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Parasites of Harmonia axyridis: current research and perspectives

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Abstract

Harmonia axyridis (Coleoptera: Coccinellidae) has been introduced widely for biological control of agricultural pests. Harmonia axyridis has established in four continents outside of its native range in Asia and it is considered an invasive alien species (IAS). Despite a large body of work on invasion ecology, establishment mechanisms of IAS and their interactions with natural enemies remain open questions. Parasites, defined as multicellular organisms that do not directly kill the host, could potentially play an important role in regulating host populations. This study presents a review of the parasites of H. axyridis, discussing their distributions and effects on host populations across the host’s native and invasive range. These parasites are: Hesperomyces virescens Thaxt. fungi, Coccipolipus hippodamiae (McDaniel and Morrill) mites, and Parasitylenchus bifurcatus Poinar and Steenberg nematodes.

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Acknowledgments

This manuscript has greatly benefited from various contributions of many researchers, collaborators, citizen scientists, and friends. Specifically, we thank: Robin M. Giblin-Davis (University of Florida, USA) for nematode-technical advice; Audrey A. Grez (Universidad de Chile) and Tania Zaviezo (Pontificia Universidad Católica de Chile) for the identification confirmation of the Argentine ladybird; Christopher Chen (Harvard College), Timothy Y. James (University of Michigan), and Tamara Szentiványi (University of Lausanne) for sharing data; Wendy Derjue-Holzer for collecting ladybirds at her parents’ house; and Bruce C. Bolin, Larry Clarfeld, John Friel, Michel Gomez, Anita Gould, David LaMason, Robert Pilla, Luciano Richino, and Christian Schwarz for their attentiveness to spot and photograph ladybirds infected with H. virescens. DH and SYZ acknowledge substantial curatorial support from James H. Boone (Field Museum of Natural History, Chicago, USA), Donald S. Chandler (University of New Hampshire), Brian D. Farrell and Philip Perkins (Harvard Museum of Comparative Zoology), Lee H. Herman (American Museum of Natural History, New York, USA), Jean-Philippe Légaré and Joseph Moisan-De Serres (Collection d’insectes du Québec at MAPAQ), Hong-bin Liang and Meiying Lin (Institute of Zoology, Chinese Academy of Sciences, Beijing, China), Shinya Miyano (Natural History Museum and Institute, Chiba, Japan), Shuhei Nomura (National Museum of Nature and Science, Tokyo, Japan), Mark F. O’Brien (University of Michigan Museum of Zoology), Shigehiko Shiyake (Osaka Museum of Natural History, Japan), Genevieve E. Tocci (Farlow Herbarium, Harvard University), and Natalia J. Vandenberg (National Museum of Natural History, Smithsonian Institution). DH acknowledges funding of the David Rockefeller Center for Latin American Studies at Harvard University and the American Museum of Natural History (New York, USA). Thanks are due to Andrew G. Howe and two anonymous reviewers for considerably improving the manuscript.

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Authors and Affiliations

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

    Danny Haelewaters

  2. Department of Integrative Biology, The University of Texas at Austin, Austin, TX, USA

    Serena Y. Zhao

  3. Centre for Invasion Biology, Department of Botany and Zoology, Stellenbosch University, Stellenbosch, South Africa

    Susana Clusella-Trullas & Ingrid A. Minnaar

  4. Southeastern Fruit and Tree Nut Research Laboratory, Agricultural Research Service, United States Department of Agriculture, Byron, GA, USA

    Ted E. Cottrell & David I. Shapiro-Ilan

  5. Botanic Garden Meise, Meise, Belgium

    André De Kesel

  6. Gymnázium Jírovcova and University of South Bohemia, Ceske Budejovice, Czech Republic

    Lukáš Fiedler

  7. Institute for Biological Control, Federal Research Centre for Cultivated Plants, Julius Kühn-Institute, Darmstadt, Germany

    Annette Herz & Regina G. Kleespies

  8. Centre for Ecology & Hydrology, Wallingford, UK

    Helen Hesketh & Helen E. Roy

  9. Centre for Invasion Biology, Department of Mathematical Sciences, Stellenbosch University, and African Institute for Mathematical Sciences, Stellenbosch, South Africa

    Cang Hui

  10. Department of Entomology, Cornell University, Ithaca, NY, USA

    John E. Losey & Rebecca R. Smyth

  11. Biological and Environmental Sciences, Stirling University, Stirling, UK

    Katie M. Murray

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

    Oldřich Nedvěd

  13. Department of Biotechnology and Microbiology, University of Debrecen, and Postdoctoral Fellowship Programme of the Hungarian Academy of Sciences (MTA), Debrecen, Hungary

    Walter P. Pfliegler

  14. Laboratory of Entomology, Wageningen University, Utrecht, The Netherlands

    C. Lidwien Raak-van den Berg

  15. Netherlands Food and Consumer Product Safety Authority, Utrecht, The Netherlands

    C. Lidwien Raak-van den Berg

  16. Agricultural Research Service, National Biological Control Laboratory, United States Department of Agriculture, Stoneville, MS, USA

    Eric W. Riddick

  17. Department of Agroecology, University of Aarhus, Aarhus, Denmark

    Tove Steenberg

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

    Paul S. van Wielink

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

    Sandra Viglášová

  20. Department of Entomology, College of Plant Protection, China Agricultural University, Beijing, China

    Zihua Zhao

  21. Faculty of Biology and Environmental Sciences, Cardinal Stefan Wyszyński University, Warsaw, Poland

    Piotr Ceryngier

Authors
  1. Danny Haelewaters
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  2. Serena Y. Zhao
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  3. Susana Clusella-Trullas
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  4. Ted E. Cottrell
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  5. André De Kesel
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  7. Annette Herz
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  8. Helen Hesketh
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  9. Cang Hui
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  10. Regina G. Kleespies
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  11. John E. Losey
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  12. Ingrid A. Minnaar
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  13. Katie M. Murray
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  14. Oldřich Nedvěd
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  15. Walter P. Pfliegler
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  16. C. Lidwien Raak-van den Berg
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  17. Eric W. Riddick
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  18. David I. Shapiro-Ilan
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  19. Rebecca R. Smyth
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  20. Tove Steenberg
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  21. Paul S. van Wielink
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  22. Sandra Viglášová
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  23. Zihua Zhao
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  24. Piotr Ceryngier
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  25. Helen E. Roy
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Corresponding author

Correspondence to Danny Haelewaters.

Additional information

Handling Editor: Lori-Jayne Lawson Handley.

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Haelewaters, D., Zhao, S.Y., Clusella-Trullas, S. et al. Parasites of Harmonia axyridis: current research and perspectives. BioControl 62, 355–371 (2017). https://doi.org/10.1007/s10526-016-9766-8

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  • DOI: https://doi.org/10.1007/s10526-016-9766-8

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