA ESTs are currently being
are damaged, messenger RNA (mRNA) sig- produced publicly for macro- or micro-
nals are translated to proteins. Unique arrays that will soon allow searches for
mRNA gene transcripts expressed in resis- expressed genes related to or involved
tant plants can now be identified by reverse in insect resistance in cereal crops
transcription, where an RNA molecule is (http://www.ncbi.nlm.nih. gov/dbEST/).
copied back into its cDNA by reverse tran-
scriptases. cDNA populations from infested
and uninfested plants can be subjected to Insect-resistance elicitors
subtractive suppressive hybridization to
remove the hybridized sequences common Plant reactions to both insect and disease
to both populations. The unhybridized attack may include hypersensitive cell death,
sequences unique to the resistant plant then as in the case of Meu1.2, activation of DR
become a ‘subtracted’ library of resistant genes and the redirection of normal cell-
cDNAs, which is then sequenced to deter- maintenance genes to plant defence. In DR-
mine the function of the putative resistance gene activation, plants produce elicitors that
genes. Several studies of expressed insect- activate plant gene expression and the syn-
resistance genes are currently in progress. thesis of volatile and non-volatile allelo-
Messenger RNA differential display, a chemicals. The similarities of plant elicitors
related technique, was used by Hermsmeier in response to attacks by different insect
et al. (2001) to study Nicotiana attenuata species may be the result of common insect
responses to feeding by tobacco hornworm, salivary enzymes, although some elicitors
Manduca sexta (Johannsen), in the first exper- regulate very insect species-specific
iment to identify mRNA transcripts pro- responses (van de Ven et al., 2000; Walling,
duced after insect attack. Over 500 genes 2000). In addition, chewing insects cause
were involved in plant response, and 27 extensive plant-tissue damage, which elicits
were verified as differentially expressed and different plant responses from those induced
sequenced. Transcripts encoding a Thr in response to feeding by piercing/sucking
deaminase gene and a pathogen-inducible insects, which cause comparatively less tis-
α-dioxygenase gene (see below), both sue damage (Fidantsef et al., 1999; Stout et al.,
involved in the plant defence response (Fig. 1999; Walling, 2000). Plant responses to
07IntpestManCh7.QXD 14/4/04 2:25 pm Page 158

158 C.M. Smith

Insect-feeding injury
plant membrane lipids
phospholipases
salicyclic acid
O2 + α-linolenic acid
α-dioxygenase (PIOX) peroxidases
lipoxygenases (LOX2), (LOX-H3)
β-1,3 glucosidase (BGL2) fatty acid peroxides
pathogen-response gene (PR-1) hydroperoxide lyase (HPL) unknown, non-JA signal

12-oxododecenoic acid (traumatin)

allene oxide synthase (AOS) hexenal, 3-hexenal

12-oxo-phytodienoic acid (12-OPDA)

OPDA reductase
jasmonic acid (JA), methyl jasmonate (MeJA) ?

defensin peptide (PDF1.2)

β-glucosidase (BGL1)
hevein-like protein (HEL)
hydroxamic acids
monosaccharide H+ symporter (STP4)
metallopeptidase-like protein (SLW-1)
peroxidases, chitinases, polyphenol oxidases β-glucosidase-like protein (SLW-3)
phenolics and polymers
phenylalanine ammonia lyase (PAL1)
Thr deaminase (TD)
proteinase inhibitors
vegetative storage proteins (VSP1, 2)

Fig. 7.3. A generalized diagram of known induced plant-resistance elicitors, genes and gene products
produced by insect damage to plant tissues. Substrates shown in shaded grey boxes, enzymes in between.
Italics indicate gene(s) expression of compounds involved in insect resistance. For detailed explanations, see
individual references (Bergvinson et al., 1994; Bell et al., 1995; Lee et al., 1997; Botha et al., 1998; Fidantsef
et al., 1999; Royo et al., 1999; Stout et al., 1999; Forslund et al., 2000; Reymond et al., 2000; Stotz et al.,
2000, 2002; van de Ven et al., 2000; Walling, 2000; Halitschke et al., 2001; Hermsmeier et al., 2001; Kessler
and Baldwin, 2001; Moran and Thompson, 2001; Slesak et al., 2001; Vancanneyt et al., 2001.)

mechanical damage also differ from those Lipoxygenases involved in cell membrane
involved in response to feeding damage lipid degradation contribute to the produc-
(Botha et al., 1998; Forslund et al., 2000; tion of jasmonic acid (JA) signals. Transcripts
Halitschke et al., 2001; Winz and Baldwin, encoding LOX and LOX2 genes have been
2001). shown to be strongly induced by feeding of
When insects damage plant tissues dur- the potato aphid, M. euphorbiae, on tomato
ing feeding, the death of tissues results in the (Fidanstef et al., 1999) and the green peach
production of an oxidative ‘burst’. This event aphid, Myzus persicae (Sulzer), feeding on
triggers the degradation of linolenic acid, Arabidopsis (Moran and Thompson, 2001).
which involves elicitors that signal the need LOX H3 genes in potato regulate resistance
of the production of allelochemical plant to the beet armyworm, Spodoptera exigua
defences, such as proteinase inhibitors, phe- (Hubner), and Colorado potato beetle, but
nolics and enzymes involved in the eventual the resistance is not regulated by JA produc-
production of plant structural defences (Fig. tion (Royo et al., 1999). The related enzyme
7.3). hydroperoxide lyase plays a role in the resis-
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Plant Resistance against Pests 159

tance of potato to the green peach aphid Hermsmeier et al. (2001) found that N. atten-
(Vancanneyt et al., 2001). In some plants, uata plants fed on by tobacco hornworm
wounding also induces increased ethylene were strongly induced to produce high
production, which blocks the JA signal but amounts of transcripts encoding the gene for
induces allene oxide synthase (AOS) produc- α-dioxygenase (PIOX), a pathogen-inducible
tion. Increased AOS levels induced by plant enzyme. The same plants expressed
tobacco hornworm feeding are thought to high levels of Thr deaminase (TD), a meta-
help sustain JA production (Ziegler et al., bolic catalyst in the production of structural
2001). and chemical defences (Fig. 7.3).
Pathways involving jasmonates (JA and Interestingly, the results of Moran and
methyl jasmonate (MeJA)), ethylene (ET) and Thompson (2001) also demonstrated that
salicylic acid (SA) induce plant defences green peach aphid feeding on Arabidopsis
after insect attack, and some types of induces major increases in the expression of
induced resistance are elicited by unknown the PR-1 and BGL2 genes, both of which are
and as yet unexplained types of elicitors. For associated with the SA defence signalling
example, both JA and ET induce the squash pathway. In related defence signal ‘cross-
gene SLW-1 for resistance to feeding by the talk’ studies, several authors have noted that
silverleaf whitefly, Bemisia argentifolii Bellows defence responses induced by JA and ET
and Perring, but an additional gene (SLW-3) may be antagonized by those induced by SA
is regulated by an unknown elicitor (van de (Dong, 1998; Reymond and Farmer, 1998;
Ven et al., 2000). Bostock, 1999; Pieterse and van Loon, 1999;
The majority of induced responses identi- Stotz et al., 2002).
fied to date in plants resulting from insect Herbivore-specific elicitors that induce
attack involve the jasmonate pathway. plant defence responses have also been iso-
Methyl JA-treated wheat plants produce lated from oral secretions of some lepi-
increased amounts of the defensive com- dopterous larvae. These include the lytic
pound hydroxamic acid and sustain reduced enzyme β-glucosidase, isolated from salivary
phloem ingestion by bird cherry oat aphid, secretions of larvae of the imported cabbage-
Rhopalosiphum padi (L.), compared with con- worm, Pieris brassicae (Linnaeus) (Mattiacci et
trol plants (Slesak et al., 2001). Methyl JA- al., 1995) and fatty acid conjugates isolated
induced accumulation of ferulic acid and from the larval regurgitant of the tobacco
phenolic polymers leads to cell-wall hornworm (Halitschke et al., 2001) and the
strengthening and increased insect resistance beet armyworm (Alborn et al., 1997). In the
in barley and maize (Bergvinson et al., 1994; tobacco hornworm–Arabidopsis interaction,
Lee et al., 1997). As cDNA library techniques the application of the caterpillar fatty acid
have become employed, genes encoding conjugates to wounded leaf tissue elicits a JA
specific defence compounds have been burst and the production of volatile plant
identified in the transcriptomes of insect- defence compounds (Turlings and Benrey,
challenged plants of several families of 1998; Halitschke et al., 2000, 2001). For addi-
plants. These include genes for a hevein-like tional discussion of the interactions between
protein (HEL) (Reymond et al., 2000), a met- different plant-defence elicitors, readers are
allopeptidase-like protein (SLW-1) (van de referred to the excellent reviews of Kessler
Ven et al., 2000), vegetative storage proteins and Baldwin (2001) and Heil and Bostock
(VSP1, 2) (Bell et al., 1995), a novel β-glucosi- (2002).
dase gene (BGL1) (Stotz et al., 2002) and Elicitor-induced responses play a role in
genes encoding the defensin peptide induced plant resistance to insects. However,
(PDF1.2), phenylalanine ammonia lyase JA-induced responses also lower plant fit-
(PAL1) and a monosaccharide symporter ness and reduce seed yields, suggesting that
(STP4) (Moran and Thompson, 2001). plants bred to respond with heightened lev-
SA promotes the development of systemic els of insect resistance when attacked may be
acquired resistance, a broad-range resistance counter-productive in relation to efficient
against pathogens and some insects. crop production (Baldwin et al., 1997;
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160 C.M. Smith

Baldwin, 1998). There are many gaps in the methods to develop increased levels of
level and extent of knowledge about this insect resistance in these important food
exciting area of resistance-expression path- crops of the semi-arid tropics.
ways. Additional research at both the bio- There are hundreds of insect-resistance
chemical and molecular levels will be critical genes deployed in improved cultivars glob-
to a better understanding of how different ally, but the continual evolution of virulent
species of plants integrate separate and mul- biotypes dictates the need for the identifica-
tiple elicitor signals generated as part of the tion of new sources of resistance and for
defences against both insects and diseases. MAS systems to identify and track these
genes. The refinement and increased use of
MAS techniques and MAS centres should be
Recommendations and Future Strategies encouraged in order to accelerate the rate
and accuracy of breeding crop plants for
Resistant cultivars have proved to be ecolog- insect resistance.
ically and socially acceptable to consumers Our knowledge of how plants recognize
and economically feasible for producers for insect-feeding attacks and the elicitors they
over 100 years. Future insect-resistant crops produce in response to insect feeding is
will play a very important role in world sus- increasing rapidly. The evolving model of
tainable agricultural systems, and the bene- the differences in plant defence-response
fits of their use will become more prominent elicitors must be researched, challenged and
as world food needs increase, especially in modified to better understand induced
the developing countries of the semi-tropics. resistance function and how plant metabo-
In spite of their successful use in devel- lism can possibly be modified to use
oped countries, the high level of Bt expres- induced crop-plant resistance in insect pest-
sion, similar to high doses of conventional management programmes.
pesticide or high levels of conventional gene There is also a great need for additional
expression, may promote the development information about the sequence and func-
of insects resistant to Bt crop plants. The tion of expressed cDNAs unique to both
longevity of Bt transgenes should be resistant and susceptible plants under
extended however, due to the advent of the attack. The use of mRNA differential display
use of IRM programmes centred on non- and subtractive suppressive hybridization
transgene refuges that allow the survival of studies should be encouraged to accomplish
homozygous susceptible pest individuals. this goal. In addition to the sequence infor-
In addition, current Bt cultivars are based on mation provided by unique cDNAs, they
the differences in only four active protein can be used to probe oligonucleotide macro-
domains of toxin expression. This should be and microarrays, in order to determine
a concern of future plant-resistance research expressed resistance-gene function based on
efforts, and strategies need to be developed mRNA expression levels.
that will allow the development and com- The existence of RGAs in many crop
mercialization of transgenic plants contain- plants suggests that current and future plant-
ing non-Bt toxic proteins in IPM systems. resistance researchers should increasingly
Future insect-resistant (primarily transgenic) utilize these genetic resources to provide in
crop-development strategies and efforts need silico information about the location and
to address the growing need to increase food function of candidate resistance genes. As a
supplies for the populations of underdevel- more complete knowledge (and eventual
oped countries. Conventional resistance- sequencing) of the genomes of additional
breeding efforts have made strides to crop plants develops, the use of genomic
improve crops such as sorghum, millet, macro- and microarrays will also become
pigeon pea and chickpea during the past valuable tools to answer questions about
several decades. However, major corporate where resistance genes are located and what
and public investments are urgently needed biochemical and biophysical gene products
now to use conventional and molecular mediate their function.
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Plant Resistance against Pests 161

The ultimate goal of resistance-gene form crop plants for insect resistance in the
expression studies, genomic studies and same way that they have been transformed
MAS systems should be to identify plant with Bt and other related transgenes toxic to
genes that can be cloned and used to trans- insects.

References

Abbott, E.A., Lucht, T., Jensen, J. and Jordan-Conde, Z. (2001) Handling of GM crop issues by the mass
media. In: Proceedings Illinois Crop Protection Technology Conference. University of Illinois, Urbana,
Illinois, pp. 11–12.
Ahn, S.N., Anderson, J.A., Sorrells, M.E. and Tanksley, S.D. (1993) Homoeologous relationships of rice,
wheat and maize chromosomes. Molecular and General Genetics 241, 483–490.
Alam, S.N. and Cohen, M.B. (1998) Detection and analysis of QTLs for resistance to the brown planthopper,
Nilapavata lugens, in a doubled-haploid rice population. Theoretical and Applied Genetics 97, 1370–1379.
Alborn, T., Turlings, T.C.J., Jones, T.H., Stenhagen, G., Loughrin, J.H. and Tumlinson, J.H. (1997) An elici-
tor of plant volatiles from beet armyworm oral secretion. Science 276, 945–949.
Al-Deeb, M.A., Wilde, G.E. and Higgins, R.A. (2001) No effect of Bacillus thuringiensis corn and Bacillus
thuringiensis on the predator Orius insidiosus (Say) (Hemiptera: Anthocoridae). Environmental
Entomology 30, 625–629.
American Phytopathological Society (APS) (1999) Threats to health reduced with Bt corn hybrids.
Available at: http://www.scisoc. org/opae/media/btcorn.htm
Anon. (2001) Corn and Biotechnology Special Analysis. National Agricultural Statistic Service, USDA,
Washington, DC.
Azzam, A., Azzam, S., Lhaloui, S., Amri, A., El Bouhssini, M. and Moussaoui, M. (1997) Economic returns
to research in Hessian fly (Diptera: Cecidomyidae) resistant bread-wheat varieties in Morocco.
Journal of Economic Entomology 90, 1–5.
Baldwin, I.T. (1998) Jasmonate-induced responses are costly but benefit plants under attack in native
populations. Proceedings of the National Academy of Sciences of the USA 95, 8113–8118.
Baldwin, I.T., Zhang, Z.-P., Diab, N., Ohnmeiss, T.E., McCloud, E.S., Lynds, G.Y. and Schmelz, E.A. (1997)
Quantification, correlations and manipulation of wound-induced changes in jasmonic acid and
nicotine in Nicotiana sylvestris. Planta 210, 397–404.
Bell, E., Creelman, R.A. and Mullet, J.E. (1995) A chloroplast lipoxygenase is required for wound-induced
jasmonic acid accumulation in Arabidopsis. Proceedings of the National Academy of Sciences of the USA
92, 8675–8679.
Bergvinson, D.J., Arnason, J.T. and Pietrzak, L.N. (1994) Localization and quantification of cell wall phe-
nolics in European corn borer resistant and susceptible maize inbreds. Canadian Journal of Botany 72,
1243–1249.
Bostock, R.M. (1999) Signal conflicts and synergies in induced resistance to multiple attackers.
Physiological and Molecular Plant Pathology 55, 99–109.
Botha, A.M., Nagel, M.A.C., Van der Westhuizen, A.J. and Botha, F.C. (1998) Chitinase isoenzymes in
near-isogenic wheat lines challenged with Russian wheat aphid, exogenois ethylene and mechanical
wounding. Botanical Bulletin of the Academica Sinica 39, 99–106.
Boyko, E.V., Gill, K.S., Mickelson-Young, L., Nasuda, S., Raupp, W.J., Ziegler, J.N., Singh, S., Hassawi,
D.S., Fritz, A.K., Namuth, D., Lapitan, N.L.V. and Gill, B.S. (1999) A high-density genetic linkage
map of Aegilops tauschii, the DS-genome progenitor of bread wheat. Theoretical and Applied Genetics
99, 16–26.
Boyko, E.V., Kalendar, R., Korzun, V., Korol, A., Schulman, A. and Gill, B.S. (2002) A high density genetic
map of Aegilops tauschii includes genes, retro-transposons, and microsatellites which provide unique
insight into cereal chromosome structure and function. Plant Molecular Biology 48, 767–790.
Brotman, Y., Silberstein, L., Kovalski, I., Perin, C., Dogimont, C., Pitrat, M., Klingler J., Thompson, G.A.
and Perl-Treves, R. (2002) Resistance gene homologues in melon are linked to genetic loci conferring
disease and pest resistance. Theoretical and Applied Genetics 104, 1055–1063.
Byrne, P., Ward, S., Harrington, J. and Fuller, L. (2003) Transgenic plants: an introduction and resource
guide. Available at: http://www.colostate.edu/programs/lifesciences/TransgenicCrops/news.
html#stillbreaking
07IntpestManCh7.QXD 14/4/04 2:25 pm Page 162

162 C.M. Smith

Cardinal, A.J., Lee, M., Sharopova, N., Woodman-Clikeman, W.L. and Long, M.J. (2001) Genetic mapping
and analysis of quantitative tratit loci for resistance to stalk tunneling by the European corn borer in
maize. Crop Science 41, 835–845.
Carrière, Y., Ellers-Kirk, C., Sisterson, M., Antilla, L., Whitlow, M., Dennehy, T.J. and Tabashnik, B.E.
(2003) Long-term regional suppression of pink bollworm by Bacillus thuringiensis cotton. Proceedings
of the National Academy of Sciences of the USA 100, 1519–1523.
Castro, A.M., Worland, A., Vasicek, A., Clua, A.A., Gimenez, D., Ellerbrook, C. and Tacaliti, M.S. (2001)
Mapping a QTL involved with greenbug and Russian wheat aphid resistance. In: Proceedings 4th
International Triticeae Symposium. Consejenia de Agricultura y Pesca, Cordoba, Spain, pp. 345–349.
Cevik, V. and King, G.L. (2002) High-resolution genetic analysis of the Sd-1 aphid resistance locus in
Malus spp. Theoretical and Applied Genetics 105, 346–354.
Chesnokov, P.G. (1953) Methods of Investigating Plant Resistance to Pests. National Science Foundation,
Washington, DC (Israel Program for Scientific Translation).
Cregan, P., Jarvik, T., Bush, A.L., Shoemaker, R.C., Lark, K.G., Kahler, A.L., Kaya, N., VanToai, T.T.,
Lohnes, D.G., Chung, J. and Specht, J.E. (1999) An integrated genetic linkage map of the soybean
genome. Crop Science 39, 1464–1490.
Cuperus, G.W., Kendall, P., Rehe, S., Frisbee, R., Hall, K., Bruhn, C., Deer, D., Woods, F., Branthaver, B.,
Weber, G., Poli, B., Buege, D., Linker, M., Andress, E., Wintersteen, W., Dost, F., Hegley, F., Aselhage,
J., Stelltflug, L., Doe, R. and Murray, G. (1991) Integration of Food Safety and Water Quality Concepts
Throughout the Food Production, Processing and Distribution Educational Programs using HACCP
Philosophies. Circular E-903, Cooperative Extension Service, Oklahoma State University, Stillwater.
Daly, J.C. and Wellings, P.W. (1996) Ecological constraints to the deployment of arthropod resistant crop
plants: a cautionary tale. In: Floyd, R.B., Shepard, A.W. and De Barro, P.J. (eds) Frontiers of Population
Ecology. CSIRO Publishing, Melbourne, pp. 311–323.
Dhaliwal, G.S. and Dilawari, V.K. (eds) (1993) Advances in Host Plant Resistance to Insects. Kalyani
Publishers, New Delhi.
Dhaliwal, G.S. and Singh, R. (eds) (2004) Host Plant Resistance to Insects: Concepts and Applications. Panima
Publishing Corporation, New Delhi.
Dong, X. (1998) SA, JA, ethylene, and disease resistance in plants. Current Opinions in Plant Biology 1,
316–323.
Dubcovsky, J., Lukaszewski, A.J., Echaide, M., Antonelli, E.F. and Porter, D.R. (1998) Molecular character-
ization of two Triticum speltoides interstitial translocations carrying leaf rust and greenbug resistance
genes. Crop Science 38, 1655–1660.
Eddleman, B.R., Chang, C.C. and McCarl, B.A. (1999) Economic benefits from grain sorghum variety
improvement in the United States. In: Wiseman, B.R. and Webster, J.A. (eds) Economic,
Environmental, and Social Benefits of Resistance in Field Crops. Thomas Say Publications, Entomological
Society of America, Lanham, Maryland, pp. 17–44.
Feuillet, C. and Keller, B. (1999) High genome density is conserved at syntenic loci of small and large
grass genomes. Proceedings of the National Academy of Sciences of the USA 96, 8265–8270.
Fidantsef, A.L., Stout, M.J., Thaler, J.S., Duffey, S.S. and Bostock, R.M. (1999) Signal interactions in pathogen
and insect attack: expression of lipoxygenase, proteinase inhibitor II, and pathogenesis-related protein
P4 in the tomato, Lycopersicon esculentum. Physiological and Molecular Plant Pathology 54, 97–114.
Forslund, K., Perrersson, J., Bryngelsson, T. and Jonnson, L. (2000) Aphid infestation induces PR-proteins
differentially in barley susceptible or resistant to the birdcherry-oat aphid. Physiologia Plantarum 110,
496–502.
Gaskell, G., Bauer, M.W., Durant, J. and Allum, N.C. (1999) Worlds apart? The reception of genetically
modified foods in Europe and the U.S. Science 285, 384–387.
Gould, F. (1998) Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology.
Annual Review of Entomology 43, 701–726.
Graham, M.A., Marek, L.F., Lohnes, D., Cregan, P. and Shoemaker, R. (2000) Expression and genome
organization of resistance gene analogs in soybean. Genome 43, 86–90.
Halitschke, R., Kessler, A., Kahl, J., Lorenz, A. and Baldwin, I.T. (2000) Ecophysiological comparison of
direct and indirect defences in Nicotiana attenuata. Oecologia 124, 408–417.
Halitschke, R., Schittko, U., Pohnert, G., Boland, W. and Baldwin, I.T. (2001) Molecular interactions
between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host
Nicotiana attenuata. III. Fatty amino-acid conjugates in herbivore oral secretions are necessary and
sufficient for herbivore-specific plant responses. Plant Physiology 125, 711–717.
07IntpestManCh7.QXD 14/4/04 2:25 pm Page 163

Plant Resistance against Pests 163

Heil, M. and Bostock, R.M. (2002) Induced systemic resistance (ISR) against pathogens in the context of
induced plant defences. Annals of Botany 89, 503–512.
Hermsmeier, D., Schittko, U. and Baldwin, I.T. (2001) Molecular interactions between the specialist herbivore
Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. I. Large-scale changes
in the accumulation of growth-and defence-related plant mRNAs. Plant Physiology 125, 683–700.
Hernández, P., Dorado, G., Prieto, P., Giménez, M.J., Ramírez, M.C., Laurie, D.A., Snape, J.W., and
Martín, A. (2001) A core genetic map of Hordeum chilense and comparisons with maps of barley
(Hordeum vulgare) and wheat (Triticum aestivum). Theoretical and Applied Genetics 102, 1259–1264.
Huang, F., Higgins, R.A. and Buschman, L.L. (1999) Transgenic Bt-plants: successes, challenges, and
strategies. Pestology 23, 2–29.
Huang, N., Parco, A., Mew, T., Magpantay, G., McCouch, S., Guiderdoni, E., Xu, J.C., Subudhi, P.,
Angeles, E.R. and Khush, G.S. (1997) RFLP mapping of isozymes, RAPD and QTLs for grain shape,
brown planthopper resistance in a doubled haploid rice population. Molecular Breeding 3, 105–113
Huang, Z., He, G., Shu, L., Li, X. and Zhang, Q. (2001) Identification and mapping of two brown
planthopper resistance genes in rice. Theoretical and Applied Genetics 102, 929–934.
Hwang, C.F., Bhakta, A.V., Truesdell, G.M., Pudlo, W.M. and Williamson, V.M. (2000) Evidence for a role
of the N terminus and leucine-rich repeat region of the Mi gene product in regulation of localized
cell death. Plant Cell 12, 1319–1329.
International Food Information Council (IFIC) (2002) U.S. consumer attitudes toward food biotechnology
survey: 23 September, 2002. Available at: http://ific.org/relatives/17860. pdf
James, C. (2000) Global Status of Commercialized Transgenic Crops. ISAAA, Briefs 21, Preview. ISAAA
Ithaca, NY. Available at: http://www.isaaa.org/publications/briefs/Brief_21.htm
Jampatong, C., McMullen, M.D., Barry, D.B., Darrah, L.L., Byrne, P.F. and Kross, H. (2002) Quantitative
trait loci for first- and second-generation European corn borer resistance derived from the maize
inbred Mo47. Crop Science 41, 584–593.
Johnson, M.T. and Gould, F. (1992) Interaction of genetically engineered host plant resistance and natural
enemies of Heliothis virescens (Lepidoptera: Noctuidae) in tobacco. Environmental Entomology 21,
586–597.
Kaloshian, I., Lange, W.H. and Williamson, V.M. (1995) An aphid-resistance locus is tightly linked to the
nematode-resistance gene, Mi, in tomato. Proceedings of the National Academy of Sciences of the USA
92, 622–625.
Kaloshian, I., Kinser, M.G., Ullman, D.E. and Williamson, V.M. (1997) The impact of Meu1-mediated
resistance in tomato on longevity, fecundity, and behaviour of the potato aphid, Macrosiphum
euphorbiae. Entomologia Experimentalis et Applicata 83, 181–187.
Katiyar, S.K., Tan, Y., Huang, B., Chandel, G., Xu, Y., Zhang, Y., Xie, Z. and Bennett, J. (2001) Molecular
mapping of gene Gm-6(t) which confers resistance against four biotypes of Asian rice gall midge in
China. Theoretical and Applied Genetics 103, 953–961.
Katsar, C.S., Paterson, A.H., Teetes, G.L. and Peterson, G.C. (2002) Molecular analysis of sorghum resis-
tance to the greenbug (Homoptera: Aphididae). Journal of Economic Entomology 95, 448–457.
Kessler, A. and Baldwin, I.T. (2001) Defensive function of herbivore-induced plant volatile emissions in
nature. Science 291, 2141–2144.
Khush, G.S. and Brar, D.S. (1991) Genetics of resistance to insects in crop plants. Advances in Agronomy 45,
223–274.
Kirsten, J. and Gouse, M. (2002) Bt cotton in South Africa: adoption and impact on farm incomes amongst
small- and large-scale farmers. ISB News Report. Available at: http://www.isb.
vt.edu/articles/oct0204.htm
Knight, J. (2003) Agency ignoring its advisers over Bt maize. Nature 422, 5.
Korzun, V., Malyshev, S., Voylokov, A.V. and Börner, A. (2001) A genetic map of rye (Secale cereale L.) com-
bining RFLP, isozyme, protein, microsatellite and gene loci. Theoretical and Applied Genetics 102,
709–717.
Kretshmer, J.M., Chalmers, K.J., Manning, S., Karakousis, A., Barr, A.R., Islam, M.R., Logue, S.J., Choe,
Y.W., Barker, S.J., Lance, R.C.M. and Langridge, P. (1997) RFLP mapping of the Ha2 cereal cyst
nematode resistance gene in barley. Theoretical and Applied Genetics 94, 1060–1064.
Lagudah, E.S., Moullet, O. and Appels, R. (1997) Map-based cloning of a gene sequence encoding a
nucleotide binding domain and a leucine-rich region at the Cre3 nematode resistance locus of
wheat. Genome 40, 659–665.
07IntpestManCh7.QXD 14/4/04 2:25 pm Page 164

164 C.M. Smith

Lander, E.S., Green, P., Abrahamson, J., Barlow, A., Daly, M.J., Lincoln, S.E. and Newburg, L. (1987) MAP-
MAKER: an interactive computer package for constructing primary genetic maps of experimental
and natural populations. Genomics 1, 174–181.
Lara, F.M. (1979) Principios de Resistancia de Plantas a Insectos – (in Portugese). Piracicaba, Livroceres, Brazil.
Lawrence, P.K. and Koundal, K.R. (2002) Plant protease inhibitors in control of phytophagous insects.
Electronic Journal of Biotechnology 5, 15 April. Available at: http://www.ejbiotechnology.info/
content/vol5/issue1/full/3/index.html
Lee, J.E., Vogt, T., Hause, B. and Lëbler, M. (1997) Methyl jasmonate induces an O-methyltransferase in
barley. Plant Cell Physiology 38, 851–862.
Leister, D., Kurth, J., Laurie, D.A., Yano, M., Sasaki, T., Graner, A. and Schulze-Lefert, P. (1999) RFLP- and
physical mapping of resistance gene homologues in rice (O. sativa) and barley (H. vulgare).
Theoretical and Applied Genetics 98, 509–520.
Li, W.L., Faris, J.D., Chitmoor, J.M., Leach, J.F., Hulbert, S.H., Liu, D.J., Chen, P.D. and Gill, B.S. (1999)
Genomic mapping of defence response genes in wheat. Theoretical and Applied Genetics 98, 226–233.
Liu, X.M., Smith, C.M., Gill, B.S. and Tolmay, V. (2001) Microsatellite markers linked to six Russian wheat
aphid resistance genes in wheat. Theoretical and Applied Genetics 102, 504–510.
Liu, X.M., Smith, C.M. and Gill, B.S. (2002) Mapping of microsatellite markers linked to the Dn4 and Dn6
genes expressing Russian wheat aphid resistance in wheat. Theoretical and Applied Genetics 104,
1042–1048.
Llewellyn, D., Cousins, Y., Mathews, A., Hartweck, L. and Lyon, B. (1994) Expression of Bacillus thurin-
gensis insecticidal protein genes in transgenic crop plants. Agriculture, Ecosystems & Environment 49,
85–93.
Losey, J.E., Rayor, L.S. and Carter, M.E. (1999) Transgenic pollen harms monarch larvae. Nature 399, 214.
Mago, R., Nair, S. and Mohan, M. (1999) Resistance gene analogues from rice: cloning, sequencing and
mapping. Theoretical and Applied Genetics 99, 50–57.
Mattiacci, L., Dicke, M. and Posthumas, M.A. (1995) Beta-glucosidase – an elicitor of herbivore-induced
plant odor that attracts host-searching parasitic wasps. Proceedings of the National Academy of Sciences
of the USA 92, 2036–2040.
Maxwell, F.G. and Jennings, P.R. (1980) Breeding Plants Resistant to Insects. John Wiley & Sons, New York.
Miller, C.A., Altinkut, A. and Lapitan, N.L.V. (2001) A microsatellite marker for tagging Dn2, a wheat
gene conferring resistance to the Russian wheat aphid. Crop Science 41, 1584–1589.
Milligan, S., Bodeau, J., Yaghoobi, J., Kaloshian, I., Zabel, P. and Williamson, V. (1998) The root-knot
nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding,
leucine-rich repeat family of plant genes. Plant Cell 10, 1307–1319.
Moharramipour, S., Tsumki, H., Sato, K. and Yoshida, H. (1997) Mapping resistance to cereal aphids in
barley. Theoretical and Applied Genetics 94, 592–596.
Moran, P.J. and Thompson, G.A. (2001) Molecular responses to aphid feeding in Arabidopsis in relation to
plant defence pathways. Plant Physiology 125, 1074–1085.
Moreira, L.A., Mollema, C. and van Heusden, S. (1999) Search for molecular markers linked to Liriomyza
trifolii resistance in tomato. Euphytica 109, 149–156.
Mullis, K. (1990) The unusual origin of the polymerase chain reaction. Scientific American April, 262, 56–65.
Murai, H., Hashimoto, Z., Sharma, P.N., Shimizu, T., Murata, K., Takumi, S., Mori, N., Kawasaki, S. and
Nakamura, C. (2001) Construction of a high resolution linkage map of a rice brown planthopper
(Nilaparvata lugens Stal) resistance gene bph2. Theoretical and Applied Genetics 103, 526–532.
Narvel, J.A., Walker, D.R., Rector, B.G., All, J.N., Parrott, W.A. and Boerma, R. (2001) A retrospective
DNA marker assessment of the development of insect resistant soybean. Crop Science 41, 1931–1939.
Nieto-Lopez, R.M. and Blake, T.K. (1994) Russian wheat aphid resistance in barley: inheritance and
linked molecular markers. Crop Science 34, 655–659.
Oppert, B.S. (2001) Transgenic plants expressing enzyme inhibitors and the prospects for biopesticide
development. In: Koul, O. and Dhaliwal, G.S. (eds) Phytochemical Biopesticides. Harwood Academic
Publishers, Amsterdam, pp. 83–95.
Painter, R.H. (1951) Insect Resistance in Crop Plants. University of Kansas Press, Lawrence, Kansas.
Panda, N. (1979) Principles of Host-Plant Resistance to Insect Pests. Allanheld, Osmun & Co. and Universe
Books, New York.
Panda, N. and Khush, G.S. (1995) Host Plant Resistance to Insects. CAB International, Wallingford, UK.
Pani, J. and Sahu, S.C. (2000) Inheritance of resistance against biotype 2 of the Asian rice gall midge,
Orseolia oryzae. Entomologia Experimentalis et Applicata 95, 15–19.
07IntpestManCh7.QXD 14/4/04 2:25 pm Page 165

Plant Resistance against Pests 165

Paterson, A., Lin, Y.-R., Li, Z., Scherta, K.F., Doebley, J.F., Pinson, S.R.M., Liu, S.-C., Stansel, J.W. and
Irvine, J.E. (1995) Convergent domestication of cereal crops by independent mutations at corre-
sponding genetic loci. Science 269, 1714–1718.
Pieterse, C.M and van Loon, L.C. (1999) Salicylic acid-independent plant defence pathways. Trends in
Plant Science 4, 52–58.
Pilcher, C.D., Obrycki, J.J., Rice, M.E. and Lewis, L.C. (1997) Preimaginal development, survival, field
abundance of insect predators on transgenic Bacillus thuringiensis corn. Environmental Entomology 26,
446–454.
Pimentel, D.S. and Raven, P.H. (2000) Bt corn pollen impacts on nontarget Lepidoptera: assessment of
effects in nature. Proceedings of the National Academy of Sciences of the USA 97, 8198–8199.
Qaim, M. and Zilberman, D. (2003) Yield effects of genetically modified crops in developing countries.
Science 299, 900–902.
Ratcliffe, R.H. and Hatchett, J.H. (1997) Biology and genetics of the Hessian fly and resistance in wheat.
In: Bobdari, K. (ed.) New Developments in Entomology. Research Signpost, Scientific Information
Guild, Trivandrum, pp. 47–67.
Rector, B.G., All, J.N., Parrott, W.A. and Boerma, H.R. (1998) Identification of molecular markers linked to
quantitative trait loci for soybean resistance to corn earworm. Theoretical and Applied Genetics 96,
786–790.
Rector, B.G., All, J.N., Parrott, W.A. and Boerma, H.R. (2000) Quantitative trait loci for antibiosis resis-
tance to corn earworm in soybean. Crop Science 40, 233–238.
Renganayaki, K., Fritz, A.K., Sadasivam, S., Pammi, S., Harrington, S.E., McCouch, S.R., Kumar, S.M. and
Reddy, A.S. (2002) Mapping and progress toward map-based cloning of brown planthopper bio-
type-4 resistance gene introgressed Oryza officinalis into cultivated rice, O. sativa. Crop Science 42,
2112–2117.
Reymond, P. and Farmer, E.E. (1998) Jasmonate and salicylate as global signals for defence gene expres-
sion. Current Opinions in Plant Biology 1, 404–411.
Reymond, P., Weber, H., Damond, M. and Farmer, E.E. (2000) Differential gene expression in response to
mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12, 707–719.
Rice, M.E. and Pilcher, C.D. (1998) Potential benefits and limitations of transgenic Bt corn for manage-
ment of the European corn borer (Lepidoptera: Crambidae). American Entomologist 44, 75–78.
Rissler, J. and Mellon, M. (1996) The Ecological Risks of Engineered Crops. MIT Press, Cambridge,
Massachusetts.
Roberts, P.A. and Thomason, I.J. (1986) Variability in reproduction of isolates of Meloidogyne incognita and
M. javanica on resistant tomato genotypes. Plant Disease 70, 547–551.
Royo, E., Leon, J., Vancanneyt, G., Albar, J.P., Rosahl, S., Ortego, F., Castanera, P. and Sanchez-Serrano, J.J.
(1999) Antisense-mediated depletion of a potato lipoxygenase reduces wound induction of pro-
teinase inhibitors and increases weight gain of insect pests. Proceedings of the National Academy of
Sciences of the USA 96, 1146–1151.
Rossi, M., Goggin, F.L., Milligan, S.B., Klaoshian, I., Ullman, D.E. and Williamson, V.M. (1998) The nema-
tode resistance gene Mi of tomato confers resistance against the potato aphid. Proceedings of the
National Academy of Sciences of the USA 95, 9750–9754.
Russell, G.E. (1978) Plant Breeding for Pest and Disease Resistance. Butterworth Publishers, Boston,
Massachusetts.
Sachs, E.S., Benedict, J.H., Taylor, J.F., Stelly, D.M., Davis, S.K. and Altman, D.W. (1996) Pyramiding
CryIA(b) insecticidal protein and terpenoids in cotton to resist tobacco budworm (Lepidoptera:
Noctuidae). Environmental Entomology 25, 1257–1266.
Sardesai, N., Kumar, A., Rajyashri, K.R., Nair, S. and Mohan, M. (2001) Identification and mapping of an
AFLP marker linked to Gm7, a gall midge resistance gene and its conversion to a SCAR marker for
its utility in marker aided selection in rice. Theoretical and Applied Genetics 105, 691–698.
Seah, S., Sivasithamparam, K., Karalousis, A. and Lagudah, E.S. (1998) Cloning and characterisation of a
family of disease resistance gene analogs from wheat and barley. Theoretical and Applied Genetics 97,
937–945.
Sears, M.K., Hellmich, R.L., Stanley-Horn, D.E., Oberhauser, K.S., Pleasants, J.M., Mattila, H.R., Siegfried,
B.D. and Dively, G.P. (2001) Impact of Bt corn pollen on monarch butterfly populations: a risk
assessment. Proceedings of the National Academy of Sciences of the USA 98, 11937–11942.
Service, R.F. (2001) Arson strikes research labs and tree farm in Pacific Northwest. Science 292, 1622–1623.
07IntpestManCh7.QXD 14/4/04 2:25 pm Page 166

166 C.M. Smith

Sharma, H.C., Sharma, K.K., Seetharama, N. and Ortiz, R. (2000) Prospects for using transgenic resistance
to insects in crop improvement. Electronic Journal of Biotechnology 3, 15 August. Available at:
http://www.ejbiotechnology.info/content/vol3/issue2/full/3/index.html
Sharopova, N., McMullen, M.D., Schultz, L., Schroeder, S., Sanchez-Villeda, H., Gardiner, J., Bergstrom,
D., Houchins, K., Melia-Hancock, S., Musket, T., Duru, N., Polacco, M., Edwards, K., Ruff, T.,
Register, J.C., Brouwer, C., Thompson, R., Velasco, R., Chin, E., Lee, M., Woodman-Clikeman, W.,
Long, M.J., Liscum, E., Cone, K., Davis, G. and Coe, E.H. Jr (2002) Development and mapping of
SSR markers for maize. Plant Molecular Biology 48, 463–481.
Shen, K.A., Meyers, B.C., Islam-Faridi, M.N., Chin, D., Stelly, D.M. and Michelmore, R.W. (1998)
Resistance gene candidates identified by PCR with degenerate oligonucleotide primers map to clus-
ters of resistance genes in lettuce. Molecular Plant–Microbe Interaction 11, 815–823.
Slesak, E., Slesak, M. and Gabrys, B. (2001) Effect of methyl jasmonate on hydroxamic acid, protease
activity, and bird cherry-oat aphid Rhoplaosiphum padi L. probing behavior. Journal of Chemical
Ecology 12, 2529–2543.
Smith, C.M. (1989) Plant Resistance to Insects – A Fundamental Approach. John Wiley & Sons, New York.
Smith, C.M. (1999) Plant resistance to insects. In: Rechcigl, J. and Rechcigl, N. (eds) Biological and
Biotechnological Control of Insects. Lewis Publishers, Boca Raton, Florida, pp. 171–205.
Smith, C.M., Khan, Z.R. and Pathak, M.D. (1994) Techniques for Evaluating Insect Resistance in Crop Plants.
Lewis Publishers, Boca Raton, Florida.
Smith, C.M., Quisenberry, S.S. and du Toit, F. (1999) The value of conserved wheat germplasm possessing
arthropod resistance. In: Clement, S.L. and Quisenberry, S.S. (eds) Global Plant Genetic Resources for
Insect Resistant Crops. CRC Press, Boca Raton, Florida, pp. 25–49.
Snelling, R.O. (1941) Resistance of plants to insect attack. Botany Reviews 7, 543–586.
Speulman, E., Bouchez, D., Holub, E. and Beynon, J.L. (1998) Disease resistance gene homologs correlate
with disease resistance loci of Arabidopsis thaliana. Plant Journal 14, 467–474.
Stanley-Horn, D.E., Dively, G.P., Hellmich, R.L., Mattila, H.R., Sears, M.K., Rose, R., Jesse, L.C.H., Losey,
J.E., Obrycki, J.J. and Lewis, L. (2002) Assessing the impact of Cry1Ab-expressing corn pollen on
monarch butterfly larvae in field studies. Proceedings of the National Academy of Sciences of the USA 98,
11931–11936.
Staub, J.E., Serquen, F.C. and Gupta, M. (1996) Genetic markers, map construction, and their application
in plant breeding. HortScience 31, 729–741.
Stotz, H.U., Pittendrigh, B.R., Kroyman, J., Weniger, K., Fritsche, J., Bauke, A. and Mitchell-Olds, T. (2000)
Induced plant defense responses against chewing insects. Ethylene signaling reduces resistance of
Arabidopsis against Egyptain cotton worm but not diamond back moth. Plant Physiology 124,
1007–1017.
Stotz, H.U., Koch, T., Biedermann, A., Weniger, K., Boland, W. and Mitchell-Olds, T. (2002) Evidence for
regulation of resistance in Arabidopsis to Egyptian cotton worm by salicylic and jasmonic acid sig-
naling pathways. Planta 214, 648–652.
Stout, M.J., Fidantsef, A.L., Duffey, S.S. and Bostock, R.M. (1999) Signal interactions in pathogen and
insect attack: systemic plant-mediated interactions between pathogens and herbivores of the
tomato, Lycopsericon esculentum. Physiological and Molecular Plant Pathology 54, 115–130.
Tada, T. (1999) PCR-amplified resistance gene analogs link to resistance loci in rice. Breeding Science 49,
267–273.
Tamura, K., Fukuta, Y., Hirae, M., Oya, S., Ashikawa, I. and Yagi, T. (1999) Mapping of the Grh1 locus for
green rice leafhopper resistance in rice using RFLP markers. Breeding Science 49, 11–14.
Tanaka, K. (1999) Quantitative genetic analysis of biotypes of the brown planthopper Nilaparvata lugens:
heritability of virulence to resistant rice varieties. Entomologia Experimentalis et Applicata 90, 279–287.
Turlings, T.C.J. and Benrey, B. (1998) Effects of plant metabolites on the behavior and development of
parasitic wasps. EcoScience 5, 321–333.
Vancanneyt, G., Sanz, C., Farmaki, T., Paneque, M., Ortego, F., Castañera, P. and Sánchez-Serrano, J.
(2001) Hydroperoxide lyase depletion in transgenic potato plants leads to an increase in aphid per-
formance. Proceedings of the National Academy of Sciences of the USA 98, 8139–8144.
van de Ven, W.T.G., LeVesque, C.S., Perring, T.M. and Walling, L.L. (2000) Local and systemic changes in
squash gene expression in response to silverleaf whitefly feeding. Plant Cell 12, 1409–1424.
Van Sanford, D.V., Anderson, J., Campbell, K., Costa, J., Cregan, P., Griffey, C., Hayes, P. and Ward, R.
(2001) Discovery and deployment of molecular markers linked to fusarium head blight resistance:
an integrated system for wheat and barley. Crop Science 41, 638–644.
07IntpestManCh7.QXD 14/4/04 2:25 pm Page 167

Plant Resistance against Pests 167

Vos, P., Hogers, R., Bleeker, M., Rijans, M., Van de Lee, T., Hornes, M., Frijters, A., Pot, J., Kuiper, M. and
Zabeau, M. (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Research 23,
4407–4414.
Vos, P., Simons, G., Jesse, T., Wijbrandi, J., Heinen, L., Hogers, R., Frijters, A., Groenendijk, J.,
Diergaarde, P., Reijans, M., Fierens-Onstenk, J., de Both, M., Peleman, J., Liharska, T., Hontelez, J.
and Zabeau, M. (1998) The tomato Mi-1 gene confers resistance to both root-knot nematodes and
potato aphids. Nature Biotechnology 16, 1315–1316.
Walling, L.L. (2000) The myriad plant responses to herbivores. Journal of Plant Growth Regulators 19,
195–216.
Wang, Y.H., Garvin, D.F. and Kochian, L.V. (2001) Nitrate-induced genes in tomato roots: array analysis
reveals novel genes that may play a role in nitrogen nutrition. Plant Physiology 127, 345–359.
Wayland, S., Mulkey, M., Johnson, S., Green, J., Kearnes, D., Barnes, D., Ellis, V., Anderson, J., Hutton, P.
and Dorsey, L. (1998) The Environmental Protection Agency’s White Paper on Bt Plant-pesticide Resistance
Management. US Environmental Protection Agency, Washington, DC, 84 pp.
Weng, Y. and Lazar, M.D. (2002) Amplified fragment length polymorphism- and simple sequence repeat-
based molecular tagging and mapping of greenbug resistance gene Gb3 in wheat. Plant Breeding 121,
218–223.
Willcox, M.C., Khairallah, M.M., Bergvinson, D., Crossa, J., Deutsch, J.A., Edmeades, G.O., Gonzalez-de-
Leon, D., Jiang, C., Jewell, D.C., Mihm, J.A., Williams, W.P. and Hoisington, D. (2002) Selection for
resistance to southwestern corn borer using marker-assisted selection and conventional backcross-
ing. Crop Science 42, 1516–1528.
Winz, R.A. and Baldwin, I.T. (2001) Molecular interactions between the specialist herbivore Manduca
sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. IV. Insect-induced ethylene
reduces jasmonate-induced nicotine accumulation by regulating N-methyltransferase transcripts.
Plant Physiology 125, 2189–2202.
Wraight, C.L., Zangerl, A.R., Carroll, M.J. and Berenbaum, M.R. (2000) Absence of toxicity of Bacillus
thuringiensis pollen to black swallowtails under field conditions. Proceedings of the National Academy
of Sciences of the USA 97, 7700–7703.
Xu, X.F., Mei, H.W., Luo, L.J., Cheng, X.M. and Li, Z.K. (2002) RFLP-facilitated investigation of the quan-
titative resistance of rice to brown planthopper (Nilaparvata lugens). Theoretical and Applied Genetics
104, 248–253.
Yencho, G.C., Cohen, M.B. and Byrne, P.F. (2000) Applications of tagging and mapping insect resistance
loci in plants. Annual Review of Entomology 45, 393–422.
Ziegler, J., Keinanen, M. and Baldwin, I.T. (2001) Herbivore-induced allene oxide synthase transcripts
and jasmonic acid in Nicotiana attenuata. Phytochemistry 58, 729–738.
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8 The Pesticide Paradox in IPM: Risk–Benefit

Analysis

Paul Guillebeau
Department of Entomology, University of Georgia Cooperative Extension Service,
Athens, GA 30602, USA
E-mail: [email protected]

Introduction pesticides in IPM programmes; situations that

result in incompatibility; and ways to better
By definition, integrated pest management incorporate pesticides into an IPM system.
(IPM) combines a variety of tactics into a
comprehensive system to manage pest popu-
lations. As much as possible, it is important Integrated pest management and pesticides,
to use components that are compatible with defining the terms
one another. Otherwise, the pest-manage-
ment programme may become overly reliant A number of people consider pesticides and
on a single tactic. Such a programme is not IPM to be incompatible. In many ways, how-
IPM, and the strategy carries greater risks. ever, this apparent paradox is a function of
The failure of a single tactic may allow a the broad and dynamic definitions of both
rapid increase in the pest population. In a ‘pesticide’ and ‘integrated pest manage-
truly integrated programme, the failure of a ment’. The Environmental Protection Agency
single component is less likely to be cata- (EPA) regulates pesticides in the USA; the
strophic because pest populations are con- Agency defines a pesticide as ‘any substance
trolled through a variety of techniques. or mixture of substances intended for pre-
Pesticides are one of the tools available to venting, destroying, repelling, or mitigating
IPM practitioners, and many pest-manage- any pest’ (US EPA, 2002b). This definition
ment programmes depend on the efficient comprises many highly toxic, broad-
use of pesticides. Unfortunately, some pesti- spectrum chemicals, but it also includes
cides impair or eliminate other components materials with a non-toxic mode of action,
of an IPM system. This occurs most com- such as pheromones. Likewise, IPM is
monly when broad-spectrum insecticides broadly defined, and the definition has
destroy populations of beneficial arthropods. changed substantially over the last few
The primary pest population may rebound decades.
or secondary pests may become a problem. The idea of integrated control is generally
In many situations, a marketable product credited to Hoskins et al. (1939). They stated:
cannot be produced economically without [B]iological and chemical control are considered
pesticides, but the focus of modern pest con- … as the two edges of the same sword …
trol is IPM. This chapter discusses the role of nature’s own balance provides the major part
© CAB International 2004. Integrated Pest Management: Potential, Constraints and Challenges
(eds O. Koul, G.S. Dhaliwal and G.W. Cuperus) 169
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170 P. Guillebeau

of protection … insecticides should be used so 75% of the US agricultural acreage under

as to interfere with natural control of pests as IPM by the year 2000 and to reduce the use
little as possible. of pesticides (US EPA, 2002a).
This definition sounds much like some cur- A government report criticized IPM
rent definitions discussed below, but one because there has been no significant reduc-
must remember that Hoskins et al. practised tion in the use of pesticides in US agriculture
pest management before the era of modern (US Congress Office of Technology
pesticides. Because the pesticides available at Assessment, 1995). Part of the criticism may
that time had limited value in many situa- be an artefact of the imprecise measurement
tions, pest management relied more heavily of IPM adoption. Monitoring and application
on non-chemical options. thresholds are key elements of most IPM def-
By the 1960s, definitions of IPM reflected initions, and these parameters have been
the use of more effective pesticides: commonly used to measure IPM adoption
(Vandeman et al., 1994). This method of mea-
Integrated control is a pest population suring IPM provides little information about
management system that utilizes all suitable
the intensity of pesticide application.
techniques either to reduce pest populations
and maintain them at levels below those
Because of the myriad definitions of IPM
causing economic injury or to so manipulate and the apparent lack of pesticide reduction,
the populations that they are prevented from some authors have suggested new terms.
causing such injury. Frisbie and Smith (1991) proposed ‘biointen-
(Smith and Van den Bosch, 1967) sive IPM’ with its focus on biological con-
trols, host-plant resistance and cultural
The focus of IPM was agricultural efficiency
controls. Likewise, the National Research
and avoiding economic losses, both strong
Council (1996) published a report on
incentives for grower acceptance of IPM.
Ecologically Based Pest Management that
Two decades later, Flint and van den
would mitigate environmental, economic
Bosch (1981) published a definition that
and safety risks. New terms have limited
acknowledged the role of pesticides while
value, however, because these same concepts
making it clear that chemicals should be the
are expressed in many of the earlier defini-
secondary line of defence:
tions for IPM.
IPM is an ecologically based pest control Although groups differ in their inter-
strategy that relies heavily on natural mortality pretations, IPM remains a useful compro-
factors … and seeks out control tactics that mise between environmental/human-health
disrupt these factors as little as possible. IPM advocacy groups and industries that may
uses pesticides, but only after systematic
need chemicals to manage out-of-control
monitoring of pest populations and natural
control factors indicates a need.
pest populations. Additionally, modern prac-
titioners agree that pesticides must be used
By the 1990s, the reduction of pesticide use judiciously if biological control is to play a
had become a basic tenet of IPM definitions: significant role in IPM. In this context, the
Integrated pest management, or IPM, is an working definition of IPM includes the goal
approach to pest control that utilizes regular of reducing pesticide risks to non-target
monitoring to determine if and when organisms, rather than focusing strictly on
treatments are needed and employs physical, reducing pesticide use. Beyond that point,
mechanical, cultural, biological and however, generalizations about pesticides
educational tactics to keep pest numbers low and IPM are of limited value. The impact of
enough to prevent intolerable damage or pesticides in a particular situation depends
annoyance. Least-toxic chemical controls are on the pesticide, the pest and the manage-
used as a last resort.
ment situation. Ironically, widespread appli-
(Olkowski and Daar, 1991)
cation of an organophosphate insecticide
In 1993, the EPA, the US Department of made possible the greatest reduction of pes-
Agriculture (USDA), and the US Food and ticide use and concomitant increase in bio-
Drug Administration (FDA) pledged to have logical control for an IPM programme.
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Risk–Benefit Analysis of Pesticides 171

Pesticides and Cotton IPM pesticide applications to control boll-weevil

had fallen to 2.7; in 1991, the average num-
The boll-weevil invasion was the beginning of ber of applications was 0.5. By 1996, pesti-
a pesticide treadmill for cotton that lasted for cide applications were no longer made to
more than 50 years. By 1917, every Georgia control boll-weevil except for spot treat-
county that produced cotton reported boll- ments made when boll-weevils were
weevils (Hunter, 1917), and cotton yields had detected in traps (Haney et al., 2001).
already decreased by 32% compared with The overall pesticide reductions associ-
pre-weevil production (Anon., 1917; Floyd ated with boll-weevil eradication are enor-
and Treanor, 1944). In 1920, cotton growers mous. In 1971, growers applied 73 million lb.
across the South applied 10 million lb. of cal- of insecticide active ingredient (Ridgeway et
cium arsenate to control boll-weevil (Coad, al., 1983) to 11.5 million acres of cotton in the
1920). Growers in 1940 were advised to apply USA (Anon., 1993), with an average of 6.8 lb.
calcium arsenate based on a threshold of wee- of active ingredient per acre. In 1992, 20 mil-
vil infestation. Even with a threshold, cotton lion lb. of insecticide active ingredient was
growers in Georgia alone applied 1.5 million applied to 11.1 million acres of cotton
lb. of calcium arsenate (Anon., 1940). (Anon., 1993; Gianessi and Anderson, 1995),
Organophosphate insecticides were intro- or 1.8 lb. of active ingredient per acre. The
duced for boll-weevil control in the 1950s average number of insecticide applications
(Rainwater and Gaines, 1951). By 1968, cot- per acre in Georgia dropped from 16.5 from
ton growers in the South were applying from 1987 to 1992 to less than 3.5 from 1993 to
ten to 18 treatments of insecticides per sea- 1999 (Haney et al., 2001).
son (Martin et al., 1968). Boll-weevil was a The eradication of boll-weevil allowed
major target; however, growers were also cotton farmers to place greater emphasis on
using multiple pesticide applications to con- biological control agents. Prior to boll-weevil
trol other pests, primarily the bollworm eradication, the economic impact (yield
complex, namely, Helicoverpa zea (Boddie) losses + cost of control) of Spodoptera exigua
and Heliothis virescens (Fabricius) (Haney et (Hubner) in Georgia averaged nearly 2% of
al., 2001). Numerous arthropod predators the cotton crop’s value (Haney et al., 2001).
and parasitoids attack bollworms (Whitcomb During the pesticide-intensive eradication
and Bell, 1964); cotton was clearly on a pesti- period, the economic impact of S. exigua
cide treadmill as bollworm populations were increased to nearly 7%. Since the boll-weevil
released from biological controls by early- programme ended, the economic impact has
season sprays. Cotton production in the remained at less than 1% (Haney et al., 2001).
southern USA remained heavily dependent Ruberson et al. (1994) concluded that the pes-
on insecticides until the boll-weevil eradica- ticidal disruption of biological controls was a
tion programme. key factor in the outbreaks of this typically
Intense pesticide application was a key minor and sporadic pest.
element of the boll-weevil eradication pro- The IPM advantages of boll-weevil eradi-
gramme (Haney et al., 2001). In 1987, the cation are also clear for major cotton pests
Georgia programme added an average of 8.4 like bollworms, H. zea and H. virescens.
treatments per acre of azinphos-methyl to Before boll-weevil eradication, annual eco-
the normal in-season spray schedule. In nomic losses from these two pests averaged
total, more than 287,000 lb. of azinphos- more than 26% of the cotton value in
methyl was applied. In 1988 and 1989, each Georgia. After boll-weevil eradication, the
cotton acre received an average of 9.1 and economic impact of bollworms fell to
12.4 additional applications, respectively, of approximately 8.5% annually (Haney et al.,
malathion; nearly 350,000 lb. of malathion 2001). A key reason for this decline is the
was applied each year. abundance of natural control agents that
After the first 3 years, pesticide applica- attack bollworms; until the eradication pro-
tions to control boll-weevil dropped substan- gramme, insecticides applied for boll-weevil
tially. In 1990, the average number of also eliminated most biocontrol agents.
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172 P. Guillebeau

Pesticides and Biological Controls suspected. In a pecan study, pyrethroids

were not toxic to larvae and adult stages of
Every pesticide is compatible with some the predatory lacewing, Chrysoperla rufilabris
other IPM techniques. Pesticide applications (Bermeister), but organophosphates and car-
do not preclude cultural controls, such as bamates were (Mizzell and Schiffhauer,
ploughing, host-plant resistance or physical 1990). Conversely, pyrethroids were toxic to
barriers, such as screens or mesh. As the def- the predatory lady beetle, Olla v-nigrum Say,
inition and techniques of IPM have evolved, but the organophosphates phosalone, methi-
however, there is greater emphasis on bio- dathion, ethion and malathion were rela-
logical control organisms. Currently, biologi- tively non-toxic. All of the pyrethroids and
cal control relates chiefly to the management the organophosphates tested were toxic to
of insects although there are examples of bio- another lady beetle, Hippodamia convergens
logical control agents for weeds and plant (Guerin-Meneville), but lindane was not.
diseases. The impacts upon beneficial populations
vary even within a single class of pesticides.
Among the pyrethroids, Wright and Verkerk
Pesticides and biological control of insects (1995) report that cypermethrin is generally
less toxic than permethrin to parasitoids;
Many pesticides have broad-spectrum activ- however, the reverse is true against preda-
ity against a variety of insects. A 1956 review tors. Similarly, the organophosphates com-
of the literature found a large number of prise many of the compounds that have the
studies that discuss the effects of pesticides greatest impact on beneficial populations,
on populations of beneficial arthropods but some of the compounds are much less
(Ripper, 1956). Similar reports throughout damaging to natural enemies (Theiling and
the years have demonstrated that insecti- Croft, 1988). A new class of chemicals, the
cides can devastate populations of beneficial neonicotinoids, also vary in effects on preda-
insects (Turnipseed et al., 1975; Wilkenson et tory arthropods (Mizell and Sconyers, 1992).
al., 1979; Roach and Hopkins, 1981). Introduced in the 1990s, the neonicotinoid
However, even the impact of broad- imidacloprid is widely used, with activity
spectrum insecticides is unpredictable. against sucking insects (e.g. aphids) and
Predator resistance to pesticides has been some species of beetles, flies and moths
documented and even selected in some situ- (Elbert et al., 1990, 1991). Some spiders, some
ations. Guillebeau and All (1989) noted simi- predatory Coleoptera and some predatory
lar-sized populations of striped lynx spider, Heteroptera are tolerant of imidacloprid
Oxyopes salticus Hentz, in control plots and (Kunkel et al., 1999; Elzen, 2001), but other
plots treated with the organophosphate closely related Coleoptera and Heteroptera
insecticide, methyl parathion. Redmond and are highly susceptible to imidacloprid
Brazzel (1968) reported methyl-parathion (Delbeke et al., 1997; Sclar et al., 1998).
resistance in populations of O. salticus in an Bacillus thuringiensis is recommended for
area with a long history of methyl-parathion organic production and IPM because of its
use. Predatory mites have been selected in low risk to non-target organisms, including
laboratory and field trials for resistance to a biological control organisms (Abbott Labora-
variety of pesticides, including carbamates tories, 1982). However, even a biorational
and organophosphates (Croft and Stickler, like B. thuringiensis can interfere with IPM.
1983; Hoy, 1985). Trials with other predators The introduced cinnibar moth, Tyria jacobaeae
have not produced stable resistance at levels (Linnaeus), has been used successfully as a
that are valuable for field application biocontrol agent for the noxious weed tansy
(Adams and Cross, 1967; Grafton-Cardwell ragwort, Senecio jacobaea L. (McEvoy et al.,
and Hoy, 1986). 1991). B. thuringiensis may also be used in the
Other studies reported predator/para- same areas to control gypsy moth, Lymantria
sitoid tolerance of some non-selective insecti- dispar (Linnaeus), and western spruce bud-
cides even when resistance was not worm, Choristoneura occidentalis Freeman
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Risk–Benefit Analysis of Pesticides 173

(Morris, 1982). Some instars of cinnabar (Lowery and Sears, 1986; Morse and Zareh,
moth are killed by B. thuringiensis, and field 1991; James, 1997).
experiments suggest that B. thuringiensis The discussion of sublethal effects contin-
applications could interfere with IPM pro- ues indefinitely with many unanswered
grammes to manage tansy ragwort (James et questions if multitrophic effects, ecological
al., 1993). interactions, behavioural effects, etc. are
As a group, insecticides have the greatest included. An exhaustive treatise is beyond
impact on beneficial arthropod populations, the scope of this chapter, but Croft (1990)
but the potential effects of other types of pes- edited a comprehensive review of the rela-
ticides should also be considered in IPM pro- tionship between arthropod biological con-
grammes. The fungicide zineb is toxic to the trols and pesticides. Wright and Verkerk
parasitoid Trichogramma cacoeciae Marchal (1995) discuss multitrophic evaluation of
(Franz and Fabrietius, 1971; Van Driesche et pesticide applications.
al., 1998). Theiling and Croft (1988) and
Mizell and Schiffhauer (1990) report, how-
ever, that commonly used fungicides and Fungicides and biological control of insects
acaricides were compatible with arthropod
predators observed in a pecan study. Some Insect pests are attacked by naturally occur-
herbicides have also been shown to affect ring fungal pathogens. Early in the 20th cen-
beneficial populations (Theiling and Croft, tury, researchers noted that fungicide
1988). applications could result in the rebound of
Although the greatest impacts of pesti- arthropod pest populations (Rolfs and
cides have been reported on arthropod pop- Fawcett, 1908). Since that time, several stud-
ulations, pesticides may also affect ies have linked increases in pest populations
populations of vertebrate predators that feed to the fungicide effects on fungal ento-
on insects. The US EPA restricted the insecti- mopathogens; Olmert and Kenneth (1974)
cides carbofuran and diazinon because of provide a review of early experiments.
adverse effects on bird populations Modern pesticides can have similar
(EXTOXNET, 2002a,b). Triazine herbicides effects. Nomuraea rileyi Farlow fungus is a
have recently been shown to emasculate naturally occurring control agent for velvet
frogs and toads (Hayes et al., 2002). Other bean caterpillar, Anticarsia gemmatalis
broad-spectrum insecticides, such as aldicarb (Hubner). Johnson et al. (1976) showed that
and methyl parathion, are toxic to a wide applications of benomyl alone and in combi-
range of vertebrate insect predators occur- nation with insecticides reduced the infection
ring in agricultural production systems rate of velvet bean caterpillar up to tenfold,
(EXTOXNET, 2002c). with a concomitant reduction in yield.
Sublethal effects of pesticides further Aphids are a serious pest of pecans and
complicate the impact of pesticides on bene- cotton; naturally occurring epizootics caused
ficial arthropods. Bracon hebetor Say laid by fungi help control populations. This phe-
fewer viable eggs after sublethal exposure to nomenon is of particular interest because
the carbamate insecticide carbaryl (Grosch, pecan aphid pests are resistant to many insec-
1975). Parker et al. (1976) reported decreased ticides (Dutcher, 1983; Dutcher and Htay,
fecundity for the coccinellid Menochilus sex- 1985). Pickering et al. (1990) reported that
maculatus (Fabricius) after sublethal doses of aphid mortality due to fungal infection was
malathion, an organophosphate. Repellent significantly reduced in pecans by the appli-
effects of pyrethroid insecticides have been cation of triphenyltin hydroxide fungicide.
reported since the 1980s (Riedl and Hoying, Smith and Hardee (1996) discovered that the
1983; Jacobs et al., 1984). Sublethal exposures application of a granular fungicide at plant-
to imidacloprid, azinphos-methyl (organo- ing could reduce the prevalence of the ento-
phosphate), carbaryl or malathion have mopathogenic fungus Neozygites fresenii
increased egg production in some pest Batkow, which helps control populations of
arthropods and some predatory arthropods the cotton aphid Aphis gossypii Glover.
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174 P. Guillebeau

In many areas of potato (Solanum tubero- An IPM strategy is the focus of most
sum L.) production, growers must protect the noxious-weeds programmes, including pes-
crop from a major insect pest, Colorado ticides and biological controls. It is important
potato beetle, Leptinotarsa decemlineata (Say), to use pesticides selectively to avoid disrup-
and fungal diseases (primarily early blight, tion of the biological components of the IPM
Alternaria solani (Ell. and Mart.) Jones and programme.
Grout, and late blight, Phytophthora infestans The California Department of Food and
(Mont. de Bary). The Colorado potato beetle Agriculture has several projects to control
is of particular concern because this pest has noxious weeds in non-agricultural settings.
become resistant to nearly every available As part of their programme to control purple
insecticide (Insecticide Resistance Action loosestrife (Lythrum salicaria L.), the
Committee, 2003). Additionally, environmen- Department releases two species of leaf bee-
tal risks escalate as growers apply higher tle (Galerucella spp.) that attack this weed.
rates of pesticides to control resistant popu- However, these beetles are considered to be
lations of Colorado potato beetle. very susceptible to pesticides, and newly
Research suggests that the fungal released colonies should be protected from
pathogen Beauvaria bassiana (Balsamo) broad-spectrum insecticides (Pitcairn,
Vullemin may be a useful biological control California, 2003, personal communication).
agent for Colorado potato beetle (Boiteau, Several releases of Galerucella spp. were
1988). If B. bassiana can be used effectively, made into riparian zones, but the beetles
growers would have an additional tool to could not be found shortly after release
manage resistance. Furthermore, B. bassiana (Pitcairn, California, 2003, personal commu-
would not have many of the undesirable nication). Repeated, similar incidents caused
environmental consequences associated with the project team to investigate and speculate
broad-spectrum conventional insecticides. about possible causes. Although the disap-
Using B. bassiana to control Colorado potato pearance of the beetles was not resolved
beetle in potatoes is challenging because dis- with certainty, the team conjectured that
ease management in potatoes relies on regular malathion applications made to control mos-
applications of fungicides (University of Idaho, quitoes in the riparian zone also killed the
1999). Todorova et al. (1998) reported that field beetles. The North Dakota State University
applications of six common fungicides Extension Service (1997) and bulletins from
(chlorothalonil, maneb, thiophanate-methyl, other states caution that insecticides used for
mancozeb, metalaxyl + mancozeb, and zineb) adult mosquito control will also kill
inhibited the growth and sporulation of B. Galerucella beetles.
bassiana; a herbicide, glufosinate-ammonium, Water hyacinth, Eichhornia crassipes Mart.,
also inhibited B. bassiana. Surprisingly, the is the target of another California weed con-
herbicide diquat synergized the insecticidal trol project. Neochetina spp. weevils attack
activity of B. bassiana. Other researchers found water hyacinth, and they are a component of
similar results using chlorothalonil and man- the California strategy. However, herbicides
cozeb (Jaros-Su et al., 1999). However, they are also widely used to control hyacinth. If
reported that applications of the fungicide the hyacinth is killed before the weevils com-
copper hydroxide had relatively little effect on plete development, the weevils also die.
B. bassiana, suggesting that it may be possible During the 1980s and 1990s, the programme
to integrate B. bassiana with some types of to release Neochetina spp. weevils was nearly
fungicides. scuttled because other programmes were
applying herbicides to water hyacinth in the
weevil-release areas (Pitcairn, California,
Pesticides and biological control of weeds 2003, personal communication). Eventually,
better cooperation and communication
The US federal government and numerous between the various programmes fostered
state agencies have programmes to actively the use of both herbicides and weevils as
control noxious weeds (USDA-APHIS, 2002). part of an IPM programme.
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Risk–Benefit Analysis of Pesticides 175

Many states have IPM programmes to of pesticide use. However, organic growers
control the invasive musk thistle, Carduus still need pesticides, although they are lim-
nutans L. The head weevil, Rhinocyllus conicus ited to a list of pesticides approved for
Froelich, and the rosette weevil, Trichosirocalus organic production. The particular chemicals
horridus (Panzer), are biological control agents vary somewhat with the government or
released to help control musk thistle. organization certifying organic production.
Herbicide applications are also commonly Insecticidal soaps and oils are permitted in
used to manage musk thistle. If the herbi- most programmes. Natural products, such as
cides are applied while the weevils are still in pyrethrum and rotenone, are also widely
the larval stage, the weevils are killed along accepted (Frick, 2002). In the USA, there is an
with the plant. To provide maximum protec- official National List of Allowed and Prohibited
tion for the weevils, herbicide should not be Substances for growers that wish to be certi-
applied to musk thistle in Oklahoma from fied as organic by USDA (USDA, 2002). Like
mid-May to mid-July. However, late May is a conventional operations, organic production
good time for growers to apply a single tries to use pesticides in ways that are com-
application of herbicide to control a spectrum patible with other pest-management tech-
of weeds (Medlin et al., 2003). Because musk niques.
thistle is a ubiquitous problem, conflict may In his review, Ripper (1956) points out
arise between adjacent properties if all parties that biological controls and pesticides are
do not control for thistle. Unlike herbicide important components of pest-management
application, weevil release does not produce systems. He suggests that research should
an immediate, obvious effect on musk thistle. aim to reduce the negative impacts of pesti-
The Oklahoma Extension Service has devel- cides in two ways: (i) manipulate application
oped a sign to indicate a weevil-release site, techniques for non-selective pesticides; and
so that nearby property owners will not think (ii) develop selective pesticides with fewer
that no action was taken against musk thistle adverse effects on beneficial populations.
(Bolin, Oklahoma, 2003, personal communi- The quarantine use of pesticides is an
cation). important tool for IPM because new pest
species do not become established.
Quarantines often mandate the use of pesti-
Making Pesticides More Compatible with cides. For example, nursery stock, grass sod
IPM and other regulated articles cannot be
shipped out of the US quarantine area for
Clearly, pesticides can have a variety of neg- imported fire ants until the materials have
ative impacts on populations of biocontrol been treated with an approved insecticide
agents. However, the effects are largely (USDA-APHIS, 1997). Japan requires fumiga-
unpredictable, even within closely related tion of plant materials with methyl bromide
groups of organisms or chemical classes. or approved substitutes if foreign pests are
Even with risk and uncertainty, however, detected (Japanese Market Information, 2002).
pesticides remain a critical component of Although quarantine use of pesticide is a criti-
IPM. Van Emden (2002) calls chemical con- cal tool for IPM, there is little or no impact on
trol, biological control, cultural control and beneficial populations of arthropods.
host-plant resistance the four main building- Even though pesticides are the primary
blocks of IPM. Pesticides will continue to be method of control recommended for many
an integral and necessary part of IPM for the turf pests, producers are implementing new
foreseeable future, especially in cropping ideas to attenuate the unwanted effects of
systems with multiple pests (Graves et al., pesticides. Sampling schemes and degree-
1999). The challenge for pest managers is to day models have been developed for the
use pesticides in ways that maintain the chinch bug complex, Blissus leucopterus
value of the other IPM components. Montandon, Blissus inularis Barber and
To many people, organic farming is the Blissus leucopterus (Say), and identification of
antithesis of conventional farming in terms the species combination determines the need
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176 P. Guillebeau

for insecticide applications (Reinert et al., row, while the seeds are placed at discrete
1995). The Handbook of Turfgrass Insect Pests, intervals within the row. A new technique lim-
edited by Brandenburg and Villani (1995), its the pesticide application to the row space
provides an overview of turf IPM and the adjacent to the seeds. Lohmeyer et al. (2003)
role of pesticides for management of other report that precision placement of the pesti-
turf insect pests. cide may reduce the pesticide rate by more
Pesticide selectivity can be improved by than 50% without sacrificing efficacy. Growers
manipulating spray parameters, such as still gain the benefits of the pesticides in their
placement or timing. Watson (1975) reported IPM programmes, but the impacts on benefi-
that applying azinphos-methyl to the lower cial populations are greatly reduced.
two-thirds of the plant could control cotton Spot applications, alternate-row middle
pests as predatory anthocorids (Orius spp.) applications, precision applications and
increased in the upper third of the plant. selective spray timing all create spatial or
Applying herbicides around the base of cot- temporal refugia for beneficials where they
ton plants conserved a complex of beneficial do not come in contact with the pesticide.
arthropods (Stam et al., 1978). Effective use of refugia requires thorough
Careful timing of pesticide applications knowledge of the interactions between the
minimizes contact between the beneficial plant, the pest and the biocontrol agent, and
organism and the pesticide. It was already information about how the interactions
recognized in the 1950s that the proper tim- change over time (Verkerk, 2002). Few stud-
ing of dichlorodiphenyltrichloroethane (DDT) ies of tritrophic interactions have been pub-
applications minimized negative impacts on lished; more data are needed to use refugia
beneficials in walnut and melon pest- more effectively (Verkerk et al., 1998).
management systems (Michelbacher and Scientists recognized early that pesticide
Middlekauff, 1950; Bartlett and Ortega, 1952). selection was an important factor in preserv-
Applications of paraquat or glyphosate to ing beneficial populations (Lord, 1949;
control orchard weeds during the spring Ripper et al., 1951; Bartlett, 1952; van den
harms populations of the predatory mite Bosch and Stern, 1962). Growers now have
Neoseiulus fallacies Garman occupying the greater flexibility as pesticide companies
ground cover (Pfeiffer, 1986); herbicide appli- introduce products with fewer impacts on
cations made in the autumn have much less beneficial arthropods. Rapid-CP (2002) uses
impact on the predatory mites because most data from the USDA Interregional Research
of them have moved into the tree canopy. Project Number 4 and USDA Office of Pest
Selective techniques enhance the role of Management policy to create a comprehen-
pesticides in IPM for apples, peaches and sive database to track potential, pending and
other stone fruits. Alternate-row middle recently registered new products.
spraying is a recommended practice in some Pymetrozine, indoxacarb, spinosad, bifen-
circumstances (Horton et al., 2002; zate, methoxyfenozide, tebufenozide and
Washington State University, 2002). Growers pyriproxyfen are new insecticides that are
apply pesticide only to the middle of every reported to have low toxicity for beneficial
other row; this method reduces pesticide insects. Because of EPA incentives to register
impacts on beneficial organisms. Ironically, reduced-risk pesticides, growers will proba-
increasing herbicide use improves insect- bly have an increased number of options
pest management. Stinkbugs and plant bugs with fewer effects on biological controls.
are key pests of stone fruits in the southern Formulation can also improve the selectiv-
USA because these insects scar the fruit. This ity of pesticides. Ripper et al. (1948) demon-
complex of pests is less common in orchards strated that a coating of cellulose made
with effective broadcast control of broad- insecticide significantly less toxic to benefi-
leaved weeds (Horton et al., 2002). cials, although there was only a slight reduc-
Pesticides are often applied at planting to tion in efficacy against the target pests. Franz
control early-season pests. Typically, the pesti- and Fabrietius (1971) reported that rates of
cide is applied in a continuous stream in the parasitism varied from 2 to 89% in the pres-
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Risk–Benefit Analysis of Pesticides 177

ence of various formulations of zineb. cotton caused high mortality for the het-
Parasitism may be affected by either the inert eropteran Nabis and Geocoris spp., but popu-
ingredients or some interaction between the lations of spiders, Chrysoperla larvae and
pesticide and the inert ingredients. hymenopteran parasitoids were nearly unaf-
In general, dust formulations are more fected (Ridgeway et al., 1967). In rice and cot-
toxic to beneficials than wettable powders or ton, the affected predator species were
emulsifiable concentrates. Bartlett (1951) facultative plant feeders.
demonstrated that dusts can kill hymenop- The EPA classifies pheromones as pesti-
teran parasitoids even in the absence of a cides even though they often have a non-
pesticide. Carbamate and organophosphate toxic mode of action. Additionally,
insecticides were more toxic to spiders when pheromones typically affect a single species
applied as dusts instead of emulsion (Yoo et or a small group of closely related species
al., 1984). Encapsulation of pesticide can (Nordland et al., 1981). Consequently,
increase selectivity, but results vary. Dahl pheromones have little or no effect on bio-
and Lowell (1984) reported 70–100% mortal- logical control agents in most cases.
ity for nabids and coccinellids in lucerne Pheromones are used directly to disrupt
sprayed with encapsulated methyl parathion mating in a number of lepidopteran pest
but little or no mortality for spiders. They species, including codling moth, Cydia
further recounted low mortality for coccinel- pomonella (Linnaeus), and pink bollworm,
lids and high mortality for hymenopterans Pectinophora gossypiella Saunders (Carde and
in cotton treated with encapsulated methyl Minks, 1995). Pheromones are commonly
parathion. Asquith et al. (1976) and Hull used to monitor pest populations so that pes-
(1979) found that encapsulated methyl ticide applications can be made at the opti-
parathion had little or no effect on mite mum time and place. Pheromones and/or
predators found on apple trees. food baits are also used in combination with
Greater pesticide selectivity is sometimes toxic agents. Programmes to contain or erad-
gained with granular formulations. Foliar icate Mediterranean fruit fly populations
pesticide applications to control lesser corn- typically include a combination of an attrac-
stalk borer on groundnuts disrupted natural tant and a poison (Roessler, 1989). As more
controls and promoted secondary outbreaks pheromones become available, pest man-
of mites and lepidopteran pests, but granular agers will have greater flexibility to integrate
formulations controlled the pest without sec- pesticides into IPM.
ondary problems (Newsom et al., 1976). Baits do not always provide as much
Granular applications of carbofuran and selectivity as pheromones because they can
thiofanox did not significantly reduce num- attract a broader range of arthropods. Nasca
bers of coccinellids, chrysopids or para- et al. (1983) reported that malathion bait
sitized aphids in barley, but foliar applications to control fruit flies were less
applications of the same materials caused toxic to predacious lacewings. Surprisingly,
substantial reductions (Ba-Angood and greater selectivity was gained by applying
Stewart, 1980). the bait to the entire tree instead of offering
Using pesticides systemically will protect the bait on plastic strips. Conversely, Ehler et
populations of some kinds of beneficial al. (1984) found that a malathion-bait spray
arthropods. Ripper (1957) showed that sys- applied for fruit flies greatly reduced popu-
temic use of schradan and oxydemeton- lations of gall-midge parasitoids, allowing
methyl had little or no effect on predatory gall-midge populations to increase 90-fold.
coccinellids or syrphids. Populations of the
spider Lycosa pseudoannulata Boesenberg
were not greatly reduced by systemic use of Policies to Improve Compatibility of
carbofuran on rice, but populations of the Pesticides and IPM
predatory bug, Cyrtorhinus lividipennis
Reuter were nearly eliminated (Dyck and Pest Management and the Environment in 2000
Orlido, 1977). Systemic use of aldicarb on was an international symposium to discuss
08IntpestManCh8.QXD 14/4/04 2:25 pm Page 178

178 P. Guillebeau

the future of pest management (Aziz et al., tain high crop yields. At the end of 2001, the
1992). One conclusion was that pesticides EPA had listed approximately 195 registered
would continue to be an essential compo- biopesticide active ingredients and 780 prod-
nent of IPM (Perfect, 1992). He also points ucts (US EPA BPPD, 2002a).
out a common paradox of pesticides and The OPP reduced-risk programme
IPM. Misapplication of pesticides is the encourages the registration of conventional
greatest threat to many IPM programmes; pesticides that fit low-risk criteria, including
however, the overuse of pesticides may also compatibility with IPM (OPP, 2002). The EPA
be the impetus for IPM with greater empha- offers greatly reduced registration time as an
sis on non-chemical controls. Resistance to economic incentive. Reduced-risk pesticides
pyrethroid insecticides caused Helicoverpa are registered in an average of 16 months
armigera (Hubner) to become one of the most versus 38 months for a conventional pesti-
economically damaging pests in Indian agri- cide not classified as reduced risk. The pesti-
culture (Sharma, 1991). In response, the cide can be marketed sooner, and the
Indian Council of Agricultural Research registrant has several more growing seasons
instigated a major programme for natural with their pesticide under patent.
controls of H. armigera, including nuclear The USDA developed a strategic plan for
polyhedrosis virus and parasitoid wasps IPM that was released in 2003 (IPM, 2002).
(Perfect, 1992). Among other goals, the plan defines specific
Although the future of IPM includes pes- targets to reduce levels of hazardous pesti-
ticides, new chemicals will be quite different cides detected in surface drinking-water
from the broad-spectrum pesticides first supplies and pesticide residues in the major
developed for agricultural-pest manage- foods consumed by infants and children. The
ment. The EPA Office of Pesticide Programs strategy calls for alternatives to pesticides
(OPP) has several programmes to accelerate that result in unacceptable residue levels in
the introduction of pesticides with fewer food-crop commodities. The USDA plan
risks to the environment, including biological clearly recognizes the role of pesticides in
control organisms (Andersen et al., 1996). The IPM. One target calls for improvement of
EPA 25b rule exempts very low-risk prod- pesticide application methods, timing and
ucts, including some biological agents and placement that results in improved efficacy
common food substances (e.g. eugenol and with reduced pesticide residues in raw agri-
soybean oil), from regulation; a complete list cultural commodities.
of 25b-exempted materials can be found In some European countries, laws were
on the Internet (http://www.epa.gov/ not specifically crafted to promote IPM, but
oppbppd1/biopesticides/regtools). Regula- growers are likely to use more non-chemical
tory relief will encourage research and mar- pest-control methods as pesticides become
keting of these products because a large less available. Sweden, Denmark and The
investment will not be necessary to fulfil Netherlands mandated a 50% or greater
EPA requirements for registration of conven- reduction in total pesticide use by 2000
tional pesticides. (Matteson, 1995). Sweden’s plan included
Andersen et al. (1996) report that the regional plant-protection centres promoting
Biopesticides and Pollution Prevention IPM.
Division (BPPD) of OPP streamlines the A number of developing countries pro-
registration process for biological pesticides, mote IPM or pesticide reduction through
including microbials, plant-incorporated official policies or regulation (Elkstrom,
protectants and biochemicals active through 2002). China introduced the Green Certificate
a non-toxic mode of action (e.g. pheromone programme and banned highly toxic pesti-
traps). Biopesticides generally affect only the cides from vegetable crops. Biological control
target pest and closely related organisms (US is a national priority for Cuba; the new pol-
EPA BPPD, 2002b). As part of an IPM pro- icy is intended to make IPM biointensive,
gramme, biopesticides can greatly decrease with 80% of pests managed through biologi-
the use of conventional pesticides and main- cal control. Iran formed the High Council of
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Risk–Benefit Analysis of Pesticides 179

Policy and Planning for Reduction of pesticides. The most efficient and sustainable
Agricultural Pesticides. A National IPM IPM programmes will recognize a critical
Committee in Malaysia is reducing pesticide role for pesticides.
use and increasing farmer knowledge of As IPM and pesticides evolve, the use of
other pest-management techniques. Nepal, pesticides is likely to increase as new chemi-
the Philippines, Sri Lanka and Indonesia cals and new application techniques make
have adopted national IPM policies. The pesticides more compatible with biological
Food and Agriculture Organization and the controls and other IPM components. The
World Health Organization work with the pesticide industry is emphasizing new prod-
international community and developing ucts with greater selectivity for natural ene-
nations to develop pesticide policy, but mies and minimal environmental impact
many developing countries have only rudi- (Sengonca, 2002). Governmental programmes
mentary regulation of pesticide use and regulations encourage the introduction
(Schaefers, 1996). of pesticides with fewer non-target effects.
Although most growers incorporate some Improved application techniques allow us to
elements of IPM (e.g. monitoring for pests), use pesticides more precisely, with less off-
many modern production systems are overly target deposition. Research is providing
dependent on pesticides that disrupt natural greater insight into interactions between bio-
controls. Reliance on pesticides has undoubt- logical controls, pests, hosts and pesticides.
edly slowed the progress of IPM. Pest man- This knowledge will help IPM practitioners
agement should not be chemically use pesticides in ways that conserve natural
dependent, but it is imprudent to ignore the controls.
benefits associated with the judicious use of

References

Abbott Laboratories (1982) Toxicology Profile: Dipel, Bacillus thuringiensis Insecticide. Chemical and
Agricultural Products Division, Chicago, Illinois.
Adams, C.H. and Cross, W.H. (1967) Insecticide resistance in Bracon mellitor, a parasite of the boll weevil.
Journal of Economic Entomology 60, 1016–1020.
Andersen, J., Leslie, A., Matten, S. and Kumar, R. (1996) The Environmental Protection Agency’s pro-
grams to encourage the use of safer pesticides. Weed Technology 10, 966–968.
Anon. (1917) Annual Report of the Georgia Department of Agriculture. Georgia Department of Agriculture
Monthly Bulletin 5, 130–131.
Anon. (1940) Annual Report of the Georgia Agriculture Extension Service. Georgia Agriculture Extension
Service, pp. 5–7
Anon. (1993) Agricultural Statistics 1993. National Agricultural Statistics Service, USDA, Washington, DC,
57 pp.
Asquith, D., Hull, L.A. and Mowry, P.D. (1976) Apple, tests of insecticides (1975). Insecticide and Acaracide
Tests 1, 17–19.
Aziz, A., Kadir, S.A. and Barlow, H.S. (eds) (1992) Pest Management and the Environment in 2000. CAB
International, Wallingford, UK, 401 pp.
Ba-Angood, S.A. and Stewart, R.K. (1980) Effect of granular and foliar insecticides on cereal aphids and
their natural enemies on field barley in southwestern Quebec. Canadian Entomologist 112, 1309–1313.
Bartlett, B.R. (1951) The action of certain inert dust materials on parasitic hymenoptera. Journal of
Economic Entomology 44, 891–896.
Bartlett, B.R. (1952) A study of insecticide resistance in strains of Drosophila melanogaster. Canadian
Entomologist 84, 189.
Bartlett, B.R. and Ortega, J.C. (1952) Relation between natural enemies and DDT-induced increases in
frosted scale and other pests of walnuts. Journal of Economic Entomology 45, 783–785.
Boiteau, G. (1988) Control of the Colorado potato beetle Leptinotarsa decemlineata: learning from the Soviet
experience. Bulletin of the Entomological Society of Canada 20, 9–15.
van den Bosch, R. and Stern, V. (1962) The integration of chemical and biological control of arthropod
pests. Annual Review of Entomology 7, 367–368.
08IntpestManCh8.QXD 14/4/04 2:25 pm Page 180

180 P. Guillebeau

Brandenburg, R.L. and Villani, M.G. (eds) (1995) Handbook of Turfgrass Insect Pests. Entomological Society
of America Press, Lanham, Maryland, 140 pp.
Carde, R.T. and Minks, A.K. (1995) Control of moth pests by mating disruption: successes and con-
straints. Annual Review of Entomology 40, 559–586.
Coad, B.R. (1920) Killing boll weevils with poison dust. United States Department of Agriculture Yearbook
1920, 241–252.
Croft, B.A. (1990) Arthropod Biological Control Agents and Pesticides. John Wiley & Sons, New York, 723 pp.
Croft, B.A. and Stickler, K. (1983) Natural enemy resistance to pesticides: documentation, characteriza-
tion, theory and application. In: Georghiou, G.P. and Saito, T. (eds) Pest Resistance to Pesticides.
Plenum, New York, pp. 669–702.
Dahl, G.H. and Lowell, J.R. (1984) Microencapsulated pesticides and their effects on nontarget insects. In:
Scher, H.B. (ed.) Advances in Pesticide Formulation Technology. American Chemical Society,
Washington, DC, pp. 141–150.
Delbee, F., Vercruysse, P., Tirry, L., DeClerq, P. and Degheele, D. (1997) Toxicity of diflubenzuron,
pyriproxyfen, imidacloprid, and diafenthruion to the predatory bug, Orius laevigatus (Heteroptera:
Anthocoridae). Entomophaga 42, 349–358.
Dutcher, J.D. (1983) Pecan pest management – where are we? In: Payne, J.A. (ed.) Pecan Pest Management
– Are We There? Miscellaneous Publication 13, Entomological Society of America, College Park,
Maryland, pp. 133–140.
Dutcher, J.D. and Htay, U.T. (1985) Impact assessment of carbaryl, dimethoate, and dialifor on foliar
pecan and nut pests of pecan orchards. Journal of the Georgia Entomological Society 18, 495–507.
Dyck, V.A. and Orlido, G.C. (1977) Control of the brown planthopper, Nilaparvata lugens, by natural
enemies and timely application of narrow-spectrum insecticides. International Rice Research Institute
Annual Report 1976, 28–72.
Ehler, L.E., Endicott, P.C., Herlein, M.B. and Alvarado-Rodriguez, B. (1984) Medfly eradication in
California: impact of malathion bait sprays on an endemic gall midge and its parasitoids.
Entomologia Experimentalis et Applicata 36, 201–208.
Elbert, A., Overbeck, H., Iwaya, K. and Tsuboi, S. (1990) Imidacloprid, a novel systemic nitromethylene
analogue insecticide for crop protection. Proceedings Brighton Crop Protection Conference on Pests and
Diseases 1, 21–28.
Elbert, A., Becker, B., Hartwig, J. and Erdelen, C. (1991) Imidacloprid: a new systemic insecticide.
Pfanzenshutz Nachrichten Bayer 44, 113–116.
Elkstrom, G. (2002) Pesticide reduction in developing countries. In: Pimentel, D. (ed.) Encyclopedia of Pest
Management. Marcel Dekker, New York, pp. 598–605.
Elzen, G.W. (2001) Lethal and sublethal effects of insecticide residues on Orius insidiosus (Hemiptera:
Anthocoridae) and Geocoris punctipes (Hemiptera: Lygaeidae). Journal of Economic Entomology 94,
55–59.
EXTOXNET (2002a) Pesticide information profiles: diazinon. Available at: http://ace.orst.edu/cgi-bin/
mfs/01/pips/diazinon.htm
EXTOXNET (2002b) Pesticide information profiles: carbofuran. Available at: http://ace.orst.edu/
cgi-bin/mfs/01/pips/carbofur.htm
EXTOXNET (2002c) Pesticide information profiles: aldicarb. Available at: http://ace.orst.edu/cgi-bin/
mfs/01/pips/aldicarb.htm
Flint, M.L. and van den Bosch, R. (1981) Introduction to Integrated Pest Management. Plenum Press, New
York, 240 pp.
Floyd, D.L. and Treanor, K. (1944) Georgia agricultural facts. University of Georgia Agriculture Extension
Service Bulletin 511, 28–29.
Franz, J.M. and Fabrietius, K. (1971) Testing the sensitivity to pesticides of entomophagous arthropods –
trials using Trichogramma. Zeitschrift für Angewandte Entomologie 68, 278–288.
Frick, B. (2002) Organic farming. In: Pimentel, D. (ed.) Encyclopedia of Pest Management. Marcel Dekker,
New York, pp. 554–557.
Frisbie, R.E. and Smith, J.W. Jr (1991) Biologically intensive integrated pest management: the future. In:
Menn, J.J. and Steinhauer, A.L. (eds) Progress and Perspectives for the 21st Century. Entomological
Society of America Press, Lanham, Maryland, pp. 151–64.
Gianessi, L.P. and Anderson, J.E. (1995) Pesticide Use in the U.S. Crop Production: National Summary Report.
The National Center for Food and Agricultural Policy, Washington, DC, 280 pp.
08IntpestManCh8.QXD 14/4/04 2:25 pm Page 181

Risk–Benefit Analysis of Pesticides 181

Grafton-Cardwell, E.E. and Hoy, M.A. (1986) Genetic improvement of common green lacewing,
Chrysoperla carnea (Neuroptera: Chrysopidae): selection for carbaryl resistance. Environmental
Entomology 15, 1130–1136.
Graves, J.B., Leonard, B.R. and Ottea, J.A. (1999) Chemical approaches to managing arthropod pests. In:
Ruberson, J. (ed.) Handbook of Pest Management. Marcel Dekker, New York, pp. 449–486.
Grosch, D.S. (1975) Reproductive performance of Bracon hebetor after sublethal doses of carbaryl. Journal
of Economic Entomology 68, 659–662.
Guillebeau, L.P. and All, J.N. (1989) Impact of weekly applications of selected new pyrethroids or
improved Bacillus thuringiensis Berliner on the arthropod predator complex in cotton. PhD disserta-
tion, University of Georgia, Athens, Gorgia.
Haney, P.B., Herzog, G. and Roberts, P.M. (2001) Boll weevil eradication in Georgia. In: Boll Weevil
Eradication in the U.S. through 1999. Cotton Foundation Reference Book Series No. 6, Memphis,
Tennessee, pp. 258–88.
Hayes, T., Haston, K., Tsui, M., Hoang, A., Haeffele, C. and Vonk, A. (2002) Feminization of male frogs in
the wild. Nature 419, 895–896.
Horton, D., Bellinger, B., Gorsuch, C. and Ritchie, D. (2002) Southeastern Peach, Nectarine, and Plum Pest
Management and Culture Guide. Bulletin 1171, Cooperative Extension Service, University of Georgia,
Athens, Georgia, 42 pp.
Hoskins, W.M., Borden, A.D and Michelbacher, A.E. (1939) Recommendations for a more discriminating
use of insecticides. In: Proceedings of the 6th Pacific Scientific Congress, Vol. 5, Davis, California,
pp. 119–123.
Hoy, M.A. (1985) Recent advances in genetics and genetic improvement of the Phytoseiidae. Annual
Review of Entomology 30, 345–370.
Hull, L.A. (1979) Apple, tests of insecticides 1978. Insecticide and Acaricide Tests 4, 20–22.
Hunter, W.D. (1917) The boll weevil program with special reference to means of reducing damage. USDA
Farmers’ Bulletin 848, 1–40.
Insecticide Resistance Action Committee (2003). Resistance depleting potato growers’ arsenal. Available
at: http://plantprotection.org/irac/Growers/Potato.htm
IPM (2002) IPM roadmap will be unveiled at meeting. Issue no. 105. Available at:
http://www.ipmnet.org/IPMnet_NEWS/news105.htm
Jacobs, R.J., Kouskolekas, C. and Gross, H. (1984) Responses of Trichogramma pretiosum (Hymenoptera:
Trichogrammatidae) to residues of permethrin and endosulfan. Environmental Entomology 13,
355–358.
James, D.G. (1997) Imidacloprid increases egg production in Amblyseius victoriensis (Acari: Phytoseiidae).
Experimental and Applied Acarology 21, 75–82.
James, R.R., Miller, J.C and Lighthart, B. (1993) Bacillus thuringiensis var. kurstaki affects a beneficial insect,
the cinnabar moth (Lepidoptera: arctiidae). Journal of Economic Entomology 86, 334–339.
Japanese Market Information (2002) Fresh fruits. Available at: http://www.pic.or.jp/jp/jmi/007.htm
Jaros-Su, J., Groden, E. and Zhang, J. (1999) Effects of selected fungicides and the timing of fungicide
application on Beauvaria bassiana induced mortality of the Colorado potato beetle. Biological Control
15, 259–269.
Johnson, D.W., Kish, L.P. and Allen, G.E. (1976) Field evaluation of selected pesticides on the natural
development of the entomopathogen, Nomuraea rileyi, on the velvet bean caterpillar in soybean.
Environmental Entomology 5, 964–966.
Kunkel, B.A., Held, D.W. and Potter, D.A. (1999) Impact of halofenozide, imidacloprid, and bendiocarb
on beneficial invertebrates and predatory activity in turfgrass. Journal of Economic Entomology 92,
922–930.
Lohmeyer, K.H., All, J.N., Roberts, P.M. and Bush, P. (2003) Precision application of aldicarb to enhance
efficiency of thrips (Thysanoptera: Thripidae) management in cotton. Journal of Economic Entomology
96, 748–754.
Lord, F.T. (1949) The influence of spray programs on the fauna of apple orchards in Nova Scotia II:
oystershell scale. Canadian Entomologist 79, 196–209.
Lowery, D.T. and Sears, M.K. (1986) Stimulation of reproduction of the green peach aphid (Homoptera:
Aphididae) by azinphosmethyl applied to potatoes. Journal of Economic Entomology 79, 1530–1533.
Martin, N.R., Nix, J.E., McArthur, W.C. and Brannen, S.J. (1968) Effects of alternative production practices
on costs and returns in producing cotton in selected areas of Georgia. University of Georgia College of
Agriculture Experimental Station–USDA Research Bulletin 34, 1–38.
08IntpestManCh8.QXD 14/4/04 2:25 pm Page 182

182 P. Guillebeau

Matteson, P.C. (1995) The 50% pesticide cuts in Europe: a glimpse of our future. American Entomologist 41,
210–220.
McEvoy, P., Cox, C. and Coombs, E. (1991) Successful biological control of ragwort, Senecio jacobaea, by
introduced insects in Oregon. Ecological Applications 4, 430–442.
Medlin, C., Bolin, P., Roduner, M. and Stritske, J. (2003) Integrated Control of Invasive Thistles in Oklahoma.
Bulletin F-7318 Stillwater, Oklahoma, Oklahoma Cooperative Extension Service, Oklahoma State
University.
Michelbacher, A.E. and Middlekauff, W.W. (1950) Control of the melon aphid in northern California.
Journal of Economic Entomology 43, 444–447.
Mizell, R.F. and Schiffhauer, D.E. (1990) Effects of pesticide on pecan aphid predators Chrysoperla
rufliabris (Neuroptera: Chrysopidae), Hippodamia convergens, Cylconeda sanguinea, Olla v-nigrum
(Coleoptera: Coccinellidae), and Aphelinus perpallidus (Hymenoptera: Encyrtidae). Journal of
Economic Entomology 83, 1806–1812.
Mizell, R.F. and Sconyers, M.C. (1992) Toxicity of imidacloprid to selected arthropod predators. Florida
Entomologist 75, 277–280.
Morris, O.N. (1982) Bacteria as pesticides: forest applications. In: Kurstak, E. (ed.) Microbial and Viral
Pesticides. Marcel Dekker, New York, pp. 239–287.
Morse, J.G. and Zareh, N. (1991) Pesticide induced hormoligosis of citrus thrips (Thysanoptera:
Thripidae) fecundity. Journal of Economic Entomology 84, 1169–1174.
Nasca, A.J., Fernandez, R.V., De Herrero, A.J. and Manzur, B.E. (1983) Incidence of chemical treatment for
control of fruit flies on chrysopids and hemerobiids on citrus trees. CITRON 1, 47–73.
National Research Council (1996) Ecologically Based Pest Management: New Solutions for a New Century.
National Academy, Washington, DC, 35 pp.
Newsom, L.D., Smith, R.F. and Whitcomb, W.H. (1976) Selective pesticides and selective use of pesti-
cides. In: Huffaker, C.B. and Messenger, P.S. (eds) Theory and Practice of Biological Control. Academic
Press, New York, pp. 565–591.
Nordland, D.A., Jones, R.L. and Lewis, W.J. (1981) Semiochemicals: Their Role in Pest Control. Wiley, New
York, 306 pp.
North Dakota State University Extension Service (1997) Biological control agents released for purple
loosestrife control. North Dakota Pesticide Quarterly 15, 9.
Olkowski, W. and Daar, S. (1991) Common Sense Pest Control. Taunton Press, Newtown, Connecticut,
715 pp.
Olmert, I. and Kenneth, R.G. (1974) Sensitivity of the entomopathogenic fungi to fungicides and insecti-
cides. Journal of Economic Entomology 31, 371–372.
OPP (2002) General overview: reduced-risk pesticide program. Available at: http://www.epa.gov/
oppfod01/trac/safero.htm
Parker, F.D., Ming, N., Pend, T. and Singh, G. (1976) The effect of malathion on fecundity, longevity, and
geotropism of Menochilus sexmaculatus. Environmental Entomology 5, 495–501.
Perfect, T.J. (1992) IPM in 2000. In: Aziz, A., Kadir, S.A. and Barlow, H.S. (eds) Pest Management and the
Environment in 2000. CAB International, Wallingford, UK, pp. 47–53.
Pfeiffer, D.G. (1986) Effects of field applications of paraquat on densities of Panonychus ulmi Koch and
Neoseiulus fallacies Garman. Journal of Agricultural Entomology 3, 322–325.
Pickering, J., Dutcher, J.D. and Ekbom, B.S. (1990) The effect of a fungicide on fungal-induced mortality
of pecan aphids in the field. Journal of Economic Entomology 83, 1801–1805.
Rainwater, C.F. and Gaines, J.C. (1951) Seasonal decline in the effectiveness of the certain insecticides
against boll weevil. Journal of Economic Entomology 44, 971–974.
Rapid-CP (2002) Recent Ag Products in Defence of Crop Plants. Available at: http://cipmtest.ent.ncsu.
edu/rapidcp/
Redmond, K.R. and Brazzel, B.R. (1968) Response of the striped lynx spider, Oxyopes salticus, to com-
monly used pesticides. Journal of Economic Entomology 61, 327–328.
Reinert, J.A., Heller, P.R. and Crocker, R.L. (1995) Pest information: chinch bugs. In: Brandenburg, R.L.
and Villani, M.G. (eds) Handbook of Turfgrass Insect Pests. Entomological Society of America Press,
Lanham, Maryland, pp. 38–42.
Ridgeway, R.L., Lingren, P.D., Cowan, C.B. and Davis, J.W. (1967) Populations of arthropod predators
and Heliothis spp. after applications of systemic insecticides to cotton. Journal of Economic Entomology
60, 1012–1016.
08IntpestManCh8.QXD 14/4/04 2:25 pm Page 183

Risk–Benefit Analysis of Pesticides 183

Ridgeway, R.L., Lloyd, E.P. and Cross, W.H. (1983) Cotton Insect Management with Special Reference to the
Boll Weevil. Agriculture Handbook 589, Agricultural Research Service, United States Department of
Agriculture, Washington, DC.
Riedl, H. and Hoying, S. (1983) Toxicity and residual activity of fenvalerate to Tryphlodromus occidentalis
(Acari: Tetranychidae) on pear. Canadian Entomologist 115, 807–813.
Ripper, W.E. (1956) Effect of pesticides on balance of arthropod populations. Annual Review of Entomology
1, 403–439.
Ripper, W.E. (1957) Selective insecticides and the balance of arthropod populations. Agricultural
Chemistry 12, 36–37, 103, 105.
Ripper, W.E., Greenslade, R.M., Health, J. and Barker, K. (1948) New formulation of DDT with selective
properties. Nature 161, 484.
Ripper, W.E., Greenslade, R.M. and Hartley, G.S. (1951) Selective insecticides and biological control.
Journal of Economic Entomology 44, 448–459.
Roach, S.H. and Hopkins, A.R. (1981) Reduction in arthropod predator populations in cotton fields
treated with insecticides for Heliothis spp. control. Journal of Economic Entomology 74, 454–457.
Roessler, Y. (1989) Insecticidal bait and cover sprays. In: Robinson, A.S. and Hooper, G. (eds) Fruit Flies,
Their Biology, Natural Enemies, and Control. Elsevier, Amsterdam, pp. 329–336.
Rolfs, P.H. and Fawcett, H.S. (1908) Fungus diseases of scale insect and whitefly. Bulletin, Florida
Agriculture Experiment Station, Gainesville, Florida, 17 pp.
Ruberson, J.R., Herzog, G.A., Lambert, W.R. and Lewis, W.J. (1994) Management of the beet armyworm
in cotton: role of natural enemies. Florida Entomologist 77, 440–453.
Schaefers, G.A. (1996) Status of pesticide policy and regulations in developing countries. Journal of
Agricultural Entomology 13, 213–222.
Sclar, D., Gerace, D. and Crenshaw, W.S. (1998) Observations of population increases and injury by
spider mites (Acari: Tetranychidae) on ornamental plants treated with imidacloprid. Journal of
Economic Entomology 91, 250–255.
Sengonca, L. (2002) Conservation of natural enemies. In: Pimentel, D. (ed.) Encyclopedia of Pest
Management. Marcel Dekker, New York, pp. 141–143.
Sharma, D. (1991) India battles to eradicate major crop pest. New Scientist 150, 10 August, 15.
Smith, M.T. and Hardee, D.D. (1996) Influence of fungicide on development of an entomopathogenic
fungus in the cotton aphid. Environmental Entomology 25, 677–687.
Smith, R.F. and van den Bosch, R. (1967) Integrated control. In: Wendell, W., Kilglore, W.W. and Doutt,
R.L. (eds) Pest Control: Biological, Physical and Selected Chemical Methods. Academic Press, New York,
pp. 295–340.
Stam, P.A., Clower, D.F., Graves, J.B. and Schilling, P.E. (1978) Effects of certain herbicides on some
insects and spiders found in Louisiana cotton fields. Journal of Economic Entomology 71, 477–480.
Theiling, K.M. and Croft, B.A. (1988) Pesticide side-effects on arthropod natural enemies: a database
summary. Agriculture, Ecosystems, and the Environment 21, 191–218.
Todorova, S.I., Coderre, D., Duchesne, R. and Cote, J. (1998) Compatibility of Beauvaria bassiana with
selected fungicides and herbicides. Biological Control 27, 427–433.
Turnipseed, S.G., Todd, J.W. and Campbell, W.V. (1975) Field activity of selected foliar insecticides
against geocorids, nabids, and spiders in soybeans. Journal of Entomological Science 10, 272–277.
United States (US) Congress Office of Technology Assessment (1995) Biologically Based Technologies for Pest
Control. US Government Printing Office, New York, 204 pp.
United States Department of Agriculture (USDA) (2002) National List of Allowed and Prohibited Substances.
The National Organic Program. Available at: http://www.ams.usda.gov/nop/
United States Department of Agriculture Animal Plant Health Inspection Service (USDA-APHIS) (1997)
Federal Domestic Quarantines. Available at: http://www.aphis.usda.gov/npb/F&SQS/usdaqua.html
United States Department of Agriculture Animal Plant Health Inspection Service (USDA-APHIS) (2002)
Federal Noxious Weed Program. Available at: http://www.aphis.usda.gov/ppq/weeds/
United States Environmental Protection Agency (US EPA) (2002a) Inception of Pesticide Environmental
Stewardship Program – IPM and Reduced Risk. Available at: http://www.epa.gov/oppbppd1/
PESP/inception.htm
United States Environmental Protection Agency (US EPA) (2002b) What is a pesticide? Available at:
http://www.epa./pesticides.
United States Environmental Protection Agency Biopesticides and Pollution Prevention Division (US EPA
BPPD) (2002a) Pesticides: biopesticides. Available at: http://www.epa.gov/oppbppd1/biopesticides/
08IntpestManCh8.QXD 14/4/04 2:25 pm Page 184

184 P. Guillebeau

United States Environmental Protection Agency Biopesticides and Pollution Prevention Division (US EPA
BPPD) (2002b) What are biopesticides? Available at: http://www.epa.gov/oppbppd1/biopesticides
University of Idaho (1999) Potato late blight. Available at: http://www.uidaho.edu/
ag/plantdisease/plbchc.htm
Vandeman, A.J., Fernandez-Cornejo, S., Jans, S. and Lin, B.H (1994) Adoption of Integrated Pest Management
in United States Agriculture. Bulletin No. 707, Economic Research Service Agriculture Information,
United States Department of Agriculture, 26 pp.
Van Driesche, R.G., Mason, J.L., Wright, S.E. and Prokopy, R.J. (1998) Effect of reduced insecticide and
fungicide on parasitism of leafminers (Phyllonorycter spp.) (Lepidoptera: Gracillariidae) in commer-
cial apple orchards. Environmental Entomology 27, 578–582.
Van Emden, H.F. (2002) Integrated pest management. In: Pimentel, D. (ed.) Encyclopedia of Pest
Management. Marcel Dekker, New York, pp. 413–415.
Verkerk, R.H.J. (2002) Refugia for pests and natural enemies. In: Pimentel, D. (ed.) Encyclopedia of Pest
Management. Marcel Dekker, New York, pp. 685–688.
Verkerk, R.H.J., Leather, S.R. and Wright, D.J. (1998) The potential for manipulating crop–pest–natural
enemy interaction for improved insect pest management. Bulletin of Entomological Research 88,
493–501.
Washington State University (2002) Crop Protection Guide for Tree Fruits in Washington. Washington State
University Cooperative Extension Service Bulletin EB0914, 84 pp. Available at: http://cru.cahe.wsu.
edu/CEPublications/eb0419/eb0419.pdf
Watson, T.F. (1975) Practical consideration in the use of selective insecticides against major crop pests. In:
Street, J.C. (ed.) Pesticide Selectivity. Marcel Dekker, New York, pp. 47–65.
Whitcomb, W.H. and Bell, K. (1964) Predaceous insects, spiders, and mites of Arkansas cotton fields.
Arkansas Agriculture Experiment Station Bulletin 690, 1–84.
Wilkenson, J.D., Biever, K.D. and Ignoffo, C.M. (1979) Synthetic pyrethroids and organophosphates
against the parasitoid, Apanteles marginventris and the predators Georcoris punctipes, Hippodamia con-
vergens, and Podisus maculiventris. Journal of Economic Entomology 72, 473–475.
Wright, D.J. and Verkerk, R.H.J. (1995) Integration of chemical and biological control systems for arthro-
pods: evaluation in a multitrophic context. Pesticide Science 44, 207–218.
Yoo, J.K., Kwon, U.W., Park, H.M. and Lee, H.R. (1984) Studies on the selective toxicity of insecticides for
rice insect pests and a predacious spider, Pirata subpiraticus. Korean Journal of Plant Protection 23,
166–171.
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9 Manipulation of Host-finding and

Acceptance Behaviours in Insects:
Importance to IPM

Richard S. Cowles
Connecticut Agricultural Experiment Station, Valley Laboratory, PO Box 248, Windsor,
CT 06095, USA
E-mail: [email protected]

Introduction Host Finding and Acceptance

Manipulating host-finding and acceptance The adult female of most insects is responsi-
behaviours can be used to shift much of a ble for finding appropriate hosts and laying
highly mobile and discriminating insect pop- eggs where the resources can sustain her
ulation to plants or traps outside our valued young. With a few notable exceptions (such
crops. Using a trap crop, insect-refuge crop, as ballooning larvae), the developing larvae
diversionary crop or mass trapping may of holometabolous insects have limited dis-
directly reduce the population density in the persal capabilities; therefore the host-seeking
valued crop below an economic threshold. and host-acceptance ‘decisions’ made by the
Behavioural manipulation alone may often mother determine to a large degree the spa-
be inadequate for plant protection, but, tial distribution of larvae within patchy and
when combined with appropriately chosen unpredictable environments and the success
antibiosis factors (insecticides or resistant or failure in larval development (Courtney
varieties), a pest-management system incor- and Kibota, 1989; Mayhew, 1997). For other
porating a behavioural dimension can yield mobile pests, such as adult hemipterans,
evolutionarily stable and favourable results. alate aphids and thrips, arrestment on hosts
The ability not only to prevent the evolution and subsequent feeding may lead to direct
of insecticide resistance but to select against crop injury and virus transmission (Kennedy
physiological resistance (both to insecticides et al., 1961). Insect behaviour adaptive for
and to varietal resistance) is an important selecting favourable hosts should involve the
outcome that could make behavioural relatively simple algorithm: move if the con-
manipulation an essential tool in modern ditions are poor, and stop (and either feed or
agriculture. Behavioural manipulation can lay eggs) if the conditions are good.
also lead to greater sustainability in agricul- The study of insect behaviour, physiol-
tural systems by improving the efficiency of ogy and chemical ecology contributes to the
biologically based population suppression understanding of the principles of host-
by concentrating the insect-pest population finding and acceptance by insects. With
in a pesticide-free diversionary crop. herbivorous insects, this has been a rich
area for study in the field of insect–plant
© CAB International 2004. Integrated Pest Management: Potential, Constraints and Challenges
(eds O. Koul, G.S. Dhaliwal and G.W. Cuperus) 185
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186 R.S. Cowles

Vision Olfaction Mechanoreception Gustation

External External
excitatory inhibitory
inputs inputs

Rolling
Internal fulcrum Internal
excitatory inputs inhibitory inputs
Accept Reject

Fig. 9.1. The rolling-fulcrum model for host-plant acceptance or rejection by insects. Sensory stimuli from
each sense may contain a mixture of positive and negative factors, which, when taken in balance,
determine the overall quality of the host. Acceptance or rejection events (for feeding or oviposition) are also
mediated by the physiological state of the insect, which is determined by internal hormonal factors and by
the negative feedback from host-acceptance or -rejection events. (Redrawn with permission from Miller and
Strickler, 1984.)

interactions. Insects use intensive examining stimuli (activants) contributes a downward

behaviours, during which cues from multi- ‘force’ on the left side. If there is sufficient
ple sensory modalities combine either syn- force, the left side of the balance is depressed
chronously or sequentially, while sampling so that it triggers a host-acceptance event.
the environment to measure the potential However, there are also sensory stimuli from
host’s qualities. All sensory modalities may deterrents or repellents that contribute a
participate: olfaction, taste (comprised of downward force on the opposing or
any contact chemoreception), vision and tac- inhibitory side. If these inhibitory stimuli
tile stimulation (Miller and Strickler, 1984; have sufficient ‘force’, the balance will tip
Harris and Miller, 1986; Papaj, 1986; sufficiently to trigger a host-rejection event.
Prokopy, 1986; Harris and Rose, 1990). At The physiological state influences the out-
the same time that host examining is taking come by determining the position of the ful-
place, the internal physiology of the insect crum, which rolls to the right under a state of
determines an acceptance threshold, which deprivation (hunger or absence of an ovipo-
governs whether those external stimuli are sitional outlet), thus making it easier for
sufficient to trigger consummatory behav- fewer or less intensely positive stimuli to
iours, such as sustained feeding or egg trigger a host-acceptance event. With satiety
laying. or depleted ovaries, the fulcrum would be
The interaction between external stimuli expected to roll far to the left, making host-
and internal physiological conditions was acceptance events unlikely. The arrows
investigated in pioneering work by Dethier beneath the rolling fulcrum indicate a
(1982), and later described by the physical negative-feedback control mechanism: each
analogy, the ‘rolling-fulcrum model’ (Miller acceptance event contributes a signal that
and Strickler, 1984). This physical model increases the internal inhibitory inputs,
depicts a seesaw (Fig. 9.1), where the sum of while rejection events increase internal exci-
behavioural inputs registering positive host tatory inputs.
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Host Finding and Acceptance in Insects 187

Insect behaviour cannot be expected to feeding bouts. With examples ranging from
work exactly like the physical model of the Thysanoptera to Orthoptera, Lepidoptera,
rolling fulcrum, because individuals may Diptera, Coleoptera and others, insects
change their response to the same set of cues appear to usually respond synergistically to
over time due to learning (Papaj, 1986; Papaj combinations of visual, chemical and tactile
and Prokopy, 1988; Bernays, 2001). The host cues (Harris and Miller, 1982, 1986;
rolling-fulcrum model may apply to two or Papaj, 1986; Gray and Borden, 1989; Harris
more levels of sensory integration, which and Rose, 1990; Judd and Borden, 1991;
introduces ambiguity into our understand- Szentesi et al., 1996). It is unlikely that all
ing of how sensory inputs affect behavioural host cues are simultaneously processed to
outcomes. Even at the level of the sensory generate an instantaneous ‘Gestalt’ (total
neurone, a well-defined stimulus can result image) of host-plant quality; rather, the
in different output depending on its complex insect is selectively ‘attentive’ to particular
interaction with other positive and negative subsets of stimuli during sequential habitat-
external stimuli and the insect’s physiologi- seeking, host-finding and examining behav-
cal condition. For example, in the generalist- iours (Bernays, 1996; Spencer et al., 1999). It
feeding gypsy moth, Lymantria dispar follows, then, that several examining behav-
(Linneaus), and tent caterpillars, Malacosoma iours may be required to fully assess host
americanum (Fabricius), the firing rate of qualities. For larger, strongly flying insects,
sugar receptors found on the maxillae was detection by receptive insects of host odours
modulated by the presence of tannins. Thus, can lead to odour-conditioned anemotaxis,
the caterpillar might sense the substrate con- which may take place as sustained flight or
taining the mixture of phagostimulants and short, hopping flights (Visser and de Jong,
deterrents as simply being less sweet than 1987; Haynes and Baker, 1989; Evans and
the same substrate without the presence of Allen-Williams, 1993, 1998; Byers, 1996;
tannins (Dethier, 1982). Therefore, the Szentesi et al., 1996; McDonald and Borden,
‘weight’ of the sugar stimulus apparently 1997; Petterson et al., 1998; Barata and
changes, depending on the combination of Araujo, 2001). Response to these odours may
other stimuli present, making a peripheral in turn lead to heightened responsiveness to
sense organ respond virtually instanta- appropriate visual cues (Bernays, 1996).
neously, like the rolling-fulcrum model. The Weaker fliers, such as aphids and thrips, may
ability within a single sensory modality to fly toward visual targets and simply settle on
integrate stimuli in a complex manner can to plants as a chemokinetic response (flight
make behavioural dissection of the response arrestment) upon intercepting appropriate
to host chemical stimuli very difficult. For odour cues (Teulon et al., 1999).
example, green-leaf volatiles are important Sequential processing of different aspects
in the response of Colorado potato beetle to of host stimuli could explain how informa-
hosts, and yet each component individually tion integrated over time leads to synergistic
has little effect on beetle behaviour (Visser responses, and gives some insight into the
and Ave, 1978). In another example, a combi- evolution of efficient information processing
nation of chemical compounds is required to in neurally constrained systems (Bernays,
evoke maximal upwind anemotactic 2001). Synergism in these instances at least
response to host volatiles (Evans and Allen- partly results from the effect a specific stimu-
Williams, 1998). lus has on the insect’s probability to transi-
Stimulus interaction can occur across sev- tion to the next finding or examining
eral modalities over time and space with the behaviour. For example, in my laboratory
whole animal, too. This is most easily comparison of onion-fly finding and examin-
observed with behavioural assays measuring ing behaviours on host models, landing on
the response of individuals or groups of red foliage was reduced by approximately
insects to host models. The simplest quanti- 45% compared with the green foliar model,
tative method is to count the behavioural equivalent to the per cent reduction in ovipo-
end result, such as numbers of eggs laid or sition. The presence of cinnamaldehyde
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188 R.S. Cowles

reduced oviposition by 86%, irrespective of evaluating sinigrin in overnight studies with

foliar colour, and did not measurably influ- caged moths, which can probably be attrib-
ence behavioural transition probabilities uted to their increased ovipositional depriva-
prior to substrate probing. The placement of tion. Alkanes and sinigrin in combination led
this ovipositional deterrent was at the base of to enhanced arrestment of moths on the sub-
the foliage model, allowing interruption of strate and rapidly proceeded to a critical
the transition from foliar-examining behav- examining behaviour and antennal swabbing
iours to ovipositor probing. When considered (seen only in the presence of joint presenta-
together, these two effects, foliar colour and tion of alkane and sinigrin), which usually
the presence of deterrents, are indeed syner- immediately preceded oviposition. Perhaps
gistic, but the mechanism is through inde- additional high-resolution behavioural obser-
pendent influence on the probability that one vation studies will lead to similar under-
examining behaviour will proceed to another standing of the particular cues to which
(Cowles, 1990). Harris and Miller (1983) also insects are ‘attentive’ during specific host-
investigated the influence of foliar colour on examining behaviours (Spencer et al., 1999).
host-acceptance behaviours, but found that, Investigators need to be careful when
in addition to influencing foliar landing, yel- conducting studies of stimulus interactions
low colour also influenced the post-alighting to avoid confounding host stimuli with addi-
behaviours of stem-runs and substrate prob- tional, semiochemical-based cues. For exam-
ing with the ovipositor. Whether an insect is ple, in the onion fly example, visual and
attentive to one or a few host characteristics chemical resources (presented alone) each
at any given time, when several steps in a received 2.8% of the total eggs deposited in
sequence of behaviours lead to the insect this laboratory choice test, but the combina-
accepting the resource, the end result is a tion visual + chemical resources received
function of the joint probability of the transi- 78% of the eggs (Miller and Harris, 1985).
tion from each behaviour to another, a multi- Part of this extreme degree of synergism may
plicative function. Using Bernays’s (2001) have been due to the additional responsive-
concept of ‘selective attention’, onion flies do ness of examining flies to previously laid
seem attentive first to host-associated odours, eggs and aggregation pheromones (Judd and
which stimulate upwind movement, fol- Borden, 1992), causing a positive-feedback
lowed temporally by responsiveness to visual dynamic. Thus, the presence of egg-associ-
cues (Judd and Borden, 1989, 1991). Thus, it ated pheromones may have interfered with
seems parsimonious that each examining isolating the response to host cues, and each
behaviour is likely to be associated with subsequent oviposition event was probably
assessment of a particular subset of sensory influenced by prior egg-laying events. Since
cues from the potential host. the presence of eggs acts as an additional
Another example of temporal synergism activant for gravid onion flies, the only way
is given by the study of stimulus interaction to tease out the effect of host stimuli would
within the chemical senses of Plutella be to present a fly with a new host model fol-
xylostella (Linnaeus) (Spencer et al., 1999). lowing each egg-laying event (Judd and
During short-term evaluation of moth behav- Borden, 1992). This example also demon-
iours, neither alkanes nor sinigrin alone stim- strates the importance of non-host cues (in
ulates much oviposition. Individual moths on this case, the presence of conspecifics) in the
substrates with stimulatory alkanes (and no calculus of host-quality assessment.
sinigrin) spent a longer time on potential host
substrates: affected behaviours in the pres-
ence of alkanes included arrestment compo- Manipulation of Host Acceptance
nents, including longer residence time, Behaviour: the Push–Pull Approach
reduced movement rates and increased turn-
ing on the substrate. Sinigrin alone did not Insect behaviours may follow generalizable
evoke arrestment or additional host-examin- patterns that can allow us to better under-
ing. There was increased oviposition when stand how either to ‘jam’ their signals by
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Host Finding and Acceptance in Insects 189

making otherwise acceptable hosts deterrent mountain pine beetle’s three-component

or to key in on specific cues that lead to semiochemical blend resulted in attraction of
increased resource acceptance. The focus of beetles to the vicinity of the pheromone
these efforts should be to maximize the dif- source and achieved the objective: to concen-
ferential between those resources attracting trate beetle attack in a small area suitable for
insects and those that are deterrent. As I clar- removal of the population through logging.
ify below, neither approach alone can be However, the beetles attacked not only the
expected to be entirely satisfactory, but the tree upon which the pheromone was
combined use might be successful if deter- released but also adjacent trees, presumably
rents were applied to valued crops and because these trees were downwind within
attractants applied to diversionary (or trap) the pheromone plume. This result was
crops. This strategy has variously been called expected, because beetles responding to
the ‘push–pull’ or ‘stimulo-deterrent’ aggregation pheromones orient visually to
approach, and was independently conceptu- trees while flying within the plume, with
alized in the USA by Miller (1986) and in greater response towards larger-diameter
Australia by Rice (1986). The efforts of these trees.
groups were focused on manipulating the Arrestment prior to arriving at the source
behaviour of the onion fly (Miller and of supernormal odour stimuli (stimuli more
Cowles, 1990; Cowles and Miller, 1992) and active than those found in nature) poses a
of Heliothis spp. (Pyke et al., 1987). potential for damage anywhere downwind
A good example for the failure of unilat- from the odour source where a responding
erally presented attractants exists with insect may become arrested at a host.
efforts to mass-trap Japanese beetles to pro- Supernormal visual stimuli, on the other
tect adjacent host plants. Japanese beetles hand, should not have this characteristic,
appear to follow the commonly observed because insects can directly locate the source
host-seeking modus operandi of strongly fly- of the visual signal (Miller and Strickler,
ing insects with the following features: (i) 1984). However, even if insects take flight in
host-finding in a patchy environment proba- response to supernormal visual stimuli, they
bly uses upwind anemotaxis, triggered by may become arrested by odour cues prior to
detection of host odours by a physiologically reaching that visual target, such as was seen
receptive beetle; (ii) upwind flight probably with thrips (Teulon et al., 1999). These obser-
increases the responsiveness of the beetle to vations suggest that an especially valuable
visual cues; and (iii) the beetle lands on visu- strategy would be to apply deterrents to hosts
ally detected potential hosts within the close to attractive traps or crops. Such a place-
odour plume (Bernays, 2001). Placed in this ment could elicit pest movement until the
context, we can expect potent chemical pest encounters the trap or attractive crop.
attractants to lead not only to excellent trap Unilateral deployment of deterrents,
catches, but also to increased damage by the repellents or crops resistant via antixenosis
pest in host vegetation downwind from the can also be expected to fail. The most impor-
odour source. This was observed for tant prediction from the rolling-fulcrum
Japanese beetle adult feeding close to floral- model is that insects will become accepting
lure-baited traps, in which defoliation of of deterrent, repellent or resistant hosts
hosts increased in relation to intensity of when deprived of highly acceptable hosts.
attractant used (the number of traps), prox- Acceptance by insects confined to deterrent
imity of the traps to the hosts and the loca- plants has been observed by many workers,
tion of the hosts downwind from the and fits a theoretical framework for individ-
attractant odour source (Gordon and Potter, ual females to maximize their lifetime fitness
1985). The same principle in host-finding (Roitberg and Prokopy, 1983; Fitt, 1986;
behaviours is seen with the use of aggrega- Mangel, 1989; Mangel and Roitberg, 1989;
tion pheromones on trees to concentrate the Aluja and Boller, 1992).
attack of bark beetles (Borden et al., 1983; Behavioural models also predict that, if
Gray and Borden, 1989). The release of the readily accepted hosts are made available,
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190 R.S. Cowles

insects will release their consummatory Deterrents and activants can be consid-
behaviour on these hosts, the insect may ered opposite sides of the same coin – inves-
never enter a deprived physiological state tigation of host-acceptance behaviours often
and deterrent hosts will continue to be discloses features of hosts that are subopti-
rejected. This phenomenon can be measured mal or even deterrent. For example, fraction-
in the field and the laboratory as the differ- ation of host-plant chemicals can yield both
ence between no-choice and choice environ- activants and deterrents (Lundgren, 1975;
ments in the acceptance of deterrent hosts. Doss, 1983; Renwick and Radke, 1987;
As early as 1871, Colorado potato beetle was Scarpati et al., 1993; Huang et al., 1994; Grant
found to accept several resistant varieties of and Langevin, 1995; Honda, 1995). These
potato grown as monocultures (a no-choice examples suggest that manipulation of host
environment), whereas in small-plot trials biochemistry could lead to changes in the
(with several varieties in proximity) these balance of attractants, phagostimulants and
varieties were rejected (Casagrande, 1987). ovipositional deterrents in plants. Plant
Therefore, superior ovipositional or feeding breeding is an obvious option for manipula-
resources may have to be provided as part of tion of host-plant chemistry. However, even
the crop system if repellents or deterrents are a subtle shift in host chemistry can yield
to be useful. unexpected changes in acceptance by insects.
The practical aspects of deploying the For example, cucumber plants inoculated
push–pull strategy will involve: (i) finding with plant growth-promoting rhizosphere
and using stimuli that cause host rejection; bacteria emit fewer cucurbitacins, elicit
(ii) finding and using stimuli that attract the reduced feeding by cucumber beetle vectors
pest, especially if they can be presented as and thereby decrease the transmission of
supernormal stimuli; and (iii) understanding Erwinia tracheiphila (Zehnder et al., 2001). In
the effect of these factors on pest movement another example, varying the nitrogen fertil-
so that the two alternatives can be spatially ization of crops can also influence the accep-
presented in an optimal manner. tance of strawberry foliage by adult black
vine weevils, which probably also influences
their fecundity and the spatial pattern of
Potential Tools for Implementing the oviposition (Cram, 1965; Hesjedal, 1984; R.S.
‘Push–Pull’ Strategy Cowles, unpublished data).
Other chemical cues may be indirectly
What tools have potential for manipulating derived from the host plant through its inter-
insect behaviour in an agricultural setting? action with insect herbivores. Olive fruit
The answer is that there are almost limitless flies, Bactrocera oleae (Gmelin), cause sap to
possibilities waiting for creative investiga- exude from olive fruits into which they have
tors to exploit. The interaction of multiple laid eggs. This sap contains several com-
sensory modalities in host recognition by pounds, both hydrophilic and lipophilic,
insects may allow the manipulation of a very which act as a marking pheromone that
wide menu of plant or environmental char- reduces the likelihood of subsequent ovipo-
acteristics to affect host finding and recogni- sition into that fruit (Girolami et al., 1981).
tion. In a crop system designed to avoid pest Bacteria colonizing plant tissues can also
deprivation, the full potential for manipulat- modify insect response. Chemical factors
ing pest behaviour has to take into account maximally stimulating onion-fly oviposition
attracting and arresting pests at traps, trap are elicited not by healthy onion plants, but
crops, refuge crops or diversionary crops, by onion tissue colonized by soft-rot bacte-
while at the same time deterring or repelling ria, particularly Erwinia carotovora (Dindonis
the same pests from valued crops. An entire and Miller, 1980, 1981; Hausmann and
suite of cues could be used to maximize the Miller, 1989). If bacterial growth could be
differential movement of pests away from prevented in this tissue, then emission of
the valued crop and into diversionary crops, these potent volatile cues could be reduced.
an approach not yet fully tested. While some of the chemical stimuli have
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Host Finding and Acceptance in Insects 191

been characterized, the full complement of Schoonhoven et al., 1990; Poirier and Borden,
chemical stimuli that release onion-fly exam- 1991; Dempster, 1992; Gabel and Thiery,
ining and oviposition is not yet completely 1992; Thiery et al., 1992). Ovipositional deter-
understood (Hausmann and Miller, 1989). rents associated with eggs have also been
Perhaps the most behaviourally potent found with weevils (Stansly and Cate, 1984;
chemical cues can be expected from the Messina et al., 1987; Kozloẃski, 1989;
pheromones and allomones of conspecifics Credland and Wright, 1990; Ferguson and
and competitors, respectively. As recently Williams, 1991; Mbata and Ramaswamy,
reviewed by Borden (1997), engraver beetles 1995). Tephritid eggs deposited internally in
are a group rich in pheromonal communica- fruit perhaps may not be detectable by con-
tion systems that can be manipulated. specifics; however, adult females of this
Complexes of species have co-evolved and group commonly lay down marking
compete with each other for the limited pheromones on the fruit surface, which usu-
resource of susceptible phloem tissue in ally deters subsequent oviposition (Prokopy,
trees. Colonizing beetles produce volatile 1981; Hurter et al., 1989; Straw, 1989; Aluja
aggregation pheromones, which at some and Boller, 1992; Papaj et al., 1992).
concentrations, along with host kairomones, Oviposition-deterring pheromone has also
attract additional conspecifics to the same been detected with cecidomyiids (Quiring et
tree. Mass attack of the tree, up to a certain al., 1998), and agromyzids (Quiring and
point, is adaptive because it allows the bee- McNeil, 1984). Hessian flies may not use
tles to overwhelm the tree’s defensive mech- oviposition-deterring pheromones, but do
anisms (sap or resin flow). At higher appear to assess previous colonization of
concentrations, the same aggregation hosts and avoid infested plants when laying
pheromone (with certain species) may act as eggs (Kanno and Harris, 2002).
an anti-aggregation pheromone, and there The presence of other cues associated
are several examples where the aggregation with the presence of conspecifics, such as
pheromone of one species can act as a deter- frass (Renwick and Radke, 1980; Dittrick et
rent for another species. These pheromones al., 1983; Anderson and Lofqvist, 1996), pul-
have been successfully deployed in verized larvae (Gross, 1984) and oral secre-
push–pull strategies to cause outbreaks to tions (Poirier and Borden, 2000), can act as
implode rather than continuing to expand. deterrents for oviposition or feeding.
Two examples suggest that synthetically Presence of other herbivores on the host can
derived attractants may perform as well as also deter oviposition or feeding (Jones et al.,
or better than compounds found naturally 1988; Finch and Jones, 1989; Schoonhoven et
occurring in hosts. Males of several tephritid al., 1990). Each of these examples suggests
species are attracted to the components of that application of synthetic pheromone
trimedlure, compounds for which the nat- could be used to prevent feeding or oviposi-
ural significance remains unknown (Foster tion on plants we wish to protect.
and Harris, 1997). Structure–activity relation- Wilson and Bossert (1963) provide a
ship work with cinnamyl compounds dis- framework for understanding the behav-
covered potent attractants for Diabrotica spp. ioural consequences and longevity of
that probably do not occur naturally in pheromone cues related to their physical
cucurbit flowers (Metcalf and Lampman, chemical properties. We should expect that,
1989). Thus, synthetic compounds may fit unlike social-insect alarm pheromones,
insects’ receptors and could take the place of which are small molecules that dissipate
natural compounds for use in behavioural rapidly (Wilson and Bossert, 1963), oviposi-
manipulation. tion-deterring pheromones will have rela-
Lepidopteran eggs are usually deposited tively long persistence and low volatility. In
on the leaf surface, often accompanied by one instance, the oviposition-deterring
pheromones deterring oviposition by con- pheromone of Pieris brassicae (Linnaeus) was
specifics (Behan and Schoonhoven, 1978; found to persist for 14 days on cabbage
Klijnstra, 1986; Schoonhoven, 1990; leaves under laboratory conditions
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192 R.S. Cowles

(Schoonhoven et al., 1981). In another exam- avoidance responses, to find non-toxic alter-
ple, the ovipositional deterrent associated natives to mimic the pesticides’ deterrent
with Callosobruchus subinnotatus eggs dissi- properties.
pated over 4 weeks following the removal of Many workers have investigated plant-
those eggs (Mbata and Ramaswamy, 1995). protective chemistry, such as essential oils, to
Long-residual properties of synthetic ovipo- deter or repel insects (e.g. Cowles et al.,
sitional deterrents could make their applica- 1990). This idea is appealing, for, if we can
tion useful in agricultural systems (Averill make a plant appear to the insect sufficiently
and Prokopy, 1987; Klijnstra and like a non-host, oviposition or feeding
Schoonhoven, 1987). should be averted. One of the challenges in
Experience from field tests of specific working with repellents is that, because they
semiochemical-based ovipositional deter- are volatile, controlled-release formulations
rents has varied from suggesting potential might be necessary to allow more than a few
for economically relevant suppression of days of effect. Larger compounds with low
oviposition with the host-marking volatility should have better residual proper-
pheromone of cherry fruit fly (Boller et al., ties. Therefore, deterrents may have more
1987) to being rather disappointing with P. practical value. Two compounds are particu-
brassicae (Klijnstra and Schoonhoven, 1987). larly interesting and may play useful roles:
P. brassicae responded to its own oviposition- azadirachtin has behavioural as well as
deterring pheromone by decreasing contact insect growth-regulator properties, and so
with treated plants and flying to the edge of can be used as a feeding deterrent
the field cage, where they then proceeded to (Simmonds and Blaney, 1996). Capsaicin has
lay their eggs. Unfortunately, this did not nearly unique pungent flavour qualities –
observably reduce the number of eggs laid. organisms ranging from barnacles to bears
Together, these experiments highlight one are deterred by this compound. Insects are
important feature of deterrents: movement also sensitive to capsaicin (Cowles et al.,
can be expected to exhibit fewer turns and 1989). However, application of such a pow-
longer bouts of straight travel following erful irritant can be very unpleasant unless
encounter with deterrents; this can be the operator is wearing full protective
expected to increase the insect’s displace- clothing.
ment from the deterrent source (Roitberg et Prokopy and Owens (1983) reviewed dis-
al., 1984). Furthermore, the effectiveness of ruption of visual stimuli used in host find-
the deterrent can be expected to decrease ing. Foliage colour may be a useful trait for
over time if exposure is continuous and the plant breeders to protect some crops. For
insect becomes deprived (Roitberg and example, red varieties of cabbage were less
Prokopy, 1983; Aluja and Boller, 1992). accepted by ovipositing Delia radicum
As reviewed by Gould (1984) and (Linnaeus) than they were of green varieties
Lockwood et al. (1984), one consequence of (Prokopy et al., 1983), just as red-leaf cotton
insecticide application is the evolution not varieties were less preferable to boll-weevil
only of physiological resistance but also of compared with those with green leaves
behaviours that allow the insect to avoid (Maxwell, 1977). Reflective mulches have
toxic residues. Therefore, insecticides been investigated extensively, and have been
applied to crops may already in some cases successful in reducing transmission of
be acting as repellents or deterrents. The viruses by aphids and thrips (Prokopy and
unfortunate side to using insecticides for Owens, 1983). The recent registration of
deterrent or repellent properties is that these kaolin-based plant protectants should give a
products would still have the same negative tool for changing not only the colour charac-
environmental consequences as if they had teristics but also the surface texture of plants,
been applied to directly kill pests. Perhaps and perhaps even the ability of an insect to
structure–activity relationship studies could sense the plant’s surface chemistry. Kaolin is
be undertaken, using bioassays and pest highly reflective of ultraviolet light; as such
populations that have evolved behavioural it can be used to deter aphid landing in the
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Host Finding and Acceptance in Insects 193

same way that reflective mulches have been How might combinations of visual and
used in the past (Bar-Joseph and Frenkel, chemical deterrents perform? Gravid onion
1983; McBride, 2000). Other aspects of ‘jam- flies were tested in the laboratory with vari-
ming’ the visual system could include cam- ous negative (or simply less positive) ovipo-
ouflaging plants with interplanted sitional stimuli, with the general resulting
vegetation to obscure hosts, or even the use observation that stimuli tended to have a
of lights to attract night-flying moths multiplicative effect on egg-laying behaviour
(Prokopy and Owen, 1983). (Cowles, 1990). For example, there were
Physical characteristics of the leaf, particu- twice as many eggs deposited around the
larly the presence of trichomes, can dramati- green as around the red foliar models and
cally affect insect feeding or oviposition. For ten times as many eggs laid around models
example, black vine-weevil adult feeding without cinnamaldehyde (a deterrent) as the
preference for strawberry foliage of the com- one with cinnamaldehyde. The green model
mercial variety ‘Totem’ vs. the species without deterrent elicited 33 times as much
Fragaria chiloensis, was experimentally oviposition as the red model combined with
demonstrated to be mediated by leaf hairs cinnamaldehyde, not significantly different
(Doss et al., 1987). In a similar way, obscure from the 20-fold difference predicted by a
root-weevil adult feeding preference for dif- behavioural model using independent
ferent species of rhododendron is largely reductions in behavioural transitions. A mul-
mediated by trichome characteristics (Doss, tiplicative model for interaction between
1983). Pubescence of leaves can also influence deterrents of different sensory modalities
ovipositional preference, as demonstrated leads to an interesting result: it may be diffi-
with Chilo partellus (Swinhoe) on maize cult to completely deter consummatory
(Kumar, 1992). Leaf texture also influences behaviours on host plants. If, for example,
pre-ovipositional behaviour in diamondback we could decrease oviposition with a visual
moths and Hessian flies, but these character- deterrent by 60%, and with a chemical deter-
istics may be difficult to manipulate (Harris rent by 25%, the combination might be
and Rose, 1990; Spencer et al., 1999). Perhaps expected to reduce oviposition not by 85%,
application of temporarily sticky or filamen- but by 70% (1 − [1 − 0.6] × [1 − 0.25]).
tous barriers on the surfaces of plants will Certain materials could dramatically
offer a direct method for interfering with change the tactile, flavour or visual appear-
host-examining barriers by insects on the leaf ance of plants for many species of insects,
surface, and thereby prevent egg laying or such as ethylene vinyl acetate fibres, cap-
feeding. Ongoing work with ethylene vinyl saicin and kaolin, respectively. These tools
acetate fibres, in appearance like candy floss, may have commercial advantages for dis-
has shown promise as a deterrent for onion rupting host finding and acceptance by
and cabbage maggots (Friedlander, 2002). insects in agriculture over specific deterrents
The fact that several chemicals can act (e.g. oviposition-deterring pheromones),
together synergistically to increase host because, like conventional pesticides, they
acceptance should give us hope that the could provide ‘broad-spectrum’ aspects for
opposite may also be true: that chemical managing pest insects.
deterrents in concert may synergistically
decrease oviposition or feeding. Studies of
onion-fly deterrents (Cowles, 1990) were Demonstrated Application of
inconclusive and could not reject the hypoth- Behavioural Manipulation in Trap Crops
esis that different compounds were acting in
an additive fashion. Chemical deterrents Manipulation of host-finding and acceptance
may affect herbivore specialist and generalist behaviours has been practised with trap
species differently (Bernays et al., 2000; cropping for many years. Trap crops,
Bernays, 2001); so controlled studies investi- reviewed by Hokkanen (1991), provide a
gating this hypothesis should ideally include resource that is more attractive to mobile
close relatives representing both. pests so that they are partitioned away from
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194 R.S. Cowles

a valued crop, thereby providing some striped cucumber beetles. A diversionary

degree of protection to the valued crop. The crop area of 15 and 50% of the area grown in
trap crop may be the same variety as the the valued crop was equivalent for reducing
main crop, but planted earlier so that the pest populations in the valued crop, and pre-
older, larger plants can produce more attrac- vented the cucumbers from having to be
tants, be more visible and thus be more sprayed. Potatoes have been used to divert
apparent to the mobile pest. Alternatively, Colorado potato beetles from feeding and
the crop may be of a different species or vari- reproducing on tomatoes (Hunt and
ety from that of the main crop, and be Whitfield, 1996). In this instance, one row of
selected for its use because it is highly attrac- potatoes for every eight of tomatoes pro-
tive and receives more eggs or feeding in vided protection, as long as the potato plants
choice tests with the main crop. Usually, were able to grow and provide sufficient
reproduction of the pest in the trap crop is resources to accommodate the beetles.
prevented, either through insecticide use or Plantings of wheat have been effective as a
crop destruction. Occasionally the trap crop diversionary crop for concentrating wire-
is justified as a means for aggregating the worms, Agriotes obscurus (Linnaeus), in strips
pest in a crop for which control options are displaced laterally from where strawberries
available, whereas these options cannot be were being planted (Vernon et al., 2000). The
used on the valued crop (Hunt and interplanted wheat reduced the mortality of
Whitfield, 1996; Pair, 1997). A variant of the strawberry plants from 43 to 5.3%. In the
trap crop concept is the attract–annihilate or strip cropping system developed to prevent
attracticide approach, which uses behav- lygus damage to cotton, lucerne was kept
ioural manipulation to bring insects to traps, growing in a lush manner. Preventing senes-
baits or insecticide deposits, with or without cence of the lucerne required mowing two
the presence of hosts. Behavioural manipula- alternate strips on a 14-day schedule, which
tion for the attracticide approach has coincidentally also caused significant mortal-
recently been reviewed (Foster and Harris, ity to lygus-bug immature stages. The lygus
1997). population remained within the lucerne crop
Trap crops have been used to concentrate to the degree that cotton bolls were protected
the pest population on fewer plants, allow- from feeding. An additional benefit was the
ing a smaller area to be treated with insecti- reproduction of several species of generalist
cides to reduce the pest population (e.g. Pair, predators within the lucerne crop, which
1997). In rare examples, growers do not need then aided management of other insect pests
to apply insecticides, either in the trap crop in cotton (Godfrey and Leigh, 1994).
or in the valued crop. A recent example used In some respects, insect pests diverted
every fifth row planted to Nicotiana away from the valued crop system could be
kawakamii to divert oviposition by Heliothis thought of in the same way as agronomists
virescens (Fabricius) from Nicotiana tabacum. think of weeds. A weed can be defined as a
The N. kawakamii appeared to not only divert plant growing where it is not wanted,
oviposition from the interplanted tobacco, whereas the same plant growing outside a
but may also have diverted oviposition from crop might be considered a wild flower. In a
nearby monoculture tobacco plots, making parallel reasoning, populations of insects
comparison of the trap-crop effect difficult. normally considered to be ‘pests’ that
The cultural practice of topping plants could develop in a place or on hosts that are not
make insecticide applications unnecessary intended for harvest may not be considered
for control of H. virescens in a valued crop of an economic threat, and so are not truly
tobacco or a diversionary crop of N. pests. These insect populations developing
kawakamii, perhaps permitting biological outside the valued crop may serve important
control agents to become better established ecological functions, especially as a nursery
(Jackson and Sisson, 1998). Radin and for the propagation of natural enemies and
Drummond (1994) used squash as a diver- as a population reservoir that is not exposed
sionary crop to protect cucumbers from to insecticides. Under most circumstances,
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Host Finding and Acceptance in Insects 195

some intervention to prevent unconstrained iological resistance can be quite complex.

reproduction of a pest in a refuge crop is nec- Gould (1984) discusses a two-gene, two-
essary, otherwise a burgeoning population allele model with selection on behavioural
could have devastating consequences due to traits associated with deterrency vs. physio-
their movement from the diversionary crop logical resistance (such as to insecticides or a
to other crops more sensitive to pest feeding crop with antibiosis-based insect resistance).
(Kennedy et al., 1987). However, if a pest Factors that need to be taken into considera-
population is highly concentrated in a diver- tion include: the quality of the treated and
sionary crop, many density-dependent pop- untreated habitats for pest survival (calcu-
ulation-regulation mechanisms, including lated as though the antibiosis-related mortal-
intraspecific competition, more efficient pre- ity factor were not present), mortality due to
dation, parasitization and disease epizootics, pesticide exposure, the manner in which
may be able to suppress the population with- insect behaviour partitions the population
out additional intervention. Physical into the two habitats and possible pleiotropic
destruction of part of the diversionary crop effects of carrying physiological-resistance or
to manipulate pest survival may have behavioural-avoidance alleles (i.e. fitness
greater pest-management value than treating costs for these alleles).
it with insecticides, as the former strategy I included each of the components
will minimize the selection for insecticide described by Gould’s (1984) model, with
resistance and the environmental impact on some modifications, into my own simulation
natural enemies, which may disperse to the model. For example, I incorporated a user-
diversionary crop remnant. defined dosage-dependent mortality func-
tion for each genotype, so that manipulation
of pesticide concentration on the resulting
Implications for Insecticide-resistance selection could be compared (Taylor and
Management Georghiou, 1979). Gould showed the results
as adaptive landscapes, in which the mean
Manipulation of insect behaviour in the fitness for every gene-frequency combination
push–pull strategy is immediately relevant is calculated. Theoretically, selection forces
to issues of insecticide resistance. populations up the nearest ‘slope’ to increase
Partitioning the insect population into two their mean fitness. Unfortunately, the fitness
habitats permits survival of a non-selected for each gene-frequency combination is not
population, which may, through interbreed- mathematically unique, because each gene-
ing with the selected population, maintain frequency combination can actually be repre-
the resistance allele(s), principally in a het- sented by a large number of combinations of
erozygous condition (Comins, 1977). As a genotype frequencies, each with its own
practical issue, these factors have been the mean fitness value (Lewin, 1988). To display
basis for the attempt to prevent the develop- the results in my model, each combination of
ment of resistance to insecticidal transgenic physiological-resistance allele frequency and
crops (valued crops) through mandated behavioural-avoidance allele frequency is
planting of non-transgenic crops as refuges characterized by its evolutionary outcome.
(Gould, 1998). Including behavioural manip- Thus, each figure is divided into four regions
ulation as part of the valued crop/refuge (at most), showing those combinations of ini-
crop design could optimize the use of refugia tial gene frequencies for which subsequent
by minimizing the amount of space planted generations are ‘attracted’ by selection to a
to the refuge crop, while at the same time ‘corner’ where the alleles become fixed. To
reducing the proportion of the population make these figures unambiguous, a modified
that ends up being selected within the val- program tracked the gene frequencies for
ued crop. sample populations, starting at specific gene
Genetic models needed for predicting the frequency combinations. Selection in these
evolutionary outcome when there are inter- sample populations is shown with arrows
actions between behavioural traits and phys- that track the population through successive
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196 R.S. Cowles

generations. This deterministic model oper- ness costs were not used in the following
ates according to the following principles: simulation results.
Results from this model are shown in the
1. The behavioural trait and physiological
following figures, with the accompanying
resistance alleles are not genetically linked.
parameter values for running the models
2. There is random mating for the entire
given in Table 9.1. Variations tested with this
population.
simulation model included the following
3. The first generation in the model assigns
pest-management strategies: a conventional
Hardy–Weinberg equilibrium frequencies for
insecticide-only crop with minimal pest
the nine genotypes.
development in a non-treated refuge with
4. Each genotype’s frequency is governed by
both very low (Fig. 9.2A) and high (Fig. 9.2B)
a random combination of the haploid
dose uses of insecticides, an attracticide or
gametes according to their proportion fol-
lethal trap-crop approach (Fig. 9.3), a refuge-
lowing selection.
crop system (Fig. 9.4) and push–pull systems
5. The insects partition themselves between
investigating variations in diversionary-crop
habitats based on the strength of habitat dis-
findability (Fig. 9.5) and suitability for insect
crimination as determined by the avoidance
development (Fig. 9.6).
trait.
In the insecticide-only simulation (Fig.
6. The survival to the next generation is
9.2), the crop is assumed to be somewhat
determined by the action on immature stages
more suitable for insect development than
of the antibiosis factor (pesticide concentra-
the difficult-to-find alternative hosts, which
tion), the quality of the habitat and the action
are envisioned perhaps to consist of weeds
of any pleiotropic fitness cost associated with
outside the field. A consequence of the alter-
carrying the physiological-resistance or
native crop being difficult to find, even for
behavioural-avoidance allele.
potential ‘avoiding’ genotypes, is that selec-
The user of this model defines the following tion rapidly favours the evolution of physio-
parameters: (i) the slope and median lethal logical resistance. The extreme selection for
dose (LD50) for the three physiological- physiological resistance in the low-dose situ-
resistance genotypes; (ii) the treated and ation (Fig. 9.2A) results from the dispropor-
untreated habitat suitability; (iii) the proba- tionate removal of homozygous susceptible
bility that the AA and aa genotypes are individuals from the population. In many
found in the treated habitat; and (iv) the fit- respects the high-dose strategy results in a
ness cost for carrying R or a alleles. The fit- variation of the refuge-crop principle: as

Table 9.1. Parameters used for running the population-genetics simulation model presented in Figs
9.2–9.6. The use of the parameters is as described by Gould (1984). No pleiotropic fitness costs were
used.

Mortality from insecticide Proportion in

Habitat quality in treated habitat treated habitat
Fig. no. Untreated Treated rr Rr RR aa Aa AA

9.2A 0.4 0.5 0.91 0.49 0.09 1.00 0.95 0.90

9.2B 0.4 0.5 1.00 0.99 0.79 1.00 0.95 0.90
9.3 0.5 0.5 1.00 0.99 0.79 0.90 0.50 0.10
9.4 0.4 0.5 1.00 0.99 0.79 0.90 0.85 0.80
9.5A 0.5 0.4 1.00 0.99 0.79 0.90 0.70 0.50
9.5B 0.5 0.4 1.00 0.99 0.79 0.95 0.50 0.05
9.6A 0.3 0.5 1.00 0.99 0.79 0.90 0.60 0.30
9.6B 0.7 0.5 1.00 0.99 0.79 0.90 0.60 0.30
9.6C 0.2 0.1 1.00 0.99 0.79 0.90 0.50 0.10
09IntpestManCh9.QXD 14/4/04 2:25 pm Page 197

Host Finding and Acceptance in Insects 197

1.0

Gene frequency A (behavioural avoidance)

1.0
Gene frequency A (behavioural avoidance)

B
0.9 A 0.9

0.8 0.8

0.7 0.7

0.6 0.6

0.5 0.5

0.4 0.4

0.3 0.3

0.2 0.2

0.1 0.1

0.0 0.0
0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0
Gene frequency R (physiological resistance) Gene frequency R (physiological resistance)

Fig. 9.2. Population-genetics simulation for an insecticide-based strategy for controlling the population in
the valued crop and with no refuge designed in the crop system. (A) Low-dose strategy, (B) high-dose
strategy. See Table 9.1 for parameter values used in the simulation.

long as there is some alternative untreated for resistance to an antibiosis factor is ini-
habitat available, selection to a non-physio- tially too high (Fig 9.2B), the population
logically resistant, behaviourally avoiding evolves to an avoiding and physiologically
population is possible. If the gene frequency resistant genotype. In these conventional

1.0
Gene frequency A (behavioural avoidance)

1.0
Gene frequency A (behavioural avoidance)

0.9 0.9
0.8 0.8
0.7 0.7
0.6 0.6
0.5 0.5
0.4 0.4
0.3 0.3
0.2 0.2
0.1 0.1
0.0 0.0
0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0
Gene frequency R (physiological resistance) Gene frequency R (physiological resistance)

Fig. 9.3. Population-genetics simulation results for Fig. 9.4. Population-genetics simulation results for
an attracticide strategy, which could entail either a the high-dose refuge-crop strategy for controlling
kairomone plus insecticide bait system, a the population in the valued crop and with no
pheromone plus insecticide or an insecticide- behavioural modifiers used to direct the pest
treated trap crop. The population would initially population to the refuge designed in the crop
respond to the attractant (an aa population) and system. See Table 9.1 for parameter values used in
evolves to either not respond to or to avoid the the simulation.
attractant. See Table 9.1 for parameter values used
in the simulation.
09IntpestManCh9.QXD 14/4/04 2:25 pm Page 198

198 R.S. Cowles

1.0 1.0
Gene frequency A (behavioural avoidance)

Gene frequency A (behavioural avoidance)

A B A B C
0.9 0.9
0.8 0.8
0.7 0.7
0.6 0.6
0.5 0.5
0.4 0.4
0.3 0.3
0.2 0.2
0.1 0.1
0.0 0.0
0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0
Gene frequency R (physiological resistance) Gene frequency R (physiological resistance)

Fig. 9.5. Population-genetics simulation results for Fig. 9.6. Population-genetics simulation results for
the push–pull strategy. The high-dose approach the push–pull strategy. The high-dose approach
controls the population in the valued crop, a refuge controls the population in the valued crop, a refuge
(diversionary crop) is designed into the crop system (diversionary crop) is designed into the crop system
and behavioural modifiers direct the pest and behavioural modifiers direct the pest
population to the refuge. (A) Lower findability for population to the refuge. (A) Low suitability for
diversionary crop, (B) higher findability for diversionary crop, (B) higher suitability for
diversionary crop. See Table 9.1 for parameter diversionary crop, (C) highly findable diversionary
values used in the simulation. crop, with low suitability for both the valued crop
and the diversionary crop. See Table 9.1 for
parameter values used in the simulation.

insecticide systems, the avoidance factor is 1997) or pheromone fibre-insecticide combi-

considered to be any behavioural trait that nations (e.g. Butler and Las, 1983). The
can permit the insect to detect differences assumption in running this model is that ini-
between the insecticidal and untreated habi- tial conditions for the insect population are a
tats. As an unmanipulated component to the high degree of response to the attractant
management system, the insect’s population (starting predominantly as the aa genotype),
could easily start out either as principally and that evolution of avoidance behaviours
avoiding (high frequency of A allele) or non- would imply loss of the attraction. While
avoiding (high frequency of a allele). As genetic variation might be presumed to be
Gould (1984) points out, deterrents could be minimal for altered response to sex
added to insecticide formulations to be cer- pheromones or host kairomones, this model
tain that the insect population can detect does raise the concern that the evolutionary
insecticides, and so will automatically start outcome when using the attracticide system
out in the upper left corner, which can be is unfavourable, and that resistance to such a
selected to an AArr population, rather than strategy is likely if genetic variation for
the unfavourable AARR or even less response to the attractant exists. The com-
favourable aaRR genotypes. plex blends of pheromone components in
Attracticidal approaches are represented some natural communication systems sug-
in Fig. 9.3. Representative crop systems gest that insects may already have adapted
would include trap crops, in which the pest to a crowded chemical communication chan-
is killed with insecticides in the trap crop, nel. Species using complex blends may thus
and also kairomonal insecticide (e.g. Pair, be more of a concern than those using single
09IntpestManCh9.QXD 14/4/04 2:25 pm Page 199

Host Finding and Acceptance in Insects 199

compounds. Insect attraction to kairomones and gene frequencies need to be exceedingly

is also complex, so there ought to be many high to allow selection of the population to
ways in which insect populations can adapt fix the physiologically resistant R allele. One
to kairomone-based attracticides. of the surprises in performing these simula-
In the high-dose refuge crop system (Fig. tions was that fairly major differences in
9.4), populations may be selected to any of diversionary-crop findability (Fig. 9.5) and
the four ‘corners’ depending on the initial suitability (Fig. 9.6) had little effect on the
gene frequencies. This model was run with resulting selection outcomes. Although the
the assumption that the refuge crop is not transition line shows the expected shift to the
easily distinguished by the insect from the right with improved findability and with
insecticidal crop, and that, if the insecticidal high suitability of the diversionary crop, the
trait were not present, insect survival in the overall outcome is virtually the same. Nearly
valued crop would be slightly better than in any initial gene frequency will eventually
the refuge crop (perhaps due to a greater lead to fixation of the A or avoidance trait,
presence of natural enemies in the non- which is favourable for pest management
insecticidal habitat). By including an alterna- because it maintains the pest population in
tive habitat in which the pest population can the diversionary crop.
develop, the gene frequency would have to I have also included an example of the
be quite high to lead to selection for the kinds of parameters that I feel would be
physiological-resistance trait. most favourable to try to design into a crop
The push–pull approach (Figs 9.5 and 9.6) system (Fig. 9.6C). In this simulation, there is
is different from the refuge crop system prin- poor survival of the pest in the valued crop,
cipally in the insects’ ability to detect differ- slightly greater survival in the diversionary
ences and discriminate between habitats. The crop and high discrimination between the
pest population would initially have a high two habitats. With these conditions, we
frequency for the A or avoidance allele would have low overall survival, mainte-
because this would be the character(s) we nance of behavioural preference for the
would manipulate to effect discrimination diversionary crop and continued susceptibil-
between habitats (deterrents, repellents and ity of the population to the physiological
attractants). Parameters affecting the evolu- antibiosis factor.
tionary outcome of the push–pull approach With all simulation efforts, the user
are given, with simulations that assess com- should beware of assumptions underlying
binations of the diversionary crop findability the results. The assumptions of large popula-
(low vs. high) and suitability (low vs. high), tions mating randomly, used in these simula-
relative to the valued crop, which is always tions, may not reflect reality. However, I
presumed to be protected with insecticides or hope that the overall favourable evolution-
genetically based antibiosis traits. ary results suggested here will spur others to
In all of these simulations, the advantage investigate behavioural manipulation as a
to using a diversionary crop becomes appar- necessary component for developing sus-
ent: behavioural avoidance is maintained tainable agricultural systems.

References

Aluja, M. and Boller, E.F. (1992) Host marking pheromone of Rhagoletis cerasi: foraging behavior in
response to synthetic pheromonal isomers. Journal of Chemical Ecology 18, 1299–1311.
Anderson, P. and Lofqvist, J. (1996) Oviposition deterrents from potato, wheat germ, larval frass, and
artificial diet for Agrotis segetum (Lepidoptera: Noctuidae). Environmental Entomology 25, 653–658.
Averill, A.L. and Prokopy, R.J. (1987) Residual activity of oviposition-deterring pheromone in Rhagoletis
pomonella (Diptera: Tephritidae) and female response to infested fruit. Journal of Chemical Ecology 13,
167–177.
Barata, E.N. and Araujo, J. (2001) Olfactory orientation responses of the eucalyptus woodborer,
Phoracantha semipunctata, to host plant in a wind tunnel. Physiological Entomology 26, 26–37.
09IntpestManCh9.QXD 14/4/04 2:25 pm Page 200

200 R.S. Cowles

Bar-Joseph, M. and Frenkel, H. (1983) Spraying citrus plants with kaolin suspensions reduces coloniza-
tion by the spirea aphid (Aphis citricola van der Goot). Crop Protection 2, 371–374.
Behan, M. and Schoonhoven, L.M. (1978) Chemoreception of an oviposition deterrent associated with
eggs in Pieris brassicae. Entomologia Experimentalis et Applicata 24, 163–179.
Bernays, E.A. (1996) Selective attention and host plant specialization. Entomologia Experimentalis et
Applicata 80, 125–131.
Bernays, E.A. (2001) Neural limitations in phytophagous insects: implications for diet breadth and evolu-
tion of host affiliation. Annual Review of Entomology 46, 703–727.
Bernays, E.A., Oppenheim, S., Chapman, R.F., Kwon, H. and Gould, F. (2000) Taste sensitivity of insect
herbivores to deterrents is greater in specialists than in generalists: a behavioral test of the hypothe-
sis with two closely related caterpillars. Journal of Chemical Ecology 26, 547–563.
Boller, E.F., Schöni, R. and Bush, G.L. (1987) Oviposition deterring pheromone in Rhagoletis cerasi: biologi-
cal activity of a pure single compound verified in semi-field test. Entomologia Experimentalis et
Applicata 45, 17–22.
Borden, J.H. (1997) Disruption of semiochemical-mediated aggregation in bark beetles. In: Cardé, R.T.
and Minks, A.K. (eds) Insect Pheromone Research: New Directions. Chapman & Hall, New York,
pp. 421–438.
Borden, J.H., Chong, L.J. and Fuchs, M.C. (1983) Application of semiochemicals in post-logging manipu-
lation of the mountain pine beetle, Dendroctonus ponderosae (Coleoptera: Scolytidae). Journal of
Economic Entomology 76, 1428–1432.
Butler, G.D. and Las, A.S. (1983) Predaceous insects: effect of adding permethrin to the sticker used in
gossyplure applications. Journal of Economic Entomology 76, 1448–1451.
Byers, J.A. (1996) Temporal clumping of bark beetle arrival at pheromone traps: modelling anemotaxis in
chaotic plumes. Journal of Chemical Ecology 22, 2133–2155.
Casagrande, R.A. (1987) The Colorado potato beetle: 125 years of mismanagement. Bulletin of the
Entomological Society of America 33, 142–150.
Comins, H.N. (1977) The development of resistance in the presence of migration. Journal of Theoretical
Biology 64, 177–197.
Courtney, S.P. and Kibota, T.T. (1989) Mother doesn’t always know best: selection of hosts by ovipositing
insects. In: Bernays, E.A. (ed.) Insect–Plant Interactions, Vol. 2. CRC Press, Boca Raton, Florida,
pp. 161–188.
Cowles, R.S. (1990) Manipulating oviposition of the onion fly, Delia antiqua (Meigen): a stimulo-deterrent
diversionary approach. Doctoral Dissertation, Michigan State University, East Lansing, Michigan.
Cowles, R.S. and Miller, J.R. (1992) Diverting Delia antiqua (Diptera: Anthomyiidae) oviposition with cull
onions: field studies on planting depth and a greenhouse test of the stimulo-deterrent concept.
Environmental Entomology 21, 453–460.
Cowles, R.S., Keller, J.E. and Miller, J.R. (1989) Pungent spices, ground red pepper, and synthetic cap-
saicin as onion fly ovipositional deterrents. Journal of Chemical Ecology 15, 719–730.
Cowles, R.S., Miller, J.R., Hollingworth, R.M., Abdel-aal, M.T., Szurdoki, F., Baur, K. and Matolcsy, G.
(1990) Cinnamyl derivatives and monoterpenoids as nonspecific ovipositional deterrents of the
onion fly. Journal of Chemical Ecology 16, 2401–2428.
Cram, W.T. (1965) Fecundity of the root weevils, Brachyrhinus sulcatus and Sciopithes obscurus on straw-
berry at different conditions of host plant nutrition. Canadian Journal of Plant Science 45, 219–225.
Credland, P.F. and Wright, A.W. (1990) Oviposition deterrents of Callosobruchus maculatus (Coleoptera:
Bruchidae). Physiological Entomology 15, 285–298.
Dempster, J.P. (1992) Evidence of an oviposition-deterring pheromone in the orange-tip butterfly,
Anthocharis cardamines (L). Ecological Entomology 17, 83–85.
Dethier, V.G. (1982) Mechanism of host-plant recognition. Entomologia Experimentalis et Applicata 40,
49–56.
Dindonis, L.L. and Miller, J.R. (1980) Host finding responses of onion and seedcorn flies to healthy and
decomposing onions and several synthetic constituents of onion. Environmental Entomology 9,
467–472.
Dindonis, L.L. and Miller, J.R. (1981) Onion fly and little house fly host finding selectively mediated by
decomposing onion and microbial volatiles. Journal of Chemical Ecology 7, 419–426.
Dittrick, L.E., Jones, R.L. and Chiang, H.C. (1983) An oviposition deterrent for the European corn borer,
Ostrinia nubilalis (Lepidoptera: Pyralidae), extracted from larval frass. Journal of Insect Physiology 29,
119–121.
09IntpestManCh9.QXD 14/4/04 2:25 pm Page 201

Host Finding and Acceptance in Insects 201

Doss, R.P. (1983) Root weevil feeding on rhododendron: a review. Journal of Environmental Horticulture 1,
67–71.
Doss, R.P., Shanks, C.H. Jr, Chamberlain, J.D. and Garth, J.K.L. (1987) Role of leaf hairs in resistance of a
clone of beach strawberry, Fragaria chiloensis, to feeding by adult black vine weevil, Otiorhynchus sul-
catus (Coleoptera: Curculionidae). Environmental Entomology 16, 764–768.
Evans, K.A. and Allen-Williams, L.J. (1993) Distant olfactory responses of the cabbage seed weevil,
Ceutorhynchus assimilis. Physiological Entomology 18, 251–256.
Evans, K.A. and Allen-Williams, L.J. (1998) Response of cabbage seed weevil (Ceutorhynchus assimilis) to
baits of extracted and synthetic host-plant odor. Journal of Chemical Ecology 24, 2101–2114.
Ferguson, A.W. and Williams, I.H. (1991) Deposition and longevity of oviposition-deterring pheromone
in the cabbage seed weevil. Physiological Entomology 16, 27–33.
Finch, S. and Jones, T.H. (1989) An analysis of the deterrent effect of aphids on cabbage root fly (Delia
radicum) egg-laying. Ecological Entomology 14, 387–391.
Fitt, G.P. (1986) The influence of a shortage of hosts on the specificity of oviposition behaviour in species
of Dacus (Diptera: Tephritidae). Physiological Entomology 11, 133–143.
Foster, S.P. and Harris, M.O. (1997) Behavioral manipulation methods for insect pest-management.
Annual Review of Entomology 42, 123–146.
Friedlander, B.P. (2002) Cornell entomologist uses ‘cotton candy’ to protect crops as maggots and worms
develop resistance to insecticides. Cornell News, 13 Feb., 2002. Available at: http://www.news.
cornell.edu/releases/Feb02/Hoffman-IPM.bpf.html
Gabel, B. and Thiery, D. (1992) Biological evidence of an oviposition-deterring pheromone in Lobesia
botrana Den. et Schiff. (Lepidoptera, Tortricidae). Journal of Chemical Ecology 18, 353–358.
Girolami, V., Vianello, A., Strapazzon, A., Ragazzi, E. and Veronese, G. (1981) Ovipositional deterrents in
Dacus oleae. Entomologia Experimentalis et Applicata 29, 177–188.
Godfrey, L.D. and Leigh, T.F. (1994) Alfalfa harvest strategy effect on lygus bug (Hemiptera: Miridae) and
insect predator population density: implications for use as a trap crop in cotton. Environmental
Entomology 23, 1106–1118.
Gordon, F.C. and Potter, D.A. (1985) Efficiency of Japanese beetle (Coleoptera: Scarabaeidae) traps in
reducing defoliation of plants in the urban landscape and effect on larval density in turf. Journal of
Economic Entomology 78, 774–778.
Gould, F. (1984) Role of behavior in the evolution of insect adaptation to insecticides and resistant host
plants. Bulletin of the Entomological Society of America 30, 34–51.
Gould, F. (1998) Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology.
Annual Review of Entomology 43, 701–726.
Grant, G.G. and Langevin, D. (1995) Oviposition deterrence, stimulation, and effect on clutch size of
Choristoneura (Lepidoptera: Tortricidae) species by extract fractions in host and nonhost foliage.
Environmental Entomology 24, 1656–1663.
Gray, D.R. and Borden, J.H. (1989) Containment and concentration of mountain pine beetle (Coleoptera:
Scolytidae) infestations with semiochemicals, validation by sampling of baited and surrounding
zones. Journal of Economic Entomology 82, 1399–1405.
Gross, H.R. Jr (1984) Spodoptera frugiperda (Lepidoptera: Noctuidae): deterrence of oviposition by aque-
ous homogenates of fall armyworm and corn earworm larvae applied on whorl-stage corn.
Environmental Entomology 13, 1498–1501.
Harris, M.O. and Miller, J.R. (1982) Synergism of visual and chemical stimuli in the oviposition behavior
of Delia antiqua. In: Visser, J.H. and Minks, A.K. (eds) Proceedings 5th International Symposium on
Insect–Plant Relationships. Pudoc, Wageningen, The Netherlands, pp. 117–122.
Harris, M.O. and Miller, J.R. (1983) Color stimuli and oviposition behaviour of the onion fly, Delia anti-
qua (Meigen) (Diptera: Anthomyiidae). Annals of the Entomological Society of America 76, 766–771.
Harris, M.O. and Miller, J.R. (1986) Host-acceptance behavior in an herbivorous fly, Delia antiqua. Journal
of Insect Physiology 34, 179–190.
Harris, M.O. and Rose, S. (1990) Chemical, color, and tactile cues influencing the oviposition behavior of
the Hessian fly (Diptera: Cecidomyiidae). Environmental Entomology 19, 303–308.
Hausmann, S.M. and Miller, J.R. (1989) Production of onion fly attractants and ovipositional stimulants
by bacterial isolates cultured on onion. Journal of Chemical Ecology 15, 905–916.
Haynes, K.F. and Baker, T.C. (1989) An analysis of anemotactic flight in female moths stimulated by host
odour and comparison with the males’ response to sex pheromone. Physiological Entomology 14,
279–289.
09IntpestManCh9.QXD 14/4/04 2:25 pm Page 202

202 R.S. Cowles

Hesjedal, K. (1984) Influence of the nitrogen content in strawberry leaves on the fecundity of the vine
weevil, Otiorhynchus sulcatus F. (Coleoptera: Curculionidae). Acta Agricultura Scandinavica 34,
188–192.
Hokkanen, H.M.T. (1991) Trap cropping in pest management. Annual Review of Entomology 36, 119–138.
Honda, K. (1995) Chemical basis of differential oviposition by lepidopterous insects. Archives of Insect
Biochemistry and Physiology 30, 1–23.
Huang, X.P., Renwick, J.A.A. and Sachdev-Gupta, K. (1994) Oviposition stimulants in Barbarea vulgaris
for Pieris rapae and P. napi oleracea: isolation, identification and differential activity. Journal of
Chemical Ecology 20, 423–438.
Hunt, D.W.A. and Whitfield, G. (1996) Potato trap crops for control of Colorado potato beetle
(Coleoptera: Chrysomelidae) in tomatoes. Canadian Entomologist 128, 407–412.
Hurter, J., Boller, E.F., Stadler, E., Raschdorf, F. and Schreiber, J. (1989) Oviposition-deterring pheromone
in Rhagoletis cerasi L.: purification and determination of the chemical constitution. In: Cavalloro, R.
(ed.) Fruit Flies of Economic Importance. Proceedings of the CEC/IOBC International Symposium, 7–10
April 1987, Rome, pp. 147–148.
Jackson, D.M. and Sisson, V.A. (1998) Potential of Nicotiana kawakamii (Solanaceae) as a trap crop for pro-
tecting flue-cured tobacco from damage by Heliothis virescens (Lepidoptera: Noctuidae) larvae.
Journal of Economic Entomology 91, 759–766.
Jones, T.H., Cole, R.A. and Finch, S. (1988) A cabbage root fly oviposition deterrent in the frass of garden
pebble moth caterpillars. Entomologia Experimentalis et Applicata 49, 277–282.
Judd, G.J.R. and Borden, J.H. (1989) Distant olfactory response of the onion fly, Delia antiqua, to host-plant
odor in the field. Physiological Entomology 14, 429–441.
Judd, G.J.R. and Borden, J.H. (1991) Sensory interaction during trap-finding by female onion flies: impli-
cations for ovipositional host-plant finding. Entomologia Experimentalis et Applicata 58, 239–249.
Judd, G.J.R. and Borden, J.H. (1992) Aggregated oviposition in Delia antiqua (Meigen): a case for media-
tion by semiochemicals. Journal of Chemical Ecology 18, 621–635.
Kanno, H. and Harris, M.O. (2002) Avoidance of occupied hosts by the Hessian fly: oviposition behav-
iour and consequences for larval survival. Ecological Entomology 27, 177–188.
Kennedy, G.G., Gould, F., DePonti, O.M.B. and Stinner, R.E. (1987) Ecological, agricultural, genetic, and
commercial considerations in the deployment of insect-resistant germplasm. Environmental
Entomology 16, 327–338.
Kennedy, J.S., Booth, C.O. and Kershaw, W.J.S. (1961) Host finding by aphids in the field. III. Visual
attraction. Annals of Applied Biology 49, 1–21.
Klijnstra, J.W. (1986) The effect of an oviposition deterring pheromone on egglaying in Pieris brassicae.
Entomologia Experimentalis et Applicata 41, 139–146.
Klijnstra, J.W. and Schoonhoven, L.M. (1987) Effectiveness and persistence of the oviposition deterring
pheromone of Pieris brassicae in the field. Entomologia Experimentalis et Applicata 45, 227–235.
Kozlowski, M.W. (1989) Oviposition and host object marking by the females of Ceutorhynchus floralis
(Coleoptera: Curculionidae). Entomologia Generalis 14, 197–201.
Kumar, H. (1992) Inhibition of ovipositional responses of Chilo partellus (Lepidoptera: Pyralidae) by the
trichomes on the lower leaf surface of a maize cultivar. Journal of Economic Entomology 85, 1736–1739.
Lewin, R. (1988) The uncertain perils of an invisible landscape. Science 240, 1405–1406.
Lockwood, J.A., Sparks, T.C. and Story, R.N. (1984) Evolution of insecticide resistance to insecticides: a
reevaluation of the roles of physiology and behavior. Bulletin of the Entomological Society of America
30, 41–50.
Lundgren, L. (1975) Natural plant chemicals acting as oviposition deterrents on cabbage butterflies, Pieris
brassicae (L.), P. rapae (L.), and P. napi (L.). Zoologica Scripta 4, 253–258.
Mangel, M. (1989) An evolutionary interpretation of the ‘motivation to oviposit.’ Journal of Evolutionary
Biology 2, 157–172.
Mangel, M. and Roitberg, B.D. (1989) Dynamic information and host acceptance by a tephritid fruit fly.
Ecological Entomology 14, 181–189.
Maxwell, F.G. (1977) Plant resistance to cotton insects. Bulletin of the Entomological Society of America 23,
199–203.
Mayhew, P.J. (1997) Adaptive patterns of host-plant selection by phytophagous insects. Oikos 79, 417–428.
Mbata, G.N. and Ramaswamy, S.B. (1995) Factors affecting the stability and recognition of the oviposition
marker pheromone of Callosobruchus subinnotatus (Pic). Journal of Stored Products Research 31,
157–163.
09IntpestManCh9.QXD 14/4/04 2:25 pm Page 203

Host Finding and Acceptance in Insects 203

McBride, J. (2000) Whitewashing agriculture. Agriculture Research 48, 14–17.

McDonald, R.S. and Borden, J.H. (1997) Host-finding and upwind anemotaxis by Delia antiqua (Diptera:
Anthomyiidae) in relation to age, ovarian development, and mating status. Environmental
Entomology 26, 624–631.
Messina, F.J., Barmore, J.L. and Renwick, J.A.A. (1987) Oviposition deterrent from eggs of Callosobruchus
maculatus: spacing mechanism or artifact? Journal of Chemical Ecology 13, 219–226.
Metcalf, R.L. and Lampman, R.L. (1989) Estragole analogues as attractants for corn rootworms
(Coleoptera: Chrysomelidae). Journal of Economic Entomology 82, 123–129.
Miller, J.R. (1986) Cull Onions as a Trap Crop for Onion Maggot. Funded proposal of USDA Competitive
Research Grants Office, Washington, DC.
Miller, J.R. and Cowles, R.S. (1990) Stimulo-deterrent diversion: a concept and its possible application to
onion maggot control. Journal of Chemical Ecology 16, 3197–3212.
Miller, J.R. and Harris, M.O. (1985) Viewing behavior-modifying chemicals in the context of behavior:
lessons from the onion fly. In: Acree, T.E. and Soderlund, D.M. (eds) Semiochemistry: Flavors and
Pheromones. Walter de Gruyter, Berlin, pp. 3–31.
Miller, J.R. and Strickler, K.L. (1984) Finding and accepting host plants. In: Bell, W.J. and Cardé, R.T. (eds)
Chemical Ecology of Insects. Chapman & Hall, New York, pp. 127–155.
Pair, S.D. (1997) Evaluation of systemically treated squash trap plants and attracticidal baits for early-
season control of striped and spotted cucumber beetles (Coleoptera: Chrysomelidae) and squash
bug (Hemiptera: Coreidae) in cucurbit crops. Journal of Economic Entomology 90, 1307–1314.
Papaj, D.R. (1986) Conditioning of leaf-shape discrimination by chemical cues in the butterfly Battus
philenor. Animal Behavior 34, 1281–1288.
Papaj, D.R. and Prokopy, R.J. (1988) The effect of prior adult experience on components of habitat prefer-
ence in the apple maggot fly (Rhagoletis pomonella). Oecologia 76, 538–543.
Papaj, D.R., Averill, A.L., Prokopy, R.J. and Wong, T.T.Y. (1992) Host-marking pheromone and use of pre-
viously established oviposition sites by the Mediterranean fruit fly (Diptera: Tephritidae). Journal of
Insect Behavior 5, 583–598.
Petterson, J., Karunaratne, S., Ahmed, E. and Kumar, V. (1998) The cowpea aphid, Aphis craccivora, host
plant odours and pheromones. Entomologia Experimentalis et Applicata 88, 177–184.
Poirier, L.M. and Borden, J.H. (1991) Recognition and avoidance of previously laid egg masses by the
oblique-banded leafroller (Lepidoptera: Tortricidae). Journal of Insect Behavior 4, 501–508.
Poirier, L.M. and Borden, J.H. (2000) Influence of diet on repellent and feeding-deterrent activity of larval
oral exudates in spruce budworms (Lepidoptera: Tortricidae). Canadian Entomologist 132, 81–89.
Prokopy, R.J. (1981) Oviposition-deterring pheromone system of apple maggot flies. In: Mitchell, E.R.
(ed.) Management of Insect Pests with Semiochemicals. Plenum Press, New York, pp. 477–494.
Prokopy, R.J. (1986) Visual and olfactory stimulus interaction in resource finding by insects. In: Payne,
T.L., Birch, M.C. and Kennedy, C.E.J. (eds) Mechanisms in Insect Olfaction. Clarendon Press, Oxford,
UK, pp. 81–89.
Prokopy, R.J. and Owens, E.D. (1983) Visual detection of plants by herbivorous insects. Annual Review of
Entomology 28, 337–364.
Prokopy, R.J., Collier, R.H. and Finch, S. (1983) Leaf color used by cabbage root flies to distinguish among
host plants. Science 221, 190–192.
Pyke, B., Rice, M., Sabine, G. and Zalucki, M. (1987) The push–pull strategy–behavioral control of
Heliothis. The Australian Cotton Grower 8, 7–9.
Quiring, D.T. and McNeil, J.N. (1984) Intraspecific competition between different aged larvae of
Agromyza frontella (Rondani) (Diptera: Agromyzidae): advantages of an oviposition-deterring
pheromone. Canadian Journal of Zoology 62, 2192–2196.
Quiring, D.T., Sweeney, J.W. and Bennett, R.G. (1998) Evidence for a host-marking pheromone in white
spruce cone fly, Strobilomyia neanthracina. Journal of Chemical Ecology 24, 709–721.
Radin, A.M. and Drummond, F.A. (1994) An evaluation of the potential use of trap cropping for control
of the striped cucumber beetle, Acalymma vittatta (F.) (Coleoptera: Chrysomelidae). Journal of
Agricultural Entomology 11, 95–113.
Renwick, J.A.A. and Radke, C.D. (1980) An oviposition deterrent associated with frass from feeding lar-
vae of the cabbage looper, Trichoplusia ni (Lepidoptera: Noctuidae). Environmental Entomology 9,
318–320.
Renwick, J.A.A. and Radke, C.D. (1987) Chemical stimulants and deterrents regulating acceptance or
rejection of crucifers by cabbage butterflies. Journal of Chemical Ecology 13, 1771–1776.
09IntpestManCh9.QXD 14/4/04 2:25 pm Page 204

204 R.S. Cowles

Rice, M. (1986) Semiochemicals and sensory manipulation strategies for behavioral management of
Heliothis spp. Oshsenheimer (Lepidoptera: Noctuidae). In: Zalucki, M.P. and Twine, P.H. (eds)
Heliothis Ecology Workshop 1985 Proceedings. Queensland Department of Primary Industries,
Brisbane, Australia, pp. 27–45.
Roitberg, B.D. and Prokopy, R.J. (1983) Host deprivation influence on response of Rhagoletis pomonella to
its oviposition deterring pheromone. Physiological Entomology 8, 69–72.
Roitberg, B.D., Cairl, R.S. and Prokopy, R.J. (1984) Oviposition deterring pheromone influences disper-
sal distance in tephritid fruit flies. Entomologia Experimentalis et Applicata 35, 217–220.
Scarpati, M.L., Lo-Scalzo, R. and Vita, G. (1993) Olea europaea volatiles attractive and repellent to the
olive fruit fly (Dacus oleae, Gmelin). Journal of Chemical Ecology 19, 881–891.
Schoonhoven, L.M. (1990) Host-marking pheromones in Lepidoptera, with special reference to two
Pieris spp. Journal of Chemical Ecology 16, 3043–3052.
Schoonhoven, L.M., Sparnaay, T., van Wissen, W. and Meerman, J. (1981) Seven-week persistence of an
oviposition-deterrent pheromone of Pieris brassicae on cabbage plants. Journal of Chemical Ecology 7,
583–588.
Schoonhoven, L.M., Beerling, E.A.M., Klijnstra, J.W. and van Vugt, Y. (1990) Two related butterfly
species avoid oviposition near each other’s eggs. Experientia 46, 526–528.
Simmonds, M.S.J. and Blaney, W.M. (1996) Azadirachtin: advances in understanding its activity as an
antifeedant. Entomologia Experimentalis et Applicata 80, 23–26.
Spencer, J., Pillai, S. and Bernays, E.A. (1999) Synergism in the ovipositional behavior of Plutella
xylostella: sinigrin and wax compounds. Journal of Insect Behavior 12, 483–500.
Stansly, P.A. and Cate, J.R. (1984) Discrimination by ovipositing boll weevils (Coleoptera:
Curculionidae) against previously infested Hampea (Malvaceae) flower buds. Environmental
Entomology 13, 1361–1365.
Straw, N.A. (1989) Evidence for an oviposition-deterring pheromone in Tephritis bardanae (Schrank)
(Diptera: Tephritidae). Oecologia 78, 121–130.
Szentesi, A., Hopkins, T.L. and Collins, R.D. (1996) Orientation responses of the grasshopper, Melanoplus
sanguinipes, to visual, olfactory and wind stimuli and their combinations. Entomologia Experimentalis
et Applicata 80, 539–549.
Taylor, C.E. and Georghiou, G.P. (1979) Suppression of insecticide resistance by alteration of gene domi-
nance and migration. Journal of Economic Entomology 72, 105–109.
Teulon, D.A., Hollister, B., Butler, R.C. and Cameron, E.A. (1999) Color and odor responses of flying
western flower thrips: wind tunnel and greenhouse experiments. Entomologia Experimentalis et
Applicata 93, 9–19.
Thiery, D., Gabel, B. and Pouvreau, A. (1992) Semiochemicals isolated from the eggs of Ostrinia nubilalis
as oviposition deterrent in three other moth species of different families. Series Entomologica 49,
149–150.
Vernon, R.S., Kabaluk, T. and Behringer, A. (2000) Movement of Agriotes obscurus (Coleoptera: Elateridae)
in strawberry (Rosaceae) plantings with wheat (Graminae) as a trap crop. Canadian Entomologist 132,
231–241.
Visser, J.H. and Ave, D.A. (1978) General green leaf volatiles in the olfactory orientation of the Colorado
beetle, Leptinotarsus decemlineata. Entomologia Experimentalis et Applicata 24, 738–749.
Visser, J.H. and de Jong, R. (1987) Plant odour perception in the Colorado potato beetle: chemoattraction
towards host plants. Series Entomologica 41, 129–134.
Wilson, E.O. and Bossert, W.H. (1963) Chemical communication among animals. Recent Progress Hormone
Research 19, 673–716.
Zehnder, G.W., Murphy, J.F., Sikora, E.J. and Kloepper, J.W. (2001) Application to rhizobacteria for
induced resistance. European Journal of Plant Pathology 107, 39–50.
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10 Integrated Pest Management in Forestry:

Potential and Challenges

Imre S. Otvos
Natural Resources Canada, Canadian Forest Service, Pacific Forestry Centre,
506 West Burnside Road, Victoria, B.C., V8Z 1M5, Canada
E-mail: [email protected]

Introduction illustrated with three examples, two involv-

ing native species and one an introduced
The forest ecosystem is much more complex species, i.e. spruce budworms (illustrating
and resilient than that of agriculture and the the transition from the use of chemical to bio-
threshold level of damage caused by insects logical pesticides), Douglas fir tussock moth
or pathogens is much higher in forestry than (DFTM) (development of the first truly IPM
what most consumers are willing to accept for a defoliator) and gypsy moth (an intro-
on or in their fruits or vegetables. When a duced species that became established in
certain segment of the population is protest- eastern North America, but is still treated as a
ing, sometimes unlawfully, even against the quarantine pest in western North America).
proper and judicious use of pesticides in the Management of bark beetles, contributions in
forest environment, they should stop and forest weed and plant-pathogen control and,
think about the number of chemical sprays it finally, a perspective on the future potentials
takes to keep their apples and tomatoes free and challenges of IPM in forestry, exotic
of blemish. They should also think of the insects, decreasing pesticide use, genetic
home gardener and the number of sprays it engineering of entomopathogens and trans-
takes to keep their roses free of aphids or genetic trees will be discussed.
other ‘creepy-crawlies’.
This chapter will briefly summarize
events leading up to the development of inte- Importance of Forestry in Canada
grated pest management (IPM). Due to the
vastness of the candidate subject, only the Forestry is important to the Canadian econ-
stages and progression towards IPM in omy, but this importance is not reflected in
forestry will be illustrated by giving the amount of money dedicated to research
Canadian examples from my perspective. of forest pest-related problems, which in
The main objectives that will be dealt with many cases is lower than that provided in
and covered include a review of the biologi- other countries where forestry is also an
cal control of forest insects in Canada (mainly important part of the economy. Even so, it is
parasitoid introductions and work with postulated that the development of insect
insect viruses). The evolution of IPM will be control in forests of other countries where
© CAB International 2004. Integrated Pest Management: Potential, Constraints and Challenges
(eds O. Koul, G.S. Dhaliwal and G.W. Cuperus) 205
10IntpestManCh10.QXD 5/5/04 2:09 pm Page 206

206 I.S. Otvos

forestry is also important to the economy has entomologists because, in forestry, pest con-
followed a similar path to that of Canada. trol does not always have to be immediate
The forests of Canada occupy 45.3% (418 and the threshold level of economic damage
million ha) of the country’s total land area. is higher than in agriculture or horticulture
Of this, 245 million ha, about 58.6%, is pro- and some damage can often be tolerated.
ductive forestland (Lowe et al., 1996; FAO, Classical biological control was first used in
2002). Canada has 15.6% of the world’s soft- Canada’s forests against exotic insects, which
wood timber resource (19.3 billion m3), and were almost always introduced without their
is only exceeded by that of the former Soviet natural enemies. The use of biological con-
Union (60.4%). Canada is a major supplier of trol in Canada has a long history, starting in
forest products in the world: in 1999, it 1910 with the introduction of over 1000 spec-
accounted for 13.5% of the world’s total imens of the ichneumonid wasp, Mesoleius
coniferous tree harvest, ranking third after tenthredinis Morley, from England to control
the USA at 26.7% and Europe at 17.9% the larch sawfly, Pristiphora erichsonii Hartig
(Council of Forest Industries, 2000). In 1999, (McGugan and Coppel, 1962). Since that
Canada produced 21.2% of the world’s soft- time, considerable use has been made of the
wood lumber, and this represented about natural enemies of insects, using first insect
47.8% of the world’s softwood lumber parasitoids and predators and more recently
exports (Council of Forest Industries, 2000). entomopathogens.
The value of forest-product exports in 2001 The majority of attempts to control insect
was about CAN$44.1 billion. In the same pests in Canada using biological agents used
year, the net foreign-exchange earnings from only one group of organisms – parasitoids.
forestry were about $34.4 billion. This repre- In some cases a combination of two groups –
sents the second greatest contribution to the generally parasitoids and nucleopoly-
economy of Canada after energy production hedrovirus (NPV) – were used, and occa-
(Statistics Canada, 2002). sionally three groups – parasitoids, NPV and
Most of the forests in Canada are publicly Bacillus thuringiensis subsp. karstäki (Btk). The
owned. As the land base managed for timber best known example of the latter is gypsy
and other forestry use is shrinking and the moth. Biological control attempts against the
size of the forest set aside for parks and eco- spruce budworm have even tried to use a
logical reserves is increasing, the appetite fourth agent, microsporidia.
and demand of the increasing population Results of biological control attempts in
has to be met from a smaller forest land base. Canada have been documented in detail in
Therefore, the losses caused by insects, dis- the four volumes of Biological Control
ease and fire activity must be reduced. The Programmes Against Insects and Weeds in
average annual volume loss due to forest Canada (McGugan and Coppel, 1962;
insect pests for 1988–1992 is estimated at 5.9 Canadian Department of Agriculture and
million m3. This is less than the estimated Canadian Department of Fisheries and
20.9 million m3 volume loss caused by dis- Forestry, 1971; Kelleher and Hulme, 1984;
eases, but is more than double the 2.7 million Mason and Huber, 2002). Hulme (1988) has
m3 burned from 1988–1992 and constitutes also published a brief summary of some of
6% of the 102.3 million m3 annual harvest the highlights. Figure 10.1 shows that the
(Wood and Van Sickle, 1994). biological control attempts were entomocen-
tric, most of the targets were insects (both
agricultural and forest pests) and most of the
Biological Control of Forest Insects in control agents introduced were also insects.
Canada Considerably fewer control programmes
were conducted on weeds and there was no
Both inoculative and inundative methods of work done on plant pathogens until the last
insect control have been used in forestry, two decades (Fig. 10.1). Only control
with varying degrees of success. Classical attempts using parasitoids and insect viruses
biological control has great appeal to forest will be discussed in this section.
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 207

IPM in Forestry 207

Since the early 20th century, biological con-

trol attempts have been conducted against 22
exotic forest insects (Table 10.1) and 27 native
forest insects (Table 10.2) in Canada. In most
60 cases the biocontrol agents used were para-
Number of targets

50 sitoids, pathogens (mainly viruses and Btk)

40 and in a few cases predators. Some of the
30 Insects early introductions were only explorative
20 Weeds and tentatively assessed (McGugan and
10 Pathogens Coppel, 1962), and a re-evaluation of the out-
0 comes of all the introductions may be in
order.
8

0
0
8

96

00
98
95

–1

–2
–1
–1

Of the 22 exotic forest pests, 17 had a sin-

59

81
69
10

gle control-agent group (parasitoids) intro-

19

19
19
19

Fig. 10.1. Comparison of the number of biological

duced to control them. Of the 17 species, the
control projects conducted against insects, weeds introduction was considered successful
and plant pathogens in Canada between 1910 and against eight (47%), resulting in long-term
2000 (after Mason and Huber, 2002). control that suppressed the pest, virtually
eliminating the damage without need for
Canada was one of the leaders of classical further direct application of the control. The
biological control, in both agriculture and introduction of parasitoids was partially suc-
forestry. There were three main reasons for cessful against two species, promising
this: against three species, unknown in two cases
and two were classified as failures. In the
● In the past, most invasive species in case of the remaining five exotic species, the
North America came from Europe, reflect- introduction of two (usually parasitoid and
ing past trading patterns and routes NPV) or three natural control-agent groups
(Mattson et al., 1994; Niemela and occurred. The outcome of these introduc-
Mattson, 1996). tions was successful with at least one of the
● The value of biological control in Canada control-agent groups (Table 10.1).
was recognized at an early date. When one is evaluating the control out-
‘Throughout the history of classical bio- come of pathogen use, it is worth consider-
logical control in Canada a close link has ing the difference between the use and
existed between CAB International (for- success of NPV and Btk in biological control.
merly IIBC or CIBC) in Delemont, NPV is to some degree self-propagating after
Switzerland, and Agriculture and Agri- it has been applied, and is usually applied
Food Canada (AFC, formerly Agriculture only once during the course of an outbreak
Canada) and Canadian Forest Service lab- to achieve control, while Btk almost always
oratories’ (Mason et al., 2002: xiii). has to be applied annually until the outbreak
● ‘The first biological control laboratory collapses or, in the case of quarantine pests,
was established in Canada … in until the target insect is eradicated. In some
Fredericton in 1912 … [then] The cases, Btk has to be applied several times in a
Dominion Parasite Laboratory was estab- season and maybe for a number of years to
lished in 1929 at Belleville [Ontario] …’ achieve the desired level of control. An
(Wallace, 1995) and was operating until example of the latter is gypsy-moth eradica-
1972, when it was closed due to cutbacks tion in western North America, where Btk is
and government reorganization. applied three or four times to the susceptible
Regarding the Belleville laboratory, stage in the course of a year for 2–3 years
Mason et al. (2002: xiii) state: ‘This labora- until eradication is achieved. Therefore, it
tory had one of the largest concentrations should be noted that although the use of bac-
of biological control specialists in the terium (Btk) application is classified as a suc-
world.’ cess, it should be classified as a ‘success’ only
Table 10.1. Evaluation of the biological control attempts against exotic forest insect pests in Canada between 1910 and 2000.a
208

Target pest Common name Control agent Outcomeb

Coleophora laricella (Hübner) Larch case-bearer Parasitoids Success

Eulecanium tiliae (Linnaeus) Lecanium scale Parasitoids Success
Fenusa pusilla (Lepeletier) Birch leaf-miner Parasitoids Success
Leucoma salicis (Linnaeus) Satin moth Parasitoids Success
Diprion similis (Hartig) Introduced pine sawfly Parasitoids Success
Gilipnia hercyniae (Hartig) European spruce sawfly Parasitoids Success
Pristiphora erichsonii (Hartig) Larch sawfly Parasitoids Success
Pristiphora geniculata (Hartig) Mountain ash sawfly Parasitoids Success
Adelges piceae (Ratzeburg) Balsam woolly adelgid Predators Partial success
Rhyacionia buoliana (Denis and Schiffmuller) European pine-shoot moth Parasitoids Partial success
Acantholyda erythrocephala (Linnaeus) Pine false web-worm Parasitoids Promising
Profenusa thomsoni (Konow) Amber-marked birch leaf-miner Parasitoids Promising
Xanthogaleruca luteola (Müller) Elm-leaf beetle Bacterium Promising
Carulaspis juniperi (Bouche) Juniper scale Parasitoids Failure
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 208

Coleophora serratella (Linnaeus) Birch case-bearer Parasitoids Failure

Euproctis chrysorrhoea (Linnaeus) Brown-tail moth Predators Unknown
Gilpinia frutetorum (Fabricius) Nursery pine sawfly Parasitoids Unknown
Lymantria dispar (Linnaeus) Gypsy moth Parasitoids [Partial] success
I.S. Otvos

Bacterium [Partial] success

NPV Partial success
Operophtera brumata (Linnaeus) Winter moth Parasitoids Success
Bacterium [Partial] success
NPV Partial success
Neodiprion lecontei (Fitch) Red-headed sawfly Parasitoids Success
Bacterium [Partial] success
NPV Success
Neodiprion sertifer (Geoffroy) European pine sawfly Parasitoids Success
NPV Success
Neodiprion swainei (Middleton) Swaine jack pine sawfly Predators Partial success
Parasitoids Partial success
NPV Success
a The list was compiled from the four volumes of the review of biocontrol programmes in Canada (McGugan and Coppel, 1962; Canadian Department of
Agriculture and Canadian Department of Fisheries and Forestry, 1971; Kelleher and Hulme, 1984; Mason and Huber, 2002).
b It should be noted that the classification categories under ‘outcome’ are somewhat confusing. Success can mean: (i) the introduction was successful and the
organism became established and has an impact on the original target host but it does not necessarily control the pest (e.g. parasitoid introduction or the use
of Btk against the gypsy moth); or (ii) the target organism is under control now after the introduction (e.g. larch sawfly or the winter moth). These will be
clarified in a later re-analysis of the control attempts.
Table 10.2. Evaluation of the biological control attempts against native forest insect pests in Canada between 1910 and 2000.a

Target pest Common name Control agent Outcomeb

Acleris gloverana (Walsingham) Western black-headed budworm Bacterium Partial success

Acleris variana (Fernald) Eastern black-headed budworm Bacterium Partial success
Hemichroa crocea (Geoffroy) Striped alder sawfly Parasitoids Success
Coleotechnites starki (Freeman) Lodgepole needle miner Parasitoids Failure
Cydia strobilella (Linnaeus) Spruce seed moth Parasitoids Failure
Lambdina fiscellaria somniaria (Hulst) Western oak looper Predators Failure
Pissodes strobi (Peck) White pine weevil Parasitoids Failure
Exoteleia pinifoliella (Chambers) Pine needle miner Parasitoids Unknown
Mindarus abietinus Koch Balsam twig aphid Predators Unknown
Neodiprion pratti Dyar Jack pine sawfly Parasitoids Unknown
Neodiprion nanulus Schedl Red pine sawfly Parasitoids Unknown
Neodiprion tsugae Middleton Hemlock sawfly Parasitoids Unknown
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 209

Neodiprion virginianus complex Pine sawfly Parasitoids Unknown

Operophtera bruceata (Hulst) Bruce spanworm NPV Unknown
Pineus strobi (Hartig) Pine bark adelgid Predators Unknown
Dendroctonus rufipennis (Kirby) Eastern spruce beetle Predators Failure
Parasitoids Failure
Choristoneura fumiferana (Clemens) Spruce budworm Parasitoids Partial success
IPM in Forestry

Bacterium Partial success

NPV Partial success
Other viruses (CPV, GV, EV) Partial success
Microsporidia Partial success
Choristoneura occidentalis Freeman Westerm spruce budworm Bacterium Partial success
NPV Partial success
Other viruses (CPV, GV, EV) Partial success
Choristoneura pinus pinus Freeman Jack pine budworm Bacterium Success
NPV Success
Lambdina fiscellaria fiscellaria Guenée Hemlock looper Parasitoids Failure
Bacterium Partial success
Lambdina fiscellaria lugubrosa Hulst Western hemlock looper Predator Unknown
209

Continued on next page

 210

Table 10.2. Continued from previous page.

Target pest Common name Control agent Outcomeb

Malacosoma disstria Hübner Forest tent caterpillar Parasitoids Success

Bacterium Partial success
NPV Failure
Microsporidia Failure
Orgyia leucostigma (J.E. Smith) White-marked tussock moth Bacterium Partial success
NPV Success
Orgyia pseudotsugata (McDunnough) Douglas fir tussock moth Bacterium Partial success
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 210

NPV Success
Zeiraphera canadensis Mutuura and Freeman Spruce bud moth Parasitoids Failure
Bacterium Failure
Nematodes Partial success
I.S. Otvos

Neodiprion abietis (Harris) Balsam fir sawfly Parasitoids Unknown

Bacterium Partial success
NPV Unknown
Pikonema alaskensis (Rohwer) Yellow-headed spruce sawfly Parasitoids Unknown
Bacterium Partial success
Nematodes Success
a The list was compiled from the four volumes of the review of biocontrol programmes in Canada (McGugan and Coppel, 1962; Canadian Department of
Agriculture and Canadian Department of Fisheries and Forestry, 1971; Kelleher and Hulme, 1984; Mason and Huber, 2002).
b It should be noted that the classification categories under ‘outcome’ are somewhat confusing. Success can mean: (i) the introduction was successful and the
organism became established and has an impact on the original target host but it does not necessarily control the pest (e.g. parasitoid introduction or the use
of Btk against the gypsy moth); or (ii) the target organism is under control now after the introduction (e.g. larch sawfly or the winter moth). These will be
clarified in a later re-analysis of the control attempts.
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 211

IPM in Forestry 211

in cases of eradication (gypsy moth from European spruce sawfly cost about
western North America). In other cases, CAN$300,000 and saved 8.5 million cords of
when Btk is applied to reduce the pest popu- wood valued at CAN$6 million, giving a
lation, its use should perhaps be classified as cost : benefit ratio of 1:20 (Reeks and
partial success, since it generally has to be Cameron, 1971). In the case of another defoli-
applied for a number of consecutive years. ating insect, the winter moth, the cost of
Control attempts were made against 27 introducing parasitoids into eastern Canada
native forest insects using parasitoids, preda- was estimated at $160,000 and the value of
tors and pathogens: 15 by a single group and the oak trees killed before the introduction
12 by multiple groups of organisms (Table was estimated at CAN$2 million. The intro-
10.2). Of the single-group introductions duction of parasitoids prevented the loss of
against native pests, three (12%) of the 15 another CAN$12 million worth of oak trees.
were classified as successful, four (26.7%) as Based on these, the cost:benefit ratio was
failures and the remaining eight (53.3%) as estimated at 1:12.5 (Embree, 1971).
unknown. Of the 12 other native pests tar-
geted with multiple-group introductions, one
(eastern spruce beetle) was a failure, and for Viral insecticides
the other 11 species at least one of the biologi-
cal control agents tried was successful. Interest in the use of viruses for forest insect
It should be noted that the outcome ‘suc- control in Canada began in the late 1930s
cess’ means that the biological control agent with the discovery of a polyhedrovirus that
tried/introduced became established (in the was credited with causing the collapse of a
case of parasitoids and predators), main- large outbreak of the European spruce
tained its population and attacked and killed sawfly, Gilpinia hercyniae Hârtig, the most
a portion of the target pest. In the case of important forest defoliator at that time
pathogens (either virus or Btk) success meant (Balch and Bird, 1944; Cameron, 1975a). The
that it infected and killed a proportion of the European spruce sawfly virus had been acci-
target insect and the introduced organisms dentally introduced from Europe, probably
did not necessarily produce an acceptable along with one of the imported parasitoids
level of control over the pest. The case of of the sawfly.
Choristoneura fumiferana (Clemens) illustrates The impressive beneficial effect of this
this point well. All the control agents listed accidental virus introduction resulted in
in Tables 10.1 and 10.2 had an effect and accelerated work with insect viruses in the
therefore could be classified as a ‘success’, hope that outbreaks of various other pests
but in terms of control all five groups had could also be terminated with viruses, simi-
only partial success because the spruce bud- lar to that of the European spruce sawfly.
worm still has to be controlled, i.e. by apply- Most of the work to develop viral insecti-
ing one of the control-agent groups listed. cides for several insect pests has been done
Data are scarce on the benefits and mone- on NPVs and granuloviruses (GV), sub-
tary return of the cost of developing and groups A and B, respectively, of the family
applying classical biological control mea- Baculoviridae. Limited work has also been
sures. No thorough cost–benefit analysis has conducted on cytoplasmic polyhedroviruses
been done in Canada on the use of biological (CPVs – Reoviridae) and entomopox virus
control. However, one such summary was (EPV – Poxviridae) as potential control
compiled for biological control activities in agents for the spruce budworm (Table 10.3;
Australia. Of the 12 biological control Cunningham and Kaupp, 1995).
attempts conducted, all were analysed, two- NPVs and GVs are highly host-specific,
thirds were considered successful and the although some viruses may infect several
overall cost:benefit ratio, based on all 12 related species in the same genus
attempts, was 1:10 (Marsden et al., 1980). (Cunningham and Kaupp, 1995), e.g. Orgyia
Hulme (1988) cited two cost : benefit esti- spp. Their high host specificity makes viral
mates from Canada. Biological control of the insecticides ideal from an ecological point of
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212 I.S. Otvos

Table 10.3. Research and operational applications of insect viruses against the more important forest
defoliators in Canada, 1971–2000 (Kelleher and Hulme, 1984; Mason and Huber, 2002).

Target insect Total area

sprayed
Common name Scientific name Virus Year(s) ha/tp

Spruce budworm Choristoneura fumiferana NPV 1971–2000 2180a

Spruce budworm Choristoneura fumiferana GV 1979–1980 16
Spruce budworm Choristoneura fumiferana EPV 1971–1972 519
Spruce budworm Choristoneura fumiferana EPV + NPV 1972 32b
Western spruce budworm Choristoneura occidentalis NPV 1976–1982 252
Western spruce budworm Choristoneura occidentalis GV 1982 172
Jack pine budworm Choristoneura pinus pinus NPV 1985 50
Gypsy moth Lymantria dispar NPV 1982–1994 1280c
Forest tent caterpillar Malacosoma disstria NPV 1976–1980 45
Balsam fir sawfly Neodiprion abietis NPV 1999 4
European pine sawfly Neodiprion sertifer NPV 1975–1993 152
Red-headed pine sawfly Neodiprion lecontei NPVd 1976–1995 5881
White-marked tussock moth Orgyia leucostigma NPV 1975–1987 43
Douglas fir tussock moth Orgyia pseudotsugata NPVe 1974–1993 2620
a Includes 16 ha sprayed with NPV and fenitrothion.
b Includes 16 ha sprayed with NPV + EPV and fenitrothion.
c Cunningham (1998).
d Red-headed pine sawfly NPV was registered in 1987 as Lecontvirus.
e Douglas fir tussock moth NPV was registered under the names Virtuss® (OpNPV produced in Orgyia
leucostigmata) and TM-Biocontrol-1 (OpMNPV produced in Orgyia pseudotsugata).
f tp, time period.

view, but it also makes their development between 1933 and 1951, of which nine
and commercialization less attractive for became established (McGugan and Coppel,
profit-making companies. Consequently, all 1962). In the late 1930s an NPV was noticed
development work and registration of in the sawfly populations and was the key
viruses for forestry use in Canada was done factor in controlling this sawfly (Balch and
in the laboratories of the Canadian Forest Bird, 1944). The virus was fortuitously intro-
Service, in cooperation with some of the duced with parasitoids from Europe. After
provincial governments. the virus epizootic in central Canada, the
Field trials using viruses have been con- virus was purposefully transferred to a num-
ducted on 19 species of forest insect pests in ber of new locations in eastern Canada
Canada; 11 Lepidoptera and eight (McGugan and Coppel, 1962). The outbreak
Hymenoptera. Both aerial and ground trials collapsed in the early 1940s and the
were conducted on eight species, while the European spruce sawfly has been controlled
remainder were tested with ground applica- since then by the introduced parasitoids and
tions only (Cunningham and Kaupp, 1995). the virus, as no further outbreaks recurred.
The more important virus tests for ten Similarly, the red-headed pine sawfly,
insects are summarized in Table 10.3. Neodiprion lecontei Fitch, is one of the most
The control of the European spruce important insects attacking young red pine,
sawfly, Gilpinia hercyniae (Hartig), may be the Pinus resinosa Aiton, plantations in eastern
best example of a biological control pro- Canada. An NPV was found in red-headed
gramme in Canada. It was an important pest pine sawfly in 1950 (Bird, 1961), and exten-
of spruce trees in eastern Canada and the sive laboratory and ground-spray trials con-
USA. Twenty-seven species of parasitoids ducted on the virus showed promise
from Europe and Japan were released (Cunningham and de Groot, 1984;
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IPM in Forestry 213

Cunningham et al., 1986). The virus was observed. Because of the economic impor-
tested experimentally between 1978 and 1980 tance of the spruce budworm, genetic
in Quebec in 92 plantations with a combined manipulation of its virus to enhance its effec-
area of 1051 ha. The virus was also tested in tiveness was a high priority of the Canadian
Ontario between 1980 and 1990 in 478 plan- government (Cunningham and Kaupp,
tations with a combined area of 3546 ha. 1995). However, no significant advancements
Based on these successful applications, the were made in improving virus efficacy over
virus received temporary registration in 1983 the last 20 years and Btk is still the only
and full registration in 1987 under the trade pathogen registered for budworm control.
name Lecontvirus®. The production of this
and other similar viruses in colony-feeding
sawflies is relatively easy and cost effective. Viruses registered for forest insect control in
Heavily infested plantations are treated with Canada
the virus by mist-blowers and the dead
colonies are collected daily (preferably), Following the more important virus trials
starting 1 week after treatment described above, three viral insecticides, all
(Cunningham and McPhee, 1986). NPVs, received temporary registration in
Orgyia pseudotsugata (McDunnough) is a 1983 and full registration in Canada in 1987:
native defoliator in British Columbia, one for the red-headed pine sawfly, N. lecon-
Canada and the north-western USA. tei, and two for the control of DFTM,
Outbreaks of this defoliator recur periodi- O. pseudotsugata. The multicapsid isolate of
cally and are terminated by an epizootic the DFTM virus (OpMNPV), produced in
caused by a native NPV. This naturally DFTM larvae, was registered in the USA in
occurring virus was considered to have an 1976 under the trade name TM Biocontrol-
excellent potential for biological control both 1®. The same product, under the same trade
in Canada and in the USA. The work on the name, TM Biocontrol-1, was also registered
virus and how the virus was incorporated for use in Canada in 1987. In addition, the
into an IPM system is described later in this same virus, produced in Canada in the
chapter. C. fumiferana is the most important white-marked tussock moth, Orgyia leu-
forest insect pest in Canada and, as such, has costigma (J.E. Smith), also received full regis-
had the greatest number of biological control tration in 1987 under the trade name
agents tested against it (Tables 10.2 and 10.3). Virtuss® (Cunningham and Kaupp, 1995).
Because attempts to control it by parasitoid The recommended dosage on the label for
introduction (from Europe and Japan) or both viruses is 2.5  1011 polyhedral inclu-
relocation (from western Canada to eastern sion bodies (PIB) per hectare (Cunningham
Canada) did not provide the desired control, and Kaupp, 1995). Negotiations are currently
insect viruses were also investigated. underway in Canada to transfer the produc-
Extensive field trials with NPV, GV and EPV tion and sale of these three registered viruses
showed NPV to be the most efficacious virus to a private company for commercialization.
tested (Cameron, 1975b). Consequently, The use of these three registered viruses is
research concentrated on NPV (Cunningham insignificant compared with the use of Btk.
and Howse, 1984; Cunningham, 1985a). NPV
and GV were also tested against the western
spruce budworm, Choristoneura occidentalis Management of Spruce Budworms
Freeman (Otvos et al., 1989) and the jack pine (Choristoneura spp.)
budworm, Choristoneura pinus Freeman
(Table 10.3). While virus infection occurred Development of the management system
in the treated plots, mortality was generally currently used for the spruce budworms
low (40–60%) and not sufficient to control (Choristoneura spp.) illustrates well how the
the treated populations. Although virus does control for these important defoliators
occur in budworm populations in the field, evolved, from the use of a single hard chemi-
natural virus epizootics have never been cal to the use of the ecologically less disrup-
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 214

214 I.S. Otvos

60 Area defoliated 20

Area treated 18

treated with chemical insecticides

Area defoliateda (’000,000 ha) 50

Percentage of defoliated area

16
14
40
12
30 10
8
20
6
4
10
2

0 0

90
80

85

95
75

19
19

19

19
19

Year

Fig. 10.2. Area defoliated by spruce budworm, Choristoneura fumiferana, from 1975 to 1995 and the
percentage of defoliated area treated with insecticides for the same years (from Canadian Council of Forest
Ministers, 2003).
a Only areas that were moderately or severely defoliated were included in the source data.

tive bacterial insecticide Btk. Before the man- All three are native to North America and
agement system is discussed, it is worth- outbreaks have occurred repeatedly over the
while to sketch the economic importance of last three centuries (Blais, 1985; Harris et al.,
the insect over time. The change in economic 1985a). They pose a threat to approximately
importance has influenced our response to 60 million ha of susceptible forests in eastern
damage. It is also useful to mention key Canada and the USA (Nigam, 1980; Kettela,
research activities (including attempts to use 1983; Talerico, 1984). Budworm larvae feed
biological control agents) that were under- on a number of conifer species, and consecu-
taken in the hope of increasing our control tive years of defoliation result in growth
options for these budworm pests. The evolu- reduction, top kill and, ultimately, tree mor-
tion of budworm control measures in tality (Alfaro and Maclauchlan, 1992).
Canada is representative of how control Normally, 4–5 years of severe defoliation are
measures evolved for most forest defoliators, required to kill susceptible trees and approx-
not only in Canada, but in other parts of the imately 7–8 years to kill less vulnerable,
world as well. immature stands (MacLean, 1980). Prior to
the 1940s, spruce budworm damage was of
little concern because its principal host, bal-
Economic importance of spruce budworms
sam fir, Abies balsamea (L.) Miller, was consid-
ered a weed species and was not utilized. As
Among the forest defoliators in Canada,
the demand for wood increased, balsam fir
three budworms are the most important.
became an important commodity. Due to this
These are the:
change in forest utilization, the damage
● spruce budworm, C. fumiferana (Clemens); caused during the budworm outbreak in the
● western spruce budworm, C. occidentalis 1940s was considered unacceptable.
Freeman; Extensive spray operations were initiated
● jack pine budworm, C. pinus pinus and had to be continued, unfortunately,
Freeman. almost annually somewhere in Canada
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 215

IPM in Forestry 215

(Prebble, 1975; van Frankenhuyzen, 1990) up History of Aerial Applications of

to the present (Fig. 10.2). Insecticides in Canada’s Forests
In fact, several biological control agents
have been investigated over the years to Use of chemical insecticides
evaluate their potential for control of C.
fumiferana. These control agents included The history of the early use of insecticides
exotic and native parasitoids, viruses was summarized in various chapters for all
microsporidia, fungi and even irradiation. of Canada in Prebble (1975). Spruce bud-
Considerable work has been conducted on worm management, up to 1965, illustrates
mass rearing and release of the native egg the first generation of control measures.
parasitoid, Trichogramma minutum Riley, Defoliator management was exclusively
against C. fumiferana. These studies have based on the application of chemical insecti-
shown that parasitism of budworm eggs cides, using the most efficacious products
could be high (about 80%) in the small (the more insects killed, the better). The first
release plots, but the cost was also high aerial applications of insecticides in forestry,
(about CAN$400/ha) (Smith et al., 2002). using calcium arsenate dust, occurred
This approach may be justified in high-value between 1927 and 1930 on about 3200 ha
seed orchards but is not practical for large- against the spruce budworm, eastern hem-
scale use in forestry. lock looper, and the western hemlock looper
(Prebble, 1975). Starting in the mid-1940s,
Western spruce budworm parasitoids, not
the availability of dichlorodiphenyl-
present in eastern Canada, were introduced
trichloroethane (DDT), a wide-spectrum
from western Canada but did not become
insecticide, and surplus aircraft from the
established. Exotic parasitoids from two
Second World War led to the widespread use
closely related species from Europe
of aerial spraying to combat insect problems
(Choristoneura murinana (Hubner)) and Japan
in Canada on a large operational scale (Figs
(Choristoneura diversana (Hubner)) were
10.2 and 10.3). DDT and related compounds
imported and released against C. fumiferana
were adopted for forest insect control
in eastern Canada but these did not become
because they appeared very promising,
established either.
based on their use in agriculture and in pub-
Extensive field trials with four virus types lic health. After the early successes with
(CPV, NPV, EPV and GV) have been con- DDT (i.e. contained a typhus epidemic and
ducted against both C. fumiferana controlled malaria), overly optimistic state-
(Cunningham and Howse, 1984; ments, such as ‘mosquito-transmitted dis-
Cunningham, 1985a,b; Cunningham and ease will disappear’, ‘some pests will
Kaupp, 1995) and C. occidentalis (Otvos et al., become extinct’ and ‘all major pest problems
1989; Shepherd et al., 1995). The goal of initi- appeared to be solved or solvable’, became
ating an epizootic to control the budworm common (Casida and Quistad, 1998: 1). DDT
populations was not achieved in any of these became the most commonly used insecticide
trials (Cunningham and Kaupp, 1995) and in forestry because of its high efficacy against
the vertical transmission of the virus all defoliators and in the control of many
decreased in subsequent years (Otvos et al., agricultural insects. The use of DDT in the
1989). forests after the Second World War
None of these biological control attempts increased, but adversely affected fish popu-
offered a practical alternative to replace the lations (Logie, 1975) and DDT accumulated
use of insecticide. Consequently, most of the in birds and other components of the envi-
control work has concentrated on aerial ronment (Pearce, 1975).
treatment of larvae with insecticide, From 1965 to 1980 the second generation of
although attempts have also been made to insect control, including the spruce budworm,
spray spruce budworm adults with chemical was based on a reactive response – waiting
insecticides during dispersal, but without until there was an insect outbreak and then
the desired results (Kettela, 1995). trying to control it. Control was largely
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 216

216 I.S. Otvos

Spruce budworm
7000 Jack pine budworm 100
Eastern hemlock looper
Othersb 90

Percentage of area treated with Btk

6000
Area treated with insecticides

80
5000 70
60
(’000 ha)

4000
50
3000
40

2000 30
20
1000
10
0 0
71

75

80

85

90

95

00
19

19

19

19

19

19

20
Year

Fig. 10.3. Forest area in Canada treated with all insecticidesa from 1971 to 2000 (from Canadian Forest
Service, 1975, 1976, 1977, 1978; van Frankenhuyzen, 1990; Armstrong and Cook, 1993; Moody, 1993a,b;
Hall, 1994, 1995, 1996; Cadogan, 1995; Canadian Council of Forest Ministers, 2002).
aFor details including what insecticides were used over the years, see the source references. bOther insects

include gypsy moth, Lymantria dispar, and forest tent caterpillar, Malacosoma disstria.

achieved by the application of synthetic management issues posed by the spruce

chemical insecticides, first using wide-spec- budworm. However, it did provide new,
trum and then, as side effects became known, much needed, tools to use. Coarse hazard-
more selective chemical insecticides. The goal rating systems were developed, based on the
was to suppress the target insect populations location and frequency of past outbreaks and
with an efficacious product, with minimal on stand susceptibility (stands with a high
side effects, and to protect the infested stands proportion of balsam fir and > 60 years old)
until harvesting could occur or the outbreak (Regniere and Lysyk, 1995). Sex pheromones
collapsed. However, public pressure was were identified and used to monitor popula-
mounting to find biological alternatives to tion fluctuations of the insect and to warn of
chemical insecticides. impending outbreaks (Sanders, 1988).
In an effort to minimize damage caused Methods were developed to sample egg
by defoliators, considerable research was masses in the autumn and the overwintering
conducted on their population dynamics, larval stage in order to forecast expected
especially that of C. fumiferana, to try to defoliation (Morris, 1954; Miller, 1957; Miller
understand how and why outbreaks devel- et al., 1971). The forecasted level of defolia-
oped and the role of natural control factors. tion was, in turn, used to decide which
The Green River Project was the first large infested areas to protect. There was a shift
programme conducted on any insect pest in from treating as much infested area as possi-
Canada, and expectations were high. The ble with the available chemicals, aircrafts
salient points of the programme were sum- and funds to a more selective treatment of
marized in a volume edited by R.F. Morris infested areas.
(1963). While the programme contributed As the undesirable side effects of hard
much new knowledge, it did not solve the chemicals (broad-spectrum insecticides)
10IntpestManCh10.QXD 5/5/04 2:10 pm Page 217

IPM in Forestry 217

became known, there was a shift towards oped for aerial application on budworm-
more benign pesticides with fewer side infested forests, as it was relatively less toxic
effects. There was also a trend away from the to fish, birds and mammals than phos-
reactive mode towards a proactive mode of phamidon, fenitrothion and trichlorfon
insect management. With the proactive (Nigam, 1975), but it could not compete in
approach, attempts were made to predict cost and efficacy with fenitrothion and
when and where outbreaks would occur and aminocarb. Mexacarbate was used in small
to forecast the expected level of damage quantities from 1969 to 1974, until the sup-
(defoliation) (Morris, 1954; Miller, 1957; ply was exhausted (Nigam, 1975, 1980).
Miller et al., 1971) rather than waiting until Fenitrothion and aminocarb were the main
the outbreaks developed and severe damage insecticides used during the latter part of
had occurred. This was aided by the Green the 1970s, when approximately 9 million kg
River Project research. of fenitrothion and 0.9 million kg of
Despite progressively reducing the aminocarb were used (Nigam, 1980).
dosages of DDT used (from 1–2 lb./acre to The area of budworm-infested stands
0.25 lb./acre (Nigam, 1975)), effects on non- treated with insecticides rose dramatically
targets were still noted and deemed unac- during the mid-1970s in response to the
ceptable. The search for more acceptable and increased size of budworm outbreaks (Fig.
ecologically less disruptive substitutes 10.3). However, the proportion of treated to
began as early as the 1950s and eventually infested forest declined (Figs 10.2 and 10.3)
led to the replacement of DDT by non-per- during this period due to a shortage of
sistent organophosphates and carbamates in chemicals, economic constraints, and mount-
the late 1960s. Four organophosphates ing public opposition to the wide-scale use
(phosphamidon, fenitrothion, trichlorfon of chemical insecticides in the forest. During
and acephate) and two carbamates the latter part of the 1970s, political reaction
(aminocarb and mexacarbate) were regis- to public pressure over the Reye’s-syndrome
tered and used extensively. Phosphamidon controversy (Wood and Bogdan, 1986) and
was used initially as a buffer spray in water- suspected carcinogenicity of fuel oil carrier
shed areas to prevent DDT contamination of led to a gradual decline in the treatment of
prime salmon fisheries waters. However, the infested forests in eastern Canada (Nigam,
use of DDT was extended to large-scale 1980). This resulted in an increase in the size
operations during the mid-1970s, due to a of the dead or dying forests in the budworm-
shortage of the other, more selective, insecti- infested stands in eastern Canada.
cides. Further use of phosphamidon was Aerial application remained the main
discontinued in 1977 because of its negative method of control; insecticides were applied
impact on birds, even at low dosages. to reduce budworm populations, protect
Fenitrothion replaced DDT in 1969 and as of foliage and prevent tree mortality. Of the
2003 it is still registered for use in New 29.9 million ha of forest sprayed from 1944 to
Brunswick, although there is considerable 1973, 43.3% was treated with DDT, 55.5%
public pressure to ban its use entirely (J.C. with phosphamidon and fenitrothion, 1.2%
Cunningham, 1996, personal communica- with other chemicals and only about 0.04%
tion). It was considered relatively safe for with biological insecticides (Prebble, 1975;
fish and birds, but had caused some mortal- Armstrong and Cook, 1993). Realizing the
ity in aquatic insects and pollinators imme- undesirable side effects of the chemical
diately after spraying (Varty, 1978). insecticides, potentially less disruptive alter-
Trichlorfon was used in place of fenitrothion natives were identified (especially ento-
from 1973 to 1977 near cultivated blueber- mopathogens), and research was initiated.
ries to minimize adverse effects on pollina- During the major spruce budworm out-
tors and was used when non-spray buffer break of the 1970s–1980s in eastern Canada
zones were placed around blueberry fields, (Kettela, 1983), significant tree mortality was
precluding the use of trichlorfon. Acephate first observed in 1973, when approximately 1
was the ‘safest’ chemical insecticide devel- million ha of dead or dying timber was
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 218

218 I.S. Otvos

recorded. Tree mortality increased over the Use of Bacillus thuringiensis

years and, by 1987, heavy mortality had
occurred over approximately 18 million ha. Btk is effective against Lepidoptera
The outbreak peaked in 1975, when nearly 50 (Dulmage, 1982), the order to which most
million ha were infested in the eastern forest defoliators belong. Although Btk is
Canadian provinces, and close to 9 million commonly found in soil microbiota (Martin
ha were treated with phosphamidon and and Travers, 1989), it has never been
fenitrothion (Fig. 10.2; Nigam, 1980; Kettela, observed to control forest insect-pest popula-
1983). A total of 13 million kg of chemical tions in nature and must be applied as an
insecticides were used to protect trees on 50 insecticidal spray, sometimes more than
million ha, from 1965 to 1980, in eastern once, over the infested area. It is now widely
Canada (Nigam, 1980; Kettela, 1983). used to control several defoliating insects in
Between 1985 and 1990, approximately 2.8 Canada. Progress in the development of Btk
million ha were treated in eastern Canada to as an operational alternative to synthetic
control spruce budworm (Cunningham and chemical pesticides has been reviewed by
van Frankenhuyzen, 1991). Cunningham (1985b), van Frankenhuyzen
There were large areas defoliated between (1990) and Cunningham and van
1981 and 1990. The areas defoliated annually Frankenhuyzen (1991).
ranged between a low of about 20 million ha The first aerial-spray trials using Btk in
in 1986 to a high of about 55 million ha in Canada were against the western black-
1990 (Fig. 10.2). headed budworm, Acleris gloverana
A bilateral multi-year project on the (Walsingham), in British Columbia
spruce budworm was initiated between (Kinghorn et al., 1961) and spruce budworm
Canadian and American researchers in 1977 in New Brunswick (Mott et al., 1961). Most of
(CANUSA). The results of this project were the early research on Btk was conducted on
published in an even larger volume (Sanders spruce budworm in the 1970s, in an effort, in
et al., 1985) than that of R.F. Morris (1963). part, to replace chemical insecticides. These
However, even these additional research early tests gave variable efficacy and popula-
findings failed to provide the knowledge tion control. It took over 25 years from its
and recommendations needed to manage first experimental use in the early 1960s to
budworm outbreaks without aerial applica- reach large-scale operational use in the mid-
tion of insecticide to prevent budworm dam- 1980s (Fig. 10.3). The following were some of
age. Insecticide treatment remained the only the contributing factors that led to the accep-
effective tool to reduce larval populations, tance of Btk as a replacement for chemical
but the use of insecticide shifted away from insecticides in defoliator control.
broad-spectrum chemicals through the more Btk potency increased from 4 billion inter-
selective chemicals towards bioinsecticides. national units (BIU) per litre in the early
Attempts were made to develop viral 1970s to 16.9 BIU/l in the mid-1980s, by
insecticides. Entomopathogenic viruses had which time the dosage rate of 30 BIU/ha was
been isolated from field-collected budworm routinely applied in 2.4 l of undiluted prod-
larvae as early as 1958 (Bird, 1959). Extensive uct for the control of spruce budworm. The
laboratory and field trials were conducted cost of Btk decreased between 1981 and 1988
with NPVs and GVs to control both the (east- from 4.5 times to only 1.2 times more expen-
ern) spruce budworm and the western spruce sive than chemical insecticides. The cost of
budworm between 1974 and 1988. The field Btk was fairly constant at between 35 and
trials with these viruses were disappointing 40¢/BIU from 1986 to 1990 (Cunningham
(Cunningham, 1985a; Otvos et al., 1989; and van Frankenhuyzen, 1991). The higher-
Cunningham and Kaupp, 1995). potency Btk products (containing more BIU
Consequently, no further work was done per litre) permitted using lower volumes and
with the naturally occurring virus strains and had the added benefits of reducing trans-
forest managers were left with the only other portation costs and increasing spray-plane
microbial agent under investigation, Btk. productivity. At the same time, Btk products
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 219

IPM in Forestry 219

were providing increased efficacy and relia- acquire a lethal dose (van Frankenhuyzen,
bility of control operations (van 1995). The effectiveness of Btk is questionable
Frankenhuyzen, 1990) and foliage protection against high densities of spruce budworm
of the treated trees. Btk was finally consid- (more than 25 larvae per branch sample).
ered a viable alternative to chemical insecti- Although Btk affects only larval stages of
cides for use against spruce budworm by Lepidoptera, some criticism has been raised
1981 (Smirnoff and Morris, 1984) and several because of its potential impact on non-target
other major forest defoliators a few years beneficial or desirable Lepidoptera. Non-
later (van Frankenhuyzen, 1990). These target Lepidoptera may be important in the
improvements, together with the political food-chain of some insectivorous birds, or
decision not to use chemical insecticides, as a they may be rare or endangered species.
result of public pressure and environmental The effect of Btk on non-target
concerns, led to favouring the use of biologi- Lepidoptera has been investigated by several
cals, resulting in the widespread acceptance authors, including Miller (1990). Studies
of Btk as a fully operational control option have shown that both numbers of non-target
for forest defoliators. insects and species richness were depressed
Btk is considered environmentally benign for 2–3 years following treatments. However,
(Otvos and Vanderveen, 1993) and is the all but the rare species recolonized the
only registered and commercially available treated areas within 2–4 years after treatment
microbial agent in Canada for forest insect (Miller, 1990). This was confirmed by
control. By 1993 there were 18 Btk products Boulton et al. (2002), who found a signifi-
registered for use in insect control in Canada cantly lower abundance of non-target
(Otvos and Vanderveen, 1993). Although Lepidoptera on plants that received an oper-
three viruses are also registered for forest ational Btk spray (30 BIU/ha) in a plot
insect control, they are not available com- treated against western spruce budworm,
mercially. The operational use of Btk for con- than on plants that were covered and
trol of spruce budworms increased from excluded Btk. The two most common insect
about 2% of the total area treated in 19801 to species on the shrubs made a full recovery
20 in 1984, 63 in 1990 and nearly 100% by within 2 years of the Btk spray. However,
1996 (Cunningham and van Frankenhuyzen, sparsely distributed species declined on both
1991; van Frankenhuyzen, 1993; Fig. 10.3). In the treated and covered plants, suggesting a
most of Canada, Btk is now the only insecti- general decline of Lepidoptera species inde-
cide used for budworm control, apart from a pendent of the spray. A different experimen-
recently registered biorational (Mimic). Only tal study, where double the regular registered
New Brunswick continues to use both chem- dose was used (60 BIU/ha), yielded similar
ical (fenitrothion) and Btk products results. Some species made a full recovery by
(Cunningham and van Frankenhuyzen, the end of the second year, but this could not
1991). By far the greatest use of Btk in be demonstrated for the sparsely distributed
Canada is for spruce budworm control, with species (Boulton, 1999; T.J. Boulton and I.S.
2.8 million ha treated between 1985 and 1990 Otvos, unpublished data).
(Cunningham and van Frankenhuyzen, The effects of Btk treatment on non-target
1991). Similar increases in the use of Btk have Lepidoptera may only be a concern when
occurred in the USA and Europe (van endangered insect species are in the spray
Frankenhuyzen, 2000). area. However, the relative ‘value’ of the
endangered species should be compared
with the potential damage the target species
Potential and constraints
will cause if no treatment takes place.
The use of Btk is not without problems. The timing of Btk treatment not only is
Depending on weather conditions in the important in terms of efficacy, but may also
field, Btk in spray droplets is considered to be a factor in preventing deleterious effects
be effective for only 3–5 days following on natural enemies. Conflicting data on the
application, after which the larvae may not effects of Btk treatments on the natural
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220 I.S. Otvos

enemies of eastern and western spruce bud- Two morphotypes of the virus have been
worm have been published. Most reports isolated from DFTM larvae and identified as
indicated no deleterious effects (Buckner et the cause of these epizootics (Hughes and
al., 1974; Reardon et al., 1982; Morris, 1983; Addison, 1970). One morphotype exhibits
Niwa et al., 1987). Otvos and Raske (1980a,b) singly occluded virus particles (OpSNPV) in
reported an apparent increase in per cent the PIB. The second has multiple viral parti-
parasitism by the two most common and cles embedded in bundles within the PIB
important budworm parasitoids, i.e. (OpMNPV) (Hughes and Addison, 1970). The
Apanteles fumiferanae Viereck and Glypta majority of the research has been conducted
fumiferanae (Viereck), while Hamel (1977) on the multiple-embedded virus. The use of
reported a negative impact. Nealis and van virus to control DFTM was considered in
Frankenhuyzen (1990) indirectly confirmed British Columbia as early as 1962, when the
the findings reported by Otvos and Raske first field trial was conducted on individual
(1980a,b) and recommended applying Btk at trees (Morris, O.N., 1963). The first aerial spray
the peak of the fourth-instar stage to increase trials using OpNPV against DFTM in British
efficacy against the spruce budworm and to Columbia were conducted jointly by person-
minimize or prevent negative effects on nel of the Canadian Forest Service, the US
these two important budworm parasitoids. Department of Agriculture (USDA) Forest
The evolution of the currently used man- Service and the British Columbia Ministry of
agement method to minimize spruce bud- Forests from 1974 to 1976 (Ilnytzky et al., 1977;
worm damage is typical of most defoliator Stelzer et al., 1977; Cunningham and
control, and is probably representative of the Shepherd, 1984). Field treatments in 1975
general approach worldwide. At first, dam- using the laboratory-produced, naturally
age caused by the insect is not considered occurring virus caused high infection and high
economically important until the affected larval mortality, but the treated stands still
resource is desired by society. Then the most sustained considerable damage because the
efficacious control method is used – usually virus was applied late in the declining phase
chemical insecticide with broad-spectrum of the outbreak. Therefore, the effect of the
effects. As non-target effects become known, virus application on the course of the outbreak
alternative control methods are developed. could not be evaluated. However, the experi-
Sometimes these have minimal side effects on ment has shown that the laboratory-produced
the environment. The use of introduced and virus behaves like the naturally occurring one
natural enemies, such as parasitoids and and can be used to cause an epizootic in the
pathogens, can also have some effects, even if field. Based on these results and safety testing
only on the biodiversity of the region. When of OpMNPV conducted in the USA, the USDA
our food and shelter are secured, segments of Forest Service registered the viral insecticide
the population become socially conscientious as TM-Biocontrol-1® in 1976.
and concerned about biodiversity. It is ironic, The experiment conducted in 1975 raised
however, that, in the same population seg- the following questions:
ments, some people still insist on buying
● Can the virus be introduced into the pop-
unblemished fruits and vegetables produced
ulation at the beginning of the outbreak,
by repeated use of chemical insecticides.
and will it cause an epizootic?
● Will such an epizootic reduce damage
normally associated with a DFTM out-
Integrated Pest Management of Douglas
break?
Fir Tussock Moth: a Case Study
● Can the virus dose be reduced to lower
the cost of application?
The management system developed for the
● Can DFTM populations be monitored to
DFTM, integrating a pheromone-detection
predict future outbreaks?
system with early application of the natu-
rally occurring, laboratory-produced virus, To introduce the virus at the beginning of an
illustrates a true IPM system. outbreak requires a reliable monitoring sys-
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IPM in Forestry 221

tem. It was necessary to determine where examined to select the most appropriate for
and when outbreaks were likely to occur. In the situation. These options include protect-
a separate study, concurrent with the virus ing infested stands by virus or insecticide
work, a dependable and sensitive application or doing nothing and letting the
pheromone monitoring system was devel- outbreak run its course. A stepwise selection
oped for early warning of impending out- process for control actions is provided as a
breaks (Shepherd et al., 1985). guideline (Shepherd and Otvos, 1986). The
use of a registered chemical insecticide with
a fast knock-down power may be considered
Monitoring with pheromone traps appropriate in high-use recreational areas,
such as parks, because the hairs of the cater-
Pheromone-baited traps were placed in sus- pillars and those on the egg masses may
ceptible stands, which were defined by over- cause a severe allergic reaction called ‘tus-
laying maps of previous outbreaks, forest sockosis’ in some sensitive people (Perlman
types and biogeoclimatic zones. The most et al., 1976).
susceptible stands, revealed by the overlays,
tended to be located in the driest part of the
range of Douglas fir, where it mixes with First experiment – 1981
ponderosa pine, Pinus ponderosa P. Laws. ex
C. Laws. Within this forest habitat, perma- A developing DFTM outbreak in south-
nent monitoring stations were established central British Columbia was discovered in
and pheromone-baited traps were operated 1980 before any defoliation occurred. This
annually to monitor changes in male moth allowed an experiment in 1981 to determine
density over the course of an outbreak cycle if a viral epizootic could be initiated at an
to reveal patterns (Shepherd et al., 1985; early phase of the outbreak, before it would
Shepherd and Otvos, 1986). occur naturally, by ground and aerial appli-
Population trends in pheromone-baited cation of the virus, and whether the applica-
traps were followed from endemic to epi- tion would reduce damage (Shepherd et al.,
demic levels during the course of one out- 1984b). Although a natural epizootic also
break. The number of successive years of occurred in the control plots containing high
upward trends of male moths caught was and moderate DFTM populations, the inci-
used to predict outbreak development. Three dence of viral infection in the treated plots
consecutive years in which the number of was considerably earlier and much higher,
male moths caught increased and exceeded indicating the beneficial effects of the viral
25 moths per trap indicated that an outbreak spray. Even at low population density, treat-
was expected within the next 1 or 2 years ment effects were excellent, and a natural
(Shepherd et al., 1985). The pheromone-trap epizootic in the control plot occurred much
system only gives advance warning that an later. The results showed that the virus can
outbreak is imminent and signals that be introduced into DFTM populations at an
another, more precise sampling system early phase of the outbreak and that a viral
should be deployed in the area. Thus, after 2 epizootic can be initiated in first- and
years of upward trends, additional networks second-instar larvae by both aerial and
of traps are placed around the indicator sta- ground treatment (Shepherd et al., 1984b).
tions to locate the foci of the developing out- The aerially applied virus caused an epi-
break and refine prediction. An egg-mass zootic among DFTM larvae at low (41
survey is then initiated during the autumn larvae/m2), medium (97 larvae/m2) and
or winter to determine the insect density at high (206 larvae/m2) population densities.
the centre of the developing infestation and Laboratory rearing of larvae collected from
to predict the level of potential damage the the field and weekly microscopic examina-
following year (Shepherd et al., 1984a). If egg tion of the dead larvae indicated that a sec-
masses are present, all available options for ond wave of epizootic occurred among the
managing the insect problem should be survivors.
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222 I.S. Otvos

Table 10.4. Douglas fir tussock moth larval and tree mortality in virusa-treated and untreated plots,
Veasy Lake, British Columbia, 1982 (from Otvos et al., 1995).

% Population % Sample trees

reduction killed by DFTM
Treatmentb 1982 pre-spray 6 weeks post-
Plot (PIB/ha in 9.4 l/ha) larvae/m2 sprayc 1983 1984

T1 1.6 × 1010 Oil 182.8 64.7 0 0

T2 8.3 × 1010 Oil 145.8 90.6 2 7
T3 2.5 × 1011 Oil 302.0 95.1 0 4
T4 2.5 × 1011 Molasses 41.8 86.6 0 0
χ = 0.6 χ = 2.8

C1 Control 197.5 53 60
C2 Control 136.9 –d –d
C3 Control 360.6 60 62
C4 Control 81.2 0 0
χ = 37.8 χ = 40.7
a The virus used was OpMNPV produced in white-marked tussock moth (Virtuss®).
b PIB, polyhedral inclusion bodies; Oil, oil-based formulation containing 25% blank oil carrier and 75%
water; Molasses, molasses formulation containing 25% commercial-grade molasses and 75% water.
c Per cent reduction was calculated by the modified Abbott’s formula (Fleming and Retnakaran, 1985).
d Trees in part of the plot were cut down during power-line construction.

Second experiment – 1982 disease was temperature-dependent and the

spread of the disease was influenced by host
In a separate experiment the following year, density. NPV infection was not detected in
water and oil based formulations, and the untreated control plots until 5 weeks
reduced dosages2 of the virus were com- after spraying and at a much lower level
pared to determine the most effective dose than in the treated plots.
and formulation and to investigate if the rec- Virus application has additional benefits
ommended application rate of 2.5 × 1011 besides direct larval mortality. Among the
PIB/ha could be reduced and still prevent surviving larvae, sublethal effects of virus
damage (Table 10.4). The initial impact of the application included higher pupal mortality,
1982 applications was that by 2 weeks post- lower per cent adult emergence and a shift in
spray 10–30% of larvae had become infected. sex ratio. More males (about twice as many)
These infected larvae died, liberated poly- than females emerged in the treated plots,
hedra on to the foliage and increased the while the sex ratio of the adults was close to
amount of inoculum. A secondary wave of 1:1 in the control plots (Otvos et al., 1987).
virus infection then developed among the This alteration of the sex ratio is probably
surviving larvae (DFTM larvae have a long due to the fact that female DFTM have one
feeding period) and by 6 weeks after spray- more larval instar than males, are exposed to
ing the population had collapsed. Per cent the virus longer and consequently suffer
infection, development of the epizootic higher mortality. This change in sex ratio
among the larvae and larval mortality, cor- among the survivors of virus treatment has
rected for natural mortality, in the treated been frequently reported in other insects,
plots were related to dosage and the second including the spruce budworm (Duan and
lowest dose of 8.3 × 1010 PIB/ha gave similar Otvos, 2001).
results (about 91% mortality) to the full dose These results indicated that it is possible
of 2.5 × 1011 PIB/ha (95% mortality). Virus to control DFTM populations with OpMNPV
transmission was higher in plots with higher at about one-third of the registered label
larval densities. Development of the viral dose (at least at 8.3 × 1010 PIB/ha) and poten-
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IPM in Forestry 223

tially even lower dosages at an early stage of Steps of the DFTM management system
an outbreak. Treatment at this lower dosage
also prevented significant tree mortality in ● Identify stands susceptible to DFTM
the treated stands (Table 10.4). attack based on overlaying defoliation
maps of past outbreaks, forest types and
biogeoclimatic zones.
Summary and benefits of the system ● Within susceptible stands, establish per-
manent monitoring stations representing
The results of the experiments with the range of past DFTM outbreaks.
pheromone traps and OpMNPV application ● Set up pheromone traps at these locations
over the past 20 years have proved that and monitor male moth catches annually
DFTM outbreaks can be prevented by a sin- for one outbreak cycle to determine the
gle application of virus at the beginning threshold of male moth catches that indi-
phase of an outbreak. Foliage protection may cates impending outbreaks.
be negligible in the year of application, but ● Deploy additional auxiliary pheromone
acceptable in the following years. Tree mor- traps to help to locate infested stands
tality can be prevented when the treatment is when male moth catches reach threshold
applied early in the outbreak cycle and to numbers.
early-instar larvae. The management system ● Search for egg masses near permanent or
developed for DFTM was successfully tested auxiliary pheromone traps when moth
during the 1990–1993 outbreak, and tree catches reach threshold numbers.
mortality was minimal in the stands treated ● When egg masses are found, consider all
with OpMNPV because early infection pre- available options to manage DFTM popu-
vented the development of full-blown out- lations and select the most appropriate
breaks in the treated stands. The one for the area.
operationally proved management system ● Implement the action chosen.
was accepted by the British Columbia
Ministry of Forests, became part of the Forest
Practices Code in the province and is used to Development of IPM for the Introduced
manage DFTM populations. Gypsy Moth in North America
The pest-management system for the
DFTM (Shepherd and Otvos, 1986) enables The gypsy moth, Lymantria dispar (Linnaeus),
forest managers to predict when and where presents a unique example of the progres-
outbreaks are likely to occur so that control sion of forest insect-pest control in North
measures can be planned and implemented America. Probably more research has been
to minimize or prevent damage. It is hoped done on the gypsy moth in North America,
that the DFTM pest-management system since its introduction c. 130 years ago, than
described above will serve as a prototype for on any other forest insect pest, either native
the development of pest-management sys- or introduced. In spite of all of this research,
tems for other defoliating forest pests else- the gypsy moth continues to spread.
where. Work is underway to develop a Hopefully, though, some important lessons
similar management system for other defo- have been learnt.
liators in British Columbia and other parts of The gypsy moth is a polyphagous
Canada. When using such a system, one may Eurasian forest defoliator that is known to
not always be able to use naturally occurring feed on over 300 species of trees and shrubs,
biological control agents to reduce damage; with oaks as the most favoured hosts
however, it should be possible to identify (Leonard, 1981). Two strains of L. dispar are
stands susceptible to attack by various defo- commonly recognized, one from Europe and
liators and this in itself will be useful to for- the other from Asia. In Europe, the gypsy
est managers. The steps of the DFTM moth feeds mainly on deciduous trees, but in
management system are provided below for Asia it also feeds on conifers, primarily larch.
possible adaptation and use for other insects. The females of the European strain, although
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 224

224 I.S. Otvos

British Nfld
Columbia Alberta

Sask.
Man. Quebec NS
NB
Ontario

Point of introduction in Massachusetts c. 1869

Area regulated for established populations (2000)
Recent infestations in western North America

Fig. 10.4. Current extent of infestation and recent introductions of gypsy moth into North America (after
Nealis, 2002). Sask., Saskatchewan; Man., Manitoba; Nfld, Newfoundland; NB, New Brunswick; NS, Nova
Scotia.

winged, cannot fly, while females of the al., 1989). Leopold Trouvelot, a naturalist,
Asian variety can fly (Baranchikov, 1989; intentionally brought the insect from France
Wallner, 1989). This makes the latter a poten- to North America and the insect escaped
tially more destructive strain than the from his laboratory during a storm.
European variety if introduced into Canada Although he reported the incident immedi-
(where most of the trees are conifers), in ately, nothing was done at the time. The
terms of both its potential faster rate of gypsy-moth infestation increased in extent
spread and greater potential damage to the and defoliation began to appear about 10
forests of Canada. These two strains of gypsy years after the initial escape. The spread of
moth hybridize in the laboratory (Keena et the gypsy moth since that time is well docu-
al., 1995) and in the field (Prasher and mented (McManus and McIntyre, 1981;
Mastro, 1995), and both sexes of the Montgomery and Wallner, 1988). An eradica-
hybridized offspring (F1 and F2) can fly tion programme was started in 1889 and
(Keena et al., 1995). appeared to be working, reducing the infes-
tation to such a degree that in 1900 the eradi-
cation programme was stopped by the state
The European strain of gypsy moth in eastern of Massachusetts (McFadden and McManus,
North America 1991). This was a fatal mistake, with serious
unforeseen consequences. Within 5 years of
The European strain was introduced under stopping the eradication programme, gypsy-
unusual circumstances at Bedford, near moth infestations increased drastically and
Boston, Massachusetts, USA, in 1869 new infestations were discovered in three
(McManus and McIntyre, 1981; Liebhold et adjacent states (McManus and McIntyre,
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 225

IPM in Forestry 225

1981), by which time the European strain of important in the spread of the gypsy moth
gypsy moth was well established in eastern than natural spread. For example, in 1983,
North America (Fig. 10.4). A prompter ten gypsy-moth infestations were found in
response and eradication programme against California about 3200 km from the infesta-
this quarantine threat might have prevented tion in the east, despite aggressive quaran-
the vast harm resulting from this incidence tine inspection at the California State border.
of pest introduction (Dunlap, 1980). In 1983, these infestations were treated with
The gypsy moth spread west between chemical insecticides to eradicate them at an
1906 and 1920, at an estimated rate of 9.6 estimated cost of US$1.5 million (McFadden
km/year. In an effort to halt the spread of and McManus, 1991).
the gypsy moth and the subsequent damage
to plants, the Domestic Plants Quarantine
Act was created in 1912 in the USA (and in Chemical control
1924 in Canada) to regulate the movement of
plant material from gypsy-moth-infested At first, the broad-spectrum insecticides
areas. A barrier zone was established in 1923, Paris green, lead arsenate and DDT were
from the Canadian border (Quebec) south used in both eradication and suppression
along the Hudson River Valley to Long projects. Of the chemical insecticides used,
Island (New York), to prevent the westward DDT was considered so effective that,
spread of the gypsy moth. Infestations inside between 1949 and 1959, 3.7 million ha of
and west of this barrier zone were to be gypsy-moth-infested stands were treated
eradicated, while infestations to the east (Liebhold and McManus, 1999). However,
were to be controlled or managed by sup- the environmental damage caused by the
pression, using various means (McFadden extensive use of DDT against the gypsy
and McManus, 1991). Eradication pro- moth was cited as a specific example of
grammes were designed to eliminate iso- unacceptable chemical pollution in Rachel
lated populations of the gypsy moth, while Carson’s book Silent Spring (1962). Even
suppression programmes were designed to though only about 50 ha of defoliation was
protect foliage and/or reduce larval popula- noted, the eradication was discontinued in
tions and slow the spread. The barrier zone 1958 because of concerns about the environ-
became infested in 1939, and eradication mental persistence of DDT. ‘Hopes of eradi-
attempts were terminated in 1941. However, cating the gypsy moth were abandoned [in
the barrier zone was reinstituted in 1953 1958] and long overdue emphasis was
after the gypsy-moth populations exploded placed on research’ (McFadden and
in 1951/52. McManus, 1991). In 1959, carbaryl (Sevin®)
The European gypsy moth can spread in replaced DDT for use in suppression pro-
two ways: natural dispersal or accidental grammes. Over time, the control products
transport of pupae or egg masses by selected and used in suppression projects
humans. Natural dispersal occurs over only evolved from broad-spectrum insecticides,
short ranges when first- or second-instar lar- such as carbaryl (Sevin®), trichlorfon
vae are transported by wind as female (Dylox®), acephate (Orthene®) and difluben-
moths cannot fly (Mason and McManus, zuron (Dimilin®) to the much more selective
1981; Elkinton and Liebhold, 1990; and environmentally more acceptable bio-
McFadden and McManus, 1991). This logical insecticides, such as Btk and virus, as
spread of first and second instar larvae by well as the use of pheromones in the 1980s
natural dispersal was estimated to be about (Liebhold and McManus, 1999). This gradual
2 km/year (Liebhold et al., 1992). change in use pattern of controlling/sup-
Inadvertent transport of cocoons and/or egg pressing the gypsy-moth populations in the
masses from infested areas to uninfested eastern USA is illustrated in Fig. 10.5A. The
areas by humans (through vacationing, use of Btk, virus and sex pheromones will
moving and transporting goods) can be over be discussed separately under biological
much larger distances and is much more control.
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 226

226 I.S. Otvos

700 Dimilin
A
Sevin
600 Dylox
Gypchek/disparvirus
500 Bacillus thuringiensis
Area treated (’000 ha)

400

300

200

100

00
85

95
75

80

90
70

20
19

19
19

19

19
19

Year

2500
B
,2 4
40 ,09
14 49
12 75
33 51
36 56
77
,1
,9
,9
,5
3
10

Dimilin
2000
Sevin
Gypchek/Disparvirus
Area treated (ha)

Bacillus thuringiensis
1500

1000

500

0
80

85
75

95

00
90
19

19
19

19

20
19

Year

Fig. 10.5. Total area treated with insecticides during suppression and eradication programmes to control the
gypsy moth (A) in the USA, 1970–2002, (from http://fhpr8.srs.fs.fed.us/wv/gmdigest, 2003); (B) in Canada,
1975–2000 (from Armstrong and Cook, 1993; Mason and Huber, 2002).
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IPM in Forestry 227

Biological control considerable work has been done on the use

of pathogens for gypsy-moth control. The
Natural enemies
pathogens investigated include Bacillus
Classical biological control (the introduction thuringiensis (Dubois, 1981), an NPV (Lewis,
of natural enemies to control recently intro- 1981) and a fungus (Entomophaga maimaiga)
duced pests), started in 1905, was the first (Hajek et al., 1990a; Elkinton et al., 1991;
line of defence. Importation of exotic para- Hajek, 1997).
sitoids and predators for gypsy-moth control Research into the use of Btk for the sup-
was one of the largest programmes in the pression of gypsy moth began in earnest in
history of biological control (Brown, 1961). the early 1960s (Cantwell et al., 1961) and, by
About 150 species of parasitoids have been the 1980s, it was accepted as an effective
reared from the gypsy moth throughout its alternative to chemical insecticide for gypsy-
distribution in Eurasia (Doane and moth control (Dubois, 1981). Btk use began in
McManus, 1981). Over the years, about 60 of 1980 and increased gradually, reaching a
these natural enemies, mainly from Europe, peak in 1985 when about 481,900 ha were
Asia and Japan (obtained from high and treated with Btk (Fig. 10.5A).
moderately high gypsy-moth populations), According to Campbell and Podgwaite
were introduced into the USA. (1971), the gypsy-moth NPV (LdNPV) was
Early attempts at parasitoid introductions probably introduced inadvertently with the
(1905–1914 and 1922–1933) were successful, gypsy moth or with one of its parasitoids
but later introductions (1960–1977) failed (Glaser, 1915). It was considered to be the
(Reardon, 1981). By 1933, 44 species of para- most important natural control agent of the
sitoids and nine species of predators had gypsy moth until 1980 (Campbell, 1963;
been introduced and, of these, 13 parasitoids Doane, 1970, 1976; Podgwaite and Campbell,
and one predator became established 1972). The development of LdNPV as a
(Dowden, 1962). Most researchers agree that biopesticide began shortly after its effective-
classical biological control did not prevent ness in reducing larval populations was real-
the spread of the gypsy moth, but it very ized. Considerable research into strain
probably contributed to the collapse of some selection, production, and laboratory and
outbreaks and possibly slowed the spread. field testing (Lewis, 1981) and other factors
The introduced parasitoids may have also (see section 6.3 of the gypsy-moth com-
kept the populations at endemic levels after pendium, edited by Doane and McManus
the collapse of an outbreak (Ticehurst et al., (1981)) preceded registration of the gypsy-
1978). Augmentative releases of some of the moth NPV in 1978 as Gypchek for gypsy-
established parasitoids resulted in increased moth control (Lewis, 1981).
parasitism in the release areas (treatment) Unfortunately, commercial production of
compared with the controls in three different Gypchek did not follow registration. Its
studies (Weseloh and Anderson, 1975; Hoy, greatest attribute, high host specificity, is also
1976; Blumenthal et al., 1978). However, the its greatest shortfall, as it makes it economi-
augmentative parasitoid releases did not cally unattractive for private companies to
appear to significantly reduce gypsy moth produce and sell it. Large companies are
egg-mass density (a measure of success) after only interested in developing products that
the releases. generate US$40–50 million in sales per year
(Podgwaite, 1999), while the market for
Gypchek is only about US$5 million per
Pathogens
year. To date, every company that tried to
During the late 1950s and early 1960s, in produce Gypchek commercially has failed
response to public concern over the use of economically (Podgwaite, 1999).
chemical insecticides, efforts were intensified Consequently, the US Forest Service (USFS)
to develop environmentally acceptable con- continues to produce Gypchek and make it
trol alternatives. Entomopathogenic micro- available on a limited basis through coopera-
organisms offered such alternatives and tive suppression programmes (Podgwaite,
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228 I.S. Otvos

1999). Since the registration of Gypchek in 1910–1911’ (Andreadis and Weseloh, 1990:
1978, only about 20,200 ha have been treated 2461).
with it in the USA. This represents less than Before the discovery of E. maimaiga in
1% of the total area treated for gypsy-moth North America in 1989, NPV was generally
control (Podgwaite, 1999; Fig. 10.5A). credited with causing the collapse of gypsy-
There is some confusion about the origin moth outbreaks (Hajek et al., 1996). LdNPV
of the gypsy-moth fungus that causes epi- epizootics generally occur at high host den-
zootics in North America (Hajek et al., 1995). sities in dry years, when rainfall is low
A fungal pathogen of the gypsy moth was (Elkinton et al., 1991), while E. maimaiga can
introduced from Japan (where it causes cause high levels of infection across a wide
extensive epizootics) into the USA on two range of host densities (Hajek et al., 1996).
separate occasions. The early introductions Since 1989, E. maimaiga epizootics have been
and releases were in 1910 and 1911 (Speare shown to decimate gypsy-moth populations
and Colley, 1912) and then later in 1985 and at both low and high host densities in years
1986 via infected larvae (Hajek et al., 1995). with higher than normal precipitation
No evidence was found indicating establish- (Elkinton et al., 1991; Hajek and Roberts,
ment of the fungus from either of these 1991; Smitley et al., 1995) and even when
releases within a few years following intro- NPV is present (Smitley et al., 1995). Several
duction (Hajek et al., 1995). After its second authors have noted a positive correlation
release, the fungus introduced from Japan between the intensity of the epizootic and
was described as a new species, E. maimaiga rainfall (Andreadis and Weseloh, 1990;
Humber, Shimazu & Soper (Soper et al., Elkinton et al., 1991; Hajek et al., 1993;
1988). An epizootic of this fungus was dis- D’Amico and Elkinton, 1995). This is not
covered in 1989 (Andreadis and Weseloh, surprising, since E. maimaiga-killed larvae
1990) and surveys in the same year showed discharge conidia in the presence of dew or
the fungus occurring in seven states and in when relative humidity is greater than 90%
virtually all samples collected from areas (Hajek et al., 1990b; Hajek and Soper, 1992).
that were infested by the gypsy moth prior In dry weather, fungal-killed gypsy moth
to 1980 (Hajek et al., 1990a). More intensive have the same appearance as NPV-killed
surveys in the following year showed that E. larvae (Hajek and Roberts, 1992). This holds
maimaiga occurs in ten states in the north- true for other insects and Entomophthorales
eastern USA (Elkinton et al., 1991) and in fungi (I.S. Otvos, personal observation). For
Ontario (Welton, 1991; Nealis et al., 1999), example, epizootics in the eastern hemlock
where the fungus must have spread on its looper, Lambdina fiscellaria fiscellaria
own as no intentional introduction of the (Guenee), in Newfoundland were attributed
fungus has occurred there. Large-scale epi- to an undetermined wilt (viral) disease for
zootics caused by E. maimaiga were wide- over 20 years. The true cause of the epi-
spread in areas colonized by the gypsy moth zootics, infection by two fungal pathogens,
prior to 1980 (Elkinton et al., 1991), but not in was only determined in 1969 (Otvos, 1973;
areas invaded more recently (Hajek et al., Otvos et al., 1973). The absence of external
1996). The wide geographical distribution of fruiting bodies on the insect cadavers
the fungal epizootic suggests that the fungus makes distinguishing between mortality
probably became established in the New caused by these pathogens in dry weather
England states from the first intentional in the field difficult. Given this information,
releases of E. maimaiga near Boston in 1910 it is not hard to imagine that earlier identifi-
and 1911 (Andreadis and Weseloh, 1990; cations of viral infection in the field would
Hajek et al., 1990a; Elkinton et al., 1991). The have also included some fungal-infected
first authors to report on the 1989 discovery insects.
of the E. maimaiga epizootic summarized it The fungus has spread dramatically
the best by saying, ‘the current epizootic between 1989 and 1992 and is prevalent in
may have resulted from the survival and areas not recently colonized by the gypsy
inapparent spread of an early introduction in moth (it does not occur in recently colonized
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IPM in Forestry 229

infestations), causing up to 100% mortality of the host at about the same time, because the
late-instar gypsy-moth larvae (Reardon and fungal infection develops faster.
Hajek, 1993). The fungus is considered by
some to be a more important pathogen than
Sex pheromones
NPV (Hajek, 1997). Consequently, it has been
intentionally ‘spread’ or introduced, espe- Disparlure is used in pheromone traps to
cially to areas newly invaded by the gypsy monitor (survey and detect) gypsy-moth
moth (Hajek et al., 1996; Smitley et al., 1995). populations (Cameron, 1974; Schwalbe,
E. maimaiga resting spores can be translo- 1981) and to suppress populations through
cated or even introduced into new fungus- mating disruption (Beroza et al., 1975;
free areas and along the leading edge of the Reardon et al., 1998). Decrease in mating suc-
spreading gypsy-moth infestation by the cess was found to be inversely dependent on
purposeful introduction of resting spores the density of the moths and directly related
(Smitley et al., 1995; Hajek et al., 1996) by to the amount of disparlure used. Greater
moving soil with resting spores from areas mating disruption occurred in lower-density
where fungal epizootics have recently gypsy-moth populations than in higher den-
occurred. However, care must be taken to sity populations. Because of the cost of dis-
ensure that pathogens, such as Armillaria parlure production, gypsy-moth population
mellea rhizomorphs, are not spread uninten- suppression by mating disruption is only
tionally as well (Reardon and Hajek, 1993). practised when low doses are used against
‘E. maimaiga is now a dominant natural low-density insect populations (Webb et al.,
enemy associated with gypsy moth in North 1990). A double application of 75 g dispar-
America’ (Hajek, 1997: 67) and might be con- lure/ha in 1 year delayed population
sidered more important than NPV in moister increase by 1 to 4 years. In low-density pop-
environments. The fungus might be an excel- ulations, mating disruption with aerially
lent candidate for introduction around lakes, applied disparlure (at 75 g/ha)4 is an effec-
on islands and on the west coast of North tive control of gypsy-moth populations
America should the gypsy moth become (Leonhardt et al., 1996), reducing mating and
established in that region. the number of fertile egg masses laid by
70–85% (Webb et al., 1990). Work is continu-
ing to evaluate the efficacy of lower dosages
Combinations of biological control agents of disparlure to achieve mating disruption,
making it more cost effective (Reardon et al.,
In order to increase their control impact, 1998).
some biological control agents have been
used in combination, such as parasitoids and
pathogens. The parasitoid Apanteles Use of the barrier concept in gypsy-moth
melanoscelus (Ratzeburg) was used in combi- management
nation with Btk, and their combined use
resulted in higher population reduction and Between 1920 and the 1950s, several large-
foliage protection than when each was used scale ‘barrier’ programmes were imple-
alone (Reardon, 1981). Studies have also mented to prevent the westward expansion
shown that parasitoids contaminated with of the gypsy moth (McManus and McIntyre,
NPV in the laboratory can transmit the virus 1981; McFadden and McManus, 1991; Sharov
to the gypsy moth, both in the laboratory et al., 1998). Until the early 1980s, the main
and in the field (Reardon, 1981). goal of the barrier-zone management con-
Dual or mixed infection by LdNPV and E. cept was eradication of infestations outside
maimaiga has been reported from the gypsy the barrier zone and suppression of the mod-
moth (Hajek and Roberts, 1991; Weseloh and erate- and high-density populations inside
Andreadis, 1992; Malakar et al., 1999). the barrier zone by various means (Sharov et
Generally, E. maimaiga out-competes LdNPV al., 1998; Liebhold and McManus, 1999). The
when both the fungus and the virus infect largest outbreak on record occurred in 1981
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230 I.S. Otvos

when 5.2 million ha were defoliated by the and management costs compared with
gypsy moth, of which 150,000 ha were AIPM, over large geographical areas
treated mostly with Dylox® (58.4%) and (Leonard and Sharov, 1995; Sharov and
Sevin® (32.2%). The second largest outbreak Liebhold, 1998a). Extensive monitoring of
was in 1990, when 2.9 million ha were defoli- low-level gypsy-moth populations was con-
ated and more than 660,000 ha of gypsy- ducted with pheromone traps. Isolated pop-
moth-infested stands were treated with Btk ulations, well in advance of the infestation
(59.0%) and Dimilin® (40.8%) (Fig. 10.5A). front (100–150 km), were suppressed or
The barrier zone management concept was preferably eradicated. Btk, Gypchek and
abandoned when the USFS embraced the Dimilin® were used to eradicate or suppress
IPM concept and different alternative gypsy moth in high-density populations and
approaches were tried (Reardon, 1991) to Gyplure (mating disruption) to manage low-
prevent gypsy-moth populations from density populations (Leonard and Sharov,
expanding. These alternative approaches 1995; R.C. Reardon, March 2003, personal
were tested in two pilot projects. communication).
The first alternative approach, tried in a The effectiveness of the treatments
pilot project (Maryland IPM 1983–1987) to applied during the STS gypsy-moth project
manage low to moderate populations of conducted by the USDA Forest Service (on
gypsy moth using IPM, involved annual sur- 188,064 ha) were analysed and compared
veillance of insect densities using (Sharov et al., 2002b). Disparlure treatment
pheromone traps to determine gypsy-moth (93 blocks) was significantly more effective
distribution and density to maximize natural against isolated low-density populations of
control and the use of direct control mea- gypsy moth than Btk treatments (173 blocks).
sures when necessary in an environmentally A large-scale evaluation of operational dis-
acceptable way (Reardon et al., 1987). parlure treatment of gypsy-moth popula-
This approach was later modified in a sec- tions has shown that this method is effective
ond pilot project over a much larger area in isolated, well-defined, low-density infesta-
(Reardon, 1991). The Appalachian Integrated tions, but does not appreciably disrupt mat-
Pest Management Gypsy Moth Project ing in high-density populations (Sharov et
(AIPM 1987–1992) was designed ‘to demon- al., 2002b). The development of mating dis-
strate the effectiveness of new and existing ruption has become the key element to the
management technology in an IPM approach success of the STS programme (Sharov et al.,
to minimize the spread and adverse effect of 2002a). Analysis of gypsy-moth spread data
the gypsy moth’ (Reardon, 1991: 108). In the has also shown that the STS programme has
first phase of this second project, three prod- reduced the spread of this insect by more
ucts (Btk, Gypchek and disparlure) were than 50% (Sharov et al., 2002a).
tested on a small scale before applying them In the past, the tendency was to eradicate
operationally (Reardon, 1991). During this isolated infestations as soon as they were
project, areas with high gypsy-moth density detected. However, analysis of the treat-
were treated with Btk, Dimilin®4 and virus. ments of gypsy-moth populations during the
Areas with low-density gypsy moth were STS programme, from 1993 to 2001, sug-
treated with synthetic flakes impregnated gested that it is better to postpone treatment
with sex pheromones (disparlure) to reduce until the gypsy-moth population is well
the number of fertile egg masses through delineated with a dense grid of pheromone
mating disruption. traps (Sharov et al., 2002b).
Following these two projects, a third one, Since 1999, the STS strategy has become a
the Slow-the-Spread (STS) pilot project comprehensive long-term national pro-
(1993–1998), was initiated by the USDA gramme to protect the trees and forests in the
Forest Service with participating state agen- USA from gypsy moth along the entire
cies. This study determined the feasibility of length of the expanding gypsy-moth front.
using IPM strategies to slow the spread of STS coordinates efforts by the USDA Forest
the gypsy moth, with reduced pesticide use Service, the Animal and Plant Health
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IPM in Forestry 231

Inspection Service (APHIS) and several and Sharov, 1995). Mating disruption with
states where the gypsy moth is not yet estab- disparlure was significantly more effective
lished (Sharov et al., 2002a). It uses three than Btk in reducing isolated low-density
strategies: gypsy-moth populations (Sharov et al.,
2002b).
● Suppressing populations within generally
The gypsy-moth virus (Gypchek),
infested areas.
because of its long incubation period and
● Slowing the spread of gypsy moth to
inconsistent efficacy (Podgwaite, 1999), is not
delay the impacts and costs associated
the best choice for defoliation prevention.
with managing gypsy-moth outbreaks.
Dimilin® would be a better choice for use in
● Eradicating isolated infestations outside
campsites and other areas where its non-
generally infested areas.
target effects might be tolerated. Disparlure
In the USA, the approach currently used has been shown to substantially reduce
is to control the advancing front of increas- gypsy-moth populations at low to medium
ing gypsy-moth populations to slow the densities (Reardon et al., 1998), and its opera-
expansion of this insect’s range. Pheromone tional use is increasing (Sharov et al., 2002a).
traps are used to detect new outbreaks on
the leading edge of the infestation, and envi-
ronmentally benign insecticides, such as Btk, Success of the STS strategy
LdNPV or mating disruption, are used in the
suppression or eradication programmes. Sharov and Liebhold (1998b) developed a
Eradication is implemented in areas where model predicting that the spread of gypsy
the gypsy moth is detected well in front moth could be slowed by as much as 50%
(100–150 km) of the spread. Suppression pro- utilizing barrier zones (Liebhold et al., 1992;
jects are conducted to reduce damage in Sharov and Liebhold, 1998b). In practice, the
areas where the gypsy moth is well estab- actual rate of spread in the Appalachian
lished. Mountains was reduced by 59% (Liebhold et
Analysis of the historical records of the al., 1992), from 21 km/year to 9 km/year
gypsy-moth spread in the eastern USA, (Sharov and Liebhold, 1998c). Sharov and
revealed three distinct time periods with dif- Liebhold (1998b) developed a model that
ferent rates of spread or expansion (Liebhold specifies optimal strategies for eradication
et al., 1992). From 1900 to 1915 the rate of and containment. Their analysis and contain-
spread was slow, about 9 km/year. The ment model disagree with the statement by
spread was reduced to c. 3 km/year from Dahlsten et al. (1989) that ‘insects that have
1916 to 1965. This reduction was very proba- already colonized parts of the United States
bly due to the aggressively managed ‘barrier or any large land mass or continent, proba-
zone’ (e.g. detection, suppression and eradi- bly should not be the targets for eradication
cation) to reduce the gypsy moth’s westward programs in other sections of the country
movement. From 1966 to 1989, the rate of because of their potential for recolonization’.
spread was very high (c. 21 km/year) Sharov and Liebhold (1998a) state that their
(Liebhold et al., 1992, 1995). ‘analysis clearly demonstrates that this state-
The STS project demonstrated the feasibil- ment is wrong. Eradication of small, isolated
ity of reducing the rate at which insect infes- colonies of the gypsy moth within barrier
tations spread. Btk, Dimilin®, Gypchek and zones is not only feasible, but also economi-
disparlure were tested to determine their cally justified because the model predicts
efficacy against different densities of gypsy- positive net benefits under realistic assump-
moth infestation. Btk, Dimilin® and Gypchek tions.’
(LdNPV) are used to eradicate outlier or to There is economic benefit to slowing the
suppress moderate to high gypsy-moth pop- spread of gypsy-moth populations
ulations, while mating disruption using (Leuschner et al., 1996; Sharov and Liebhold,
Gyplure is used to manage low-density pop- 1998a). The costs of slowing the spread of
ulations (Reardon et al., 1994, 1998; Leonard gypsy moth have been estimated to be about
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232 I.S. Otvos

25% of the expected potential benefits the USA. After the failure to eradicate the
(Sharov et al., 1998). Since about two-thirds gypsy moth in eastern Canada, only sup-
of the potential area in the USA containing pression programmes were conducted
highly susceptible host trees (mainly in the against the European strain of gypsy moth.
south-eastern USA) remains uninfested The outbreak in Quebec peaked in 1977, with
(Liebhold et al., 1997), slowing the spread of 518,000 ha of defoliated stands and in
gypsy moth into these areas is economically Ontario in 1985, with 246,000 ha defoliated.
beneficial (Leuschner et al., 1996; Sharov and The area infested in Ontario decreased to
Liebhold, 1998a). Estimated benefits associ- almost 168,000 ha of moderate to severe
ated with reducing the rate of spread out- defoliation in 1986 (Jobin, 1995), of which
weighed the cost of implementing the STS 103,094 ha were treated (Nealis et al., 2002).
programme (detecting and treating isolated In the aerial-spray operations conducted
infestations along and ahead of the expand- between 1960 and 1974, chemical insecti-
ing gypsy-moth population front) by at least cides, mainly Sevin® and some DDT, were
3 : 1 (Leuschner et al., 1996). This perceived used (Brown, 1975). Until 1969, the main
or real benefit is indicated by individual purposes of these control operations were
households5 who, when surveyed, indicated twofold: eradication of small, incipient infes-
a willingness to pay between US$13 and tations and suppression of larger infesta-
57/ha for gypsy-moth control (Miller and tions. After 1969 the principal aims of these
Lindsay, 1993). spray operations were, as in the USA, to sup-
press gypsy-moth larval populations and
delay the spread of gypsy moth into unin-
Gypsy moth in eastern Canada fested areas (Jobin, 1995). Between 1975 and
1989 Btk, Sevin® and Dimilin® were mainly
The use of chemicals and biological insecti- used operationally for suppression (Jobin,
cides for eradication, suppression and delay- 1995). Btk was used almost exclusively oper-
ing the spread of gypsy-moth populations, ationally after 1981 (Nealis et al., 2002; Fig.
as well as the introduction of natural ene- 10.5B).
mies, followed the same general trend in Work on the use of pathogens (Btk and
Canada (Fig. 10.5B) as in the USA (Fig. LdNPV) for gypsy-moth suppression did not
10.5A). Therefore, for the sake of brevity, start in Canada until the 1970s (Griffiths and
only the highlights will be mentioned here. Quednau, 1984). Btk slowly gained accep-
In eastern Canada, the gypsy moth was tance as an effective suppression tool of
first recorded in Quebec near the US border gypsy-moth populations and, at its peak use
in 1924, and covered about 90 ha. Control in 1986, over 103,000 ha of gypsy-moth-
measures using lead arsenate commenced infested stands were treated in Ontario
the following year, and within 3 years the (Jobin, 1995; Nealis et al., 2002).
infestation was eradicated. A second inva- Although the virus (LdNPV) is also regis-
sion of gypsy moth, detected in New tered and effective for suppression of gypsy-
Brunswick in 1936, was successfully eradi- moth populations, it is not yet commercially
cated by 1940 (Jobin, 1995). No further intro- available. Consequently, the virus was only
ductions of gypsy moth were found in used experimentally in Canada (Jobin, 1995;
eastern Canada for the next 16 years. Nealis et al., 2002), unlike in the USA where
A survey and detection programme using the USDA Forest Service produces and uses
pheromone-baited traps was initiated in 1954 it in cooperative projects.
and resulted in the discovery of a third infes- Since the establishment of the gypsy moth
tation in 1956, near the site of its first intro- in North America, 26 species of parasitoids
duction in Quebec (Cardinal, 1967). Spray native to North America have been found to
operations, initiated in 1960, to control this successfully attack and develop in this
infestation failed. The gypsy moth was later unwanted newcomer (Griffiths, 1976;
detected in Ontario in 1969, the infestation Sabrosky and Reardon, 1976; Griffiths and
originating from a separate invasion from Quednau, 1984). In addition, 17 native insect
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IPM in Forestry 233

predators and four mammalian predators Gypsy moth on the west coast
also prey on the gypsy moth (Griffiths, 1976).
Of the 26 parasitoid species that attack gypsy In western North America, neither the
moth in the USA, 14 species were also reared European nor the Asian strains of the gypsy
from other hosts in southern Ontario and moth have become established to date.
Quebec near the US border (Griffiths and Effective detection grids using pheromone
Quednau, 1984), indicating the generalist traps around ports and in suspect areas and
nature of most of these parasitoids. immediate eradication are the policy on the
A review of the world literature on the Pacific coast of Canada and the USA. So far,
parasitoids and predators of the gypsy moth only small spot infestations of these two
showed that there are close to 400 species of strains (mainly the European strain) have
natural enemies associated with the gypsy been found in British Columbia, Washington
moth (Griffiths, 1976). Some of these were and Oregon, and all have been successfully
originally introduced against the browntail eliminated through aggressive aerial and
moth, Euproctis chrysorrhoea (Linnaeus) ground application of Btk, as was the infesta-
(Hewitt, 1916). Of the over 50 species of tion of the Asian strain introduced into
exotic parasitoids and predators released in North Carolina in 1993 on US military equip-
the USA, 13 species of exotic parasitoids and ment returning from Germany, at a cost of
one predator became established, 29 para- about US$9 million (Wallner, 1996).
sitoids and eight predators did not (Griffiths, The first interception of the gypsy moth
1976). Of these 13 exotic species of para- on the west coast was in 1911 in British
sitoids established in the USA, nine species Columbia, when egg masses were found on
spread into Canada on their own. In fact, ornamental Thuja trees from Japan (Brown,
four of these parasitoid species were recov- 1975). The egg masses were destroyed but
ered in southern Ontario and Quebec before not before a few larvae hatched (Humble
the gypsy moth was recorded in the area and and Stewart, 1994). The interceptions and
before any exotic parasitoids were intro- repeated eradications of the gypsy moth in
duced against the gypsy moth in Canada British Columbia (both European and Asian
(Griffiths and Quednau, 1984). Based on the strains) have been summarized by Humble
review of literature of gypsy-moth para- and Stewart (1994). In eradication pro-
sitoids and predators (Griffiths, 1976) and grammes, application is generally from the
their own work (including egg parasitoids) air, although at times the less effective and
in Canada, Griffiths and Quednau (1984) more expensive ground treatments are used
concluded, ‘The establishment of exotic as a result of court challenges by environ-
insect parasites [parasitoids] on the gypsy mental groups opposing the eradication pro-
moth in Canada is proceeding well largely grammes and/or aerial spraying of Btk or
through natural dispersal’ and ‘there is little any other insecticidal product.
more to be done in the introduction of bio- The Asian strain was introduced in 1991
logical control agents because there are no by Russian ships coming from the Far East
more suitable candidates’ (Griffiths and but was also eradicated successfully in 1992
Quednau, 1984). However, most of the seven (Humble and Stewart, 1994). During this
introduced parasitoids were collected in eradication, 19,000 ha were treated, at an
moderate to high gypsy-moth populations. estimated cost of CAN$6.5 million (Nealis,
Consequently, since 1980, work in Canada 2002). Since this incident, federal inspectors
has focused on finding parasiotids in Europe have banned ships from inshore waters
that might be effective at low gypsy-moth when gypsy-moth egg masses are discovered
densities. This resulted in the introduction on the superstructure of freighters during
and release of a little known tachinid fly in larval hatch and development (Humble and
Canada (Mills and Nealis, 1992; Nealis and Stewart, 1994).
Quednau, 1996). However, it is too early to Eradication gets complicated when non-
evaluate the impact of this latest introduc- infested countries or regions impose trade
tion on the gypsy-moth population. embargoes. Such was the case with the 1999
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234 I.S. Otvos

eradication programme in British Columbia, within 3 or 4 weeks of attack, but the foliage
which resulted from an unusual situation may not change colour until the following
arising among the various government agen- year. For the host trees attacked by the other
cies responsible for responding to the exotic- three destructive bark-beetle species, the
insect threat and trying to meet trade process of tree death is similar to that caused
conditions imposed by regions that are by the mountain-pine beetle. Periodic bark-
threatened by L. dispar invasion. Until 1998, beetle outbreaks frequently cause cata-
the federal government’s Canadian Food strophic economic losses. During the last
Inspection Agency (CFIA) conducted eradi- outbreak (1972 to 1985) the mountain pine
cation programmes against the gypsy moth beetle killed approximately 195.7 million
(both European and Asian strains) in British pines in British Columbia, representing an
Columbia. Following the eradication pro- estimated potential economic loss of $14.4 to
gramme in 1998, CFIA announced that it 19.6 billion, of which about $4.0 to 5.4 billion
would no longer consider eradication of the worth of beetle-killed trees could not even be
European gypsy moth from British salvaged (Borden, 1990). During the peak of
Columbia and would only regulate infested the outbreak in 1983, an estimated 43 million
areas. Consequently, the USA imposed trade mature lodgepole pine (Pinus contorta Dougl.
restrictions on lumber and log exports from ex. Loud. var. latifolia Engelm.), represent-
British Columbia, forcing the provincial gov- ing enough lumber to build 270,000 three-
ernment to pass an order-in-council to bedroom homes (S.R. Whitney, 1985, per-
enable them to treat the 13,000 ha that had sonal communication), were killed in
been delineated for treatment, based on infestations that covered nearly half a
pheromone-trap catches on southern million hectares of forests (Wood et al., 1983).
Vancouver Island. This eradication pro- The current mountain pine beetle outbreak
gramme, conducted in 1999, cost c. CAN$3.7 in British Columbia, which started around
million (Nealis, 2002). 1992, now (2003) covers an estimated 2.0
million ha. Infestations by D. rufipennis and
D. pseudotsugae occurred over an additional
Management of Bark Beetles 1.2 million ha (British Columbia Ministry of
Forests, 2003). There is no indication of a
Over 200 species of scolytid bark beetles decline in the mountain pine beetle outbreak.
occur in Canada and Alaska (Bright, 1976). At present, bark-beetle outbreaks of this
Nine are economically important and seven magnitude can only be terminated by un-
of these attack conifers. The most destructive seasonably cold temperatures (−35°C or lower
conifer-attacking bark beetles, in descending for several days) (Somme, 1964) with little or
economic importance, are: no snow cover around the infested bole.
The earliest control operations against
● mountain pine beetle, Dendroctonus pon-
bark beetles occurred in the late 1910s and
derosae Hopkins;
were directed at D. rufipennis and D. pon-
● spruce beetle, Dendroctonus rufipennis
derosae outbreaks in eastern and western
(Kirby);
Canada, respectively. These early control
● Douglas fir beetle, Dendroctonus pseudot-
attempts involved harvesting the infested
sugae Hopkins;
stands or performing individual tree treat-
● western balsam bark beetle, Dryocoetes
ments such as fell-and-burn, or peeling and
confusus Swaine.
burning the infested bark. By the late 1940s,
These beetles breed in the inner bark and the chemical insecticides ethylene dibromide
phloem of the main bole of their host trees. (EDB), a fumigant, and benzene hexachlo-
Needles of trees successfully attacked by ride (BHC (lindane)), were the most com-
bark beetles first fade and then turn to a red- monly used chemicals. BHC was formulated
dish-brown colour (pines, firs, Douglas fir) in fuel oil, usually as a 2% solution, and used
or the faded needles fall off (spruce). The as a bark-penetrating insecticide to kill
trees attacked by mountain pine beetle die broods under the bark or as a water emul-
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IPM in Forestry 235

sion for protecting trees from beetle attack. value or high-impact areas, such as parks
Trap trees, felled or standing, either treated and campsities, the lower boles of trees can
or not treated with chemical insecticides, be treated with 2% active ingredient (AI) car-
were commonly used after the 1940s, and baryl in water to protect trees from lethal
aerial-detection surveys were used for delin- attack (McMullen et al., 1986).
eating infestations. By the late 1970s, the use Preventive management is the preferred
of BHC and EDB was phased out, owing to option, and entails long-term planning and
environmental concerns, and were replaced the use of forestry practices that reduce
by a systemic pesticide, monosodium stand susceptibility. For D. ponderosae, pre-
methane arsenate (MSMA). ventive management is based on reducing
the susceptibility of lodgepole pine stands
(Shore and Safranyik, 1992; Shore et al., 2000)
Management methods and involves forestry practices such as spac-
ing, age stratifying, stocking and stand con-
Management options are available for two of version and species control, which may be
the most important beetles: the mountain combined with sanitary harvesting/logging.
pine beetle and the spruce beetle (McMullen One or a combination of the following man-
et al., 1986; Safranyik et al., 1990; agement options that prevent or delay out-
Maclauchlan and Brooks, 1994). Bark-beetle break development can reduce stand
management is based on two approaches: susceptibility, i.e. shorter rotation age, con-
direct control and prevention (McMullen et version of forest type to a less susceptible
al., 1986). one, creation of mixed-age stands, creation of
Direct control is currently used oper- mixed-host-species stands and changing
ationally, and is most effective when a beetle stand structure and stocking (Safranyik et al.,
infestation is small or just beginning to 1974). All of these options are used in British
develop. At this time the direct-control mea- Columbia. The spacing and thinning of
sures are implemented to lower beetle popu- stands and partial cutting have been effec-
lations to endemic levels or until one of the tive in reducing losses caused by mountain
other management options can be imple- pine beetle in mature lodgepole pine
mented. There are two main operational (Mitchell et al., 1983; Cole and McGregor,
direct-control measures: sanitary logging of 1985) and second-growth ponderosa pine
infested stands and treatment of individual (Sartwell and Dolph, 1976) in the USA.
trees, mainly using lethal and conventional Semiochemicals – chemicals eliciting
trap trees or fell-and-burn, or using sevin interactions between organisms – can be
(carbaryl) as a bark-penetrating chemical. used to manipulate mountain pine beetle
Silvicultural methods, such as sanitation– (Borden, 1989). During the past 25 years, the
salvage logging or felling and burning of the use of population-aggregating pheromones
infested trees (McMullen et al., 1986), will became standard practice to contain and con-
reduce beetle populations if applied in a centrate infestations in order to increase the
timely fashion, that is, before the new gener- efficacy of the control operation. The aggre-
ation of adult beetles leaves the infested gation pheromone can be used in surveys to
trees. Individual trees are ‘treated’ by the monitor beetle populations or to concentrate
cut–pile–burn method or by injecting the flying beetles in trees where they can be
infested trees with the herbicide MSMA to treated with a systemic herbicide, such as
kill the new brood of larvae (McMullen et al., MSMA. Baiting of individual trees and small
1986). MSMA has to be applied within a few isolated stands with bark-beetle aggregation
weeks of the attack while the trees are still pheromone concentrates beetle attacks,
alive and can translocate the poison. decreasing the spread of the infestation and
Sanitation logging is generally used to treat increasing the cost-effectiveness of direct-
larger, more diffuse infestations, and control operations through sanitation log-
involves removing (logging) the attacked ging (Borden et al., 1983). Treating individual
trees containing the beetle brood. In high- or small groups of trees with anti-aggrega-
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 236

236 I.S. Otvos

Table 10.5. Major forestry weed species competing with the production of commercial forest crop trees
in Canada (from Wall et al., 1992).

Species Common name Region

Trees
Acer macrophyllum Pursh Big-leaf maple Coastal British Columbia
Acer rubrum L. Red maple Ontario, Quebec, Maritimes
Acer spicatum Lambert Mountain maple Ontario, Quebec, Manitoba, Maritimes
Alnus incana (L.) Moench Speckled alder Transcontinental
Alnus rubra Bongard Red alder Coastal British Columbia
Corylus cornuta Marshall Beaked hazelnut Transcontinental
Populus tremuloides Trembling aspen Transcontinental
Michaux
Salix spp. Willows Transcontinental

Shrubs
Gaultheria shallon Pursh Salal Coastal British Columbia
Ribes spp. Currants and British Columbia, Ontario,
gooseberries Quebec, Maritimes
Rubus idaeus L. Red raspberry Ontario, Quebec, Maritimes
Rubus parviflorus Nuttall Thimbleberry British Columbia
Rubus spectabilis Pursh Salmonberry Coastal British Columbia
Sambucus spp. Elderberries Transcontinental

Herbaceous plants
Calamagrostis canadensis Blue-joint grass Alberta, interior British Columbia
(Michx.) Palisot de Beauvois
Epilobium angustifolium (L.) Fireweed Transcontinental
Kalmia angustifolia L. Sheep laurel Newfoundland, Maritimes
Pteridium aquilinum (L.) Kuhn Bracken fern Transcontinental

tion pheromone is thought to repel beetles Vegetation Management in Forestry

from the trees in the treated stand. Variation
in the use of these aggregation and anti- Unwanted (weedy) vegetation is a major
aggregation pheromones, as proposed and source of competition for water, nutrients,
tested by Borden (1995), has met with vary- light and space in nurseries, plantations and
ing degrees of success. areas of natural conifer regeneration (Watson
Population-aggregating pheromones are and Wall, 1995). Some weeds, such as Ribes
used extensively to increase the efficacy of spp. and fireweed, Epilobium angustifolium
control programmes. Direct-control opera- (Linnaeus), are alternative hosts of important
tions are guided by pretreatment population forest-tree rust diseases (Ziller, 1974; Hansen
and damage assessments and an appropriate and Lewis, 1997). Competition from weedy
strategy and set of tactics that are based on vegetation can delay seedling establishment,
the field assessment combined with consider- reduce growth, decrease timber yield and
ation of environmental and socio-economic delay harvest (increase rotation age) of
concerns. The management operations are conifer crop trees. The economic losses
guided by decision support systems that caused by weeds in forestry were not fully
determine susceptibility and risk (Shore and appreciated until recently (Walstad and
Safranyik, 1992; Shore et al., 2000) and feasi- Kuch, 1987).
ble strategies and tactics to be used in partic- Most forest weeds are native species.
ular situations (Maclauchlan and Brooks, Among the major competitors of crop-tree
1994). species, nine are fast-growing hardwood
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 237

IPM in Forestry 237

70

Chemical
60
Manual
50

Area treated (’000 ha)

Manual/chemical

40 Sheep

30

20

10

0
4

2
2

/9
/8

/8

/8

/9
/8

89
83

85

87

91
81

19
19

19

19

19
19

Year
Fig. 10.6. Methods and trends of vegetation management in forest areas on crown-land in British Columbia,
1981–1993 (after Boateng, 1996).

trees, six are shrubs and four are herbaceous with the establishment and growth of crop-
plants (Wall et al., 1992; Table 10.5). In most tree species (Feller, 1996). Fire does not elimi-
cases, the unwanted vegetation can only be nate the roots of perennial weeds and in fact
managed, not eliminated. In forestry, as in stimulates sprouting of some perennial
agriculture, competing vegetation has to be weeds and tree species (Prasad, 1996).
managed to favour the growth of the crop Grazing by animals, mainly sheep, has
species. A number of methods have been, been tried experimentally on a relatively
and are still, used for vegetation manage- small scale in Australia, Canada, Ireland,
ment, as illustrated in Fig. 10.6. In British New Zealand, Sweden and the USA
Columbia, of the vegetation management (Sharrow et al., 1989; Cayford, 1993). Sheep
treatments conducted during a 10-year grazing is now used operationally in forestry
period (1981/82–1992/93), 57% were done to control weeds, but only in small planta-
by using herbicides alone, 36% by using tions. Mulching with allelopathic plant mate-
manual cutting, 4% by using a combination rial (i.e. chemicals that leach out of the mulch
of herbicides and cutting and 3% by sheep and suppress weed growth) has been tried
grazing (Fig. 10.6). Manual removal of the experimentally (McDonald and Fiddler,
competing vegetation is expensive and inef- 1996). Mulching, as well as brush and plastic
ficient (Pendl and D’Anjou, 1990). blankets, works well in nurseries and in
Mechanical methods, using various kinds of small intensively managed plantations, but
machinery for site preparation after logging, operational use of these methods is not yet
are also expensive and, in addition, favour practical in forestry (Jobidon et al., 1989;
resprouting of some weedy species and tend Jobidon, 1991a).
to compact the soil (Prasad, 1996). Some microorganisms and plants produce
Prescribed fire is sometimes used in an natural herbicides that are toxic to some weed
attempt to eliminate weed seeds, unwanted species (Duke, 1986; Duke and Lydon, 1987).
seedlings and stumps. It also retards the For example, bialophos (aminohydroxy-
regrowth of vegetation that would compete phospho-vinyl-butyryl-alanine), originally
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 238

238 I.S. Otvos

ronmental concerns (DeBoo and Prasad,

60 1997) and for political reasons (Halleran,
50
1990).
Area treated (’000 ha)

Restrictions on pesticide use for weed

40 control in forestry will probably increase.
Therefore, it is necessary to develop one or
30 more cost-effective and environmentally
20 acceptable methods of weed control (i.e.
alternatives to chemical herbicides) in
10 forestry. Biological control (especially in the
case of introduced organisms) and the so-
0 called bioherbicides may offer such an
90

00
80

85

95
75

option. Bioherbicides are ‘living entities’

19

20
19

19

19
19

Year used to deliberately suppress the growth of

weeds or reduce weed populations to eco-
Fig. 10.7. Forest area treated with herbicidesa for nomically acceptable levels in areas where
weed management in British Columbia by the
they compete with the desired crop grown
Ministry of Forests and Forest Companies between
1975 and 2000 (from Humphreys, 1986, 1990;
(Watson, 1989; Auld and Morin, 1995). These
Canadian Council of Forest Ministers, 2003). controls may include insects and pathogens
a Herbicides applied in large-scale operations (bacteria, fungi and viruses). The terms bio-
include 2,4-D, 2,4-E, fosamine, glyphosate, logical herbicides, bioherbicides and myco-
hexazinone, MSMA, picloram and triclopyr. herbicides are used interchangeably in the
Glyphosate has been used preferentially since scientific literature to describe all pathogens
1985. (Winder and Shamoun, 1991). The term
mycoherbicides, however, is more appropri-
isolated from the soil microbe Streptomyces ate when referring to herbicides based on
viridochromogens (Jobidon, 1991b), controls fungal pathogens. For the purposes of this
red raspberry (Rubus idaeus L.) in forest plan- chapter, the term originally used in the paper
tations. However, it is expensive, is toxic to is retained when reference is made to a par-
some conifers and has only limited use in ticular paper.
forestry (Jobidon, 1991b; Prasad, 1992). Biological control strategies in weed man-
Competition by herbaceous and woody agement in forestry include both classical
vegetation frequently requires treatment (inoculative) and inundative (augmentative)
with commercial herbicides. Although the inoculation with plant pathogens (Watson
use of herbicides has been part of forest and Wall, 1995; Wall and Hasan, 1996). The
management since the mid-1940s, in British inoculative (classical) approach is generally
Columbia, Canada, the area treated annually employed when the noxious weed was acci-
was small (about 5000 ha/year) until the dentally or intentionally introduced, usually
early 1980s (DeBoo and Prasad, 1997). from one continent to another. The natural
Chemical herbicides were the choice of treat- enemy (usually a pathogen) or most promis-
ment (mainly 2,4-dichlorophenoxyacetic acid ing enemies are introduced in the hope that
(2, 4-D) and 2, 4, 5-trichlorophenoxyethanoic they will spread throughout the ‘pest’ host
acid (2, 4, 5-T)) and have been used for vege- population, resulting in control. The inunda-
tation management in British Columbia since tive approach is mainly employed against
the mid-1970s (Fig. 10.7) and are the most endemic weedy populations. The weeds are
cost-effective, especially if they can be treated with a large amount of indigenous
applied from the air (Thorpe, 1996). After natural enemies, usually fungal pathogens of
1983, increased funding was available for the weeds, which augment the local, natu-
forest management, resulting in generally rally occurring pathogens. The remainder of
increased pesticide use until 1992 (Fig. 10.7). this section will review the major accom-
After 1985, 2,4-D and 2,4,5-T were replaced plishments using these approaches for vege-
by glyphosate because of health and envi- tation management in forestry.
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IPM in Forestry 239

The biological control of weeds in agricul- white-rot fungus Cylindrobasidium laeve

ture has a long history, with many notable (Pers.: Fr.) Chamois has been registered as
successes (McLeod, 1962; Harris, 1984; Stumpout™ for the control of introduced
Kelleher and Hulme, 1984), but it is rela- wattle trees, Acacia spp. (Morris et al., 1998).
tively new in forestry (Fig. 10.1). Similar suc- However, some introductions can lead to
cesses are also reported from the USA. The controversy. When the gorse mite,
study of biological controls for vegetation Tetranychus lintearius Dufour, was imported
and plant-pathogen management started to control the introduced gorse, Ulex
only recently, in the last 20 years. In Canada europaeus L., in New Zealand, it became con-
between 1981 and 2000, there were 20 studies troversial because the introduction gave only
on the biocontrol of weeds of agricultural variable control and the exotic mites inter-
crops and only five on forest weeds and two bred with one of the native mite species
on forest-tree diseases (Mason and Huber, (Syrett et al., 1985).
2002).

Bioherbicides
Inoculative strategy (classical biological
control) Despite three decades of research, the devel-
opment of effective bioherbicides for weed
The classical biological control strategy control in forestry is still in its infancy. Many
(introducing insect enemies of exotic weeds) preliminary results indicate the great poten-
has been used successfully in agriculture tial value derived from the use of biological
(Harris, 1984; Julien and Griffiths, 1998; control in vegetation management in forestry
Harris and Shamoun, 2002). (Shamoun, 2000; Shamoun and DeWald,
The European blackberry (Rubus frutico- 2002; Shamoun et al., 2002, and references
sus L. agg.) has been introduced to many therein). In fact, to date, only two mycoherbi-
parts of the world and is regarded as an cides are commercially available for control-
important weed pest in several countries, ling weeds along hydroelectric power lines
including Australia, where it invades pas- and for forestry use (Morris et al., 1998;
tures, forest and national parks (Amor and Shamoun and Hintz, 1998a,b). Of the bioher-
Richardson, 1980; Wall and Hasan, 1996). bicides tested, the manipulation of indige-
The rust fungus Phragmidium violaceum nous fungi probably offers the best chance
(Shultz) was introduced into Australia, for the development of mycoherbicides
where it controlled the European blackberry because they are native and generally persist
under the shady canopy of pine trees, at endemic levels in the environment.
thereby freeing pine seedlings from black- Research on plant pathogens as potential
berry competition and allowing them to biocontrol agents for weed control started in
grow normally after the release. However, the 1970s to suppress ericaceous shrubs on
the rust was less effective on blackberries cut-over sites in eastern Canada (Wall, 1977)
growing under the more open eucalyptus and later to control Rubus spp. (Wall, 1983).
stands. This was not unexpected because the Of the biocontrol agents examined,
microclimate is probably drier in the more Chondrostereum purpureum Fr./Pouzar was
open stand of eucalyptus. the most promising bioherbicide (Wall,
A gall-forming rust fungus, Uromycladium 1990).
tepperianum (Sacc.) McAlp., was introduced In western Canada, research has focused
into South Africa against the weed tree, on weedy trees (Acer macrophyllum Pursh,
Acacia saligna (Labill) Wendl. Both the fungus Alnus rubra Bong., Populus tremuloides
and the host tree originated in Australia. The Michx.), and shrubs (Rubus parviflorus Nutt.,
fungus became established in South Africa Rubus spectabilis Pursh., Gaultheria shallon
and infected and formed galls on the flowers Pursh.). Pathogens from all of these target
of A. saligna, killing some of the trees species have been identified and many of
(Morris, 1991, 1997). In South Africa, the them have been tested as potential biocontrol
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 240

240 I.S. Otvos

agents (Dorworth, 1990, 1992; Sieber et al., scarcity of examples proving the commercial
1990a,b; Wall and Shamoun, 1990b). viability of this approach. The main reason
When applied to cut stumps, C. pur- for this is due to the fact that C. purpureum
pureum provided spectacular results and can only enter through an open wound of
gave 90% control of black cherry (Prunus the host tree and at present this can only be
serotina Ehrhert) regrowth in conifer planta- achieved through manual inoculation of the
tions in Holland. This level of control wound (cut surface) of the target plant. In
matched the effectiveness of the chemical forestry, on a large scale, this is probably not
herbicide glyphosate (Scheepens and feasible, but it may be practical to use under
Hoogerbrugge, 1989). However, in Canada, hydroelectric powerlines.
the same treatment gave somewhat less
spectacular results against Populus spp., Acer
spp., Betula spp., Prunus pensylvania and Silvicultural Management of Root
Alnus rubra (Wall and Shamoun, 1990a; Wall, Diseases
1994). Considerable research has also been
done on C. purpureum in Canada. Myco- Root diseases caused by Armillaria ostoyae
Forestis Corporation (Quebec) has registered (Romagn.) Herink, Phellinus weirii (Murr.)
one strain (HQ-1) under the name Myco- Gilb. and Inonotus tomentosus (Fr.: Fr.) Teng.
Tech™ Paste for use east of the Rocky are among the most destructive pathogens of
Mountains in Canada. Another strain (PFC trees, mainly conifers grown for timber, in
2139) is currently being registered for use in western North America. They cause signifi-
western Canada and the entire USA cant growth loss and tree mortality in man-
(Shamoun and Hintz, 1998a,b). After consid- aged forests (Bloomberg and Reynolds, 1985;
erable testing, C. purpureum has been McDonald et al., 1987; Morrison et al., 1988,
adopted, with a refined formulation, and 1992; Bloomberg and Morrison, 1989; Ives
patented for control of hardwoods in North and Rentz, 1993; Woods, 1994). Of these,
American forests (Wall et al., 1996). However, Armillaria root disease caused by A. ostoyae,
C. purpureum has not been registered as a is the most important. It occurs in all forest
mycoherbicide in Holland but is used only regions of Canada. In the interior of British
as a wood-decay promoter (Ravensberg, Columbia it is estimated to cause losses of
1998). Presumably, it was not registered there 2–3 million m3 annually (A. Van Sickle, 1999,
as a herbicide because of the cost of registra- personal communication). Even in undis-
tion and the expected return on this invest- turbed stands (Morrison and Mallet, 1996),
ment. The same economic considerations up to 80% of the trees in a stand can be
may hinder the commercial production and infected. All three root diseases reduce mer-
sale of mycoherbicide in forestry worldwide. chantable volume at the end of the planned
Some bioherbicides have been tested rotation, change species composition over
against several hardwood trees (Shamoun et
the rotation by killing the most susceptible
al., 2002), marsh reed grass (Calamagrostis
hosts and may lengthen the rotation age
canadensis (Michx.) Beauv) (Mallet et al.,
(Morrison and Mallett, 1996; Sturrock, 2000).
2002), Rubus spp. (Oleskevich et al., 1998),
The same management strategies can be
fireweed (Epilobium spp.) (Winder, 2002),
applied to reduce the impact for all three
Scotch broom, Cytisus scoparius (Linnaeus)
root diseases. It is best to apply treatments at
Link (Prasad, 2002a) and gorse (Ulex
the time of harvest and at stand regenera-
europaeus L.) (Prasad, 2002b). However, there
tion. The two most effective ways of reduc-
are several obstacles to the development of
ing the root diseases and their impacts are
commercial products, such as application
the following:
technology, formulation to increase efficacy
of the product so that it can be stored and 1. Machine-assisted removal of inoculum
readily applied in the field, optimum volume source (infected stumps and large roots) at
and droplet size to give the optimum effi- the time of harvesting or by push–pull log-
ciency, which are still unknown, and the ging of trees in root-diseased stands
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 241

IPM in Forestry 241

(Morrison et al., 1992; Sturrock et al., 1994; associated costs are justified by increased
Morrison and Mallett, 1996; Sturrock, 2000). rates of return in the next rotation: that is,
2. Planting resistant trees. Birch, aspen and the volume grown on the treated sites will
poplar are tolerant of A. ostoyae (Morrison more than pay for the inoculum removal.
and Mallett, 1996). All hardwoods are
immune to P. weirii (Morrison et al., 1988, Notes
1992) and birch is immune to I. tomentosus 1 The remainder was treated with the chemical
(Sturrock, 2000). insecticides fenitrothion and aminocarb
(Cunningham and van Frankenhuyzen, 1991).
Both mechanical methods to remove 2 The virus has to be produced in living insects,
sources of inoculum are called stumping therefore it is expensive to make. The cost of
(Morrison and Mallett, 1996). Stumping producing enough virus to treat 1 ha at the
exposes infected roots to the sun, thus dry- recommended label dose of 2.51011 PIB/ha is
about CAN$40–50/ha.
ing the roots and killing the fungi. Removal 3 The cost of disparlure treatment at this dose was
of the source of the inoculum from the soil estimated at US$64/ha, while double application
reduces the possibility of infection in the of Btk cost c. US$64–69/ha (Sharov et al., 2002b).
4 Dimilin® is a chitin synthesis inhibitor, and only
next crop of trees. Economic analysis con-
ducted for P. weirii in western Washington affects arthropods. However, it can kill or
negatively affect many non-target arthropods
(Russell et al., 1986) and for A. ostoyae in New (Butler et al., 1994).
Zealand (Shaw and Calderon, 1977) indicates 5 The survey was conducted in New Hampshire
that the high disease incidence and losses and included both households that had and had
that occur on non-treated sites can be not experienced gypsy-moth damage to their
properties.
reduced by removing the inoculum. The

References

Alfaro, R.I. and Maclauchlan, L.E. (1992) A method to calculate the losses caused by western spruce bud-
worm in uneven-aged Douglas-fir forests of British Columbia. Forest Ecology and Management 55,
295–313.
Amor, R.L. and Richardson, R.G. (1980) The biology of Australian weeds 2. Rubus fruticosus L. agg.
Includes distribution and ecological aspects. Journal of the Australian Institute of Agricultural Science
46, 87–97.
Andreadis, T.G. and Weseloh, R.M. (1990) Discovery of Entomophaga maimaiga in North American gypsy
moth, Lymantria dispar. Proceedings of the National Academy of Sciences of the USA 87, 2461–2465.
Armstrong, J.A. and Cook, C.A. (1993) Aerial Spray Applications on Canadian Forests: 1945–1990.
Information Report ST-X-2, Forestry Canada, Ottawa, Ontario, 266 pp.
Auld, B. and Morin, L. (1995) Constraints in the development of bioherbicides. Weed Technology 9,
638–652.
Balch, R.E. and Bird, F.T. (1944) A disease of the European spruce sawfly, Gilpinia hercyniae (Htg.), and its
place in natural control. Scientific Agriculture 25, 65–80.
Baranchikov, Y.N. (1989) Ecological basis of the evolution of host relationships in Eurasian gypsy moth
populations. In: Wallner, W.E. and McManus, K.A. (technical coordinators) Proceedings, Lymantriidae:
a Comparison of New and Old World Tussock Moths, June 26-July 1, 1988, New Haven, Connecticut.
General Technical Report NE-123, USDA Forest Service, Northeastern Forest Experiment Station,
Broomall, Pennsylvania, pp. 319–338.
Beroza, M., Hood, C.S., Trefey, D., Leonard, D.E., Knipling, E.F. and Klassen, W. (1975) Field trials with
disparlure in Massachusetts to suppress mating of the gypsy moth. Environmental Entomology 4,
705–711.
Bird, F.T. (1959) Polyhedrosis and granulosis virus causing single and double infections in the spruce
budworm. Journal of Insect Pathology 1, 406–430.
Bird, F.T. (1961) Transmission of some insect viruses with particular reference to ovarial transmission and
its importance in the development of epizootics. Journal of Insect Pathology 3, 352–380.
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 242

242 I.S. Otvos

Blais, J.R. (1985) The ecology of the eastern spruce budworm: a review and discussion. In: Sanders, C.J.,
Stark, R.W., Mullins, E.J. and Murphy, J. (eds) Recent Advances in Spruce Budworms Research:
Proceedings of CANUSA Spruce Budworms Research Symposium, Bangor, Maine, September 16–20, 1984.
Canadian Forestry Service, Ottawa, Ontario, pp. 49–59.
Bloomberg, W.J. and Morrison, D.J. (1989) Relationship of growth reduction in Douglas-fir to infection by
Armillaria root disease in southeastern British Columbia. Phytopathology 79, 482–487.
Bloomberg, W.J. and Reynolds, G. (1985) Growth loss and mortality in laminated root rot infection cen-
tres in second-growth Douglas-fir on Vancouver Island. Forest Science 31, 497–508.
Blumenthal, E.M., Fusco, R.A. and Reardon, R.S. (1978) Augmentative release of two established para-
site species to suppress populations of the gypsy moth. Journal of Economic Entomology 72,
281–288.
Boateng, J. (1996) Past and future trends in forest vegetation management in BC. In: Coroneau, P.G.,
Harper, G.J., Blache, M.E., Boateng, J.O. and Gilkeson, L.A. (eds) Integrated Forest Vegetation
Management: Options and Applications. Proceedings of the Fifth British Columbia Forest Vegetation
Management Workshop, November 29–30, 1993 Richmond, British Columbia. Forest Resource
Development Agreement Report No. 251, Canadian Forest Service and British Columbia Ministry of
Forests, Victoria, British Columbia, pp. 1–4.
Borden, J.H. (1989) Semiochemicals and bark beetle populations: exploitation of natural phenomena by
pest management strategists. Holarctic Ecology 12, 501–510.
Borden, J.H. (1990) Semiochemicals to manage coniferous tree pests in western Canada. In: Ridgway,
R.L., Silverstein, R.M. and Inscoe, M.N. (eds) Behavior-modifying Chemicals for Insect Management:
Applications of Pheromones and Other Attractants. Marcel Dekker, New York, pp. 281–315.
Borden, J.H. (1995) Development and use of semiochemicals against bark and timber beetles. In:
Armstrong, J.A. and Ives, W.G.H. (eds) Forest Insect Pests in Canada. Natural Resources Canada,
Canadian Forest Service, Ottawa, Ontario, pp. 431–449.
Borden, J.H., Chong, L.J., Pratt, K.E.G. and Gray, D.R. (1983) The application of behaviour-modifying
chemicals to contain infestations of the mountain pine beetle, Dendroctonus ponderosae Hopk. The
Forestry Chronicle 59, 235–239.
Boulton, T.J. (1999) Impacts of Bacillus thuringiensis subsp. kurstaki (Btk) on the population dynamics of
non-target Lepidoptera on Ribes cereum. MSc thesis, University of Victoria, Victoria, British
Columbia, 287 pp.
Boulton, T.J., Otvos, I.S. and Ring, R.A. (2002) Monitoring nontarget Lepidoptera on Ribes cereum to
investigate side effects of an operational application of Bacillus thuringiensis subsp. kurstaki.
Environmental Entomology 31, 903–913.
Bright, D.E. Jr (1976) The Insects and Arachnids of Canada. Part 2: The Bark Beetles of Canada and Alaska.
Coleoptera: Scolytidae. Publication 1576, Biosystematics Research Institute, Research Branch,
Canadian Department of Agriculture, Ottawa, Ontario, 241 pp.
British Columbia Ministry of Forests (2003) Forest Health Conditions 2002, Aerial Overview Survey
Summary. Available at: www.for.gov.bc.ca/hfp/FORSITE/overview/2002table.htm
Brown, G.S. (1975) Gypsy moth Porthetria dispar (L.). In: Prebble, M.L. (ed.) Aerial Control of Forest Insects
in Canada. Environment Canada, Ottawa, Ontario, pp. 208–212.
Brown, W.L. Jr (1961) Mass insect control programs: four case histories. Psyche 68, 75–111.
Buckner, C.H., Kingsbury, P.D., McLeod, B.B., Mortensen, K.L. and Ray, D.G.H. (1974) Impact of aerial
treatment on non-target organisms, Algonquin Park, Ontario, and Spruce Woods, Manitoba. In:
Chemical Control Research Institute (ed.) Bacillus thuringiensis – Evaluation of Commercial
Preparation of Bacillus thuringiensis With and Without Chitinase Against Spruce Budworm. Information
Report CC-X-59, Chemical Control Research Institute, Ottawa, Ontario, pp. F1-F72.
Butler, L., Chrislip, G.A., Kondo, V.A. and Townsend, E.C. (1974) Effect of diflubenzuron on nontarget
canopy arthropods in closed, deciduous watersheds in Central Appalachian forest Journal of
Economic Entomology 90, 784-779.
Cadogan, B.L. (1995) Jack pine budworm, Choristoneura pinus. In: Armstrong, J.A. and Ives, W.G.H. (eds)
Forest Insect Pests in Canada. Natural Resources Canada, Canadian Forest Service, Ottawa, Ontario,
pp. 123–126.
Cameron, E.A. (1974) Programs utilizing pheromones in survey or control: the gypsy moth. In: Birch,
M.C. (ed.) Pheromones. American Elsevier Publication Company, New York, pp. 431–435.
Cameron, J.M. (1975a) Biological insecticides. In: Prebble, M.L. (ed.) Aerial Control of Forest Insects in
Canada. Department of Environment, Ottawa, Canada, pp. 25–33.
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 243

IPM in Forestry 243

Cameron, J.M. (1975b) Field trials of spruce budworm viruses, 1971–1973. In: Prebble, M.L. (ed.) Aerial
Control of Forest Insects in Canada. Department of Environment, Ottawa, Canada, pp. 134–137.
Campbell, R.W. (1963) The role of disease and desiccation in the population dynamics of the gypsy moth
Porthetria dispar (L.) (Lepidoptera: Lymantriidae). The Canadian Entomologist 95, 426–434.
Campbell, R.W. and Podgwaite, J.D. (1971) The disease complex of the gypsy moth. I. Major components.
Journal of Invertebrate Pathology 18, 101–107.
Canadian Council of Forest Ministers (2003) National Forestry Database Programme. Available at:
http://nfdp.ccfm.org
Canadian Department of Agriculture and Canadian Department of Fisheries and Forestry (1971)
Biological Control Programmes Against Insects and Weeds in Canada 1959–1968. Technical
Communication No. 4, Commonwealth Institute of Biological Control, Commonwealth Agricultural
Bureaux, Slough, UK, 266 pp.
Canadian Forest Service (1975) Report of the Annual Forest Pest Control Forum. Environment Canada,
Canadian Forest Service, Ottawa, Ontario, 225 pp.
Canadian Forest Service (1976) Report of the Annual Forest Pest Control Forum. Environment Canada,
Canadian Forest Service, Ottawa, Ontario, 341 pp.
Canadian Forest Service (1977) Report of the Annual Forest Pest Control Forum. Environment Canada,
Canadian Forest Service, Ottawa, Ontario, 337 pp.
Canadian Forest Service (1978) Report of the Annual Forest Pest Control Forum. Environment Canada,
Canadian Forest Service, Ottawa, Ontario, 443 pp.
Cantwell, G.E., Dutky, S.R., Keller, J.C. and Thompson, C.G. (1961) Results of tests with Bacillus
thuringiensis Berliner against gypsy moth larvae. Journal of Invertebrate Pathology 8, 228–233.
Cardinal, J.A. (1967) Lutte contre la spongieuse Porthetria dispar L. (Lepidoptera: Lymantriidae) au
Québec. Phytoprotection 48, 92–100.
Carson, R.L. (1962) Silent Spring. Houghton Mifflin, Boston, Massachusetts, 368 pp.
Casida, S.E. and Quistad, G.B. (1998) Golden age of insecticide research: past, present or future? Annual
Review of Entomology 43, 1–16.
Cayford, J.H. (1993) Sheep for vegetation management. The Forestry Chronicle 69, 27.
Cole, W.E. and McGregor, M.D. (1985) Reducing and preventing mountain pine beetle outbreaks in
lodgepole pine stands by selective cutting. In: Safranyik, L. (ed.) Role of the Host in the Population
Dynamics of Forest Insects: Proceedings of IUFRO Conference, Banff, Alberta, September 4–7, 1983.
Canadian Forestry Service, Pacific Forestry Centre, Victoria, British Columbia, 240 pp.
Council of Forest Industries (2000) British Columbia Forest Industry Fact Book, Vancouver, British
Columbia, 82 pp. Available at: www.cofi.org/reports/factbooks.htm
Cunningham, J.C. (1985a) Status of viruses as biocontrol agents for spruce budworms. In: Grimble, D.G.
and Lewis, F.B. (eds) Microbial Control of Spruce Budworms and Gypsy Moth. General Technical Report,
GTR-NE-100, Northeastern Forestry Experimental Station, US Department of Agriculture Forest
Service, Broomall, Pennsylvania, pp. 61–67.
Cunningham, J.C. (1985b) Biorationals for control of spruce budworms. In: Sanders, C.J., Stark, R.W.,
Mullins, E.J. and Murphy, J. (eds) Recent Advances in Spruce Budworm Research: Proceedings of
CANUSA Spruce Budworm Research Symposium, September 16–20, 1984, Bangor, Maine. Canadian
Forestry Service, Ottawa, Ontario, pp. 320–349.
Cunningham, J.C. (1998) North America. In: Hunter-Fujita, F.R., Entwistle, P.F., Evans, H.F. and Cook,
N.E. (eds) Insect Viruses and Pest Management. John Wiley and Sons, Chichester, UK, pp. 313–331.
Cunningham, J.C. and de Groot, P. (1984) Neodiprion lecontei (Fitch), redheaded pine sawfly
(Hymenoptera: Diprionidae). In: Kelleher, J.S. and Hulme, M.A. (eds) Biological Control Programmes
Against Weeds and Insects in Canada 1969–1980. Commonwealth Agricultural Bureaux, Slough, UK,
pp. 323–329.
Cunningham, J.C. and Howse, G.M. (1984) Viruses: application and assessment. In: Kelleher, J.S. and
Hulme, M.A. (eds) Biological Control Programmes Against Weeds and Insects in Canada 1969–1980.
Commonwealth Agricultural Bureaux, Slough, UK, pp. 248–259.
Cunningham, J.C. and Kaupp, W.J. (1995) Insect viruses. In: Armstrong, J.A. and Ives, W.G.H. (eds) Forest
Insect Pests in Canada. Natural Resources Canada, Canadian Forest Service, Ottawa, Ontario,
pp. 327–340.
Cunningham, J.C. and McPhee, J.R. (1986) Production of Sawfly Viruses in Plantations. Technical Note
No. 4, Canadian Forestry Service, Forest Pest Management Institute, Sault Ste Marie, Ontario,
4 pp.
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 244

244 I.S. Otvos

Cunningham, J.C. and Shepherd, R.F. (1984) Orgyia pseudotsugata (McDunnough), Douglas-fir tussock
moth (Lepidoptera: Lymantriidae). In: Kelleher, J.S. and Hulme, M.A. (eds) Biological Control
Programmes against Insects and Weeds in Canada, 1969–1980. Commonwealth Agricultural Bureaux,
Slough, UK, pp. 363–367.
Cunningham, J.C. and van Frankenhuyzen, K. (1991) Microbial insecticides in forestry. The Forestry
Chronicle 67, 473–480.
Cunningham, J.C., de Groot, P. and Kaupp, W.J. (1986) A review of aerial spray trials with Lecontvirus for
control of red-headed pine sawfly, Neodiprion lecontei (Hymenoptera: Diprionidae), in Ontario.
Proceedings of the Entomological Society of Ontario 117, 65–72.
Dahlsten, D.L., Garcia, R. and Lorraine, H. (1989) Eradication as a pest management tool: concepts and
contexts. In: Dahlsten, D.L. and Garcia, R. (eds) Eradication of Exotic Pests: Analysis with Case
Histories. Yale University Press, New Haven, Connecticut, 296 pp.
D’Amico, V. and Elkinton, J.S. (1995) Rainfall effects on transmission of gypsy moth (Lepidoptera:
Lymantriidae) nuclear polyhedrodis virus. Environmental Entomology 24, 1144–1149.
DeBoo, R.F. and Prasad, R. (1997) Pesticide use in forest management: the British Columbia experience
since 1946. Pesticide Outlook 8, 9–14.
Doane, C.C. (1970) Primary pathogens and their role in the development of an epizootic in the gypsy
moth. Journal of Invertebrate Pathology 15, 21–33.
Doane, C.C. (1976) Ecology of pathogens of the gypsy moth. In: Anderson, J.F. and Kaya, H.K. (eds)
Perspectives in Forest Entomology. Academic Press, New York, pp. 285–293.
Doane, C.C. and McManus, M.L. (eds) (1981) The Gypsy Moth: Research Toward Integrated Pest Management.
Technical Bulletin 1584, Forest Service, US Department of Agriculture, Washington, DC, 757 pp.
Dorworth, C. (1990) Use of indigenous microorganisms for forest weed biocontrol – the PFC enhance-
ment process. In: Basset, C., Whitehouse, L.J. and Zabkiewicz, J.A. (eds) Alternatives to the Chemical
Control of Weeds: Proceedings of an International Conference held at the Forest Research Institute, Rotorua,
New Zealand, July 25–27, 1989. Forest Research Institute Bulletin 155, Forest Research Institute,
Ministry of Forestry, Rotorua, New Zealand, pp. 116–119.
Dorworth, C.E. (1992) Biological control of weeds using indigenous pathogens. In: Shrimpton, G. (ed.)
Canadian Forest Nursery Weed Management Association: Proceedings of Annual Meeting. Victoria, British
Columbia, July 6–8, 1992. BC Ministry of Forests, Victoria, British Columbia, pp. 17–24.
Dowden, P.B. (1962) Parasites and Predators of Forest Insects Liberated in the United States through 1960.
Agricultural Handbook 226, Forest Service, US Department of Agriculture, Washington, DC, 70 pp.
Duan, L. and Otvos, I.S. (2001) Influence of larval age and virus concentration on mortality and sublethal
effects of a nucleopolyhedrovirus on the western spruce budworm (Lepidoptera: Tortricidae).
Environmental Entomology 30, 136–146.
Dubois, N.R. (1981) Bacillus thuringiensis. In: Doane, C.C. and McManus, M.L. (eds) The Gypsy Moth:
Research Toward Integrated Pest Management. Technical Bulletin 1584, Forest Service, US Department
of Agriculture, Washington, DC, pp. 445–453.
Duke, S.O. (1986) Naturally occurring chemical compounds as herbicides. Reviews of Weed Science 2,
15–44.
Duke, S.O. and Lydon, J. (1987) Herbicides from natural compounds. Weed Technology 1, 122–128.
Dulmage, H.T. (1982) Distribution of Bacillus thuringiensis in nature. In: Kurstak, E. (ed.) Microbial and
Viral Pesticides. Marcel Dekker, New York, pp. 209–237.
Dunlap, T.R. (1980) The gypsy moth: a study in science and public policy. Journal of Forest History 24,
116–126.
Elkinton, J.S. and Liebhold, A.M. (1990) Population dynamics of gypsy moth in North America. Annual
Review of Entomology 35, 571–596.
Elkinton, J.S., Hajek, A.E., Boettner, G.H. and Simons, E.E. (1991) Distribution and apparent spread of
Entomophaga maimaiga (Zygomycetes: Entomophthorales) in gypsy moth (Lepidoptera:
Lymantriidae) populations in North America. Environmental Entomolgy 20, 1601–1605.
Embree, D.G. (1971) The biological control of the winter moth in eastern Canada by introduced parasites.
In: Huffaker, C.B. (ed.) Biological Control. Plenum, New York, pp. 217–226.
FAO (Food and Agriculture Organization of the United Nations) (2002) FAO Statistics. Available at:
www.fao.org/forestry/index.jsp
Feller, M. (1996) Use of prescribed fire for vegetation management. In: Comeau, P.G., Harper, G.J., Blache,
M.E., Boateng, J.O. and Gilkeson, L.A. (eds) Integrated Forest Vegetation Management: Options and
Applications. Proceedings of the Fifth British Columbia Forest Vegetation Management Workshop, November
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 245

IPM in Forestry 245

29–30, 1993, Richmond, British Columbia. Forest Resource Development Agreement Report No. 251,
Canadian Forest Service and British Columbia Ministry of Forests, Victoria, British Columbia,
pp. 17–34.
Fleming, R. and Retnakaran, A. (1985) Evaluating single treatment data using Abbott’s formula with ref-
erence to insecticides. Journal of Economic Entomology 78, 1179–1181.
van Frankenhuyzen, K. (1990) Development and current status of Bacillus thuringiensis for control of
defoliating forest insects. The Forestry Chronicle 66, 498–507.
van Frankenhuyzen, K. (1993) The challenge of Bacillus thuringiensis. In: Entwistle, P.F., Cory, J.S., Bailey,
M.J. and Higgs, S. (eds) Bacillus thuringiensis, an Environmental Pesticide: Theory and Practice. J.
Wiley & Sons, New York, pp. 1–35.
van Frankenhuyzen, K. (1995) Development and current status of Bacillus thuringiensis for control of
defoliating forest insects. In: Armstrong, J.A. and Ives, W.G.H. (eds) Forest Insect Pests in Canada.
Natural Resources Canada, Canadian Forest Service, Ottawa, Ontario, pp. 315–325.
van Frankenhuyzen, K. (2000) Application of Bacillus thuringiensis in forestry. In: Charles, J.F., Delecluse,
A. and Nielsen-LeRoux, C. (eds) Entomopathogenic Bacteria: From Laboratory to Field Application.
Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 355–370.
Glaser, R.W. (1915) Wilt of gypsy-moth caterpillars. Journal of Agricultural Research 4, 101–128.
Griffiths, K.J. (1976) The Parasites and Predators of the Gypsy Moth: a Review of the World Literature with
Special Application to Canada. Information Report O-X-243, Canadian Forestry Service, Great Lakes
Forest Research Centre, Sault Ste Marie, Ontario, 92 pp.
Griffiths, K.J. and Quednau, F.W. (1984) Lymantria dispar (L.), gypsy moth (Lepidoptera:
Lymantriidae). In: Kelleher, J.S. and Hulme, M.A. (eds) Biological Control Programmes Against
Weeds and Insects in Canada 1969–1980. Commonwealth Agricultural Bureaux, Slough, UK,
pp. 303–310.
Hajek, A.E. (1997) Fungal and viral epizootics in gypsy moth (Lepidoptera: Lymantriidae) populations in
central New York. Biological Control 10, 58–68.
Hajek, A.E. and Roberts, E.W. (1991) Pathogen reservoirs as a biological control resource: introduction of
Entomophaga maimaiga to North American gypsy moth, Lymantria dispar, populations. Biological
Control 1, 29–34.
Hajek, A.E. and Roberts, E.W. (1992) Field diagnosis of gypsy moth (Lepidoptera: Lymantriidae) larval
mortality caused by Entomophaga maimaiga and the gypsy moth nuclear polyhedrosis virus.
Environmental Entomology 21, 706–713.
Hajek, A.E. and Soper, R.S. (1992) Temporal dynamics of Entomophaga maimaiga after death of gypsy
moth (Lepidoptera: Lymantriidae) larval hosts. Environmental Entomology 21, 129–135.
Hajek, A.E., Humber, R.A., Elkinton, J.S., May, B., Walsh, S.R.A. and Silver, J.C. (1990a) Allozyme and
RFLP analyses confirm Entomophaga maimaiga responsible for 1989 epizootics in North American
gypsy moth populations. Proceedings of the National Academy of Sciences of the USA 87, 6979–6982.
Hajek, A.E., Carruthers, R.I. and Soper, R.S. (1990b) Temperature and moisture relations of sporulation
and germination by Entomophaga maimaiga (Zygomycetes: Entomophthoraceae), a fungal pathogen
of Lymantria dispar (Lepidoptera: Lymantriidae). Environmental Entomology 19, 85–90.
Hajek, A.E., Larkin, T.S., Carruthers, R.I. and Soper, R.S. (1993) Modeling the dynamics of Entomophaga
maimaiga (Zygomycetes: Entomophthorales) epizootics in gypsy moth (Lepidoptera: Lymantriidae)
populations. Environmental Entomology 22, 1172–1187.
Hajek, A.E., Humber, R.A. and Elkinton, J.S. (1995) Mysterious origin of Entomophaga maimaiga in North
America. American Entomologist 41, 31–42.
Hajek, A.E., Elkinton, J.S. and Witcosky, J.J. (1996) Introduction and spread of the fungal pathogen
Entomophaga maimaiga (Zygomycetes: Entomophthorales) along the leading edge of gypsy moth
(Lepidoptera: Lymantriidae) spread. Environmental Entomology 25, 1235–1247.
Hall, P.J. (comp.) (1994) Forest Insect and Disease Conditions in Canada 1992. Forest Insect and Disease
Survey, Forestry Canada, Ottawa, Ontario, 120 pp.
Hall, P.J. (comp.) (1995) Forest Insect and Disease Conditions in Canada 1993. Forest Insect and Disease
Survey, Forestry Canada, Ottawa, Ontario, 133 pp.
Hall, P.J. (comp.) (1996) Forest Insect and Disease Conditions in Canada 1994. Forest Insect and Disease
Survey, Forestry Canada, Ottawa, Ontario, 112 pp.
Halleran, M. (1990) Forest vegetation management and the politics of environment. The Forestry Chronicle
66, 369–371.
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 246

246 I.S. Otvos

Hamel, D.R. (1977) The effects of Bacillus thuringiensis on parasitoids of the western spruce budworm,
Choristoneura occidentalis (Lepidoptera: Tortricidae), and the spruce coneworm, Dioryctria reniculel-
loides (Lepidoptera: Pyralidae), in Montana. The Canadian Entomologist 109, 1409–1415.
Hansen, E.M. and Lewis, K.J. (eds) (1997) Compendium of Conifer Diseases. American Phytopathological
Society Press, St Paul, Minnesota, 101 pp.
Harris, J.W.E., Alfaro, R.I., Dawson, A.F. and Brown, R.G. (1985a) The Western Spruce Budworm in British
Columbia 1909–1983. Information Report BC-X-257, Canadian Forestry Service, Pacific Forestry
Centre, Victoria, British Columbia, 32 pp.
Harris, P. (1984) Current approaches to biological control of weeds. In: Kelleher, J.S. and Hulme, M.A.
(eds) Biological Control Programmes Against Weeds and Insects in Canada 1969–1980. Commonwealth
Agricultural Bureaux, Slough, UK, pp. 95–103.
Harris, P. and Shamoun, S.F. (2002) Biological control of weeds in Canada: results, opportunities, and
constraints. In: Claudia, R., Nantel, P. and Muckle-Jeffs, E. (eds) Alien Invaders in Canada’s Waters,
Wetlands, and Forests. Canadian Forest Service, Natural Resources Canada, Ottawa, Ontario,
pp. 291–302.
Hewitt, G.C. (1916) The introduction and establishment in Canada of the natural enemies of the brown-
tail and gypsy moth. The Agricultural Gazette of Canada 3, 20–21.
Hoy, M.A. (1976) Establishment of gypsy moth parasitoids in North America: an evaluation of possible
reasons for establishment or non-establishment. In: Anderson, J.F. and Kaya, H.K. (eds) Perspectives
in Forest Entomology. Academic Press, New York, pp. 215–232.
Hughes, K.M. and Addison, R.B. (1970) Two nuclear polyhedrosis viruses of the Douglas-fir tussock
moth. Journal of Invertebrate Pathology 16, 196–204.
Hulme, M.A. (1988) The recent Canadian record in applied biological control of forest insect pests. The
Forestry Chronicle 64, 27–31.
Humble, L. and Stewart, A.J. (1994) Gypsy Moth. Forest Pest Leaflet 75, Canadian Forest Service and
British Columbia Ministry of Forests, Victoria, British Columbia, 8pp.
Humphreys, P. (1986) Pesticide Use in British Columbia Forestry 1985. Forest Service Internal Report
PM–PB–26, British Columbia Ministry of Forests and Lands, Victoria, British Columbia, 31 pp.
Humphreys, P. (1990) Pesticide Use in British Columbia Forestry 1989. Forest Service Internal Report
PM–PB–46, British Columbia Ministry of Forests, Victoria, British Columbia, 73 pp.
Ilnytzky, S., McPhee, J.R. and Cunningham, J.C. (1977) Comparison of field-propagated nuclear polyhe-
drosis virus from Douglas-fir tussock moth with laboratory virus. Fisheries and Environment Canada,
Forestry Service, Bi-monthly Research Notes 33, 5–6.
Ives, W.G.H. and Rentz, C.L. (1993) Factors Affecting the Survival of Immature Lodgepole Pine in the Foothills
of West-Central Alberta. Information Report NOR-X-330, Canadian Forest Service, Northwest Region,
Northern Forestry Centre, Edmonton, Alberta, 49 pp.
Jobidon, R. (1991a) Some future directions for biologically based vegetation control in forestry. The
Forestry Chronicle 67, 514–519.
Jobidon, R. (1991b) Potential use of bialaphos, a microbially produced phytotoxin, to control red raspberry
in forest plantations and its effect on black spruce. Canadian Journal of Forest Research 21, 489–497.
Jobidon, R., Thibault, J.R. and Fortin, J.A. (1989) Phytotoxic effect of barley oat and wheat-straw mulches
in eastern Quebec forest plantations 1. Effects on red raspberry (Rubus idaeus). Forest Ecology and
Management 29, 277–294.
Jobin, L. (1995) Gypsy moth, Lymantria dispar. In: Armstrong, J.A. and Ives, W.G.H. (eds) Forest Insect
Pests in Canada. Natural Resources Canada, Canadian Forest Service, Ottawa, Ontario, pp. 133–139.
Julien, M.H. and Griffiths, M.W. (1998) Biological Control of Weeds: a World Catalogue of Agents and their
Target Weeds. CAB International, Wallingford, UK, 223 pp.
Keena, M.A., Grinberg, P.S. and Wallner, W.E. (1995) Asian gypsy moth genetics: biological consequences
of hybridization [abstract]. In: Fosbroke, S.L.C. and Gottschalk, K.W. (eds) Proceedings: U.S.
Department of Agriculture Interagency Gypsy Moth Research Forum 1995, January 17–20, 1995, Loews
Annapolis Hotel, Annapolis, Maryland. General Technical Report NE-213, USDA Forest Service,
Northeastern Forest Experiment Station, Radnor, Pennsylvania, p. 80.
Kelleher, J.S. and Hulme, M.A. (eds) (1984) Biological Control Programmes Against Weeds and Insects in
Canada 1969–1980. Commonwealth Agricultural Bureaux, Slough, UK, 410 pp.
Kettela, E.G. (1983) A Cartographic History of Spruce Budworm Defoliation from 1967 to 1981 in Eastern North
America. Information Report DPC-X-14, Canadian Forestry Service, Maritimes Research Centre,
Fredericton, New Brunswick, 8 pp.
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 247

IPM in Forestry 247

Kettela, E.G. (1995) Attempts to develop strategies to control spruce budworm, Choristoneura fumiferana,
moth populations by spraying. In: Armstrong, J.A. and Ives, W.G.H. (eds) Forest Insect Pests in
Canada. Natural Resources Canada, Canadian Forest Service, Ottawa, Ontario, pp. 113–117.
Kinghorn, J.M., Fisher, R.A., Angus, T.A. and Heimpel, A.M. (1961) Aerial spray trials against the black-
headed budworm in British Columbia. Department of Forestry, Forest Entomology and Pathology
Branch, Bi-monthly Progress Report 17, 3–4.
Leonard, D.E. (1981) Bioecology of the gypsy moth. In: Doane, C.C. and McManus, M.L. (eds) The Gypsy
Moth: Research Toward Integrated Pest Management. Technical Bulletin 1584, Forest Service, US
Department of Agriculture, Washington, DC, pp. 9–29.
Leonard, D.S. and Sharov, A.A. (1995) Slow the spread project update: developing a process for evalua-
tion. In: Fosbroke, S.L.C. and Gottschalk, K.W. (eds) Proceedings: US Department of Agriculture
Interagency Gypsy Moth Research Forum 1995, January 17–20, 1995, Annapolis, Maryland. General
Technical Report NE-213, Northeastern Forest Experiment Station, USDA Forest Service, Radnor,
Pennsylvania, pp. 82–85.
Leonhardt, B.A., Mastro, V.C., Leonard, D.S., McLane, W., Reardon, R.C. and Thorpe, K.W. (1996) Control
of low-density gypsy moth (Lepidoptera: Lymantriidae) populations by mating disruption with
pheromone. Journal of Chemical Ecology 22, 1255–1272.
Leuschner, W.A., Young, J.A., Waldon, S.A. and Ravlin, F.W. (1996) Potential benefits of slowing the
gypsy moth’s spread. Southern Journal of Applied Forestry 20, 65–73.
Lewis, F.B. (1981) Registration and cost effectiveness. In: Doane, C.C. and McManus, M.L. (eds) The
Gypsy Moth: Research Toward Integrated Pest Management. Technical Bulletin 1584, Forest Service, US
Department of Agriculture, Washington, DC, pp. 514–515.
Liebhold, A. and McManus, M. (1999) The evolving use of insecticides in gypsy moth management.
Journal of Forestry 97, 20–23.
Liebhold, A., Mastro, V. and Schaefer, P.W. (1989) Learning from the legacy of Léopold Trouvelot. Bulletin
of the Entomological Society of America 35, 20–22.
Liebhold, A.M., Halverson, J.A. and Elmes, G.A. (1992) Gypsy moth invasion in North America: a quanti-
tative analysis. Journal of Biogeography 19, 513–520.
Liebhold, A.M., MacDonald, W.L., Bergdahl, D. and Mastro, V.C. (1995) Invasion by Exotic Forest Pests: a
Threat to Forest Ecosystems. Forest Science Monograph 30, Society of American Foresters, Bethesda,
Maryland, 49 pp.
Liebhold, A.M., Gottschalk, K.W., Mason, D.A. and Bush, R.R. (1997) Forest susceptibility to the gypsy
moth. Journal of Forestry 95, 20–24.
Logie, R.R. (1975) Effects of aerial spraying of DDT on salmon populations of the Miramichi River. In:
Prebble, M.L. (ed.) Aerial Control of Forest Insects in Canada. Department of the Environment, Ottawa,
Canada, pp. 293–300.
Lowe, J.J., Power, K. and Gray, S.L. (1996) Canada’s Forest Inventory 1991: the 1994 Version. An Addendum to
Canada’s Forest Inventory 1991. Information Report BC-X-362E, Natural Resources Canada, Canadian
Forest Service, Pacific Forestry Centre, Victoria, British Columbia, 23 pp.
Maclauchlan, L.E. and Brooks, J.E. (eds) (1994) Strategies and Tactics for Managing the Mountain Pine Beetle,
Dendroctonus ponderosae. British Columbia Forest Service, Kamloops Region, Forest Health,
Kamloops, British Columbia, 60 pp.
MacLean, D.A. (1980) Vulnerability of fir-spruce stands during uncontrolled spruce budworm outbreaks:
a review and discussion. The Forestry Chronicle 56, 213–222.
Malakar, R., Elkinton, J.S., Hajek, A.E. and Burand J.P. (1999) Within-host interactions of Lymantria dispar
(Lepidoptera: Lymantriidae) nucleopolyhedrosis virus and Entomophaga maimaiga (Zygomycetes:
Entomophthorales). Journal of Invertebrate Pathology 73, 91–100.
Mallet, K.I., Macey, D.E. and Winder, R.S. (2002) Calamagrostis canadensis (Michaux) Palisot de Beauvois,
Marsh Reed Grass (Poaceae). In: Mason, P.G. and Huber, J.T. (eds) Biological Control Programmes in
Canada, 1981–2000. CAB International, Wallingford, UK, pp. 298–301.
Marsden, J.S., Martin, G.E., Parham, D.J., Ridsill-Smith, T.J. and Johnston, B.G. (1980) Returns on
Australian Agricultural Research: Joint IAC-CSIRO Benefit Cost Study of the CSIRO Division of
Entomology. Commonwealth Scientific and Industrial Research Organization, Canberra, Australia,
107 pp.
Martin, P.A.W. and Travers, R.S. (1989) Worldwide abundance and distribution of Bacillus thuringiensis
isolates. Applied and Environmental Microbiology 55, 2437–2442.
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 248

248 I.S. Otvos

Mason, C.J. and McManus, M.L. (1981) Larval dispersal of the gypsy moth. In: Doane, C.C. and
McManus, M.L. (eds) The Gypsy Moth: Research Toward Integrated Pest Management. Technical Bulletin
1584, Forest Service, US Department of Agriculture, Washington, DC, pp. 161–202.
Mason, P.G. and Huber, J.T. (eds) (2002) Biological Control Programmes in Canada, 1981–2000. CAB
International, Wallingford, UK, 583 pp.
Mason, P.G., Huber, J.T. and Boyetchko, S.M. (2002) Introduction. In: Mason, P.G. and Huber, J.T. (eds)
Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK, pp. xi–xiv.
Mattson, W.J., Niemela, P., Millers, I. and Inguanzo, Y. (1994) Immigrant Phytophagous Insects on Woody
Plants in the United States and Canada: An Annotated List. General Technical Report NC-169, Forest
Service, US Department of Agriculture, North Central Forest Experiment Station, St Paul,
Minnesota, 27 pp.
McDonald, G.I., Martin, N.E. and Harvey, A.E. (1987) Armillaria in the Northern Rockies: Pathogenicity and
Host Susceptibility on Pristine and Disturbed Sites. Research Note INT-371, Forest Service, US
Department of Agriculture, Intermountain Research Station, Ogden, Utah, 3 pp.
McDonald, P.M. and Fiddler, G.O. (1996) Mulching: a persistent technique for weed suppression. In:
Comeau, P.G., Harper, G.J., Blache, M.E., Boateng, J.O. and Gilkeson, L.A. (eds) Integrated Forest
Vegetation Management: Options and Applications: Proceedings of the Fifth British Columbia Forest
Vegetation Management Workshop, November 29–30, 1993, Richmond, British Columbia. Forest Resource
Development Agreement Report No. 251, Canadian Forest Service and British Columbia Ministry of
Forests, Victoria, British Columbia, pp. 51–58.
McFadden, M.W. and McManus, M.E. (1991) An insect out of control? The potential for spread and estab-
lishment of the gypsy moth in new forest areas in the United States. In: Baranchikov, Y.N., Mattson,
W.J., Hain, F.P. and Payne, T.L. (eds) Forest Insect Guilds: Patterns of Interaction with Host Trees:
Proceedings of a Joint IUFRO Working Party Symposium, Abakan, Siberia, USSR, August 13–17, 1989.
General Technical Report NE-153, Forest Service, US Department of Agriculture, Northeastern
Forest Experiment Station, Radnor, Pennsylvania, pp. 172–186.
McGugan, B.M. and Coppel, H.C. (1962) Part II: Biological control of forest insects, 1910–1958. In:
McLeod, J.H., McGugan, B.M. and Coppel, H.C. (compilers) A Review of the Biological Control
Attempts Against Insects and Weeds in Canada. Commonwealth Agricultural Bureaux, Slough, UK,
pp. 35–127.
McLeod, J.H. (1962) Part I: Biological control of pests of crops, fruit trees, ornamentals, and weeds in
Canada up to 1959. In: McLeod, J.H., McGugan, B.M. and Coppel, H.C. (compilers) A Review of the
Biological Control Attempts Against Insects and Weeds in Canada. Commonwealth Agricultural
Bureaux, Slough, UK, pp. 1–33.
McManus, M.L. and McIntyre, T. (1981) Introduction: historical chronology. In: Doane, C.C. and
McManus, M.L. (eds) The Gypsy Moth: Research Toward Integrated Pest Management. Technical Bulletin
1584, Forest Service, US Department of Agriculture, Washington, DC, pp. 1–7.
McMullen, L.H., Safranyik, L. and Linton, D.A. (1986) Suppression of Mountain Pine Beetle Infestations in
Lodgepole Pine Forests. Information Report BC-X-276, Canadian Forestry Service, Pacific Forestry
Centre, Victoria, British Columbia, 20 pp.
Miller, C.A. (1957) A technique for estimating the fecundity of natural populations of the spruce bud-
worm. Canadian Journal of Zoology 35, 1–13.
Miller, C.A., Kettela, E.G. and McDougall, G.A. (1971) A Sampling Technique for Overwintering Spruce
Budworm and its Applicability to Population Surveys. Information Report M-X-25, Department of
Fisheries and Forestry, Canadian Forest Service, Maritimes Forest Research Centre, Fredericton,
New Brunswick, 11 pp.
Miller, J.C. (1990) Field assessment of the effects of a microbial pest control agent on nontarget
Lepidoptera. American Entomologist 36, 135–139.
Miller, J.D. and Lindsay, B.E. (1993) Willingness to pay for a state gypsy moth control program in New
Hampshire: a contingent valuation case study. Journal of Economic Entomology 86, 828–837.
Mills, N.J. and Nealis, V.G. (1992) European field collections and Canadian releases of Ceranthia samaren-
sis (Dipt.: Tachinidae), a parasitoid of the gypsy moth. Entomophaga 37, 181–191.
Mitchell, R.G., Waring, R.H. and Pitman, G.B. (1983) Thinning lodgepole pine increases tree vigor and
resistance to mountain pine beetle. Forest Science 29, 204–211.
Montgomery, M.E. and Wallner, W.E. (1988) The gypsy moth: a westward migrant. In: Berryman, A.A.
(ed.) Dynamics of Forest Insect Populations: Patterns, Causes, Implications. Plenum Press, New York,
pp. 253–275.
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 249

IPM in Forestry 249

Moody, B.H. (comp.) (1993a) Forest Insect and Disease Conditions in Canada 1991. Forest Insect and Disease Survey,
Forestry Canada, Ottawa, Ontario, 99 pp.
Moody, B.H. (comp.) (1993b) Forest Insect and Disease Conditions in Canada 1990. Forest Insect and Disease
Survey, Forestry Canada, Ottawa, Ontario, 115 pp.
Morris, M.J. (1991) The use of plant pathogens for biological weed control in South Africa. Agriculture,
Ecosystems and Environment 37, 239–255.
Morris, M.J. (1997) Impact of the gall-forming rust fungus, Uromycladium tepperianum on the invasive tree Acacia
saligna in South Africa. Biological Control 10, 75–82.
Morris, M.J., Wood, A.R. and den Breeyen, A. (1998) Development and registration of a fungal inoculant to pre-
vent re-growth of cut wattle tree stumps in South Africa. In: Burge, M.N. (ed.) IV International Bioherbicides
Workshops – Programmes and Abstracts, 6–7 August, 1998. University of Strathclyde, Glasgow, p. 15.
Morris, O.N. (1963) The natural and artificial control of the Douglas-fir tussock moth, Orgyia pseudotsugata
McDunnough, by a nuclear-polyhedrosis virus. Journal of Insect Pathology 5, 401–414.
Morris, O.N. (1983) Comparative efficacy of Thuricide 16B and Dipel 88 against the spruce budworm,
Choristoneura fumiferana (Lepidoptera: Tortricidae) in balsam fir stands. The Canadian Entomologist 115,
1001–1006.
Morris, R.F. (1954) A sequential sampling technique for spruce budworm egg surveys. Canadian Journal of
Zoology 32, 302–313.
Morris, R.F. (ed.) (1963) The Dynamics of Epidemic Spruce Budworm Populations. Memoirs of the Entomological
Society of Canada 31, Ottawa, Ontario, Canada, 332pp.
Morrison, D. and Mallett, K. (1996) Silvicultural management of armillaria root disease in western Canadian
forests. Canadian Journal of Plant Pathology 18, 194–199.
Morrison, D.J., Merler, H. and Norris, D. (1992) Detection, Recognition and Management of Armillaria and Phellinus
Root Diseases in the Southern Interior of British Columbia. Forest Resource Development Agreement Report 179,
Canadian Forest Service and British Columbia Ministry of Forests, Victoria, British Columbia, 25 pp.
Morrison, D.J., Wallis, G.W. and Weir, L.C. (1988) Control of Armillaria and Phellinus Root Diseases: 20-year Results
from the Skimikin Stump Removal Experiment. Information Report BC-X-302, Canadian Forestry Service,
Pacific Forestry Centre, Victoria, British Columbia, 16 pp.
Mott, D.G., Angus, T.A., Heimpel, A.M. and Fisher, R.A. (1961) Aerial spraying of Thuricide against the spruce
budworm in New Brunswick. Department of Forestry, Forest Entomology and Pathology Branch, Bi-monthly
Progress Report 17, 2.
Nealis, V.G. (2002) Gypsy moth in Canada: case study of an invasive insect. In: Claudia, R., Nantel, P. and
Muckle-Jeffs, E. (eds) Alien Invaders in Canada’s Waters, Wetlands and Forests. Natural Resources Canada,
Science Branch, Canadian Forest Service, Ottawa, Ontario, pp. 151–159.
Nealis, V.G. and Quednau, F.W. (1996) Canadian field releases and overwinter survival of Ceranthia samarensis
(Villeneuve) (Diptera: Tachinidae) for biological control of the gypsy moth, Lymantria dispar (L.)
(Lepidoptera: Lymantriidae). Proceedings of the Entomological Society of Ontario 127, 11–20.
Nealis, V.G. and van Frankenhuyzen, K. (1990) Interactions between Bacillus thuringiensis Berliner and Apanteles
fumiferanae Vier. (Hymenoptera: Braconidae), a parasitoid of the spruce budworm, Choristoneura fumiferana
(Clem.) (Lepidoptera: Tortricidae). The Canadian Entomologist 122, 585–594.
Nealis, V.G., Roden, P.M. and Ortiz, D.A. (1999) Natural mortality of the gypsy moth along a gradient of infesta-
tion. The Canadian Entomologist 131, 507–519.
Nealis, V.G., Carter, N., Kenis, M., Quednau, F.W. and van Frankenhuyzen, K. (2002) Lymantria dispar (L.), gypsy
moth (Lepidoptera: Lymantriidae). In: Mason, P.G. and Huber, J.T. (eds) Biological Control Programmes in
Canada, 1981–2000. CAB International, Wallingford, UK, pp. 159–168.
Niemela, P. and Mattson, W.J. (1996) Invasion of North American forests by European phytophagous insects –
legacy of the European crucible? BioScience 46, 741–753.
Nigam, P.C. (1975) Chemical insecticides. In: Prebble, M.L. (ed.) Aerial Control of Forest Insects in Canada.
Department of the Environment, Ottawa, Canada, pp. 8–24.
Nigam, P.C. (1980) Use of chemical insecticides against the spruce budworm in eastern Canada. CANUSA
Newsletter 11, 1–3.
Niwa, C.G., Stelzer, M.J. and Beckwith, R.C. (1987) Effects of Bacillus thuringiensis on parasites of western spruce
budworm (Lepidoptera: Tortricidae). Journal of Economic Entomology 80, 750–753.
Oleskevich, C., Shamoun, S.F., Vesonder, R.F. and Punja, Z.K. (1998) Evaluation of Fusarium avenaceum and other
fungi for potential as biological control agents of invasive Rubus species in British Columbia. Canadian
Journal of Plant Pathology 20, 12–18.
Otvos, I.S. (1973) Biological Control Agents and Their Role in the Population Fluctuation of the Eastern Hemlock Looper
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 250

250 I.S. Otvos

in Newfoundland. Information Report N-X-102, Environment Canada, Newfoundland Forest

Research Centre, St John’s, Newfoundland, 34 pp.
Otvos, I.S. and Raske, A.G. (1980a) The Effects of Fenitrothion, Matacil, and Bacillus thuringiensis plus
Orthene on Larval Parasites of the Spruce Budworm. Information Report N-X-184, Canadian Forestry
Service, Newfoundland Forest Research Centre, St John’s, Newfoundland, 24 pp.
Otvos, I.S. and Raske, A.G. (1980b) Effects of Aerial Application of Matacil on Larval and Pupal Parasites of the
Eastern Spruce Budworm, Choristoneura fumiferana (Lepidoptera: Tortricidae). Information Report N-
X-189, Canadian Forest Service, Newfoundland Forest Research Centre, St John’s, Newfoundland,
12 pp.
Otvos, I.S. and Vanderveen, S. (1993) Environmental Report and Current Status of Bacillus thuringiensis var.
kurstaki Use for Control of Forest and Agricultural Insect Pests. Joint report by Forestry Canada, Pacific
Forestry Centre and British Columbia Ministry of Forests, Victoria, British Columbia, 81 pp.
Otvos, I.S., MacLeod, D.M. and Tyrrell, D. (1973) Two species of Entomophthora pathogenic to the eastern
hemlock looper (Lepidoptera: Geometridae) in Newfoundland. Canadian Entomologist 105,
1435–1441.
Otvos, I.S., Cunningham, J.C. and Friskie, L.M. (1987) Aerial application of nuclear polyhedrosis virus
against Douglas-fir tussock moth, Orgyia pseudotsugata (McDunnough) (Lepidoptera: Lymantriidae):
I. Impact in the year of application. The Canadian Entomologist 119, 697–706.
Otvos, I.S., Cunningham, J.C. and Kaupp, W.J. (1989) Aerial application of two baculoviruses against the
western spruce budworm (Lepidoptera: Tortricidae) in British Columbia. The Canadian Entomologist
121, 209–217.
Otvos, I.S., Cunningham, J.C. and Shepherd, R.F. (1995) Douglas-fir tussock moth, Orgyia pseudotsugata.
In: Armstrong, J.A. and Ives, W.G.H. (eds) Forest Insect Pests in Canada. Natural Resources Canada,
Canadian Forest Service, Ottawa, Ontario, pp. 127–132.
Pearce, P.A. (1975) Effects on birds. In: Prebble, M.L. (ed.) Aerial Control of Forest Insects in Canada.
Department of the Environment, Ottawa, Canada, pp. 306–313.
Pendl, F. and D’Anjou, B. (1990) Effect of Manual Treatment Timing on Red Alder Regrowth and Conifer
Response. Forest Resource Development Agreement Report 112, Canadian Forestry Service and
British Columbia Ministry of Environment, Victoria, British Columbia, 21 pp.
Perlman, F.D., Press, E., Googins, J.A., Malley, A. and Poarea, H. (1976) Tussockosis: reactions to Douglas-
fir tussock moth. Annals of Allergy 36, 302–307.
Podgwaite, J.D. (1999) Gypchek: biological insecticide for the gypsy moth. Journal of Forestry 97, 16–19.
Podgwaite, J.D. and Campbell, R.W. (1972) The disease complex of the gypsy moth. II. Aerobic bacterial
pathogens. Journal of Invertebrate Pathology 20, 303–308.
Prasad, R. (1992) Some aspects of biological control of weeds in forestry. In: Richardson, R.G. (compiler)
Proceedings of the First International Weed Control Congress, February 17–21, 1992, Monash University,
Melbourne, Australia, Vol. 2. Weed Science Society of Victoria Inc., Melbourne, Australia,
pp. 398–402.
Prasad, R. (1996) Development of bioherbicides for integrated weed management in forestry. In: Brown,
H. (ed.) Proceedings, Second International Weed Control Congress, Copenhagen, Denmark, June 25–28
1996. Department of Weed Control and Pesticide Ecology, Slagelse, Denmark, pp. 1197–1203.
Prasad, R. (2002a) Cytisus scoparius (L.) Link, Scotch Broom (Fabaceae). In: Mason, P.G. and Huber, J.T.
(eds) Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK,
pp. 343–345.
Prasad, R. (2002b) Ulex europaeus L., Gorse (Fabaceae). In: Mason, P.G. and Huber, J.T. (eds) Biological
Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK, pp. 431–433.
Prasher, D. and Mastro, V.C. (1995) Genotype analyses of 1994 port specimens. In: Hilburn, D., Johnson,
K.J.R. and Mudge, A.D. (eds) Proceedings of the 1994 Annual Gypsy Moth Review: Held at the Portland
Hilton, Portland, Oregon, October 30-November 2, 1994. US National Gypsy Moth Management Board,
Salem, Massachusetts, pp. 61–63.
Prebble, M.L. (ed.) (1975) Aerial Control of Forest Insects in Canada. Environment Canada, Ottawa, Ontario,
330 pp.
Ravensberg, W.J. (1998) BioChon: Effective Biological and Environmentally Friendly Product. Pest Leaflet,
Koppert Biological Systems, The Netherlands, 2 pp.
Reardon, R.C. (1981) Summary. In: Doane, C.C. and McManus, M.L. (eds) The Gypsy Moth: Research
Toward Integrated Pest Management. Technical Bulletin 1584, Forest Service, US Department of
Agriculture, Washington, DC, pp. 412–413.
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 251

IPM in Forestry 251

Reardon, R.C. (1991) Appalachian gypsy-moth integrated pest-management project. Forest Ecology and
Management 39, 107–112.
Reardon, R. and Hajek, A. (1993) Entomophaga maimaiga in North America: a Review. AIPM Technology
Transfer, US Department of Agriculture Forest Service, Northeastern Area, Morgantown, West
Virginia, 22 pp.
Reardon, R.C., Johnson, D.R., Narog, M.G., Banash, S.E. and Hubbard, H.B. Jr (1982) Efficacy of two for-
mulations of Bacillus thuringiensis on populations of spruce budworm (Lepidoptera: Tortricidae) on
balsam fir in Wisconsin. Journal of Economic Entomology 75, 509–514.
Reardon, R., McManus, M., Kolodny-Hirsch, D., Tichenor, R., Raupp, M., Schwalbe, C., Webb, R. and
Meckley, P. (1987) Development and implementation of a gypsy moth integrated pest management
program. Journal of Arboriculture 13, 209–216.
Reardon, R.C., Dubois, N.R. and McLane, W. (1994) Bacillus thuringiensis for Managing Gypsy Moth: a
Review. FHM-NC-01–94, National Centre of Forest Health Management, US Department of
Agriculture Forest Service, Morgantown, West Virginia, 32 pp.
Reardon, R.C., Leonard, D.S., Mastro, V.C., Leonhardt, B.A., McLane, W., Talley, S., Thorpe, K.W. and
Webb, R.E. (1998) Using Mating Disruption to Manage Gypsy Moth: A Review. USDA Forest Service,
Morgantown, West Virginia, 85 pp.
Reeks, W.A. and Cameron, J.M. (1971) Current approach to biological control of forest insects. In:
Canadian Department of Agriculture and Canadian Department of Fisheries and Forestry (ed.)
Biological Control Programmes Against Insects and Weeds in Canada 1959–1968. Technical
Communication No. 4, Commonwealth Institute of Biological Control, Commonwealth Agricultural
Bureaux, Slough, UK, pp. 105–113.
Regniere, S. and Lysyk, T.J. (1995) Population dynamics of the spruce budworm, Choristoneura fumiferana.
In: Armstrong, J.A. and Ives, W.G.H. (eds) Forest Insect Pests in Canada. Natural Resources Canada,
Canadian Forest Service, Ottawa, Ontario, pp. 95–105.
Russell, K., Johnsey, R. and Edmonds, R. (1986) Disease and insect management for Douglas-fir. In:
Oliver, C.D., Hanley, D.P. and Johnson, J.A. (eds) Douglas-fir: Stand Management for the Future.
Contribution No. 55, College of Forest Resources, Institute of Forest Resources, University of
Washington, Seattle, Washington, pp. 189–207.
Sabrosky, C.W. and Reardon, R.C. (1976) Tachinid Parasites of the Gypsy Moth, Lymantria dispar, with Keys
to Adults and Puparia. Miscellaneous Publications of the Entomological Society of America 10,
Lanham, Maryland, 126 pp.
Safranyik, L., Shrimpton, D.M. and Whitney, H.S. (1974) Management of Lodgepole Pine to Reduce Losses
from the Mountain Pine Beetle. Forestry Technical Report 1, Canadian Forestry Service, Pacific
Forestry Centre, Victoria, British Columbia, 24 pp.
Safranyik, L., Simmons, C. and Barclay, H.J. (1990) A Conceptual Model of Spruce Beetle Population
Dynamics. Information Report BC-X-316, Forestry Canada, Pacific Forestry Centre, Victoria, British
Columbia, 13 pp.
Sanders, C.J. (1988) Monitoring spruce budworm population density with sex pheromone traps. Canadian
Entomologist 120, 175–183.
Sanders, C.J., Stark, R.W., Mullins, E.J. and Murphy, J. (eds) (1985) Recent Advances in Spruce Budworms
Research: Proceedings of CANUSA Spruce Budworms Research Symposium, Bangor, Maine, September
16–20, 1984. Canadian Forestry Service, Ottawa, Ontario, 527 pp.
Sartwell, C. and Dolph, R.E. Jr (1976) Silvicultural and Direct Control of Mountain Pine Beetle in Second-
Growth Ponderosa Pine. Research Note PNW-268, US Department of Agriculture Forest Service,
Pacific Northwest Forest and Range Experiment Station, Portland, Oregon, 8 pp.
Scheepens, P.C. and Hoogerbrugge, A. (1989) Control of Prunus serotina in forests with the endemic fun-
gus Chondrostereum purpureum. In: Delfosse, E.S. (ed.) Proceedings, VII International Symposium on
Biological Control of Weeds, March 6–11, 1988, Rome, Italy. Commonwealth Scientific and Industrial
Research Organization Publications, East Melbourne, Australia, pp. 545–551.
Schwalbe, C.P. (1981) Disparlure-baited traps for survey and detection. In: Doane, C.C. and McManus,
M.L. (eds) The Gypsy Moth: Research Toward Integrated Pest Management. Technical Bulletin 1584,
Forest Service, US Department of Agriculture, Washington, DC, pp. 542–548.
Shamoun, S.F. (2000) Application of biological control to vegetation management in forestry. In: Spence,
N.R. (ed.) Proceedings of the X International Symposium on Biological Control of Weeds, 4–14 July 1999.
Montana State University, Bozeman, Montana, pp. 87–96.
Shamoun, S.F. and DeWald, L.E. (2002) Management strategies for dwarf mistletoes: biological, chemical,
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 252

252 I.S. Otvos

and genetic approaches. In: Geils, B.W., Tovar, J.C. and Moody, B. (technical coordinators) Mistletoes
of North American Conifers. US Department of Agriculture Forest Service General Technical Report
RMRS-GTR-98, US Department of Agriculture, Rocky Mountain Research Station, Fort Collins,
Colorado, pp. 75–82.
Shamoun, S.F. and Hintz, W.E. (1998a) Development and registration of Chondrostereum purpureum as a
mycoherbicide for hardwood weeds in conifer reforestation sites and utility rights-of-way. In:
Burge, M.N. (ed.) IV International Bioherbicide Workshop – Programme and Abstracts, 6–7 August, 1998.
University of Strathclyde, Glasgow, p. 14.
Shamoun, S.F. and Hintz, W.E. (1998b) Development of Chondrostereum purpureum as a biological control
agent for red alder in utility rights-of-way. In: Wagner, R.G. and Thompson D.G. (compilers) Third
International Conference on Forest Vegetation Management, Popular Summaries. Forest Research
Information Paper No. 141, Ontario Ministry of Natural Resources, Ontario Forest Research
Institute, pp. 308–310.
Shamoun, S.R., Macey, D.E., Prasad, R. and Winder, R.S. (2002) Acer, Alnus, Betula, Populus and Prunus
spp., weedy hardwood trees (Aceraceae, Betulaceae, Salicaceae, Rosaceae). In: Mason, P.G. and
Huber, J.T. (eds) Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford,
UK, pp. 283–289.
Sharov, A.A. and Liebhold, A.M. (1998a) Bioeconomics of managing the spread of exotic pest species
with barrier zones. Ecological Applications 8, 833–845.
Sharov, A.A. and Liebhold, A.M. (1998b) Model of slowing the spread of gypsy moth (Lepidoptera:
Lymantriidae) with a barrier zone. Ecological Applications 8, 1170–1179.
Sharov, A.A. and Liebhold, A.M. (1998c) Quantitative analysis of gypsy moth spread in the Central
Appalachians. In: Baumgartner, J., Brandmayr, P. and Manly, B.F.J. (eds) Population and Community
Ecology for Insect Management and Conservation: Proceedings of the Ecology and Population Dynamics
Section of the 20th International Congress of Entomology, Florence, Italy, 25–31 August, 1996. A.A.
Balkema, Rotterdam, pp. 99–110.
Sharov, A.A., Liebhold, A.M. and Roberts, E.A. (1998) Optimizing the use of barrier zones to slow the
spread of gypsy moth (Lepidoptera: Lymantriidae) in North America. Journal of Economic
Entomology 91, 165–174.
Sharov, A.A., Leonard, D., Liebhold, A.M., Roberts, E.A. and Dickerson, W. (2002a) ‘Slow the Spread’: a
national program to contain the gypsy moth. Journal of Forestry 100, 30–36.
Sharov, A.A., Leonard, D., Liebhold, A.M. and Clemens, N.S. (2002b) Evaluation of preventative treat-
ments in low-density gypsy moth populations using pheromone traps. Journal of Economic
Entomology 95, 1205–1215.
Sharrow, S.H., Leininger, W.C. and Rhodes, B. (1989) Sheep grazing as silvicultural tool to suppress
brush. Journal of Range Management 42, 2–4.
Shaw, C.G. III and Calderon, S. (1977) Impact of Armillaria root rot in plantations of Pinus radiata estab-
lished on sites converted from indigenous forest. New Zealand Journal of Forest Science 7, 359–373.
Shepherd, R.F. and Otvos, I.S. (1986) Pest Management of Douglas-fir Tussock Moth: Procedures for Insect
Monitoring, Problem Evaluation and Control Actions. Information Report BC-X-270, Canadian Forestry
Service, Pacific Forestry Centre, Victoria, British Columbia, 14 pp.
Shepherd, R.F., Otvos, I.S. and Chorney, R.J. (1984a) Pest management of the Douglas-fir tussock moth
(Lepidoptera: Lymantriidae): a sequential sampling method to determine egg mass density. The
Canadian Entomologist 116, 1041–1049.
Shepherd, R.F., Otvos, I.S., Chorney, R.J. and Cunningham, J.C. (1984b) Pest management of the Douglas-
fir tussock moth (Lepidoptera: Lymantriidae): prevention of a Douglas-fir tussock moth outbreak
through early treatment with a nuclear polyhedrosis virus by ground and aerial applications. The
Canadian Entomologist 116, 1533–1542.
Shepherd, R.F., Gray, T.G., Chorney, R.J. and Daterman, G.E. (1985) Pest management of the Douglas-fir
tussock moth: monitoring endemic populations with pheromone traps to detect incipient outbreaks.
The Canadian Entomologist 117, 839–848.
Shepherd, R.F., Cunningham, J.C. and Otvos, I.S. (1995) Western spruce budworm, Choristoneura occiden-
talis. In: Armstrong, J.A. and Ives, W.G.H. (eds) Forest Insect Pests in Canada. Natural Resources
Canada, Canadian Forest Service, Ottawa, Ontario, pp. 119–121.
Shore, T.L. and Safranyik, L. (1992) Susceptibility and Risk Rating Systems for the Mountain Pine Beetle in
Lodgepole Pine Stands. Information Report BC-X-336, Forestry Canada, Pacific Forestry Centre,
Victoria, British Columbia, 12 pp.
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 253

IPM in Forestry 253

Shore, T.L., Safranyik, L. and Lemieux, J.P. (2000) Susceptibility of lodgepole pine stands to the mountain
pine beetle: testing of a rating system. Canadian Journal of Forest Research 30, 44–49.
Sieber, T.N., Sieber-Canavesi, F. and Dorworth, C.E. (1990a) Identification of Key Pathogens of Major Coastal
Forest Weeds. Forest Resource Development Agreement Report No. 113, Canadian Forest Service and
British Columbia Ministry of Forests, Victoria, British Columbia, 54 pp.
Sieber, T.N., Sieber-Canavesi, F. and Dorworth, C.E. (1990b) Simultaneous stimulation of endophytic
Cryptodiaporthe hystrix and inhibition of Acer macrophyllum callus in dual culture. Mycologia 82,
569–575.
Smirnoff, W.A. and Morris, O.N. (1984) Field development of Bacillus thuringiensis Berliner in eastern
Canada, 1970–80. In: Kelleher, J.S. and Hulme, M.A. (eds) Biological Control Programmes Against
Weeds and Insects in Canada 1969–1980. Commonwealth Agricultural Bureaux, Slough, UK,
pp. 238–247.
Smith, S.M., van Frankenhuyzen, K., Nealis, V.G. and Bourchier, R.S. (2002) Choristoneura fumiferana
(Clemens), eastern spruce budworm (Tortricidae). In: Mason, P.G. and Huber, J.T. (eds) Biological
Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK, pp. 58–68.
Smitley, D.R., Bauer, L.S., Hajek, A.E., Sapio, F.J. and Humber, R.A. (1995) Introduction and establishment
of Entomophaga maimaiga, a fungal pathogen of gypsy moth (Lepidoptera: Lymantriidae) in
Michigan. Environmental Entomology 24, 1685–1695.
Somme, L. (1964) Effects of glycerol on cold hardiness in insects. Canadian Journal of Zoology 42, 87–101.
Soper, R.S., Shimazu, M., Humber, R.A., Ramos, M.E. and Hajek, A.E. (1988) Isolation and characteriza-
tion of Entomophaga maimaiga sp. nov., a fungal pathogen of gypsy moth, Lymantria dispar, from
Japan. Journal of Invertebrate Pathology 51, 229–241.
Speare, A.T. and Colley, R.H. (1912) The Artificial Use of the Brown-tail Fungus in Massachusetts, with
Practical Suggestions for Private Experiment, and a Brief Note on a Fungus Disease of the Gypsy Caterpillar.
Wright and Potter, Boston, Massachusetts, 31 pp.
Statistics Canada (2002) International Trade. Available at: http://www.statcan.ca/ english/Pgdb/intern.
htm
Stelzer, M.J., Neisess, J., Cunningham, J.C. and McPhee, J.R. (1977) Field evaluation of baculovirus stocks
against Douglas-fir tussock moth in British Columbia. Journal of Economic Entomology 70, 243–246.
Sturrock, R.N. (2000) Management of Root Diseases by Stumping and Push-falling. Technology Transfer Note,
Canadian Forest Service, Pacific Forestry Centre, Victoria, British Columbia, 8 pp.
Sturrock, R.N., Phillips, E.J. and Fraser, R.G. (1994) A Trial of Push-Falling to Reduce Phellinus weirii
Infection of Coastal Douglas-fir. Forest Resource Development Agreement Report No. 217, Canadian
Forest Service and British Columbia Ministry of Forests, Victoria, British Columbia, 22 pp.
Syrett, P., Hill, R.L. and Jessep, C.T. (1985) Conflict of interest in biological control of weeds in New
Zealand. In: Delfosse, E.S. (ed.) Proceedings of the VI International Symposium on the Biological Control
of Weeds, August 19–25, 1984, Vancouver, British Columbia. Agriculture Canada, Ottawa, Ontario,
pp. 391–397.
Talerico, R.L. (1984) General biology of the spruce budworm and its hosts. In: Schmitt, D.M., Grimble,
D.G. and Searcy, J.L. (eds) Managing the Spruce Budworm in Eastern North America. Agriculture
Handbook No. 620, US Department of Agriculture Forest Service, Washington, DC, pp. 1–10.
Thorpe, S. (1996) Chemical and manual treatment in the northern interior. In: Comeau, P.G., Harper, G.J,
Blache, M.E., Boateng, J.O. and Gilkeson, L.A. (eds) Integrated Forest Vegetation Management: Options
and Applications. Proceedings of the Fifth British Columbia Forest Vegetation Management Workshop,
November 29–30, 1993, Richmond, British Columbia. Forest Resource Development Agreement Report
No. 251, Canadian Forest Service and British Columbia Ministry of Forests, Victoria, British
Columbia, pp. 61–66.
Ticehurst, M., Fusco, R.A., Kling, R.P. and Unger, J. (1978) Observations on parasites of gypsy moth in
first cycle infestations in Pennsylvania from 1974–1977. Environmental Entomology 7, 355–358.
Varty, I.W. (1978) 1977 Environmental Surveillance of Insecticide Spray Operations in New Brunswick’s
Budworm-infested Forests. Information Report M-X-87, Canadian Forestry Service, Maritimes Forest
Research Centre, Fredericton, New Brunswick, 24 pp.
Wall, R.E. (1977) Ericaceous Ground Cover on Cutover Sites in Southwestern Nova Scotia. Information Report
M-X-71, Canadian Forestry Service, Maritimes Forest Research Centre, Fredericton, New Brunswick,
55 pp.
Wall, R.E. (1983) Fireblight of wild raspberry on clear-cut forest areas. Environment Canada, Canadian
Forestry Service, Research Notes 3, 2–3.
10IntpestManCh10.QXD 14/4/04 2:26 pm Page 254

254 I.S. Otvos

Wall, R.E. (1990) The fungus Chondrostereum purpureum as a silvicide to control stump sprouting in hard-
woods. Northern Journal of Applied Forestry 7, 17–19.
Wall, R.E. (1994) Biological control of red alder using stem treatments with the fungus Chondrostereum
purpureum. Canadian Journal of Forest Research 24, 1527–1530.
Wall, R.E. and Hasan, S. (1996) Management of plant pathogens for vegetation control in forestry. In:
Raychaudhuri, S.P. and Maramorosch, K. (eds) Forest Trees and Palms: Diseases and Control. Oxford &
IBH Publishing Co., New Delhi, pp. 1–19.
Wall, R.E. and Shamoun, S.F. (1990a) Experiments on Vegetation Control with Native Pathogenic Fungi in the
Southern Interior of BC. Forest Resource Development Agreement Report No. 134, Canadian Forest
Service and British Columbia Ministry of Forests, Victoria, British Columbia, 18 pp.
Wall, R.E. and Shamoun, S.F. (1990b) Diseases of Rubus parviflorus in British Columbia. Canadian Plant
Disease Survey 70, 133–135.
Wall, R.E., Prasad, R. and Shamoun, S.F. (1992) The development and potential role of mycoherbicides
for forestry. The Forestry Chronicle 68, 736–741.
Wall, R.E., Prasad, R. and Sela, E. (1996) Biological control for weed trees. US Patent No. 5,587,158.
United States Patent Trademark Office, Washington, DC.
Wallace, D.R. (1995) Classical biological control. In: Armstrong, J.A. and Ives, W.G.H. (eds) Forest Insect
Pests in Canada. Natural Resources Canada, Canadian Forest Service, Ottawa, Ontario, pp. 385–395.
Wallner, W.E. (1989) An overview of pest Lymantriids of North America. In: Wallner, W.E. and McManus,
K.A. (technical coordinators) Proceedings, Lymantriidae: A Comparison of New and Old World Tussock
Moths, June 26-July 1, 1988, New Haven, Connecticut. General Technical Report NE-123, USDA Forest
Service, Northeastern Forest Experiment Station, Broomall, Pennsylvania, pp. 65–80.
Wallner, W.E. (1996) Invasive pests (‘biological pollutants’) and US forests: whose problem, who pays?
Bulletin OEPP/EPPO Bulletin 26, 167–180.
Walstad, J.D. and Kuch, P.J. (1987) Forest Vegetation Management for Conifer Production. John Wiley & Sons,
New York, 318 pp.
Watson, A.K. (1989) Current advances in bioherbicide research. In: Proceedings of the British Crop Protection
Conference, Vol. 3. British Crop Protection Council, Brighton, UK, pp. 987–996.
Watson, A.K. and Wall, R.E. (1995) Mycoherbicides: their role in vegetation management in Canadian
forests. In: Charest, P.J. and Duchesne, L.C. (compilers) Recent Proceedings in Forest Biotechnology in
Canada. Information Report PI-X-120, Natural Resources Canada, Canadian Forest Service,
Petawawa National Forestry Institute, Chalk River, Ontario, pp. 74–82.
Webb, R.E., Leonhardt, B.A., Plimmer, J.R., Tatman, K.M., Boyd, V.K., Cohen, D.L., Schwalbe, C.P. and
Douglass, L.W. (1990) Effect of racemic disparlure released from grids of plastic ropes on mating
success of gypsy moth (Lepidoptera: Lymantriidae) as influenced by dose and by population den-
sity. Journal of Economic Entomology 83, 910–916.
Welton, M. (1991) Fungal pathogens: forest tent caterpillar and gypsy moth. Forest Pest Management
Institute Newsletter 9, 7.
Weseloh, R.M. and Anderson, J.F. (1975) Inundative release of Apanteles melanoscelus against the gypsy
moth. Environmental Entomology 4, 33–36.
Weseloh, R.M. and Andreadis, T.G. (1992) Epizootiology of the fungus Entomophaga maimaiga, and its
impact on gypsy moth populations. Journal of Invertebrate Pathology 59, 133–141.
Winder, R.S. (2002) Chamerion angustifolium (L.) Holub, fireweed (Onagraceae). In: Mason, P.G. and
Huber, J.T. (eds) Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford,
UK, pp. 314–318.
Winder, R.S. and Shamoun, S.F. (1991) Terminology in microbial control of weeds. Biological Control 1,
339.
Wood, C.S. and Van Sickle, A. (1994) Forest Insect and Disease Conditions in British Columbia and Yukon –
1994. Information Report BC-X-354, Natural Resources Canada, Canadian Forestry Service, Victoria,
Canada, 39 pp.
Wood, C.S., Van Sickle, G.A. and Shore, T.C. (1983) Forest Insect and Disease Conditions in British Columbia
and the Yukon. Information Report BC-X-246, Environment Canada, Canadian Forestry Service,
Pacific Forest Research Centre, Victoria, Canada, 27 pp.
Wood, R.B. Jr and Bogdan, G.F. (1986) Reye’s syndrome and spruce budworm insecticide spraying in
Maine USA 1978–1982. American Journal of Epidemiology 124, 671–677.
Woods, A.J. (1994) The behaviour and impacts of Armillaria osyoyae in mature stands and plantations in
the Shuswap region of British Columbia. MSc thesis, Department of Forest Science, University of
British Columbia, Vancouver, British Columbia, 121 pp.
Ziller, W.G. (1974) The Tree Rusts of Western Canada. Publication No. 1329, Canadian Forest Service,
Victoria, British Columbia, 272 pp.
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11 Consumer Response to IPM: Potential

and Challenges

Craig S. Hollingsworth and William M. Coli

Department of Entomology, University of Massachusetts, Amherst, MA 01003, USA
E-mail: [email protected]

Introduction began to ask whether it was possible to bet-

ter understand the nature of consumer con-
In the period since the Second World War, cerns about agriculture and to publicize the
agriculture has experienced unprecedented use of IP techniques in a manner that allays
growth in both yield and production effi- these concerns. It was postulated that, by so
ciency. This growth has been due, at least in doing, consumer attitudes towards agricul-
part, to enhanced availability of fertilizers and ture would improve, and farm profitability
a vast array of highly effective crop-protection would also be enhanced. In this chapter we
chemicals. However, for growers of some review examples of efforts to test this
crops, profitability has not kept pace with hypothesis, and describe both the potential
improved yields and quality, and many farm- for and challenges to success.
ers now operate on thin profit margins if they
make any profit at all. In addition, well-publi-
cized examples of environmental contamina- The Consumer
tion from agrochemicals have caused many in
the non-farming public to develop negative Attitudes about the food supply and the
attitudes towards modern agriculture (Morris environment
et al., 1993; Govindasamy and Italia, 1998).
Since the 1970s with the growth in devel- Surveys indicate that consumers have signif-
opment and use of integrated pest manage- icant concerns about the chemicals used to
ment (IPM) and integrated production (IP), grow food products, especially effects related
significant reductions in unnecessary pesti- to their own health and that of their children.
cide use have been achieved and a significant Pesticide use on food crops was identified as
shift has occurred away from the more envi- the primary food-safety concern of con-
ronmentally risky, broad-spectrum chemicals sumers in Georgia (Ott et al., 1991) and New
towards novel pesticide chemistries that are Jersey (Govindasamy et al., 1998). Fifty-nine
both environmentally more benign and more per cent of New England (six north-eastern
precisely targeted against key pests. states) consumers feel that pesticide use is
In spite of these gains, consumers’ atti- unsafe and unnecessary (Hollingsworth et
tudes to agriculture have not improved, and al., 1993). Nearly all the consumers in a sur-
sustainable levels of profitability remain elu- vey by Pool (1996) expressed concern over
sive in many cases. With this in mind, some pesticide residues in food; consumers who
© CAB International 2004. Integrated Pest Management: Potential, Constraints and Challenges
(eds O. Koul, G.S. Dhaliwal and G.W. Cuperus) 255
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256 C.S. Hollingsworth and W.M. Coli

purchase greater amounts of produce Atlantic, 1997) found that 91% of consumers
expressed a higher level of concern. Morris et support the use of environmentally safe agri-
al. (1993) found that the majority of the cultural practices and would purchase prod-
American public believes that it is very ucts that identify this on the label. These
important for US farmers to switch to low- consumers (89%) indicated that food prod-
chemical production strategies that rely pri- ucts that claim to have improved environ-
marily on natural methods. mental performance should be certified or
Pool (1996) found that perceptions of the labelled, and 70% reported that they read
hazards of pesticides to health are not con- information on food products and want
stant, but are affected by ethnicity, age, edu- more detailed information. Product labels
cation level and numbers of children in the that identify environmentally positive traits
home. For example, among upstate New are called ‘eco-labels’.
York consumers, Hispanic and African-
American respondents were more likely to
be very concerned about chemical residues Consumer knowledge and attitudes about IPM
than Asian and white respondents, and peo-
ple with rural experience were less con- In the USA, the public’s awareness of IPM as
cerned about pesticide residues in foods. it relates to environmental performance is
Consumers’ concerns about produce are not well developed. Surveys in the north-
complex. While aspects of cosmetic quality east USA (Grant et al., 1990; Hollingsworth et
interact with consumer concerns over food al., 1993; Anderson et al., 1996; Pool, 1996)
safety, consumers also express concerns for found that few consumers (12–24%) have
water quality, environmental degradation, heard of IPM. Approximately 7% of respon-
farm-worker safety and other secondary dents to a telephone survey of 972 individu-
issues (Cuperus et al., 1991). Hartman (1996) als throughout 48 states indicated that they
explored the potential market for environ-
knew at least ‘a fair amount’ about IPM and
mentally produced goods and found that
over one-third knew at least ‘a little’ about
over half of American consumers have inter-
IPM (Blend and van Ravenswaay, 1998).
ests in such products, but that their interests
Other studies show that consumers find
are not uniform. Factors such as education,
terms such as ‘IPM,’ ‘organic’ and ‘residue-
media exposure, geography and the influ-
free’ confusing (Shelton et al., 1990;
ence of children are important factors in
determining the level of consumer interest in Cartwright et al., 1993). Even where produce
environmental products. Purchase criteria was labelled as ‘IPM-grown,’ only 8% of con-
also differ with individual products and sumers were aware of the label (Anderson et
Hartman suggests that different marketing al., 1996). However, active marketing (direct
strategies need to be developed for differing contact with the consumer, rather than pas-
market segments. Hartman cautioned that sive signs) significantly increased awareness
environmental enhancement is not the dri- of IPM and a trend towards greater interest
ving force for purchase, but, with education, in IPM-certified produce (Anderson et al.,
consumers can perceive environmental qual- 1996). Paschall et al. (1992) surveyed compo-
ities as added value. Hartman (1997) found nents of the food industry of New England
that people most interested in environmen- and found that, once the concept of IPM was
tally produced products were most familiar explained, 86% of consumers and 30% of
with groundwater pollution by pesticides. food processors, wholesalers and retailers
Concern over water pollution was rated supported the idea of marketing ‘IPM-
higher than biological control of pests, thus grown’ produce.
suggesting that marketing claims associated Perceptions of agriculture are influenced
with water protection will resonate with con- when information about IPM is provided. In
sumers more strongly than other environ- a study by Bruhn et al. (1992), consumers’
mental or ecological issues. perceptions regarding food safety and risk
A survey conducted for the Massachusetts perception were tested. Then, following a
Department of Food and Agriculture (Pan 2 min video explaining IPM, those percep-
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Consumer Response to IPM 257

tions were reassessed. Concerns about food unblemished sweet corn and cabbage that
safety and farming practices were signifi- had received weekly pesticide applications,
cantly reduced after the explanation about but when the pesticide history of the pro-
IPM. duce was revealed, the majority selected
When IPM is explained, consumers IPM-grown or unsprayed produce.
express interest in IPM-grown produce. Similarly, the majority of consumers with
Where initially 45% of farmstand and farm- knowledge of the pesticide history of their
ers’ market customers said that they did not produce selected IPM-grown oranges with
care how their food was grown, 85% of these 20% surface damage over conventionally
customers stated a preference for IPM-grown grown blemish-free oranges (Bunn et al.,
produce over conventionally grown after a 1990).
short definition of IPM had been presented A consistent predictor of the willingness
(Anderson et al., 1996). Other studies also to purchase organic or IPM-grown produce
show little consumer awareness of IPM ini- is concern over pesticide residues in food
tially but 86–92% preference for IPM-grown (Govindasamy and Italia, 1997; Loureiro et
produce after IPM has been defined (Burgess al., 2001). The majority of consumers stating
et al., 1989; Hollingsworth et al., 1993; Pool, a preference for IPM-grown produce per-
1996). ceived it as healthier or safer (Hollingsworth
Consumers made aware of IPM indicate et al., 1993; Anderson et al., 1996). Pool (1996),
that they will pay more for IPM-grown pro- however, found that concern about pesticide
duce. Fifty-seven per cent of Massachusetts residues in food does not, of itself, make
consumers indicated that they would pay at respondents more likely to purchase IPM
least 10% more for IPM-grown produce grown produce. While people who perceive
(Hollingsworth et al., 1993) and 75% of New pesticides as a significant environmental
York consumers responded that they would contaminant are more likely to purchase
pay 9% more and 23% would pay between IPM-grown produce, most respondents,
10 and 24% more for IPM-grown produce regardless of their concern about pesticide
(Pool, 1996). In another study, 92% of New residues in food, indicated that they would
York consumers indicated that they would likely buy IPM-grown produce.
pay at least 10% more and 55% would pay Loureiro et al. (2001) looked at consumers’
25% more for IPM-grown produce (Burgess relative perceptions of apples grown with
et al., 1989). Further, 29% reported that they conventional, IPM and organic practices. In
would be ‘very likely’ to change grocers in terms of the environment, food safety and
order to purchase IPM-grown produce. consumers’ willingness to pay a premium,
Underhill and Figueroa (1993) found that organic apples were preferred, followed by
younger, higher-earning individuals and those grown using IPM. Consumer response
those who live in urban settings were the to eco-labels was influenced by a number of
most likely to pay more for IPM-certified factors, including the presence of small chil-
produce. Van Ravenswaay and Blend (1999) dren in the family and attitudes towards the
found that over a third of households would environment and food safety. Size of family
be willing to pay a premium of US$0.40/lb. had a negative effect, which was correlated
for eco-labelled apples. with price – that is, for larger families, price
Focus groups of New York consumers was a significant factor. When eco-labelled
ranked freshness, ripeness, colour and lack products cost more, consumers from larger
of blemishes over whether chemicals were families eschewed them. Organic apples
used in production (Shelton et al., 1990). were perceived as safer and more environ-
However, while consumers tend to choose mentally friendly, and strong environmental
visually appealing produce, Collins et al. attitudes expressed by consumers increased
(1992) found that consumers’ selection crite- the probability of their purchasing organic
ria of produce could be changed when the over eco-labelled. Thus, organic and IPM
pesticide history of the product was labels compete under criteria of price and
revealed. Consumers tended to select fruit quality.
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258 C.S. Hollingsworth and W.M. Coli

Eco-labels emphasis placed on monitoring pest popula-

tions. When compliance with IPM standards
An eco-label differentiates environmentally or guidelines is documented, presence of
preferable products based on an environ- ‘Certified IPM’ crops in the market-place can
mental impact assessment of the product assure concerned consumers that the pro-
compared with other products in the same ducer is taking measures to protect the envi-
category (Loureiro et al., 2001). The eco-label ronment while growing crops. This presents
may emphasize any of a number of environ- an opportunity to educate customers about
mentally related themes, including biodiver- the realities of farming and pest damage and
sity, social justice, energy conservation or the rationale behind judicious pesticide use.
agricultural sustainability.
While the purpose of an eco-label is ulti-
mately to market one product over another, Challenge: assessing IPM practices
labels carry significant educational content
as well as implicit and sometimes explicit, For consumers to give credibility to an eco-
guarantees that the labelled product has label, the labelling programme must have a
improved quality or benefits compared with basis in ecological principles, criteria to
those that are not labelled. For example, judge the progress towards those principles,
‘Dolphin Safe’ tuna, one of the first eco- standards for practical measurement of those
labels to achieve widespread distribution in criteria and certification documenting that
the USA, became the industry standard the standards are followed (Kurki and
because of consumer awareness and concern Matheson, 2001).
that dolphins were being killed as a ‘by- If IPM is to be used as a marketing label,
catch’ by commercial tuna fishers. IPM practices must be documented and certi-
One of the best-known food-related eco- fied. Self-certification is not adequate.
labels is the organic food designation. This McDonald and Glynn (1994) found that, while
label has achieved success in the market-place 85% of apple-growers surveyed described
by combining explicit environmental guaran- themselves as practising IPM, many of them
tees (e.g. that practitioners strive to maintain did not follow general IPM practices. For
biological diversity and to maintain and example, only 17% of self-described IPM
improve soil health on their farms) and growers waited for pest action thresholds to
implicit quality guarantees (e.g. nutritional be reached before applying pesticides.
superiority, absence of toxic chemical Hamilton et al. (1997) found similar contradic-
residues). Organic labels cite the promise of tions when growers were asked to classify
sustainable agriculture and health of the soil, their own farming systems.
in part, by avoiding the use of synthetic fertil- A wide array of IPM evaluation systems
izers and pesticides, though naturally occur- exists, including output-oriented systems and
ring pesticides such as rotenone, ryania and input-oriented systems (Swinton and
copper are generally allowed. The ‘Certified Williams, 1998). Output-oriented systems
Organic’ label and its many relatives are gov- measure such variables as pesticide use,
erned by various organizations throughout residues or hazard indices. Input-oriented
the world. In the USA, organic standards have systems relate to completion of IPM practices
been codified into federal law (Anon., 2000). and are commonly used to assess farm com-
IPM and IP programmes, with their focus pliance, as in programmes in Massachusetts
on understanding ecological aspects of crop (Hollingsworth and Coli, 1999), New York
production and on reducing or eliminating (Petzoldt and Kovach, 1996) and those under
the use of pesticides, particularly those with the umbrella of the International Organization
negative non-target effects, are natural candi- of Biological Control (IOBC) (Cross and
dates for eco-labels. Compliance with IPM/IP Dickler, 1994). Wisconsin’s Protected Harvest
systems is similar to those in organic agricul- guidelines (Benbrook et al., 2002) combine
ture, though there is generally less emphasis outputs (pesticide-hazard indices) and inputs
placed on proscribed chemicals and more (specific farmer practices).
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Consumer Response to IPM 259

Consumers interested in purchasing growers; a sense of increasing government

goods with environmental labels indicate a regulation; reluctance to discuss the use of
strong preference for an independent or pesticides with consumers; and potential
government-associated organization to ver- costs associated with a programme (e.g.
ify completion of practices. New England Acuff, 1997). While farmers have expressed
consumers, farmers, food processors and reluctance to promote IPM produce as
retailers supported the role of state depart- ‘good’, because it might taint their conven-
ments of agriculture as a certifying agency tional produce as ‘bad’, in our experience
over private or farmer organizations this is not an issue of concern to consumers
(Paschall et al., 1992; Pan Atlantic, 1997). (Hollingsworth, 1994).
IPM-grown goods also face many of the
same challenges to market penetration that
Challenge: marketing all goods encounter. Beamer and Preston
(1991), exploring the process of allocation of
Several challenges to the marketing of IPM- shelf space in stores, confirmed that stores
grown produce have been identified by employ different strategies in selecting
Shelton et al. (1990): the term integrated pest brands and labels. Factors that could affect
management or IPM is perceived negatively the acceptance of IPM-grown produce
by consumers; the terms and concepts asso- include: variety, in that some stores provide
ciated with IPM (e.g. cultural techniques, more consumer options than others; unifor-
biological controls, genetic resistance, pest- mity, the need for a store chain to provide
population levels, etc.) are technical and very similar products among its stores; sea-
complex; there are negative attitudes associ- sonality, for stores to provide produce
ated with pests and chemical applications; throughout the year; and firm image. A firm’s
and there is a lack of personal experience image may emphasize low prices, wide vari-
with pesticides among urban consumers. ety, high quality, or, perhaps, awareness of
However, as shown above (Bruhn et al., social and environmental causes. Another
1992), consumers are receptive to the ideas barrier in the penetration of some markets is
behind IPM and, by educating consumers the ‘loyalty factor’ between established grow-
through marketing, potential obstacles can ers and store managers or buyers.
be overcome. One approach to educating the
public is through eco-labels, discussed
below. Another approach, through schools, Examples of IPM labels
can provide both passive and active educa-
tion of IPM. In the USA, many states have A number of IPM certification programme
passed legislation that requires schools to labels have been promoted in recent years.
practise and document their practice of IPM. The following are examples of programmes
Thus, individuals associated with schools are that promote IPM farms and products
learning its terms and principles. Schools are through the use of farm certification. These
also teaching IPM: the Pennsylvania examples do not include labels for organic
Department of Education (2002) mandates products, discussed above, but do include
that children in grades 4, 7, 10 and 12 those labels that include IPM as a significant
demonstrate knowledge of increasingly com- promotional trait. The field of IPM
plex concepts of IPM. Various extension pro- certification is dynamic: new IPM labels are
grammes and independent agencies have developed and others are phased out. Hence,
developed numerous IPM curricula the following examples are not comprehen-
(http://www.ipminstitute.org). sive, but are provided for the purpose of
Reluctance to promote IPM labels has also illustration. Current information on these
formed institutional barriers within grower and other eco-labels can be found in Barstow
groups, universities and government organi- (2002) and through websites of the IPM
zations. Reasons for opposition to IPM labels Institute of North America (http://www.
include: reluctance to differentiate produce ipminstitute.org) and the Consumers Union
from that of a large clientele of conventional (http://www.ecolabels.org).
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260 C.S. Hollingsworth and W.M. Coli

Integrated production (IOBC) certification programme in the USA (Reed,

1995). Certification requirements were based
Since the late 1980s, the IOBC has provided on those of the IFP programme of the IOBC,
standards for commercial labelling of pome though it also incorporated an environmen-
fruit grown under ‘integrated fruit produc- tal impact scoring system for pesticide use.
tion’ (IFP) practices (Malavolta et al., 1998). Two hundred and fifty growers of apple,
Now under the label of IP, IOBC standards cherries and pears participated in the pro-
for stone fruit, soft fruit, viticulture and sub- gramme.
tropical fruit have been promulgated. These
generalized standards are used to develop
regional IP guidelines by local or national Wegmans supermarkets
organizations or agencies.
Currently, over 50 regional or national Under the motto, ‘Food You Can Feel Good
agencies in more than 20 countries, in About’, Wegmans Food Markets of Rochester,
Europe, North America, South America and New York has promoted fruit and vegetable
the South Pacific have IP certification pro- products grown using IPM. Farmers who
grammes, with the greatest adoption in grow for the Wegmans programme adhere to
Western Europe (Table 11.1). Switzerland has a point-system evaluation developed in coop-
the most extensive adoption of IP standards, eration with Cornell University. Although the
including 85% of Swiss pome fruit, 81% of programme started initially with fresh pro-
stone fruit, 73% of soft fruit and 81% of wine duce, processed foods (e.g. sweet corn, beans)
grapes (Dickler, 1999). bearing the Wegmans brand also bear a New
York IPM logo. IPM information, including
video loops, is prominently displayed in
Responsible Choice Wegmans stores. IPM-labelled foods do not
command a higher price at Wegmans (W.
Administered through Stemilt Growers Inc., Poole, 2001, personal communication), but
a fruit-grower’s cooperative in Washington support the company’s theme, ‘Food You
State, Responsible Choice was the first IPM Can Feel Good About,’ by supporting local

Table 11.1. Regional integrated fruit production (IFP) certification of pome fruit (1000 ha) (from Dickler,
1999).

Country IP Conventional Per cent

Argentina 396 35,104 1.1

Australia 12,000 3,000 80.0
Austria 6,030 1,061 85.0
Croatia 820 540 60.3
Denmark 670 852 44.0
Germany 26,042 5,859 81.6
Great Britain 10,184 3,289 75.6
Italy 32,191 22,699 58.6
Norway 66 1,874 3.4
Poland 5,100 136,900 3.6
Portugal 350 7,650 4.4
Slovenia 1,200 1,868 39.1
Spain 600 16,643 3.5
Switzerland 4,316 778 84.7
Uruguay 183 4,010 4.4
USA (Hood River, Oregon) 105 745 12.4

Total 100,253 242,904 29.2

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Consumer Response to IPM 261

farmers, providing healthy food and caring permitted. Other regulations address land use,
about the environment water treatment, worker conditions, wildlife
conservation and community relations.
The Rain Forest Alliance claims that the
Partners with Nature certification process benefits farmers by
increasing production efficiency, reducing
A collaboration of the Massachusetts costly inputs and improving farm manage-
Department of Food and Agriculture, the ment and that certified farmers have better
University of Massachusetts Extension IPM access to speciality buyers, contract stability,
Programme and the US Department of favourable credit options, publicity, technical
Agriculture (USDA) Farm Service Agency, assistance and niche markets. Most farmers
Partners with Nature (PWN) certified receive a price premium on average from
Massachusetts-grown IPM vegetables and 5 to 20% (http://www.rainforest-alliance.
small fruits from 1993 to 1999. Certification org/programs/cap/index.html).
was based on best management practices,
which were weighted and assigned points
(Hollingsworth and Coli, 1999). The pro- Food Alliance-approved
gramme focused on consumer and grower
education, certifying 109 different growers The Food Alliance was founded in the north-
over 6 years. In 1999, the programme certi- western USA in 1994 and expanded to the
fied 53 growers of 13 different crops. When Midwest in 2002. It recognizes farmers who
polled, 92% of growers enrolled in the pro- seek alternatives to conventional pesticides,
gramme agreed that educating the public protect soil and water and promote the well-
was the most important role of the pro- being of farm workers (http://www.
gramme. Nearly 90% agreed that the pro- thefoodalliance.org). Approved commodities
gramme provided them with a greater include fruits, vegetables, wheat, livestock,
understanding of IPM and encouraged dairy products and wine. In 2002, nearly 200
greater adoption of IPM practices. A third of farms and ranches in eight states partici-
the growers noted an increase in profits pated in the programme and approved prod-
through the programme. An independent ucts are sold in retail outlets in 20 states.
survey (Bonanno, 1997) demonstrated that Marketing and promotional campaigns
certified PWN growers used less than half resulted in a peak consumer awareness of
the amount of pesticides than self-described the programme of 24% in 2001. The pro-
IPM growers (http://www.umass.edu/ gramme plans to expand to the north-eastern
umext/ipm/ipm_projects/education/ USA (Kane and Ennis, 2002).
partners_with_nature.html).

Core Values Northeast (CVN)

Eco-OK
Founded by the consumer education organi-
Originally founded by the Rain Forest Alliance zation, Mothers and Others for a Livable
in 1991, Eco-OK certifies coffee, banana, cocoa Planet, in 1995 to promote IPM-grown and
and orange farms according to social and locally grown apples, CVN certified tree fruit,
environmental standards, including IPM. As small fruits and some vegetables. In 2002, they
of June 2001, 218 farms/cooperatives were listed 18 participating farms from six states
certified in Costa Rica, Colombia, Ecuador, (http://www. corevalues.org).
Guatemala, Honduras, Panama, Mexico, El
Salvador and Hawaii. The programme’s
guidelines regulate agrochemicals: pesticides Linking Environment and Farming (LEAF)
approved in the USA are specified, though
any pesticides designated by the Pesticide Promoting awareness and adoption of inte-
Action Network as in the ‘dirty dozen’ are not grated farm management (IFM) in Britain,
11IntpestManCh11.QXD 14/4/04 2:26 pm Page 262

262 C.S. Hollingsworth and W.M. Coli

LEAF relies on farmers’ self-assessment of were enrolled in the programme. Currently,

the economic and environmental conse- Protected Harvest certifies only ‘Healthy
quences of current and potential farm prac- Grown’ brand potatoes.
tices. Public awareness is promoted through
press releases and tours at participating
farms. Thirty-six cooperating farms through- Conclusions
out Britain are currently listed and a label for
fresh produce is under development While a significant number of consumers are
(http://www.leafuk.org). interested in supporting environmentally
friendly products, the concepts of IPM are
complex and difficult to communicate to the
Protected Harvest harried shopper whose goal is to purchase
the requisite amount of groceries in the mini-
A collaboration of the World Wildlife Fund, mum amount of time. The success of an IPM
the Wisconsin Potato and Vegetable Growers label is dependent on the success of its sup-
Association and the University of Wisconsin, porting marketing programme and eco-
Protected Harvest certifies potatoes grown labels with strong marketing support (e.g.
using IPM. Guidelines have been under Food Alliance) have shown significant
development since 1996 and the certification growth. Labels are only part of the educa-
programme began in 2001. Certification is tional process. Other media, such as
based on ‘preventive practice points’, which brochures, posters, news releases and media
measure the position of the grower along the events, help support the educational process.
‘IPM continuum’ (Benbrook, 1996) and an Clearly, IPM is much more than a marketing
additive index of the toxicity of pesticides incentive, but marketing efforts not only pro-
used in crop production (Benbrook et al., mote the product, but also educate the con-
2002). Certain pesticides and genetically sumer about agriculture, affecting attitudes
engineered cultivars are prohibited from use and perceptions about farming in general
(Sexson and Dlott, 2001). In 2001, 20 growers (Bruhn et al., 1992; Hollingsworth, 1994).

References

Acuff, G. (1997) Labels send wrong message. Fruit Grower September, 29.
Anderson, M.D., Hollingsworth, C.S., Van Zee, V., Coli, W.M. and Rhodes, M. (1996) Consumer response
to integrated pest management and certification. Agriculture, Ecosystems and Environment 60, 97–106.
Anon. (2000) National organic program; final rule. US Federal Register 65(245); 80547–80596.
Barstow, C. (2002) The Eco-Foods Guide, 1st edn. New Society Publishers, Gabriola Island, British
Columbia, Canada, 271 pp.
Beamer, B.G. and Preston, W.P. (1991) Shelf space allocation in the produce section: implications for mar-
keting specialty produce. Journal of Food Distribution Research September, 23–35.
Benbrook, C.M. (1996) Pest Management at the Crossroads. Consumers Union, Yonkers, New York, 272 pp.
Benbrook, C.M., Sexon, D.L., Wyman, J.A., Stevenson, W.R., Lynch, S., Wallendal, J., Diercks, S., Van
Haren, R. and Granadino, C.A. (2002) Developing a pesticide risk assessment tool to monitor
progress in reducing reliance on high-risk pesticides. American Journal of Potato Research 79, 183–199.
Blend, J. and van Ravenswaay, E.O. (1998) Consumer Demand for Ecolabelled Apples: Survey Methods and
Descriptive Results. Staff Paper No. 98–20, Department of Agricultural Economics, Michigan State
University, East Lansing, Michigan.
Bonanno, R. (1997) New England Vegetable Growers Association Pesticide Use. Report to US Environmental
Protection Agency Region I.
Bruhn, C., Peterson, S., Phillips, P. and Sakovidh, K. (1992) Consumer response to information on inte-
grated pest management. Journal of Food Safety 12, 315–326.
Bunn, D., Feenstra, G.W., Lynch, L. and Sommer, R. (1990) Consumer acceptance of cosmetically imper-
fect produce. Journal of Consumer Affairs 24, 268–279.
11IntpestManCh11.QXD 14/4/04 2:26 pm Page 263

Consumer Response to IPM 263

Burgess, R., Kovach, J., Petzoldt, C., Shelton, A. and Tette, J. (1989) Results of IPM marketing survey. In:
Proceedings of the Fifty-First Annual New York State Pest Management Conference. Cornell University,
Ithaca, New York.
Cartwright, B., Collins, J.K. and Cuperus, G.W. (1993) Consumer influences on pest control strategies for
fruits and vegetables. In: Leslie, A.R. and Cuperus, G.W. (eds) Successful Implementation of Integrated
Pest Management for Agricultural Crops. Lewis Publishers, Boca Raton, Florida, pp. 151–171.
Collins, J.K., Cuperus, G.W., Cartwright, B., Stark, J.A. and Ebro, L.L. (1992) Consumer attitudes on pro-
duction systems for fresh produce. Journal of Sustainable Agriculture 3, 67–77.
Cross, J.V. and Dickler, E. (1994) Guidelines for integrated production of pome fruits in Europe. Technical
Guideline III. International Organization of Biological Control WPRS Bulletin 17, 9.
Cuperus, G.W., Kendall, P., Rehe, S., Sachs, S., Frisbie, R., Hall, K., Bruhn, C., Deer, H., Woods, F.,
Branthaver, B., Weber, G., Poli, P., Buege, D., Linker, M., Andress, E., Wintersteen, W., Dost, F.,
Damicone, J., Herzfeld, D., Collins, J., Cartwright, B. and McNeal, C.D. (1991) Integration of Food
Safety and Water Quality Concepts Throughout the Food Production, Processing and Distribution
Educational Programmes: Using Hazard Analysis Critical Control Point (HACCP) Philosophies. Oklahoma
Cooperative Extension Service Circular E-903, Stillwater, Oklahoma.
Dickler, E. (1999) Encuesta sobre producciòn integrada de frutas en el Periodo 1995–1997. Producciòn
integrada de frutas en Europa y en el mundo. In: Curso international de Producciòn integrada y organica
de frutas mayo, General Roca, Rio Negro, Argentina, Vol. 2, pp. 1–7.
Govindasamy, R. and Italia, J. (1997) Consumer Response to Integrated Pest Management and Organic
Agriculture: an Econometric Analysis. New Jersey Agricultural Experiment Station Publication P-
02137–2-97, New Brunswick, New Jersey.
Govindasamy, R. and Italia, J. (1998) Consumer Concerns about Pesticide Residues. New Jersey Agricultural
Experiment Station Publication FS896, New Brunswick, New Jersey.
Govindasamy, R., Italia, J. and Rabin, J. (1998) Consumer Response and Perceptions to Integrated Pest
Management Produce. New Jersey Agricultural Experiment Station Publication P-02137–5-98, New
Brunswick, New Jersey.
Grant, J., Tette, J., Petzoldt, C. and Kovach, J. (1990) Feasibility of an IPM-Grower Recognition Program in
New York State. IPM No. 3, New York Agricultural Experiment Station, Geneva, New York.
Hamilton, G.C., Robson, M.G., Ghidiu, G.M., Samulis, R. and Prostko, E. (1997) 75% adoption of inte-
grated pest management by 2000? A case study from New Jersey. American Entomologist 43, 74–78.
Hartman, H. (1996) The Hartman Report on Food and the Environment: a Consumer’s Perspective, Phase I. The
Hartman Group, Bellevue, Washington.
Hartman, H. (1997) The Hartman Report on Food and the Environment: a Consumer’s Perspective, Phase II. The
Hartman Group, Bellevue, Washington.
Hollingsworth, C.S. (1994) Integrated pest management certification: a sign by the road. American
Entomologist 40, 74–75.
Hollingsworth, C.S. and Coli, W.M. (eds) (1999) Massachusetts Integrated Pest Management Guidelines: Crop
Specific Definitions. University of Massachusetts Extension Publication IP-IPMA, Amherst,
Massachusetts, 66 pp.
Hollingsworth, C.S., Paschall, M.J., Cohen, N.L. and Coli, W.M. (1993) Support in New England for certi-
fication and labeling of produce grown using integrated pest management. American Journal of
Alternative Agriculture 8, 78–84.
Kane, D.J. and Ennis, J.F. (2002) The Food Alliance: transforming a regional success story into a national
network. In: Proceedings of the Conference on Ecolabels and the Greening of the Food Market. Boston,
Massachusetts, 7–9 November 2002. Tufts University, Medford, Massachusetts.
Kurki, A. and Matheson, N. (2001) Eco-labelled foods: profit or problems? Appropriate Technology Transfer
for Rural Areas News 8(3).
Loureiro, M.L., McCluskey, J.L. and Mittelhammer, R.C. (2001) Willingness to Pay for Sustainable
Agricultural Products. Report to U.S. Federal State Marketing Improvement Programme. Department of
Agricultural Economics, Washington State University, Pullman, Washington, 55 pp.
McDonald, D.G. and Glynn, C.J. (1994) Difficulties in measuring adoption of apple IPM: a case study.
Agriculture, Ecosystems and Environment 48, 219–230.
Malavolta, C., Avilla, J., Boller, E.F., Gendrier, J.P. and Jorg, E. (1998) Integrated production, recent envi-
ronmental policy and market trends: the role of IOBC? International Organization of Biological Control
WPRS Bulletin 21, 23–27.
11IntpestManCh11.QXD 14/4/04 2:26 pm Page 264

264 C.S. Hollingsworth and W.M. Coli

Morris, P.M., Rosenfield, A. and Bellinger, M. (1993) What Americans Think about Agrichemicals. A
Nationwide Survey on Health, the Environment and Public Policy. Public Voice for Food and Health
Policy, Washington, DC.
Ott, S.L., Huang, C.L. and Misra, S.K. (1991) Consumers’ perceptions of risk from pesticide residue and
demand for certification of residue-free produce. In Caswell, J.A. (ed.) Economics of Food Safety.
Elsevier, New York, pp. 176–188.
Pan Atlantic Consultants (1997) Report to the Massachusetts Department of Food and Agriculture on Consumer
Preferences and Attitudes Regarding Massachusetts Grown Agricultural Products. Massachusetts
Department of Food and Agriculture, Boston, Massachusetts.
Paschall, M.J., Hollingsworth, C.S., Coli, W.M. and Cohen, N.L. (1992) Attitudes and perceptions of New
England consumers and the food industry toward a certification program for integrated pest man-
agement. Fruit Notes (University of Massachusetts Extension) 57, 3–11.
Pennsylvania Department of Education (2002) Academic Standards for Environment and Ecology. 22
Pennsylvania Code. Chapter 4, Appendix B.
Petzoldt, C. and Kovach, J. (1996) New York IPM Elements. New York IPM Program, New York
Agricultural Experiment Station, Geneva, New York.
Pool, W.M. (1996) The influence of consumer attitudes and perceptions about pesticides and produce
quality on technology transfer. MS thesis, Rochester Institute of Technology, Rochester, New York,
160 pp.
van Ravenswaay, E.O. and Blend, J.R. (1999) Measuring consumer demand for eco-labelled apples.
American Journal of Agricultural Economics 81, 1078–1083.
Reed, A.N. (1995) Responsible choice: a systems approach to growing, packing and marketing fruit. In:
Hull, J. Jr and Perry, R. (eds) The 125th Annual Report of the Secretary of the State Horticultural Society of
Michigan for the Year 1995. Hartford, Michigan, pp. 68–78.
Sexson, D.L. and Dlott, J. (2001) Companion documentation for the eco-potato standards. Available at:
http://ipcm.wisc.edu/bioIPM
Shelton, A.M., Burgess, R., Lanier, J., Petzoldt, C.H., Kovach, J., Grant, J. and Tette, J. (1990) Market
research in consumer attitudes to IPM. In: Proceedings of the Fifty-Second Annual New York State Pest
Management Conference. Cornell University, Ithaca, New York.
Swinton, S.M. and Williams, M.B. (1998) Assessing the Economic Impacts of Integrated Pest Management:
Lessons from the Past, Directions for the Future. Staff Paper No. 98–12, Department of Agricultural
Economics, Michigan State University, East Lansing, Michigan.
Underhill, S.E. and Figueroa, E.E. (1993) Consumer Preferences for Non-conventionally Grown Produce.
Agricultural Economics Staff Paper 93–07. Department of Applied Economics and Management,
Cornell University, Ithaca, New York.
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12 The Essential Role of IPM in Promoting

Sustainability of Agricultural Production
Systems for Future Generations

G.W. Cuperus,1 R.C. Berberet1 and R.T. Noyes2

1Department of Entomology and Plant Pathology,
2Departmentof Biosystems and Agricultural Engineering,
Oklahoma State University, Stillwater, Oklahoma, USA
E-mail: [email protected]

Introduction merits of our basic premise. We consider sus-

tainable agriculture to be ‘an agriculture that
Two of the most common phrases used since can evolve indefinitely toward greater
the early 1980s in relation to systems human utility, greater efficiency of resource
designed for production of food and fibre are use, and a balance with the environment that
‘sustainable agriculture’ and ‘ integrated pest is favourable both to humans and to most
management’ (IPM). These phrases almost other species’ (Harwood, 1990). The follow-
invariably appear in publications that stress ing conditions (modified from Benbrook,
the efficiency and profitability of production 1990) must be satisfied for agricultural sys-
systems and, more emphatically, the neces- tems to be sustainable:
sity of protecting soil, water and the human
food supply from contamination by agro- • Soil resources must not be degraded
chemicals. Our goal in this chapter is to sup- through erosion, salination or contamina-
port the concept that improving the tion with toxic compounds (e.g. pesti-
sustainability of production systems and cides).
implementation of IPM must be linked. Our • Water resources must be managed to meet
basic premise is that employment of princi- needs for irrigation and to prevent degra-
ples of IPM is essential to optimizing sus- dation with silt and toxic compounds.
tainability of agricultural systems. We The biological and ecological integrity of
believe that the future development and suc- systems must be preserved through careful
cess of IPM are quite important to the sus- management of genetic resources (for both
tainability of agriculture for the coming crops and livestock), nutrient cycles and pest
centuries. species.
Many definitions have been proposed to
describe sustainable agriculture and IPM, • Production systems must be economically
and we realize the necessity of presenting viable, returning an acceptable profit to
those that we intend to use in assessing the farmers.
© CAB International 2004. Integrated Pest Management: Potential, Constraints and Challenges
(eds O. Koul, G.S. Dhaliwal and G.W. Cuperus) 265
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266 G.W. Cuperus et al.

• Social expectations must be satisfied, and concerns was Rachel Carson in her classic
food and fibre needs must be met in terms commentary on pesticides entitled Silent
of quality and quantity of commodities Spring (Carson, 1962). In the years since 1962,
available at reasonable prices to con- it has become increasingly apparent that
sumers. employing chemical controls unilaterally
will not provide safe and effective regulation
These attributes give a clear emphasis for of pests over the long term (Cuperus et al.,
two primary goals of sustainable systems. 1990). Problems ranging from pesticide resis-
These systems must be economically viable, tance in target species (resulting in control
and they must contribute to desirable envi- failures) to environmental degradation and
ronmental qualities over the long term. contamination of food products by pesticide
The basic approach for pest regulation residues have proved that reliance on unilat-
that we envision is consistent with these pri- eral controls seriously detracts from sustain-
mary goals for sustainability, as is clearly ability. The IPM philosophy has evolved
evident in a recent definition proposed for through approaches designed to solve these
IPM: types of problems. Clearly, an attribute that
The judicious use and integration of various must be added to those previously stated for
pest control tactics in the context of the sustainable systems is that these systems
associated environment of the pests in ways ‘employ integrated management programs
that complement and facilitate the biological for safe and effective regulation of pest
and other natural controls of pests to match species’.
economic, public health, and environmental
goals.
(Anon., 2000) Mandates for Sustainability
This definition implies that IPM employs In our view, there are three mandates to be
ecologically based management processes addressed in assuring sustainability of agri-
developed with an understanding of natural cultural production systems. Contributions
cycles and natural regulators of those species of IPM are critical to meeting these eco-
that compete with humans for resources in nomic, environmental and social mandates.
agricultural production systems (Cate and
Hinkle, 1994). Successful IPM programmes,
by this definition, are those that will enhance Economic mandate
the profitability of the agricultural enterprise
and protect the environment for the indefi- Economic considerations basic to IPM are
nite future. consistent with the requirement for prof-
Our basic premise that IPM is essential to itability in sustainable agricultural systems.
sustainability stems from our contention that Rather than insisting upon eradication of
insect pests, pathogenic microorganisms and pests, an understanding has evolved with
weeds pose substantial threats to yields and the development of IPM that low population
quality of agricultural commodities. It is densities of pests usually do not threaten the
essential to the productivity and profitability profitable production of agricultural com-
of agriculture that effective means for regu- modities. While this concept is accepted
lating these species be employed. Production most readily in the discipline of entomology,
systems that do not include effective pest it has support in plant pathology and weed
regulation cannot remain profitable over the science as well. This aspect of IPM philoso-
long term; stated another way, they cannot phy has resulted from the development of
be sustainable. Also of great concern have ‘economic injury level’ and ‘economic
been the increasing difficulties experienced threshold’ concepts (Stern et al., 1959). The
over the last 50 years resulting from reliance economic injury level concept is based on the
on single control agents, particularly chemi- assumption that a pest species must be pre-
cal pesticides. One of the first to voice these sent at some minimum population level
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Sustainability of Agricultural Production Systems 267

before losses resulting from that species will which may be potential pollutants, and
exceed the cost of available controls, typi- farming practices such as tillage operations,
cally the cost of applying chemical pesti- which may contribute to soil erosion, be
cides. Derived from the economic injury employed in a manner that does not result in
level is the economic threshold, the operative the degradation of soil and water. In addi-
concept for decision making regarding pesti- tion, there is increasing concern about farm-
cide applications, in particular. The economic ing inputs and operations that threaten
threshold is defined as ‘the pest population wildlife species, either by direct mortality or
level at which the potential loss exceeds the by disruption of habitats. The contention has
cost of control’. When control applications been made that there is an overemphasis on
are made at the time that pest populations removing pests from agricultural systems,
have reached this defined population den- even when concepts of IPM are employed.
sity, as determined by systematic sampling Perhaps more attention should be paid to
in commodity-production areas, maximum integrated ‘habitat’ management, addressing
profits from the pest-control enterprise in a broad sense the influence of habitat
accrue to farmers. modifications in agriculture on pests and
The economic injury level/economic other species that may be present (Zorner,
threshold concept is employed in regulation 2000).
of most key insect pests and is being adopted The appropriate use of chemical pesti-
with some modifications in control pro- cides in agricultural production systems has
grammes for plant-pathogenic microorgan- been central to the development of IPM
isms and weeds, for which sampling since its inception (Newsom, 1967; Smith,
methods and timing of controls may differ 1970). Through IPM, the judicious use of
from what are usual for insect pests. This artificial pest controls, particularly chemical
sequence of sampling to assess the preva- pesticides, is emphasized to: (i) preserve
lence of pests followed by decision making natural control agents, such as ento-
using criteria of economic thresholds sup- mophagous insects, and beneficial micro-
ports the basic tenet of both IPM and sus- organisms; (ii) decrease the potential for
tainable agriculture, i.e. production systems mortality of an array of non-target organ-
must be economically viable over the long isms, such as wildlife species; and (iii) limit
term. In this regard, the economic injury the accumulation of toxic residues in the
level and economic threshold are parameters environment. Much more work is needed to
that not only serve as criteria for decision develop the same level of comprehensive
making, but are also important for defining understanding of effects of habitat modifica-
the contribution of effective pest manage- tions typical of agricultural ecosystems on
ment to the sustainability of production sys- the whole array of plant and animal species
tems. As the frequency of pest occurrence at in residence. Greater efforts to address con-
population densities exceeding the cost of cerns about habitat preservation for natural
available controls and the profitability of enemies of pests and for wildlife species are
pest-control measures are summarized over being initiated.
time, the value of pest management in pro-
duction systems can be estimated.
Social mandate

Environmental mandate Health and well-being are highly valued in

societies around the world, resulting in
The idea that profitability in agricultural pro- demands for a safe, wholesome food supply
duction and protection of the environment that is produced without harm to the envi-
are jointly attainable goals is central to the ronment or hazards to those who work in
philosophy of IPM and sustainable agricul- agriculture. Meeting this mandate for the
ture. It is critical to sustainability that the use indefinite future may be quite challenging
of off-farm inputs such as agrochemicals, because of the added expectation in many
12IntpestManCh12.QXD 14/4/04 2:26 pm Page 268

268 G.W. Cuperus et al.

countries that food must remain relatively implementation of IPM, even when pro-
inexpensive and be free of any traces of grammes involve the use of the products of
damage by pests. To the present time, pesti- biotechnology such as genetically modified
cides have provided the primary means for crops, are a sound investment of resources in
limiting pest populations so that abundant support of sustainable agricultural produc-
supplies of unblemished produce are made tion for the future.
available. However, it seems apparent that
consumers in the USA may regard the use of
pesticides as the most critical hazard to a Developing Resources for IPM in the
safe food supply (Pomerantz, 1995). Clearly, Future
the demands of people around the world for
a safe, abundant food supply can be met Our intent in this section is not to develop an
only by the development of sustainable agri- exhaustive review of all resources that may
cultural systems that can effectively com- possibly contribute to more effective pest
bine pest controls with profitability and the management for the future, but to select sev-
maintenance of a safe environment and eral topic areas that will make essential con-
human food supply. While pesticides are tributions to sustainable agricultural
most often cited as the most serious threat to systems. Among the disciplines of entomol-
food safety, there is a great need for ogy, plant pathology and weed science, there
improved understanding of the hazards is a wide array of ecological considerations
posed by bacterial and fungal contaminants and pest controls that may have utility in the
in food commodities. In addition to provid- design and implementation of IPM pro-
ing a safe and effective means for reducing grammes. We have selected several types of
damage to commodities by all types of resources for our discussions, realizing that
pests, IPM is also the primary means by there are other resources with which those
which hazards of both chemical and micro- we describe will be integrated in developing
bial contamination of food commodities IPM programmes. Also important is the con-
may be greatly decreased. cept that specific resources may have limited
Public understanding must be extended value for pest control until they are com-
beyond somewhat vague misgivings about bined in comprehensive programmes, and
the safety of the environment and the human we have included a commentary relating to
food supply. Strong negative reactions by the integration of resources in the sections to
people in several countries to the production follow.
of food commodities using genetically modi-
fied plants or animals have left little doubt of
the need to educate the public regarding Diagnostic tools
risks and benefits associated with the prod-
ucts of biotechnology. It is critical, as well, Effective management decisions depend
that the public be informed about the poten- greatly on accurate diagnosis of pest species or
tial for pests of all types to limit the availabil- biotypes/races in association with symptoms
ity of foods and certainly to cause food observed in crops or livestock. The need for
prices to increase. The perception of an accurate diagnosis is steadily becoming more
unlimited supply of cheap food that exists in acute as particular biotypes/races within pest
many countries could rapidly be proved an species adapt to pesticides, crop cultivars or
illusion if effective means of pest manage- genetically modified strains. While identifica-
ment are not maintained through judicious tion of pest species by anatomical or structural
use of existing control technologies and con- features was once sufficient for most instances
sistent investments in research to develop of pest diagnosis, the more typical case now
new avenues for pest control for the future. and in the future will involve more complex
Through deliberate and persistent educa- procedures involving immunological or
tional efforts, the public must come to appre- nucleic-acid analyses. The most common
ciate that the development and immunological approaches involve one of
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Sustainability of Agricultural Production Systems 269

three methods for labelling antibodies: (i) with ning appropriate agronomic and pest-control
enzymes, such as in the enzyme-linked operations. These presentations, when com-
immunosorbent assay (ELISA); (ii) with pared over time can provide important
coloured particles; and (iii) with materials insights on patterns of weed interference and
such as radioisotopes or fluorophores. These areas most likely to be infested by insects or
approaches have great utility for detecting the plant pathogens. For soil insects such as the
presence of specific pathogens in plants or for lesser cornstalk borer, Elasmopalpus lignosel-
testing insect-species populations that may lus (Zeller), that exhibit spatial patterns in
serve as vectors for plant pathogens for the fields that are greatly influenced by soil tex-
presence of specific microorganisms. Their use ture and drainage (Berberet et al., 1986), the
is increasing greatly for detection of specific application of GIS technology can provide
microbial products, such as toxins of the bac- valuable maps to assist in scouting and deci-
terium, Bacillus thuringiensis (Bt), that are pre- sion making for controls. Mapping over large
sent in genetically modified crop cultivars. areas can provide important information on
Diagnostic kits are available for identifying broad migrational patterns of insects and
several viruses that infect plants, such as movement from field to field. For both tar-
cucumber mosaic virus and tomato spotted- geted sampling and area-wide management,
wilt virus, in the field. Also available are field GIS/GPS technologies will be critical for the
kits for differentiating between eggs of the cot- incorporation of IPM into precision agricul-
ton bollworm, Helicoverpa zea (Boddie), and ture for the future (Ellsbury et al., 2000).
those of the tobacco budworm, Heliothis
virescens (Fabricius) (Agdia Inc., Elkhart,
Indiana). Weather forecasting
The same concept can be used in the
preparation and labelling of nucleic-acid Accurate weather forecasting and record
probes developed for polymerase chain reac- keeping are essential for IPM programmes.
tion (PCR) processes that are being used to Weather data will continue to be important
detect viruses and other types of organisms in two primary ways. The first of these is to
that may be targeted in IPM programmes. It provide basic information that, when cou-
is remarkable that many of these diagnostic pled with species population data, is used in
processes have been adapted for field use or preparing models of seasonal life histories or
for field collection of samples for rapid labo- life systems for crops or pests. For example,
ratory processing when response time is crit- insects and plants are poikilothermic, and
ical, as is often the case for decision making temperature conditions are usually the pri-
regarding the application of pest-control mary determinant for population growth in
agents. It is clear that the availability of these these species. In comparison, for fungal
techniques will continue to increase and pathogens of crops or of insects, rainfall and
greatly enhance more traditional diagnostics relative humidity conditions are major deter-
that employ morphological examinations minants for the prevalence of infections. The
and bioassays. models generated from weather data and
Other important technologies that will results of sampling are based on events that
enhance the value and application of infor- have occurred and are often used in simula-
mation made available through improved tions to develop predictions about future
diagnostic capabilities are geographical events, such as population increases in insect
information systems (GIS) and global posi- species or increased prevalence of infection
tioning systems (GPS). These systems have a by a fungal pathogen, given certain weather
great capacity for organizing, mapping and conditions.
applying information from a variety of diag- The second major application of weather
nostic processes. The capability exists for data is in decision making for current or
farmers to map soil types, topography, soil future pest-control activities. By coupling
fertility and spatial patterns for pest infesta- current weather data with the predictions
tions within individual fields for use in plan- based on models, forecasts for crop develop-
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270 G.W. Cuperus et al.

ment or pest activity are prepared. These IPM programmes because they not only
forecasts often have great value in allowing directly reduce losses due to pests but have
farmers to conduct pest-control activities in a also performed well in combination with
more timely manner, which is often critical – pesticides, biocontrols or other approaches in
with applications of fungistatic compounds comprehensive management programmes.
for limiting infections of pathogens, for An excellent example of the contributions of
example. Weather parameters such as traditional breeding exists in the lucerne
degree-day accumulations for insect devel- crop, for which there are currently over 200
opment or relative humidity conditions will cultivars registered in the USA, covering all
be increasingly important in regard to ranges of winter dormancy, from those well
improved decision making for pest-control adapted for production in Canada to those
activities. suited for southern California. These culti-
Major improvements in data collection for vars have varying degrees of host resistance
IPM programmes have occurred with the to over ten insect pests and plant pathogens
establishment of weather networks, such as that occur in different regions of the world
the Oklahoma Mesonet system. This system (Anon., 1999).
collects weather data at 117 sites in While products of traditional plant breed-
Oklahoma, which are used to develop com- ing will continue to be important for
prehensive summaries of current and past improved productivity of crops and applica-
conditions. Integrated with this system are a tions in IPM, the advent of biotechnology
number of programmes that make important has over the last 10 years resulted in the
contributions to IPM in the state, such as cal- development and release of crop
culations of degree-day accumulations for germplasms that are already making remark-
development of the lucerne weevil, Hypera able contributions to agriculture. It is not
postica (Gyllenhall). These calculations are possible at this time to even estimate realisti-
used in conjunction with current field-sam- cally the great potential of transgenic plants,
pling data for decision making relative to the not only for pest management but also for
need for insecticide applications (Berberet the production of foods with enhanced nutri-
and Mulder, 1993). Increasingly, site-specific tional qualities, pharmaceuticals for human
weather-data systems are being developed health and a variety of industrial products,
that will enhance decision making on farm- such as plastics. Two major contributions for
by-farm or field-by-field bases in the future. IPM to date have involved insect-protected
One such service currently operating is cultivars and those with tolerance to herbi-
SkyBit, Inc. (Boalsburg, Pennsylvania, USA), cides. Insect-protected cultivars, such as
a company that has pioneered the imple- BOLLGARD® (INGARD®) cotton, into which
mentation of automated weather services at genes controlling production of endotoxins
the farm scale (Russo, 2000). Improved in the bacterium Bt have been placed are
means for obtaining and applying weather already showing excellent results in limiting
data are essential for both agronomic and damage by the cotton bollworm, H. zea
pest-management decisions in crop produc- (armigera), and tobacco budworm, H.
tion. virescens, in the USA and several other coun-
tries, such as Australia, China and Argentina
(Fitt and Wilson, 2000). The efficacy of
Transgenic plants BOLLGARD® cotton has permitted reduc-
tions of >50% in insecticide applications and
Traditional plant-breeding approaches have has greatly enhanced IPM programmes
provided high-yielding, pest-resistant crops through increased populations of beneficial
that have made major contributions to mod- insects and ready integration with selective
ern agricultural systems, in terms of both insecticides and cultural controls. The tech-
overall productivity and limiting losses due nology used to transfer genes from B.
to insect pests and plant pathogens. In a very thuringiensis into crop plants can also be
real sense, these cultivars have been basic to used to incorporate genes controlling pest-
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Sustainability of Agricultural Production Systems 271

resistance factors from a variety of plant inception of the IPM concept. Initially, the
sources into cultivated crops. approach that generated the greatest interest
To date, the greatest number of US was classical biological control, i.e. introduc-
Department of Agriculture (USDA) permits ing beneficial species to control introduced
issued for regulated technologies relating to pests. There have been many instances of
transgenic plants have been for herbicide- successful control of pest species by the clas-
tolerant crops. Of over 30 million ha of these sical approach. This approach will clearly
crops planted worldwide in 1998, about 80% remain quite important for the future, espe-
were located in the USA. The most widely cially with the problem of introduced pests
grown have been maize, soybeans and cot- becoming more serious around the world,
ton having tolerance to glyphosate (Hess and and the critical need to identify and intro-
Duke, 2000). However, there are many culti- duce natural enemies to regulate the popula-
vars available each with tolerance for one of tions of these pests. For both insect (and
several herbicides in addition to glyphosate. other arthropod) pests and weeds, there is a
These cultivars hold great promise for IPM great need worldwide for increased explo-
because they allow farmers to replace pre- ration, identification of species (and bio-
emergence herbicide applications made types/races) of potentially effective natural
without assessing weed interference with enemies and importation/establishment of
post-emergence applications that are need- these natural enemies in regions where intro-
based. Further, the herbicide-tolerance trait duced pests are causing damage. Along with
can be combined with insect or disease resis- emphases on classical approaches, the poten-
tance in cultivars to form the foundation for tial for effective biological control by both
pest-management programmes (Hess and augmentation and conservation of natural
Duke, 2000). As with insect-protected culti- enemies for a large number of important pest
vars, the contributions of herbicide-tolerant species, including insects, plant-pathogenic
cultivars can be great, especially when cou- microorganisms and weeds, must be real-
pled with considerations such as reduced ized.
soil erosion in crops, made possible because Although there have been extensive pro-
reduced tillage systems are enhanced with grammes for the mass rearing and release of
these cultivars. beneficial insects, such as Trichogramma spp.,
The potential is great for contributions by to control a variety of insect pests, perhaps
transgenic plants to enhance productivity the greatest potential for successful biologi-
and pest management in all types of crops. cal control through augmentation of natural
Currently, it appears that this potential may enemies exists with pathogenic microorgan-
be limited by concerns of the general public isms, those infecting insects or weeds and
about the acceptability of transferring genes those that compete with plant-pathogenic
among plant and animal species. This con- agents. Currently, there are about 20
cern has been fuelled by relatively small microorganisms used in formulating regis-
groups of people having great fears about tered microbial insecticides in the USA.
application of gene-transfer technology in While most of these are bacteria, there are
agriculture. Clearly, the future of transgenic also preparations of several viruses and
crops and the future availability of this fungi. These products are applied on about 1
tremendous resource for sustainable agricul- million ha annually (Federici, 2000). The util-
tural production are greatly dependent upon ity of these agents has been limited by diffi-
public education and acceptance around the culties in the production and formulation of
world. products, particularly with viruses and
fungi, and by limited spectra of activity
against pest complexes in comparison with
Biological control chemical insecticides. However, recent
research has indicated that the efficacy of
Biological control was regarded as an impor- bacteria and viruses may be improved
tant tool for managing pests before the through recombinant DNA technology
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272 G.W. Cuperus et al.

(Baum et al., 1998; Treacy, 1998). The advan- cidal agents are currently being investigated
tages of microbial insecticides over chemical for possible registration. Clearly these prod-
insecticides in terms of reduced threats to ucts could make valuable contributions in
non-target species and limited potential for the future to IPM programmes where it is
environmental degradation are compelling desirable and profitable to target particular
reasons for increasing efforts to improve weed species with agents that do not have
these agents and increase their utility for adverse effects on non-target species. In
IPM programmes. reviewing the range of products and applica-
Although the use of such products has tions that have been identified using micro-
not covered large areas, the integration of bial formulations for the control of insects,
biological control agents for plant pathogens plant pathogens and weeds, it seems appar-
into IPM programmes has become more ent that these agents will make important
common since the early 1990s. Currently, contributions to IPM programmes in the
there are more than 35 commercial products future.
available for the control of plant-pathogenic Habitat management to enhance the sur-
organisms (Loper and Stockwell, 2000). vival and increase the effectiveness of nat-
Notable success attained with two agents in ural enemies is the aim of conservation
the USA – Agrobacterium radiobactor K84, for biological control (Barbosa, 1998). While it is
control of crown gall in nursery tree crops not possible to avoid all disruptions to bene-
caused by Agrobacterium tumefaciens, and ficial species in farming systems, the goal of
Pseudomonas fluorescens A506, for control of habitat management in IPM is to develop
fire blight in pome fruits caused by Erwinia systems that favour natural enemies over
amylovora – has clearly demonstrated that pest species. The relatively newly defined
there is great potential for the biological con- discipline of landscape ecology examines
trol of plant pathogens. The value of these structure, function and change in ecosys-
and other biological controls for plant tems. To enhance the conservation of natural
pathogens is enhanced by their utility in IPM enemies, disturbance regimes in agricultural
programmes where they have been used in production systems must be understood
combination with cultural controls and even (Landis et al., 2000). For successful conserva-
some types of chemical pesticides (Loper tion programmes, resources must be made
and Stockwell, 2000). available in cropland areas and in adjacent
Seven products that are formulations con- riparian areas to sustain beneficial species
taining microorganisms used as bioherbi- throughout the year. An excellent example of
cides have been registered since 1980. These habitat management for the enhancement of
products have emerged from a total of about natural enemies are the so-called ‘beetle
250 agents having proved efficacy for weed banks’ employed in Europe, where raised
control. There has been relatively little inter- strips have been planted to grasses within
est from the agrochemical industry in these fields to provide overwintering sites for ben-
agents because of their host (target) speci- eficial insects (Thomas et al., 1992). Studies in
ficity and limited sales potential in compari- the USA have also demonstrated the value of
son with chemical herbicides (Charudattan, providing ‘refuge strips’ for beneficial insects
2000). The first of these products to be regis- within fields or at field edges (Landis et al.,
tered in the USA, a preparation of 2000). In many instances, habitats for natural
Phytophthora palmivora called DeVine®, has enemies can be provided within areas that
been in use since 1980 for the control of are established in fields or adjacent to fields
strangler-vine, Morrenia odorata, in Florida for purposes other than the conservation of
citrus-production areas (Kenney, 1986). beneficial species, such as grass waterways
Another product named Collego®, a formu- designed to reduce soil erosion and conser-
lation of Colletotrichum gloeosporioides f. sp. vation headlands established for soil, water
aeschynomene, has been registered for the and wildlife conservation. In the coming
control of northern joint-vetch, Aeschynomene years, studies in landscape ecology will
virginica. At least 12 other potential bioherbi- make great contributions to IPM, aiding in
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Sustainability of Agricultural Production Systems 273

the design of habitat management systems some crops, such as cotton, lucerne and
that enhance the activity of the natural ene- apples. It is essential that research continues
mies of pests while conserving soil and in the future to develop even more accurate
water for the increased productivity of crops. and efficient sampling/decision-making
Simply put, these studies will be essential for processes.
the sustainability of crop production sys- Additionally, improving the effectiveness
tems. of alternative controls has resulted in
Also essential to conservation and the reduced reliance on chemical pesticides, as
enhancement of beneficial species in crop has occurred in lucerne production in the
production is an improved understanding of USA. The release of a broad array of multiple-
the potential effects of pest-resistant cultivars pest resistant cultivars has greatly reduced
developed by traditional breeding the need for insecticide applications against
approaches and transgenic, insect-protected species such as the spotted lucerne aphid,
cultivars on successful biological control Therioaphis trifolii f. maculata (Buckton), and
with parasitoids and predators. Knowledge the pea aphid, Acyrthosiphon pisum (Harris).
of the multitrophic effects of these cultivars Also, successful biological control of the
may offer opportunities to reduce potential lucerne weevil with several species of
deleterious effects on beneficial species hymenopteran parasites has greatly reduced
and/or allow opportunities for the incorpo- the need for insecticide applications in the
ration of traits that will enhance the effec- eastern and central areas of the USA
tiveness of these species. (Kingsley et al., 1993).
Much greater efficiency and sustainability
in the use of chemical pesticides for the
Chemical pesticides future will be related to the development
and registration of new types of products.
Since the early 1950s, chemical pesticides Since 1980, several new classes of insecti-
have been the predominant input for pest cides, fungicides and herbicides have been
control in agricultural production systems. developed and registered that require the
The role of chemical pesticides as the most application of but a small fraction of the
commonly used tool for the regulation of active ingredient that has been typical of pes-
pests has not changed greatly since the ticides registered previously to give highly
inception of IPM. Although the use of pesti- effective pest control. Among these com-
cides is expected to decline with the adop- pounds are the strobilurin fungicides (e.g.
tion of IPM, it is important to state that azoxystrobin), sulphonylurea herbicides (e.g.
elimination of chemical pesticides is not prosulphuron, triasulphuron) and insecti-
regarded as a goal of IPM. Still, there are sev- cides such as neonicotinoids (e.g. imidaclo-
eral objectives for IPM programmes that prid), spinosyns (e.g. spinosad) and
relate to these compounds, including: (i) avermectins (e.g. emamectin benzoate).
reduced reliance on chemical pesticides as These compounds and other new chemistries
unilateral controls for pests; (ii) decreasing yet to be discovered will greatly enhance the
the potential for the disruption of non-target contributions of chemical pesticides to IPM
species, such as natural enemies of pests; programmes by providing a high degree of
and (iii) limiting contamination of the envi- efficacy while posing limited threats of non-
ronment by residues of pesticides. Progress target toxicity and environmental contami-
has been made in addressing these objectives nation.
through improved pest monitoring and New types of compounds and improved
decision-making processes relating to pesti- application equipment must be combined
cide applications. Use of more efficient and with improved decision-making processes to
accurate sampling procedures and employ- promote the safest and most efficient use of
ing economic thresholds in treatment deci- chemical pesticides for the future. The use of
sions has resulted in reductions in pesticide pesticides in IPM programmes in a manner
use, particularly in insecticide applications in that contributes to the sustainability of agri-
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274 G.W. Cuperus et al.

cultural systems for the indefinite future will the sustainability of agricultural production
require the adoption of the fundamental systems could be placed at risk. Resistance to
principles proposed below (adapted from chemical pesticides is described by the
Dennehy, 2000): World Health Organization as ‘the develop-
ment of an ability in a strain of some organ-
• Limiting the use of pesticides to condi-
ism to tolerate doses of a toxicant which
tions where the potential for losses due to
would prove lethal to the majority of indi-
pests exceeds the cost of control (applica-
viduals in a normal population of the same
tion of economic thresholds) and/or there
species’ (World Health Organization, 1957).
is no effective alternative to these com-
We define resistance to transgenic, insect-
pounds.
protected cultivars in a similar manner as
• Selecting pesticides that are most compat-
‘the ability of an arthropod species or plant
ible with other components of the IPM
pathogenic organism to grow and reproduce
programme. The development and regis-
on plants that would not normally serve as
tration of new types of compounds holds
suitable hosts for the species’. Since the
great promise for more effective integra-
report of resistance in the San José scale,
tion of chemical and non-chemical con-
Quadraspidiotus perniciosus (Comstock), to
trols.
lime sulphur (Melander, 1914), the problem
• Applying appropriate rates of active
of pest adaptation to chemical insecticides
ingredients, taking into account the
and/or acaricides has become increasingly
required efficacy, the potential non-target
more serious. Currently, a total of over 500
effects of compounds and the safety of
species of Arthropoda have developed resis-
food commodities for consumers.
tance to chemical pesticides (Pedigo, 1999).
• Using application technology that pro-
The efficacy of many chemical insecticides
vides the greatest safety for those who are
and acaricides has been compromised and
applying pesticides, the lowest probabil-
many have been rendered completely inef-
ity of drift into non-target areas and the
fectual against certain pests. For some
best protection against unwarranted envi-
species, such as the Colorado potato beetle,
ronmental contamination.
Leptinotarsa decemlineata (Say), effective con-
trol with chemical insecticides has become
nearly impossible because of resistance to
Meeting the Challenges Posed by Pest chemical toxicants, including even the most
Adaptation recently registered materials, such as imida-
cloprid (Ferro, 2000). Laboratory studies
One of the greatest challenges to the long- have shown the potential of pest adaptation
term contributions of IPM programmes to to other new forms of insecticides, as in the
the sustainability of agricultural systems is case of the tobacco budworm, H. virescens,
adaptation by pests, a phenomenon with exhibiting a resistance ratio greater than 355-
demonstrated potential to render ineffectual fold after 11 generations of selection with
several important types of control agents, spinosad (Bailey et al., 1999).
including chemical pesticides, crop cultivars Before the registration of fungicides hav-
developed by traditional plant breeding and ing systemic properties and fairly specific
transgenic, insect-protected cultivars. It is modes of action began in the late 1960s, there
essential to continued progress for the devel- had been relatively little evidence of resis-
opment and implementation of IPM pro- tance in plant pathogens to the conventional
grammes that the efficacy of these agents be dithiocarbamate (e.g. maneb) and phthalim-
preserved through the adoption of strategies ide (e.g. captan). These fungicides exhibit a
that allow them to be used indefinitely with- non-specific mode of action, to which the
out selecting for resistant populations of pathogens apparently cannot adapt (Koller,
pests. If adaptation by key pests to these 1991). However, the resistance of pathogens
essential resources for IPM continues at the to newer classes of compounds, such as the
rate, that has occurred since the early 1970s, benzimidazoles (e.g. benomyl) and phenyl-
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Sustainability of Agricultural Production Systems 275

amides (e.g. metalaxyl), has resulted in many strains of pests should they evolve in the
control failures and the need to apply mix- field.
tures of fungicides and to introduce alterna- Resistance detection should include an
tive compounds in some crops to achieve array of biochemical, immunological, molec-
consistent disease control (Koller, 1991). ular and bioassay approaches. The objective
Before 1970, there were no proven cases of of these methods is to detect/identify the
resistance in weeds to chemical herbicides presence of members of pest populations
(Georghiou, 1986). In part, the absence of having specific enzymes or other proteins
resistance could have been due to traditional that may be important in detoxifying active
emphases on non-chemical controls, such as ingredients in pesticides or bacterial endo-
tillage and crop rotation. Also, many weeds toxins (Roe et al., 2000). Several of these
complete only one reproductive cycle (gener- approaches are similar to those described in
ation) per year and have long seed- the section on diagnostics for purposes of
dormancy periods, which may reduce the pest identification and the delineation of
rate of adaptation in comparison with insects races or biotypes. Bioassays could be used at
and plant pathogens. However, proven regular intervals to test samples of pests for
instances of herbicide resistance in weeds are increasing levels of tolerance/resistance to
increasing rapidly with reduced-tillage sys- toxicants. The ‘feeding-disruption assay’ is a
tems and greater usage of these compounds. specific type of bioassay that has been devel-
Over 50 species have been proved to be resis- oped to detect changes in susceptibility to
tant to triazine herbicides and, more recently, the endotoxins of B. thuringiensis in popula-
some species with resistance have been tions of the cotton bollworm and tobacco
reported to have evolved resistance to the budworm (Roe et al., 2000).
sulphonylurea compounds (e.g. chlorsul- The management of resistance in pest
phuron). species to active ingredients in synthetic
Adaptation to resistant crop cultivars chemical pesticides or microbial toxins is a
developed through traditional breeding major challenge to the sustainability of agri-
approaches has been proved for many insect culture. Basically, resistance-management
pests (Nielson et al., 1970; Zarrabi et al., 1995; programmes require first that an effective
Porter et al., 2000; Ratcliffe et al., 2000) and plan be formulated with input from
plant pathogens (Masterbroek, 1984; Kolmer researchers, extension specialists, consul-
and Dyck, 1994; Young et al., 1994). The tants, representatives of agribusiness and
potential for pest adaptation to transgenic, clientele groups that are to be the end-users.
insect-protected cultivars such as those that A basic premise for these plans should be the
produce the toxins of B. thuringiensis, cannot limitation of pesticide use in accordance with
be denied. Resistance to endotoxins pro- appropriate decision-making criteria for
duced by B. thuringiensis when the bacterium applications. The types of toxicants used
is applied as a microbial insecticide has should be diversified, with excessive reliance
already been proved (Tabashnik et al., 1990). on any particular mode of action being elimi-
It is critical to IPM programmes for the nated. There should be serious attempts to
future that protocols be developed to guide utilize alternatives to pesticides and to har-
the appropriate integration of innovative monize pesticide usage with all other types
types of chemical pesticides and transgenic of controls that are included in the IPM pro-
plants into IPM programmes. The efficacy of gramme for the particular crop(s) involved.
these valuable resources must be protected Secondly, the management plan must be
to the greatest extent possible for the long implemented through extensive education
term. This will necessitate the wide-scale programmes with all potential end-users.
adoption of aggressive methods for the Crop consultants and representatives of the
detection of resistance in pests and the agrochemical and seed industries must be
implementation of resistance management closely involved in implementation. This
plans to reduce the possibility of pest adap- step relies heavily on aspects of communica-
tation and limit the spread of resistant tion and adoption, which are discussed in
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276 G.W. Cuperus et al.

the next section of this chapter. Thirdly, as limited potential for long-term efficacy of
the plan is implemented, monitoring proce- these agents when there are no management
dures must be used to allow continual evalu- plans designed to reduce pest adaptation.
ation of the efficacy of the management The record shows literally hundreds of cases
strategies. Regular sampling of pest popula- of pest resistance to these compounds. There
tions, with testing to detect the presence of is no clear reason to suggest that experience
resistant individuals in pest populations, with transgenic plants would be different
must be conducted. Finally, the plan must be from what has already occurred with prod-
flexible enough to allow modifications when ucts of traditional plant breeding and with
they are required based on results of moni- chemical pesticides. In fact, instances of pest
toring or of ongoing research. adaptation to cultivars developed by tradi-
An ongoing programme following this tional plant breeding are abundant. It is in
model for resistance management has oper- formulating plans to promote the lasting
ated successfully in Arizona dealing with the effectiveness of these essential resources for
silver-leaf whitefly, Bemisia argentifolii agriculture that the principles of IPM will
Bellows & Perring, in winter vegetables, mel- have great value. These plans will rely on the
ons, lucerne and cotton (Dennehy, 2000). The effective integration of control measures and
primary purpose of this plan has been to realistic analyses of benefits, risks and costs
maintain the effectiveness of several types of relative to all aspects of pest-control pro-
insecticides, including insect growth regula- grammes, considerations that are viewed as
tors (buprofezin and pyriproxyfen), syn- strengths of IPM.
thetic pyrethrins and imidacloprid, in
attaining effective, long-term control of the
whitefly and other insect pests, such as Lygus Communication is Critical to the
bugs. Adoption of IPM by End-users
A similar design has been used in formu-
lating a resistance-management plan To provide the greatest contributions
designed to sustain the effectiveness of the towards the sustainability of agricultural
transgenic cotton, INGARD®, against the systems, the improvement in resources for
cotton bollworm/tobacco budworm in IPM resulting from innovative research
Australia under the direction of the efforts must be matched by more effective
Transgenic and Insecticide Management efforts to promote the adoption of pest-man-
Strategy (TIMS) Committee (Fitt and Wilson, agement programmes. Our discussion to this
2000). The primary elements of this plan point has addressed several types of
include: resources that are essential to the enhance-
ment of IPM programmes. For these
• Placement of refuges (susceptible cotton)
resources to be utilized effectively there is a
on each farm where INGARD® cotton is
critical need for improved information trans-
grown.
fer among all groups who work in the devel-
• Enforcement of a defined planting sched-
opment, implementation and application of
ule for INGARD® cotton.
IPM. Our comments will pertain primarily to
• Mandatory cultivation of crop residues to
means for improving communications
destroy overwintering insect pupae.
among researchers, extension specialists,
• Use of defined economic thresholds to
consultants, representatives of agribusiness
control surviving cotton bollworms.
concerns and farmers, all of whom must
• Regular monitoring of Bt resistance levels
work cooperatively to achieve the greatest
in field populations.
success in the adoption of IPM.
Resistance-management plans signal a A critical aspect that must be addressed is
radical departure from what has been the more effective communication and coopera-
usual approach for pesticide applications tion among scientific disciplines. Our inten-
since the early 1950s. We have abundant tion is not to suggest that such cooperation
information and experience regarding the does not exist or that there are no examples
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Sustainability of Agricultural Production Systems 277

of excellent interdisciplinary programmes. For IPM to make the greatest possible

However, with the passage of over 30 years contribution to the sustainability of agricul-
since cooperation among scientists was first ture, a critical aspect of information transfer
promoted under the banner of IPM, disci- must be an effective dialogue between farm-
plines such as entomology, plant pathology, ers and those who develop the programmes
weed science, and economics continue to use and market the technology and services. The
different vocabularies when addressing con- utility of resources developed for pest man-
cepts such as the definition of IPM, formula- agement depends greatly on how well these
tion and application of economic thresholds resources can be adapted to the needs and
and problems/solutions relating to races/ priorities of individual farmers. While con-
strains/biotypes within pest species that cepts of IPM are often expressed as general
have adapted to pesticides or host-plant principles, applications in IPM must be site-
resistance. In the process of planning all specific. Those who develop IPM pro-
aspects of IPM programmes, scientists from grammes must constantly monitor success in
these disciplines must concentrate not only the application of these programmes and be
on the critical resources and components prepared to make adjustments as these are
needed but also on more effective means of needed. One of the best ways to monitor the
communicating among the disciplines and effectiveness and to improve the adoption of
with clientele. Often, potential end-users of IPM is to seek feedback from the end-users.
information are required to interpret ‘mixed Information transfer is not intended to be
messages’ coming from specialists within solely from those in academia, consultancies,
disciplines that may actually pertain more to and industry to the farmers.
different vocabularies than to disagreement Although fact sheets, farmer meetings
on basic pest-management approaches. and field days will continue to provide
While progress has certainly been made, important avenues for communication for
much work remains for the delivery of more the adoption of IPM, the Internet is a new
fully integrated programmes communicated resource that offers great potential for
to farmers with a more integrated vocabu- improving information transfer. The Center
lary for pest management. for Integrated Pest Management located at
A second issue to be addressed regarding North Carolina State University (http://
information transfer relates to more effective cipm.ncsu.edu) was founded in 1991 to
interaction of researchers and extension spe- enhance programme development and com-
cialists with crop consultants and representa- munication for IPM. This centre was among
tives of agribusiness in delivering pro- the first to promote IPM information sharing
grammes to farmers. The consultants and on the Worldwide Web and now supports an
business representatives have a vested inter- Internet system with cooperators in over 35
est in the success of farmers and must be fully states within the USA. Another effort,
engaged in communicating the most cost- involving federal–state cooperation in the
effective and safest means of management to USA, to make the latest and most accurate
end-users. Pest management is becoming an pest-management information available to
increasingly complex aspect of agricultural users is the National IPM Network
production, and farmers often require assis- (http://www.ipm.ncsu.edu). Many addi-
tance in developing the technical skills neces- tional websites have been established to
sary to adopt the current methods and address IPM in particular cropping systems,
technologies employed in IPM. It is in the best such as cotton (http://www.gaipm.org/
interest of farmers and consumers that coop- cotton/) and lucerne (http://www.agr.
erative relationships exist among all parties okstate.edu/alfalfa). And, the establishment
involved in the development and marketing of websites is by no means restricted to the
of products and services for agriculture. And USA, as sites are appearing around the
such cooperation can assist greatly in further world using the Internet to promote
reducing the volume of ‘mixed messages’ information transfer for IPM, including
with which farmers must contend. those in Australia (http://www.cse.csiro.au/
12IntpestManCh12.QXD 14/4/04 2:26 pm Page 278

278 G.W. Cuperus et al.

research), China (http://www.ipmchina. tions of the public to research into and the
net/) and Europe (http://www.ipmeurope. registration of transgenic crops have served to
org) (Stinner, 2000). emphasize the necessity for public education
It is difficult to predict the overall contri- and acceptance of methods used in crop pro-
butions of the Internet to enhanced informa- duction. Effective communication with the
tion transfer among those who develop, public regarding the goals and approaches for
market and employ resources for IPM, even IPM is critical to the sustainability of agricul-
within just the next 10 years. The potential of ture. Consumers must be educated to appreci-
Internet-driven information sharing world- ate the fact that safer, more effective means of
wide is virtually limitless. As technology pest management are constantly being devel-
improves to make Internet sites more inter- oped. In our opinion, the current turmoil
active and hardware resources are developed regarding transgenic crops has resulted, in
to make Internet access available to greater large measure, from a failure to communicate
numbers of end-users worldwide, the adop- the benefits and risks associated with the
tion of IPM programmes will increase dra- technology used in the development of these
matically. crops. A major challenge for the effective
In a world that is rapidly becoming more adoption of IPM is communication with the
and more urbanized, it is critical that consen- general public. The Internet must be
sus be developed in the general population to employed to meet this challenge just as it is
support needs attendant to production and employed to inform and educate farmers who
processing of food and fibre commodities. make the decisions to use IPM.
Recent experiences involving negative reac-

References

Anon. (1999) Fall Dormancy and Pest Resistance Ratings for Alfalfa Varieties. Certified Alfalfa Seed Council,
Davis, California
Anon. (2000) Definition for integrated pest management. USDA CSREES, Washington, DC. Available at:
http://www.reeusda.gov
Bailey, W.D., Young, H.P. and Roe, R.M. (1999) Laboratory selection of a Tracer-resistant strain of the
tobacco budworm and comparisons with field strains from the southeastern US. In: Proceedings of
the Beltwide Cotton Conference. National Cotton Council, Memphis, Tennessee, pp. 1221–1224.
Barbosa, P. (1998) Conservation Biological Control. Academic Press, San Diego, California.
Baum, J.A., Johnson, T.B. and Carlton, B.C. (1998) Bacillus thuringiensis, natural and recombinant bioinsec-
ticide products. In: Hall, F.R. and Menn, J.J. (eds) Methods in Biotechnology, Vol. 5, Biopesticides: Use
and Delivery. Humana Press, Totowa, New Jersey, pp. 189–209.
Benbrook, C.M. (1990) Society’s stake in sustainable agriculture. In: Edwards, C.A., Lal, R., Madden, P.,
Miller, R.H. and House, G. (eds) Sustainable Agricultural Systems. St Lucie Press, Delray Beach,
Florida, pp. 68–76.
Berberet, R. and Mulder, P. (1993) Scouting for the Alfalfa Weevil in Oklahoma. OSU Current Report CR-
7177, Oklahoma Cooperative Extension Service, Stillwater, Oklahoma.
Berberet, R.C., Wall, R.G. and Peters, D.C. (1986) The Lesser Cornstalk Borer: a Key Pest of Peanuts in
Oklahoma. Bulletin B-778, Oklahoma Agricultural Experiment Station.
Carson, R. (1962) Silent Spring. Fawcett Crest, New York.
Cate, J.R. and Hinkle, M.K. (1994) Integrated Pest Management: the Path of a Paradigm. National Audubon
Society, Washington, DC.
Charudattan, R. (2000) Current status of biological control of weeds. In: Kennedy, G.G. and Sutton, T.B.
(eds) Emerging Technologies for Integrated Pest Management. American Phytopathological Society
Press, St Paul, Minnesota, pp. 269–288.
Cuperus, G.W., Noyes, R.T., Fargo, W.S., Clary, B.L., Arnold, D.C. and Anderson, K. (1990) Successful
management of a high risk stored wheat system in Oklahoma. American Entomologist 36, 129–134.
12IntpestManCh12.QXD 14/4/04 2:26 pm Page 279

Sustainability of Agricultural Production Systems 279

Dennehy, T.J. (2000) Fulfilling the role of resistance management to preserve effectiveness of new insecti-
cide technologies. In: Kennedy, G.G. and Sutton, T.B. (eds) Emerging Technologies for Integrated Pest
Management. American Phytopathological Society Press, St Paul, Minnesota, pp. 400–417.
Ellsbury, M.M., Clay, S.A., Fleischer, S.J., Chandler, L.D. and Schneider, S.M. (2000) Use of GIS/GPS sys-
tems in IPM: progress and reality. In: Kennedy, G.G. and Sutton, T.B. (eds) Emerging Technologies for
Integrated Pest Management. American Phytopathological Society Press, St Paul, Minnesota,
pp. 419–438.
Federici, B.A. (2000) Genetically engineered pathogens of insects for IPM: concepts and status. In:
Kennedy, G.G. and Sutton, T.B. (eds) Emerging Technologies for Integrated Pest Management. American
Phytopathological Society Press, St Paul, Minnesota, pp. 163–176.
Ferro, D.N. (2000) Success and failure of Bt products: Colorado potato beetle – a case study. In: Kennedy,
G.G. and Sutton, T.B. (eds) Emerging Technologies for Integrated Pest Management. American
Phytopathological Society Press, St Paul, Minnesota, pp. 177–189.
Fitt, G.P. and Wilson, L.J. (2000) Genetic engineering in IPM: Bt cotton. In: Kennedy, G.G. and Sutton, T.B.
(eds) Emerging Technologies for Integrated Pest Management. American Phytopathological Society
Press, St Paul, Minnesota, pp. 108–125.
Georghiou, G.P. (1986) Pesticide Resistance: Strategies and Tactics for Management. National Academy Press,
Washington, DC.
Harwood, R.R. (1990) A history of sustainable agriculture. In: Edwards, C.A., Lal, R., Madden, P., Miller,
R.H. and House, G. (eds) Sustainable Agricultural Systems. St Lucie Press, Delray Beach, Florida,
pp. 3–19.
Hess, F.D. Sr and Duke, S.O. (2000) Genetic engineering in IPM: a case study: herbicide tolerance. In:
Kennedy, G.G. and Sutton, T.B. (eds) Emerging Technologies for Integrated Pest Management. American
Phytopathological Society Press, St Paul, Minnesota, pp. 126–140.
Kenney, D.S. (1986) De-Vine – the way it was developed – an industrialist’s view. Weed Science 34 (suppl.
1), 15–16.
Kingsley, P.C., Bryan, M.D., Day, W.H., Burger, T.L., Dysart, R.J. and Schwalbe, C.P. (1993) Alfalfa weevil
(Coleoptera: Curculionidae) biological control: spreading the benefits. Environmental Entomology 22,
1234–1250.
Koller, W. (1991) Fungicide resistance in plant pathogens. In: Pimentel, D. (ed.) Handbook of Pest
Management in Agriculture, Vol. II. CRC Press, Boca Raton, Florida, pp. 679–720.
Kolmer, J.A. and Dyck, P.L. (1994) Gene expression in the Triticum aestivum–Puccinia recondita fsp. tritici
gene-for-gene system. Phytopathology 84, 437–440.
Landis, D.A., Menalled, F.B., Lee, J.C., Carmona, D.M. and Perez-Valdez, A. (2000) Habitat management
to enhance biological control in IPM. In: Kennedy, G.G. and Sutton, T.B. (eds) Emerging Technologies
for Integrated Pest Management. American Phytopathological Society Press, St Paul, Minnesota,
pp. 226–239.
Loper, J.E. and Stockwell, V.O. (2000) Current status of biological control of plant diseases. In: Kennedy,
G.G. and Sutton, T.B. (eds) Emerging Technologies for Integrated Pest Management. American
Phytopathological Society Press, St Paul, Minnesota, pp. 240–256.
Masterbroek, H.D. (1984) Utility of defeated resistance genes to powdery mildew, Erysiphe graminis fsp.
hordei, in spring barley variety mixtures. Netherlands Journal of Plant Pathology 90, 257–265.
Melander, A.L. (1914) Can insects become resistant to sprays? Journal of Economic Entomology 7, 167.
Newsom, L.D. (1967) Consequences of insecticide use on non-target organisms. Annual Review of
Entomology 12, 257–286.
Nielson, M.W., Don, H., Schonhorst, M.H., Lehman, W.F. and Marble, V.L. (1970) Biotypes of the spotted
alfalfa aphid in western United States. Journal of Economic Entomology 63, 1822–1825.
Pedigo, L.P. (1999) Entomology and Pest Management. Prentice Hall, Upper Saddle River, New Jersey.
Pomerantz, M.L. (1995) A profile of the fresh produce consumer. The Packer 54, 30–39.
Porter, D.R., Burd, J.D., Shufran, K.A. and Webster, J.A. (2000) Efficacy of pyramiding greenbug
(Homoptera: Aphididae) resistance genes in wheat. Journal of Economic Entomology 93, 1315–1318.
Ratcliffe, R.H., Cambron, S.E., Flanders, K.L., Bosque-Perez, N.A., Clement, S.L. and Ohm, H.W. (2000)
Biotype composition of hessian fly (Diptera: Cecidomyiidae) populations from the southeastern,
midwestern, and northwestern United States and virulence to resistance genes in wheat. Journal of
Economic Entomology 93, 1319–1328.
Roe, R.M., Bailey, W.D., Gould, F., Sorenson, C.E., Kennedy, G.G., Bacheler, J.S., Rose, R.L., Hodgson, E.
and Sutula, C.L. (2000) Detection of resistant insects and IPM. In: Kennedy, G.G. and Sutton, T.B.
12IntpestManCh12.QXD 14/4/04 2:26 pm Page 280

280 G.W. Cuperus et al.

(eds) Emerging Technologies for Integrated Pest Management. American Phytopathological Society
Press, St Paul, Minnesota, pp. 67–84.
Russo, J.M. (2000) Weather forecasting for IPM. In: Kennedy, G.G. and Sutton, T.B. (eds) Emerging
Technologies for Integrated Pest Management. American Phytopathological Society Press, St Paul,
Minnesota, pp. 453–473.
Smith, R.F. (1970) Pesticides: their use and limitations in pest management. In: Rabb, R.L. and Guthrie,
F.E. (eds) Concepts of Pest Management. North Carolina State University, Raleigh, North Carolina,
pp. 103–118.
Stern, V.M., Smith, R.F., van den Bosch, R. and Hagen, K.S. (1959) The integrated control concept.
Hilgardia 29, 81–101.
Stinner, R.E. (2000) Information management: past, present, and future. In: Kennedy, G.G. and Sutton,
T.B. (eds) Emerging Technologies for Integrated Pest Management. American Phytopathological Society
Press, St Paul, Minnesota, pp. 474–481.
Tabashnik, B.E., Cushing, N.L., Finson, N. and Johnson, M.W. (1990) Field development of resistance to
Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae). Journal of Economic
Entomology 83, 1671–1676.
Thomas, M.B., Wratten, S.D. and Sotherton, N.W. (1992) Creation of ‘island’ habitats in farmland to
manipulate populations of beneficial arthropods: predator densities and species composition.
Journal of Applied Ecology 29, 524–531.
Treacy, M.F. (1998) Recombinant baculoviruses. In: Hall, F.R. and Menn, J.J. (eds) Methods in Biotechnology,
Vol. 5, Biopesticides: Use and Delivery. Humana Press, Totowa, New Jersey, pp. 321–367.
World Health Organization (1957) Seventh Report of the Expert Committee on Insecticides. Technical Report
Series No, 125, 31 pp.
Young, B.A., St Martin, S.K., Schmitthenner, A.F., Buzzell, R.I. and McBlain, B.A. (1994) Absence of resid-
ual effects of defeated resistance genes on Phytophthora rot of soybean. Crop Science 34, 409–414.
Zarrabi, A.A., Berberet, R.C. and Caddel, J.L. (1995) New biotype of Acyrthosiphon kondoi (Homoptera:
Aphididae) on alfalfa in Oklahoma. Journal of Economic Entomology 88, 1461–1465.
Zorner, P.S. (2000) Shifting agricultural and ecological context for IPM. In: Kennedy, G.G. and Sutton, T.B.
(eds) Emerging Technologies for Integrated Pest Management. American Phytopathological Society
Press, St Paul, Minnesota, pp. 32–41.
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13 Opportunities and Challenges for IPM in

Developing Countries

David Bergvinson
International Maize and Wheat Improvement Center (CIMMYT),
El Batán, Mexico, CP 56130, Mexico
E-mail: [email protected]

Introduction the first green revolution (Rosegrant et al.,

2001). To meet this challenge, integrated crop
Dramatic increases in rice and wheat pro- management (ICM) technologies must be
duction during the green revolution were applied to overcome the production con-
achieved through the introduction of short- straints faced by resource-poor farmers in
stature, high-yielding wheat and rice vari- LDCs. A central component of ICM is inte-
eties into Asia as part of a production grated pest management (IPM). To realize
package that included fertilizers and pesti- the full potential of IPM, sufficient govern-
cides to meet the urgent food demands dur- ment support for IPM research and a
ing the 1960s and 1970s. During the next two favourable policy environment must be
decades, the world will have to feed approxi- maintained (Pinstrup-Andersen, 2002).
mately 2.5 billion more people, with less Researchers, extension providers and farm-
arable land, fewer non-renewable and ers will need to collaborate to develop, adapt
renewable resources and a smaller percent- and adopt IPM technologies and also to
age of people working in the agricultural influence the formulation of policies that
sector. This challenge will be particularly favour the adoption of sustainable cropping
acute in the less developed countries (LDCs), technologies generally.
where food production will largely come Using a strengths, weaknesses, opportu-
from production increases rather than expan- nities and threats (SWOT) analysis, this
sion into marginal lands. This will take place chapter highlights factors that will bear
against the backdrop of climate change and directly on the acceptance and use of IPM
its poorly understood impact on agroeco- within the context of sustainable cropping
systems. systems in LDCs. Because each region of the
Today, the rate of production gains from world has unique constraints and advan-
conventional breeding for staple food crops tages related to the adoption and deploy-
has slowed from 2.9% (green revolution era) ment of IPM, sections of the chapter briefly
to 1.9% in LDCs, with gains frequently being look at such particulars for Africa, Latin
offset by environmental stresses and declin- America and Asia. A short exploration of
ing soil fertility. In order to address the what the future might hold for IPM in LCDs
looming production shortfall, crop produc- is explored through the use of four scenarios,
tion must increase as much as it did during which were developed by International
© CAB International 2004. Integrated Pest Management: Potential, Constraints and Challenges
(eds O. Koul, G.S. Dhaliwal and G.W. Cuperus) 281
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282 D. Bergvinson

Maize and Wheat Improvement Center tainable cropping systems. Due to the com-
(Spanish acronym CIMMYT) scientists to plexity of constraints that farmers face in
assist them in mapping out directions for commercial and small-scale agriculture –
crop research in coming years. The chapter including marketing, economic use of inputs
finishes with concluding observations and and complex biological interactions – IPM
thoughts about how to ensure that best- programmes have evolved to become part of
practice pest-management technologies and ICM (Meerman et al., 1996). The objective of
dissemination strategies meet the needs of ICM is to manage a production system in a
LDC farmers in the 21st century. way that optimizes the use of natural
resources, protects the environment and
maximizes output in a sustainable manner,
Strengths: Factors Encouraging IPM Use taking into consideration the socio-economic
in Developing Countries and technological framework and the inter-
action of management components. The
IPM enjoys the support of the international management components focus on different
development community because it is recog- production constraints, with control of pests
nized as a key component to sustainable assuming a prominent position, especially in
rural development in LDCs. It is uniquely developing countries, where insect and dis-
positioned for deployment in LDCs, thanks ease pressures tend to be severe due to the
to the increasing trend towards participatory subtropical and tropical climates found
research methods that enable farmers to fully there. With ICM gaining widespread accep-
engage in the development and deployment tance, the importance of and preference for
of IPM. Through socio-economic research in IPM have also grown.
LDCs, our knowledge of indigenous IPM Geier described the spectrum of IPM
practices has increased, as has our under- philosophies. At the tactical end of the spec-
standing of cropping constraints posed by trum is pest control, which ‘amounts to
diverse agroecological and socio-economic hardly more than bulldozing nature without
conditions. LDCs host a wealth of diversity thought to consequences and frequently cre-
in the form of cropping systems and species ates more problems than it solves’ (Geier,
diversity in tropical and subtropical ecolo- 1966: 471). At the strategic end of the spec-
gies, which will serve as a tremendous asset trum is integrated ‘pest management’, which
to the development and adoption of IPM ‘is intended to convey the idea of intelligent
technologies. Centres of origin for the major manipulation of nature for man’s lasting
crops found in LDCs already serve the world benefit, as in wildlife management’ (Geier,
by providing genetic diversity for crop- 1966: 474). Morse and Buhler (1997) summa-
improvement programmes, in both indus- rized the differences between control and
trial countries and LDCs, through their own management as a control beating the pest
breeding efforts and those of international into submission using direct interventions,
agricultural research centres (IARCs). This with little knowledge of the pest population
section discusses in greater detail how all and community interactions and usually
these factors serve as a positive foundation operating at a local level (i.e. field).
for the expanded use of IPM in the farm Management is considered a knowledge-
fields of developing countries. intensive control strategy that takes into
account the pest complex and social issues to
achieve a balanced ecosystem, using a
The role of IPM in the context of integrated diverse range of interventions to bring the
crop management pest population below an economic thresh-
old over a large area. The management phi-
Although IPM has a long history in both losophy has been supported in developing
industrial countries and LDCs (Morse and countries, in part, through loans by the
Buhler, 1997), it is now being viewed as a key World Bank and their Operational Directive
component within the wider context of sus- 4.03, which states: ‘The Bank’s policy is to
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IPM in Developing Countries 283

promote effective and environmentally from the research to the farmer, as new crop-
sound pest management practices in Bank- management interventions are developed.
supported agricultural development’ (World Farmer input has been largely confined to
Bank, 1992). This policy was reinforced by fine-tuning the intervention. Under the best
funding in the USA for IPM, totalling more of circumstances, information is fed back to
than US$180 million annually, to promote research scientists through extension,
IPM research and education as part of a cam- although, in actual practice, little, if any,
paign to implement IPM on 75% of the feedback occurs. This model has worked for
nation’s crop area by the year 2000 (Jacobsen, many agricultural interventions in industrial
1996). Clearly there is political will and sup- countries and has evolved to include the pri-
port for IPM in both the developing and vate sector as a major player in technology
developed world, but how this will play out delivery with improved feedback from both
in the future and what types of technologies farmers and consumers on the types of tech-
are likely to be promoted under different nologies that should be developed.
policy environments remain open questions. Consumer feedback has largely been chan-
nelled through the popular press to influence
government policy, which sets research man-
Participatory learning and technology dates. Although this model has worked well
development for simple interventions, it has achieved less
success with knowledge-intensive technolo-
Historically, technology development and gies, such as IPM. Morse and Buhler (1997)
transfer has followed the so-called ‘transfer point out that, under the TOT model, blame
of technology’ (TOT) approach, in which for the lack of IPM adoption falls on the
extension played a pivotal role in communi- shoulders of extension providers, with their
cating information between the farmer and shortcoming attributed to being understaffed
researcher (Fig. 13.1A). This model is a ‘top- or inadequately trained. This is often the
down’ approach to technology development case for LDCs, where extension services are
in which information flows predominantly often poorly staffed and equipped and

Research
Transfer of Participatory technology
technology innovation
Government creates
enabling conditions
Extension Government
(i.e. policies)

Private sector Research

Private sector

Farmers Farmers
Extension

Consumers
(A) (B)

Fig. 13.1. Technology dissemination models for IPM. (A) Transfer of technology model and (B) participatory
technology innovation model. (Adapted from Bruin and Meerman, 2001:22.)
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284 D. Bergvinson

operating funds for transferring technologies employed effective ITK to manage maize
to farmers are limited or non-existent. pests – mainly storage pests and termites –
During the last two decades, an increas- and when these were integrated with ICM
ing body of evidence has shown that partici- techniques it led to a 37% increase in produc-
patory methods for technology development tivity.
and transfer result in high adoption rates, Tools for participatory research and tech-
due to a sense of ownership of the process by nology development have evolved to
those for whom the technology is targeted. address interrelated steps that cover the fol-
Morse and Buhler (1997) have called for a lowing areas: defining the problem, under-
paradigm shift from the ‘technology first’ standing the problem, developing and
approach, in which farmers play a subordi- testing solutions making the interventions
nate role, to a ‘farmer first’ approach. This available to farmers to choose from and
view places IPM within the broad context of monitoring adoption to define impact and
the needs of the local people, with the farm- refine the intervention. The key first partici-
ers’ constraints being clearly identified and patory step – defining the problem – is
indigenous technical knowledge (ITK) about achieved using rapid rural appraisal (RRA)
crop management being recognized as a or participatory rural appraisal (PRA) in the
starting point for further technology devel- targeted communities to characterize the
opment. This was promoted earlier by social organization, agricultural system and
Matteson et al. (1984), who stated: ‘Useful pest constraints. An RRA is less participatory
pest control characteristics of traditional sys- than a PRA, in which the survey results are
tems must be preserved or augmented discussed and a joint plan of action is formu-
whenever possible and suggested changes lated within the community (Bruin and
should be tested to make sure they are con- Meerman, 2001). Both these techniques,
sonant with the farmers’ environment and however, enable researchers to document
socio-economic circumstances.’ ITK used by farmers to address constraints
Under this participatory model (Fig. in crop production. Participatory technology
13.1B), farmers are seen as equal partners in development (PTD) looks for practical solu-
the development of IPM technologies through tions to the problems, which include the use
their contribution of information about ITK, of ITK. Farmers and researchers work
socio-economic factors and ecological condi- together to characterize the agroecosystem
tions. Scientists and extension providers con- followed by farmer-led testing, monitoring
tribute basic IPM principles, assist in a better and evaluation of different interventions.
understanding of the agroecosystem, offer During the process, farmers develop the ana-
experimental know-how to assess new IPM lytical capacity to sustain technology devel-
options and facilitate interaction and effective opment to address future constraints.
feedback. The private sector is an important FFSs are another form of PTD, whereby
partner in delivering input technologies (i.e. farmers learn by doing and eventually
improved seed, appropriate pesticides) and become ‘IPM experts in their own field’
marketing. Practical examples of the effective (Gallagher, 1992). Training of trainers is the
application of the participatory model may be first step in which IPM training, if required,
found in various IPM and ICM development is provided for extension providers, along
projects in Zanzibar on rice, cassava, banana with facilitation skills and the principles of
and vegetables (Bruin and Meerman, 2001). adult education. Trainers then engage farm-
Another example is found in Zambia where ers in an intensive 3-month course during
participatory methods were used to assess the cropping season to learn basic IPM prin-
ITK and production constraints for maize ciples and develop a better understanding of
farmers (Nkunika, 2002). Using a farmer field the agroecosystem, including pests, biologi-
school (FFS) approach, demonstration plots cal controls, environmental hazards and
integrated improved fertilizer and cultural good cropping practices. The four goals of
practices (early weeding) with ITK for pest FFSs for IPM are to grow a healthy crop, to
control. Researchers found that farmers conserve natural enemies, to conduct regular
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IPM in Developing Countries 285

field observations and to make farmers IPM be apparent to farmers based on observation
experts. Farmers are encouraged to share (e.g. metamorphosis of insects or spores of
their knowledge with their neighbours to diseases), while farmers need to convey ITK
disseminate lessons learned from the FFSs. to scientists, based on years of farmer experi-
This participatory approach has been mentation. Looking strictly at IPM, compre-
adopted by various development organiza- hension of the ‘folk’ language and
tions to develop IPM programmes for differ- classification of the farmers’ biotic world
ent crops around the world. based on cultural experiences is essential for
Another participatory technique, recently effective communication about simple con-
employed in southern Africa, is the ‘mother– cepts (tactical IPM and pesticide handling)
baby’ testing system, used specifically to and knowledge-intensive technologies
evaluate experimental and commercial (strategic IPM and managing the agroeco-
maize varieties (Bänziger and de Meyer, system).
2002). In this testing system, a complete trial, Innovative thinking about how best to
called the ‘mother’, is grown under recom- communicate messages related to reducing
mended conditions at a school or agricul- pesticide use and exposure in developing
tural training centre to serve as the focal countries has advanced considerably since
point for community discussions about the the early 1990s. Calendar spraying serves as
best varieties. Individual farmers in the com- a useful illustration. In some parts of the
munity are given four of these varieties, each developing world, those who do not spray
called a ‘baby’, to grow under their own their crops at the first sign of insect damage
management practices. At harvest, farmers are perceived as lazy or poor agriculturalists.
evaluate the crops for different traits and the This practice, however, often conflicts with
relative importance of these traits is deter- those advocated by IPM tactics. In this situa-
mined through farmer interviews. This tion, the question arises, how does one
approach is very relevant to what change the perceptions and consequently the
Brundtland (1987) calls ‘complex, diverse practices of whole farming communities?
and risk-prone’ (CDR) agriculture, which is One approach, called ‘conflict informa-
practised by the majority of resource-poor tion’, is to shock the farmers and create a
farmers in developing countries. Varieties state of dissonance that challenges them to
undergoing testing have been improved for evaluate and change their perceptions in
resistance to important biotic stresses and respect of a simple rule of thumb, or heuris-
tolerance to drought and low soil fertility – tic, that is scientifically supported but in con-
production constraints often faced by flict with their prevailing views (Heong and
resource-poor farmers. This scheme may Escalada, 1997). This approach was tested on
well lend itself to future testing of localized rice farmers in the Philippines, with the
IPM interventions. heuristic being that leaf-folder control is not
necessary during the first 30 days after trans-
planting. Research had shown, contrary to
Communication methods farmers’ beliefs, that rice plants tolerate early
defoliation by the rice leaf-folder,
Understanding how farmers perceive and Cnaphalocrocis medinalis (Guenée) (Heong et
classify pests, as well as their terminology al., 1994). Farmers were asked to measure
for ITK is a basic starting-point for effective out a 500 m2 plot that would not be sprayed
communication between scientists and farm- with insecticide for the first 30 days after
ers (Bentley and Rodríguez, 2001). The transplanting to later compare with their
importance of this communication linkage plots that were sprayed. It was quickly
has received renewed attention with the observed that yields from the unsprayed plot
emergence of farmer participatory learning were equal to those of the sprayed plots.
and technology development. Communi- Farmer opinion on the need to spray for leaf-
cation is a two-way street, in which scientists feeding insects early in the season changed
need to communicate concepts that may not from 62% supporting it down to 10%.
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286 D. Bergvinson

Furthermore, related to benefits of adopting not subsidized, will not be maintained; and
the new practice, 94% recognized that there (iii) the media used should be an accepted
would be financial savings, 35% cited form of communication for the whole farm
reduced labour requirements, 26% perceived family, because social obligations (family)
reduced exposure to health hazards, 11% often enforced the pesticide safety message.
noted reduced insecticide residues in rice
and 2% said it would help conserve biologi-
cal control agents. This approach holds con- Biodiversity
siderable promise in reaching a larger
audience of farmers where the overuse of Developing countries predominantly have
insecticides is prevalent. subtropical or tropical agroecosystems,
Another innovative approach enjoying which generally have high levels of biodiver-
wide use is ‘social marketing’, which sity. Altieri (1995) described biodiversity as
employs marketing principles and tech- the key element in sustainable agriculture,
niques to advance a social cause, idea or not only in the maintenance of diversified
behaviour (Kotler and Zaltman, 1971). cropping systems, but also in the mainte-
Marketing a commercial product is achieved nance of diverse varieties of a given crop.
by setting a measurable objective, marketing Within the spectrum of LDC farming sys-
research, developing a product that meets a tems, small-scale farming systems generally
genuine need, creating awareness and employ mixed cropping systems and subse-
demand through advertising, and establish- quently promote greater diversity than large-
ing prices that generate a return and meet scale, commercial agriculture. Several
the original marketing objective. Atkin and examples of the beneficial effects of
Leisinger (2000) report on the impact of increased biodiversity are reported in this
social marketing to promote the adoption of book (see Verkerk, Chapter 4, this volume)
safe and effective practices for insecticide use and in recent reviews (Landis et al., 2000).
for maize in Mexico and for cotton in India Since the early 1990s, the concept of
and Zimbabwe. Surveys were conducted to agroecology has been promoted by many
assess knowledge, attitudes and practices groups working in LDCs as a means of
(KAP) as a baseline for identifying pesticide- achieving sustainable crop production
related illnesses and safety practices. through the promotion of environmentally
Following the KAP survey, the prominent and socially sensitive technologies, espe-
handling and application health hazards cially for small-scale or subsistence farming
were addressed through communication systems (Altieri, 1993). Altieri (1995) depicts
campaigns using different media. The cost– an agroecological approach as the conver-
benefit analysis of this study identified, mea- gence of three circles: social, economic and
sured and validated the benefits (improved environmental goals. Under the environmen-
health, reduced use of sprays based on eco- tal goal, biodiversity and the stability that
nomic injury level (EIL)) and costs (protec- results are important objectives in low-input
tive gear, equipment maintenance, lost cropping systems. Altieri’s approach empha-
opportunity due to time spent scouting and sizes the social and environmental compo-
washing after pesticide applications). Critical nents in cropping systems to promote equity
to this approach are choosing the most effec- and the use of local resources while sustain-
tive media to promote the message and ing yields and economic viability.
couching the message in socially and cultur- In relation to IPM, management of the
ally acceptable terms. In Mexico, comic environment overlaps with habitat manage-
books and posters proved effective, while ment, which plays an important role in the
local radio and theatrical plays for parents conservation of biological control agents,
and schoolchildren worked well in India and namely, parasitoids and predators. Main-
Zimbabwe, respectively. The lessons learnt tenance of suitable conditions within the agri-
from these case studies were: (i) the message cultural landscape is necessary to ensure food
must be simple; (ii) costly interventions, if (pollen and nectar sources), shelter, hosts and
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IPM in Developing Countries 287

alternative prey for the biological control grown with no intervention and 1 : 2.3 for the
agents, in order to increase their survival, push–pull strategy (using napier grass and
fecundity, longevity and ultimate effectiveness desmodium).
(Landis et al., 2000). Knowledgeable use of Secondary plant compounds are also an
habitat management holds considerable important part of the diversity equation in
promise both for buffering the environment LDC ecologies. There has been a growing
for biological control agents and, as we shall interest since the inception of IPM to exploit
see later, to serve as a refugia in managing natural plant products for pest control. The
insect resistance to genetically engineered most popular examples are pyrethrum and
(GE) plants. neem oil. Pyrethrum, derived from chrysan-
Several good examples of biological con- themum plants, originated in Africa and has
trol through habitat management have been served as the model molecule for the synthe-
documented in LDCs. One particularly inno- sis of pyrethroid insecticides which have
vative strategy, the ‘push–pull strategy’, is proved to be effective and safe. The neem
currently being exploited in eastern Africa to tree (Azadirachta indica) from India produces
control stem borers in small-scale maize a mixture of insecticidal tetranortri-
farming systems (Khan et al., 1997). The two terpenoids, with the most active being
predominant stem borers, Chilo partellus azadirachtin (Schmutterer, 1995). Over the
(Swinhoe) and Busseola fusca (Fuller), are centuries, Indians have processed neem
‘pulled’ from the maize plots by planting seeds, bark and leaves for their insecticidal
highly susceptible trap crops around the and medicinal properties (Koul, 1996).
field perimeter – in this case, napier grass Several other plants belonging to Meliaceae,
(Pennisetum purpureum Schumach) and apart from A. indica, have been characterized
Sudan grass (Sorghum vulgare sudanense for their biological activity. Given the wealth
Stapf.). The ‘push’ component is provided by of knowledge derived from a single genus,
intercropping maize with grasses that repel one wonders how much phytochemical
the stem borers, such as molasses grass diversity remains to be characterized and
(Melinis minutiflora Beauv.) or species of utilized as control treatments in IPM. Clearly,
Desmodium (D. uncinatum Jacq. or D. intortum LDCs are home to most of the world’s phyto-
Urb). Although the repellent crop does not chemical diversity, which holds great
provide complete control, M. minutiflora pro- promise for the future development of
duces a volatile, nonatriene, which attracts botanical pesticides. It is likely that botanical
the parasitoid Cotesia sesamiae (Cameron), pesticides will become increasingly impor-
thereby increasing the rate of parasitism tant in LDCs for a number of reasons: (i) they
fourfold (Khan et al., 1997). Recent on-farm provide effective control of insects that have
studies confirmed the efficacy of the become resistant to synthetic insecticides; (ii)
push–pull strategy in reducing stem borer they generally pose a low risk to non-target
populations to 25% of the levels found in organisms; (iii) they are naturally occurring
control plots (Khan et al., 2001). The strategy and so are sometimes accepted by organic
yields other benefits as well. In the predomi- certification programmes; and (iv) they are
nantly mixed crop–livestock farming sys- often more accessible than synthetic insecti-
tems of eastern Africa, the napier grass, a cides in the LDCs where they are grown
popular livestock forage, contributes directly (Weinzierl, 1999).
to farm income. Meanwhile, the desmodium, Genetic diversity within crop species is
a leguminous plant, when sown in alternat- another important contribution developing
ing rows with maize, increased soil fertility, countries have made to IPM. As is current
which resulted in the suppression of Striga practice, plant breeding in the future will
spp., a parasitic weed that is prevalent in utilize genetic diversity to develop crops
low-fertility soils in Africa. An economic with unique and desirable traits, including
analysis of the push–pull strategy generated conventional host-plant resistance (HPR)
from this study found the cost : benefit ratio (see Smith, Chapter 7, this volume). When
to be 1 : 1.4 for improved maize varieties one considers the centres of origin, and
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288 D. Bergvinson

hence diversity, for the major crops of the Research networks: Consultative Group on
world, developing countries have already International Agricultural Research Centres
made a tremendous contribution to plant
improvement, both in situ and ex situ (in the The green revolution achieved its success in
form of germplasm bank collections held in large part through the networks consisting of
trust around the world). Centres of diversity IARCs and national agricultural research and
for selected crops include Mexico and extension systems (NARES). The first IARC,
Central America for maize (Zea mays), beans the International Rice Research Institute
(Phaseolus spp.), cotton (Gossypium hirsutum) (IRRI), was established in 1960 and its sister
and tomato (Lycopersicon esculentum); South centre, CIMMYT, was formally established in
America for sweet potato (Ipomoea batatas), 1966. These two centres took the lead in
rubber (Hevea brasiliensis), cotton (Gossypium developing and releasing high-yielding vari-
barbadense), potato (Solanum tuberosum) and eties for developing countries, especially in
cassava (Manihot esculenta); East Africa for south Asia where real and projected food
finger millet (Eleusine coracan), sorghum shortages placed a sense of urgency on
(Sorghum bicolor), cowpea (Vigna unguiculata) increasing rice and wheat production. In
and coffee (Coffea spp.); West Africa for bul- 1971, the Consultative Group on
rush millet (Pennisetum americanum) and rice International Agricultural Research (CGIAR)
(Oryza glaberrima); North Africa for rye was formed to serve as an umbrella organiza-
(Secale cereale); south-west Asia for barley tion to coordinate funding to the then five-
(Hordeum vulgare), South-east Asia for rice member group of IARCs. Today, the CGIAR
(Oryza sativa) and citrus (Citrus spp.); New includes 16 IARCs, each having a mandate
Guinea for sugarcane (Saccharum spp.); the region, crop or cropping system (CGIAR,
Fertile Crescent in the Iran/Iraq/Syria/ 2003). Many of these IARCs hold genetic
Turkey region for wheat (Triticum spp.); and resources of the main cereal and pulse crops
China for soybeans (Glycine max) in germplasm banks. These collections of
(Simmonds, 1976). This long list of basic food global accessions are held ‘in trust’ under a
crops highlights the important role develop- Food and Agriculture Organization (FAO)
ing countries have played and will continue agreement signed in 1994. Under this agree-
to play in the future stewardship of genetic ment, the IARCs are responsible for the long-
resources, which could contribute to IPM term storage and regeneration of holdings for
strategies both locally and around the world. the benefit of the international community.
Arthropod diversity is also a tremendous Most sources of conventional HPR originated
resource to be utilized more fully in the from materials now held in germplasm
future. Historically, some of the limitations banks, which will continue to serve as a valu-
for using introduced or exotic biological able resource for HPR development.
control agents in classical biological con- Morse and Buhler (1997) assert that the
trol have been misidentification of species, green revolution laid the foundation for the
collection of biotypes not adapted to the later adoption of IPM. It enabled higher pro-
target agroecology and quarantine duction and lower grain prices, which bene-
capacity to facilitate the introduction fited both farmers and consumers.
(Neuenschwander, 1993). With the estab- Productivity gains also benefited the environ-
lishment of research organizations such as ment, as they largely arrested the further
EcoPort, BioNET and the International expansion of agriculture into marginal lands
Organization for Biological Control, infor- in many parts of Asia. However, the green
mation management and exchange will be revolution has also been criticized for harm-
enhanced to enable the identification and ing the environment by reducing genetic crop
localization of potential control agents and diversity and beneficial insect populations in
to ensure the highest probabilities of suc- agroecosystems and adversely affecting
cess by using site-similarity tools to target farmers’ health through the overuse and mis-
collection activities for classical biological handling of pesticides. Across Asia, insecti-
control programmes. cide consumption increased from US$347
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IPM in Developing Countries 289

million in 1980 to a peak of US$1.08 billion in broad range of development objectives. As a

1990 (Pingali et al., 1997). The resurgence of result, funding for ICM development and
secondary pests, such as the brown planthop- deployment is generally low, which results
per, Nilaparvata lugens (Stål) in rice (Heinrichs in low to moderate levels of financial sup-
et al., 1982), was a driving force for the devel- port for agricultural research and extension.
opment and promotion of IPM technology. Government funding for improved infra-
The goal was simple: maintain established structure, telecommunications in particular,
yield gains with reduced pesticide use. needs to continue, as it will enable IPM prac-
This unique network of IARCs has served titioners to keep abreast of IPM advances
as a hub for coordinating research within and within their region and around the world.
between developing countries around the IPM is also challenged by the economic
world. Although in its early days the CGIAR trend of farmers pursuing off-farm employ-
focused on pressing food demands, in more ment when possible, which often results in
recent years the CGIAR centres have aimed to labour shortages and less active engagement
respond more actively to environmental, in agricultural production. These factors are
social and small-farmer concerns as part of the reviewed in more detail below.
quest to further sustainable rural develop-
ment. In that spirit, the CGIAR established a
system-wide programme on IPM, which LDC regulatory agencies
brought together ten IARCs to address issues
related to the development, promotion and LDCs have established regulatory bodies
adoption of IPM technologies in different similar in function to the Environmental
cropping systems. During the late 1990s, Protection Agency, the US Department of
membership was expanded and current stake- Agriculture (USDA) Animal and Plant
holders now include various national agricul- Health Inspection Service (APHIS) and the
tural research systems (NARS), diverse Food and Drug Administration in the USA.
promoters of IPM, such as FAO and the World The mandate for these agencies is to ensure
Bank, advocacy groups, such as the Pesticide that agricultural products, including agro-
Action Network and other non-governmental chemicals and GE crops, are safe for con-
organizations (NGOs) and the private sector sumers and the environment and improve
(CropLife International) (James et al., 2003). the quality and quantity of food produced.
Together, these parties have developed and The high cost associated with the commer-
promoted IPM technologies for a range of cialization of agrochemical products has
global pests including the whitefly, Trialeurodes encouraged agrochemical companies to
vaporariorum (Westwood); stem borers, C. place a high priority on product stewardship
partellus and B. fusca; Striga species, S. hermon- and the use of modern science to promote
thica and S. asiatica; leaf-miners, Liriomyza tri- sustainable agriculture (CropLife, 2003).
folii (Burgess), Liriomyza sativae Blanchard and However, such vigilance is often lacking in
Liriomyza huidobrensis (Blanchard); and white LDCs because the small agrochemical com-
grubs (e.g. Phyllophagus spp.). The system- panies, which are often major suppliers,
wide programme partners are also addressing often have little interest in product steward-
broader themes that bear on IPM, including ship. Commonly they sell products based on
farmer participatory research, invasive older chemistry that have a low profit mar-
species, impact assessment and the use of GE gin and are generally more damaging to
crops in LDCs. human health and the environment. The
ability of the regulatory agencies to enforce
their mandates and ensure safe and sustain-
Weaknesses: Factors Working against able crop production range from that
IPM Use in LDCS demonstrated in recently industrialized
countries, as seen by the exemplary Taiwan
In contrast to industrial countries, LDCs Agricultural Chemicals and Toxic Substances
have fewer financial resources to address a Research Institute (TACTRI) in Taiwan
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290 D. Bergvinson

(TACTRI, 2002), to countries that have yet to these and other issues related to capacity
establish regulatory bodies for various rea- building in agriculture within LDCs (ISNAR,
sons. As the profitability of agriculture 2003).
increases and export markets develop, it is
anticipated that these maturing agencies will
better regulate pesticide use and enforce Telecommunications
policies that favour IPM technologies. Where
profitability is expected to decline, one fears Although the Internet and other forms of
the opposite will happen. telecommunication are taken for granted in
the industrial countries, their limited avail-
ability (including affordability) and poor
Government investment in agricultural reliability in some LDCs are a constraint to
research their extensive use. Poor telecommunication
infrastructure impedes the use of Internet-
In most LDCs, government funding for agri- oriented systems that link interdisciplinary
cultural research and extension is low, which research and extension teams and users and
is not surprising given the demands placed providers of new technology within a coun-
on their limited treasuries by health, educa- try and between countries. Frequently we
tion and other competing development find adequate telecommunication capabili-
fields. Public-sector agricultural research is ties in a LDC’s capital city, but poor or no
not keeping pace with the private sector in communication system serving the country-
terms of facilities, operational funds and side, where the researchers and extensionists
compensation. This results in many of the conduct their work and farmers reside.
most capable scientists being lured away to Between the LDCs and the industrial coun-
the private sector or to positions abroad and, tries, many refer to a widening of the ‘digital
for those who remain, the prospect of not divide’ (Kates et al., 2001), which leaves
being given the resources to perform their developing countries in the technological
jobs properly. As LDCs build up their agri- wake of their more developed colleagues;
cultural and industrial sectors and, with this would also apply to IPM. The Internet
them, their export markets, it is hoped that will become increasingly important for IPM
more funding will be directed towards agri- networks in LDCs. It will enable scientists
cultural research, but, unfortunately, this and policy makers to access IPM expertise
cannot be assumed at this time. through various databases, including one
International development organizations, recently offered through the Global IPM
which recognize the importance of agricul- Facility (http://www.wisard.org/wisard/
ture in development, complement national clients/ippm), which lists more than 400
funding through projects, but these funding IPM experts around the developing world.
sources carry a finite time link, typically 3–5
years. For IPM, a project may not have suffi-
cient time to characterize, identify, test, scale Off-farm employment
up and monitor management interventions.
The problem is exacerbated by a high In industrial countries, agriculture has
turnover rate of research and technical staff increasingly become a capital-intensive
in some NARES, due to the reasons cited enterprise which achieves high production
above. Another important problem receiving but often requires off-farm employment to
more attention of late is gender imbalance as supplement farm revenue. In many industri-
it relates to extension and researchers work- alized countries less than 25% of the popula-
ing in communities where women are tion works in agriculture, while in many
engaged in crop management (Bruin and developing countries this figure is generally
Meerman, 2001). Organizations such as the above 60% (Bongaarts, 2002). Off-farm
International Service for National employment is also a reality for many farm
Agricultural Science (ISNAR) are looking at families in LDCs, but the trend is for young
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IPM in Developing Countries 291

adults, frequently male, to leave the farm to tems included banana (rust thrips,
seek urban employment, leaving behind an Chaetanaphothrips orchidii (Moulten) and
agricultural workforce that is either older or banana weevil, Cosmopolites sordidus
dominated by young women (Pingali, 2001). (Germar), Costa Rica); cotton (secondary
Income forecasting by farmers in LDCs is pests such as Argyrotaenia sphaleropa
becoming increasingly difficult as imported (Fernald) and Platynota sp., Peru); mangoes
grain can upset local grain prices due to the (mealy-bug, Drosicha stebbingi (Green),
absence of effective marketing boards that Pakistan); cassava (mealy-bug, Phenacoccus
enable farmers to plan farm activities based manihoti Matile-Ferrero, Congo); coconut
on expected future income. Ethiopia and (rhinoceros beetle, Oryctes rhinoceros
Malawi are two examples of price fluctua- (Linnaeus), Malaysia); cocoa (bark-boring
tions cited by Pinstrup-Andersen (2002): caterpillars, Malaysia); crucifers (diamond-
2000–2001 maize prices in Ethiopia fell to back moth, Plutella xylostella (Linnaeus),
20% of the 1999–2000 price and, in the course Asia); and rice (brown planthopper, N. lugens,
of the following year, maize prices in Malawi Asia), among others. The key features shared
increased 400%. The lack of infrastructure by some of the programmes included recog-
that results in such price fluctuations leave nition that chemical control eliminates nat-
resource-poor farmers in a dilemma in terms ural enemies, which results in pest
of both investing in inputs to improve crop outbreaks; failure of chemical control leads
performance and securing income from out- to IPM adoption; IPM strategies emphasized
side sources to cover basic expenses, such as the reduction and/or use of selective pesti-
education fees. cides, which in turn, restored natural ene-
mies; pest problems declined after reducing
pesticide use; research focused on field prob-
Opportunities lems; there was close collaboration between
researchers, extension providers and farm-
Scientific advances in IPM and supporting ers; IPM had a strong biological control com-
disciplines have been tremendous in the past ponent; and the presence of strong
two decades in industrial countries and, to a government and management support.
lesser extent, in LDCs. This section high-
lights recent successes and opportunities for
further development of IPM component Biological control
research in LDCs.
Biological control programmes in LDCs offer
some of the most dramatic examples of
Past successes and the lessons learned impact and high cost:benefit ratios realized
by IPM. One of the most celebrated cases of
Since its inception in the early 1960s, many classical biological control involved the cas-
examples of successful IPM programmes sava mealy bug P. manihoti and the para-
have been reported, mainly in industrial sitoid Epidinocarsis lopezi (De Santis). The
countries, where the overuse of pesticides mealy-bug was introduced from South
had reached a critical level. Several relatively America to Central Africa in the early 1970s
recent reviews have pointed to similar suc- and, in the absence of its natural enemies, it
cesses in developing countries (Mengech et rapidly established itself as a devastating
al., 1995; Guan Soon, 1996; Bruin and pest of cassava, a staple food in sub-Saharan
Meerman, 2001). Crop-specific studies – for Africa (Herren et al., 1987). The use of insecti-
instance, on rice (Matteson, 2000) and cas- cides was judged to be an impractical control
sava (Bellotti et al., 1999) – lend further strategy for the mealy bug given the low
weight to the efficacy of IPM in LDCs. Guan crop value, economic constraints and
Soon (1996) examined ten IPM programmes farmers’ lack of experience in handling
in developing countries to identify common insecticides. Biological control was seen as a
features that they shared. The cropping sys- promising alternative and options were
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292 D. Bergvinson

sought through the formation, in 1979, of a searchable databases to accelerate the imple-
network headed by the International mentation of classical biological control pro-
Institute for Tropical Agriculture (IITA), grammes in the future, especially using
which included the Center for Tropical south-to-south exchanges.
Agriculture (CIAT), the Brazilian Diversified cropping systems and
Agricultural Research Corporation reduced rates of targeted pesticides will
(EMBRAPA), the International Institute of encourage the conservation of biological con-
Biological Control (IIBC) in London, the trol agents. Cropping practices can be devel-
Inter-African Phytosanitary Council (IAPSC) oped and implemented that allow natural
and the Nigerian quarantine service enemies to realize their full potential to sup-
(Neuenschwander, 1993). Identification of press pests. This can be done through identi-
suitable foreign biological controls required fication and remediation of negative
that national biological control programmes influences that suppress natural enemies or
be established, with national scientists by enhancing habitats for resident natural
trained in the handling and testing of candi- enemies (i.e. providing pollen and nectar
date control agents within their country. sources) (Landis et al., 2000). This approach
Releases were made in collaboration with has been encouraged in many IPM pro-
national institutions and often accompanied grammes, especially the FFSs, in which farm-
by media coverage, which popularized the ers are introduced to indigenous biological
concept of biological control with both control agents and are encouraged to adopt
farmers and consumers. practices that do not have an adverse impact
In 1981, the parasitoid Apoanagyrus on non-target insects.
(Epidinocarsis) lopezi De Santis (Hymenoptera:
Encyrtidae) was imported from Paraguay
into Nigeria for use in the biological release Host-plant resistance
programme for cassava mealy-bug control.
Three years after the parasitoid’s initial series Farmers, especially small-scale farmers, have
of releases, it had spread over 200,000 km2 in selected directly or indirectly for traits of
south-western Nigeria. By 1985, more than 50 interest, including resistance to pests, over
releases in 12 African countries had been the millennia. One reason farmers cite for
made, which by 1990 resulted in E. lopezi not adopting improved, high-yielding vari-
being established in 24 countries covering eties is because of their perceived suscepti-
more than 12 million km2 (Neuenschwander bility to local pests and diseases. HPR is an
et al., 1990). economically viable and environmentally
With ever-increasing transborder move- appealing technology for LDCs. Resistant
ment of people and international trade, the varieties provide a number of advantages:
incidence and hazards posed by invading they lessen the need for costly imported pes-
alien species will also increase – and, with ticides, reduce hazards posed by exposure to
them, the demand for solutions using classi- pesticides and misuse of recycled pesticide
cal biological control and other IPM compo- containers and minimize pesticide residues
nents. The Convention on Biological on produce, with subsequent benefits to con-
Diversity recognized the ‘taxonomic impedi- sumer health and safety. The economic
ment’ for the management of biodiversity, in impact of HPR on farmers can be significant,
large part due to knowledge gaps and short- not just in reduced purchases of pesticides
age of trained taxonomists. Networks such but also in increased insect biodiversity
as BioNET-International focus on increasing through reduced applications of synthetic
taxonomic infrastructure in LDCs by provid- insecticides. The estimated value of insect
ing training and technologies that enable a resistance in wheat at a global level is over
country to be self-reliant (BioNET- US$250 million/year (Smith, 1999). The rice
International, 2003). A global taxonomic plat- variety IR36, with resistance to brown plant-
form to standardize the inventory of living hopper, green leafhopper, striped stem-borer
organisms would enable the development of and gall midges, saves rice farmers an
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IPM in Developing Countries 293

estimated US$1 billion (Khush and Brar, incorporate conventional resistance into
1991). It should be noted, however, that crop-breeding programmes. HPR has
impact assessment for conventional host- tremendous potential in LDCs, as the tech-
plant resistance is scarce and should be pro- nology is packaged in the seed and does not
moted in the future. require additional knowledge to utilize it,
Huge strides have been made in the but it may require education about its man-
development of methodologies to select and agement to maintain a high level of resis-
incorporate HPR (Panda and Khush, 1995). tance in recycled or ‘saved’ seed, a practice
Inheritance of HPR falls into two broad cate- that is commonly used by subsistence farm-
gories: major gene resistance and polygenic ers.
(quantitative) resistance. Major gene resis-
tance involves a single gene, usually domi-
nant, that confers resistance to a pest or Genetically engineered crops
disease that is usually specialized on that
crop. Polygenic resistance involves several Much debate has taken place regarding the
genes, each contributing a small level of use, benefits and risks of GE crops in indus-
resistance, which is often influenced by the trial countries, in particular Europe. In fact,
environment. Given these characteristics, GE crops have been the predominant topic in
more plant varieties with major gene resis- integrated crop protection literature in the
tance have been deployed; however, the past 5 years. In the USA, the Council for
single-gene approach has also resulted in the Agricultural Science and Technology (CAST)
development of resistant pest biotypes, such undertook a review of the impacts of agricul-
as brown planthopper resistance to Bph tural biotechnology to assess its impact in
genes in rice and Hessian fly biotypes in cotton, maize and soybean on environmental
wheat. One can observe from the summary and sustainability issues, such as pesticide
by Khush and Brar (1991) that major gene use, soil management and conservation
resistance is more prevalent against tillage, crop weediness, gene flow, pest resis-
Homoptera, Hemiptera and Diptera, while tance, pest population shifts (secondary
polygenic resistance is more prevalent for pests) and non-target organisms (Carpenter
Lepidoptera, Coleoptera and mites. Through et al., 2002). The report recommended the use
the use of modern molecular tools (see of GE technologies as a means of sustainable
Smith, Chapter 7, this volume) and an intensification of crop production as the
understanding of the biochemical or bio- results showed an increase in insect biodi-
physical basis of resistance, the process of versity (Bacillus thuringiensis (Bt)-based tech-
incorporating resistance into accepted, high- nology) and enhanced adoption of
yielding varieties has accelerated and been soil-conservation technologies (herbicide-
refined as only the genomic regions of inter- resistance genes to facilitate no-till in soy-
est are incorporated into the improved vari- bean) associated with GE crops. The best
eties without the extra genetic ‘baggage’ expression of utility of GE crops is by farmer
from the resistant source. Molecular markers adoption, which shows that there are eco-
have been used in conventional insect resis- nomically tangible benefits with GE crops
tance in several crops (Yencho et al., 2000; that are reflected in the dramatic increase in
Willcox et al., 2002) and are being adopted by area planted to genetically modified (GM)
NARS in LDCs. Future HPR efforts will con- crops in both industrial and developing
tinue to play a major role in developing countries (Fig. 13.2).
resistance to pests, with gene sequencing of Although investment in agricultural
dominant genes potentially serving as con- biotechnology is concentrated in industrial
structs for future transformation efforts. countries, three developing countries have
As was noted earlier, most crops have committed significant levels of public fund-
their centres of diversity in developing coun- ing to biotechnology, namely China (US$112
tries. Much remains to be done to character- million), India (US$15 million) and Brazil
ize and utilize this diversity in order to (US$2 million) (Huang et al., 2002). China has
13IntpestManCh13.QXD 14/4/04 2:26 pm Page 294

294 D. Bergvinson

60 James, C., 2003a). Between 1999 and 2001, the

Industrial reduction in insecticide applied to cotton was
Genetically engineered crops

50 Developing 123,000 t of formulated product, which

(area in millions of ha)

Total resulted in a 75% reduction in insecticide poi-

40 sonings of cotton farmers using knapsack
sprayers (James, 2002). Economic benefit has
30 been the main driving force for adoption,
with an average reduction of 13 sprays (49
20 kg)/ha, amounting to a cost savings of
US$762/ha, excluding labour costs (Huang et
10 al., 2002). The net effect has been a 28%
reduction in production costs and reduced
0 exposure and poisonings by farmers to pro-
1996 1997 1998 1999 2000 2001 2002 duce a product of the same value.
Year Scientists like Florence Wambugu (1999)
Fig. 13.2. Area planted to genetically engineered have highlighted the economic and health
crops in developing and industrial countries benefits derived from Bt crops to promote
between 1996 and 2002 (from James, C., 2003b). their use in Africa. Wambugu states, ‘Africa
missed the green revolution, which helped
Asia and Latin America achieve self-
announced plans to raise plant-biotechnol- sufficiency in food production. Africa cannot
ogy budgets by 400% before 2005, which afford to be excluded or to miss another
would then account for approximately one- major global “technology revolution”. It must
third of the world’s public investment in join the biotechnology endeavour.’ A Kenyan
plant biotechnology. This level of investment project entitled Insect Resistant Maize for
by LDCs is driven by expected returns, Africa (IRMA) is looking at the issues sur-
which for IPM include the reduction in rounding Bt maize to control stem borers in
insecticide use by both large-scale and small- both commercial and subsistence maize crop-
scale farmers. ping systems (Mugo et al., 2001). Yield-loss
Recent studies show that small-scale farm- studies from the project established that stem
ers in developing countries stand to benefit borer losses in Kenya amount to US$72 mil-
more from GE technology than commercial lion per annum (De Groote, 2002). PRAs were
farmers in industrial countries, due to the used to establish farmer constraints, which,
limited access to agrochemicals and greater apart from stem borers, include other biotic
losses associated with insect pests in tropical (storage pests, maize streak virus) and abiotic
and subtropical agroecologies (Qaim and (drought and low soil fertility) stresses.
Zilberman, 2003). The best example of GE Expected benefits from Bt maize in Kenya
crop-protection technology in LDCs is Bt cot- will include increased profitability to farmers
ton containing the cry1Ac gene from Bacillus and increased insect biodiversity within the
thuringiensis, which is being grown in on- mixed maize cropping system of small-scale
farm trials in India (Qaim and Zilberman, farmers.
2003) and commercially in China (Huang et Although Bt cotton and maize have
al., 2002). In China, Bt cotton was approved reduced insecticide use, a central tenet in
for commercial release in 1997, due to a sharp IPM, the use of Bt crops begs the question of
reduction in cotton production caused by its impact on other IPM components, such as
losses and control costs associated with the biological control, and the agroecosystem in
cotton bollworm, Helicoverpa armigera general. The large-scale deployment of Bt
(Hübner). The response by China’s poor crops has generated public concern regard-
farmers to Bt cotton has been astonishing, ing its ecological, food-safety and social con-
increasing from 2000 ha in 1997 to 2 million sequences. These concerns were heightened
ha in 2002, accounting for approximately half by a laboratory study showing mortality of
the cotton area in China (Huang et al., 2002; the monarch butterfly, Danaus plexippus
13IntpestManCh13.QXD 14/4/04 2:26 pm Page 295

IPM in Developing Countries 295

(Linnaeus) after consuming pollen from Bt growers’ objective of controlling insect pests
maize expressing CryIAb toxin (Losey et al., and would be virtually impossible to enforce
1999). Concern was also raised regarding given the large number of small-scale farm-
impacts on biological controls when Hilbeck ers relative to extension agents available for
et al. (1998) demonstrated adverse effects of monitoring compliance. China is one exam-
Bt maize, mediated through the herbivore ple where resistance management is not
prey, on lacewing larvae, Chrysoperla carnea mandatory for commercial Bt cotton (Zhao et
(Stephens). While laboratory studies are use- al., 2000). Developing viable IRM strategies
ful in pointing to potential risks, it is difficult will require participatory research involving
to translate these results to a field setting. In socio-economists, entomologists and policy
the case of the monarch butterfly, Bt maize makers to develop strategies that are socially,
had a negligible impact due to low exposure culturally and economically viable for small-
rates under field conditions (Sears et al., scale farmers in LDCs.
2001). Field trials in maize comparing differ- Establishing IRM strategies and convey-
ent control interventions on insect diversity ing IRM’s importance to small-scale farmers
found that Bt (Thuricide®)-sprayed plots are a challenge currently being undertaken
hosted greater diversity and abundance of by the IRMA project in Kenya. Farm surveys
non-target insects than insecticide in different agroecological zones quantified
(Dimethoate and Bulldock)-sprayed plots, the area planted to maize and other crops
with both treatments controlling stem borer that are known hosts of stem borers. Field
attack (Songa, 2002). Baseline surveys for trials were conducted by planting plots of
insect abundance and diversity in different these alternative hosts bordered by commer-
maize cropping systems in Kenya have also cial maize varieties to establish moth ovipo-
been established to monitor the future sition preference and productivity by
impact of Bt maize on non-target insects counting exit holes from the different crops.
(Songa et al., 2002). Such an approach should Using the surveys and moth production
be considered for future GE projects to data, the area of effective refugia can be esti-
enable monitoring and more conclusive mated for each agroecology. Using geo-
statements to be made about the impact of Bt graphical information systems (GIS), regions
crops on non-target organisms. were identified that contained a ‘natural’
Recent reviews compiled on the impact of refugia equivalent to 20% maize. Lowland
Bt crops on non-target organisms (including tropical ecologies contain a diverse range of
soil biota), outcrossing to weedy relatives, alternative hosts for stem borers (mostly for-
horizontal gene transfer (gene movement age grasses) and have an adequate natural
between plants and bacteria) and resistance refugia; however, commercial maize areas
by targeted pests (Carpenter et al., 2002; will require a structured refugia (Mulaa et al.,
Shelton et al., 2002) have concluded that the 2001). This approach would complement the
risks are low. However, the issue of resis- ‘push–pull’ strategy outlined earlier for stem
tance management remains a serious con- borer control in maize, as napier grass would
cern for Bt crops (Shelton et al., 2002). serve as a refugia while Bt maize would pro-
Currently, the only insect-resistance manage- vide more complete protection than that cur-
ment (IRM) strategy available for commer- rently being offered by desmodium. In the
cial GE crops is the high-dose/refugia end, IRM strategies for use on small-scale
strategy. The central principle of this strategy farms in LDCs must be economically attrac-
involves the use of a refugia to maintain sus- tive and must fit into the farmers’ cropping
ceptible alleles in insect populations by not system.
imposing a selection pressure on a portion of In the future, monitoring for insect resis-
the pest population (Gould, 1996). In the tance may be achieved through molecular
USA, farmers are expected to plant a struc- markers for resistance genes, such as the
tured refugia. In developing countries, recently identified cadherin alleles associated
enforcement of a structured refugia will be with resistance in the pink bollworm,
difficult as this often runs counter to the Pectinophora gossypiella (Saunders) (Morin et
13IntpestManCh13.QXD 5/5/04 2:16 pm Page 296

296 D. Bergvinson

al., 2003). Clearly, IRM in LCDs will be chal- and sprayers by machine manufactures
lenging but not impossible if: (i) robust vari- (Ekboir, 2002). Monsanto supported a project
eties containing two or more complementary in Brazil to refine the technology package for
resistance genes are developed; (ii) the abun- small-scale farmers and, within 2 years, 90%
dance of alternative hosts to serve as a refuge of the farmers (820,000 ha) were using no-till.
are well characterized; (iii) resistance- The popularity of no-till with farmers has
management programmes can be integrated increased dramatically with the advent
into established cropping systems; and (iv) of herbicide-resistant soybean, which
GIS is used to target monitoring efforts. accounted for the largest area planted to GE
As with synthetic pesticides, which were crops (62% of the global total) in 2002 (James,
perceived to be a panacea for pest control C., 2003a). It also accounted for the largest
over half a century ago, transgenic technol- area of GE crops in LDCs, with Argentina
ogy should be considered as an important growing 13.5 million ha of Round-up
component (HPR) in an IPM programme. Bt Ready® soybean. The high adoption rate of
crops should not displace but rather should this technology has been driven by economic
complement indigenous technologies for returns; it has been estimated that farmers
pest control in LDCs, to avoid overreliance using no-till management obtain savings,
on one technology, which could break down due to reduced labour, fuel and pesticide
if alternative control strategies are not use, of about US$56/ha. This resulted in a
utilized. nationwide savings of US$356 million in
2000 (James, 2002). Environmental benefits
include reduced soil erosion and runoff of
Resource conservation technology pesticide residues, improved air and water
quality and reduced exposure to pesticides
Resource conservation technologies (RCTs), (Carpenter et al., 2002), which make this
such as no-till practices, have experienced technology attractive for other crops in
rapid adoption in recent years. No-till agri- LDCs. Herbicide consumption will continue
culture started to be adopted by large-scale to increase in regions where no-till is being
farmers in Brazil and Argentina in the early adopted, such as Latin America and the USA
1990s, associated with price reductions in (Fig. 13.3), with herbicide consumption
glyphosate (broad-spectrum herbicide) and accounting for 45% of the global pesticide
the development of more suitable planters market (FAOSTAT, 2002). The role of

200 Insecticide
Herbicide
Consumption (t ¥ 1000)

160
Fungicide/ Bactericide

120

80

40

0
Africa LA & Car. Asia USA Other
industrial
Fig. 13.3. Consumption of insecticides, herbicides, fungicides and bactericides in developing countries
within Africa, Latin America–Caribbean, Asia and industrial countries. Based on 89 countries, not including
China. (Based on FAOSTAT, 2002, for 1997.)
13IntpestManCh13.QXD 14/4/04 2:26 pm Page 297

IPM in Developing Countries 297

herbicide-resistant products will increase as the interactions (positive and negative) to

the rural workforce continues its urban develop intensified, sustainable cropping
migration in the coming years (Pingali, systems in LDCs.
2001). However, IPM has not kept pace with
the practice of zero-till in Argentina.
Monitoring of pests, diseases and biological Geographical information systems to target
control agents should be undertaken, with technologies and monitor insect pest and
proper baseline studies being conducted to disease movement
help in the development of IPM programmes
tailored for no-till cropping systems. Geographical Information Systems (GIS) will
The rice–wheat cropping systems (RWCS) probably play an ever-increasing role in IPM,
of the Indo-Gangetic Plain occupy 13.5 mil- in both developed and developing countries.
lion ha and account for one-third of the total In developing countries, GIS can be used to
rice and wheat production in this heavily assess and predict the distribution of weed
populated region. A falling water-table, and insect pests, by enabling scientists to
excessive soil erosion and low organic- visualize geographically large data sets, pro-
matter content in the soil are major produc- vided the collection sites are geographically
tion constraints in the region, with farmers referenced (latitude and longitude).
using elevated nitrogen rates to compensate Databases for GIS include FAO’s classifica-
for reduced soil fertility, resulting in tion of soils, temperature, rainfall, potential
increased losses from disease and insect evapotranspiration, population, rivers, roads
attack (Srivastava, 2000). Given these prob- and specialized databases such as insect
lems, the region is an excellent candidate for population density and species distribution.
RCTs and associated IPM strategies. A good example of specialized databases is
In 1994, the Rice–Wheat Consortium was that developed at the International Centre
established to tackle these constraints by for Insect Physiology and Ecology (ICIPE) to
introducing RCTs into farmers’ fields. After characterize the distribution of maize stem-
harvesting rice, wheat is direct-drilled into borers in East Africa (Irungu et al., 2003).
rice residue to avoid ploughing, utilize the Several native species of stem borer are
residual moisture in the soil and conserve found in Africa, but the spotted stem-borer,
the straw residue. Labour, fuel and water C. partellus, has expanded into new agro-
savings have driven the rapid adoption of ecologies since its introduction into the
no-till, but concern about the impact of region about 50 years ago. GIS are being
residues on insect pests and diseases has used to predict the distribution and potential
been expressed. Insect control was tradition- impact of classical biological control efforts
ally achieved using cultural-control prac- following the introduction of the parasitic
tices, such as removing rice stubble to reduce wasp, Apanteles flavipes (Cameron) (Emana et
stem borer populations (Srivastava, 2000). al., 2002). They have also been used to define
Conversely, under the no-till system, which climatic factors favour the develop-
reduced disturbance of the agroecosystem ment of C. partellus and the location of those
increases the abundance and diversity of bio- agroecologies to better target the release of
logical control agents that regulate stem biological control agents in the future. GIS
borer populations (P. Hobbs, Mexico, 2003, may also help researchers target locations for
personal communication). Understanding the collection of biological control agents to
the interactions of conservation-tillage prac- better reflect the agroecology in which the
tices with agroecosytems will become biological control agent is to be released, thus
increasingly important as more farmers in ensuring that the collected species/biotype is
LDCs adopt RCTs, such as zero-till, in order already conditioned to the target ecology.
to increase the profitability and sustainability The application of appropriate GIS tools
of farm enterprises. Since RCT and IPM are and databases can also help scientists in
both key components of future ICM pro- LDCs to make better decisions regarding
grammes, it will be important to characterize where to target their pest-control interven-
13IntpestManCh13.QXD 14/4/04 2:26 pm Page 298

298 D. Bergvinson

tions and what control interventions used in found in larger towns in LDCs and increas-
other countries may be most suited to their ingly in smaller villages. This means that a
targeted agroecology. However, for most researcher, extension provider or farmer can
LDC scientists, this technology has remained now access information regarding new tech-
largely in the domain of GIS experts, due to nologies being used on the other side of the
impediments such as cost, complexity and world. For the time being, most of these
the availability of standardized data sets that ‘exchanges’ are in one direction, North to
have sufficient resolution to be useful in South. However, as Internet-based networks
IPM. Some of these constraints are now for IPM become established, exchanges
being addressed by the development of new between IPM practitioners in LDCs will
software platforms that are easy to learn and increase as scientists and farmers look to
are able to integrate GIS tools with extensive each other in similar agroecologies to find
databases relevant to agriculture (Irungu et common solutions for crop-production con-
al., 2003). straints.
Another promising area is the marriage of All the IARCs have websites that provide
GIS and global positioning systems (GPS) useful introductions to the research centre,
along with satellite images and detailed soil but, as the Internet has matured, so has the
mapping, prerequisites for precision agricul- power of those websites in enabling NARS
ture. This cutting-edge package of techno- scientists to access technologies recently
logical tools allows farmers to apply developed by the IARCs, including
agrochemicals, such as fertilizers and pesti- germplasm, ICM and IPM for different
cides, only as needed. From the perspective staple crops. These sites are accessed
of tactical pest control, precision IPM would through the CGIAR (http://www.cgiar.org)
mean the application of selective pesticides or directly by substituting the centre’s
to control weeds, insects and diseases when acronym (e.g. IRRI for the International Rice
and where it is necessary to maximize Research Institute) for ‘cgiar’. The IRRI web-
returns in commercial crop production. The site is a good example of how the Internet
prospect of using precision agriculture in can serve LDC farmers by helping them
LDCs may seem a distant dream, but this identify crop-production constraints and
may come sooner than we think, particularly address them with solutions, including IPM
in the large-scale commercial operations technologies. The website is called the
found in some of these countries. Expected Rice Knowledge Bank (http://www.
technology cost decreases, particularly for knowledgebank.irri.org/) and it provides
the imaging and GPS components, should the latest information on ICM for rice crop-
spur greater adoption. Browsing the Internet, ping systems in LDCs. The website contains
one can find several on-line degree-day decision tools for crop management and pest
models for several insects and diseases in identification, which enables identification of
industrial countries. The availability of com- pests versus non-target insects during field
parable databases and models for LDCs will surveys, resulting in fewer insecticide appli-
depend on demonstrating the utility to com- cations. NARS can access research materials
mercial farmers and on collaborative field such as manuals on hybrid rice seed produc-
research efforts between NARS, advanced tion, IPM, rice taxonomy, technology-
research institutes and IARCs. transfer methods and support skills such as
consensus building, e-learning and presenta-
tion and training skills. Similar websites are
Internet access to IPM technology and being developed at other IARCs to accelerate
networks the devolution of technology to NARS and
other research partners. The IARCs are also
As illustrated in the previous section, the in the process of developing websites that
Internet has opened up information and can serve as a forum for ICM in developing
technology exchange between the North and countries. The most advanced example of
the South. Internet cafés are now commonly IPM networking in developing countries is
13IntpestManCh13.QXD 14/4/04 2:26 pm Page 299

IPM in Developing Countries 299

the System-wide Programme on IPM the aggregated decline in pesticide use in

(SP–IPM) (James et al., 2003). As discussed Asia during the past decade (Fig. 13.4) has
earlier, this network represents a diverse set largely come from IPM efforts on several
of IPM stakeholders in both the public and fronts: host-plant resistance (insects and dis-
private sectors and focuses on addressing eases), promotion (by IPM programmes) of
the most pressing biotic constraints of the the judicious use of pesticides and with-
resource-poor through IPM. Noteworthy drawal of government-subsidized pesticide
websites that link to additional resources programmes in most Asian countries
include FAO, the Technical Centre for (Pingali et al., 1997). Indonesia, which subsi-
Agricultural and Rural Cooperation (CTA) dized up to 85% of the cost of pesticides dur-
and PEST CABWeb (http://pest.cabweb. ing the early 1980s, banned by presidential
org/), among others. The Internet, through decree the use of 57 of the 66 broad-spectrum
such sites as the SP-IPM, has been a valuable pesticides used on rice. By 1989, pesticide
tool for disseminating information, thereby subsidies were no longer offered (Gallagher,
increasing public awareness of the benefits of 1992). The impact these policies, among oth-
IPM and raising the profile of IPM within ers, had on Indonesian rice production from
communities. We can expect these trends to 1984 to 1990 was dramatic; production rose
grow exponentially in the years to come. from 38 to 45 million t while Indonesia went
from being a net importer of pesticides
(US$47 million) to a net exporter (US$15 mil-
Threats lion) (FAOSTAT, 2002). By 2002, rice produc-
tion reached 51 million t, providing a good
A threat is a perceived imminent danger and, example of what progressive policies com-
for IPM, these imminent dangers can be bined with massive farmer training can
averted by advocacy on the part of scientists, accomplish.
farmers and the general public in shaping Among international agencies, the World
the political and social environment to Bank is one of the most influential in promot-
favour the adoption of sustainable technolo- ing IPM. For loans to be granted, project pro-
gies. Many of these threats are well recog- posals must conform to the World Bank
nized and are now being addressed by some, Operational Policy 4.09, which defines IPM as:
but not all, LDC governments. The purpose a mix of farmer-driven, ecologically based
of highlighting some selected threats is to pest control practices that seeks to reduce
encourage strategic thinking about advocacy reliance on synthetic chemical pesticides. It
measures and new directions in public involves a) managing pests (keeping them
awareness. below economically damaging levels) rather
than seeking to eradicate them; b) relying, to
the extent possible, on nonchemical
measures to keep pest populations low; and
Policy
c) selecting and applying pesticides, when
they have to be used, in a way that
Public policy, perhaps more than any other minimizes adverse effects on beneficial
factor, holds sway over the course of IPM. organisms, humans and the environment.
During the early stages of the green revolu- (World Bank, 1998)
tion, intensified rice production was visibly
and sometimes severely damaged by insects, The policy does not allow the use of class Ia
which created apprehension among some and Ib pesticides and promotes the reduction
scientists and policy makers about a major of synthetic pesticide use in developing
outbreak. To address this threat, policies countries. However, organizations such as
were implemented that made pesticides the Pesticide Action Network North America
readily available and affordable to farmers have called for tighter monitoring of the pol-
(Pingali et al., 1997). Unfortunately, farmers icy during project implementation to ensure
received little training at that time about the that the policy is adhered to (Ishii-Eiteman et
safe and judicious use of pesticides. Today, al., 2002).
13IntpestManCh13.QXD 14/4/04 2:26 pm Page 300

300 D. Bergvinson

Import of pesticides 9000

1600
8000
1400
7000
Developing countries

Industrial countries
1200
6000
1000 Africa import
5000
800 Asia import
4000
LA & Car. import
600 3000
Industrial import
400 2000
200 1000
0 0
1962 1970 1980 1990 2000

Export of pesticides 9000

1600
8000
1400
7000
Developing countries

1200

Industrial countries
Africa export 6000
1000 Asia export 5000
800 LA & Car. export
4000
600 Industrial export
3000
400 2000
200 1000

0 0
1962 1970 1980 1990 2000

1000 Net import of pesticides 6000

5000
Developing countries

800
Industrial countries

Africa import 4000

600
Asia import
3000
400 LA & Car. import
2000
Industrial export
200 1000

0 0
1962 1970 1980 1990 2000

Years
Fig. 13.4. Import, export and net import of pesticides (millions of US$) over the past 40 years in developing
countries within Africa, Latin America–Caribbean, Asia and industrial countries (based on FAOSTAT, 2002,
for years 1962, 1970, 1980, 1990 and 2000).
13IntpestManCh13.QXD 14/4/04 2:26 pm Page 301

IPM in Developing Countries 301

Globalization Intensification of agriculture

Globalization is a trend that will probably Crop production in developed and develop-
continue due to the benefits accrued from ing countries should use all crop-manage-
trade liberalization, increased exchange of ment tools that have met biosafety,
knowledge, technology and culture and environmental and health standards to be
increased mobility of capital and labour. If applied to the challenge of meeting the food
correct policies and institutions are in place, demands of the next 50 years. Pesticides
globalization could enhance economic have been and will continue to be an impor-
growth and poverty alleviation in develop- tant component of modern agriculture in
ing countries (Pinstrup-Andersen, 2002). both developed and developing countries.
One potential outcome would be increased Crop-protection technology, along with fer-
competition in agricultural markets, which tilizers and improved crop varieties, has
would promote the cultivation of crops that resulted in unprecedented increases in pro-
are best adapted to a given agroecology and ductivity over the past half-century.
are thus most profitable. However, these gains have been built on the
However, globalization also presents intensification of cropping systems, such as
challenges to IPM, perhaps the most notable
rice production systems in which two or
being the introduction of exotic pests, associ-
three crops are grown annually, resulting in
ated with increased trade liberalization and
pest outbreaks attributed to the absence of
movement of labour. Making the problem
dry-fallow to break the pest cycle (Litsinger,
worse, many developing countries do not
1989). Most intensified cropping systems
have the human and financial resources
were not designed with sustainability or the
needed to operate effective quarantine facili-
maintenance of biological diversity in mind.
ties. Moreover, the number of taxonomists
The upshot of this is narrow-based agroecolo-
available worldwide to conduct the neces-
gies that are susceptible to pest invasions.
sary monitoring for exotic pests is inade-
quate. Through networks such as Sustainable crop management systems
BioNET-International, taxonomists can pool must be maintained in the forefront of tech-
their expertise through regional networks nology development to ensure the future
and common databases to address the chal- viability of production systems. Agricultural
lenges in monitoring pest introductions and technologies that have a high potential for
prescribing biological control agents that can sustainability include intercropping
be used to regulate introduced pest species. (increases soil fertility when legumes are
Agricultural subsidies in industrial coun- used and reduces pest attack, as in the
tries further complicate world food security push–pull strategy); rotations; agroforestry
by increasing production in developed coun- (trees can exploit water and nutrients and
tries which depresses international grain provide mulch, while herbaceous crops pre-
markets, often to the detriment of the rural vent erosion); sylvo-pasture (trees and pas-
poor in developing countries, whose sole ture for mixed livestock systems); green
source of income is agriculture (Pinstrup- manuring (legumes to fix nitrogen for incor-
Andersen, 2002). Depressed prices are exacer- poration to improve soil fertility); conserva-
bated by the inability of small-scale farmers tion tillage (reduced soil erosion); biological
to store their production, forcing them to sell control; and IPM (Conway, 1998).
their harvest quickly into saturated local
markets, which further reduces their farm
revenue. This points to the need for increased Reduced international funding for
research on reducing postharvest losses for agricultural development in LDCs
resource-poor farmers through improved
storage systems at both local and national A decade-long decline in funding for agricul-
levels to buffer the effects of the variable pro- tural development in LDCs by countries of
duction often experienced in semi-arid the North has seriously slowed progress in
regions of the developing world. this vital area, with some projects being dis-
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302 D. Bergvinson

continued before their benefits can reach destruction of natural habitats. Insect pest
farmers’ fields. IPM projects have not gone and disease pressures are projected to
unaffected and, should support continue in increase, potentially resulting in larger agri-
this downward direction, the consequences cultural and forestry losses in Africa (Gitay et
are very worrying. To counter this trend, the al., 2002). A contributing factor would be the
potential and actual impact of IPM must be possible decoupling of biological control
documented in a scientifically sound manner agents from their prey and new pests being
and presented in simple terms to govern- controlled with increased use of pesticides,
ment officials and policy makers in develop- which would negatively affect non-target
ing and industrial countries. An impact species. Reduced tillage, continual ground
assessment of IPM programmes should be cover, agroforestry and IPM promote biodi-
implemented at the beginning of projects to versity and offer a buffer against these effects
document the impact and enable mid-course of climate change (Gitay et al., 2002).
adjustments to better meet the socio- In order to position IPM to meet these
economic needs of farmers and to validate environmental changes, scientists need to
the investments made in the technology. think ahead to the types of abiotic–biotic
Emphasis should also be given to IPM’s con- interactions that will have an impact on pest
tribution to sustainable cropping systems management, especially in LDCs, where
and improved quality of life (better human these interactions are not well defined.
health and reduced pesticide loading in the Without any biotic stresses, maize produc-
environment). tion in Africa and Latin America is expected
to decline by 10% and by as much as 30% in
some parts of Brazil, Venezuela and South
Climate change Africa (Jones and Thorton, 2003). Plants
grown under environmental stress condi-
Greenhouse gases (CO2, CH4 and N2O) have tions associated with climate change are gen-
risen dramatically during the past century erally more susceptible to insects (Heinrichs,
due to combustion of fossil fuels, changes in 1988) and diseases (Coakley et al., 1999).
land use, etc., with CO2 levels increasing However, the change in pest/disease status
31% (Gitay et al., 2002). In the same period, would depend on the specific insect– or
global mean surface temperature has disease–host complex as well as technologi-
increased by 0.6°C, with the largest increases cal and socio-economic changes that occur
occurring in the mid- and high latitudes of within a given agroecological region.
northern continents. The Intergovernmental Modelling and GIS will be essential comple-
Panel on Climate Change (IPCC) estimates mentary tools for simulating and mapping
that the mean temperature increase for the expected changes in biotic stresses and for
band encompassing most developing coun- providing LDC policy makers and stake-
tries (30°S to 30°N) will increase by 3°C and holders with comprehensive advice on
changes in precipitation patterns will vary impacts and mitigation strategies, including
among continents (IPCC, 2001). The impacts IPM programmes.
of climate change on people’s livelihoods
will be greatest in the tropics and subtropics,
in particular Africa, as many poor small- Regional IPM Issues
scale farmers will have few alternatives to
agriculture (Gitay et al., 2002). Using scenar- Although LDCs worldwide have much in
ios, the IPCC has described ‘ecosystem common when it comes to IPM, they also
movements’, in which entire ecosystems have considerable differences, based on
migrate to new locations, and ‘ecosystem socio-economic, cultural, political, economic
modification’, in which in situ changes in and climatic conditions, which will affect
species composition and dominance occur. IPM development and adoption. The follow-
Overall, biodiversity is expected to decrease ing sections briefly highlight some of the
because of increased land-use intensity and unique issues that are likely to influence IPM
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IPM in Developing Countries 303

practices in each region and areas of research economic studies should be incorporated
emphasis to meet the changing political and into all IPM projects to ensure that the right
physical climate in which IPM operates. technology is being targeted to the farmers’
needs and is economically attractive.
Biological control programmes have gener-
Africa ally been extremely successful and well
accepted in Africa, given their sustainability
African agriculture is predominantly small- (no cost to farmers) once established and
scale, mixed crop/livestock farming systems, they have not suffered from the overuse of
consisting of holdings of less than 1 ha to a pesticides, given the low application rates
few hectares. Often, farmers do not own the commonly used by subsistence farmers.
land but have the right to farm the land their Development of host-plant resistance for dis-
ancestors cultivated, under the regulation of eases and insects will become more impor-
village headmen or local government offi- tant as the technologies to efficiently
cials. Indigenous crops include: finger millet incorporate resistance into local varieties
(E. coracan), bulrush millet (P. americanum), become established in Africa. Already, con-
rice (O. glaberrima), sorghum (S. bicolor), cow- ventional sources of resistance are being pro-
pea (V. unguiculata), coffee (Coffea spp.) and moted in several crops.
rye (S. cereale), with sorghum and millet GE crops with genes for insect, disease
being well adapted to arid ecologies and herbicide resistance will play an impor-
(Simmonds, 1976). The most important intro- tant role in sustainable cropping systems for
duced crops include maize, cassava, sweet Africa. Herbicide-resistant maize with a seed
potato and Irish potato. Successful IPM treatment containing imazapyr and pyri-
interventions in Africa were recently thiobac has been identified as an effective
reviewed (Zethner, 1995; Dabrowski, 1997; control for the parasitic weeds S. hermonthica
Abate et al., 2000). Pesticide usage in Africa and S. asiatica (Kanampiu et al., 2002) in on-
has been slowly increasing (Fig. 13.4), but farm trials in Kenya. This technology would
remains much lower than in other regions. be particularly suited to low-fertility soils,
However, sustainable crop protection that where the yield losses to Striga are most
improves farm income is a main driving severe. The use of Bt maize and virus-
force for African development projects; some resistant sweet potato is also expected to
of these have focused on research and devel- play an important part in boosting crop pro-
opment of biological control (cassava, sweet duction to meet future demands in Africa
potato, maize, sorghum, stored products, (Wambugu, 1999). An important constraint
fruit production, coffee, cotton and cowpea) facing the large-scale adoption of GE crops
and, to a lesser extent, host-plant resistance will be the harmonization of biosafety proto-
(maize, sweet potato, cassava); and chemical cols within Africa, which are now under dis-
control, mainly in rice and cotton (Zethner, cussion at a regional level in East Africa (C.
1995). Although pests are a problem, farmers Ngichabe, Nairobi, 2003, personal communi-
face other, often more pressing, constraints, cation).
such as poor soil fertility, erosion, drought
and severe fluctuations in market prices. An
ICM approach is required to address these Latin America
wide-ranging issues. The ‘push–pull’ strat-
egy for stem borer control in maize provides Latin America and the Caribbean are home
a good example of ICM used to address sev- to numerous agroecologies and cropping
eral constraints (stem borers, Striga, soil fer- systems, with farms ranging from subsis-
tility) using economically viable crops tence plots to large-scale commercial oper-
(napier grass for livestock). ations growing several crops. Indigenous
As in the past, successful IPM will need to crops in this region include maize (Z. mays),
show a clear economic benefit to the farmer beans (Phaseolus spp.), cotton (Gossypium hir-
for adoption to occur. This means that socio- sutum, G. barbadense), tomato (L. esculentum),
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304 D. Bergvinson

sweet potato (I. batatas), rubber (H. brasilien- principal food and fibre crops. EMBRAPA
sis), potato (S. tuberosum) and cassava (M. and the Argentinean National Institute for
esculenta) (Simmonds, 1976). Given the large Agricultural Technology (INTA) have pro-
number of indigenous crops, this region rep- vided host-plant resistance, commercial
resents an important source of biodiversity capacity for rearing biological control agents
for providing new genes for host-plant resis- and sustainable crop management methods
tance as well as biological control agents for (i.e. no-till). Exploration for new biological
classical biological control or augmented controls will be an important contribution
release within the region. The overuse and from this region to the international commu-
misuse of pesticides have been a motivating nity and it should be coordinated through a
force for IPM in this region, with Brazil central platform such as BioNET-
accounting for approximately half of the pes- International, to ensure that passport data on
ticide consumption in Latin America (FAO- putative control agents is available to IPM
STAT, 2002). The impact of IPM in South practitioners and government quarantine
American countries has recently been com- facilities. Using a central platform will also
piled by Campanhola et al. (1995), with most accelerate the use of these assets in classical
IPM projects focusing on the judicious use of biological control programmes.
selective pesticides (including biopesticides),
crop rotations and cultural methods.
Augmented release of parasitoids – A. Asia
flavipes, Trichogramma pretiosum Riley,
Paratheresia claripalpis (Wulp) and Asia was the home of the green revolution
Metagonistylum minense Townsend – has also and will probably be the major player in the
been used successfully to control the sugar- ‘doubly green revolution’. Prior to the green
cane borer, Diatraea saccharalis Fabricius, in revolution, Filipino farmers grew local rice
Brazil and Colombia. varieties with only 7.5% using synthetic pes-
The adoption of IPM has been largely dri- ticides in 1954; this grew to 90% by 1994,
ven by economics, but also by a growing with a concomitant doubling of yield to
public awareness of the hazards pesticides 2.7 t/ha (Teng, 1994). However, by the 1970s,
pose to human health and the environment. this was recognized as an unsustainable
As with the other regions, IPM fits well trend and, since then, rice scientists have
within the context of ICM strategies. In refocused their research to IPM for rice pests,
Argentina and Brazil, the adoption of mini- including the development of insect- and
mum and no-till has increased herbicide con- disease-resistant rice varieties.
sumption (Fig. 13.3), but it has also reduced In Asia, however, pesticides have become
soil erosion and made farming more prof- part of the rice production culture, a ten-
itable and sustainable, once the appropriate dency that is slowly being changed through
planting equipment was made available regional IPM programmes using an FFS
(Ekboir, 2002). The development of herbicide- approach. However, only a relatively small
resistant soybean, which is now grown on portion of the large Asian farming commu-
approximately 13 million ha in Argentina nity has been exposed to IPM courses, but
(James, C., 2003a), has greatly accelerated new communication techniques, as outlined
adoption of RCTs. Given the expansive area in the Strengths/Communication section,
planted to herbicide-resistant soybean, IRM show signs of accelerating the dissemination
strategies should be enforced for the long- process.
term efficacy of this soil-conservation tech- Market price also plays a key role in pesti-
nology. As with Africa, regional biosafety cide use in parts of Asia. As cropping sys-
protocols should be established to enable the tems increasingly diversify into high-value
trade of GE crops in the future. commodities, in which aesthetics determine
Latin America has several strong NARS market price, farmers will probably return to
capable of taking the lead in the develop- prophylactic sprays as a way of ensuring
ment of alternative control strategies for the high market value for their crops (Pingali,
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IPM in Developing Countries 305

2001). Although FAO is already working at socio-economic systems to generate ‘alterna-

addressing this issue through FFS pro- tive futures’ (IPCC, 2001). The four divergent
grammes, such issues might best be handled socio-economic circumstances they devel-
though policy and pesticide registration pro- oped fall into four quadrants based on a
cedures that are tightly enforced through regional/global axis and an economic/envi-
monitoring of pesticide residues and subse- ronmental axis (Fig. 13.5). For the purpose of
quent penalties for violators. This system has a strategic planning exercise in CIMMYT,
been used successfully in Taiwan to reduce these different socio-economic environments
pesticide residues in vegetables, through a were labelled by cropping system to capture
programme known as Good Agricultural the ‘flavour’ of the agricultural impact of
Practice (GAP). Farmers obtain a higher mar- each scenario (D. Watson and M. van Ginkel,
ket price when their products are inspected Mexico, 2003, personal communication).
and labelled with the GAP logo, enabling These scenarios are driven by diverse forces,
consumers to recognize products that con- including globalization, rate of technology
form to safety regulations, which often change, degradation of natural resources,
results in a higher price for the farmer water scarcity, climate change, changing
(TACTRI, 2002). farming structure and agricultural marketing,
China and India have been dubbed ‘super consumer behaviour/preferences, health
NARS’ by some involved in agricultural issues and nutrition, urbanization, national
development, based on their immense capac- and international instability and conflict,
ities in agricultural research, which is now changing roles of key actors, demographics,
expanding into biotechnology. Biotech- environment and food trade policies, gover-
nology will probably assume an increasingly nance and intellectual property rights (IPCC,
important role in delivering crop varieties 2001; Pinstrup-Andersen, 2002).
with greater tolerance to abiotic and biotic The ‘Monoculture’ (global/economic) sce-
stresses, which will serve as the cornerstone nario predicts rapid economic growth and
of ICM programmes of the future. Already, rapid development of technologies due to
the use of Bt cotton in China has demon- global markets and large financial invest-
strated the economic, health and environ- ment of the private sector in technology
mental benefits to be realized by commercial development (IPCC, 2001). One example of
and small-scale farmers (Huang et al., 2002). this would be pesticide research to target
Future biotechnology applications will prob- major crops in both industrialized and devel-
ably include the development of drought- oping countries. Increased polarization of
tolerant crops and the use of herbicide resis- wealth, population growth and climate
tance to address weed control in intensified change will have an adverse effect on natural
cropping systems, as labour costs increase resources, including reduced biodiversity.
(Pingali, 2001). As with pesticide policies, the Production systems would scale up to com-
use of natural resources such as water, will pete in global markets, which would proba-
probably require legislation to deter abuse of bly result in the increased use of pesticides
water resources and to make water access as part of a tactical control strategy in order
more equitable within and between countries. to meet the increased production demands.
These policies may affect IPM as reduced irri- The ‘Intercropping’ (global/environmen-
gation may cause a shift in the pest complex tal) scenario would see the interaction and
and require new cultural management strate- interdependence of countries to attain more
gies to regulate new pest complexes. social equity and environmental sustainabil-
ity, at some cost to economic development.
Internationally agreed-upon policies would
A Look to the Future: Impact of Four be enforced in a more uniform manner to
Socio-economic Scenarios on IPM reduce environmental degradation and regu-
late the management of renewable resources
IPCC has used scenarios as a tool to paint the (IPCC, 2001). Crop diversity would increase,
backdrop of the future world under different as crops would be targeted to agroecologies
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306 D. Bergvinson

Environmental

Strategic (Integrated Pest Management)

‘Intercropping’ ‘Gardens’

GE R&D

Investment-intensive Dissemination of
Global Regional
global applications local technologies

Pesticide R&D

‘Monoculture’ ‘Slash-and-burn’

Tactical (Integrated Pest Control)

Economic
Fig. 13.5. Socio-economic scenarios based on global versus regional markets and economic (tactical IPM)
versus environmental (strategic IPM) emphasis for technology development in crop management. R&D,
research and development. (Based on scenarios developed by the Intergovernmental Panel on Climate
Change (IPCC, 2001).)

in which they are most suited for cost- petitiveness (IPCC, 2001). Agroecology
effective production, with production subsi- would be the predominant agricultural
dies being reduced. Under this scenario, ICM philosophy to promote biodiversity and
would be promoted to deliver sustainable, focus on indigenous IPM technologies, which
high-yielding cropping systems. Pesticide would be exchanged between communities
use would be reduced in favour of alterna- or within a region as described by Altieri
tive control strategies. GE crops would be (1995). ICM would be promoted using low-
the focal point for private sector investment cost technologies, with capital-intensive tech-
to deliver sustainable cropping technologies. nologies, such as genomics or GE crops, not
IPM technologies would be developed to having a large enough market to stimulate
operate at a global level for a common good, commercial interest in developing countries.
with such examples being the global moni- The final scenario, ‘Slash-and-Burn’
toring of pests and diseases using GIS and (regional/economic), would lead to a hetero-
enhanced cooperation and exchange of bio- geneous world in which the main theme
logical control agents for ‘classical’ biological would be self-reliance and the preservation
control programmes. of local identity. This scenario would see the
The ‘Gardens’ (regional/environmental) degradation of the environment and misuse
scenario would place less emphasis on of natural resources, as socio-economic sys-
globalization and more on local/regional tems are focused on local exploitation and
markets. In some ways this resembles an not sustainability (IPCC, 2001). Resource-
agricultural version of E.F. Schumacher’s poor nations would not be able to support
vision put forward in Small is Beautiful (1975). agricultural research and development,
Agricultural policies would be developed for resulting in low adoption of knowledge-
sustainable agriculture, at a possible cost to intensive technologies, such as IPM, and the
production efficiency and international com- use of old and possibly obsolete pesticides
13IntpestManCh13.QXD 14/4/04 2:26 pm Page 307

IPM in Developing Countries 307

(when economically viable), or they may will rely heavily on ICM and IPM in particu-
resort to using no external inputs, resulting lar. In order to address this looming produc-
in low and variable yields, especially in mar- tion demand, a ‘doubly green revolution’
ginal environments. will be required that exploits two areas of
Examples of all four scenarios exist in the modern science: biotechnology to under-
world today and this mosaic will probably stand and manipulate living organisms and
continue for the foreseeable future given the modern ecology to understand the dynamics
divergent development and trade policies of agricultural and natural-resource ecosys-
supported by different governments. tems (Conway, 1998). Such technologies can
However, the ‘Monoculture’ scenario is the only be developed in partnership between
most prevalent socio-economic scenario farmers, extension, researchers and policy
today, one that largely focuses on crop-pro- makers.
duction efficiency. Under this scenario, IPM Intensification of cropping systems must
would not be a high priority unless it came be approached from a sustainable-
at little additional cost to the producer or agriculture perspective. If care is not used in
was mandated through national/interna- increasing production, biodiversity, which
tional policies. Increased net import of pesti- has buffered many mixed cropping systems
cides by developing countries since the early in LDCs, may be compromised and, with it,
1960s (Fig. 13.4) is evidence that this scenario the diversity of organisms associated with
will probably predominate at least in the tropical agroecologies. Management strate-
short term. The political will to move gies and technologies that minimize distur-
towards the ‘Intercropping’ scenario appears bances to agroecosystems should be
to exist, as seen in US policy on IPM promoted, such as conservation-tillage tech-
(Jacobsen, 1996), the European Union (EU) nology and the strategic use of habitat man-
promoting ICM in agricultural policy agement to enhance the efficacy of biological
(Wattiez et al., 2003) and the World Bank controls and reduce the use of broad-
Operational Policy 4.09 (World Bank, 1998). spectrum pesticides.
ICM is strongly promoted in the Pesticide use in LDCs has increased over
‘Intercropping’ scenario, which would see the last 30 years, with Asia becoming a major
the use of all control forms, including GE exporter of pesticides and Latin America
crops, to develop sustainable cropping sys- becoming the largest consumer of pesticides,
tems. When it comes to IPM, there is an in large part due to conservation-tillage prac-
apparent dichotomy between the policies tices. Pesticides will continue to be an impor-
supporting IPM and the economic realities, tant component in ICM, but the
as reflected by the global increase in pesti- discontinuance of class 1a and 1b pesticides
cide use. should be strongly promoted through the
World Bank Operational Policy 4.09 and pes-
ticide subsidies should be eliminated to
Conclusions allow market forces to exert economic pres-
sure to minimize their use. Chemical manu-
During the next two decades, it is estimated facturers have become active in product
that the world will have to feed approxi- stewardship, either directly or through a
mately 2.5 billion more people, with most of consortium like CropLife International. The
this growth occurring in LDCs, resulting in a private sector will probably expand its role
projected shortfall of cereal production in in technology dissemination and training, by
LDCs of 197 million t (Rosegrant et al., 2001). providing educational material to farmers to
Most of this production will need to come promote product safety and stewardship to
from LDCs, which are showing stagnation in enhance the efficacy, safety and long-term
per cent yield gains, dropping from 2.9% effectiveness of pesticide products in the
during the green revolution to a predicted developing world.
1.2% during the next 20 years (Rosegrant et The use of biotechnology to produce
al., 2001). Increasing the rate of yield gain insect-, disease- and herbicide-resistant
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308 D. Bergvinson

plants has already become established in policies ex ante. Using these tools to communi-
North America, Australia, Argentina and cate the positive impact IPM has made will be
China, along with a steady rate of increased critical in generating public and political sup-
adoption in several developing countries port to increase the adoption of proven IPM
(Fig. 13.2). The use of genetic engineering technologies.
holds considerable promise in reducing the Given the environmental and social com-
environmental and health costs associated plexity of farming systems in developing
with pesticide use, as well as increasing farm countries, participatory methods have
revenue. Since GE crops contain the pest proved to be the most successful approach
control trait in the seed, distribution of the for disseminating IPM practices to farmers in
control technology to farmers should be LDCs. Viewing farmers as an equal partner
accomplished in an easy and equitable man- in technology development and testing will
ner. In order to realize the full potential of foster ownership of IPM technologies and
GE crops, biosafety and intellectual property increase adoption. Farmers should be offered
legislation, at both national and international a ‘basket of options’ to test, given the socio-
levels, must be established in LDCs. Traits to economic complexity of farming systems in
be incorporated should be decided in consul- LDCs. Dissemination of proven techniques
tation with farmers, consumers and scientists that have clear economic and health benefits
to ensure that GE crops meet the needs of to farmers must be promoted, using various
these groups and pose no significant risk to media and containing a simple message that
the environment. is couched in a socially sensitive way to
Digital technology and high-speed inform and persuade the farm family.
telecommunications have enabled information The green revolution, which addressed
to be accessed from around the world via the the food-security crisis of the 1960s and
Internet. Although there was a great discrep- 1970s, involved scientific innovation and
ancy in digital technology between industrial active promotion of high-yielding varieties
and LDCs at the end of the 20th century, this that could transform fertilizer inputs into
divide is rapidly narrowing as LDCs develop
grain production – but it did not involve
the telecommunication capacity to fully partic-
IPM. For the ‘doubly green revolution’ to
ipate in the Internet. Most IPM websites are
succeed in feeding the world through sus-
currently hosted in industrial countries; how-
tainable cropping systems, a concerted and
ever, this trend is changing, as more
integrated effort on the part of scientists,
researchers in developing countries are able to
farmers and policy makers will be required
establish websites that promote local IPM
to create awareness and a political and regu-
technologies. The use of GPS will complement
latory environment in which sustainable
web networks by providing researchers and
technologies like IPM are embraced to meet
extension providers with tools that will enable
the food and fibre demands of the 21st
them to define regions where production con-
straints are most acute, develop targeted tech- century.
nologies for those regions and monitor their
use. The use of GIS will also become more
important as increased effort is made to define Acknowledgements
the impact of IPM on crop production in
LDCs; this is particularly true for the spread of Support by the Syngenta Foundation for
classical biological control agents and resistant Sustainable Agriculture is gratefully
varieties. It will also provide a visual aid for acknowledged. The author wishes to thank
researchers and policy makers to define prior- D. Poland for editing the manuscript and M.
ity areas for ICM and to better define produc- van Ginkel and D. Beck for reviewing the
tion constraints and assess the impacts of manuscript.
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IPM in Developing Countries 309

References

Abate, T., van Huis, A. and Ampofo, J.K.O. (2000) Pest management strategies in traditional agriculture:
an African perspective. Annual Review of Entomology 45, 631–659.
Altieri, M.A. (ed.) (1993) Crop Protection Strategies for Subsistence Farmers. Westview Press, Boulder,
Colorado, 197 pp.
Altieri, M.A. (1995) Agroecology: the Science of Sustainable Agriculture. Westview Press, Boulder, Colorado,
433 pp.
Atkin, J. and Leisinger, K.M. (2000) Safe and Effective Use of Crop Protection Products in Developing
Countries. CAB International, Wallingford, UK, 163 pp.
Bänziger, M. and de Meyer, J. (2002) Collaborative maize variety development for stress-prone environ-
ments in southern Africa. In: Cleveland, D.A. and Soleri, D. (eds) Farmers, Scientists and Plant
Breeding. CAB International, Wallingford, UK, pp. 269–296.
Bellotti, A.C., Smith, L. and Lapointe, S.L. (1999) Recent advances in cassava pest management. Annual
Review of Entomology 44, 343–370.
Bentley, J.W. and Rodríguez, G. (2001) Honduran folk entomology. Anthropology Research 42, 285–301.
BioNET-International (2003) The Global Network for Taxonomy. Available at: http://www.bionet-
intl.org
Bongaarts, J. (2002) Demography. In: Sustainable Food Security for All by 2020. Proceedings of an International
Conference, 4–6 September, Bonn, Germany. IFPRI, Washington, DC, pp. 53–55.
Bruin, C.A. and Meerman, F. (2001) New Ways of Developing Agricultural Technologies: the Zanzibar
Experience with Participatory Integrated Pest Management. Wageningen University and Research
Centre/CTA, Wageningen, The Netherlands, 167 pp.
Brundtland, G.H. (1987) Our Common Future: World Commission on Environment and Development. Oxford
University Press, Oxford, UK, 383 pp.
Campanhola, C., de Moraes, G.J. and deSá, L.A.N. (1995) Review of IPM in South America. In: Mengech,
A.N., Saxena, K.N. and Gopalan, H.N.B. (eds) Integrated Pest Management in the Tropics: Current
Status and Future Prospects. John Wiley & Sons, New York, pp. 117–152.
Carpenter, J., Felsot, A., Goode, T., Hammig, M., Onstad, D. and Sankula, S. (2002) Comparative
Environmental Impacts of Biotechnology-derived and Traditional Soybean, Corn and Cotton Crops. Council
for Agricultural Science and Technology, Ames, Iowa, 189 pp.
CGIAR (2003) Consultative Group on International Agricultural Research: Who we are. Available at:
http://www.cgiar.org/who/index.html
Coakley, S.M., Scherm, H. and Chakraborty, S. (1999) Climate change and plant disease management.
Annual Review of Phytopathology 37, 399–426.
Conway, G. (1998) The Doubly Green Revolution: Food for All in the 21st Century. Cornell University Press,
Ithaca, New York , 335 pp.
CropLife (2003) CropLife International. Available at: http://www.croplife.org
Dabrowski, Z.T. (1997) Integrated Pest Management in Vegetables, Wheat and Cotton in the Sudan: a
Participatory Approach. ICIPE Science Press, Nairobi, 245 pp.
De Groote, H. (2002) Maize yield losses from stem borers in Kenya. Insect Science and its Application 22,
89–96.
Ekboir, J. (2002) CIMMYT 2000–2001 World Wheat Overview and Outlook: Developing No-till Packages for
Small-scale Farmers. CIMMYT, Mexico, DF, 65 pp.
Emana, G., Overholt, W.A., Kairu, E., MacOpiyo, L. and Zhou, G. (2002) Predicting the distribution of
Chilo partellus (Swinhoe) and its parasitoid Cotesia flavipes Cameron in Ethiopia using correlation,
step-wise regression and geographic information systems. Insect Science and its Application 22,
131–137.
FAOSTAT (2002) FAOSTAT Agricultural Data. Rome. Available at: http://apps.fao.org/page/
collections?subset=agriculture
Gallagher, K.D. (1992) IPM development in the Indonesian National IPM Programme. In: Aziz, A., Kadir,
S.A. and Barlow, H.S. (eds) Pest Management and the Environment in 2000. CAB International,
Wallingford, UK, pp. 82–89.
Geier, P.W. (1966) Management of insect pests. Annual Review of Entomology 11, 471–490.
Gitay, H., Suàrez, A., Watson, R.T. and Dokken, D.J. (2002) Climate Change and Biodiversity. IPPCC
Technical Paper V, Intergovernmental Panel on Climate Change, WMO, UNEP, Geneva,
Switzerland, 77 pp. Available at: http://www.ipcc.ch/pub/tpbiodiv.pdf
13IntpestManCh13.QXD 14/4/04 2:26 pm Page 310

310 D. Bergvinson

Gould, F. (1996) Deploying pesticidal engineered crops in developing countries. In: Persley, G.J. (ed.)
Biotechnology and Integrated Pest Management. Biotechnology in Agriculture Series No. 15, CAB
International, Wallingford, UK, pp. 264–293.
Guan Soon, L. (1996) Integrated pest management in developing countries. In: Persley, G.J. (ed.)
Biotechnology and Integrated Pest Management. Biotechnology in Agriculture Series No. 15, CAB
International, Wallingford, UK, pp. 61–75.
Heinrichs, E.A. (ed.) (1988) Plant Stress–Insect Interactions. John Wiley & Sons, New York, 492 pp.
Heinrichs, E.A., Aquino, G.B., Chelliah, S., Valencia, S.L. and Reissig, W.H. (1982) Resurgence of
Nilaparvata lugens (Stål) populations as influenced by method and timing of insecticide applications
in lowland rice. Environmental Entomology 11, 78–84.
Heong, K.L. and Escalada, M.M. (1997) Perception changes in rice pest management: a case study of
farmers’ evaluation of conflict information. Journal of Applied Communications 81, 3–17.
Heong, K.L., Escalada, M.M. and Mai, V. (1994) An analysis of insecticide use in rice: case studies in the
Philippines and Vietnam. International Journal of Pest Management 40, 173–178.
Herren, H.R., Neuenschwander, P., Hennessey, R.D. and Hammond, W.N.O. (1987) Introduction and dis-
persal of Epidinocarsis lopezi (Hom., Pseudococcidae), in Africa. Agriculture, Ecosystems and
Environment 19, 131–144.
Hilbeck, A., Baumgartner, M., Freid, P.M. and Bigler, F. (1998) Effects of Bacillus thuringiensis corn-fed prey on
mortality and development time of immature Chrysoperla carnae. Environmental Entomology 27, 480–487.
Huang, J., Rozelle, S., Pray, C. and Wang, Q. (2002) Plant biotechnology in China. Science 295, 674–677.
IPCC (2001) Climate Change 2001: Mitigation – Contribution of Working Group III to the Third Assessment
Report. Intergovernmental Panel on Climate Change, World Meteorological Organization, Geneva.
700 pp. Available at http://www.grida.no/climate/ipcc_tar/wg3/pdf/TAR-total.pdf
Irungu, R.W., Hodson, D. and Muchugu, E.I. (2003) Awhere-ACT: predicting pest outbreaks in Africa.
ICT Update, CTA, Issue 11. Available at: http://ictupdate.cta.int/index.php/article/
articleview/193/1/34/
Ishii-Eiteman, M., Hamburger, J. and Lee, C. (2002) Monitoring the World Bank’s Pest Management Policy, a
Guide for Communities. Pesticide Action Network North America, San Franscisco, California, 20
pp. Available at: http://www.panna.org/ resources/documents/monitoringWB.pdf
ISNAR (2003) International Service for National Agricultural Science. Available at:
http://www.isnar.cgiar.org/topics.htm
Jacobsen, B. (1996) USDA integrated pest management initiative. National IPM Network. Available at:
http://ipmworld.umn.edu/ chapters/jacobsen.htm
James, B., Neuenschwander, P., Markham, R.H., Anderson, P., Braun, A., Overholt, W., Khan, K.,
Makkouk, K. and Emechebe, A. (2003) Bridging the gap with the CGIAR Systemwide Program on
Integrated Management. In: Maredia, K., Dakouo, D. and Mota-Sanchez, D. (eds) Integrated Pest
Management in the Global Arena. CAB International, Wallingford, UK, pp. 419–434.
James, C. (2002) Global review of commercialized transgenic crops: 2001. Feature: Bt cotton. ISAAA
Briefs No. 26, Ithaca, New York. Available at: http://www.isaaa.org/publications/
briefs/Brief_26.htm
James, C. (2003a) Global status of commercialized transgenic crops: 2002. ISAAA Briefs No. 27,
International Service for the Acquisition of Agri-biotech Applications. Available at:
http://www.isaaa.org
James, C. (2003b) Global status of GM crops. ISAAA Global Status. International Service for the
Acquisition of Agri-biotech Applications. Available at: http://www.isaaa.org/kc/Bin/gstats/
index.htm
Jones, P.G. and Thornton, P.K. (2003) The potential impacts of climate change on maize production in
Africa and Latin America in 2055. Global Environmental Change 13, 51–59.
Kanampiu, F., Ransom, J., Gressel, J., Jewell, D., Friesen, D., Grimanelli, D. and Hoistington, D. (2002)
Appropriateness of biotechnology to African agriculture: Striga and maize as paradigms. Plant Cell,
Tissue and Organ Culture 69, 105–110.
Kates, R.W., Clark, W.C., Corell, R., Hall, J.M., Jaeger, C.C., Lowe, I., McCarthy, J.J., Schellnhuber, H.J.,
Bolin, B., Dickson, N.M., Faucheux, S., Gallopin, G.C., Grübler, A., Huntley, B., Jäger, J., Jodha, N.S.,
Kasperson, R.E., Mabogunje, A., Matson, P., Mooney, H., Moore, B. III, O’Riordan, T. and Svedlin, U.
(2001) Environment and development: sustainability science. Science 292, 641–642.
Khan, Z.R., Ampong-Nyarko, K., Chiliswa, P., Hassanali, A., Kimani, S., Lwande, W., Overholt, W.A.,
Pickett, J.P., Smart, L.E., Wadhams, L.J. and Woodcock, C.M. (1997) Intercropping increases para-
sitism of pests. Nature 388, 631–632.
13IntpestManCh13.QXD 14/4/04 2:26 pm Page 311

IPM in Developing Countries 311

Khan, Z.R., Pickett, J.A., Wadhams, L. and Muyekho, F. (2001) Habitat management strategies for the
control of cereal stemborers and striga in maize in Kenya. Insect Science and its Application 21,
375–380.
Khush, G.S. and Brar, D.S. (1991) Genetics of resistance to insects in crop plants. Advances in Agronomy 45,
223–274.
Kotler, P. and Zaltman, G. (1971) Social marketing: strategies for changing public behavior. Journal of
Marketing 35, 3–12.
Koul, O. (1996) Neem research and development: present and future scenario. In: Handa, S.S. and Koul,
M.K. (eds) Supplement to Cultivation and Utilization of Medicinal Plants. PID, CSIR, New Delhi,
pp. 583–611.
Landis, D.A., Wratten, S.D. and Gurr, G.M. (2000) Habitat management to conserve natural enemies
of arthropod pests in agriculture. Annual Review of Entomology 45, 175–201.
Litsinger, J.A. (1989) Second generation insect pest problems on high yielding rices. Tropical Pest
Management 35, 235–242.
Losey, J., Raynor, L. and Carter, M.E. (1999) Transgenic pollen harms monarch larvae. Nature 399, 214.
Matteson, P.C. (2000) Insect pest management in tropical Asian irrigated rice. Annual Review of
Entomology 45, 549–574.
Matteson, P.C., Altieri, A. and Gagne, W.C. (1984) Modification of small farmer practices for better pest
management. Annual Review of Entomology 29, 383–402.
Meerman, F., van de Ven, G.W.J., van Keulen, H. and Breman, H. (1996) Integrated crop management: an
approach to sustainable agricultural development. International Journal of Pest Management 42, 13–24.
Mengech, A.N., Saxena, K.N. and Gopalan, H.N.B. (1995) Integrated Pest Management in the Tropics:
Current Status and Future Prospects. John Wiley & Sons, New York, 171 pp.
Morin, S., Biggs, R.W., Sisterson, M.S., Shriver, L., Ellers-Kirk, C., Higginson, D., Holley, D., Gahan, L.J.,
Heckel, D.G., Carriere, Y., Dennehy, T.J., Brown, J.K. and Tabashnik, B.E. (2003) Three cadherin alle-
les associated with resistance to Bacillus thuringiensis in pink bollworm. Proceedings of the National
Academy of Science 100, 5004–5009.
Morse, S. and Buhler, W. (1997) Integrated Pest Management: Ideals and Realities in Developing Countries.
Lynne Rienner, Boulder, Colorado, 171 pp.
Mugo, S., Bergvinson, D. and Hoisington, D. (2001) Options in developing stemborer-resistant maize:
CIMMYT’s approaches and experiences. Insect Science and its Application 21, 409–415.
Mulaa, M., Bergvinson, D. and Mugo, S. (2001) IRMA researchers work to develop insect resistance
management strategies. IRMA Updates 2(1), 3. Available at: http://www.cimmyt.org/ABC/
investin-insectresist/pdf/IRMA_2&1.pdf
Neuenschwander, P. (1993) Human interactions in classical biological control of cassava and mango
mealybugs on subsistence farms in tropical Africa. In: Altieri, M.A. (ed.) Crop Protection Strategies for
Subsistence Farmers. Westview Press, Boulder, Colorado, 197 pp.
Neuenschwander, P., Hammond, W.N.O., Ajuonu, O., Gado, A., Echendu, N., Bokonon-Ganta, A.H.,
Allomasso, R. and Okon, I. (1990) Biological control of the cassava mealybug, Phenacoccus manihoti
(Hom., Pseudococcidae) by Epidinocarsis lopezi (Hym., Encyrtidae) in West Africa, as influenced by
climate and soil. Agriculture, Ecosystems and Environment 32, 39–55.
Nkunika, P.O. (2002) Smallholder farmers’ integration of indigenous technical knowledge (ITK) in maize
IPM: a case study in Zambia. Insect Science and its Application 22, 235–240.
Panda, N. and Khush, G.S. (1995) Host-plant Resistance to Insects. CAB International, Wallingford, UK,
431 pp.
Pingali, P.L. (2001) Environmental consequences of agricultural commercialization in Asia. Environmental
and Development Economics 6, 483–502.
Pingali, P.L., Hossain, M. and Gerpacio, R.V. (1997) Asian Rice Bowls: the Returning Crisis? CAB
International, Wallingford, UK, 341 pp.
Pinstrup-Andersen, P. (2002) Food and agricultural policy for a globalizing world: preparing for the
future. American Journal of Agricultural Economics 84, 1201–1214.
Qaim, M. and Zilberman, D. (2003) Yield effects of genetically modified crops in developing countries.
Science 299, 900–902.
Rosegrant, M.W., Paisner, M.S., Meijer, S. and Witcover, J. (2001) Global Food Projections to 2020: Emerging
Trends and Alternative Futures. IFPRI, Washington, DC, 206 pp. Available at:
http://www.ifpri.org/pubs/ books/gfp/gfp.pdf
13IntpestManCh13.QXD 14/4/04 2:26 pm Page 312

312 D. Bergvinson

Schmutterer, H. (1995) The Neem Tree: Source of Unique Natural Products for Integrated Pest Management,
Medicine, Industry and Other Purposes. VCH Publishers, New York, 696 pp.
Schumacher, E.F. (1975) Small is Beautiful: Economics as if People Mattered. Harper and Row, New York,
305 pp.
Sears, M.K., Hellmich, R.L., Stanley-Horn, D.E., Oberhauser, K.S., Pleasants, J.M., Mattila, H.R., Siegfried,
B.D. and Dively, G.P. (2001) Impact of Bt corn pollen on monarch butterfly populations: a risk
assessment. Proceedings of the National Academy of Science 98, 11937–11942.
Shelton, A.M., Zhao, J.-Z. and Roush, R.T. (2002) Economic, ecological, food safety and social conse-
quences of the deployment of Bt transgenic plants. Annual Review of Entomology 47, 845–881.
Simmonds, N.W. (1976) Evolution of Crop Plants, 1st edn. Longman, New York, 339 pp.
Smith, C.M. (1999) Plant resistance to insects. In: Rechcigl, J. and Rechcigl, N. (eds) Biological and
Biotechnological Control of Insects. Lewis Publishers, Boca Raton, Florida, pp. 171–205.
Songa, J. (2002) Study compares effect of Bt biopesticide and conventional insecticides on nontarget
arthropods. IRMA Updates 3(3), 5–6. Available at: http://www.cimmyt.org/ABC/InvestIn-
InsectResist/pdf/IRMA_ 3&3.pdf
Songa, J., Bergvinson, D.J. and Mugo, S (2002) A reference collection for non-target arthropods of Bt
maize in Kenya. IRMA Updates 4(3), 8. Available at: http://www.cimmyt.org/ABC/ InvestIn-
InsectResist/pdf/IRMA_3_I4.pdf
Srivastava, S.K. (2000) Effect of farm practices on natural resources and strategy of transfer of ecofriendly
technologies. In: International Conference on Managing Natural Resources for Sustainable Agricultural
Production in the 21st Century, 14–18 February. Indian Society of Soil Science, New Delhi,
pp. 1134–1135.
TACTRI (2002) Taiwan Agricultural Chemicals and Toxic Substances Research Institute, Council of
Agriculture. Available at: http://www.tactri.gov.tw
Teng, P.S. (1994) Integrated pest management in rice. Experimental Agriculture 30, 115–137.
Wambugu, F. (1999) Why Africa needs agricultural biotech. Nature 400, 15–16.
Wattiez, C., Scheuer, S. and Iwasaki-Riss, J. (2003) European Parliament passes a resolution calling for a
reduction in pesticide use. Available at: http://www.icmfocus.com/inbrief.asp?Section=
Display&NewsID=34
Weinzierl, R.A. (1999) Botanical insecticides, soaps and oils. In: Recheigl, J.E. and Recheigl, N.A. (eds)
Biological and Biotechnological Control of Insect Pests. Agriculture and Environment Series, CRC Press,
Boca Raton, Florida, pp 101–121.
Willcox, M.C., Khairallah, M.M., Bergvinson, D., Crossa, J., Deutsch, J.A., Edmeades, G.O., Gonzalez-de-
Leon, D., Jiang, C., Jewell, D.C., Mihm, J.A., Williams, W.P. and Hoisington, D. (2002) Selection for
resistance to southwestern corn borer using marker-assisted selection and conventional backcross-
ing. Crop Science 42, 1516–1528.
World Bank (1992) Agricultural Pest Management. Operational Directive 4.03, World Bank, Washington,
DC, 5 pp.
World Bank (1998) Operational Policy 4.09. World Bank, Washington, DC, 2 pp. Available at:
http://wbln0018.worldbank.org/Institutional/Manuals/OpManual.nsf/bytype/665DA6CA847982
168525672C007D07A3?OpenDocument
Yencho, G.C., Cohen, M.B. and Byrne, P.F. (2000) Applications of tagging and mapping insect resistance
loci in plants. Annual Review of Entomology 45, 393–422.
Zethner, O. (1995) Practice of integrated pest management in tropical and sub-tropical Africa: an
overview of two decades. In: Mengech, A.N., Saxena, K.N. and Gopalan, H.N.B. (eds) Integrated Pest
Management in the Tropics: Current Status and Future Prospects. John Wiley & Sons, New York,
pp. 1–67.
Zhao, J.Z., Rui, C.H., Lu, M.G., Fan, X.L., Ru, L.J. and Meng, X.Q. (2000) Monitoring and managing of
Helicoverpa armigera resistance to transgenic Bt cotton in Northern China. Research on Pest Management
Newsletter 11, 28–31.
14Integrated pest index 5/5/04 2:20 pm Page 313

Index

Abies balsamea 214 Agroforestry 302

Abiotic–biotic interactions 302 Agromyzids 191
Acacia saligna 239 Agrotis ipsilon 27
Acacia sp. 239 Agrotis obscurus 194
Acantholyda erythrocephala 208 Agrotis segetum 89, 91
Acaricides 173, 274 Agrotis spp. 28
Acephate 217, 225 Alarm pheromone 191
Acer macrophyllum 236, 239 Alcohols 91–96, 110
Acer rubrum 236 Aldehydes 91, 92, 95, 96
Acer spicatum 236 Aldicarb 173, 177
Acer spp. 240 Aldrin 4
Acetates 91–96, 110 Alkanes 188
Acleris gloverana 209, 218 Alkyl thiocyanates 2
Acleris variana 209 Allele 195, 198
Active 171 Allelochemicals 58–60, 64, 65, 73, 74
ingredients 171 non-volatile 157
toxins 125
plant defences 158
Acute toxicity 126, 130
volatile 157
Acyrthosiphon pisum 273
Allelopathic plant 237
Additive interactions 137
Allene oxide synthase 158, 159
Adelges piceae 208
Allethrin 4
Aerosols 99, 100, 102, 106
Alnus incana 236
delivery system 101, 103, 105
emitting devices 99 Alnus rubra 236, 239, 240
Aeschynomene virginica 272 Alomones 73, 74, 191
Aggregation pheromones 188, 189, 191, 235, 236 Alternaria solani 174
Agricultural 2, 7, 302 Alternative crops 23
losses 302 Alternative hosts 23, 28
pest 2 Amaranthus sp. 59
Agrobacterium 148 Amber-marked birch leaf-miner 208
Agrobacterium radiobactor 272 Ambrosia beetles 81, 82
Agrobacterium tumefacians 272 American bollworm 25
Agrochemical 4, 86, 255, 261, 265, 275, 289, 294, 298 Amino acid motifs 156
Agroecosystem 9, 11, 16, 21, 22, 24, 31, 33, 39, 40, Aminocarb 217
55, 56, 60, 61, 64, 65, 124, 129, 133–136, 139, Aminohydroxy-phospho-vinyl-butyryl-alanine
149, 281, 284–286, 288, 294, 297, 307 237

313
14Integrated pest index 5/5/04 2:20 pm Page 314

314 Index

Amplified fragment length polymorphism (AFLP) Augmentation 59, 271

markers 154 Augmentative inoculation 238
-Amylase inhibitors 126, 149 Augmentative releases 227
Anagrus epos 61 Autodissemination 81, 84
Analogy model 43 Avermectins 273
Analytic models 44 Avoidance 22, 23
Anemotactic response 187 allele 199
Anemotaxis 189 Azadirachta indica 63, 287
Annual crops 22, 34, 76 Azadirachtin 63, 192, 287
Antagonistic 56 Azinphos-methyl 77, 171, 173, 176
effects 26 Azoxystrobin 273
Antennal swabbing 188
Anthonomus grandis grandis 124
Antibiosis 64, 74, 127, 152, 153, 195–197, 199 Bacillus fusca 289
factors 185 Bacillus lentimorbus 3
traits 199 Bacillus popilliae 3
Antibiotic effects 133 Bacillus thuringiensis (Bt) 3, 58, 64, 125, 129, 138,
Antibodies 269 147–150, 160, 161, 172, 173, 226, 227, 269,
Anticarsia gemmatalis 173 270, 275, 293–295
Antithesis 175 aizawai 58
Antixenosis 128, 152, 189 cotton 4, 134, 136–138, 150, 294, 295, 305
Ants 175 crops 149, 151, 152, 160, 294–296
Apanteles flavipes 297, 304 cultivars 139, 160
Apanteles fumiferanae 220 endotoxin 133
Apanteles melanoscelus 229 integrated risk-management programmes
Aphid 30, 57, 59, 61, 63, 156, 172, 173, 177, 185, 151
187, 192, 205 kurstaki (Btk) 58, 123, 206, 207, 208, 210, 211,
Aphidius matricariae 63 213, 214, 218–220, 225, 227, 229–231, 233
Aphidius rhopalosiphi 57 maize 134, 149–152, 294, 295, 303
Aphis gossypii 29, 155, 173 potatoes 150
Apoanagyrus lopezi 292 resistance 216
Apparency theory 127 management 140
Apple-bud moth 79, 110 toxins 64, 123, 125, 126, 137–140
Apple maggot 76, 84 semi-activated 125
fly 81 transgenes 160
Aquatic insects 217 transgenic cotton 137
Arabidopsis thaliana 155–159 cultivar 129, 136, 137
Argyrotaenia pulchellana 79 potato 134
Argyrotaenia sphaleropa 291 virulence 152
Argyrotaenia velutinana 89, 90, 101, 103–105 Bacteria 1, 2, 190, 238, 271, 295
Armillaria 240 Bacterial 31, 214
Armillaria mellea 229 artificial chromosome 156
Armillaria ostoyal 240, 241 contaminants 268
Armyworm 27, 32 genes 125
Arthropods 24, 25, 31, 56, 61, 73, 147, 169, 171–173, infection 63
175–177, 271, 274 insecticide 214
colonization 135 pathogens 31, 58
diversity 288 Bactericide 296
faunas 134 Bactocera oleae 83, 190
pests 21, 24, 34, 147 Baculoviridae 211
resistance 148 Baculovirus 84, 124
resistant cultivars 155 Baits 177, 194
species 274 Balsam fir 214, 216
Artificial pest control 267 sawfly 210, 212
Asimina spp. 57 twig aphid 209
Attractant 75, 77–84, 177, 189–191, 193, 197–199 woolly adelgid 208
Attracticide 194, 196–199 Banana weevil 27, 291
14Integrated pest index 5/5/04 2:20 pm Page 315

Index 315

Barbarea vulgaris 61 Biological herbicides 238

Bark beetles 82, 189, 205, 234 Biological insecticides 217, 225, 232
Bark-boring caterpillars 291 Biological organisms 39, 47
Bean leaf beetle 30, 33, 35 Biological pesticides 205
Beauveria bassiana 58, 63, 174 Biological processes 42
Beet armyworm 58, 81, 136, 158, 159 Biological traits 86
Beet leafhopper 30 Bionomics 22
Beet pests 60 Biopesticide 178, 227, 303
Beetle banks 272 Biophysical gene products 160
Beetles 33, 35, 172, 174, 187, 189, 191, 194, 235, 236 Biorational method 63
Behavioural avoidance 197–199 Biotypes 151, 268, 271, 275, 277, 288, 297
allele 196 virulent 160
allele frequency 195 Birch leaf-miner 208
Behavioural control 112 Bird cherry oat aphid 159
Behavioural trait 195, 196, 198 2, 2-bis (p-chlorophenyl)-1, 1, 1-trichloroethane 4
Behaviour-modifying chemicals 39, 103, 111 Black cutworms 27
Bemisia argentifolii 159, 276 Black swallowtail 149
Beneficial arthropods 33, 149 Black vine-weevil 190, 193
Beneficial insects 24, 28, 32, 34, 270–272, 288 Blissus inularis 175
Beneficial microorganisms 267 Blissus leucopterus 175
Beneficial organisms 299 Blueberry maggot fly 81
Beneficial predators 33 Bollgard® 270
Beneficial species 33, 271–273 Boll-weevil 25, 30, 124, 171, 192
Benomyl 173, 274 Bollworm 3, 30, 60, 136, 150
Benzenehexachloride 34, 235 complex 171
Benzimidazoles 274 Bombycal 92
Betula spp. 240 Botanical 10
Bialophos 237 extracts 63
Bifenzate 176 insecticides 2, 3
Biochemical gene products 160 pesticides 2, 3, 287
Biochemicals 178 Bracon hebetor 173
Biocides 2 Braconid parasitoid 60, 64
Biocontrol 212, 213, 220, 270 Brassica kaber 61
agents 171, 172, 175, 176, 207, 239 Brassica oleracea var. capitata 58
programmes 208 Brevicoryne brassicae 57, 63
Biodiversity 31, 220, 258, 286, 292, 302, 304, 306, Broad-leaved weeds 34, 176
307 Broad-spectrum chemicals 218
Biofix 76 Broad-spectrum herbicides 296
Bioherbicidal agents 272 Broad-spectrum insecticides 216
Bioherbicides 238–240, 272 Broad-spectrum pesticides 307
Bioinsecticides 218 Brown planthopper 5, 16, 151, 154, 156, 289, 291,
Biointensive crop protection 26 292
Biointensive IPM 25, 170 Brown-tail moth 208, 233
Biointensive pest control system 26 Bruce spanworm 209
Biointensive systems 25 Bucculatrix thurberiella 136
Biological activity 31, 287 Bud-blight virus 30
Biological agents 206 Budworm 213–215, 217
Biological control 2–4, 8, 9, 22, 24, 26, 27, 31, Budworm parasitoids 220
33–35, 39, 55–57, 59–61, 64–66, 84, 109, Buprofezin 276
123, 125–130, 133, 134, 136–140, 169–176, Busseola fusca 32, 287
178, 179, 207, 209, 213, 215, 225, 227, 229, Butyl hexanoate 84
233, 238, 239, 258, 259, 266, 271, 272, 284,
286–288, 291, 292, 294, 295, 301, 303, 304,
307 Cabbage aphid 63
agents 2, 171, 174, 175, 177, 194, 211, 213–215, Cabbage looper 136
223, 286, 297, 301, 302, 304, 306 Cabbage maggots 193
Biological diversity 24, 258, 292 Cabbage white butterfly 62
14Integrated pest index 5/5/04 2:20 pm Page 316

316 Index

Cabbage worm 159 Choristoneura diversana 215

Cadherin alleles 295 Choristoneura fumiferana 76, 107, 209, 211–214, 216
Calamagrostis canadensis 236, 240 Choristoneura murinana 215
Calcium arsenate 171, 215 Choristoneura occidentalis 172, 209, 212–215
Callosobruchus subinnotatus 192 Choristoneura pinus 213
Campoletis sonorensis 133, 134 Choristoneura pinus pinus 209, 212, 214
Campylomma verbasci 76 Choristoneura rosaceana 89, 90, 103–106, 108
Capsaicin 192, 193 Choristoneura spp. 213
Captan 274 Chronic effects 126
Carbamate 3, 4, 78, 172, 173, 177, 217 Chronic secondary pest 135
Carbaryl 173, 225, 235 Chrysanthemum 23, 287
Carbofuran 173, 177 Chrysoperla 177
Carbohydrate binding proteins 149 Chrysoperla carnea 295
Cardiochiles nigriceps 59 Chrysoperla rufilabris 172
Carduus nutans 175 Chrysopidae 63
Caricature model 43 Chrysopids 177
-Carotene 139 Chymotrypsin inhibitors 149
Carpophilus beetles 81 Cicadulina mbila 30
Carrot flies 32 Cigarette beetle 81
Carulaspis juniperi 208 Cinnamaldehyde 187, 193
Cassava 284, 288, 291, 303, 304 Cinnamyl compounds 191
crop 4 Cinnibar moth 172, 173
mealy bug 4, 291, 292 Classical biological control 206, 207, 211, 227, 239,
Cecidomyiidae 63, 191 271, 288, 291, 292, 297, 304, 306, 308
Cellulase 176 Classification based sequential sampling models
Central nervous system 81, 88, 105, 106 50
Cephus cinctus 26, 27, 34 Cnaphalocrocis medinalis 285
Cereal cyst nematode 155 Coccinellidae 63
Cereal leaf beetle 27 Coccinellid 173, 177
Cerotoma trifurcata 33 Codlemone 77, 97, 110
Chaetanaphothrips orchidii 291 Codling moth 8, 26, 29, 76–81, 85, 86, 92, 94, 95,
Chemicals 15, 169, 170, 172, 175, 178, 179, 193, 232 100, 103, 104, 108, 110, 124, 177, 194
contamination 268 Coffea spp. 288, 303
control 2, 3, 5, 6, 8, 26, 55, 64, 74, 112, 124, Coleophora laricella 208
169, 175, 225, 274, 291, 303 Coleophora serratella 208
cues 132, 191 Coleoptera 27, 149, 172, 187, 293
defences 127, 139, 159 Coleotechnites starki 209
deterrents 193 Cole-wort 58, 62
herbicide 240, 272, 275 Colletotrichum gloeosporioides aeschynomene 272
insecticides 215, 217–221, 225, 227, 232, 234, Colonizing aphids 28
235, 271, 272 Colorado potato beetle 33, 150, 158, 174, 187, 190,
pesticides 14, 22, 25, 266, 267, 272–276 274
toxicants 274 Commercial herbicides 238
Chemointensive crop protection 26 Computer modelling 43, 48
Chemointensive pest control systems 26 Conidia 84, 288
Chemokinetic response 187 Conifer bark beetle 82
Cherry fruit fly 192 Conifers 78, 223, 224, 234, 238, 240
Chewing insects 57, 157 Conjugated diene system 97
Chilo partellus 193, 287, 289, 297 Conotrachelus nenuphar 26
Chilo suppressalis 27, 30 Conservation 271
Chinch bug complex 175 biological control 272
Chinese tortrix 81, 82 Constitutive defences 157
Chitinases 158 Consummatory behaviours 186, 190, 193
Chlordane 4 Conventional 110
Chlorothalonil 174 farming 175
Chlorsulphuron 275 gene expression 151
Chondrostereum purpureum 239, 240 insecticides 10, 63, 64, 135, 174, 196, 197
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Index 317

pest control 110 2, 4-D 238

pesticides 151, 160, 178, 193, 261 Damaging insects 2
phenotypic selection 155 Danaus plexippus 149, 294
resistance 152 Dectes texanus 27
Copidosoma floridanum 57 Defence response genes 148
Corn borers 25 Defensin peptide 158, 159
Corylus cornuta 236 Defoliating forest pests 223
Cosmopoletes sordidus 27, 291 Defoliating insect 211, 218
Cotesia marginiventris 132 Defoliator 213, 215, 216
Cotesia plutella 64, 131 control 218, 220
Cotesia sesamiae 32, 287 management 215
Cotton aphid 29, 173 Delia radicum 192
Cotton bollworm 25, 27, 29, 269, 270, 275, 276, Dendritic membranes 87
294 Dendroctonus ponderosae 83, 234, 235
Cotton cushion scale 2, 3 Dendroctonus pseudotsugae 234
Cotton fleahopper 29 Dendroctonus rufipennis 209, 234
Cotton leaf perforator 136 Desmodium 287, 295
Cover crops 23, 33, 34 Desmodium intortum 287
Cranberry bugs 99 Desmodium uncinatum 287
Critical control points 151 Deterministic model 44, 45
Crop diversification 23 Deterrents 73, 83, 186–193, 198, 199
Crop diversity 32, 306 DFTM virus 213, 221–223
Crop ecology 22 Diabrotica longicornis 31
Diabrotica spp. 21, 28, 32, 124, 191
Crop growth models 49
Diabrotica undecimpunctata 34
Crop injury 185
Diabrotica virgifera 31, 152
Crop-loss models 49
Diadegma insularis 62
Crop management 22, 25, 124, 129, 139, 152, 283,
Diadegma semiclausum 63
284, 290, 298, 301, 306
Diaeretiella rapae 60
Crop pests 2, 56, 66
Diamond-back moth 29, 58, 61–63, 84, 193, 291
Crop protection 8–10, 14
Diapause 31
Crop resistance 126
Diaphania hyalinata 60
Crop rotation 2, 22–24, 28, 30, 31, 275, 304
Diatraea grandiosella 29, 155
Cropping systems 21, 22, 24, 35
Diatraea saccharalis 131, 304
Crown gall 272 Diazinon 173
CryIA(b) protein 150 Dichlorodiphenyltrichloroethane (DDT) 3, 4, 176,
CryIAb toxin 295 215, 217, 225, 232
CryIAc 294 Dieldrin 4
Cry toxins 149, 151 Diflubenzuron 225
Cryptophlebia leucotreta 26 Digestibility reducers 127, 128
Cucumber beetle 190 DIMBOA 127
Cucumber mosaic virus 269 Dimethoate 83, 295
Cucurbitacins 190 Dimilin® 225, 226, 230–232
Cultural control 2, 9, 14, 21–24, 26, 34, 35, 39, 65, -Dioxygenase 158, 159
66, 170, 172, 175, 270, 272, 297 gene 157
Cultural method 74, 112, 304 Diprion similis 208
Cultural practice 2, 8, 21, 25, 29, 194 Diptera 57, 187, 293
Curly-top virus 30 Diseases 1, 7, 17, 25, 172, 195
Cutworms 28, 34 control 24, 275
Cydia molesta 89 fungal 28, 174
Cydia pomonella 8, 29, 101, 104, 124, 177 resistance 155, 156, 271
Cydia strobiella 209 resistant plants 301
Cydia trasias 82 resistant rice 304
Cylindrobasidium laeve 239 Disparlure 229–231
Cypermethrin 172 Disparvirus 226
Cyrtorhinus lividipennis 177 Dispersing pheromone 101
Cytisus scoparius 240 Dithiocarbamate 274
Cytoplasmic polyhedroviruses 211 Ditrophic interactions 64
14Integrated pest index 5/5/04 2:20 pm Page 318

318 Index

Diuraphis noxia 41, 42, 44, 45, 47, 155, 156 -Endotoxin 3, 125, 148
Diversified cropping systems 292 Endotoxins 58, 270, 275
Diversionary crop 195, 196, 198, 199 Engraver beetles 191
cDNA 160 Entomopathogens 84, 205, 217
library techniques 159 fungal 173
Douglas fir beetle 234 microorganisms 227
Douglas fir tussock moth 47, 205, 210, 212, 220 virus 218
Drosicha stebbingi 291 Entomophaga maimaiga 227–229
Dryocoetes confuses 234 Entomophagous insects 267
Dust formulation 177 Entomophthorales 228
Dylox® 225, 226, 230 Entomopox virus 211
Dynamic models 46, 47, 51 Environment 3–5, 9, 10, 178
degradation 256
Environmental Protection Agency 169
2, 4-E 238 incentives 176
EAG 89, 90, 98 Enzyme inhibitors 125–127, 130, 138
Earias insulana 27 Enzyme linked immunosorbent assay (ELISA) 269
Early blight 174 Enzymes 154, 158, 269, 275
Eastern black-headed budworm 209 Eoreuma loftini 131
Eastern hemlock looper 209, 215, 216 Ephemeral crops 129
Eastern spruce beetle 209, 211 Ephestia kuhniella 82
Eastern spruce budworm 218, 220 Epidinocarsis lopezi 291
Eco-apples 257 Epilachna varivestis 33, 60
Epilobium angustifolium 236
Eco-labels 256, 258, 259, 262
Epilobium spp. 240
Ecology 8
Epiphyas postvittana 98
Economically damaging level 299
Epizootic 173, 213, 215, 220, 222, 228
Economic control 22
fungal 229
Economic damage 10, 206
EPV 212, 213, 215
Economic injury 9, 10, 124, 170
Eradication 207, 211, 224–226, 229, 231–234
level models 49
Eriophyes tosichella 28
levels 3, 9, 24, 25, 124, 137, 266, 267, 286
Erosion 34, 265, 303
Economic losses 170, 171
Erwinia amylovora 272
Economic thresholds 3, 8, 11, 48–50, 62, 137, 185,
Erwinia carotovora 190
266, 267, 273, 274, 276, 277, 282 Erwinia tracheiphila 190
Ecosystem 24, 51, 302, 307 Erythroneura elegantula 61
Egg-laying behaviour 193 Essential oils 192
Egg parasite 61 Estigmene acrea 136
Egg parasitoids 215, 233 Ethion 172
Eichhornia crassipes 174 Ethyl-(2E,4Z)-2, 4-decadienoate 80
Elasmopalpus lignosellus 269 Ethylene dibromide 234, 235
Elcar 3 Ethylene vinyl acetate 193
Eleusine coracan 288, 303 Eugenol 178
Elicitors 132 Eukaryotic DNA 154
Elm-leaf beetle 208 Eulecanium tiliae 208
Emamectin benzoate 273 Eulophid parasitoid 60
Empoasca fabae 30 Eulophus pennicornis 130
Empoasca spp. 32 Euproctis chrysorrhoea 208, 233
Emulsifiable concentrates 177 Eurasian forest defoliator 223
Emulsion 177 European corn borer 27, 30, 78, 134, 136, 150, 152
Encapsulation 177 European grapevine moth 97
Encarsia formosa 63 European gypsy moth 225, 234
Encyrtid 57 European pine sawfly 208, 212
parasitoid 63 European pine-shoot moth 208
Encyrtidae 292 European spruce sawfly 208, 211, 212
Endemic 221, 238 Exoteleia pinifoliella 209
levels 227, 235 Exotic forest insects 205–207, 208
Endopiza viteana 27 Exotic mites 239
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Index 319

Exotic parasitoids 215, 227 Genetically engineered 25

Exotic pest 75, 301 cultivars 262
Exotic weeds 239 plant resistance 25
Expressed sequence tag (EST) 148 plants 287
Genetically modified 149, 269
crops 150, 269, 293
Fall armyworm 59, 132, 136 organisms 149
False codling moth 26 plants 268
FAO 4–7, 9 strains 268
Fatty acid peroxidases 158 Genetic crop diversity 288
Feeding deterrent 192 Genetic diversity 139, 282, 287
Fenitrothion 212, 217–219 Genetic engineering 64, 205, 308
Fenusa pusilla 208 Genetic models 195
Ferulic acid 159 Genomic DNA 154
Fire blight 272 Genotype 153, 154, 195, 196–198
Flies 76, 83, 84, 172, 188 Geocoris spp. 177
Fluorophores 269 Geographical information systems (GIS) 295, 297,
Flying beetles 235 302
Flying insects 187 Gibberella zeae 155
Foliage-feeding insects 3, 29 Gilpinia fruteforum 205
Forecasting models 43 Gilpinia hercyniae 208, 211, 212
Forest beetles 82, 83 -Glucosidase 158, 159
Forest defoliator 211, 214, 218, 219 lytic enzyme 159
Forest ecosystem 205 protein 158
Forest insect control 211 Glycine max 288
Forest insects 205, 206, 207, 209, 211 Glyphosate 176, 238, 240, 271, 296
pest 212, 213 Glypta fumiferanae 220
Forest tent caterpillar 210, 212, 216 Gorse mite 239
Forest weeds 205 Gossypium barbadense 288, 303
Fragaria chiloensis 193 Gossypium hirsutum 288, 303
Frankliniella occidentalis 58 Granular formulations 177
Fruit flies 26, 83, 177 Granuloviruses 211–213, 215, 218
Fumigant 234 Grape berry moth 27, 85, 95
Fumigation 175 Grape phylloxera 2, 3, 27
Fungal contaminants 268 Grapholita molesta 79, 104
Fungal infection 173, 228 Grasshoppers 47, 48
Fungal pathogens 31, 84, 173, 174, 228, 269 Greater peach-tree borer 107, 110
Fungi 1, 2, 84, 214, 238, 271 Green bug 27, 156
Fungicides 173, 174, 273–275, 296 resistance gene 156
strobilurin 273 Green lacewings 3
Fungistatic compounds 270 Green leafhopper 292
Fungus 173, 227–229 Green lice leafhopper 156
Furanocoumarins 57 Green model 193
Fusarium graminearum 155 Green peach aphid 159
Fusarium head blight 155 Greenhouse whitefly 58
Growth regulators 3, 192
Gypchek 226–228, 230, 231
Galanthus nivalis 130 Gyplure 230, 231
Galerucella spp. 174 Gypsy moth 58, 63, 95, 172, 187, 205–208, 210–212,
Gall 57 216, 223–233
-forming rust 239 NPV 227
midge 151, 177, 292 virus 231
Gaultheria shallon 236, 239
GE crops 289, 293–296, 303, 304, 306, 307
Gene 159 Habitat management 25, 51, 272, 273, 286, 287, 307
flow 293 Haploid gametes 196
frequency 197–199 Hardy–Weinberg equilibrium 196
14Integrated pest index 5/5/04 2:20 pm Page 320

320 Index

Hazard analysis critical control point (HACCP) Hymenoptera 129, 272, 292
151 Hymenopteran 177
Head weevil 175 parasites 273
Helicoverpa 124 parasitoids 177
NPV 3 Hypera postica 30, 270
Helicoverpa armigera 178, 294 Hyperparasitoid 55
Helicoverpa zea 27, 58, 78, 133, 134, 171, 269
Heliothis 124, 137
Heliothis virescens 59, 89, 91, 133, 134, 150, 171, 194, Icerya purchasi 2
269, 270, 274 Ichneumonid parasitoid 62
Heliothis zea 27, 29, 30, 59, 270 Ichneumonid wasp 206
Hemiptera 293 Imazapyr 303
Hemlock looper 228 Imidacloprid 127, 173, 273, 274, 276
Hemlock sawfly 209 Indigenous 284, 285
Heptachlor 4 biological control 292
Herbicides 173–176, 235, 237, 270, 271, 273, 296, IPM 306
304 natural enemies 238
resistance 275, 303, 305 Induced crop plant resistance 160
gene 293 Induced defences 157
resistant maize 303 Induced resistance 159
soybean 296, 304 Ingard® 270, 276
tolerance trait 271 Injury level models 49
Herbivore 29, 32, 55–57, 59, 60, 62–64, 127–129, Inonotus tomentosus 240, 241
131, 132, 139, 140, 159, 190, 191, 193 Insect 73, 195
colonization 127 behaviour 73, 185, 187, 188, 190, 195
density 58 biodiversity 293, 294, 295
prey 295 cadavers 228
specific elicitors 159 chemical ecology 185
Herbivorous 61, 62 control 3, 8, 206, 215, 219, 297
arthropods 61 cuticle 95
insects 185 density 221
mites 62 enemies 239
pests 135 growth regulators 76, 78, 276
Hessian flies 3, 28, 30, 147, 151, 191, 193 herbivores 190
Heterodera avenae 155 management 217
Heteroptera 64, 172 parasites 233
resistance 156 pest 2, 3, 7, 8, 22, 26, 33, 34, 57, 58, 63, 75, 78,
Hevea brasiliensis 288, 304 99, 110, 123, 126, 128, 150, 173, 185, 194,
Hevein-like protein 158, 159 206, 216, 218, 223, 266, 267, 270, 275, 276,
Hexachlorocyclohexane (HCH) 3, 4 294, 295, 297, 302
Hexanol 92 protected cultivars 270, 273–275
Hexazinone 238 resistance 3, 271
Hexenal, 3-hexenal 158 management 151, 152, 295, 296, 304
Hippodamia convergens 134, 172 resistant cultivars 123, 126, 139, 147, 148,
Holism model 43 153–161, 287, 292, 293, 303
Holometabolus insects 185 resistant QTLs 155
Homoeosoma electellum 60 sex attractant 99
Homoptera 126, 293 vectors 128
Hordeum vulgare 288 virulence management 168
Host-marking pheromone 192 viruses 205, 206, 211, 213
Host–parasitoid systems 63 Insecticidal 287
Host-plant resistance 25, 39, 55, 56, 63, 65, 139, activity 3, 125, 174
170, 172, 175, 287, 292, 293, 299, 303, 304 control 33, 111, 137
Hover fly 57, 61, 63 crop 199
Hydroperoxidase lyase 158 crystal 149
Hydrophyllaceae 61 protein 125
Hydroxamic acids 158, 159 cultivars 123
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Index 321

effects 136 Kaolin 192, 193

plants 149 -based plant protectants 192
products 233 Key pest 74, 140, 176, 255, 274
proteins 131, 148
residues 147, 286
resistance 11, 74, 77, 185, 195 Lacanobia oleracea 130
spray 218 Lacewings 61
toxins 134, 136 larvae 295
trait 199 Ladybird beetle 3, 134
Insecticide 2–4, 7, 8, 24, 33, 35, 41, 42, 60, 63, 64, Lambdina fiscellaria fiscellaria 209, 228
73, 74, 76–78, 82–84, 86, 102–104, 108, 109, Lambdina fiscellaria somniaria 209
111, 123, 124, 128, 134–138, 147, 150, Larch case-bearer 208
169–171, 173, 174, 176, 185, 192, 194, 195, Larch sawfly 206, 208, 210
199, 215–217, 221, 231, 269, 270, 273, 276, Late blight 174
285, 286, 288, 291, 294, 295, 298 LdNPV 228, 229, 231, 232
bait system 197 Leaf 193
Insects 1, 8, 14, 16, 17, 23, 26, 27, 30, 57, 63, 64, beetles 32, 174
73–75, 78–80, 82, 83, 88, 89, 91, 123–127, -feeding 285
129, 139, 149, 151, 152, 155–161, 172–174, -folder 285
176, 185–193, 196, 198, 199, 205, 206, 207, -hoppers 26, 28, 30, 32
214, 216, 217, 219–221, 223, 224, 228–231, -miners 289
234, 238, 269–272, 275, 285, 287, 292, 295, -rollers 85, 92, 95, 102, 103, 106, 109
297–299, 302, 303 Lecanium scale 208
Integrated control 3, 8, 9, 169, 170 Lecontvirus® 212, 213
Integrated crop management 55, 56, 64, 281, 282, Lectins 126, 127, 130, 138
284, 289, 297, 298, 303–308 GNA 132
Integrated crop protection 293 Lepidoptera 27, 59, 149, 152, 155, 187, 212, 218,
Integrated farm management 261 219, 293
Integrated pest control 306 Lepidopteran pests 77, 85, 137, 177
Integrated pest management (IPM) 1–17, 21–25, Leptinotarsa decemlineata 150, 174, 274
31, 32, 35, 39, 40, 45, 47, 49–51, 55, 56, 59, Lesser cornstalk borer 177, 269
63–65, 73, 80, 81, 106, 108, 123–129, Lesser peach borer 26, 104, 110
135–137, 139, 140, 147, 151, 152, 169–179, Lethal trap crop 196
205, 220, 230, 255–262, 265–278, 281, Leucoma salicis 208
283–292, 294, 297–308 Life models 43
tactical 306 Light brown apple moth 81, 97
Intensified cropping systems 305 Lindane 172, 234
Intercropping 21, 22, 31, 32, 60, 287, 301, Linear statistical models 49
305–306 -Linolenic acid 158
row 32 Lipoxygenases 158
Invertebrates 9, 64 Liriomyza huidobrensis 289
Ipomoea batatas 288, 304 Liriomyza sativae 289
Ips typographus 82 Liriomyza trifolii 289
Lobesia botrana 89
Lodgepole needle-miner 209
Jack pine budworm 209, 212–214, 216 LRR motifs 156
Jack pine sawfly 208, 209 Lucerne 5, 271
Japanese beetle 3, 81, 82, 84, 189 Lucerne weevil 30, 270, 273
Jasmonates 159 Lure-baited traps 189
Jasmonic acid 158 LUX H3 gene 158
Jeffers classification systems 43, 44, 46 Lycopersicon esculentum 288, 303
Juniper scale 208 Lycopersicon peruvianum 148, 155
Lycosa pseudoannulata 177
Lygus bugs 32, 194, 276
Kairomonal insecticide 198 Lymantria dispar 58, 63, 172, 187, 208, 212, 216, 223,
Kairomones 73–75, 78, 80, 132, 191, 197–199 234
Kalmia angustifolia 236 Lythrum salicaria 174
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322 Index

Macrosiphum euphorbiae 28, 148 Mexican rice-borer 131, 132

Maize armyworm 58 Microbial 178
Maize earworm 27, 29, 34, 58, 133, 134, 136 agent 218, 219
Maize leaf aphid 155 contamination 268
Maize leafhopper 30 formulation 272
Maize pests 284 insecticide 3, 269, 271, 272, 275
Maize rootworm 28, 29, 31, 124 toxins 275
Maize stem-borers 297 Microcapsules 99, 101
Maize streak virus 294 Microencapsulated formulation 100, 109
Major gene resistance 293 Microencapsulated pheromones 102
Malacosoma americanum 187 Microorganisms 2, 269, 272
Malacosoma disstria 210, 212, 216 pathogenic 266, 271
Malathion 83, 124, 171–173, 177 plant pathogenic 267, 271
Mancozeb 174 Microplitis croceipes 134
Manduca sexta 3, 157 Microsatellite markers 154
Maneb 174, 274 Microsporidia 206, 209, 210, 214
Manihot esculenta 288 Mindarus abietinus 209
Marker-assisted selection (MAS) 153, 155 Minute pirate bugs 134
system 160, 161 Miridae 64
Marking pheromones 190 Mites 1, 27, 34, 58, 62, 177, 293
Marsh reed grass 240 Mixed cropping 23, 307
Mass trapping 81–84, 111, 185 Mobile parasitoids 135
Mathematical models 44, 51 Mobile pest 135, 185, 193, 194
Mating behaviour 86 Mobile predators 135
Mating disruption 74, 75, 77, 80, 83–89, 94, 97–100, Modelling process 40, 48
102, 103, 105–111, 229–231 Modelling techniques 50
Matrix models 46, 47 Modern gene-transfer technique 64
Mattesia trogodermae 84 Molasses 222
Mealy bug 291 grass 32, 287
Mechanical control 2, 14 Molecular markers 148, 153, 154, 157, 293, 295
Mechanical methods 237, 241 Monarch butterfly 149, 294, 295
Mechanoreception 186 Monocropping 21
Medicago sativa 61 Monocrops 34
Mediterranean flour moths 82 Monocultures 31, 32, 60, 190, 194, 305, 306, 307
Mediterranean fruit fly 177 Monosodium methane arsenate 235
Meliaceae 287 Morphological markers 153, 154
Meligethes viridescens 33 Morphotypes 220
Melinis minutiflora 32, 287 Morrenia odorata 272
Meloidogyne spp. 148, 155 Mortality hypothesis 57
Melon aphid 155 Mosquito 174, 215
Menochilus sexmaculatus 173 Moth behaviour 188
Mesoleius tenthredinis 206 Mountain ash sawfly 208
Mesostigmatid mites 29 Mountain pine beetle 81, 234, 235
Metagonistylum minense 304 MSMA 238
Metallopeptidase 159 Multicapsid 213
-like protein 158 Multiple cropping system 31, 32
Metarhizium anisopliae 84 Multiple embedded virus 220
Methidathion 172 Multiple enzyme pathways 126
Methoprene 3 Multiple linear regression model 45
Methoxyfenozide 176 Multiple-pest resistant cultivars 273
Methyl acetate 91 Multiple pests 175
Methyl bromide 175 Multiple viral particles 220
Methyl jasmonate 158, 159 Multitrophic effects 273
Methyl parathion 172, 173, 177 Multivariate models 46, 47
Metopolophium dirhodum 57 Multivoltine species 109
Mexacarb 217 Mycoherbicides 238–240
Mexican bean beetle 33, 60 Mycoinsecticides 63
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Index 323

Mycotoxins 149 Noxious weed 172, 174, 238

Myzus persicae 63, 158 Nuclear polyhedrosis virus (NPV) 58, 63, 178,
206–210, 212, 213, 215, 218, 222, 227–229
native 213
Nabis spp. 177 Nucleic acid analysis 268
Nachman models 43 Nursery pine sawfly 208
Napier grass 287, 295, 303
Natural biological control 24, 135
Natural communication system 198 Oblique-banded leaf-rollers 79, 107, 109, 110
Natural control 17, 24, 25, 179, 216, 227, 230, 266 (Z),(Z)-3, 13-Octadecadienyl acetate 87, 110
agent 207, 267 Odour-conditioned anemotaxis 187
Natural enemies 4, 7, 11, 22, 23, 31–34, 39, 55–66, Odour cues 187, 189
74, 83, 109, 124, 126–129, 131–136, 139, Oils 175
140, 172, 179, 194, 195, 199, 206, 219, 220, seed 33
227, 229, 232, 233, 238, 267, 271–273, 284, seed rape plants 126, 131
292 Olfactory receptors 87–89
diversity 66 neurones 106
Natural herbicides 237 Oligonucleotide 160
Natural pheromone 105 microassays 157
Natural plant products 287 primers 154
Naupactus spp. 30 Olive fly 81, 83
NBS motifs 156 Olive fruit flies 190
Neem 2, 3, 63 Olla v-nigrum 172
extract 63
Omnivorous leaf-roller 85
leaves 3
Omphalocera munroei 57
oil 287
Onion fly 187–191, 193
tree 287
deterrents 193
Nematodes 1, 2, 23, 33, 148, 156, 210
OPDA reductase 158
plant-parasitic 31
Operophtera bruceata 209
resistance 155, 156
Operophtera brumata 208
root-knot 155
OpMNPV 212, 213, 220, 222, 223
Neochetina spp. 174
OpSNPV 220
Neodiprion abietis 210
Optimization models 46, 48, 49
Neodiprion annulus 209
Neodiprion lecontei 208, 212, 213 Organic matter 27–29, 31
Neodiprion pratti 209 Organophosphates 4, 170–173, 177
Neodiprion sertifer 78, 208, 212 phasalone 172
Neodiprion swainei 208 Orgyia leucostigma 210, 212, 213
Neodiprion tsguae 209 Orgyia pseudotsugata 210, 212, 213
Neodiprion virginianus 209 Orgyia spp. 211
Neonicotinoids 78, 172, 273 Oriental fruit moth 78, 80, 85, 92, 93, 95, 100, 103,
Neoseiulus fallacies 176 104, 107–110
Neozygites fresenii 173 Orius insidiosis 134
Nephotettix cincticeps 156 Orius spp. 176
Nephotettix inpicticeps 26 Orius tristicolor 134
Nicotiana attenuata 157, 159 Orseolia oryzae 151, 154
Nicotiana kawakamii 194 Orthene 225
Nicotiana tabacum 194 Orthoptera 187
Nilaparvata lugens 132, 151, 154, 156, 289, 291 Oryctes rhinoceros 291
Nomuraea rileyi 173 Oryza glaberrima 288, 303
Non-agricultural spartina grassland system 62 Oryza sativa 288
Non-target organisms 170, 172 Oryzia pseudotsugata 47
Non-transgenics 131, 134 Osmotic lysis 149
crops 134 Ostrinia nubilalis 27, 78, 134, 150
cultivars 135 Oulema melanopus 27
maize 130, 132 Oviposition 27, 73, 74, 186–188, 190, 191–194
refuge 138, 160 deterring pheromone 192, 193
tobacco 133 Ovipositional deterrent 188, 190–192
14Integrated pest index 5/5/04 2:20 pm Page 324

324 Index

Ovipositional stimuli 193 action threshold 258

Ovipositor 188 adaptation 274, 275
probing 188 aphids 156
12-Oxododecenoic acid 158 arthropods 33
12-Oxophytodienoic acid 158 attack 22, 28
Oxydemeton methyl 177 behaviour 190
Oxyopes salticus 172 biology 86
colonization 124
complex 305
Paecilomyces fumosoraseus 58 control 2, 4–6, 8, 10–15, 22, 23, 25–27, 65, 77,
Pandemis leaf-roller 107 81, 82, 84, 85, 94, 102, 103, 109–111, 169,
Panonychus ulmi 62 170, 206, 266–269, 273, 284, 287, 296–299
Papaipema nebris 30 damage 82, 138
Papilio polyxenes 149 density 74, 75, 79, 80, 82, 102, 104, 106–109,
Paradigm perfection model 43 111
Paraquat 176 ecology 86
Parasitism 32, 57, 59, 60, 63, 127, 128, 130, 132, 133, free seed 22
176, 177, 215, 220, 227 injury 25, 28, 29
Parasitization 195 management 2, 3, 8, 9, 10–12, 16, 17, 24, 31,
Parasitoids 7, 24, 27, 33, 34, 55, 57–64, 129–136, 39, 41, 47, 51, 56, 61, 62, 64–66, 73–75, 81,
139, 171–173, 177, 205–213, 220, 229, 232, 109, 111, 124–129, 136, 137, 160, 169, 170,
233, 273, 286, 287, 291, 292, 304 175, 177–179, 185, 195, 196, 199, 223, 267,
native 215 268, 270, 271, 277, 278, 282, 283, 302
Parasporal bodies 125 monitoring 273
Paratheresia claripalpis 304 outbreaks 24, 29, 31
Parathion 3, 4 population 62, 169, 170, 173, 177, 192, 194,
Participatory rural appraisal 284 194, 195, 197–199, 259
Pathogen epidemiology 10 pressure 104, 107
Pathogenic protozoan 84 resistance 16, 31, 155, 156, 270, 276, 293
Pathogens 2, 9, 34, 55, 56, 58, 64, 84, 129, 157, 159, vegetable 28, 29, 78
205, 207, 211, 213, 220, 227, 229, 232, 238, Pesticides 2–11, 14–17, 22, 26, 31, 33, 34, 39, 47, 56,
240, 269 61, 65, 66, 74, 102, 111, 123, 136–138, 147,
inducible plant enzyme 159 149, 150, 169–179, 185, 192, 195, 196, 205,
plant 10, 21, 22, 25, 28, 29, 33, 34, 205–207, 238, 255–257, 259–262, 265–268, 273, 274,
239, 269, 270, 272, 275 277, 281, 284–286, 288–293, 296, 298–308
Pea aphid 273 paradox 169
Peach borer 26 rational 13
Peach–potato aphid 63 residues 4, 292, 296, 305
Peach-tree borer 86, 92–95, 97, 103, 104 selectivity 176, 177
Peach-twig borer 85, 92, 94, 95 treated spheres 81, 83
Pecan aphid 173 Phacelia tanacetifalia 61
Pectinophora gossypiella 27, 124, 150, 177, 295 Phagostimulants 187, 190
Pennisetum americanum 288, 303 Phaseolus spp. 288, 303
Pennisetum purpureum 287 Phellinus weirii 240, 241
Pentyl acetate 91 Phenacoccus manihoti 291
Perennial 22 Phenological asynchronies 23, 29
crops 22, 78 Phenology models 49, 50
plants 34 Phenylalanine ammonia lyase 158, 159
weeds 237 Phenylamides 274
Persistence 15, 191, 225 Pheromone 58, 74, 75, 77–110, 132, 169, 177,
Pest 1–4, 6–12, 14–17, 21–24, 27–33, 35, 39–41, 49, 188–191, 197, 198, 220, 221, 225, 235
50, 56, 58, 61–65, 73–79, 82–86, 88, 99, baited traps 97, 101, 103–105, 108, 232
102–104, 106, 107, 109, 110, 124, 126–129, based disruption 97
131–139, 147, 151, 153, 160, 169–171, delivery strategies 106
173–179, 189, 190, 192–199, 205, 207, 211, product 109
215, 227, 238, 256, 258, 259, 265–271, 273, sex 198, 216, 225, 229, 230
274, 276, 277, 282, 284, 285, 289, 292, 293, synthetic 77, 104, 191
297, 299, 301–303, 306 sex 75
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Index 325

traps 75–79, 84, 178, 221, 223, 229–231, 233, Potato leafhopper 30
234 Potato tuberworm 28
Phosphamidon 217, 218 Poxviridae 211
Phospholipases 158 Predaceous insects 3
Phragmidium violaceum 239 Predaceous lacewings 172, 177
Phthalimide 274 Predation 127–129, 133, 195
Phthorimaea operculella 28 Predator colonization 34
Phyllophagus spp. 289 Predators 7, 24, 27, 32, 34, 55, 57, 58, 60–63, 129,
Physical control 2, 14 130, 134–136, 139, 171–173, 177, 194, 206,
Physiological antibiosis factor 199 207, 209, 211, 227, 233, 273, 286
Physiological resistance 185, 192, 195–199 ground dwelling 62
allele 196 Predatory anthocorids 176
allele frequency 195 Predatory arthropods 27, 61
trait 199 Predatory coccinellids 177
Phytophthora infestans 174 Predatory lady beetle 172
Phytophthora palmivora 272 Predatory mite 59, 62, 172, 176
Picloram 238 Prey 27, 57, 60, 128, 130, 132–135, 233, 287, 302
Pieris brassicae 62, 157, 159, 191, 192 density 58
Pikonema alaskensis 78, 210 Primary pests 102, 109, 134, 136, 169
Pine-bark adelgid 209 Pristiphora erichsonii 206, 208
Pine beauty moth 57 Pristiphora geniculata 208
Pine beetle 83, 189 Profenusa thomsoni 208
Pine false web-worm 208 Prophylactic sprays 304
Prosulphuron 273
Pine needle-miner 209
Protease inhibitors 126
Pine sawfly 209
Proteinase inhibitors 149, 158
Pineus strobis 209
Proteolytic cleavage 125
Pink bollworm 25, 29, 85, 99, 108, 124, 136, 150,
Protoxin molecules 125
177, 295
Prunus pensylvania 240
Pinus contorta 57
Prunus serotina 240
var. latifolia 234
Pseudaletia unipunctata 27
Pinus ponderosa 221
Pseudatamoscelis seriatus 29
Pinus resinosa 212
Pseudomonas fluorescens 272
Plant defence elicitors 159
Pteridium aquilinum 236
Platynota idaeusalis 79
Pteromalus spp. 63
Platynota spp. 291 Pupa parasites 62
Pleiotropic effects 195 Push–pull strategy 287, 301, 303
Pleiotropic fitness 196 Pymetrozine 176
Plum curculio 26 Pyrethroids 172, 173, 178
Plutella xylostella 29, 58, 61, 63, 64, 84, 188, 291 synthetic 4
Poikilotherms 50, 269 Pyrethrum 3, 175, 287
Pollinators 4, 73, 217 Pyriproxyfen 176, 276
Polyculture 31, 32, 60 Pyrithiobac 303
Polyethylene dispensers 97
Polyhedral inclusion bodies 213, 222
Polyhedrovirus 211 Quadraspidiotus perniciosus 274
Polymerase chain reaction (PCR) 269 Quantitative resistance 153
technique 154 Quantitative trait loci (QTL) 153
Polymorphism 154 analysis 155
Polyphenol oxidase 158 Quarantine pests 205, 207
Ponderosa pine 221, 235
Population dynamics models 49
Population-genetics simulation 197, 198 Radioactive isotopes 154, 269
model 196 Random amplified polymorphic DNA (RAPD)
Populus spp. 240 markers 154
Populus tremuloides 236, 239 Rangeland IPM 48
Potato aphid 28, 148, 155, 158 Rape-blossom beetle 33
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326 Index

Rapid rural appraisal (RRA) 284 Rosette weevil 175

Recombinant frequency 153 Rotenone 2, 175, 258
Red-banded leaf-roller 103, 107, 110 Rubus fruticosus 239
Red-headed pine sawfly 212, 213 Rubus idaeus 236, 238
Reflective mulches 192, 193 Rubus parviflorus 236, 239
Refuge crop 190, 195, 199 Rubus spectabilis 236, 239
Refugia 33, 60–62, 64, 176, 195 Rubus spp. 239, 240
Regional crop management 124, 125 Russian wheat aphid 155, 156
Regression models 45, 49 Rust fungus 239
Reoviridae 211 Rust thrips 28, 291
Repellent 173, 186, 189, 190, 192, 199 Ryania 258
Resistance 9, 23, 25, 59, 64, 65, 74, 77, 78, 111, 124,
126–129, 133, 138, 139, 147–153, 155–160,
172, 174, 178, 198, 274, 275, 277, 285, 292, Saccharum spp. 288
293, 295, 303 Salicylic acid 158, 159
allele 195 Salination 265
biotypes 153 Salivary enzymes 157
cDNA 157 Salix sp. 236
conservation technology (RCT) 296 Salt-marsh caterpillar 136
factors 55 Sambucus spp. 236
genes 160, 161, 295, 296 Sampling models 43, 49, 50
putative 157 Sanitation 22, 23, 25–27
management 126, 127, 138, 275, 276, 295, 296 San José scale 274
plant 26, 55, 58, 65, 124, 126, 127, 129, 133, Satin moth 208
136, 137, 152, 153, 155, 157–160 Sawfly 57, 78, 212, 213
polygenic 293 Scale model 43
ratio 274 Schizaphis graminum 27, 156
Resistant pest 127, 128, 138 Scolytid bark beetles 234
biotypes 293 Secale cereale 288, 303
plants 57, 127, 128, 157 Secondary 56
populations 274 chemicals 56
strains 275 infections 28
traits 147 outbreak 177
trees 241 pest 102, 109, 124, 135–137, 169, 289, 291, 293
varieties 2, 3, 11, 23, 185, 190, 292, 308 outbreaks 33, 64
Restriction fragment length polymorphism (RFLP) Selective pesticides 175, 291, 298, 304
markers 153, 157 Semiochemicals 73–76, 82, 84–86, 91, 111, 112, 189,
Reverse transcriptases 157 192, 235
RGA sequences 155, 156, 160 based cues 188
Rhagoletis mendax 83 based ovipositional deterrents 192
Rhagoletis pomonella 83 Senecio facobaea 172
Rhinoceros beetle 291 Sequence-characterized amplified regions (SCARs)
Rhinocyllus conicus 175 154
Rhizosphere bacteria 190 Sequence tagged site (STS) markers 154
Rhopalosiphum maidis 155 Sevin 225, 226, 230, 232, 235
Rhopalosiphum padi 159 Silverleaf whitefly 159, 276
Rhyacionia buoliana 208 Simple-sequence repeat (SSR) markers 153, 155
Ribes spp. 236 Simplification model 43
Rice brown planthopper 132 Simulation 49
Rice gall midge 154 model 43, 44, 195
Rice gene sequence 155 Sinigrin 188
Rice leaf-folder 285 Soft-rot bacteria 190
Richardson classification system 43 Sogatella furcifera 26
Rodolia cardinalis 2 Soil biota 295
Rolling fulcrum model 186, 187, 189 Soil erosion 267, 271, 272, 296, 297, 304
Root weevil 193 Soil fertility 21, 29, 34, 269, 281, 285, 287, 294, 297,
Root worm 21, 27 301, 303
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Soil management 41, 293 Sustainable crop management 301, 304

Soil texture 21, 269 Sutainable cropping systems 281, 282, 297, 303,
Soil tillage 23, 27 307, 308
Solanum tuberosum 174, 288, 304 Symbolism model 43
Sorghum bicolor 288, 303 Synanthedon exitiosa 26, 86, 104
Sorghum vulgare sudanense 287 Synanthedon pictipes 26
Southwestern corn borer 155 Synergism 25, 26, 133, 187, 188
Soybean thrips 30 Synergistic 56, 130, 133
Sparganothis fruitworm 85 responses 187
Speckled alder 236 Synergistically 126, 127, 137–139
Spider mites 29 Synomones 59, 73, 132
Spiders 34, 134, 172, 177 Synthetic ovipositional deterrents 192
Spinosad 176, 273, 274 Synthetic pesticides 8, 15, 61, 66, 258, 287, 292, 296,
Spinosyns 273 299, 304
Spodoptera exigua 58, 158, 171 Synthetic pyrethrins 276
Spodoptera frugiperda 32, 59, 132 Syrphidae 57, 63
Spodoptera littoralis 28 Syrphid fly 33
Spores 125, 229, 285 Systemic acquired resistance 159
Sporulation 174 Systemic herbicide 235
Spotted lucerne aphid 273 Systemic pesticide 235
Spotted stem borer 297
Spruce beetle 234, 235
Spruce budmoth 210 Tachinid fly 233
Spruce budworm 76, 107, 205, 206, 209, 211, 213,
Tactical control strategy 305
214, 216, 218, 219, 222
Tannins 187
Spruce seed moth 209
Tansy ragwort 172, 173
Squash bugs 28
Target pest 4, 74, 176, 178
Squash gene 159
Taylor’s power law models 43
Staple crops 136, 138, 139, 298
Tebufenozide 176
Stem borers 26, 29, 30, 32, 287, 289, 294, 295, 297,
Telenomus remus 59
303
Temporal synergism 188
Sterile-insect technique 3
Tent caterpillars 187
Stimulo-deterrent 189
Tephritid fruit flies 83
Stink bugs 28, 176
Stochastic model 44–46 Termites 284
Storage pests 284, 294 Terpenoids 150
Strategic IPM 306 Terpinyl acetate 80
Streptomyces viridochromogens 238 Tetranortriterpenoids 287
Striga asiatica 289, 303 Tetranychus lintearius 239
Striga hermonthica 289, 303 Tetranychus mites 28
Striga spp. 287, 289 Tetranychus urticae 134
Strip cropping 22, 32 Therioaphis trifoli f. maculata 273
system 194 Thiophanate methyl 174
Striped alder sawfly 209 Thr deaminase 158, 159
Striped cucumber beetles 194 gene 157
Striped lynx spider 172 Threshold level 128, 205, 206
Striped rice borer 30 Threshold numbers 223
Striped stem borer 292 Thrips 32, 185, 187, 189, 192
Sublethal effects 126, 129, 222 Thuricide 295
Subtractive suppressive hybridization 160 Thysanoptera 187
Sugar-binding lectins 125 Tobacco budworm 3, 81, 84, 133, 134, 136, 150, 269,
Sugarcane borer 25, 131, 132, 304 270, 274–276
Sulphonylurea 275 Tobacco hornworm 157, 159
herbicides 273 Tolerance 128, 131, 184, 152, 172, 270, 271, 275, 285,
Sunflower moth 60 305
Sustainable agriculture 265–267, 286, 289, 307 Tomato fruit worm 30
production 271 Tomato moth 130
systems 268 Tomato pinworm 85, 104, 107
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328 Index

Tortricids 109 Tritrophic systems 65

Toxaphene 4 Trogoderma glabrus 84
Toxic 148, 149, 217, 237, 238 Tryporyza incertulas 27
chemical residues 258, 267 Tussockosis 221
compounds 265 Two-spotted spider mites 134
Toxicant 78, 83, 84, 274, 275 Typhlodromus spp. 62
Toxicity 136, 262, 273 Tyria facobaceae 172
Toxins 64, 127, 130, 131, 152, 160, 269, 275
Transcriptomes 159
Transgenic 4, 123, 275 Ulex europaeus 239, 240
Bt crop 149 Uromycladium tepperianum 239
cotton 136, 148, 276
crop cultivars 125, 126, 129, 130
crop risk assessment 151 Varietal resistance 185
crops 64, 124, 129, 134–136, 138, 149, 195, 271, Vectors 47, 190, 269
278 Vedalia beetle 2, 3
cultivars 123, 125–140, 273, 274 Vegetative propagation 26
food 150 Vegetative storage protein 159
insecticidal cultivars 135, 136, 139 Velvet bean caterpillar 173
insecticide management strategy 276 Vigna unguiculata 288, 303
insect resistance 148 Viral insecticides 211, 218, 220
maize 130, 132, 148 Viroids 1
hybrids 147 Virtuss® 212, 213, 222
Viruses 1, 2, 58, 185, 192, 207, 211–213, 215,
plant 3, 126, 130, 131, 139, 149, 152, 160, 270,
219–223, 225, 229, 230, 232, 238, 269, 271
271, 275, 276
epizootic 212, 213, 221
potato 130
resistant 303
cultivars 148
transmission 185
resistance 152
Viteus vitifoliae 2
techniques 39
Viticulture 260
technology 152, 296
Vullemin 174
tobacco 133
Trap crop 23, 32, 33, 35, 61, 185, 189, 190, 193, 194,
198, 287
Water hyacinth 174
Trap cropping 23, 35
Water management 23, 29
Traps 71, 73, 74 Waxes 95, 97
Traumatin 158 Weeds 1–3, 9, 10, 17, 21–23, 25, 28, 34, 50, 63, 172,
Trialeurodes vaporariorum 58, 63, 289 174–176, 194, 196, 206, 207, 214, 236, 238,
Triasulphuron 273 239, 266, 267, 269, 271, 275, 277, 297, 298,
Triazine 173 305
herbicide 275 control 24, 28, 32, 272
Trichlorfon 217, 225 management 27
2, 4, 5-Trichlorophenoxyethanoic acid 238 parasitic 287, 303
Trichogramma cacoeciae 173 pest 239
Trichogramma minutum 215 seeds 237
Trichogramma pretiosum 134, 304 Weevils 30, 171, 174, 175, 190, 191
Trichogramma spp. 32, 59, 271 Western balsam bark beetle 234
Trichomes 193 Western black-headed budworm 209, 218
Trichoplusia 137 Western flower thrips 58
Trichoplusia ni 57, 84, 89, 136 Western grape leafhopper 61
Trichosirocalus horridus 175 Western hemlock looper 209, 215
Trimedlure 191 Western maize rootworm 152
Triphenyltin hydroxide 173 Western oak looper 209
Triticeae 156 Western spruce budworm 172, 209, 212–215,
Triticum aestivum 41 218–220
Triticum spp. 288 Wheat curl mite 28
Tritrophic interactions 176 Wheat sawfly 26, 27, 29, 34
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White-backed planthopper 26 Xanthogaleruca luteola 208

White flies 28, 32, 63, 276, 289
White-fringed beetle 30, 31
White grubs 27, 289 Yellow-headed spruce sawfly 210
White-marked tussock moth 210, 212, 213, 222
White pine weevil 209
White-rot fungus 239 Zea mays 288, 303
Wilt disease 228 Zeiraphera canadensis 210
Winter moth 208, 210, 211 Zineb 173, 174, 177
Wireworm 27, 31, 194
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