Diversity and Distributions Invasive alien predator causes rapid declines of native European ladybirds Journal:For Diversity Review and Distributions Only Manuscript ID: Draft Manuscript Type: Biodiversity Research Date Submitted by the n/a Author: Complete List of Authors: Roy, Helen; Biological Records Centre, Centre for Ecology and Hydrology Adriaens, Tim; Research Institute for Nature and Forest (INBO) Isaac, Nick; Centre for Ecology & Hydrology Kenis, Mark; CABI Europe-Switzerland Onkelinx, Thierry; Research Institute for Nature and Forest (INBO) SAN MARTIN, Gilles; Université catholique de Louvain, Behavioural Ecology & Conservation Group Earth and Life Institute Brown, Peter; Anglia Ruskin University HAUTIER, Louis; Centre wallon de Recherches agronomiques, Sciences du vivant; Université Libre de Bruxelles, Lutte biologique et Ecologie spatiale Poland, Remy; Clifton College Roy, David; Centre for Ecology & Hydrology Comont, Richard; Centre for Ecology & Hydrology Eschen, René; CABI Europe-Switzerland Frost, Robert; Anglia Ruskin University Zindel, Renate; CABI Europe-Switzerland Van Vlaenderen, Johan; CABI Europe-Switzerland Nedvěd, Oldřich; University of South Bohemia Ravn, Hans Peter; University of Copenhagen Grégoire, Jean-Claude; Université Libre de Bruxelles de BISEAU, Jean-Christophe; Université Libre de Bruxelles, Evolution Biologique et Ecologie Maes, Dirk; Research Institute for Nature and Forest (INBO) Biological invasion, Population decline, Harmonia axyridis, Biotic Keywords: homogenisation, Citizen science Diversity and Distributions Page 1 of 23 Diversity and Distributions 1 2 3 1 Diversity and Distributions – Biodiversity Research 4 5 2 6 3 Invasive alien predator causes rapid declines of native European ladybirds 7 8 4 9 1 2 1 3 2 4 5 Helen E. Roy *, Tim Adriaens , Nick J.B. Isaac , Marc Kenis , Thierry Onkelinx , Gilles San Martin , 10 11 6 Peter M.J. Brown 5, Louis Hautier 6, 11 , Remy Poland 7, David B. Roy 1, Richard Comont 1, René Eschen 3, 12 3,8 3 9 10 13 7 Robert Frost, Renate Zindel , Johan Van Vlaenderen , Oldřich Nedvěd , Hans Peter Ravn , Jean- 14 8 Claude Grégoire 11 , Jean-Christophe de Biseau 12 , Dirk Maes 2 15 16 9 17 18 10 *Corresponding author:For Helen E. ReviewRoy ( [email protected] ) and OnlyTim Adriaens ( [email protected] ) 19 11 20 21 12 1Centre for Ecology & Hydrology, Benson Lane, Crowmarsh Gifford, Oxfordshire, OX10 8BB, UK; 22 23 13 [email protected] , [email protected] , [email protected] , [email protected] 24 14 2Research Institute for Nature and Forest (INBO), Kliniekstraat 25, B-1070 Brussels, Belgium; 25 26 15 [email protected] ; [email protected] ; [email protected] 27 3 16 CABI Europe-Switzerland, 1 Rue des Grillons, 2800 Delémont, Switzerland [email protected] ; 28 29 17 [email protected] 30 4 31 18 Universite catholique de Louvain, Earth and Life Institute, Biodiversity Research Centre, Behavioural 32 19 Ecology and Conservation group Croix du Sud 4, B-1348 Louvain-la-Neuve, Belgium. 33 34 20 [email protected] 35 21 5Animal & Environmental Research Group, Department of Life Sciences, Anglia Ruskin University, 36 37 22 East Road, Cambridge, CB1 1PT, UK; [email protected] 38 6 39 23 Unité Protection des plantes et écotoxicologie, Département Sciences du vivant, Centre wallon de 40 24 Recherches agronomiques, Rue de Liroux, 2, B-5030 Gembloux, Belgium. [email protected] 41 7 42 25 Clifton College, 32 College Rd, Clifton, Bristol, Avon, BS8 3JH, UK 43 26 8Department of Biology, University of Fribourg, Chemin du Musée 10, 1700 Fribourg, Switzerland 44 45 27 9University of South Bohemia, Faculty of Biological Sciences and Institute of Entomology, Academy of 46 47 28 Sciences of the Czech Republic, Branišovská 31, CZ-37005 České Budějovice, Czech Republic. 48 29 [email protected] 49 50 30 10 University of Copenhagen, Forest & Landscape, Rolighedsvej 23, DK-1958 Frederiksberg C. 51 31 Denmark; [email protected] 52 53 32 11 Lutte biologique et Ecologie spatiale (Biological Control and Spatial Ecology Lab), CP 160/12, 54 55 33 Université Libre de Bruxelles, 50 av FD Roosevelt, 1050 Bruxelles, Belgium 56 34 12 Evolution Biologique et Ecologie, Université Libre de Bruxelles, CP 160/12, Av. F.D. Roosevelt 50 - 57 58 35 1050 Bruxelles, Belgium. [email protected] 59 60 1 Diversity and Distributions Diversity and Distributions Page 2 of 23 1 2 3 36 4 5 37 HER, TA and MK led data collection and collation. NJBI, TO and DM assembled the data and 6 38 performed the analyses with assistance from HER, LH, RC and GSM. HER, TA, RP and PMJB collated 7 8 39 the national distributional data. PMJB, RF, GSM, LH, J-CG, J-CB, RE, JVV, RZ and MK conducted the 9 40 field surveys resulting in abundance data. HER wrote the first draft of the manuscript, and all 10 11 41 authors contributed substantially to revisions. 12 13 42 14 43 Abstract 15 16 44 Invasive alien species (IAS) are recognised as major drivers of biodiversity loss but few causal 17 45 relationships between IAS and species declines have been documented. We report rapid, dramatic 18 For Review Only 19 46 and ongoing declines in the distribution of formerly common and widespread native ladybirds in 20 21 47 Belgium and Britain following the arrival of Harmonia axyridis , a globally rapidly expanding IAS. Four 22 48 (Belgium) and seven (Britain) of eight species studied show substantial declines attributable to the 23 24 49 arrival of H. axyridis . Indeed, the 2-spot ladybird, Adalia bipunctata , declined by 30% (Belgium) and 25 26 50 44% (Britain) over five years after the arrival of H. axyridis . Trends in ladybird abundance revealed 27 51 similar patterns of declines across three countries. Together, these analyses show H. axyridis to be 28 29 52 displacing native ladybirds with high niche overlap, probably through predation and competition. 30 Such rapid biotic homogenisation at the continental scale could impact on the resilience of 31 53 32 54 ecosystems and severely diminish the services they deliver. 33 34 55 35 56 Keywords 36 37 57 Harmonia axyridis, invasive alien species, non-native species, Coccinellidae, biological control, 38 39 58 biological invasion, population decline, citizen science, biotic homogenisation 40 59 41 42 60 Introduction 43 Rates of global extinction are orders of magnitude higher than historical estimates and show no sign 44 61 45 62 of slowing (Millenium Ecosystem Assessment, 2005). The Convention on Biological Diversity and the 46 th 47 63 10 Conference of the Parties (Nagoya in 2010), identified invasive alien species (IAS) as one of five 48 64 major pressures driving biodiversity loss, and ultimately extinction of species (Winter et al., 2009, 49 50 65 Hooper et al., 2005, Thomas et al., 2004). IAS have direct ecological effects on other species through 51 52 66 a variety of mechanisms (Parker et al., 1999). In particular, invertebrate predators may displace 53 67 indigenous species by direct predation, exploitative competition for food or space, lower immunity 54 55 68 to shared natural enemies, introduction of new pathogens or disrupted mating systems (Snyder & 56 Evans, 2006, Kenis et al., 2009). 57 69 58 59 60 2 Diversity and Distributions Page 3 of 23 Diversity and Distributions 1 2 3 70 4 5 71 IAS are unlike other drivers of change because the time at which an IAS arrives within an ecosystem 6 72 is often known. Perhaps surprisingly then, there have been few clear demonstrations that IAS cause 7 8 73 biodiversity loss. The majority of studies implicating IAS in species declines involve basic correlations 9 74 in degraded ecosystems (Didham et al., 2005, Gurevitch & Padilla, 2004) at small spatial-scales and 10 11 75 over short time-scales. Such evidence has been criticised as circumstantial, leading to suggestions 12 13 76 that IAS might be passengers, as opposed to drivers, of change (MacDougall & Turkington, 2005). 14 77 The difficulty of distinguishing between correlates and causes of population decline has been widely 15 16 78 debated by ecologists (Ricciardi, 2004, Clavero & Garcia-Berthou, 2005, Didham et al., 2005). 17 79 Likewise, it is equally difficult to determine the relative importance of different causal mechanisms 18 For Review Only 19 80 acting on the same system (Didham et al., 2005). The correlation between the presence of the 20 21 81 invasive alien zebra mussel, Dreissena polymorpha (Pallas), and decline of unionid mussels in North 22 82 America (Ricciardi & Rasmussen, 1999, Ricciardi et al., 1998) is unquestionable (Ricciardi, 2004) but 23 24 83 the arrival of this particular IAS appears to be only one link in the “chain of causality” (Didham et al., 25 26 84 2005). 27 85 28 29 86 The arrival of the alien predator Harmonia axyridis (Pallas) in Europe provides an opportunity to 30 investigate the distribution status of native species before and after establishment of an IAS. 31 87 32 88 Harmonia axyridis , a native of central and eastern Asia, was released for the control of pest insects 33 34 89 across North America from 1916 and Europe from the late 1980s (Brown et al., 2008, Brown et al., 35 90 2008). It is now considered an IAS in North America and many European countries, having 36 37 91 undergone a period of rapid expansion, spreading in many countries without deliberate release 38 39 92 (Brown et al., 2008). Harmonia axyridis is a large and voracious predator that threatens biodiversity 40 93 because it outcompetes and displaces native ladybirds and other aphidophagous insects (Majerus et 41 42 94 al., 2006, Roy et al., 2011, Brown et al., 2011). The potential loss of such beneficial and charismatic 43 organisms is an important issue because of their important role in maintaining a properly 44 95 45 96 functioning ecosystem and their intrinsic aesthetic value (Department for Environment, Food and 46 47 97 Rural Affairs, 2011).