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Long-Term Changes in Communities of Native Coccinellids: Population fluctuations and the Effect of Competition from an Invasive Non-Native Species

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Long-Term Changes in Communities of Native Coccinellids: Population fluctuations and the Effect of Competition from an Invasive Non-Native Species Insect Conservation and Diversity (2016) 9, 202–209 doi: 10.1111/icad.12158 Long-term changes in communities of native coccinellids: population fluctuations and the effect of competition from an invasive non-native species ALOIS HONEK,1 ZDENKA MARTINKOVA,1 ANTHONY F.G. DIXON,2 3 4 HELEN E. ROY and STANO PEKAR 1Crop Research Institute, Prague, Czech Republic, 2Department of Biodiversity Research, Global Change Research Centre AS CR, Brno, Czech Republic, 3NERC Centre for Ecology & Hydrology, Wallingford, UK and 4Department of Botany and Zoology, Faculty of Sciences, Masaryk University, Brno, Czech Republic Abstract. 1. We assessed the changes in abundance and community composi- tion of native species of coccinellids (Coleoptera: Coccinellidae) on deciduous trees that occurred between 1970s and 2010s, in the Czech Republic. 2. As the composition of adult communities varies with host plant and sea- son, coccinellids were sampled in May–June from Acer, Betula and Tilia trees using a standardised sweeping method. This was done before (1976–1986) and after (2011–2014) the arrival of Harmonia axyridis in 2006, with interim samples from a period immediately before it arrived in the Czech Republic (2002–2006). 3. Twenty-one native species were identified in the total sample of 2674 adults. The abundance of Adalia bipunctata, Coccinella quinquepunctata and Propylea quatuordecimpunctata decreased over the whole period sampled. Decli- nes in abundance of these species were already evident prior to the arrival of H. axyridis. Recent declines in Adalia decempunctata and Calvia quatuordecimgut- tata followed the arrival H. axyridis. Their abundance was increasing prior to the arrival of H. axyridis, but decreased following its invasion and the latter species might have affected their decline. The abundance of only one species, Calvia decemguttata, increased. Although the abundance of many species decreased and the frequency of some species varied, the diversity of native coc- cinellid populations (Shannon index) was similar over the 40 years of this study. 4. The changes in species composition can in part be attributed to H. axyri- dis, the role of other factors (e.g. climate change, habitat degradation) in the long-term fluctuations in abundance of coccinellids should be considered in future assessments. Key words. Adalia, Anatis, Calvia, Coccinella, Halyzia, Harmonia, intraguild predation, invasive alien species, ladybird beetles, Propylea. Spread of non-native organisms in areas outside their loss or become a threat to biodiversity (DAISIE, 2009; native geographic range are an important problem in a Vila et al., 2011). An important rapidly spreading invader globalised World (Hulme, 2009). Invasive non-native spe- is the Harlequin ladybird, Harmonia axyridis (Pallas) cies in recently occupied areas frequently cause economic (Coleoptera: Coccinellidae), which is native to eastern Asia and Siberia (Roy & Brown, 2015). After unsuccessful attempts to introduce it into Europe and North America, Correspondence: Alois Honek, Crop Research Institute, Drnovska 507, 16106 Prague 6-Ruzyne, Czech Republic. this aphidophagous species, originally considered a useful E-mail: [email protected] biological control agent, started to spread spontaneously 202 Ó 2016 The Authors Insect Conservation and Diversity published by John Wiley & Sons Ltd on behalf of Royal Entomological Society. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Long-term changes in coccinellid communities 203 through tropical and temperate biotas around the world term changes in communities caused by an invading with the exception of Australia (Brown et al., 2008; Roy species. et al., 2012). In addition to its supposed positive role in Our main interest is in the processes determining the regulating pest aphid populations on crops, it has negative structure of native coccinellid communities, which may effects on native guilds of aphid predators (Pell et al., have been affected by the arrival of H. axyridis. The long- 2008). In recently occupied areas, H. axyridis is a top term (1976–2014) standardised, systematic surveys of the intraguild predator and potentially negatively affects the abundance of coccinellids on different host plants within diversity of native aphidophagous species (Roy et al., the Czech Republic provide an invaluable source of data 2012). Under laboratory conditions, larvae of this species for evaluating the effects of H. axyridis on cocinellid com- win inter-specific contests and eat larvae of native coc- munities (Honek et al., 2014). The aim of this paper is to cinellids and other aphidophagous insects. Consequently, describe the pattern in the long-term changes that have H. axyridis is predicted to decrease the diversity of native occurred in the structure of communities. We used a part coccinellid communities (Pell et al., 2008). Therefore, it is of this data, those collected from trees and at a particular relevant to study the long-term changes in the abundance time of the year. This was done to determine whether (i) of native species of ladybirds. the species composition of a native coccinellid community The dominance of H. axyridis within coccinellid com- varied over time and (ii) the arrival of H. axyridis has munities since its establishment through western Europe adversely affected native coccinellid communities. has been extensively documented (Brown et al., 2011; Panigaj et al., 2014). The negative consequences of H. axyridis, through competition and predation, have been Material and methods demonstrated (Brown et al., 2008; Roy et al., 2012; Roy & Brown, 2015). However, as for many other invaded Coccinellids were sampled in the western part of the communities, it is difficult to precisely quantify the effect Czech Republic. Sampling was performed in a c. 50 km2 of invasive non-native species on native coccinellid com- area at north-west margin of Prague situated in between munities. The lack of records of coccinellids for years 50.08 and 50.14 N and 14.21 and 14.33 E (see Honek before the arrival of H. axyridis can be limiting; indeed, et al., 2015 for details). At this area, coccinellids were many studies were initiated after its arrival and so docu- sampled at 24 sites with an area of 0.2–0.5 ha grown by a ment developments in native coccinellid communities in stand of tree species sampled for coccinellid presence. At which H. axyridis is already present (Eschen et al., 2007; each site, there was a group of ≥5 trees of a particular Adriaens et al., 2008; Roy et al., 2012). Occurrence data species aged ≥30 years, and at some sites, there were more compiled over decades by volunteer recorders can be used than one species of tree (Honek et al., 2015). The sampled to assess distribution trends before and after the arrival of tree species were lime (Tilia cordata Mill. and Tilia platy- an invasive non-native species (Roy et al., 2012). How- phyllos Scop.), maple (Acer platanoides L. and Acer pseu- ever, these long-term datasets comprise occurrence data doplatanus L.) and birch (Betula pendula Roth.). A that are not collected systematically (Pocock et al., 2015). sampling of coccinellids at particular site, tree species and Therefore, datasets comprising abundance of species sam- date is further called a sampling session. We limited the pled in a standard way (standardising part of season and analysis to data of sampling sessions made in May–July sampled host plant species) can provide valuable addi- whose list is provided in Appendix S1. The beetles were tional population-level information. swept from the lower canopy (below c. 3 m height) using Here, we evaluate the community composition of coc- an entomology sweepnet (35 cm diam., 140 cm handle). cinellid species and compare their abundance and distribu- The survey was standardised by using the same person tion before and after the arrival of H. axyridis.Itis (AH) to collect the beetles and a standard sweepnet. Sam- possible to evaluate the changes that occurred in the spe- pling was done on sunny and still days, between 08:00 cies composition of all the coccinellids in a community and 18:00 h. Each sampling session lasted 15–30 minute including H. axyridis after its invasion. In doing this, the depending on the number of trees. The coccinellid adults mere presence of an added component changes the rela- were identified to species immediately and released at the tive abundance of native species and characteristics of the site. This was done from 1976 to 1986 (period 1 = P1, 56 community. In this case, the invasive non-native species sampling sessions), 2002–2006 (period 2 = P2, 28 sessions) becomes a part of the form taken by the community, and and 2011–2014 (period 3 = P3, 245 sampling sessions). In as a consequence, a ‘formal cause’ of the change. Alterna- total, there were 329 sampling sessions with a mean of tively, one may compare the community of native coc- 113 Æ 4 (range 50–300) sweeps per session. The coccinel- cinellids per se, i.e. the assemblage of species in this lids were thus sampled long before (P1), shortly before community before and after the invasion of H. axyridis. (P2) and shortly after (P3) the arrival of H. axyridis to The introduced species can then be considered an ‘efficient central Czech Republic in 2006 (Sprynar, 2008). cause’, an external factor acting upon the native commu- For each sampling session, the number of individuals of nity, which changes its abundance, diversity, equitability, each species per 100 sweeps was counted. We compared etc. The meaning of the term ‘community of native coc- the coccinellid communities in the three periods by assess- cinellids’ is adopted in this paper when evaluating long- ing the changes in (i) the abundance of the following ten Ó 2016 The Authors Insect Conservation and Diversity published by John Wiley & Sons Ltd on behalf of Royal Entomological Society, 9, 202–209 204 Alois Honek et al.
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