Ten years of invasion: Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in Britain

Abstract

1. Harmonia axyridis was first recorded in Britain in 2004. Two subsequent earlier records were received from 2003.
2. The UK Ladybird Survey, a citizen science initiative involving online recording, was launched in 2005 to encourage people across Britain to track the spread of H. axyridis. Tens of thousands of people have provided records of H. axyridis and other species of ladybirds, creating an invaluable dataset for large-scale and long-term research. Declines in the distribution of seven (of eight assessed) native species of ladybird have been demonstrated, and correlated with the arrival of H. axyridis, using the records collated through the UK Ladybird Survey.
3. Experimental research and field surveys have also contributed to our understanding of the ecology of H. axyridis and particularly the process of invasion. Harmonia axyridis arrived in Britain through dispersal and introduction events from regions in which it was deliberately released as a biological control agent. The rapid spread of this species has been attributed to its high natural dispersal capability by means of both flight and anthropogenic transport. A number of factors have contributed to the successful establishment and indeed dominance of this polymorphic species within aphidophagous guilds, including high reproductive capacity, intra-guild predation, eurytopic nature, high resistance to natural enemies within the invaded range, and potentially phenotypic plasticity.
4. The global invasion by H. axyridis and subsequent research on this species has contributed to the general understanding of biological invasions.

Full text

For Review Only
Ten years of invasion:
Harmonia axyridis (Pallas)
(Coleoptera: Coccinellidae) in Britain
Journal:
Ecological Entomology
Manuscript ID:
14-0318-EEN.R2
Manuscript Type:
Invited Review
Date Submitted by the Author:
14-Feb-2015
Complete List of Authors:
Roy, Helen; Centre for Ecology & Hydrology, BRC
Brown, Peter; Anglia Ruskin University, Life Sciences
Keywords:
Biological invasions, citizen science, non-native species, invasive species,
intra-guild predation, monitoring and surveillance
Ecological Entomology

For Review Only
Ten years of invasion: Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in Britain 1
Helen E. Roy
1
and Peter M.J. Brown
2
2
3
1
Centre for Ecology & Hydrology, Benson Lane, Wallingford, Oxfordshire, OX10 8BB, UK 4
2
Animal and Environment Research Group, Life Sciences Department, Anglia Ruskin University, East 5
Road, Cambridge, CB1 1PT, UK 6
7
Abstract. 1. Harmonia axyridis was first recorded in Britain in 2004. Two subsequent earlier records 8
were received from 2003. 9
2. The UK Ladybird Survey, a citizen science initiative involving on-line recording, was launched in 10
2005 to encourage people across Britain to track the spread of H. axyridis. Tens of thousands of 11
people have provided records of H. axyridis and other species of ladybirds which provides an 12
invaluable dataset for large-scale and long-term research. Declines in the distribution of seven (of 13
eight assessed) native species of ladybird have been demonstrated, and correlated with the arrival 14
of H. axyridis, using the records collated through the UK Ladybird Survey. 15
3. Experimental research and field surveys have also contributed to our understanding of the 16
ecology of H. axyridis and particularly the process of invasion. Harmonia axyridis arrived in Britain 17
through dispersal and introduction events from regions in which it was deliberately released as a 18
biological control agent. The rapid spread of this species has been attributed to its high natural 19
dispersal capability by means of both flight and anthropogenic transport. A number of factors have 20
contributed to the successful establishment and indeed dominance of this polymorphic species 21
within aphidophagous guilds, including high reproductive capacity, intra-guild predation, eurytopic 22
nature, high resistance to natural enemies within the invaded range and potentially phenotypic 23
plasticity. 24
4. The global invasion by H. axyridis and subsequent research on this species has contributed to our 25
general understanding of biological invasions. 26
27
Key words. Biological invasions, citizen science, intra-guild predation, invasive species, monitoring 28
and surveillance, non-native species. 29
30
Running title. Ten years of the harlequin ladybird invasion 31
32
Page 1 of 28 Ecological Entomology

For Review Only
33
Introduction 34
The first British record of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), the harlequin 35
ladybird, was from Sible Hedingham, Essex, England in 2004 (Majerus et al., 2006). Widely 36
introduced across continental Europe as a biological control agent of aphids it had never been 37
intentionally introduced into Britain (Brown et al., 2008a). However, it was perhaps inevitable that 38
individuals from the introduced populations in Europe would arrive in Britain because H. axyridis has 39
excellent dispersal abilities (Brown et al., 2008b, Jeffries et al., 2013). 40
41
The first record of H. axyridis within Britain, alongside the rapid spread of this species elsewhere in 42
Europe, triggered a number of responses: 43
1. Rapid development of on-line recording and the launch of the UK Ladybird Survey including the 44
Harlequin Ladybird Survey (encompassing the Biological Records Centre (BRC) hosted Coccinellidae 45
Recording Scheme). 46
2. Research collaborations across Europe through the establishment of a working group “Risks and 47
benefits of exotic biological control agents” within the International Organisation for Biological and 48
Integrated Control (IOBC). 49
3. Publication of a review within Ecological Entomology outlining potential impacts of the arrival of 50
H. axyridis (Majerus et al., 2006). 51
52
The review published within Ecological Entomology (Majerus et al., 2006) outlined a number of 53
predictions (Table 1) and provided a framework for research specifically within Britain but with 54
relevance across Europe and beyond. Indeed H. axyridis was noted as providing “entomologists 55
with a unique and exciting opportunity to monitor the spread and impacts of an invasive alien insect 56
in British environments that might prove a timely model study for future ecological impact 57
assessments.” The long history of invasion of H. axyridis in America was highlighted in the review 58
and it was recognised that there was much to be gained from comparative studies building on the 59
research findings available from America (Koch and Galvan, 2008). 60
61
Harmonia axyridis has been the inspiration and focus of research across the globe (Sloggett, 2012, 62
Sloggett, 2005). Indeed 19 papers were published in a special issue of the journal BioControl as a 63
result of the collaboration through the IOBC working group “Risks and benefits of exotic biological 64
control agents” (Roy and Wajnberg, 2008). These publications have been widely cited and 65
demonstrate the collaborative approach to research on H. axyridis. Here we provide an overview of 66
Page 2 of 28Ecological Entomology

For Review Only
research findings, particularly in Britain, over the last ten years. We highlight the contributions made 67
through research on H. axyridis to the field of invasion biology, focussing on predictions from 68
Majerus et al. (2006); the manuscript has been structured to align with the review (Majerus et al., 69
2006). 70
71
Factors affecting the population demography of Harmonia axyridis in Britain 72
The records of H. axyridis received through the UK Ladybird Survey have enabled the spread of this 73
invader to be documented from early in the invasion process (Brown et al., 2008b). The considerable 74
media attention in response to immediate notification of the arrival of H. axyridis in England led to 75
approximately 100 verified records of the species from September to December 2004. These 76
records were mainly from the south-east of England, with many from coastal areas, and only three 77
outlying 10 km squares recorded in northern England (Brown et al., 2008b). Harmonia axyridis 78
spread west and north within Britain, with the northerly spread rate from 2004-08 calculated as 105 79
km year
-1
(Brown et al., 2008b) and by 2009 was recorded in 1022 10-km squares encompassing all 80
regions of England and Wales, with approximately 75% of 10-km squares within the invaded range 81
having verified records (Figure 1). 82
83
Eurytopic nature 84
Harmonia axyridis is highly eurytopic in Britain, thriving in a wide range of habitats, as predicted by 85
Majerus et al. (2006). It is particularly successful in urban localities, spreading faster into areas 86
containing a high proportion of urban land (Purse et al., 2014). The species also thrives in rural 87
locations; based on UK Ladybird Survey data, 19% of the 1km squares with H. axyridis records were 88
predominantly arable or horticultural land (Brown, 2010). The population dynamics of H. axyridis in 89
crop systems (wheat, corn, broad bean and potato crops) have been studied in Belgium and indicate 90
that H. axyridis arrives 7-8 days after the dominant native coccinellids (Jansen and Hautier, 2008, 91
Vandereycken et al., 2013). A one year study (2008) involving field observations in wheat and bean 92
crops within southern England reported an absence of H. axyridis in wheat (aphid abundance was 93
reported as low) but presence of H. axyridis co-occurring with other coccinellids in bean crops 94
(Wells, 2011).
Harmonia axyridis was the most common aphid enemy species in bean crops and
95
the presence of this species was correlated with aphid abundance (Wells, 2011).
96
97
In Britain, 5% of H. axyridis records were from 1km squares dominated by woodland (mostly 98
broadleaved or mixed). The percentages of records submitted to the UK Ladybird Survey from 99
various vegetation types were: deciduous trees and shrubs 56%; herbaceous plants 29%; evergreen 100
Page 3 of 28 Ecological Entomology

For Review Only
trees and shrubs 11%; grasses and others 4% (Brown, 2010). Indeed H. axyridis has been recorded 101
from more than 75 plant families, dominated by Aceraceae (14% of records with associated plant 102
data), Rosaceae (13%) and Malvaceae (10%) (Brown, 2010). Larvae of the species were recorded 103
from about 50 of these families (Brown et al., 2011a), notably Aceraceae (22% of records with 104
associated plant data), Malvaceae (18%), Rosaceae (10%) and Urticaceae, Betulaceae and Salicaceae 105
(5% each) (Brown, 2010). Thus in Britain H. axyridis thrives on deciduous trees and shrubs such as 106
limes, maples, birches and roses, as well as on a variety of herbaceous plants, including stinging 107
nettle. Similar patterns of host plant association have been observed in other regions of Europe 108
(Panigaj et al., 2014, Roy et al., 2012). Records of H. axyridis from coniferous trees in Britain are 109
quite limited, unlike in parts of its native range (Brown et al., 2011a). 110
111
The widespread distribution of H. axyridis in the UK reflects the eurytopic nature of this species. 112
Indeed the ability of H. axyridis to thrive in association with a diverse range of host plants 113
undoubtedly explains the observed breadth of habitat types occupied by H. axyridis. A recent study 114
on the spread of H. axyridis, including consideration of landscape factors, suggests that coniferous 115
woodland, after correcting for bias in recording intensity, may negatively affect the spread of this 116
species (Purse et al., 2014). Currently there is limited information within the UK Ladybird Survey 117
database on specific plant associations, indeed this is mainly found within comments fields and so 118
requires considerable work to extract (Brown, 2010). Further developments of the UK Ladybird 119
Survey will include capturing information on plant associations as defined data fields within the on-120
line recording forms to enable future research on ecological networks. 121
122
Climate 123
Climatic conditions have not been a barrier to the colonization and spread of H. axyridis in southern 124
Britain, but are speculated to have limited its abundance in northern England and in Scotland (Brown 125
et al., 2008b). In these northern areas, records of successful breeding by H. axyridis are very limited. 126
Climatic modelling studies have indicated that nearly all of mainland Britain is suitable for H. axyridis, 127
with the exception of northern Scotland (Poutsma et al., 2008). The model proposed by Poutsma et 128
al. (2008) has proven to be a good predictor of the expanding distribution of H. axyridis in Europe 129
(Brown et al., 2011b) but the parameters used may need slight refinement to include observations 130
on distribution from the UK Ladybird Survey. The combination of lower temperatures and higher 131
precipitation in Scotland compared to England appears to restrict H. axyridis to warm urban 132
localities within Scotland, especially in terms of successful reproduction. The Orkney Islands and 133
Shetland Islands (off the north-west coast of Scotland) are indicated as climatically unsuitable for H. 134
Page 4 of 28Ecological Entomology

For Review Only
axyridis (Poutsma et al., 2008); whilst there have been isolated records of individual adults from 135
these northern islands, these ladybirds seem to have arrived on produce imported from the 136
mainland (Ribbands et al., 2009) and there are no records here of juveniles of H. axyridis, or indeed 137
of any other coccinellid species. 138
139
The most northerly record of H. axyridis in Europe is from Trondheim, Norway (Saethre et al., 2010), 140
substantially further north than the Shetland Islands, but Oslo appears to be the most northerly 141
location where H. axyridis has become established. Majerus et al. (2006) predicted that climate 142
change may provide H. axyridis with a further competitive advantage over native British coccinellids. 143
Predictions from modelling approaches suggest that H. axyridis may indeed benefit from climate 144
warming through further northward expansion (Purse et al., 2014) and increased voltinism is also 145
possible. As in parts of its native range such as Japan (Osawa, 2011), H. axyridis is multivoltine in 146
Britain and usually completes two generations per year (Brown et al., 2008b) (Figure 2). Larval peaks 147
are in June and October and there is the potential for three generations in particularly favourable 148
years. Records of larvae in late December (winter) are not unusual. The resultant high population 149
pressure is presumed to encourage higher rates of dispersal for the species compared to native, 150
univoltine species. 151
152
While climate models in part explain the distribution of H. axyridis within the invaded range, there 153
are clear discrepancies between the observed and predicted distributions of H. axyridis. There are, 154
of course, many factors that influence the invasion process and the distribution of species over time. 155
Indeed, the interactions between landscape factors, climate and species traits (such as 156
polymorphism) in determining the distribution of ladybirds are complex (Comont et al., 2014a). 157
158
Summarising, the apparent lack of success of H. axyridis in Scotland could be attributed to a number 159
of factors: 160
(i) Biogeographic features such as mountain ranges may act as barriers to species dispersal and 161
invasion (Wilson et al., 2009). Such barriers to H. axyridis in Britain include the Cambrian mountains 162
(Wales) and particularly the Pennine mountains (northern England) (Brown et al., 2011b). The 163
reasons why mountains may block dispersal are effectively encompassed within habitat and climatic 164
limitations (see below). 165
(ii) Habitat factors such as soil type, land use and vegetation type have a direct effect on ladybird 166
prey species and therefore an indirect effect on ladybird populations (Comont et al., 2014a). 167
Eurytopic ladybirds such as H. axyridis tend to thrive in habitats (such as arable and urban) with high 168
Page 5 of 28 Ecological Entomology

For Review Only
prey abundance. In less favourable habitats such as those at higher altitudes (principally moorland 169
and heathland in Britain) H. axyridis is found at lower densities, if at all. 170
(iii) The cooler and wetter climate typical of northern and upland regions of Britain is less favourable 171
to many predatory insect species and their prey. Whilst the native range of H. axyridis includes 172
southern Siberia, with very cold winter temperatures (e.g. mean January temperatures of -13°C 173
(daily high) to -18°C (daily low) in Novosibirsk), it may be the combination of wet conditions with 174
cold temperatures that is particularly unfavourable for H. axyridis in Scotland. Native ladybirds tend 175
to be much lower in both species number and abundance in Scotland than in England; indeed, in 176
Scotland 25 of the 46 resident British coccinellid species are either absent or occur very rarely (Roy 177
et al., 2011a). 178
(iv) Lower human population density in Scotland compared to England and Wales could partially 179
explain the low number of records in Scotland. This places a potential bias on our dataset, as clearly 180
we would expect to receive fewer records from less populated areas. However, there are many 181
10km within Scotland with high numbers of records of other species of ladybird suggesting that the 182
level of recording intensity is sufficient to derive a robust assessment of the distribution of H. 183
axyridis throughout Britain. 184
185
There is still much to reveal about the spread of H. axyridis and it is important to recognise that 186
invasions are dynamic processes. The UK Ladybird Survey dataset has been used in many studies 187
exploring the interactions between abiotic and biotic factors in determining the distribution of 188
ladybirds (Comont et al., 2014a, Brown, 2010, Brown et al., 2008b, Purse et al., 2014) and 189
demonstrates the huge value of such citizen science initiatives for continued analysis of large-scale 190
and long-term ecological processes. 191
192
Phenotypic adaptability 193
There have been some intriguing insights into the phenotypic adaptability of H. axyridis over the last 194
ten years. Perhaps the most compelling evidence of phenotypic adaptability is in relation to colour 195
pattern polymorphism. Harmonia axyridis is a polymorphic species for both the pattern and colour 196
of the pronota and elytra (Majerus et al., 2006). Three main colour morphs have been reported in 197
Britain: f. succinea, f. spectabilis and f. conspicua. Additionally there are a few records of f. equicolor 198
and f. aulica; the nominate form – f. axyridis – has not been reported in Britain. The non-melanic f. 199
succinea is the most abundant colour form and comprises approximately 80% of records (Brown et 200
al., 2008b, Purse et al., 2014). The influence of temperature on f. succinea is intriguing; individual H. 201
axyridis f. succinea (non-melanic) eclosing from pupae late in the year have larger spots than those 202
Page 6 of 28Ecological Entomology

For Review Only
eclosing in spring and early summer (Michie et al., 2010). Recent research has indicated that the 203
phenotypic plasticity displayed by H. axyridis enables local adaptation at temporal and spatial scales 204
(Michie et al., 2010), whereby melanism, which may be important in thermoregulation (Brakefield 205
and de Jong, 2011), is considered costly in summer and beneficial in winter (Michie et al., 2010). 206
Michie et al. (2011) proposed that melanisation may have accelerated the spread of H. axyridis. 207
208
Modelling approaches using the UK Ladybird Survey dataset have explored the prediction that 209
melanic colour forms have a thermal regulatory advantage and consequently spread more rapidly 210
than the non-melanic colour form (Purse et al., 2014). It was apparent that while increased sunshine 211
significantly enhanced the spread of the non-melanic form (f. succinea), the spread was more rapid 212
within hectads containing a high proportion of urban land cover and marginally slower in hectads 213
containing high conifer cover (Purse et al., 2014). Additional recent research suggests that the colour 214
pattern polymorphism of H. axyridis and variation in other life-history traits could contribute to the 215
invasion success of this species (Majerus et al., 2006, Purse et al., 2014, Michie et al., 2010). 216
217
There have been a number of studies exploring the influence of life-history traits on the distribution 218
of coccinellids including H. axyridis (Comont et al., 2014a, Comont et al., 2012). The traits database 219
compiled for these studies provides a rare opportunity to explore variation in life-history traits 220
between species. Indeed it has been insightful to include information on species traits alongside the 221
distribution data from the UK Ladybird Survey to explain trends in the distribution patterns of 222
ladybirds in Britain (Comont et al., 2014a). Climate and habitat datasets available for Britain have 223
added further value to these analyses (Comont et al., 2014a). It would be fascinating to extend this 224
research beyond Britain to consider life-history traits in a biogeographic context. Additionally, 225
modelling approaches enable eloquent exploration of large-scale and long-term datasets to test 226
predictions and ultimately construct further hypotheses. Detailed empirical approaches are required 227
to examine the mechanisms at play. 228
229
Dispersal potential 230
The rapid spread of H. axyridis has been a consequence of both natural dispersal by flight and 231
anthropogenic processes. Recent research using innovative research tools, namely vertical-looking 232
entomological radar, have provided intriguing insights into the flight patterns of H. axyridis . 233
Harmonia axyridis and C. septempunctata were detected at 1100 m above ground level moving at 60 234
km/h and sustaining flight for up to two hours, indicating a high capacity for long-distance dispersal . 235
236
Page 7 of 28 Ecological Entomology

For Review Only
Much of Britain is densely populated and has an elaborate transport network, and there are many 237
reports of H. axyridis being transported accidentally in or on vehicles. Inadvertent movement with 238
people and goods has undoubtedly facilitated the spread of the species in Britain. For example, in 239
2007 H. axyridis was first recorded from Scotland (Holroyd et al., 2008) as a result of the ladybird 240
being transported in a suitcase; the first record from the Orkney islands (northern Scotland) (2008) 241
(Ribbands et al., 2009) and from Northern Ireland (2007) (Murchie et al., 2008) involved the 242
ladybirds being transported with vegetables from mainland Britain. The most noticeable record in 243
this regard is that of the population that was initiated by transport of ladybirds to a supermarket in 244
Derby (north-central England) in 2004. The beetles spread rapidly from there and are likely to have 245
accelerated the northerly spread of the species from 2005. 246
247
Natural enemy interactions 248
Natural enemy escape provides an appealing hypothesis for explaining the success of an invader 249
(Roy et al., 2011b). The Enemy Release Hypothesis (ERH) (Elton, 1958, Torchin et al., 2003) predicts 250
that an alien species will be less affected by specialised natural enemies (predators, parasites and 251
pathogens) than will native species. Thus, the alien gains a competitive advantage and may rapidly 252
increase in abundance and distribution (Elton, 1958, Torchin et al., 2003, Colautti et al., 2004). The 253
premise of this theory is that natural enemies are important in regulating populations (Roy and 254
Lawson Handley, 2012) but the empirical evidence for this and consequently the ERH is limited (Roy 255
et al., 2011b, Roy and Cottrell, 2008). There have been some advances in understanding the role of 256
natural enemies in the H. axyridis invasion over the last ten years (Kenis et al., 2008, Comont et al., 257
2014b, Roy et al., 2013). 258
259
Arguably the most important natural enemies of ladybirds in Britain are pathogens (such as 260
Beauveria bassiana) and several species of endoparasitic Hymenoptera and Diptera (Roy et al., 2013, 261
Roy et al., 2011a, Comont et al., 2014b, Ceryngier et al., 2012). There were early indications that 262
some of the ladybird natural enemies native to Britain would attack H. axyridis (Ware et al., 2010, 263
Hall et al., 2009) but laboratory studies indicated the low susceptibility of this invader in comparison 264
to native species (Koyama and Majerus, 2008, Roy et al., 2008b). Laboratory research indicates that 265
H. axyridis is an unfavourable host for Dinocampus coccinellae (Schrank) (Hymenoptera: Braconidae) 266
(Berkvens et al., 2010b, Hoogendoorn and Heimpel, 2002). The exact mechanism involved in the 267
resistance of H. axyridis to D. coccinellae is unclear but teratocyte cells produced by D. coccinellae 268
(involved in both immunosuppression of the host and nutrition of the parasitoid) follow an abnormal 269
pattern of growth within H. axyridis which could explain the impeded development of D. coccinellae 270
Page 8 of 28Ecological Entomology

For Review Only
within this invader (Firlej, 2012). The fungal pathogen B. bassiana commonly infects native species of 271
ladybird (such as C. septempunctata) but again H. axyridis appears to be highly resistant (Roy et al., 272
2008b). A recent study also demonstrated that H. axyridis individuals contain high numbers of 273
obligate parasitic microsporidia which appear to have no adverse affects on H. axyridis but cause 274
high mortality when artificially injected into C. septempunctata (Vilcinskas et al., 2013). The 275
ecological relevance of this study requires further investigation because injection is an artificial 276
process and far removed from the natural mechanisms involved in microsporidia transmission . 277
278
Clearly there is a need to extend studies of natural enemies to the field in order to ensure ecological 279
relevance. One recent study from Britain confirmed low rates of parasitism of
H.
axyridis, 280
particularly in comparison to the native C. septempunctata (Comont et al., 2014b). Indeed, pupae of 281
H. axyridis were parasitized, primarily by Phalacrotophora fasciata (Fallén) and Phalacrotophora 282
berolinensis Schmitz (Diptera: Phoridae), at an exceptionally low level (1.73%) and adults were not 283
found to be parasitized at all in this study. In contrast, parasitism of the co-occurring C. 284
septempunctata was high (20.91% pupae, 5.67% adults). This provides evidence in support of the 285
ERH, i.e. success of the invader may result from a reduction or absence of natural enemies (Elton, 286
1958, Torchin et al., 2001). However, further work is required to elucidate population-level effects 287
of this difference in parasitism rates between the alien and native species. There is no doubt that H. 288
axyridis represents an excellent opportunity to explore natural enemy interactions and their role in 289
the invasion process. 290
291
Impacts 292
Benefits as a pest control agent 293
There has been little focus in Britain on the role of H. axyridis as a beneficial pest control agent 294
(Wells, 2011). The effects of H. axyridis on aphid populations in British crop systems are unknown 295
and are worthy of further investigation, particularly with respect to ecosystem services and 296
resilience (Koch and Galvan, 2008, Vilà et al., 2009). 297
298
Negative effects on pest and non-pest herbivorous insects 299
Harmonia axyridis has a wide diet breadth (reviewed by Hodek and Evans, 2012) and in the absence 300
of aphids can complete development on a combination of other foods including coccids, adelgids, 301
psyllids and many other insects including conspecifics (Tedders and Schaefer, 1994, Majerus et al., 302
2006, Koch, 2003, Onofre Soares et al., 2005, Flowers et al., 2005, Hodek and Evans, 2012)
but also 303
Ephestia kuehniella (Lepidoptera: Pyralidae) eggs (Berkvens et al., 2010a) and pollen (Berkvens et al., 304
Page 9 of 28 Ecological Entomology

For Review Only
2008, Berkvens et al., 2010a). Therefore, H. axyridis is predicted to pose a threat to many species 305
(Roy et al., 2009). However, there have been few studies exploring the population-level effects of H. 306
axyridis on non-target herbivorous insects. One study recognised the potential for H. axyridis to 307
negatively affect monarch butterflies, Danaus plexippus (L.) (Lepidoptera: Nymphalidae), in the US 308
(Koch et al., 2003). Within the UK Ladybird Survey database there are records of H. axyridis 309
predating lepidopterans (such as the eggs of noctuid moths) in Britain, but the extent of such 310
predation is unknown. Further research is required to examine the population dynamics of these 311
interacting species. It is also important to note that H. axyridis is not unique amongst the 312
coccinellids in having a wide diet breadth (Sloggett, 2012). 313
314
Negative effects on other aphidophages 315
Harmonia axyridis is widely recognised as a top predator within aphidophagous guilds (Pell et al., 316
2008). However, as highlighted by Majerus et al. (2006) the negative effects of H. axyridis are likely 317
to be the result of a complex range of interactions, with H. axyridis having a competitive edge 318
through resource competition, intra-guild predation (IGP) and a more plastic phenotype than other 319
aphidophagous species. There have been many published studies exploring such interactions, 320
particularly IGP, and to a lesser extent, competition (Phoofolo and Obrycki, 1998, Ware et al., 2009). 321
Initially these were mostly small-scale laboratory studies of ladybird interactions within Petri dishes 322
which demonstrated strong asymmetric IGP in favour of H. axyridis over native ladybirds (Ware and 323
Majerus, 2008, Ware et al., 2008, Roy et al., 2008a, Pell et al., 2008). In contrast it is apparent that in 324
such Petri dish experiments Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) is an intra-325
guild predator of H. axyridis (Nedvěd et al., 2013), but in mesocosm experiments IGP was in favour 326
of H. axyridis over C. carnea (Wells, 2011). 327
328
Understanding of intra-guild interactions has progressed by increasing the scale with the use of 329
more realistic experimental arenas than Petri dishes. Mesocosm studies have included interactions 330
between coccinellids and non-coccinellid aphidophages such as neuropterans (Wells et al., 2010, 331
Wells, 2011) and syrphids (Ingels and De Clercq, 2011). Such approaches to exploring IGP are critical 332
for informing risk assessment by enabling rapid assessment of interactions for a range of potential 333
prey species and different life stages of both the intra-guild predator and prey. Additionally, 334
assessing the effects of aphid density on IGP provides additional context to the experiments (Wells, 335
2011, Ware et al., 2009) but results so far suggest that the prevalence of IGP is not reduced by 336
increased aphid density (Wells, 2011). However, extrapolating findings from laboratory studies to 337
the field is challenging and many questions remain with respect to the ecological relevance of IGP. 338
Page 10 of 28Ecological Entomology

For Review Only
Molecular tools provide exciting opportunities for investigating community interactions in the field 339
(Roy and Lawson Handley, 2012). Analyses using the polymerase chain reaction (PCR) have been 340
used to detect prey DNA from the guts of field-collected H. axyridis samples. Initial work in Britain 341
assessed larval gut contents for two intra-guild prey - Adalia bipunctata (L.) (Coleoptera: 342
Coccinellidae) and A. decempunctata (L.) (Coleoptera: Coccinellidae) and both were detected within 343
H. axyridis (Thomas et al., 2013). This work was extended to investigate predation of neuropterans 344
and syrphids by H. axyridis with testing of samples from five European countries (Brown et al., 2014). 345
Through this study it was apparent that while syrphids were detected in the gut of H. axyridis, 346
neuropterans were not. Gas chromatography-mass spectrometry (GC-MS), has been used in 347
mainland Europe for detection of ladybird IGP and revealed similar results (Hautier et al., 2011). 348
349
The taxonomic breadth of studies demonstrating IGP by H. axyridis supports the contention that H. 350
axyridis is an aggressive coccinellid with a tendency for intra-guild predation that could seriously 351
affect the abundance of native coccinellids and dramatically reduce their available niches in the 352
predator complex (Elliott et al., 1996). Furthermore, observations from the UK Ladybird Survey (Roy 353
et al., 2012) highlight the potential for H. axyridis to dramatically disrupt native guilds in Britain 354
(Majerus et al., 2006). However, further understanding of the implications of IGP by H. axyridis on 355
ecological resilience and function should be prioritised. Recent research from America found no 356
evidence that H. axyridis consumed coccinellid eggs in the field but suggested that exploitative and 357
apparent competition might explain declines of native species in the presence of H. axyridis (Smith 358
and Gardiner, 2013). There is an urgent need for detailed field studies to quantitatively document 359
the interactions between invaders and other species within the community. Ecological network 360
analysis provides exciting opportunities for detailed exploration of the complex interactions across 361
the aphidophagous community (Roy and Lawson Handley, 2012). It will be particularly intriguing to 362
explore the concept of ecological resilience and extend research on ecological networks to 363
consideration of other invaded systems (Romanuk et al., 2009). 364
365
Negative effects on humans 366
Overwintering aggregations of H. axyridis have undoubtedly been one of the most notable aspects of 367
invasion by this species. Many people report sightings from their houses during autumn and winter 368
to the UK Ladybird Survey, with the annual peak of records generally being in late October and early 369
November. Many people have reported problems associated with overwintering aggregations of H. 370
axyridis, specifically staining of soft furnishings and unpleasant smell associated with the secretion of 371
reflex blood. There have been observations of thousands of individuals within houses and the bell 372
Page 11 of 28 Ecological Entomology

For Review Only
towers and porches of churches (Roy et al., 2011a). However the impacts on people, beyond a 373
minor nuisance, are limited within Britain. Allergic reactions to H. axyridis are rare (Goetz, 2008) but 374
there have been a few reports of such reactions within Britain. 375
376
In wine growing regions of North America H. axyridis has attained the status of a pest (Koch et al., 377
2004, Koch and Galvan, 2008). This is not the case for all vineyard owners, some of whom have 378
looked on its appearance in their (British) vineyards favourably (DeCourcy, 2009), despite concerns 379
elsewhere over negative effects on wine production (Galvan et al., 2008). There are no known 380
reports of negative impacts in vineyards in Britain, where grape-growing is rare. Harmonia axyridis 381
has a tendency to aggregate on soft fruits including grapes and exacerbates damage through 382
feeding, but also contaminates the crop because it is difficult to separate the beetles at harvest. The 383
tainting caused by H. axyridis crushed with the grapes is problematic. However, recently concerns 384
have been raised that it is not just H. axyridis that causes such problems in North America but also C. 385
septempunctata, native to Britain but an alien species within North America (Botezatu et al., 2013). 386
Both H. axyridis and C. septempunctata contribute alkyl methoxypyrazines, and particularly isopropyl 387
methoxypyrazine, to wine at concentrations that are considered to have a negative impact on wine 388
quality (Botezatu et al., 2013). Although there are no effective and recommended control strategies 389
available for H. axyridis (Kenis et al., 2008), there are indications that sulphur dioxide (in the form of 390
potassium metabisulphite) a commonly used antimicrobial and antioxidant in wine production, 391
repels H. axyridis from grape vines (Glemser et al., 2012). 392
393
Potential control strategies 394
Methods for controlling the spread of H. axyridis have been proposed (Kenis et al., 2008). Harmonia 395
axyridis produces an aggregation pheromone to attract other individuals to overwinterwing habitats 396
(Verheggen et al., 2007). The use of the aggegration pheromone within a networks of traps has been 397
proposed and could potentially work at a local scale (such as within a vineyard where preventing H. 398
axyridis from aggregating within bunches of grapes would be advantageous). However, at a large 399
scale there would be practical implications that would render this approach unfeasible; a very large 400
number of traps would be needed and the costs involved in managing the traps would be 401
prohibitively high. 402
403
There are a number of natural enemies of H. axyridis that could potentially exert control but 404
population-level effects of natural enemies on the regulation of ladybirds is poorly understood 405
(Comont et al., 2014b, Roy et al., 2011c). Additionally, as outlined above, studies on the interactions 406
Page 12 of 28Ecological Entomology

For Review Only
between H. axyridis and natural enemies strongly indicate that H. axyridis is less susceptible to 407
attack by native parasitoids and pathogens than are native ladybirds, although this may change in 408
the future. The ectoparasitic mite Coccipolipus hippodamiae (McDaniel & Morrill) (Acarina: 409
Podapolipidae) naturally occurs in Europe and causes sterility in female H. axyridis (Rhule et al., 410
2010). Therefore, this mite has been considered as a biological control candidate (Rhule et al., 2010). 411
However, some native ladybird species are also susceptible to the mite. Whilst H. axyridis may be 412
more susceptible because of the nature of its life cycle, rigorous risk assessments would be needed 413
before any artificial releases of the mite are considered (Rhule et al., 2010), and in our opinion the 414
mite represents a control strategy that is too risky. 415
416
Implications for invasion biology 417
Harmonia axyridis was speculated as a model species for understanding invasion (Roy and Wajnberg, 418
2008). The unified framework for invasion biology proposed by Blackburn et al. (2011) recognises 419
that the invasion process can be considered as discrete stages and that there are barriers which a 420
species must overcome to establish and subsequently spread. There are many ways in which 421
research on invasion by H. axyridis has provided evidence to underpin mechanisms of invasion 422
(Table 2). From the transport of this invader beyond the limits of its native geographic range to the 423
dramatic spread of this species within the invaded range, there has been extensive ecological 424
research documenting the processes and exploring the underlying mechanisms of invasion. 425
However, there are still many knowledge gaps and ways in which H. axyridis can contribute to our 426
understanding of invasion biology. 427
428
Future directions: the next ten years 429
The arrival of H. axyridis in Britain was met with trepidation; indeed in the press release announcing 430
the arrival of H. axyridis Professor Michael Majerus described this species as “the most invasive 431
ladybird on Earth”. The dramatic spread of H. axyridis suggests it is one of the fastest spreading 432
invaders worldwide and worthy of this description. However, H. axyridis has successfully been used 433
as a model invasive alien species and has been the inspiration for global collaborations; the last 434
decade of research is indicative of the enthusiasm and commitment of many invasion biologists. 435
Nevertheless there is scope to expand the collaborations, particularly to increase the breadth of 436
parallel studies conducted in the native and invaded regions. A recent symposium on H. axyridis in 437
China (International Congress on Biological Invasions, Qingdao, 23rd – 27th October 2013)
438
highlighted the willingness for such global collaboration and the insights that can be gained from 439
scientists working across Asia. 440
Page 13 of 28 Ecological Entomology

For Review Only
441
There have been an impressive number of studies on H. axyridis over the last ten years that have 442
provided mechanistic evidence (Table 1) alongside models explaining large-scale patterns and 443
processes. The potential of IGP as an important force structuring aphidophagous communities has 444
been highlighted, but understanding of the ecological relevance of IGP across complex networks of 445
species is lacking. Additionally, the relative importance of competition and IGP should be assessed, 446
indeed it is thought that competitive interactions might be more important than IGP in driving 447
declines of native species (Smith and Gardiner, 2013). The numerical dominance of H. axyridis in 448
many habitats across Britain is evident but the effects of the species on ecosystem function are 449
unclear. There are clear indications that H. axyridis is escaping natural enemies within the invaded 450
range but over the next ten years it would seem plausible that the natural enemies will begin to 451
adapt. Indeed H. axyridis represents an abundant resource for parasites and pathogens. 452
453
Harmonia axyridis has provided unique and detailed insights into invasion biology over the decades 454
and the demand for scientific evidence to underpin invasion biology will undoubtedly be high over 455
the next ten years. In recent years the European Commission (EC) has intensified its commitment to 456
provide a comprehensive and manageable solution to invasive alien species in Europe. A European 457
Union (EU) Regulation http://eur-lex.europa.eu/legal-458
content/EN/TXT/?qid=1417443504720&uri=CELEX:32014R1143 has recently been adopted. 459
Scientifically robust risk assessments, as laid down in the Regulation, will be essential. The number 460
of records of H. axyridis received by the UK Ladybird Survey demonstrates the critical role that 461
people can play in alien species surveillance. Such surveillance is critical to strategies for early-462
warning and rapid response. A recent horizon scanning exercise has highlighted the species most 463
likely to arrive, establish and threaten biodiversity within the next ten years and the top 30 species 464
includes six terrestrial invertebrates (Roy et al., 2014). 465
466
Acknowledgements 467
The late Professor Michael Majerus was instrumental in the establishment of the Harlequin Ladybird 468
Survey and encouraged so many people around the world in their entomological research. We are 469
extremely grateful to the thousands of people who have shared their ladybird observations over the 470
years and contributed so richly to our ecological understanding. The UK Ladybird Survey is hosted by 471
the Biological Record Centre, which receives support from both the Natural Environment Research 472
Council and the Joint Nature Conservation Committee. The IOBC Working Group “Risks and Benefits 473
of Exotic Biological Control Agents” and the COST Action TD1209 “Alien Challenge” have facilitated 474
Page 14 of 28Ecological Entomology

For Review Only
discussions and collaborations on H. axyridis. We thank the editor and anonymous reviewers for 475
their helpful suggestions. Finally we thank Ecological Entomology for publishing “The potential 476
impacts of the arrival of the harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera : 477
Coccinellidae), in Britain” (Majerus et al., 2006) which inspired this review. 478
479
Page 15 of 28 Ecological Entomology

For Review Only
480
Page 16 of 28Ecological Entomology

For Review Only
Table 1. Predictions following the arrival of H. axyridis in the UK (Majerus et al., 2006) alongside a summary of recent evidence, supporting references and 481
overall conclusions, based on current understanding, with respect to the importance of factors in determining success of invasion by this species (+ 482
indicates important factor; - indicates unimportant; ? indicates undecided). 483
Prediction
Evidence
References
Conclusion
Eurytopic nature of
H. axyridis
will
contribute to rapid spread
The range of host plant associ
ations and widespread distribution of
H.
axyridis in the UK reflects the eurytopic nature of this species although
coniferous woodlands may negatively affect the spread of H. axyridis.
Habitat breadth is an important factor contributing to the invasion success
of H. axyridis.
(
Brown et al.,
2008b, Brown et
al., 2011a)
+
Climatic adaptability of
H. axyridis
will give it a competitive advantage over
some of the more niche-specific native
ladybirds
Climatic conditions have not been a barrier to the colonization and spread of
H. axyridis in southern Britain, but are speculated to have limited its
abundance in northern England and in Scotland.
There are clear discrepancies between the observed and predicted (climate
model) distributions of H. axyridis, it is apparent that climate is an
important factor in determining the spread of this species but alongside
other interacting biotic and abiotic factors.
(
Purse et al., 2014
,
Comont et al.,
2012)
+ / ?
Maritime climate o
f Britain will allow
H. axyridis to breed throughout the
summer, with no requirement for a summer
dormancy
Continual breeding of this species is apparent and at least two generations
of H. axyridis have been observed each year since arrival.
Multivoltinism contributes to the rapid rate of population growth of H.
axyridis each year and consequently spread.
(
Brown et al.,
2008b, Roy et al.,
2011a)
+
Phenotypic plasticity will allow
H. axyridis
to
successfully and regularly extend its
breeding season to September, October,
and even into November
Phenotypic plasticity displayed by
H. axyridis
enables local adaptation
at
temporal and spatial scales, increase in autumnal melanisation may have
accelerated the spread of H. axyridis.
Further work required to elucidate the importance of phenotypic plasticity
in the invasion success of H. axyridis.
(
Michie et al.,
2010, Purse et al.,
2014)
?
H. axyridis
will spread across the entire
British mainland by 2008
The first record of
H. axyridis
in Scotland was in 2007. However, there are
relatively few records in Scotland and its distribution and breeding there is
limited.
(
Roy et al., 2011a
,
Brown et al.,
2008b, Brown et
+
Page 17 of 28 Ecological Entomology

For Review Only
Highly dispersal ability of this species has clearly been demonstrated in
most of England and Wales.
al., 2008a
,
Brown
et al., 2011b)
Spread and increase of
H. axyridis
in Britain
may therefore prove to be beneficial to crop
systems by restricting aphid numbers below
economically damaging levels and so
reducing the use of chemical pesticides
Recent research highlights the importance of
H. axyridis
as an aphid
predator in crop systems in the UK.
Further work required to explore the ecosystem-level impact of H. axyridis
on pest insects and particularly the ecosystem service provided by this
alien predator.
(
Wells, 2011
)
?
Harmonia axyridis
is likely to have a
negative effect on other aphidophages in
three ways: resource competition, intra-
guild predation, and intraspecific
competition
Considerable evidence of intra
-
guild predation from laboratory and field
observations.
Observations from the UK Ladybird Survey highlight strong correlation
between presence of H. axyridis and declines in the distribution of native
ladybird species.
Further work required on competitive interactions although recent research
in laboratory mesocosms suggests that high aphid density does not reduce
intra-guild predation.
Considerable evidence of negative effects of H. axyridis on other species
but effects on ecosystem function requires further work.
(
Roy e
t al., 2012
,
Ware and Majerus,
2008, Brown et al.,
2014, Wells et al.,
2010, Wells, 2011,
Ware et al., 2009,
Brown et al.,
2011a)
+
Efficient chemical defence and relatively
large size would provide H. axyridis
with a significant reproductive advantage
over many native British species
A few studies indicate the importance of chemical defence and body size in
intra-guild interactions.
The importance of chemical defence and large size in contributing to
reproductive advantage of H. axyridis over native species requires further
investigation.
(
Ware et al., 2008
,
Bezzerides et al.,
2007)
+ / ?
H. axyridis
will become a nuisance to
humans
There have been many reports of
H. axyridis
forming large aggregations in
domestic dwellings and in some cases people have reported this species as a
nuisance.
Some evidence of negative effects on humans.
(
Roy et al., 2011a
)
-
Page 18 of 28Ecological Entomology

For Review Only
Table 2. Examples of studies on Harmonia axyridis over the last ten years that have provided 484
evidence to underpin understanding of the invasion process (Blackburn et al., 2011). The stage of 485
invasion and barrier (with extracts of the relevant text provided in italics) are defined by Blackburn 486
et al. (2011) and selected evidence derived from research on H. axyridis is outlined. 487
Stage of invasion
Barrier
Evidence
Transport
Geography
Species that has been
transported beyond the
limits of its native
geographic range and that
has established a
population in an area
where it was not known to
occur previously
The Altai mountains provide a biogeographic barrier to
spread from the native range, but introduction as a
biological control agent enabled the global spread of H.
axyridis (Brown et al., 2011b).
Accidental transport from continental Europe to Britain
alongside natural dispersal contributed to the arrival of H.
axyridis in 2004 (Brown et al., 2008b).
Introduction
Captivation or cultivation
Species can be prevented
from becoming an invader
by a human-imposed
barrier. Many animal
and plant species exist in
captivity and/or
cultivation beyond the
limits of their native
ranges, but fail to cross
the physical barriers of a
fence or hedge. This
barrier is probably lower
for species in cultivation
than for those in captivity
Introductions of
H. axyridis
within continental Europe
were predominantly in glasshouses for the control of
aphids but individuals could have escaped into the wider
countryside (Adachi-Hagimori et al., 2011).
Many widespread invasions arise from successful invasive
populations rather than directly from the native range
(invasive bridgehead effect) and this has been
demonstrated for H. axyridis. An invasive population in
eastern North America appears to have been the source
that invaded the European, South American and African
continents, with some admixture with a biological control
strain in Europe (Lombaert et al., 2010).
Es
tablishment
Survival
Introduced population can
fail to establish because
individuals in the
population fail to survive.
Failure to establish can
result from factors
associated with the
species (e.g. reproductive
rate or specialism), the
location (e.g. presence of
enemies or mutualists),
apparently stochastic
features of the individual
introduction event
(especially propagule
Successful overwintering in Britain since 2004
-
05
(
Brown
et al., 2008b).
Harmonia axyridis is climatically matched with most
regions of the world, including mainland Britain (Poutsma
et al., 2008).
Low susceptibility to natural enemies within the invaded
range (Comont et al., 2014b, Berkvens et al., 2010b, Roy et
al., 2011b, Roy et al., 2008b, Roy et al., 2011c).
Page 19 of 28 Ecological Entomology

For Review Only
pressure) or, often, their
interaction (e.g. species
location, such as climate
matching); these factors
can act on survival or
reproduction, or both
Reproduction
an introduced
population can fail to
establish because
individuals in the
population either fail to
survive, or survive but fail
toreproduce
Successful breeding in Britain since 2005
(
Brown et al.,
2008b).
Multivoltine species (Brown et al., 2008b).
Spread
Dispersal
a spreading population
essentially faces multiple,
sequential establishment
events, under an ever
greater range of
environmental conditions
Ability to exploit resources i
n a wide range of habitats has
ensured spread across Britain but limited spread north of
Pennine and west of Cambrian mountains (Brown et al.,
2011b).
Low susceptibility to natural enemies within the invaded
range (Comont et al., 2014b, Berkvens et al., 2010b,
Koyama and Majerus, 2008, Roy et al., 2008b).
Harmonia axyridis are able to travel 18 km in a “typical”
high-altitude flight, but up to 120 km if flying at higher
altitudes, indicating a high capacity for long-distance
dispersal (Jeffries et al., 2013).
Environmental
The invasive range is
determined by the extent
of suitable environment,
and the Environmental
barrier sets the limits to
this.
Exploitation of buildings as favourable overwintering
location (Brown, Adriaens et al. 2008).
Exploitation of wide range of habitats, especially
anthropogenic ones including urban and crop systems
(Brown et al., 2011b).
488
489
490
491
Page 20 of 28Ecological Entomology

For Review Only
492
Figure headings 493
Figure 1 Harmonia axyridis occurrence in 10 km squares in Britain from 2004 to 2014. Where a 494
square has been recorded in more than one year, occurrence in the earliest year is shown (blue = 495
2003-2004; green = 200-2006; yellow = 2007-2008; orange = 2009-2010; red = 2011-2012; burgundy 496
= 2013-2014). 497
498
Figure 2 Harmonia axyridis phenogram displaying number of H. axyridis records within the UK 499
Ladybird Survey database as monthly counts. 500
501
Page 21 of 28 Ecological Entomology

For Review Only
502
References 503
ADACHI-HAGIMORI, T., SHIBAO, M., TANAKA, H., SEKO, T. & MIURA, K. 2011. Control of Myzus 504
persicae and Lipaphis erysimi (Hemiptera: Aphididae) by adults and larvae of a flightless 505
strain of Harmonia axyridis (Coleoptera: Coccinellidae) on non-heading Brassica cultivars in 506
the greenhouse. BioControl, 56, 207-213. 507
BERKVENS, N., BONTE, J., BERKVENS, D., DEFORCE, K., TIRRY, L. & DE CLERCQ, P. 2008. Pollen as an 508
alternative food for Harmonia axyridis. From Biological Control to Invasion: the Ladybird 509
Harmonia axyridis as a Model Species. Springer. 510
BERKVENS, N., LANDUYT, C., DEFORCE, K., BERKVENS, D., TIRRY, L. & DE CLERCQ, P. 2010a. 511
Alternative foods for the multicoloured Asian lady beetle Harmonia axyridis (Coleoptera: 512
Coccinellidae). Eur. J. Entomol, 107, 189-195. 513
BERKVENS, N., MOENSA, J., BERKVENS, D., SAMIHC, M. A., TIRRY, L. & DE CLERCQ, P. 2010b. 514
Dinocampus coccinellae as a parasitoid of the invasive ladybird Harmonia axyridis in Europe. 515
Biologocal Control, 53, 92-99. 516
BEZZERIDES, A. L., MCGRAW, K. J., PARKER, R. S. & HUSSEINI, J. 2007. Elytra color as a signal of 517
chemical defense in the Asian ladybird beetle Harmonia axyridis. Behavioral Ecology and 518
Sociobiology, 61, 1401-1408. 519
BLACKBURN, T. M., PYŠEK, P., BACHER, S., CARLTON, J. T., DUNCAN, R. P., JAROŠÍK, V., WILSON, J. R. 520
U. & RICHARDSON, D. M. 2011. A proposed unified framework for biological invasions. 521
Trends in Ecology & Evolution, 26, 333-339. 522
BOTEZATU, A. I., KOTSERIDIS, Y., INGLIS, D. & PICKERING, G. J. 2013. Occurrence and contribution of 523
alkyl methoxypyrazines in wine tainted by Harmonia axyridis and Coccinella 524
septempunctata. Journal of the Science of Food and Agriculture, 93, 803-810. 525
BRAKEFIELD, P. M. & DE JONG, P. W. 2011. A steep cline in ladybird melanism has decayed over 25 526
years: a genetic response to climate change? Heredity, 107, 574-578. 527
BROWN, P. M. J. 2010. The spread of the harlequin ladybird Harmonia axyridis (Coleoptera: 528
Coccinellidae) in Europe and its effects on native ladybirds. PhD, Anglia Ruskin University. 529
BROWN, P. M. J., ADRIAENS, T., BATHON, H., CUPPEN, J., GOLDARAZENA, A., HAGG, T., KENIS, M., 530
KLAUSNITZER, B. E. M., KOVAR, I., LOOMANS, A. J. M., MAJERUS, M. E. N., NEDVED, O., 531
PEDERSEN, J., RABITSCH, W., ROY, H. E., TERNOIS, V., ZAKHAROV, I. A. & ROY, D. B. 2008a. 532
Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. BioControl, 533
53, 5-21. 534
BROWN, P. M. J., FROST, R., DOBERSKI, J., SPARKS, T., HARRINGTON, R. & ROY, H. E. 2011a. Decline 535
in native ladybirds in response to the arrival of Harmonia axyridis: early evidence from 536
England. Ecological Entomology, 36, 231-240. 537
BROWN, P. M. J., INGELS, B., WHEATLEY, A., RHULE, E. L., DE CLERCQ, P., VAN LEEUWEN, T. & 538
THOMAS, A. 2014. Intraguild predation by Harmonia axyridis (Coleoptera: Coccinellidae) on 539
native insects in Europe: molecular detection from field samples. Entomological Science, 540
n/a-n/a. 541
BROWN, P. M. J., ROY, H. E., ROTHERY, P., ROY, D. B., WARE, R. L. & MAJERUS, M. E. N. 2008b. 542
Harmonia axyridis in Great Britain: analysis of the spread and distribution of a non-native 543
coccinellid. BioControl, 53, 55-67. 544
BROWN, P. M. J., THOMAS, C. E., LOMBAERT, E., JEFFRIES, D. L., ESTOUP, A. & HANDLEY, L.-J. L. 545
2011b. The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): distribution, 546
dispersal and routes of invasion. BioControl, 56, 623-641. 547
CERYNGIER, P., ROY, H. E. & POLAND, R. L. 2012. Natural enemies of ladybird beetles. In: HODEK, I., 548
VAN EMDEN, H. F. & HONEK, A. (eds.) Ecology and behaviour of the ladybird beetles 549
(Coccinellidae). John Wiley & Sons. 550
Page 22 of 28Ecological Entomology

For Review Only
COLAUTTI, R. I., RICCIARDI, A., GRIGOROVICH, I. A. & MACISAAC, H. J. 2004. Is invasion success 551
explained by the enemy release hypothesis? Ecology Letters, 7, 721-733. 552
COMONT, R., ROY, H., HARRINGTON, R., SHORTALL, C. & PURSE, B. 2014a. Ecological correlates of 553
local extinction and colonisation in the British ladybird beetles (Coleoptera: Coccinellidae). 554
Biological Invasions, 16, 1805-1817. 555
COMONT, R. F., PURSE, B. V., PHILLIPS, W., KUNIN, W. E., HANSON, M., LEWIS, O. T., HARRINGTON, 556
R., SHORTALL, C. R., RONDONI, G. & ROY, H. E. 2014b. Escape from parasitism by the invasive 557
alien ladybird, Harmonia axyridis. Insect Conservation and Diversity, 7, 334-342. 558
COMONT, R. F., ROY, H. E., LEWIS, O. T., HARRINGTON, R., SHORTALL, C. R. & PURSE, B. V. 2012. 559
Using biological traits to explain ladybird distribution patterns. Journal of Biogeography, 39, 560
1772-1781. 561
DECOURCY, G. 2009. Long term implications of the arrival in the British Isles of Harmonia axyridis, 562
the harlequin ladybird. 563
ELLIOTT, N., KIECKHEFER, R. & KAUFFMAN, W. 1996. Effects of an invading coccinellid on native 564
coccinellids in an agricultural landscape. Oecologia, 105, 537-544. 565
ELTON, C. S. 1958. The ecology of invasions by animals and plants, London, UK Methuen. 566
FIRLEJ, I. 2012. Teratocytes growth pattern reflects host suitability in a host–parasitoid assemblage. 567
Annals of the Entomological Society of America, 105, 328-338. 568
FLOWERS, R., SALOM, S. & KOK, L. 2005. Competitive interactions among two specialist predators 569
and a generalist predator of hemlock woolly adelgid, Adelges tsugae (Homoptera: 570
Adelgidae), in the laboratory. Environmental entomology, 34, 664-675. 571
GALVAN, T. L., KOCH, R. L. & HUTCHISON, W. D. 2008. Impact of fruit feeding on overwintering 572
survival of the Multicolored Asian lady beetle, and the ability of this insect and paper wasps 573
to injure wine grape berries. Entomologia Experimentalis Et Applicata, 128, 429-436. 574
GLEMSER, E. J., DOWLING, L., INGLIS, D., PICKERING, G. J., MCFADDEN-SMITH, W., SEARS, M. K. & 575
HALLETT, R. H. 2012. A Novel Method for Controlling Multicolored Asian Lady Beetle 576
(Coleoptera: Coccinellidae) in Vineyards. Environmental Entomology, 41, 1169-1176. 577
GOETZ, D. W. Harmonia axyridis ladybug invasion and allergy. Allergy and Asthma Proceedings, 578
2008. OceanSide Publications, Inc, 123-129. 579
HALL, R., WARE, R. & MICHIE, L. J. 2009. First record of field parasitism of immature stages of the 580
Harlequin Ladybird Harmonia axyridis (Pallas) (Col.: Coccinellidae) by the braconid wasp 581
Dinocampus coccinellae (Shrank) (Hym.: Braconidae). The Entomologist's Record and Journal 582
of Variation, 121, 57-58. 583
HAUTIER, L., SAN MARTIN, G., CALLIER, P., DE BISEAU, J.-C. & GRÉGOIRE, J.-C. 2011. Alkaloids provide 584
evidence of intraguild predation on native coccinellids by Harmonia axyridis in the field. 585
Biological Invasions, 13, 1805-1814. 586
HODEK, I. & EVANS, E. W. 2012. Food relationships. In: HODEK, I., VAN EMDEN, H. F. & HONEK, A. 587
(eds.) Ecology and behaviour of the ladybird beetles (Coccinellidae). John Wiley & Sons. 588
HOLROYD, O., BROWN, P. M. J., ROY, H. E. & MAJERUS, M. E. N. 2008. The harlequin ladybird, 589
Harmonia axyridis, reaches Scotland. Entomologist's Record and Journal of Variation, 120, 590
42-43. 591
HOOGENDOORN, A. & HEIMPEL, G. 2002. Indirect interactions between an introduced and a native 592
ladybird beetle species mediated by a shared parasitoid. Biological Control, 25, 224-230. 593
INGELS, B. & DE CLERCQ, P. 2011. Effect of size, extraguild prey and habitat complexity on intraguild 594
interactions: a case study with the invasive ladybird Harmonia axyridis and the hoverfly 595
Episyrphus balteatus. BioControl, 56, 871-882. 596
JANSEN, J. P. & HAUTIER, L. 2008. Ladybird population dynamics in potato: comparison of native 597
species with an invasive species, Harmonia axyridis. BioControl, 53, 223-233. 598
JEFFRIES, D. L., CHAPMAN, J., ROY, H. E., HUMPHRIES, S., HARRINGTON, R., BROWN, P. M. J. & 599
LAWSON HANDLEY, L. J. 2013. Characteristics and Drivers of High-Altitude Ladybird Flight: 600
Insights from Vertical-Looking Entomological Radar. PLoS ONE 8(12): e82278 601
Page 23 of 28 Ecological Entomology

For Review Only
KENIS, M., ROY, H. E., ZINDEL, R. & MAJERUS, M. E. N. 2008. Current and potential management 602
strategies against Harmonia axyridis. BioControl, 53, 235-252. 603
KOCH, R., BURKNESS, E., BURKNESS, S. J. W. & HUTCHISON, W. 2004. Phytophagous preferences of 604
the multicolored Asian lady beetle (Coleoptera: Coccinellidae) for autumn-ripening fruit. 605
Journal of Economic Entomology, 97, 539-544. 606
KOCH, R. L. 2003. The Multicolored Asian lady beetle, Harmonia axyridis: a review of its biology, uses 607
in biological control, and non-target impacts. J Insect Sci, 3, 32. 608
KOCH, R. L. & GALVAN, T. L. 2008. Bad side of a good beetle: the North American experience with 609
Harmonia axyridis. BioControl, 53, 23-35. 610
KOCH, R. L., HUTCHISON, W. D., VENETTE, R. C. & HEIMPEL, G. E. 2003. Susceptibility of immature 611
monarch butterfly, Danaus plexippus (Lepidoptera : Nymphalidae : Danainae), to predation 612
by Harmonia axyridis (Coleoptera : Coccinellidae). Biological Control, 28, 265-270. 613
KOYAMA, S. & MAJERUS, M. E. N. 2008. Interactions between the parasitoid wasp Dinocampus 614
coccinellae and two species of coccinellid from Japan and Britain. BioControl, 53, 253-264. 615
LOMBAERT, E., GUILLEMAUD, T., CORNUET, J.-M., MALAUSA, T., FACON, B. & ESTOUP, A. 2010. 616
Bridgehead Effect in the Worldwide Invasion of the Biocontrol Harlequin Ladybird. Plos One, 617
5, e9743. 618
MAJERUS, M., STRAWSON, V. & ROY, H. 2006. The potential impacts of the arrival of the harlequin 619
ladybird, Harmonia axyridis (Pallas) (Coleoptera : Coccinellidae), in Britain. Ecological 620
Entomology, 31, 207-215. 621
MICHIE, L. J., MALLARD, F., MAJERUS, M. E. N. & JIGGINS, F. M. 2010. Melanic through nature or 622
nurture: genetic polymorphism and phenotypic plasticity in Harmonia axyridis. Journal of 623
Evolutionary Biology, 23, 1699-1707. 624
MURCHIE, A. K., MOORE, J. P., MOORE, G. A. & ROY, H. E. 2008. The harlequin ladybird (Harmonia 625
axyridis (Pallas)) (Coleoptera: Coccinellidae), found in Ireland. Ir Nat J, 29, 25–26. 626
NEDVĚD, O., XENIA, F., UNGEROVA, D. & KALUSHKOV, P. 2013. Alien vs. Predator–the native 627
lacewing Chrysoperla carnea is the superior intraguild predator in trials against the invasive 628
ladybird Harmonia axyridis. Bulletin of Insectology, 66, 73-78. 629
ONOFRE SOARES, A., CODERRE, D. & SCHANDERL, H. 2005. Influence of prey quality on the fitness of 630
two phenotypes of Harmonia axyridis adults. Entomologia experimentalis et applicata, 114, 631
227-232. 632
OSAWA, N. 2011. Ecology of Harmonia axyridis in natural habitats within its native range. BioControl, 633
56, 613-621. 634
PANIGAJ, L., ZACH, P., HONĚK, A., NEDVĚD, O., KULFAN, J., MARTINKOVÁ, Z., SELYEMOVÁ, D., 635
VIGLÁŠOVÁ, S. & ROY, H. E. 2014. The invasion history, distribution and colour pattern forms 636
of the harlequin ladybird beetle Harmonia axyridis (Pall.)(Coleoptera, Coccinellidae) in 637
Slovakia, Central Europe. ZooKeys, 89. 638
PELL, J. K., BAVERSTOCK, J., ROY, H. E., WARE, R. L. & MAJERUS, M. E. N. 2008. Intraguild predation 639
involving Harmonia axyridis: a review of current knowledge and future perspectives. 640
BioControl, 53, 147-168. 641
PHOOFOLO, M. W. & OBRYCKI, J. J. 1998. Potential for intraguild predation and competition among 642
predatory Coccinellidae and Chrysopidae. Entomologia Experimentalis et Applicata, 89, 47-643
55. 644
POUTSMA, J., LOOMANS, A. J. M., AUKEMA, B. & HEIJERMAN, T. 2008. Predicting the potential 645
geographical distribution of the harlequin ladybird, Harmonia axyridis, using the CLIMEX 646
model. BioControl, 53, 103-125. 647
PURSE, B. V., COMONT, R., BUTLER, A., BROWN, P. M. J., KESSEL, C. & ROY, H. E. 2014. Landscape 648
and climate determine patterns of spread for all colour morphs of the alien ladybird 649
Harmonia axyridis. Journal of Biogeography, n/a-n/a. 650
Page 24 of 28Ecological Entomology

For Review Only
RHULE, E. L., MAJERUS, M. E., JIGGINS, F. M. & WARE, R. L. 2010. Potential role of the sexually 651
transmitted mite< i> Coccipolipus hippodamiae</i> in controlling populations of the invasive 652
ladybird< i> Harmonia axyridis</i>. Biological Control, 53, 243-247. 653
RIBBANDS, B., BROWN, P. M. J., ROY, H. E. & MAJERUS, M. E. N. 2009. The most northerly record of 654
the Harlequin ladybird (Col., Coccinellidae) in the British Isles. Entomologist's Monthly 655
Magazine, 145, 43-44. 656
ROMANUK, T. N., ZHOU, Y., BROSE, U., BERLOW, E. L., WILLIAMS, R. J. & MARTINEZ, N. D. 2009. 657
Predicting invasion success in complex ecological networks. Philosophical Transactions of the 658
Royal Society B: Biological Sciences, 364, 1743-1754. 659
ROY, H. E., ADRIAENS, T., ISAAC, N. J. B., KENIS, M., ONKELINX, T., SAN MARTIN, G., BROWN, P. M. J., 660
HAUTIER, L., POLAND, R. L., ROY, D. B., COMONT, R., ESCHEN, R., FROST, R., ZINDEL, R., VAN 661
VLAENDEREN, J., NEDVĚD, O., RAVN, H. P., GRÉGOIRE, J.-C., DE BISEAU, J.-C. & MAES, D. 662
2012. Invasive alien predator causes rapid declines of native European ladybirds. Diversity 663
and Distributions, 18, 717-725. 664
ROY, H. E., BACON, J., BECKMANN, B., POLAND, R. L., MICHIE, L. J., RHULE, E., BROWN, P. M. J., 665
THOMAS, A., PELL, J. K., BAVERSTOCK, J., WELLS, P. M., LAWSON HANDLEY, L. J., THOMAS, C. 666
& BURLING, J. 2009. Ladybird, ladybird: unravelling the story of an alien invader. Royal 667
Society Summer Science. 668
ROY, H. E., BAVERSTOCK, J., WARE, R. L., CLARK, S. J., MAJERUS, M. E. N., BAVERSTOCK, K. E. & PELL, 669
J. K. 2008a. Intraguild predation of the aphid pathogenic fungus Pandora neoaphidis by the 670
invasive coccinellid Harmonia axyridis. Ecological Entomology, 33, 175-182. 671
ROY, H. E., BROWN, P. M. J., COMONT, R. F., POLAND, R. L., SLOGGETT, J. J., MAJERUS, M. & KEARNS, 672
P. W. E. 2013. Naturalists' Handbook 10: Ladybirds, Exeter, Pelagic Publishing. 673
ROY, H. E., BROWN, P. M. J., FROST, R. & POLAND, R. L. 2011a. Atlas of the ladybirds (Coccinellidae) 674
of Britain and Ireland, Wallingford, UK., Biological Records Centre. 675
ROY, H. E., BROWN, P. M. J., ROTHERY, P., WARE, R. L. & MAJERUS, M. E. N. 2008b. Interactions 676
between the fungal pathogen Beauveria bassiana and three species of coccinellid: Harmonia 677
axyridis, Coccinella septempunctata and Adalia bipunctata. BioControl, 53, 265-276. 678
ROY, H. E. & COTTRELL, T. E. 2008. Forgotten natural enemies: Interactions between coccinellids and 679
insect-parasitic fungi. European Journal of Entomology, 105, 391-398. 680
ROY, H. E., HANDLEY, L. J. L., SCHOENROGGE, K., POLAND, R. L. & PURSE, B. V. 2011b. Can the enemy 681
release hypothesis explain the success of invasive alien predators and parasitoids? 682
BioControl, 56, 451-468. 683
ROY, H. E. & LAWSON HANDLEY, L.-J. 2012. Networking: a community approach to invaders and their 684
parasites. Functional Ecology, 26, 1238–1248. 685
ROY, H. E., PEYTON, J., ALDRIDGE, D. C., BANTOCK, T., BLACKBURN, T. M., BRITTON, R., CLARK, P., 686
COOK, E., DEHNEN-SCHMUTZ, K., DINES, T., DOBSON, M., EDWARDS, F., HARROWER, C., 687
HARVEY, M. C., MINCHIN, D., NOBLE, D. G., PARROTT, D., POCOCK, M. J. O., PRESTON, C. D., 688
ROY, S., SALISBURY, A., SCHÖNROGGE, K., SEWELL, J., SHAW, R. H., STEBBING, P., STEWART, 689
A. J. A. & WALKER, K. J. 2014. Horizon scanning for invasive alien species with the potential 690
to threaten biodiversity in Great Britain. Global Change Biology, n/a-n/a. 691
ROY, H. E., RHULE, E., HARDING, S., HANDLEY, L.-J. L., POLAND, R. L., RIDDICK, E. W. & STEENBERG, T. 692
2011c. Living with the enemy: parasites and pathogens of the ladybird Harmonia axyridis. 693
BioControl, 56, 663-679. 694
ROY, H. E. & WAJNBERG, E. 2008. From biological control to invasion: the ladybird Harmonia axyridis 695
as a model species. BioControl, 53, 1-4. 696
SAETHRE, M. G., STAVERLØKK, A. & HOFSVANG, T. 2010. The history of Harmonia axyridis (Pallas 697
1773) in Norway. IOBC/wprs Bulletin (Working Group “Benefits and Risks of exotic biological 698
Control Agents”), 58, 97-104. 699
SLOGGETT, J. J. 2005. Are we studying too few taxa? Insights from aphidophagous ladybird beetles 700
(Coleoptera: Coccinellidae). European Journal of Entomology, 102, 391. 701
Page 25 of 28 Ecological Entomology

For Review Only
SLOGGETT, J. J. 2012. Harmonia axyridis invasions: Deducing evolutionary causes and consequences. 702
Entomological Science, 15, 261-273. 703
SMITH, C. A. & GARDINER, M. M. 2013. Biodiversity Loss following the Introduction of Exotic 704
Competitors: Does Intraguild Predation Explain the Decline of Native Lady Beetles? PloS one, 705
8, e84448. 706
TEDDERS, W. L. & SCHAEFER, P. W. 1994. Release and establishment of Harmonia axyridis 707
(Coleoptera, Coccinellidae) in the southeastern United States. Entomological News, 105, 708
228-243. 709
THOMAS, A. P., TROTMAN, J., WHEATLEY, A., AEBI, A., ZINDEL, R. & BROWN, P. M. J. 2013. Predation 710
of native coccinellids by the invasive alien Harmonia axyridis (Coleoptera: Coccinellidae): 711
detection in Britain by PCR-based gut analysis. Insect Conservation and Diversity, 6, 20-27. 712
TORCHIN, M., LAFFERTY, K. & KURIS, A. 2001. Release from parasites as natural enemies: increased 713
performance of a globally introduced marine crab. Biological Invasions, 3, 333-345. 714
TORCHIN, M. E., LAFFERTY, K. D., DOBSON, A. P., MCKENZIE, V. J. & KURIS, A. M. 2003. Introduced 715
species and their missing parasites. Nature, 421, 628-630. 716
VANDEREYCKEN, A., BROSTAUX, Y., JOIE, E., HAUBRUGE, E. & VERHEGGEN, F. J. 2013. Occurrence of 717
Harmonia axyridis (Coleoptera: Coccinellidae) in field crops. European Journal of 718
Entomology, 110, 285-292. 719
VERHEGGEN, F. J., FAGEL, Q., HEUSKIN, S., LOGNAY, G., FRANCIS, F. & HAUBRUGE, E. 2007. 720
Electrophysiological and behavioral responses of the multicolored Asian lady beetle, 721
Harmonia axyridis Pallas, to sesquiterpene semiochemicals. Journal of Chemical Ecology, 33, 722
2148-2155. 723
VILÀ, M., BASNOU, C., PYŠEK, P., JOSEFSSON, M., GENOVESI, P., GOLLASCH, S., NENTWIG, W., 724
OLENIN, S., ROQUES, A. & ROY, D. B. 2009. How well do we understand the impacts of alien 725
species on ecosystem services? A pan-European, cross-taxa assessment. Frontiers in Ecology 726
and the Environment, 8, 135-144. 727
VILCINSKAS, A., STOECKER, K., SCHMIDTBERG, H., ROHRICH, C. R. & VOGEL, H. 2013. Invasive 728
Harlequin Ladybird Carries Biological Weapons Against Native Competitors. Science, 340, 729
862. 730
WARE, R., MICHIE, L., OTANI, T., RHULE, E. & RJ, H. 2010. Adaptation of native parasitoids to a novel 731
host: the invasive coccinellid Harmonia axyridis. IOBC Bulletin, 58, 175-182. 732
WARE, R. L. & MAJERUS, M. E. N. 2008. Intraguild predation of immature stages of British and 733
Japanese coccinellids by the invasive ladybird Harmonia axyridis. BioControl, 53, 169-188. 734
WARE, R. L., RAMON-PORTUGAL, F., MAGRO, A., DUCAMP, C., HEMPTINNE, J. L. & MAJERUS, M. E. 735
N. 2008. Chemical protection of Calvia quatuordecimguttata eggs against intraguild 736
predation by the invasive ladybird Harmonia axyridis. BioControl, 53, 189-200. 737
WARE, R. L., YGUEL, B. & MAJERUS, M. E. N. 2009. Effects of competition, cannibalism and intra-guild 738
predation on larval development of the European coccinellid Adalia bipunctata and the 739
invasive species Harmonia axyridis. Ecological Entomology, 34, 12-19. 740
WELLS, P. M. 2011. Intraguild predation by Harmonia axyridis: effects on native enemies and aphid 741
suppression. PhD, University of Cambridge. 742
WELLS, P. M., BAVERSTOCK, J., MAJERUS, M. E. N., JIGGINS, F. M., ROY, H. E. & PELL, J. K. 2010. 743
Intraguild predation of non-coccinellid aphid natural enemies by Harmonia axyridis: prey 744
range and factors influencing intraguild predation. IOBC/wprs Bulletin (Working Group 745
“Benefits and Risks of exotic biological Control Agents”), 58, 185-196. 746
WILSON, J. R. U., DORMONTT, E. E., PRENTIS, P. J., LOWE, A. J. & RICHARDSON, D. M. 2009. 747
Something in the way you move: dispersal pathways affect invasion success. Trends in 748
Ecology & Evolution, 24, 136-144. 749
750
751
Page 26 of 28Ecological Entomology

For Review Only
Figure 1 Harmonia axyridis occurrence in 10 km squares in Britain from 2004 to 2014. Where a square has
been recorded in more than one year, occurrence in the earliest year is shown (blue = 2003-
2004; green =
200-2006; yellow = 2007-2008; orange = 2009-2010; red = 2011-2012; burgundy = 2013-2014).
229x261mm (300 x 300 DPI)
Page 27 of 28 Ecological Entomology

For Review Only
Figure 2 Harmonia axyridis phenogram displaying number of H. axyridis records within the UK Ladybird
Survey database as monthly counts.
177x177mm (300 x 300 DPI)
Page 28 of 28Ecological Entomology