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BioControl

, Volume 62, Issue 3, pp 355–371 | Cite as

Parasites of Harmonia axyridis: current research and perspectives

  • Danny Haelewaters
  • Serena Y. Zhao
  • Susana Clusella-Trullas
  • Ted E. Cottrell
  • André De Kesel
  • Lukáš Fiedler
  • Annette Herz
  • Helen Hesketh
  • Cang Hui
  • Regina G. Kleespies
  • John E. Losey
  • Ingrid A. Minnaar
  • Katie M. Murray
  • Oldřich Nedvěd
  • Walter P. Pfliegler
  • C. Lidwien Raak-van den Berg
  • Eric W. Riddick
  • David I. Shapiro-Ilan
  • Rebecca R. Smyth
  • Tove Steenberg
  • Paul S. van Wielink
  • Sandra Viglášová
  • Zihua Zhao
  • Piotr Ceryngier
  • Helen E. Roy
Review

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.

Keywords

Coccipolipus hippodamiae Enemy release hypothesis Harmonia axyridis Hesperomyces virescens Parasites Parasitylenchus bifurcatus 

Notes

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.

Supplementary material

10526_2016_9766_MOESM1_ESM.pdf (1.1 mb)
Supplementary material 1 (PDF 1122 kb)
10526_2016_9766_MOESM2_ESM.xls (310 kb)
Supplementary material 2 (XLS 310 kb)

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Copyright information

© International Organization for Biological Control (IOBC) 2016

Authors and Affiliations

  • Danny Haelewaters
    • 1
  • Serena Y. Zhao
    • 2
  • Susana Clusella-Trullas
    • 3
  • Ted E. Cottrell
    • 4
  • André De Kesel
    • 5
  • Lukáš Fiedler
    • 6
  • Annette Herz
    • 7
  • Helen Hesketh
    • 8
  • Cang Hui
    • 9
  • Regina G. Kleespies
    • 7
  • John E. Losey
    • 10
  • Ingrid A. Minnaar
    • 3
  • Katie M. Murray
    • 11
  • Oldřich Nedvěd
    • 12
  • Walter P. Pfliegler
    • 13
  • C. Lidwien Raak-van den Berg
    • 14
    • 15
  • Eric W. Riddick
    • 16
  • David I. Shapiro-Ilan
    • 4
  • Rebecca R. Smyth
    • 10
  • Tove Steenberg
    • 17
  • Paul S. van Wielink
    • 18
  • Sandra Viglášová
    • 19
  • Zihua Zhao
    • 20
  • Piotr Ceryngier
    • 21
  • Helen E. Roy
    • 8
  1. 1.Department of Organismic and Evolutionary BiologyHarvard UniversityCambridgeUSA
  2. 2.Department of Integrative BiologyThe University of Texas at AustinAustinUSA
  3. 3.Centre for Invasion Biology, Department of Botany and ZoologyStellenbosch UniversityStellenboschSouth Africa
  4. 4.Southeastern Fruit and Tree Nut Research Laboratory, Agricultural Research ServiceUnited States Department of AgricultureByronUSA
  5. 5.Botanic Garden MeiseMeiseBelgium
  6. 6.Gymnázium Jírovcova and University of South BohemiaCeske BudejoviceCzech Republic
  7. 7.Institute for Biological Control, Federal Research Centre for Cultivated PlantsJulius Kühn-InstituteDarmstadtGermany
  8. 8.Centre for Ecology & HydrologyWallingfordUK
  9. 9.Centre for Invasion Biology, Department of Mathematical SciencesStellenbosch University, and African Institute for Mathematical SciencesStellenboschSouth Africa
  10. 10.Department of EntomologyCornell UniversityIthacaUSA
  11. 11.Biological and Environmental SciencesStirling UniversityStirlingUK
  12. 12.University of South Bohemia and Institute of EntomologyCeske BudejoviceCzech Republic
  13. 13.Department of Biotechnology and MicrobiologyUniversity of Debrecen, and Postdoctoral Fellowship Programme of the Hungarian Academy of Sciences (MTA)DebrecenHungary
  14. 14.Laboratory of EntomologyWageningen UniversityUtrechtThe Netherlands
  15. 15.Netherlands Food and Consumer Product Safety AuthorityUtrechtThe Netherlands
  16. 16.Agricultural Research Service, National Biological Control LaboratoryUnited States Department of AgricultureStonevilleUSA
  17. 17.Department of AgroecologyUniversity of AarhusAarhusDenmark
  18. 18.Berkel-EnschotThe Netherlands
  19. 19.Institute of Forest EcologySlovak Academy of SciencesZvolenSlovakia
  20. 20.Department of Entomology, College of Plant ProtectionChina Agricultural UniversityBeijingChina
  21. 21.Faculty of Biology and Environmental SciencesCardinal Stefan Wyszyński UniversityWarsawPoland

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