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The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology

  • Insect Invasions
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Abstract

The harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), is native to Asia but has been intentionally introduced to many countries as a biological control agent of pest insects. In numerous countries, however, it has been introduced unintentionally. The dramatic spread of H. axyridis within many countries has been met with considerable trepidation. It is a generalist top predator, able to thrive in many habitats and across wide climatic conditions. It poses a threat to biodiversity, particularly aphidophagous insects, through competition and predation, and in many countries adverse effects have been reported on other species, particularly coccinellids. However, the patterns are not consistent around the world and seem to be affected by many factors including landscape and climate. Research on H. axyridis has provided detailed insights into invasion biology from broad patterns and processes to approaches in surveillance and monitoring. An impressive number of studies on this alien species have provided mechanistic evidence alongside models explaining large-scale patterns and processes. The involvement of citizens in monitoring this species in a number of countries around the world is inspiring and has provided data on scales that would be otherwise unachievable. Harmonia axyridis has successfully been used as a model invasive alien species and has been the inspiration for global collaborations at various scales. There is considerable scope to expand the research and associated collaborations, particularly to increase the breadth of parallel studies conducted in the native and invaded regions. Indeed a qualitative comparison of biological traits across the native and invaded range suggests that there are differences which ultimately could influence the population dynamics of this invader. Here we provide an overview of the invasion history and ecology of H. axyridis globally with consideration of future research perspectives. We reflect broadly on the contributions of such research to our understanding of invasion biology while also informing policy and people.

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Acknowledgments

The paper had its origin at a workshop on “Drivers, impacts, mechanisms and adaptation in insect invasions” hosted by the DST-NRF Centre of Excellence for Invasion Biology in Stellenbosch, South Africa, in November 2014. Additional financial support was provided by HortGro, the National Research Foundation of South Africa, Stellenbosch University, and SubTrop. We thank all our collaborators, and particularly the volunteer community, who have contributed to research around the world on H. axyridis. The number of references included reflects the range of inspiring studies on H. axyridis from so many people—we look forward to new and continued collaborations in the future. We are grateful to the editors of this special issue for inviting this review and providing an opportunity to explore ideas through the “Invasive Insects Workshop funding (NRF South Africa, CIB)”. We also thank the anonymous reviewers for all their useful comments and reflections. The UK Ladybird Survey and associated co-authors are supported by the Biological Records Centre (part of the Centre for Ecology & Hydrology), which receives support from both the Natural Environment Research Council and the Joint Nature Conservation Committee. The IOBC WPRS and Global Working Groups “Benefits and Risks of Exotic Biological Control Agents” and the COST Action TD1209 “Alien Challenge” have facilitated discussions and collaborations on H. axyridis. This study was supported by the French Agropolis Fondation (Labex Agro-Montpellier, BIOFIS Project Number 1001-001) and by a grant from the ERA-Net BiodivERsA, with the national funders ANR (France), DFG (Germany) and BELSPO (Belgium), as part of the 2012–2013 BiodivERsA call for research proposals. Support has been also received from FONDECYT 1140662 (Chile). The study of M.J. Orlova-Bienkowskaja and I. A. Zakharov was supported by Russian Science Foundation, Project No. 16-16- 00079. Gabriele Rondoni acknowledges financial support from Fondazione Cassa di Risparmio di Perugia. Riaan Stals acknowledges funding from the Department of Science and Technology, South Africa. The research of Peter Zach and colleagues was funded by the project VEGA 2/0035/13 and VEGA 2/0052/15. A. Honěk and Z. Martinkova were supported by grants GACR 14-26561S and COST CZ LD14084. Research in Switzerland is funded by the Swiss Federal Office for the Environment. Hans Peter Ravn was supported by the Villum Foundation. Danny Haelewaters acknowledges funding from the David Rockefeller Center for Latin American Studies at Harvard University and from the Mycological Society of America.

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Authors and Affiliations

  1. Centre for Ecology and Hydrology, Wallingford, Oxfordshire, OX10 8BB, UK

    Helen E. Roy, Steph L. Rorke & Sandra Viglášová

  2. Animal and Environment Research Group, Anglia Ruskin University, Cambridge, CB1 1PT, UK

    Peter M. J. Brown

  3. Research Institute for Nature and Forest (INBO), Kliniekstraat 25, 1070, Brussels, Belgium

    Tim Adriaens & Dirk Maes

  4. Institute for Agricultural and Fisheries Research, Department of Plant Crop Protection Entomology, Burgemeester Van Gansberghelaan 96, 9820, Merelbeke, Belgium

    Nick Berkvens

  5. cE3c - ABG - Center for Ecology, Evolution and Environmental Changes and Azorean Biodiversity Group, Department of Biology, University of the Azores, 9501-801, Ponta Delgada, Portugal

    Isabel Borges, Artur Gil & Antonio Onofre Soares

  6. Centre for Invasion Biology, Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Matieland, 7602, South Africa

    Susana Clusella-Trullas & Ingrid A. Minnaar

  7. Bumblebee Conservation Trust, Stirling, UK

    Richard F. Comont

  8. Department of Crop Protection, Ghent University, Coupure Links 653, 9000, Ghent, Belgium

    Patrick De Clercq

  9. CABI, Delémont, Switzerland

    Rene Eschen & Marc Kenis

  10. Inra, UMR 1062 Cbgp, Montpellier, France

    Arnaud Estoup & Benoit Facon

  11. Department of Biology, Utah State University, Logan, UT, 84322-5305, USA

    Edward W. Evans

  12. Department of Entomology, The Ohio State University Ohio Agricultural Research and Development Center, 1680 Madison Avenue, Wooster, OH, USA

    Mary M. Gardiner

  13. Facultad de Ciencias Veterinarias y Pecuarias, Universidad de Chile, Casilla 2-15, Santiago, Chile

    Audrey A. Grez

  14. Inra, UMR 1355 ISA, Sophia-Antipolis, France

    Thomas Guillemaud & Eric Lombaert

  15. Université de Nice Sophia Antipolis, UMR ISA, Sophia-Antipolis, France

    Thomas Guillemaud & Eric Lombaert

  16. CNRS, UMR 7254 ISA, Sophia-Antipolis, France

    Thomas Guillemaud & Eric Lombaert

  17. Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, 02138, USA

    Danny Haelewaters

  18. Farlow Reference Library and Herbarium of Cryptogamic Botany, Harvard University, 22 Divinity Avenue, Cambridge, MA, 02138, USA

    Danny Haelewaters

  19. Institute for Biological Control, JKI, Heinrichstr 243, 64287, Darmstadt, Germany

    Annette Herz

  20. Crop Research Institute, Prague-Ruzyne, Czech Republic

    Alois Honek & Zdenka Martinkova

  21. Department of Geosciences and Natural Resource Management, University of Copenhagen, Rolighedsvej 23, 1958, Frederiksberg, Denmark

    Andy G. Howe & Hans Peter Ravn

  22. Centre for Invasion Biology, Department of Mathematical Sciences, Stellenbosch University, Matieland, 7602, South Africa

    Cang Hui

  23. The African Institute for Mathematical Sciences, Cape Town, 7945, South Africa

    Cang Hui

  24. Department of Entomology, University of Minnesota, Saint Paul, MN, 55108, USA

    William D. Hutchison & Robert L. Koch

  25. Institute of Forest Ecology, Slovak Academy of Sciences, Zvolen, Slovakia

    Jan Kulfan, Sandra Viglášová & Peter Zach

  26. Evolutionary Biology Group, Department of Biological Sciences, University of Hull, Hull, UK

    Lori Lawson Handley

  27. Department of Entomology, National Reference Centre, National Plant Protection Organization, P.O. Box 9102, 6700 HC, Wageningen, The Netherlands

    Antoon Loomans

  28. Department of Entomology, Cornell University, Ithaca, NY, 14853, USA

    John Losey

  29. Berezinskiy Biosphere Reserve, Domzheritsy, 211188, Lepel Distr., Vitebsk Reg., Belarus

    Alexander O. Lukashuk

  30. University of Toulouse - ENFA, UMR CNRS/UPS/ENFA 5174 Évolution et diversité biologique, 31326, Castanet-Tolosan, France

    Alexandra Magro

  31. Biological and Environmental Sciences, Stirling University, Stirling, FK9 4LA, UK

    Katie M. Murray & Matthew C. Tinsley

  32. Plant Protection and Ecotoxicology Unit, Life Sciences Department, Walloon Agricultural Research Centre, Rue de Liroux 2, 5030, Gembloux, Belgium

    Gilles San Martin

  33. University of South Bohemia and Institute of Entomology, Ceske Budejovice, Czech Republic

    Oldřich Nedved

  34. A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, 33 Leninskiy Prospect, Moscow, Russia, 119071

    Marina J. Orlova-Bienkowskaja

  35. Graduate School of Agriculture, Kyoto University, Kitashirakawa Oiwake-cho, Sakyo-ku, Kyoto, 606-8502, Japan

    Naoya Osawa

  36. Environment Agency Austria, Vienna, Austria

    Wolfgang Rabitsch

  37. Department of Agricultural, Food and Environmental Sciences, University of Perugia, Borgo XX Giugno 74, 06121, Perugia, Italy

    Gabriele Rondoni

  38. Baranovichi State University, Voykova str. 21, 225404, Baranovichi, Brest Reg., Belarus

    Sergey K. Ryndevich

  39. Biotechnology and Plant Health Division, Department of Entomology and Nematology, Bioforsk - NIBIO-Norwegian Institute of Bioeconomy Research, Høgskoleveien 7, 1432, Ås, Norway

    May-Guri Saethre

  40. Maastricht Science Programme, Maastricht University, P.O. Box 616, 6200 MD, Maastricht, The Netherlands

    John J. Sloggett

  41. South African National Collection of Insects, ARC-Plant Protection Research, Private Bag X134, Queenswood, Pretoria, 0121, South Africa

    Riaan Stals

  42. Gembloux Agro-Bio Tech, Functional and Evolutionary Entomology, University of Liege, Passage des Déportés 2, 5030, Gembloux, Belgium

    Axel Vandereycken

  43. Tobias Asserlaan 126, 5056 VD, Berkel-Enschot, The Netherlands

    Paul van Wielink

  44. Vavilov Institute of General Genetics, Gubkin Str. 3, Moscow, Russia, 119991

    Ilya A. Zakharov

  45. Facultad de Agronomía e Ingeniería Forestal, Pontificia Universidad Católica de Chile, Casilla 306-22, Santiago, Chile

    Tania Zaviezo

  46. Department of Entomology, China Agricultural University, Beijing, 100193, China

    Zihua Zhao

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Corresponding author

Correspondence to Helen E. Roy.

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Guest editors: Matthew P. Hill, Susana Clusella-Trullas, John S. Terblanche & David M. Richardson / Insect Invasions

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Roy, H.E., Brown, P.M.J., Adriaens, T. et al. The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol Invasions 18, 997–1044 (2016). https://doi.org/10.1007/s10530-016-1077-6

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