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Species assemblages of ladybirds including the harlequin ladybird Harmonia axyridis: a comparison at large spatial scale in urban habitats

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Abstract

We evaluated the status of native ladybird assemblages in the presence of the non-native ladybird Harmonia axyridis Pallas (Coleoptera: Coccinellidae) in three European countries. To achieve this, we assessed the abundance of ladybirds from common host plants in urban areas of Great Britain, Czech Republic and Slovak Republic in 2014. We determined (i) the effects of season, host plant, location, abundance of H. axyridis and aphids on the ladybird species assemblage, (ii) the relationship between ladybird abundance and aphid density, (iii) the relationship between diversity of native ladybird species and the abundance of H. axyridis. There was a non-linear relationship between abundance of ladybirds and abundance of aphids but we found the abundance of other ladybird species was not correlated with H. axyridis. We highlight the value of large-spatial scale studies for revealing patterns in community assemblages and ultimately informing understanding of ecosystem resilience.

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References

  • Adriaens T, y Gomez GSM, Maes D (2008) Invasion history, habitat preferences and phenology of the invasive ladybird Harmonia axyridis in Belgium. BioControl 53:69–88

    Article  Google Scholar 

  • Adriaens T, San Martin G, Hautier L, Branquart E, Maes D (2010) Toward a Noah’s Ark for native ladybirds in Belgium. IOBC/WPRS Bull 58:1–3

    Google Scholar 

  • Alyokhin A, Sewell G (2004) Changes in a lady beetle community following the establishment of three alien species. Biol Invasions 4:463–471

    Article  Google Scholar 

  • Bahlai CA, Colunga-Garcia M, Gage SH, Landis DA (2015) The role of exotic ladybeetles in the decline of native ladybeetle populations: evidence from long-term monitoring. Biol Invasions 17:1005–1024

    Article  Google Scholar 

  • Barahona-Segovia RM, Grez AA, Bozinovic F (2016) Testing the hypothesis of greater eurythermality in invasive than in native ladybird species: from physiological performance to life-history strategies. Ecol Entomol 41:182–191

    Article  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300

    Google Scholar 

  • Brown MW, Miller SS (1998) Coccinellidae (Coleoptera) in apple orchards of eastern West Virginia and the impact of invasion by Harmonia axyridis. Entomol News 109:143–151

    Google Scholar 

  • Brown PMJ, Adriaens T, Bathon H, Cuppen J, Goldarazena A, Hägg T, Kenis M, Klausnitzer BEM, Kovář I, Loomans AJM, Majerus MEN, Nedvěd O, Pedersen J, Rabitsch W, Roy HE, Ternois V, Zakharov IA, Roy DB (2008) Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. BioControl 53:5–21

    Article  Google Scholar 

  • Brown PMJ, Frost R, Doberski J, Sparks TIM, Harrington R, Roy HE (2011) Decline in native ladybirds in response to the arrival of Harmonia axyridis: early evidence from England. Ecol Entomol 36:231–240

    Article  Google Scholar 

  • Brown PMJ, Ingels B, Wheatley A, Rhule EL, de Clercq P, van Leeuwen T, Thomas A (2015) Intraguild predation by Harmonia axyridis (Coleoptera: Coccinellidae) on native insects in Europe: molecular detection from field samples. Entomol Sci 18:130–133

    Article  Google Scholar 

  • Burgio G, Ferrari R, Pozzati M, Boriani L (2004) The role of ecological compensation areas on predator populations: an analysis on biodiversity and phenology of Coccinellidae (Coleoptera) on non-crop plants within hedgerows in Northern Italy. Bull Insectol 57:1–10

    Google Scholar 

  • Canty A, Ripley B (2015) Boot: bootstrap R (S-Plus) functions. R package version 1:3–17

  • Comont RF, Roy HE, Harrington R, Shortall CR, Purse BV (2014) Ecological correlates of local extinction and colonisation in the British ladybird beetles (Coleoptera: Coccinellidae). Biol Invasions 16:1805–1817

    Article  Google Scholar 

  • Dixon AFG (2000) Insect predator-prey dynamics: ladybird beetles and biological control. Cambridge University Press, Cambridge

    Google Scholar 

  • Efron B, Tibshirani R (1986) Bootstrap methods for standard errors: confidence intervals and other measures of statistical accuracy. Stat Sci 1:54–77

    Article  Google Scholar 

  • Evans EW, Toler TR (2007) Aggregation of polyphagous predators in response to multiple prey: ladybirds (Coleoptera: Coccinellidae) foraging in alfalfa. Popul Ecol 49:29–36

    Article  Google Scholar 

  • Gardiner MM, Landis DA, Gratton C, Schmidt NP, O’Neal M, Mueller ED, Chacon J, Heimpel GE, DiFonzo CD (2009) Landscape composition influences patterns of native and exotic ladybeetle abundance. Divers Distrib 15:554–564

    Article  Google Scholar 

  • Grez AA, Zaviezo T, Hernández J, Pedro RS, Acuña P (2014) The heterogeneity and composition of agricultural landscapes influence native and exotic coccinellids in alfalfa fields. Agr Forest Entomol 16:382–390

    Article  Google Scholar 

  • Grez AA, Zaviezo T, Roy HE, Brown PMJ, Bizama G (2016) Rapid spread of Harmonia axyridis in Chile and its effects on local coccinellid biodiversity. Divers Distrib 22:982–994

    Article  Google Scholar 

  • Gruppe A (2007) Spatial distribution of Neuropterida in the LAK stand: significance of host tree specificity. In: Unterseher M, Morawetz W, Klotz S, Arndt E (eds) The canopy of a temperate floodplain forest. Universitätsverlag, Leipzig, pp 91–96

    Google Scholar 

  • Harmon JP, Stephens E, Losey J (2007) The decline of native coccinellids (Coleoptera: Coccinellidae) in the United States and Canada. J Insect Conserv 11:85–94

    Article  Google Scholar 

  • Haviar M (2007) Biodiversity of Ladybirds. PhD thesis. Comenius University in Bratislava, Bratislava

  • Honěk A (2012) Distribution and habitats. In: Hodek I, Honěk A, van Emden HF (eds) Ecology and behaviour of the ladybird beetles (Coccinellidae). Wiley, Chichester, pp 110–140

    Chapter  Google Scholar 

  • Honěk A, Martinková Z, Kindlmann P, Ameixa OM, Dixon AF (2014) Long-term trends in the composition of aphidophagous coccinellid communities in Central Europe. Insect Conserv Diver 7:55–63

    Article  Google Scholar 

  • Honěk A, Martinková Z, Dixon AF (2015) Detecting seasonal variation in composition of adult Coccinellidae communities. Ecol Entomol 40:543–552

    Article  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical J 50:346–363

    Article  Google Scholar 

  • Hui C, Richardson DM, Landi P, Minoarivelo HO, Garnas J, Roy HE (2016) Defining invasiveness and invasibility in ecological networks. Biol Invasions 18:971–983

    Article  Google Scholar 

  • Ingels B, de Clercq P (2010) Intraguild predation between Harmonia axyridis and the hoverfly Episyrphus balteatus. IOBC WPRS Bull 58:53–54

    Google Scholar 

  • Jansen JP, Hautier L (2008) Ladybird population dynamics in potato: comparison of native species with an invasive species, Harmonia axyridis. BioControl 53:223–233

    Article  Google Scholar 

  • Jost L (2006) Entropy and diversity. Oikos 113:363–375

    Article  Google Scholar 

  • Kindlmann P, Honěk A, Martinková Z (2017) Spreading of alien species and diversity of communities. BioControl. doi:10.1007/s10526-017-9787-y

  • Koch RL, Galvan TL (2008) Bad side of a good beetle: the North American experience with Harmonia axyridis. BioControl 53:23–35

    Article  Google Scholar 

  • Kozlov MV (2015) Changes in ladybird (Coleoptera: Coccinellidae) communities along a steep pollution gradient in subarctic forests of European Russia. Eur J Entomol 112:728–733

    Google Scholar 

  • Majerus MEN (1994) Ladybirds. Harper Collins Academic, London

    Google Scholar 

  • Majerus MEN, Strawson V, Roy HE (2006) The potential impacts of the arrival of the harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), in Britain. Ecol Entomol 31:207–215

  • Majzlan O (2013) Phenology and activity of beetles (Coleoptera) in calamity forest in High Tatras. Entomofauna Carpathica 25:21–30

    Google Scholar 

  • Megan WJ, Landis DA (2014) Coccinellid response to landscape composition and configuration. Agr For Entomol 16:341–349

    Article  Google Scholar 

  • Nault BA, Kennedy GG (2000) Seasonal changes in habitat preference by Coleomegilla maculata: implications for Colorado potato beetle management in potato. Biol Control 17:164–173

    Article  Google Scholar 

  • Nedvěd O (1999) Host complexes of predaceous ladybeetles (Coleoptera, Coccinellidae). J Appl Entomol 123:73–76

    Google Scholar 

  • Nedvěd O (2015) Ladybird beetles (Coccinellidae) of Central Europe. Academia, Praha

    Google Scholar 

  • O’Hara RB, Kotze DJ (2010) Do not log-transform count data. Methods Ecol Evol 1:118–122

    Article  Google Scholar 

  • Ormond EL, Thomas AP, Pugh PJ, Pell JK, Roy HE (2010) A fungal pathogen in time and space: the population dynamics of Beauveria bassiana in a conifer forest. FEMS Microbiol Ecol 74:146–154

    Article  CAS  PubMed  Google Scholar 

  • Pell JK, Baverstock J, Roy HE, Ware RL, Majerus MEN (2008) Intraguild predation involving Harmonia axyridis: a review of current knowledge and future perspectives. BioControl 53:147–168

    Article  Google Scholar 

  • Purse BV, Comont R, Butler A, Brown PMJ, Kessel C, Roy HE (2014) Landscape and climate determine patterns of spread for all colour morphs of the alien ladybird Harmonia axyridis. J Biogeogr 42:575–588

    Article  Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/

  • Ricci C, Ponti L (2005) Seasonal food of Ceratomegilla notata (Coleoptera: Coccinellidae) in mountain environments of Northern Italian Alps. Eur J Entomol 102:527–530

    Article  Google Scholar 

  • Roy HE, Brown PMJ (2015) Ten years of invasion: Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in Britain. Ecol Entomol 40:336–348

    Article  PubMed  PubMed Central  Google Scholar 

  • Roy HE, Lawson Handley LJ (2012) Networking: a community approach to invaders and their parasites. Funct Ecol 26:1238–1248

    Article  Google Scholar 

  • Roy HE, Brown P, Frost R, Poland R (2011) Atlas of the ladybirds (Coccinellidae) of Britain and Ireland. Biological Records Centre, Wallingford

    Google Scholar 

  • Roy HE, Adriaens T, Isaac NJB, Kenis M, Onkelinx T, San Martin G, Brown PMJ, Hautier L, Poland R, Roy DB, Comont R, Eschen R, Frost R, Zindel R, van Vlaenderen J, Nedvěd O, Ravn HP, Grégorie J-C, de Biseau J-C, Maes D (2012) Invasive alien predator causes rapid declines of native European ladybirds. Divers Distrib 18:717–725

    Article  Google Scholar 

  • Roy HE, Brown PMJ, Adriaens T, Berkvens N, Borges I, Clusella-Trullas S, De Clercq P, Eschen R, Estoup A, Evans EW, Facon B, Gardiner MM, Gil A, Grez A, Guillemaud T, Haelewaters D, Honek A, Howe AG, Hui C, Hutchison WD, Kenis M, Koch RL, Kulfan J, Lawson Handley L, Lombaert E, Loomans A, Losey J, Lukashuk AO, Maes D, Magro A, Murray KM, San Martin G, Martinkova Z, Minnaar I, Nedved O, Orlova-Bienkowskaja MJ, Rabitsch W, Peter Ravn H, Rondoni G, Rorke SL, Ryndevich SK, Saethre M-G, Onofre Soares A, Stals R, Tinsley MC, Vandereycken A, van Wielink P, Viglášová S, Zach P, Zaviezo T, Zhao Z (2016) The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol Invasions 18:997–1044

    Article  Google Scholar 

  • Savoiskaya GI (1983) Coccinellids. Izdatelstvo Nauka Kazakhskoi SSR, Alma-Ata

    Google Scholar 

  • Schellhorn NA, Andow DA (2005) Response of coccinellids to their aphid prey at different spatial scales. Popul Ecol 47:71–76

    Article  Google Scholar 

  • Selyemová D, Zach P, Nemethová D, Kulfan J, Úradník M, Holecová M, Kršiak B, Vargová K, Olšovský T (2007) Assemblage structure and altitudinal distribution of lady beetles (Coleoptera, Coccinellidae) in the mountain spruce forests of Poľana Mountains, the West Carpathians. Biologia 62:610–616

    Article  Google Scholar 

  • Sengonca C, Kranz J, Blaeser P (2002) Attractiveness of three weed species to polyphagous predators and their influence on aphid populations in adjacent lettuce cultivations. Anzeiger Für Schädlingskunde 75:161–165

    Article  Google Scholar 

  • Ter Braak CJF, Šmilauer P (2012) Canoco reference manual and user’s guide: software for ordination (Version 5.0). Microcomputer power, Itaca

  • Thomas AP, Trotman J, Wheatley A, Aebi A, Zindel R, Brown PM (2013) Predation of native coccinellids by the invasive alien Harmonia axyridis (Coleoptera: Coccinellidae): detection in Britain by PCR-based gut analysis. Insect Conserv Diver 6:20–27

    Article  Google Scholar 

  • Timms JEL, Leather SR (2008) How do the consumption and development rates of the conifer specialist Aphidecta obliterata respond to temperature, and is it better adapted to limited prey than a generalist? Ann Appl Biol 153:63–71

    Article  Google Scholar 

  • Timms JEL, Oliver TH, Straw NA, Leather SR (2008) The effects of host plant on the coccinellid functional response: is the conifer specialist Aphidecta obliterata (L.) (Coleoptera: Coccinellidae) better adapted to spruce than the generalist Adalia bipunctata (L.) (Coleoptera: Coccinellidae)? Biol Control 47:273–281

    Article  Google Scholar 

  • Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York

    Book  Google Scholar 

  • Wang Y, Naumann U, Wright S, Eddelbuettel D, Warton D (2016) mvabund: statistical methods for analysing multivariate abundance data. R package version 3.11.9

  • Woin N, Volkmar C, Wetzel T (2000) Seasonal activity and diversity of ladybirds (Coleoptera: Coccinellidae) as ecological bioindicators in paddy fields. Mitteilungen der Deutschen Gesellschaft für Allgemeine und Angewandte Entomologie 12:203–206

    Google Scholar 

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Acknowledgements

The authors acknowledge Lukáš Fiedler and Katie Murray for help in sampling of ladybirds, the EU COST (TD1209 and LD14084) Action Alien Challenge, VEGA 2/0052/15 and 2/0012/17, APVV 14-0567 and grant 7AMB14SK016 provided by the Ministry of Education of the Czech Republic. Helen Roy is funded through the Biological Record Centre, part of the Centre for Ecology & Hydrology, which receives support from the Joint Nature Conservation Committee and the Natural Environment Research Council (via National Capability funding to the Centre for Ecology & Hydrology, Project NEC04932).

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Authors and Affiliations

  1. Institute of Forest Ecology, Slovak Academy of Sciences, Ľ. Štúra 2, 960 53, Zvolen, Slovak Republic

    Sandra Viglášová, Peter Zach, Ján Kulfan & Michal Parák

  2. Faculty of Science, University of South Bohemia, Branišovská 1760, 370 05, České Budějovice, Czech Republic

    Oldřich Nedvěd

  3. Institute of Entomology, Biology Centre AS CR, Branišovská 31, 370 05, České Budějovice, Czech Republic

    Oldřich Nedvěd

  4. Crop Research Institute, Drnovská 507/73, Ruzyně, 161 06, Prague – 6, Czech Republic

    Alois Honěk & Zdenka Martinková

  5. Centre for Ecology & Hydrology, Wallingford, OX10 8BB, UK

    Helen E. Roy

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  1. Sandra Viglášová
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  2. Oldřich Nedvěd
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Correspondence to Sandra Viglášová.

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Viglášová, S., Nedvěd, O., Zach, P. et al. Species assemblages of ladybirds including the harlequin ladybird Harmonia axyridis: a comparison at large spatial scale in urban habitats. BioControl 62, 409–421 (2017). https://doi.org/10.1007/s10526-017-9793-0

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