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Potential for Exploitative Competition, Not Intraguild Predation, Between Invasive Harlequin Ladybirds and flowerbugs in Urban Parks

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Potential for Exploitative Competition, Not Intraguild Predation, Between Invasive Harlequin Ladybirds and flowerbugs in Urban Parks See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/284805770 Potential for exploitative competition, not intraguild predation, between invasive harlequin ladybirds and flowerbugs in urban parks Article in Biological Invasions · November 2015 DOI: 10.1007/s10530-015-1024-y CITATIONS READS 11 140 4 authors, including: Andy G Howe Christian Bressen Pipper University of Copenhagen LEO Pharma 23 PUBLICATIONS 286 CITATIONS 145 PUBLICATIONS 3,142 CITATIONS SEE PROFILE SEE PROFILE Alex Aebi Université de Neuchâtel 123 PUBLICATIONS 1,363 CITATIONS SEE PROFILE Some of the authors of this publication are also working on these related projects: Teaching, supervising, project development, writing! View project Modelling grouped survival data View project All content following this page was uploaded by Alex Aebi on 23 February 2016. The user has requested enhancement of the downloaded file. Potential for exploitative competition, not intraguild predation, between invasive harlequin ladybirds and flowerbugs in urban parks Andy G. Howe, Hans Peter Ravn, Christian Bressen Pipper & Alexandre Aebi Biological Invasions ISSN 1387-3547 Volume 18 Number 2 Biol Invasions (2016) 18:517-532 DOI 10.1007/s10530-015-1024-y 1 23 Your article is protected by copyright and all rights are held exclusively by Springer International Publishing Switzerland. This e- offprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Biol Invasions (2016) 18:517–532 DOI 10.1007/s10530-015-1024-y ORIGINAL PAPER Potential for exploitative competition, not intraguild predation, between invasive harlequin ladybirds and flowerbugs in urban parks Andy G. Howe . Hans Peter Ravn . Christian Bressen Pipper . Alexandre Aebi Received: 31 December 2014 / Accepted: 19 November 2015 / Published online: 25 November 2015 Ó Springer International Publishing Switzerland 2015 Abstract In aphidophagous insect communities nemoralis DNA. The presence of lime aphid DNA in invaded by the harlequin ladybird Harmonia axyridis predators was higher: 56.5 and 47.9 % of H. axyridis Pallas (Coleoptera: Coccinellidae), intraguild preda- larvae and adults, respectively, contained E. tiliae tion (IGP) is widely implicated in the displacement of DNA, whereas 60.8 % of adult A. nemoralis tested native predators, however, indirect trophic interac- positive for aphid DNA. Incorporating insect densities tions are rarely assessed. Using molecular gut-content revealed that the density of H. axyridis larvae had a analysis, we investigated the relative frequencies of strong negative effect on the likelihood of detecting IGP by H. axyridis on the predatory flowerbug aphid DNA in A. nemoralis. Prey overlap for E. tiliae Anthocoris nemoralis Fabricius (Heteroptera: Antho- was widespread in space (2–13 m height in tree coridae) and prey overlap for a shared prey, the lime crowns) and time (May–October 2011) which sug- aphid Eucallipterus tiliae L. (Hemiptera: Aphididae), gests that interspecific exploitative competition, medi- in Tilia 9 europaea crowns in urban parks. The ated by predator life-stage, more so than IGP, is an frequency of IGP by H. axyridis was low: 2.7 % of important indirect trophic interaction between co- larvae and 3.4 % of adults tested positive for A. occurring H. axyridis and A. nemoralis. Whether exploitative competition equates to displacement of A. nemoralis populations requires further investigation. Electronic supplementary material The online version of Our results emphasize the need to incorporate indirect this article (doi:10.1007/s10530-015-1024-y) contains supple- mentary material, which is available to authorized users. interactions in studies of insect communities follow- ing invasion, not least because they potentially affect A. G. Howe (&) Á H. P. Ravn more species than direct interactions alone. Department of Geosciences and Natural Resource Management, University of Copenhagen, Rolighedsvej 23, 1958 Frederiksberg C, Denmark Keywords Indirect effects Á Molecular gut content Á e-mail: [email protected] Anthocoris nemoralis Á Harmonia axyridis Á Eucallipterus tiliae Á Predator–prey interactions C. B. Pipper Section of Biostatistics, Department of Public Health, University of Copenhagen, Øster Farimagsgade 5, 1014 Copenhagen K, Denmark Introduction A. Aebi Laboratoire de Biologie du Sol, Institut de biologie, Universite´ de Neuchaˆtel, Emile-Argand 11, Invasive generalist insect predators are typically 2000 Neuchaˆtel, Switzerland involved in complex ecological interactions with 123 Author's personal copy 518 A. G. Howe et al. members of invaded communities, often resulting in studies employing molecular gut-content techniques negative impacts on resident native species (Snyder reveal IGP of native coccinellids by invasive H. and Evans 2006; Crowder and Snyder 2010). As axyridis is spatially widespread and relatively intense, generalist invaders often achieve high densities in providing support that this mechanism contributes to introduced communities, and given the relatively short native species declines (Gagnon et al. 2011b; Brown time periods over which invasions occur, trophic et al. 2015). interactions might be particularly vulnerable to change Interspecific exploitative competition involves an by invaders with potential effects extending beyond indirect interaction between two species mediated single trophic levels (Snyder and Evans 2006; Kenis through changes in abundance of a third species et al. 2009). Within trophic communities species are (Lawton and Hassell 1984; White et al. 2006). An linked through a myriad of direct and/or indirect invasive generalist competitor may be superior at trophic interactions, most of which are not readily utilising a limited shared prey through better har- perceptible (White et al. 2006; Tylianakis 2008). By vesting ability and/or resource conversion efficiency, way of their omnivorous diets, invasive generalist and reduced density of the limiting resource can predators interact with multiple trophic levels in food result in indirect negative effects on native species, webs; not only do they consume herbivorous prey, but e.g. reduction in fecundity, growth or survival also other predators, detritivores, plants and/or detritus (Brown et al. 1994; Obrycki et al. 1998; Kasper may comprise parts of their diet (Polis and Strong et al. 2004; Evans et al. 2011). Resource competition 1996; Snyder and Evans 2006). among aphidophages is likely to be widespread due An invasive generalist predatory beetle implicated to the ephemeral distribution of aphids in space and in disruption of trophic interactions is Harmonia time (Hironori and Katsuhiro 1997; Dixon 1998; axyridis Pallas (Coleoptera: Coccinellidae). Origi- Osawa 2000; Ware et al. 2009). Predator niche nally introduced to North America as a biological overlap for shared prey involving H. axyridis pop- control agent (BCA) against aphids and coccids ulations in invaded communities has received limited (Chapin and Brou 1991; Brown et al. 2011b), long- attention (Pell et al. 2008; Kenis et al. 2010), despite term studies from North America have documented that niche overlap can contribute to native species coccinellid declines in agroecosystems (Michaud displacement (Kasper et al. 2004). On the other hand, 2002; Alyokhin and Sewell 2004; Harmon et al. spatial and temporal niche partitioning of competitors 2007), while the spread of H. axyridis in Europe has may reduce effects of interspecific interactions impinged several native coccinellids whose niches involving invasive generalist predators, thereby con- overlap (Adriaens et al. 2008; Brown et al. 2011a; Roy tributing to coexistence (Amarasekare 2003; Crowder et al. 2012). Intraguild predation (IGP) and resource and Snyder 2010). competition by H. axyridis are suspected of contribut- The predatory insect Anthocoris nemoralis F. ing to native species declines (Michaud 2002; Lucas (Heteroptera: Anthocoridae) is common throughout et al. 2007; Alhmedi et al. 2010; Roy et al. 2012). Western Europe (Pe´ricart 1996), and tracks prey on However, while studies of IGP by H. axyridis among leaf surfaces of deciduous trees (Anderson 1962; native coccinellids in agroecosystems have received Lattin 1999; Sigsgaard 2010). Both H. axyridis and A. most attention, indirect trophic interactions such as nemoralis are found on common lime Tilia 9 eu- exploitative and apparent competition have barely ropaea L., Malvaceae (Anderson 1962; Adriaens et al. been explored in the field (Alhmedi et al. 2010; Roy 2003; Brown et al. 2008), which also hosts the and Handley 2012). monophagous aphid and dominant herbivore Eucal- Intraguild predation occurs when predators sharing lipterus tiliae L. (Hemiptera: Aphididae; Dixon a common extraguild (EG) prey engage in predation of 1971a). Eucallipterus tiliae (EG prey; Fig. 1)is each other (Polis et al. 1989), and is often associated shared prey for H. axyridis (IG predator; Fig. 1) and with
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