Pons, roca, lumbierres & lucas 2015 sjar

Spanish Journal of Agricultural Research
13(2), e1006, 11 pages (2015)
eISSN: 2171-9292
http://dx.doi.org/10.5424/sjar/2015132-7054
Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA)
RESEARCH ARTICLE OPEN ACCESS
Nevertheless, data from Spain are scarce (Brown
et al., 2008, 2011a). The coccinellid was introduced
in Almería (South East Spain) for aphid control in
1995 (Jacas et al., 2006), some adults were observed
in the Canary Islands in 2003 and 2004 (Machado,
2006) and one single specimen was found in a pub-
lic garden in Bilbao (Northern Spain) in 2007 (Gol-
dazarena & Calvo, 2007). In spite of these release
and findings, no evidence of population establish-
ment occurred (Brown et al., 2008, 2011a). Beyond
of these records, there were some years without
public records until that Carbonell & Sesma (2013)
reported the occurrence of isolated individuals in
several localities of Catalonia (North-eastern Spain)
and one overwintering aggregation, quite close to
the France border. However, no description of the
characteristics of any Spanish aggregation has been
Characterization of a newly established aggregation
of the invasive ladybeetle Harmonia axyridis and current status
of the invader in Spain
Xavier Pons1
, Meritxell Roca1
, Belén Lumbierres1
and Éric Lucas2,3
1
Universitat de Lleida, Department of Crop and Forest Sciences. Agrotecnio Center. Rovira Roure 191. 25198 Lleida, Spain.
2
Institut de Recerca i Tecnologia Agroalimentària (IRTA), Unitat d’Entomologia. Ctra. de Cabrils, Km 2, 08348 Cabrils, Spain.
3
Université du Québec à Montréal, Département des Sciences Biologiques. CP 8888, Succursale Centre-Ville, Montréal (Québec), H3C 3P8 Canada.
Abstract
The multicoloured Asian ladybeetle, Harmonia axyridis (Pallas), an invasive biocontrol agent introduced in North and South
America, as well as in Europe for aphid control, drastically affected assemblages of native coccinellid species, local communities
and people. Although the insect is common in several European countries and it was released in Spain for aphid control in 1995, no
evidence of population establishment has been reported until 2011. In the present paper, 1) we summarize the records of the invasive
ladybeetle in Spain and provide numerous new mentions, and 2) we follow for the first time an overwintering aggregation from
autumn to spring and characterize some individual features which allow us to determine its phenology of the establishment and
spreading. The results establish clearly that: 1) H. axyridis is (until now) restricted to Catalonia (NE Spain) but the invading process
is in progress and the insect is able to occupy different habitats; 2) the ladybeetle overwinters successfully in Spain without sig-
nificant natural mortality or parasitism; 3) the form succinea represents 73-81% of the overwintering individuals, and 4) the invasion
takes probably its origin from Southern France. The potential impact of the invasion by H. axyridis in Spain is discussed.
Additional key words: multicoloured Asian ladybeetle; overwintering; invasive species; coccinellids; European expansion;
harlequin ladybird.
Citation: Pons, X.; Roca, M.; Lumbierres, B.; Lucas, E. (2015). Characterization of a newly established aggregation of the in-
vasive ladybeetle Harmonia axyridis and current status of the invader in Spain. Spanish Journal of Agricultural Research, Volume 13,
Issue 2, e1006, 11 pages. http://dx.doi.org/10.5424/sjar/2015132-7054.
Received: 06 Nov 2014. Accepted: 04 May 2015
Copyright © 2015 INIA. This is an open access article distributed under the Creative Commons Attribution License (CC by 3.0),
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Funding: The authors received no specific funding for this work.
Competing interests: The authors have declared that no competing interests exist.
Correspondence should be addressed to Xavier Pons: xavier.pons@irta.cat
Introduction
The multicoloured Asian ladybeetle, Harmonia axy-
ridis (Pallas), is an east-paleartic species (native from
Japan, China, Korea, Mongolia and Siberia) introduced
in North-and South-America, Asia and Europe for aphid
control, which has generated unexpected impacts on
native coccinellid populations, ecosystems and people
(Koch, 2003; Roy & Wajnberg, 2008). In Europe, H.
axyridis was introduced for the control of aphids in
Ukraine and Byelorussia in the last sixties and in France
in the last eighties, but was not commercialized until
middle nineties (Brown et al., 2008). Since its introduc-
tion in these countries, the expansion of H. axyridis
through Europe has been continuous (Brown et al., 2008)
and its effects on crops, urban areas and ecosystems have
been widely studied and described.

Xavier Pons, Meritxell Roca, Belén Lumbierres and Éric Lucas
Spanish Journal of Agricultural Research June 2015 • Volume 13 • Issue 2 • e1006
2
advisers in Central Spain, Valencia, Andalusia and Astu-
rias was required for reporting current or existing obser-
vations of the recent presence of the ladybird in their
geographical areas and for scouting.
Characterization of the aggregations
Firstly, we characterized the sites where aggregations
occurred: geographic coordinates, altitude, surrounding
landscape, building characteristics, etc. Among the four
aggregation sites reported, we selected the population of
Les Llosses, since it was the largest. Characterization of
this aggregation included natural mortality, parasitism rate,
and phenology of the overwintering beetles, elytra colour
pattern, sex ratio, weight, size, and female ovariole devel-
opmental stage before and after the overwintering period.
To determine the overwintering phenology, the ag-
gregation was periodically monitored from November to
May and the changes in colonies settle in visible places
recorded. Yellow sticky traps and pollen bait traps were
also placed inside and outside the Les Llosses overwinter-
ing site at the end of February and weekly monitored to
detect individuals leaving the site. Along the overwinter-
ing period, individuals were collected and brought to the
laboratory in order to determine sex, weight, size, ovari-
ole development and parasitism. The adults were main-
tained in a refrigerator at 5 °C for 1-2 days before being
individually photographed under stereoscopic microscope
(Leica MZ8) on a millimetre paper. Then, specimens
were individually preserved in ethanol 70°. The body
length and width was measured from photos using the
software programme ImageJ (Rasband W.S., US Na-
tional Institutes of Health, Bethesda, MD, USA, http://
imagej.nih.gov/ij/, 1997-2014). Alcohol preserved indi-
viduals were sexed under the microscope and then dis-
sected in Beadle’s solution in order to establish ovariole
developmental stage and potential parasitism. Weight and
size were compared at the beginning and after overwin-
tering by an ANOVA. Sex ratio was compared to 1:1
proportion by chi-square analyses.
By the end of the overwintering period, beetles
started to be more active. Their distribution within the
house (level and orientation) was periodically record-
ed (from 14 March to 2 May).
Results
Status of H. axyridis in Spain
Table 1 and Fig. 1 show the historical records of
H. axyridis in Spain, with the new mentions. In addition
to the findings of the ladybird in Spain described in the
reported and their ability to overwinter in Spain
remains to be established.
We were alerted of several aggregations of coccinel-
lids adults occurring in houses in four localities of
Northern Catalonia: a bigger one in Les Llosses (Girona
province) and two smaller ones in Alpens and Borredà
(Barcelona province) in November 2013, and another
one in Capmany (Girona province) in January 2014. We
identified all aggregations as H. axyridis and started to
monitor the overwintering population and to prospect
for new occurrences of the ladybird, mainly in Catalonia.
The present report aims 1) to describe the current
status of H. axyridis in Spain, and 2) to characterize
and follow for the first time an overwintering aggrega-
tion of the invader in the Spanish context.
Material and methods
Status of H. axyridis in Spain
Data on the occurrence of H. axyridis in Spain were
collected by a thorough review of the literature and
also by direct mentions from authors and colleagues.
In addition to the monitoring of reported aggregations
during autumn and winter, from the end of the overwin-
tering period until August, periodically (every 2-3 weeks)
a sampling was done in several locations of Catalonia
and the Basque Country on different types of vegetation.
Sampled locations in Catalonia were La Seu d’Urgell
[Lleida province; alfalfa and maize crop fields and plants
in field margins; sweep net and Vortis® suction sampler
(Burkard Manufacturing Co. Ltd., Ricksmanworth, UK)
in alfalfa and visual sampling in maize and field mar-
gins], Alpens and Borredà (Barcelona province; margin
vegetation in roads and gravel roads; visual sampling),
Barcelona city (urban parks, visual sampling and yellow
sticky traps), Lleida city (botanical garden and urban
parks; visual sampling and yellow sticky traps), Lleida’s
city surroundings and Gimenells (Lleida province; maize
fields, visual sampling and yellow sticky traps), Cabrils
(Barcelona province; margin vegetation in roads and in
parks; visual sampling), and Torroella de Montgrí (Gi-
rona province; vegetation of the banks of river Ter; vis-
ual sampling). Scouting in the Basque Country was
visually carried on in vegetable gardens and urban parks
of Zarautz (Gipuzkoa province). Occasionally, some
localities of northern Aragon (Jaca) and Navarra (Ochaga-
vía, Elizondo, Pamplona) were also visually sampled by
authors in forest and urban parks. The presence of the
insect in Catalonia was also communicated by scientists
and collaborators (colleagues from universities and re-
search centres, urban landscape managers, farm advisers,
etc.). Information to several colleagues and technical

3Characterization of a new aggregation of the ladybeetle Harmonia axyridis in Spain
Table 1. Period and locality of the records of Harmonia axyridis in Spain. When the reference is “Authors”, it means that H. axyridis
was recorded by the authors of the present study or their collaborators
Year (Month) Locality (Region)1
Insect
developmental
stage
No. of individuals Site Reference
1995 Almería (And) ― Undetermined 2
Greenhouses SIFA(2004); Jacas et al.
(2006)
2003-04 (Oct) La Laguna (Tenerife, Can) Adult 1 individual Garden Machado (2006)
2006 Tenerife (Can) Adult 1 individual Garden Brown et al. (2008)
2007 (Jun) Loiu (Biscay, Bas) Adult 2 individuals Urban park on Tilia platyphyllos Scop.
(Eucallipterus tiliae L.)
Goldazarena Calvo
(2007)
2010 (Jul) Sant Dalmai (Girona, Cat) Adult 1 individual Next to crops Carbonell Sesma (2013)
2010 (Nov) Girona (Cat) Larva 1 individual Urban park Carbonell Sesma (2013)
2011 (Nov) Girona (Cat) Adult 1 individual Garden Carbonell Sesma (2013)
2011 (Sep) Beuda (Girona, Cat) Adult 1 individual House Carbonell Sesma (2013)
2011 (Oct) St Llorenç de la Muga
(Girona, Cat)
Adult Overwintering aggregation
(200 individuals)
House Carbonell Sesma (2013)
2011 (Nov) Gualba (Barcelona, Cat ) Adult 1 individual Village Carbonell Sesma (2013)
2012 (Jul) Barcelona (Cat) Adult 1 individual Urban park Carbonell Sesma (2013)
2012 (Jul) Santandria (Menorca, Bal) Adult 1 individual Garden Carbonell Sesma (2013)
2013 (Sep) Zarautz (Bas) Adult 1 individual Beach Lumbierres et al. (2014)
2013 (Nov) Les Llosses (Girona, Cat) Adult Overwintering aggregation
(500 individuals)
House. Some individuals on
weeds
Lumbierres et al. (2014)
2013 (Nov) Borredà (Barcelona, Cat) Adult Overwintering aggregation
(200 individuals)
House Authors
2014 (Jan) Campmany (Girona, Cat) Adult Overwintering aggregation
(100 individuals)
Farm hut Authors
2014
(Feb-May)
Les Llosses (Girona, Cat) Adult Post overwintering
dispersing individuals
(750 individuals, see text)
House Authors
2014 (Mar) Lleida (Cat) Adult 1 individual Urban (inside a car) Authors
2014 (Mar) Lluçà (Barcelona, Cat) Adult 1 individual House Authors
2014 (April) Alpens (Barcelona, Cat) Adult Post overwintering dispersing
individuals (30 indiv.)
House Authors
2014 (April) Torroella de Montgrí
(Girona, Cat)
Adult Post overwintering
(3 individuals)
Field margin on Rumex sp.
(Aphis fabae Scopoli)
Authors
2014 (April) Sant Dalmai (Girona, Cat) Adult Several individuals Next to crops Sesma (2015)
2014 (April) Roses (Girona, Cat) Adult 1 individual Urban park Sesma (2015)
2014 (April) Vilassar de Mar
(Barcelona, Cat)
Adults 1 individual Urban Sesma (2015)
2014 (May) Torroella de Montgrí
(Girona, Cat)
Adult +
Egg
Mating adults + eggs
(6 individuals)
Field margin on Arundo donax L.
(Melanaphis donacis (Passerini))
Authors
2014 (Jun) Cabrils (Barcelona, Cat) Adult +
Larva
2 adults + 1 larva Gravel road on A. donax
(M. donacis)
Authors
2014 (Jun) Borredà (Barcelona, Cat) Adult 1 individual Road edge on Urtica sp.
(Aphis urticata Gmelin)
Authors
2014 (Jun) Sabadell (Barcelona, Cat) Larva 1 individual Urban park on Liriodendron tulipifera L.
(Illinoia liriodendri (Monell)
Authors
2014 (Jun-Jul) Barcelona
(Barcelona, Cat)
Larva
Adult
1 individual
1 individual
Urban park
House
Authors
2014 (Jun) Soria Adult 1 individual Urban park Sesma (2015)
2014 (Jul) La Jonquera-Cantallops
(Girona, Cat)
Adult 1 individual Meadow Sesma (2015)
2014 (Jul) Cal Riera (Barcelona, Cat) Adult 1 individual River bank Sesma (2015)
2014 (Aug) L’Estartit (Girona, Cat) Adult Several individuals Beach Sesma (2015)
2014
(Jun, Sep)
Sant Martí d’Albars
(Barcelona, Cat)
Larva
Adult
1 individual
1 individual
Next to crops Sesma (2015)
1
And: Andalusia; Can: Canary Islands; Bas: Basque Country; Cat: Catalonia; Bal: Balearic Islands. 2
Released for biological control.

4
Fifty meters slope down of the building there is a water
stream with bank river vegetation.
The aggregation from Borredà was observed within
a room of the east side of a several attached buildings
of an isolated four-storey farm house. The house was
located on the SE slope of a hill of 970 m, at 800 m
altitude. The building was surrounded by garden veg-
etation, meadows and cereal fields and separated from
a pine and oak forest (around 100 m) and from a water
stream with bank river vegetation (150 m).
The aggregation of Alpens was observed inside a
room of the east side of a three storey farm-house,
150 m to the East from the end of the village at 870 m
altitude. The house was located in an area dominated
by pine and oak forest and uncultivated lands. Near the
house there is a road and beyond it a cultivated area
with fields of winter cereals and grasses which ends
400 m slope down at 810 m altitude.
The aggregation of Capmany occurred inside a tool-hut
and in a wood pile besides that building. The site was in a
plane area at 100 m altitude. The hut was surrounded by
orchards with vegetables and some scattered fruit trees, an
almond tree field (0.5 ha) and a vineyard of nearly 1 ha.
Characterization of the Les Llosses aggregation
Overwintering phenology. The house owner realized
the presence of the coccinellids in middle October
Introduction section, and those reported from Carbonell
Sesma (2013) and Sesma (2015) through photograph-
ic records in the website http://www.biodiversidadvirtual.
org, we have recorded overwintering aggregations in
several new sites of central and north Catalonia and the
presence in spring and summer of individuals (adult,
larvae or eggs) in some others close or far away locali-
ties from the overwintering sites. Most of the records
are concentrated in Catalonia, the only region where
overwintering aggregations have been reported.
In spring and summer, we found adults and larvae of
H. axyridis in some herbaceous plants (Rumex sp., Ur-
tica sp.), on giant reed (Arundo donax L.) and on some
trees (Liriodendron tulipifera L.) infested by aphids
(Table 1). Other coccinellid species were also collected
in these sites: Adalia decempunctata L., Coccinella
septempunctata L., Hippodamia variegata Goeze, Pro-
pylea quatuordecimpunctata L., and Scymnus sp.
Overwintering sites
The aggregation from Les Llosses occurred in a
isolated three-storey house of 135 m2
floor and 7.90 m
height, at 795 m altitude in the south-east slope of a
915 m altitude forest hill dominated by pines (Pinus
sylvestris L.) and oaks (Quercus rubor L.). The house
is surrounded by a meadow field and a tiny garden of
vegetables and with some pear, plum and quince trees.
Figure 1. Geographic distribution of Harmonia axyridis in Spain (see also Table 1). : Records from other authors in Spain and
Andorra: 1
Almeria; 2
Tenerife; 3
Loiu; 10
Menorca; 11
Soria; 12
Ordino (Andorra). : Records from other authors in Catalonia: 4
St Dalmai;
5
Girona; 6
Beuda; 7
St Llorenç de la Muga; 8
Gualba; 9
Barcelona; 21
Roses; 22
Vilassar de Mar; 26
La Jonquera-Cantallops; 27
Cal Riera;
28
L’Estartit; 29
St Martí d’Albars. *: Records from authors: 13
Zarautz (43°17’17.86”N; 2°10’01.34”W); 14
Les Llosses (42°08’37.28”N;
02°03’11.68E); 15
Borredà (42°08’10.24”N; 02°02’50.73”E); 16
Capmany (42°22’15.67”N; 02°55’22.92”E); 17
Lleida (41°37’50.45”N;
0°36’12.24”E); 18
Lluçà (42°05’00.61”N; 2°01’05.17” E); 19
Alpens (42°07’05.94N; 02°06’19.14”E); 20
Torroella de Montgrí
(42°02’32.20”N; 3°07’40.45”E); 23
Cabrils (41°31’20.92N”; 2°22’18.95”E); 24
Sabadell (41°32’39”N; 2°05’28”E); 25
Barcelona
(41°22/3.28”N; 2°9’22.65”E).

viduals collected after overwintering (14 and 28 March)
(25.0±1.5 mg) (F=8.71; p=0.0034; df=1, 277). This
difference was also significant according to beetle sexes
(F=5.35; p=0.0214, df=1, 277) with a weight loss of
15% in females and of 28% in males.
The length and width did not vary with the elytra
pattern form, but again changes with sex. Body size of
females was significantly greater than males at the three
sampling dates (Table 3).
Ovariole development. Dissection of females showed
that before overwintering the ovarioles were empty of
eggs. However, after overwintering there was a progres-
sive increase of the proportion of ovarioles with eggs,
reaching more than 60% by the end of March (Table 4).
No copulating individuals were observed.
Mortality and parasitism. No old dead corpse from
previous years was found. Three hundred and fifty-
eight adults (males and females) were dissected and
no parasitized individuals were found. Neither ec-
toparasitic fungi, nor ectoparasite mites were recorded.
when she observed that in several days a large number
of a new “type” of ladybird stayed on the outer East
and South walls of her house. More than 500 adults
stayed on that walls for some days and later insects
were punctually observed within the house. On 4 No-
vember 2014, we recorded more than 200 individuals
in several quiet groups, mainly on the East inner wall
of the house. Some few adults were also observed on
herbaceous plants and grasses around the building.
During winter, overwintering individuals were mostly
hidden, but several clusters remained quiets in visible
places. An adult of Harmonia quadripunctata Pontop-
pidan was also identified within the aggregation. On 5
March, we detected movement of individuals and from
then to the end of April active adults in the house were
recorded. These individuals abandoned progressively
the house and dispersed. On 2 May, no adults remained
inside the house. No captures of adults were obtained
from yellow sticky traps or pollen bait traps.
The end of the overwintering period started at the
same time for the populations from Borredà and Alpens
but occurred a little bit earlier in Capmany (end of
February).
Elytra colour pattern. Forms succinea, conspicua
and spectabilis (according Osawa Nishida, 1992;
Mitchie et al., 2010) were found over the sampling
period. The form succinea was the prevalent over the
whole period and represented between 73 to 81% of
the individuals (Fig. 2). Among melanic forms, spect-
abilis was lightly more abundant than conspicua. There
was no difference in the elytral colour pattern between
sexes and between individuals collected before and
after overwintering.
Sex. The sex ratio was not statistically different from
1:1 for any insect form and sampling date, although
more females than males were recorded after overwin-
tering (Table 2).
Weight and size. The weight of adult individuals was
not affected by colour forms (F=1.93, p=0.1473; df=2,
271) but influenced by sex (F=4.18, p=0.0419, df=1,
271), females weighting more than males at each sam-
pling date (Table 3). Also, individual weight changed
according to the sampling date (F=4.52, p=0.0118,
df=2, 271). Individuals collected before overwintering
(4 November) being heavier (30.8±0.7 mg) than indi-
Proportion(%)
Colour Pattern
4-Nov 26-Feb 14-Mar 20-Mar
succinea
spectabilis
conspicua
28-Mar
100
80
60
40
20
0
Figure 2. Proportion of colour forms of Harmonia axyridis from
Les Llosses (Girona, Catalonia) at overwintering (November 4
and February 26) and after overwintering (March 14, 20 and 28).
Table 2. Sex ratio (%) of Harmonia axyridis individual from
the population of Les Llosses before and after overwintering
Period
% of individuals
χ2
p
♀ ♂
Before overwintering 44.6 55.4 1.16 0.28
After overwintering 57.2 42.8 2.07 0.15
Table 3. Mean ± S.E. values of weight, length and width of females and males of Harmonia axyridis from Les Llosses (Girona,
Catalonia) at the beginning of overwintering (4 November) and after overwintering (14 and 28 March)
Body
measure
4 Nov 14 Mar 28 Mar
♀ ♂ ♀ ♂ ♀ ♂
Weight (mg) 32.78 ± 1.22 a 19.22 ± 0.57 b 28.27 ± 1.26 a 21.98 ± 1.12 b 27.67 ± 3.04 a 20.73 ± 0.46 b
Length (mm) 6.91 ± 0.08 a 6.61 ± 0.16 a 7.20 ± 0.10 a 6.62 ± 0.08 b 7.16 ± 0.05 a 6.63 ± 0.05 b
Width (mm) 5.54 ± 0.07 a 5.37 ± 0.04 b 5.82 ± 0.09 a 5.56 ± 0.06 b 5.81 ± 0.04 a 5.59 ± 0.05 b

6
sion is the fact that until now, the ladybeetle is re-
stricted to the North-East of Spain (Catalonia). Records
from other regions of Spain (Basque Country, Balear-
ic and Canary Islands, Andalusia, and the latest in Soria
(http://www.biodiversidadvirtual.org) suggest that the
insect has not been established there yet.
What is the origin of the invasive population?
Two hypotheses can be formulated about the po-
tential origin of the population: first, the Spanish
origin (colonization derived from previously released
ladybeetle in Almeria, south of Spain) and second,
the European origin. Logically, the Almeria hypoth-
esis should be discarded, since the release was con-
sidered unestablished (Jacas et al., 2006; Brown et al.,
2011a), and no individual has been reported from the
south of Spain since this time. Considering the Euro-
pean hypothesis, Lombaert et al. (2010, 2014) re-
ported three routes of invasion of the European
populations of the beetle, one coming from its native
area released for biocontrol 1982 in France (named,
European Biocontrol Strain), and another two, each
one coming from eastern or western USA. In absence
of genetic analyses, it is impossible to determine
without any doubt the origin of the Spanish popula-
tions. However, the relative proportion of elytral color
forms can be quite different among populations from
different countries. For example, in USA and Eastern
Canada, melanic forms are virtually absent (Koch,
2003; Lucas, pers. obs.). In the Spanish aggregation
about 20% of the individuals have melanic forms and
the relative proportion of elytral color forms (Fig. 2)
is similar to other European populations (Adriaens
et al., 2008; Burgio et al., 2008; Brown et al., 2008;
Stankovic et al., 2011). Brown et al. (2008) suggest
During the monitoring of the aggregation, no mortal-
ity was recorded.
Distribution of active ladybeetles in the overwinter-
ing house. A total of 761 observations of active indi-
viduals after overwintering were effectively done. In-
dividuals were frequently found in groups, especially
in the corners of the windows, or below window frames
on the wall, or in the corners of ornamental devices on
shelves on the wall. Most of the first active individuals
were observed at the first floor, probably because it
was the warmer level of the house. Later on the season,
although active ladybeetles were observed in all house
storeys, most of them were at the ground floor
(Fig. 3A). In relation to the orientation, the insects
preferred the East side of the house (Fig. 3B).
Discussion
The present results on the overwintering aggrega-
tions of the Asiatic ladybeetle and the numerous new
mentions of the beetle reported establish clearly that
the invasion process is in progress in Spain. Harmonia
axyridis is present, reproduces, lays eggs, develops and
overwinters successfully in Spain. The second conclu-
Table 4. Number of Harmonia axyridis females with ovari-
oles containing eggs at three dates of the overwintering pro-
cess: before (November 4) and after (March 14 and 28) over-
wintering
Date
Female
dissected
number
No. of females % of females
with ovarioles containing eggs
4 November 45 0 0
14 March 36 3 8.33
28 March 99 63 63.63
S N E
(A) (B)
1st floor 2nd floorGround flour
Mar 14
100 %
80 %
60 %
40 %
20 %
0 %
Mar 20
100 %
80 %
60 %
40 %
20 %
0 %
Mar 28 Apr 4 Apr 10 May 2 Mar 14 Mar 20 Mar 28 Apr 4 Apr 10 May 2
Figure 3. Proportion of active individuals recorded after overwintering in the three house-storeys (A) and on each orientation of
the inner walls of the house (B). No ladybeetles were recorded on May 2 and on Western walls.

reproductive processes. Several studies reports a short
diapause followed by a quiescence period allowing
insects to be active if weather conditions become fa-
vourable (Iperti Bertrand, 2001; Raak-van den Berg
et al., 2012; Awad et al., 2013). The population from
Campmany, a northern locality close to France border,
finished the overwintering period before that of Les
Llosses. This may be due to a milder weather in
Capmany (due to lower altitude) according to a closer
proximity to the sea: 14.4 to 8.3 °C from October to
March in Les Llosses and 18.3 to 11.9 °C in Capmany,
with minimum 3.7 and 8.2 °C in Les Llosses and
Capmany, respectively (Servei Meteorològic de Cata-
lunya, http://www.meteocat.cat). Further studies should
be conducted in order to precise overwintering features
of the Spanish populations of H. axyridis according to
temperature, altitude, latitude and distance from the
sea.
Some Asiatic populations are female biased due to
the presence of a male-killing bacterium from genus
Spiroplasma sp. This male killer has not been reported
from H. axyridis in its introduced range (Kenis et al.,
2008). In spite of that, Awad et al. (2013) found in
Czech populations a lower survival rate during winter
of males than females resulting in a low proportion of
males in spring. We did not record significant differ-
ences to 1:1 sex ratio between sampling dates, although
a lower proportion of males was recorded after over-
wintering.
After overwintering, insects from the aggregation of
Les Llosses abandoned the house refugia and dispersed
without evidence of their destination, although a few
individuals were found in June relatively close to the
different overwintering sites. The mentions of indi-
viduals in spring and summer far of the overwintering
sites may be an evidence of the movement of the
populations or could be due to the presence of other
existing overwintering aggregations. H. axyridis is
often considered as a good flyer (Hodek et al., 1993)
and a rate of spread up to 200 km per year in Europe
has been evaluated (Brown et al., 2011a), but spreading
could also be favored by involuntary human transport
(one mention reports an adult ladybeetle in Lleida
within a car coming from northern Catalonia). It would
be very important to follow the colonization of the
Iberian Peninsula by systematic samplings of indi-
viduals during spring-summer and of overwintering
populations during winter.
Beside the spreading capacity, individuals collected
in the present study show that H. axyridis is able to
occupy very different habitats (urban landscapes, reed
beds, riparian or ruderal zones, etc.) on trees, shrubs
and herbaceous plants and that it seems that there is an
expansion from northern to central areas of Catalonia.
that the elytral color similarity in European popula-
tions is linked to limited points of origin in Europe,
as Lombaert et al. (2014) has recently stated. Finally,
all the reported mentions of H. axyridis in the present
paper come from sites at less than 150 km from the
French border. The entry may then have occurred from
France trough the Pyrenees either by natural disper-
sion of the insect, or via human transport. The finding
of the insect in Andorra (Sesma, 2015) supports this
hypothesis.
What is the phenology of the establishment
and spreading of the invasive aggregations?
Considering the timing of the invasion, the Spanish
overwintering aggregation of Les Llosses is probably
a new invasive population from 2013, since no cadav-
ers were found from previous years and since the owner
of the house who is living there had never seen the
invader before. This aggregation successfully overwin-
ters in 2013-14 and the phenology of the overwintering
coincides with the described general pattern in the
invaded countries of Europe and the Northern Hemi-
sphere (Iperti Bertrand, 2001; Koch, 2003; Raak-van
den Berg et al., 2012).
Overwintering started with the gathering of indi-
viduals in mid October, the hibernation by the end of
October or the beginning of November, and the end of
the overwintering occurred at the beginning of March.
Adults preferred mainly the East side of the house for
overwintering as is suggested by the records during the
aggregation period and by the distribution of active
insects within the house in March and April.
The presence of undeveloped ovaries in females and
the weight decrease in male and females by loss of fat
body content have been reported as signals of hibernat-
ing individuals (Sakurai et al., 1992; Iperti Bertand,
2001; Raak-van der Berg et al., 2012). Females of the
Les Llosses’ aggregation had their ovaries empty of
eggs until middle of March, when they started develop-
ing ovarioles and, by the end of March, nearly two of
each three females had eggs in their ovarioles. Further-
more, males and females lose weight, although loss
was higher in males than in females. The results on
female ovariole development and adult weight suggest
that the aggregation of Les Llosses has suffered a real
hibernation. Ceryngier et al. (2004) showed that fe-
males of some coccinellid species may have inactive
ovaries in early dormancy but sperm in their sper-
matheca, facilitating an early fertilization process in
overwintering sites or nearby them. The lower weight
loss in females than in males in the Les Llosses’s ag-
gregation may be an indicator that females started their

8
Katsanis et al., 2013), negative impact on them
should be expected also in urban landscapes. In
Eastern Canada, A. bipunctata has disappeared from
urban landscapes since the arrival of H. axyridis
(Lucas, pers. obs.).
The Asian lady beetle would also probably invade
forestal and more-open natural environments. For ex-
ample, fifteen years after its arrival in Quebec (Cana-
da), the multicoloured H. axyridis was clearly the
dominant species in undisturbed wild meadow ecosys-
tems demonstrating that these habitats will not consti-
tute a natural refuge from the invader for native species
(Bélanger Lucas, 2011).
To improve their survival during winter, H. axy-
ridis feeds on sugar-containing fruits like apples, pears
or grapes in late autumn (Koch, 2003; Lucas et al.,
2007b; Galvan et al., 2008). In the case of grapevines,
insects could be harvested with the fruit and during the
process beetles release haemolymph containing sub-
stances that can alter the smell and taste of wine (see
Pickering et al., 2004). The invasion by H. axyridis
could then constitute a threat for the fruit and wine
industry in Spain.
No parasitized individuals were recorded from the
aggregation of Les Llosses in samples taken at the
beginning and after overwintering. Furthermore, no
parasitized individuals were collected in spring or sum-
mer. Dinocampus coccinellae Schrank (Hymenoptera:
Ichneumonidae) and Hesperomyces viriscens Thaxt.
(Ascomycota; Laboubeniales) are common parasites
of coccinellids recorded in Catalonia on several coc-
cinellid species as C. septempunctata, H. variegata, O.
conglobata and A. decempunctata (Lumbierres, pers.
obs.), so that H. axyridis is susceptible to be parasitized
by these parasites. However, a recent study shows that
natural enemies are still unable to control populations
of H. axyridis in Europe (Raak-van den Berg et al.,
2014). In America also, despite the fact that D. coc-
cinellae readily attacks H. axyridis, the success of the
parasitism is very low and lower than on other coc-
cinellid species, due to host behavioral defenses and
unsuitability (Firlej et al., 2005, 2010).
Van Lenteren et al. (2008) defined H. axyridis as a
potentially risky species for Northwest Europe and
Brown et al. (2008) predicted than the expansion of
the invader in Europe would occur mainly to the north-
ern and eastern countries and that the spread southward
is uncertain (see also Kontodimas et al., 2008; Soares
et al., 2008). However, the reports of Kulijer (2010)
in Bosnia-Herzegovina, Stankovic et al. (2011) in
Croatia and the present study, demonstrate the high
potential of invasion in southern Mediterranean coun-
tries. The Asiatic ladybeetle has a huge phenotypical
plasticity. The insect is euryphagous, eurytopic and
What will be the impact of the invasion
by H. axyridis and what should we expect
in the future?
The impacts of the invasion by the Asiatic ladybee-
tle have been thoroughly reported in the invaded re-
gions, with positive but mainly negative effects related
to its establishment [see Majerus et al. (2006) as a
revision]. Since the establishment of the beetle in Spain
is now demonstrated, impacts of H. axyridis should be
expected, and negative ones should be similar to those
described elsewhere. Firstly, domestic problems would
occur with high densities of the insect invading human
houses for overwintering, as it was the case in the pre-
sent study.
Secondly, impact on native or already established
ladybeetle species may also occur. The arrival of H.
axyridis is associated to drastic changes in coccinellid
assemblages all around the word (Colunga-Garcia
Gage, 1998; Michaud, 2002; Lucas et al., 2007a,b;
Pell et al., 2008; Bélanger Lucas, 2011; Roy et al.,
2012). Catalonia has a diverse agriculture dominated
by winter cereals, maize, alfalfa, vegetables in open
air and greenhouse, fruit orchards and vineyards. H.
axyridis has been reported in all of these crops over
Europe and America, as well as in urban landscapes.
For example, in Belgium, Vandereycken et al. (2013)
reported that maize is one of the crops most affected.
Some of the most abundant coccinellids in Spanish
arable crops (that is, C. septempunctata, H. varie-
gata and P. quatuordecimpunctata) move between
alfalfa, winter cereals and maize to follow aphid
populations and demonstrate clear patterns of relative
abundance (Pons Eizaguirre, 2009; di Lascio et al.,
unpublished data). In the present study, no H. axy-
ridis has been recorded in maize and alfalfa (two
crops where coccinellids are abundant) and this sug-
gests that the invasion of the Asian ladybeetle is re-
cent. However, the invasion of crop fields should be
promptly observed, as has happened in other coun-
tries, and all these three native coccinellids species
are showed to be in disadvantage intraguild predation
experiments with H. axyridis (Ware Majerus, 2008;
Lucas, 2012; Katsanis et al., 2013).
Spring and summer records from the present study
show that H. axyridis has already colonized urban
landscapes in Spain. In these environments, Oenopia
conglobata L., Adalia bipunctata L., A. decempunc-
tata, H. variegata and Scymnus sp. are the predom-
inant ladybeetle species (Lumbierres et al., 2005;
Pons Lumbierres, 2013). Since asymmetric in-
traguild predation in favor of the invader has been
reported for all the native ladybeetle species (Ware
Majerus, 2008; Brown et al., 2011b; Lucas, 2012;

Brown PMJ, Frost R, Doberski J, Sparks T, Harrington R,
Roy HE, 2011b. Decline in native ladybirds in response
to the arrival of Harmonia axyridis: early evidence from
England. Ecol Entomol 36: 231-240. http://dx.doi.
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Burgio G, Santi F, Lanzoni A, Masetti A, De Luigi V, Mel-
andri M, Reggiani A, Ricci C, Loomans AMJ, Maini S,
2008. Harmonia axyridis recordings in northern Italy. B
Insectol 61: 361-364.
Carbonell R, Sesma JM, 2013. Confirmada la presencia de
Harmonia axyridis (Pallas, 1773) en la Península Ibérica.
Primeras citas para Cataluña e Islas Baleares (Coleoptera:
Coccinellidae). BV news 16: 12-17.
Ceryngier PP, Havelka J. Hodek I, 2004. Mating and activ-
ity of gonads in pre-dormant and dormant ladybirds
(Coleoptera: Coccinellidae). Invert Repr Dev 45: 127-135.
http://dx.doi.org/10.1080/07924259.2004.9652582
Colunga-Garcia M, Gage SH, 1998. Arrival, establishment, and
habitat use of the multicolored Asian ladybeetle (Coleoptera:
Coccinellidae) in a Michigan landscape. Environ Entomol
27: 1574-1580. http://dx.doi.org/10.1093/ee/27.6.1574
Firlej A, Boivin G, Lucas E, Coderre D, 2005. First report
of parasitism of Harmonia axyridis parasitism by Dino-
campus coccinellae Schrank in Canada. Biol Invasions 7:
553-556. http://dx.doi.org/10.1007/s10530-004-5848-0
Firlej A, Lucas E, Coderre D, Boivin G, 2010. Impact of host
behavioral defenses on parasitization efficacy of a larval
and adult parasitoid. Biocontrol 55: 339-348. http://dx.doi.
org/10.1007/s10526-009-9262-5
Galvan TL, Koch RL, Hutchinson WD, 2008. Impact of fruit
feeding on overwintering survival of the multicolored Asian
lady beetle, and the ability of this insect and paper wasps
to injure wine grape berries. Entomol Exp Appl 12: 429-
436. http://dx.doi.org/10.1111/j.1570-7458.2008.00731.x
Goldazarena A, Calvo D, 2007. First record of Harmonia
axyridis (Coleoptera: Coccinellidae) from the Iberian
Peninsula. Bol Soc Entomol Aragonesa 41: 437-439.
Hodek I, Iperti G, Hodkova M, 1993. Long-distance flights
in Coccinellidae (Coleoptera). Eur J Entomol 90: 403-414.
Iperti G, Bertrand E, 2001. Hibernation of Harmonia axy-
ridis (Coleoptera: Coccinellidae) in South-Eastern France.
Acta Soc Zool Bohem 65: 207-210.
Jacas JA, Urbaneja A, Viñuela E, 2006. History and future
of introduction of exotic arthropod biological control
agents in Spain: a dilemma? BioControl 51: 1-30. http://
dx.doi.org/10.1007/s10526-005-5808-3
Katsanis A, Barbendreier D, Nentwig W, Kenis M, 2013.
Intraguild predation between the invasive ladybird Har-
monia axyridis and non-target European coccinellid spe-
cies. BioControl 58: 73-83. http://dx.doi.org/10.1007/
s10526-012-9470-2
Kenis M, Roy HE, Zindel R, Majerus MEN, 2008. Current
and potential management strategies against Harmonia
axyridis. BioControl 53: 235-252. http://dx.doi.
org/10.1007/s10526-007-9136-7
Koch RL, 2003. The multicolored Asian lady beetle, Har-
monia axyridis: A review of its biology, uses in biological
control, and non-target impacts. J Insect Sci 3: 1-16. http://
dx.doi.org/10.1673/031.003.3201
has successfully colonized drastically different coun-
tries and landscapes (Brown et al., 2008). In spite of
the different climatic conditions of Spain (oceanic in
north and west, continental in center, and Mediterra-
nean in northeast, east and south) we may expect the
invasion process to continue until colonization of the
complete country, even the sub-tropical area of south-
west Almería, Granada, Málaga) may be colonized
since H. axyridis was recently reported in Kenya
(Nedved et al., 2011). Furthermore, the relatively
warm Spanish climate would probably allow a higher
survival rate during winter, and would not act as a
barrier in absence of human houses such as in Canada
(Labrie et al., 2008).
In conclusion, the results of this paper show that H.
axyridis is already established in Spain and, although
until now is restricted to Catalonia, the invading pro-
cess is in progress.
Acknowledgements
We thank Carme Forcada and Montse Barniol for
allowing us to monitor the overwintering aggregation
in Les Llosses. We also thank Cristina Castañé, Mat-
ilde Eizaguirre, Ramon Albajes, Anaïs Lucas, Anna
Lleixà, Joan Gual, Filipe Madeira, David Pons and
Oscar Alomar for helping in sampling and the new
records advising and all the other colleagues and tech-
nical advisers who scouted the ladybird for us in other
regions of Spain.
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