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BIODIVERSITY Invasive alien predator causes rapid RESEARCH declines of native European ladybirds Helen E. Roy1*, Tim Adriaens2, Nick J. B. Isaac1, Marc Kenis3, Thierry Onkelinx2, Gilles San Martin4, Peter M. J. Brown5, Louis Hautier6,7, Remy Poland8, David B. Roy1, Richard Comont1, Rene´ Eschen3, Robert Frost, Renate Zindel3,9, Johan Van Vlaenderen3, Oldrˇich Nedveˇd10, Hans Peter Ravn11, Jean-Claude Gre´goire7, Jean-Christophe de Biseau12, Dirk Maes2

1NERC Centre for Ecology & Hydrology, ABSTRACT Benson Lane, Crowmarsh Gifford, Oxfordshire, Aim Invasive alien species (IAS) are recognized as major drivers of biodiversity OX10 8BB, UK, 2Research Institute for Nature and Forest (INBO), Kliniekstraat 25, B-1070 loss, but few causal relationships between IAS and species declines have been Brussels, Belgium, 3CABI Europe-Switzerland, documented. In this study, we compare the distribution (Belgium and Britain) 1 Rue des Grillons, 2800 Dele´mont, and abundance (Belgium, Britain and Switzerland) of formerly common and Switzerland, 4Behavioural Ecology and widespread native ladybirds before and after the arrival of Harmonia axyridis,a Conservation group, Biodiversity Research globally rapidly expanding IAS. Centre, Earth and Life Institute, Universite Location Europe catholique de Louvain, Croix du Sud 4, B-1348 Louvain-la-Neuve, Belgium, 5Animal & Methods We used generalized linear mixed-effects models (GLMMs) to assess Environmental Research Group, Department of the distribution trends of eight conspicuous and historically widespread and Life Sciences, Anglia Ruskin University, East common species of ladybird within Belgium and Britain before and after the Road, Cambridge, CB1 1PT, UK, 6Unite´ arrival of H. axyridis. The distribution data were collated largely through public Protection des plantes et e´cotoxicologie, participatory surveys but verified by a recognized expert. We also used GLMMs to De´partement Sciences du vivant, Centre wallon model trends in the abundance of ladybirds using data collated through de Recherches agronomiques, Rue de Liroux, 2, systematic surveys of deciduous trees in Belgium, Britain and Switzerland. B-5030 Gembloux, Belgium, 7Lutte biologique et Ecologie spatiale (Biological Control and Results Five (Belgium) and seven (Britain) of eight species studied show Spatial Ecology Lab), CP 160/12, Universite´ substantial declines attributable to the arrival of H. axyridis. Indeed, the two-spot Libre de Bruxelles, 50 av FD Roosevelt, 1050 ladybird, Adalia bipunctata, declined by 30% (Belgium) and 44% (Britain) over Bruxelles, Belgium, 8Clifton College, 32 College 5 years after the arrival of H. axyridis. Trends in ladybird abundance revealed Rd, Clifton, Bristol, Avon, BS8 3JH, UK, similar patterns of declines across three countries. 9Department of Biology, University of Fribourg, Main conclusion Together, these analyses show H. axyridis to be displacing http://doc.rero.ch Chemin du Muse´e 10, 1700 Fribourg, native ladybirds with high niche overlap, probably through predation and Switzerland, 10Faculty of Biological Sciences competition. This finding provides strong evidence of a causal link between the and Institute of Entomology, University of arrival of an IAS and decline in native biodiversity. Rapid biotic homogenization South Bohemia, Academy of Sciences of the Czech Republic, Branisˇovska´ 31, CZ-37005 at the continental scale could impact on the resilience of ecosystems and severely Cˇeske´ Budeˇjovice, Czech Republic, 11University diminish the services they deliver. of Copenhagen, Forest & Landscape, Keywords Rolighedsvej 23, DK-1958 Frederiksberg C. Biological control, biological invasions, citizen science, , Harmonia 12 Denmark, Evolution Biologique et Ecologie, axyridis, population decline. Universite´ Libre de Bruxelles, CP 160/12, Av. F.D. Roosevelt 50 – 1050 Bruxelles, Belgium

*Correspondence: Helen E. Roy, NERC Centre for Ecology & Hydrology, Benson Lane, Crowmarsh Gifford, Oxfordshire, OX10 8BB, UK and Tim Adriaens, Research Institute for Nature and Forest (INBO), Kliniekstraat 25, B-1070 Brussels, Belgium. E-mail: [email protected]; [email protected]

 aphidophagous communities across North America but INTRODUCTION concluded that it was difficult to make general conclusions Rates of global extinction are orders of magnitude higher than as to the effect of these alien species on native coccinellid historical estimates and show no sign of slowing (Millenium assemblages. However, the potential loss of beneficial and Ecosystem Assessment, 2005). The Convention on Biological charismatic coccinellids is an important issue because of their Diversity and the 10th Conference of the Parties in Nagoya role in maintaining a properly functioning ecosystem and their (2010) identified invasive alien species (IAS) as one of the five intrinsic aesthetic value (Department for Environment, Food major pressures driving biodiversity loss and ultimately and Rural Affairs, 2011). extinction of species (Thomas et al., 2004; Hooper et al., Here, we document trends in the distribution and abun- 2005; Winter et al., 2009). IAS have direct ecological effects on dance of native ladybird species during the period of arrival other species through a variety of mechanisms (Parker et al., and rapid expansion of H. axyridis. We take advantage of 1999). In particular, invertebrate predators may displace extensive citizen-driven field surveys in Belgium and Britain indigenous species by direct predation, exploitative competi- spanning decades, as well as intensive monitoring by scientists tion for food or space, lower immunity to shared natural in three countries. The combination of fine-scale data collec- enemies, introduction of new pathogens or disrupted mating tion, replicated in time (over decades and including detailed systems (Snyder & Evans, 2006; Kenis et al., 2009). observations before and after the arrival of an IAS) and with Invasive alien species are unlike other drivers of change extensive coverage in three European countries, allied with because the time at which an IAS arrives within an ecosystem is powerful modern statistical techniques, thus provides a often known. Perhaps surprisingly then, there have been few uniquely rigorous test of the impacts of an IAS on biodiversity. clear demonstrations that IAS cause biodiversity loss. Vila` et al. (2011) provide compelling evidence, through a meta-analysis METHODS approach, that alien plant species exert significant impacts on resident plant species, communities and ecosystems. However, Distribution data source: large-scale ladybird surveys the majority of studies implicating IAS in species declines involve basic correlations in degraded ecosystems (Gurevitch & The Belgian and British checklists contain 38 and 25 native Padilla, 2004; Didham et al., 2005) at small spatial scales and ladybird species (Baugne´e et al., 2011; Roy et al., 2011a), over short time-scales. Such evidence has been criticized as respectively, from the subfamilies Chilocorinae, Coccinellinae circumstantial, leading to suggestions that IAS might be and Epilachninae. Distribution data have been collated largely passengers, as opposed to drivers, of change (MacDougall & through public participatory surveys. In Britain, a Coccinel- Turkington, 2005). The difficulty of distinguishing between lidae Recording Scheme has been run through the Biological correlates and causes of population decline has been widely Records Centre (NERC Centre for Ecology & Hydrology) since debated by ecologists (Ricciardi, 2004; Clavero & Garcia- 1971 with an online survey launched in 2005 (Roy et al., Berthou, 2005; Didham et al., 2005). Likewise, it is equally 2011a). In Belgium, the Coccinula Recording Scheme has been difficult to determine the relative importance of different active since 1999 with an online survey (Baugne´e et al., 2011); causal mechanisms acting on the same system (Didham et al., however, ad hoc earlier records exist and were included in 2005). The correlation between the presence of the invasive analyses. All records used in these analyses have been verified http://doc.rero.ch alien zebra mussel, Dreissena polymorpha (Pallas), and decline by a recognized expert. The observations are georeferenced to of unionid mussels in North America (Ricciardi et al., 1998; 1-km2 resolution using the Ordinance Survey British national Ricciardi & Rasmussen, 1999) is unquestionable (Ricciardi, grid reference system in Britain and the Universal Transverse 2004), but the arrival of this particular IAS appears to be only Mercator (UTM) in Belgium. The British and Belgian one link in the ‘chain of causality’ (Didham et al., 2005). databases contain 89,994 and 67,561 observations, respectively The arrival of the alien predator Harmonia axyridis (Pallas) (Table 1). in Europe provides an opportunity to investigate the distribu- tion status of native species before and after establishment of Distribution data analysis an IAS. Harmonia axyridis, a native of central and eastern Asia, was released for the control of pest across North Analyses are based on separate data sets for each country from America from 1916 and Europe from the late 1980s (Brown the respective survey databases, in which each row of data et al., 2008a,b). It is now considered an IAS in North America corresponds to a unique combination of year and 1-km2. The and many European countries, having undergone a period of columns refer to different ladybird species, and the data are 1 rapid expansion, spreading in many countries without delib- (present, i.e. recorded) and 0 (absence inferred) for each erate release (Brown et al., 2008a,b). Harmonia axyridis is a species 1-km2-year combination. The survey database contains large and voracious predator that threatens biodiversity presence-only records, and so the absence of ladybird species because it out-competes and displaces native ladybirds and was inferred from the presence of others, such that if three other aphidophagous insects (Majerus et al., 2006; species were recorded in a particular 1-km2-year, we inferred Brown et al., 2011; Roy et al., 2011a,b). Harmon et al. that all other species were absent (Biesmeijer et al., 2006). By (2007) highlighted the dominance of alien coccinellids in definition, all 1-km2-year combinations contain at least one

 Table 1 Summary of ladybird distribution data in Belgium and Britain). Parameter H estimates the net effect of H. axyridis in Britain. Data were collated from volunteer recorders through that 1-km2 (years prior to arrival and 1-km2 that were never national schemes: each record corresponds to an observation of a colonized were coded as zero). Thus, for a British grid cell that 2 ladybird species within a 1-km square in a given year. Our was colonized by H. axyridis in 2007, the fitted value for 2009 analyses were based on a filtered data set consisting of nine ‘focal’ is given by the intercept plus 5*Y plus 2*H. The model fits the species for which > 1000 records were available since 1990, and probability of occupancy on the logit scale. Our null hypothesis including only 1-km2-year combinations that were ‘well sampled’. 2 for each species is that parameter H is equal to zero. We The arrival year of Harmonia axyridis varies among 1-km , and 2 this variation was included within the models included 1-km as random intercept and year as random slope (to allow for different trends in each 1-km2), as well as an Species Belgium Britain observation-level random effect to account for overdispersion. All models were fitted in R 2.11.1 (Ihaka & Gentleman, 1996) Total number of records 67,560 89,994 with the lme4 package version 0.999375-37 (Bates & Maechler, (all years, all species) 2010). Total number of surveyed 5300 14,364 1-km2 since 1990* Number of 1-km2-year 9889 23 929 Systematic surveys of ladybird abundance combinations since 1990 2 Ladybird abundance data were collected using systematic Number of 1-km -year 1419 1746

combinations used for analysis fortnightly surveys in Brussels (Belgium) during spring 2003, · Number of 1-km2 used for analysis 365 411 2005 and 2008, in lime (Tilia vulgaris Hayne) and sycamore Number of 1-km2 with H. axyridis 269 249 ( L.) trees in 12 urban localities (parks, Median year of arrival 2004 2007 avenues and roadsides). Surveys at four sites in Cambridge- shire (Britain) and 15 sites in north-western Switzerland span *Focal species only. 2006–2010: each site was surveyed 7–9 times per year between Only includes 1-km2 with ‡ 2 focal species recorded in each of April and October. All Cambridgeshire sites were in suburban ‡ 3 years. locations and consisted primarily of deciduous trees; Swiss sites were 50 m sections of mixed deciduous hedges. In all record (i.e. 1-km2-year combinations with no records were countries, surveys were conducted using standard sampling assumed not to have been surveyed). We guarded against the methods including tree-beating and sweep-netting (Adriaens & possibility that incorrectly inferring absence might lead to Maes, 2004; Eschen et al., 2007; Brown et al., 2011). At all sites, spurious results by restricting our analyses to a small number branches were beaten with a stick (approximately 1 m) above a of ‘focal’ species in ‘well-sampled’ 1-km2. Focal species are beating tray (variable diameter for each country ranging from those for which there were > 1000 observations per country 0.65 to 1.25 m). At each of the Brussels sites, 100 branches since 1990 (nine species, Adalia bipunctata, Adalia decempunc- were sampled in deciduous trees. This sampling was tata, Calvia quatuordecimguttata, Coccinella septempunctata, performed across 10 randomly selected trees within each site. Exochomus quadripustulatus, sedecimguttata, Propylea In Switzerland, data were obtained from hedgerows consisting quattuordecimpunctata, Psyllobora vigintiduopunctata and of mixed deciduous woody species (either planted hedges or http://doc.rero.ch H. axyridis in each country). All ladybird species included forest edge), and the branches of all shrubs and trees up to a were conspicuous and historically widespread and common height of 3.5 m were sampled. In the Cambridgeshire sites (Roy et al., 2011a), and so we were confident in inferring deciduous trees were sampled for a fixed time period (20– absence of a species on the basis of the presence of other 60 min depending on the area of the site). Adults of all species. We defined ‘well-sampled’ combinations as those in ladybirds were counted and identified before being released which at least two focal species were observed. Furthermore, on-site. we included only 1-km2 that were ‘well sampled’ in at least 3 years. These criteria restricted our data set to the small Population data analysis proportion (7% in Britain, 14% in Belgium) of high-quality data (Table 1). We repeated our analyses with different We modelled the abundance of each species at our systematic thresholds for the definition of ‘well sampled’, but the results survey sites in each country separately, including only were qualitatively unchanged (Supplementary Table S1). ladybird species associated with deciduous trees and for To analyse the distribution data, we used generalized linear which at least 50 individual lady birds were captured. We also mixed-effects models (GLMMs) with binomial errors and logit modelled the total abundance of all native species and the link function. For each species and country, we modelled the total number of species. We used GLMMs with Poisson probability of 1-km2 occupancy (presence versus absence) as errors and log link with the year centred on the year of the the sum of two linear trends, Y and H. Parameter Y is the linear arrival of H. axyridis (2001 in Belgium, 2004 in Britain and occupancy trend in the absence of H. axyridis, estimated using 2006 in Switzerland) as a fixed effect. The random effects a fixed effect of year centred on the time of H. axyridis arrival included site, visit and observation (to account for overdi- in the respective country (2001 in Belgium and 2004 in spersion).

 RESULTS DISCUSSION

Here, we have assessed the effects of the arrival of an IAS on Distribution data: large-scale ladybird surveys the distribution and abundance of native species across The median year of arrival of H. axyridis in Belgium was 2004 European countries. Our results clearly indicate that native and in Britain 2007 (Table 1). Harmonia axyridis colonized at ladybirds have declined markedly in response to the arrival of least 269 of the 365 1-km2 (74%) analysed for Belgium and 249 H. axyridis. This finding provides strong evidence of a causal of the 411 1-km2 (61%) analysed for Britain (Table 1). In the link between the arrival of an IAS and decline in native absence of H. axyridis, similar numbers of species expanded biodiversity. and contracted their British ranges, whereas in Belgium, there The decline in the distribution and abundance of previously were more species expanding than contracting (Table 2; widespread and common native ladybirds after the arrival of Fig. 1). Harmonia axyridis had a significant negative impact H. axyridis is striking. The dramatic decline of A. bipunctata (H < 0) on the distribution of five species in Belgium and all over the five years following the arrival of H. axyridis is of but one of the eight species in Britain (Table 2). The particular note. This species is now near the threshold of magnitude of these effects is large, that is, |H|>|Y|, such that detection, in both Europe (Brown et al., 2011) and North these species have shown substantial range retraction (Table 2; America (Harmon et al., 2007), in habitats in which it was Fig. 1). This is exemplified by A. bipunctata, which declined by previously common. Harmonia axyridis appears to be displac- 30% in Belgium and 44% in Britain over the five years ing those native ladybirds with which it shares a high niche following the arrival of H. axyridis (Fig. 2). A few ladybirds overlap (Adriaens et al., 2008), such as A. bipunctata. The were declining prior to the arrival of H. axyridis (Y < 0), but likely mechanisms are both intra-guild competition and H. axyridis has significantly accelerated the rate of this decline. predation based on asymmetry of body size (H. axyridis is about 1.5 times larger than A. bipunctata) and superior physical and chemical defences in comparison with other Systematic surveys of ladybird abundance species of ladybird (Pell et al., 2008; Roy et al., 2008). Population trends, revealed by data from systematic surveys at Laboratory studies have indicated the potential of H. axyridis specific sites in Belgium, Britain and Switzerland, strongly to act as a unidirectional intra-guild predator of entomopatho- supported the distribution trends (Table 3). One species genic fungi (Roy et al., 2008), coccinellids (Ware & Majerus, (A. bipunctata) showed significant declines in abundance in 2008; Ware et al., 2009) and other invertebrates (Koch & all three countries, and another species (E. quadripustulatus) Galvan, 2008; Roy et al., 2011a). Additionally, a recent field showed significant declines in two countries (Britain and study, in which exogeneously sequestered alkaloids were used Switzerland). Three species showed significant declines in only as a tool for detecting the consumption of other coccinellids, one of the three countries (Table 3). All three countries revealed a high prevalence of intra-guild predation (Hautier showed a significant increase in the abundance of H. axyridis et al., 2008, 2011) by H. axyridis. In some sites, more than 30% (Table 3), whilst at the same time, the total ladybird of H. axyridis larvae contained the alkaloids adaline, calvine or abundance (excluding H. axyridis) declined significantly in propyleine representing intra-guild predation of Adalia spp., all three countries. Calvia spp. and P. quattuordecimpunctata (Hautier et al., 2011). http://doc.rero.ch

Table 2 Trends in the distribution of European ladybirds before and after the arrival of the invasive alien predator Harmonia axyridis. Numbers are parameters extracted from mixed-effects models for each species based on 1419 and 1746 observations (1-km2-year combi- nations) for Belgium and Britain, respectively.

Belgium Britain

Species % aY H % aY H

Harmonia axyridis 42 )2.160 – 0.826*** 25 )18.191 – 9.540*** Adalia bipunctata 52 0.521 )0.106*** )0.216*** 68 1.294 0.059*** )0.535*** Adalia decempunctata 22 )1.251 0.051** )0.187** 32 )0.888 )0.024 )0.330*** Calvia quatuordecimguttata 28 )0.975 0.013 )0.139* 21 )1.775 )0.051* )0.205* Coccinella septempunctata 78 1.392 0.002 0.014 75 1.403 )0.016 )0.092 Exochomus quadripustulatus 24 )1.556 0.078** )0.187** 33 )1.032 0.091*** )0.216** Halyzia sedecimguttata 25 )1.458 0.125*** )0.085 22 )1.532 0.200*** )0.396*** Propylea quattuordecimpunctata 55 0.336 )0.018 )0.104* 41 )0.405 )0.045** )0.307*** Psyllobora vigintiduopunctata 40 )0.504 )0.021 0.033 28 )1.312 )0.070*** )0.285***

%: percentage of observations where the species is present, a: intercept (logit probability at year of first introduction), Y: trend in the absence of H. axyridis and H: effect of the presence of H. axyridis on the trend. ***P < 0.001, **P < 0.01, *P < 0.05.

 Country H. axyridis

Belgium Absent

Britain Present

Adalia bipunctata Adalia decempunctata Calvia quatuordecimguttata Coccinella septempunctata

100%

80%

60%

40%

20%

0%

Exochomus quadripustulatus Halyzia sedecimguttata Propylea quattuordecimpunctata Psyllobora vigintiduopunctata

Probability 100%

80%

60%

40%

20% http://doc.rero.ch

0% 1990 1995 2000 2005 2010 1990 1995 2000 2005 2010 1990 1995 2000 2005 2010 1990 1995 2000 2005 2010 Year

Figure 1 Effects of Harmonia axyridis on the distribution of eight native ladybirds based on predictions for an average 1-km2. Prediction is based on the fixed effects of the models and ignores random variation in occupancy among specific 1-km2. Absent assumes the 1-km2 is not colonized by H. axyridis, and present assumes the 1-km2 was colonized in 2001 (Belgium) or 2004 (Britain) by H. axyridis. Note that our predictions are shown in the measurement scale (probability of occupancy), rather than the modelled scale (logit).

Halyzia sedecimguttata (L.) is a mycophagous ladybird and climate warming has increased the availability of mildew for is, unlike most of the species within our study, not in this mycophagous species. However, this trend is reversed in competition with H. axyridis for food. This ladybird has Britain in the presence of H. axyridis. The feeding niches of undergone a dramatic increase in abundance and distribution H. axyridis and H. sedecimguttata do not overlap, but their in Britain (Roy et al., 2011a) and Belgium, which reflects a habitats do. Halyzia sedecimguttata is likely to be particularly recent shift in habitat preference, previously associated with vulnerable to predation by H. axyridis in the autumn when, oak it is now also commonly found feeding on mildew of ash unlike most ladybird species, H. sedecimguttata and H. axyridis and sycamore trees (Roy et al., 2011a). It is possible that exist predominantly as larvae and pupae (immature stages). At

 of H. axyridis. This common ladybird is mainly associated with 100% Country herbaceous vegetation (Roy et al., 2011a) and so does not

Belgium overlap with H. axyridis to the extent of the four tree specialists (A. bipunctata, A. decempunctata, C. quattuordecimguttata and 80% Britain E. quadripustulatus). Additionally, C. septempunctata is a large ladybird, of similar size to H. axyridis. Coccinella septempunc- tata is itself a successful IAS in the USA and Canada, where it is 60% thought to have contributed to declines in native species

H. axyridis (Harmon et al., 2007).

with Historically, the decline of widespread and common species

2 40% has gone largely unnoticed, and there is a paucity of

1−km quantitative information on such declines (Gaston & Fuller, 2007; Van Dyck et al., 2009), especially among invertebrates. 20% The pronounced decline of species widely regarded as unth- reatened (none of the declining species are categorized according to IUCN conservation designations) highlights the 0% importance of continued large-scale monitoring of both rare and common species within the wider countryside. The decline

1990 1995 2000 2005 in ladybird species across Europe and associated alterations to Year community composition could have far-reaching effects on ecosystem services (Hooper et al., 2005). Predatory ladybirds Figure 2 Invasion of Belgium and Britain by Harmonia axyridis, expressed as the percentage of all ‘well-sampled’ 1-km2 that were are known to provide a major ecosystem service by regulating colonized. The diffuse ribbons delimit the 95% confidence intervals. pest insects. Although H. axyridis is an effective biological control agent in crop systems (Tedders & Schaefer, 1994; Brown & Miller, 1998; Alyokhin & Sewell, 2004; Heimpel et al., this time, the , the main prey of H. axyridis, are in 2010), it is unclear whether it can fulfil all the functional roles decline, and so alternative prey including the immature stages of the species it is displacing. Harmonia axyridis is rapidly of other insects such as H. sedecimguttata is consumed (Brown expanding its global range: our results imply that this will cause et al., 2011). It is likely that subtle differences in the phenology ecological extinctions (Estes et al., 1989) of native species, of ladybirds within Belgium and Britain alter the interactions notably deciduous tree specialists, over large areas. between species. There is considerable debate over the relationship between One species, C. septempunctata, within our study provides a species diversity and ecosystem processes. It is apparent that particularly interesting contrast in that its distribution and species diversity enhances productivity and stability in some abundance appear to be stable across Europe despite the arrival ecosystems, but not in others (Johnson et al., 1996; Rey

http://doc.rero.ch Table 3 Trends in the abundance of European ladybirds at a number of deciduous tree sites within Britain, Belgium and Switzerland after the arrival of the invasive alien predator Harmonia axyridis. The systematic surveys were repeated 7–9 times per field season (April–October). Numbers are parameters extracted from mixed-effects models for each species

Britain Belgium Switzerland

Species n Trend n Trend n Trend

H. axyridis 1 824 1.278*** 2 651 0.550*** 1 344 0.894*** Adalia bipunctata 931 )0.472*** 689 )0.877*** 293 )0.571** Adalia decempunctata 1 702 )0.169* 198 )0.125 356 )0.058 Calvia quatuordecimguttata 249 0.031 145 0.035 138 )0.272 Coccinella septempunctata 1 557 0.193 – – – – Exochomus quadripustulatus 753 )0.200* 160 )0.192 83 )0.957*** Halyzia sedecimguttata – – 126 0.397*** – – Propylea quattuordecimpunctata 428 )0.039 66 )0.142 251 )0.629*** Calvia decemguttata – – 179 )0.091 – – Oenopia conglobata – – 125 )0.623*** – – Total (all native species) 10,793 )0.091* 1711 )0.220*** 1376 )0.465*** Number of native species 16 )0.028 12 )0.084** 18 )0.329***

n, number of individual ladybirds. ***P < 0.001, **P < 0.01, *P < 0.05.

 Benayas et al., 2009). However, it is often difficult to predict Biesmeijer, J.C., Roberts, S.P.M., Reemer, M., Ohlemuller, R., which species are critical to functioning or provide resilience Edwards, M., Peeters, T., Schaffers, A.P., Potts, S.G., Kleu- and resistance to environmental changes. Additionally, the kers, R., Thomas, C.D., Settele, J. & Kunin, W.E. (2006) arrival of an IAS (or, indeed, other anthropogenic perturba- Parallel declines in pollinators and -pollinated plants in tion) is more likely to change the relative abundance of species Britain and the Netherlands. Science, 313, 351–354. rather than result in extinction of a species, but the relation- Brown, M.W. & Miller, S.S. (1998) Coccinellidae (Coleoptera) ship between community composition (species richness) and in apple orchards of eastern West Virginia and the impact of ecosystem functioning has focussed on effects of species invasion by Harmonia axyridis. Entomological News, 109, extinctions (Chapin et al., 2000). We predict that the domi- 143–151. nance of H. axyridis, and associated reduction of diversity, will Brown, P.M.J., Adriaens, T., Bathon, H., Cuppen, J., Goldaraz- decrease the resilience of aphidophagous guilds and severely ena, A., Hagg, T., Kenis, M., Klausnitzer, B.E.M., Kovar, I., diminish the services they deliver (Biesmeijer et al., 2006; Loomans, A.J.M., Majerus, M.E.N., Nedveˇd, O., Pedersen, J., Winter et al., 2009). Rabitsch, W., Roy, H.E., Ternois, V., Zakharov, I.A. & Roy, D.B. (2008a) Harmonia axyridis in Europe: spread and distri- bution of a non-native coccinellid. BioControl, 53, 5–21. ACKNOWLEDGEMENTS Brown, P.M.J., Roy, H.E., Rothery, P., Roy, D.B., Ware, R.L. & The late Professor Michael Majerus, our colleague and friend Majerus, M.E.N. (2008b) Harmonia axyridis in Great Britain: from the University of Cambridge, was instrumental in estab- analysis of the spread and distribution of a non-native lishing this research collaboration. The authors are extremely coccinellid. BioControl, 53, 55–67. grateful to the many thousands of people across Belgium and Brown, P.M.J., Frost, R., Doberski, J., Sparks, T., Harrington, Britain who have contributed their ladybird findings to the R. & Roy, H.E. (2011) Decline in native ladybirds in response surveys. Their enthusiasm has been inspirational. H.E.R., N.I. to the arrival of Harmonia axyridis (Coleoptera: Coccinelli- and D.B.R. are funded through the NERC Centre for Ecology & dae): early evidence from England. Ecological Entomology, 36, Hydrology and the Joint Nature Conservation Committee. The 231–240. development of the online surveys in Britain was in part through Chapin, F.S., Zavaleta, E.S., Eviner, V.T., Naylor, R.L., Vitousek, funding received from the Department for Environment, Food P.M., Reynolds, H.L., Hooper, D.U., Lavorel, S., Sala, O.E., and Rural Affairs (Defra). We are grateful to Natuurpunt and Hobbie, S.E., Mack, M.C. & Diaz, S. (2000) Consequences of Natagora for providing the online encoded records of ladybirds changing biodiversity. Nature, 405, 234–242. in Belgium. Research in Switzerland was funded by a grant from Clavero, M. & Garcia-Berthou, E. (2005) Invasive species are a the Swiss Federal Office for the Environment (F232-0377) and leading cause of extinctions. Trends in Ecology & the EU FP6 project ALARM (GOCE-CT-2003-506675). ON was Evolution, 20, 110–110. funded by grant numbers QH82047 by the Ministry of Agricul- Department for Environment Food and Rural Affairs (2011) ture and 6007665801 by the Ministry of Education of the Czech The Natural Choice: securing the value of nature. (ed Defra). Republic. HPR was funded through the Villum Foundation. The Stationery Office Limited, London. Didham, R.K., Tylianakis, J.M., Hutchison, M.A., Ewers, R.M. & Gemmell, N.J. (2005) Are invasive species the drivers of http://doc.rero.ch REFERENCES ecological change? Trends in Ecology & Evolution, 20, 470– Adriaens, T. & Maes, D. (2004) Voorlopige verspreidingatlas 474. van lieveheersbeestjes in Vlaanderen. Bertram, 1bis, 1–71. Eschen, R., Babendreier, D., Nauer, S., Bigler, F. & Kenis, M. Adriaens, T., Gomez, G.M.Y. & Maes, D. 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