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Indigenous arthropod natural enemies of the invasive brown marmorated stink bug in North America and Europe

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Abstract

Since the establishment of the brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) in North America and Europe, there has been a large, multi-group effort to characterize the composition and impact of the indigenous community of arthropod natural enemies attacking this invasive pest. In this review, we combine 98 indigenous natural enemy datasets spanning a variety of sampling methods, habitats, and geographic areas. To date, the vast majority of H. halys biological control research has focused on the egg stage, using sentinel egg masses to characterize indigenous parasitoid and predator communities and their contribution to H. halys egg mortality. Although egg parasitism and predation levels by indigenous natural enemies are low (typically <10% each) in most surveys, total egg mortality attributable to natural enemies can be higher (typically between 5 and 25%; up to 83%)—even though these values were likely underestimated in most cases because some mortality due to biological control was not recognized. In North America, where the most data are available, it appears that the relative prevalence of different indigenous parasitoid species varies among habitat types, particularly between crop and non-crop habitats. Predator species responsible for egg mortality are much less commonly identified, but appear to include a wide variety of generalist chewing and sucking predators. To date, studies of natural enemies attacking H. halys nymphs and adults are relatively rare. Based on our review, we identify a number of key research gaps and suggest several directions for future research.

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Acknowledgements

The authors wish to thank the following for research assistance collecting data used in this review: Clint Fleshman, Dana Martin, Chad Kramer, Lindsay Stump, Chelsea Berish, Sarah Detraz, Waydon Yates, the UKY farm crew, Emma Thrift, Treva Rowley, Nathan Erwin, Rose Borror, Zachary Johnson, Heather Leach, Megan Lowlor, Brooke Merrill, Devon Newsom, Gary Parason, Ryan Paul, Trisha Samota, McKenzie Allen, Brittany Poling, Morgan Douglas, Samuel Brandt, Torri Hancock, John Cullum, Adam Cave, Tina Dancau, Dennis Quach, Chris Hughes, Lot Miller, Kathy Wholaver, Katy Ellis, Silvia T. Moraglio, Marco G. Pansa, Kathy Tatman, Kylie Mendonca, Kody Transue, Max Sinton, Andrew Lyons, Elizabeth Fread, Abigail Rosenburg, Jeremy Turner, and Steve Schoof. We thank the following grower cooperators: Jeff Dickinson, Mike Laughlin, Sue Borton, Guy Ashmore, Redbud Farm, Barry Rice, and Scott Slaybaugh. Funding for the work synthesized in this review includes grants from the USDA-NIFA-OREI No. 2012-51300-20097; USDA-NIFA-SCRI Nos. 2011-51181-30937; USDA NE-1032 Multistate Hatch Project; Federally funded Specialty Crop Block Grant 13054, administered by the California Department of Food & Agriculture; State Horticultural Association of Pennsylvania; Pennsylvania State University Hatch Project No. Pen04619. The USDA does not endorse any commercial product mentioned in this research. USDA is an equal opportunity provider and employer.

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Authors and Affiliations

  1. Agriculture and Agri-Food Canada, Agassiz Research and Development Centre, Agassiz, BC, Canada

    Paul K. Abram

  2. Beneficial Insects Introduction Research Unit, USDA Agricultural Research Service, Newark, DE, USA

    Kim A. Hoelmer

  3. Alson H. Smith Jr. Agricultural Research and Extension Center, Virginia Tech, Winchester, VA, USA

    Angelita Acebes-Doria & J. Christopher Bergh

  4. Department of Horticulture, Oregon State University, Corvallis, OR, USA

    Heather Andrews, David Lowenstein & Nik G. Wiman

  5. Washington State University, Tree Fruit & Extension Center, Wenatchee, WA, USA

    Elizabeth H. Beers & Joshua M. Milnes

  6. Department of Entomology, University of Kentucky, Lexington, KY, USA

    Ric Bessin & Rachelyn Dobson

  7. Pennsylvania State University, Fruit Research & Extension Center, Biglerville, PA, USA

    David Biddinger

  8. Department of Entomology, Michigan State University, East Lansing, MI, USA

    Paul Botch, Ernest S. Delfosse, Matthew Grieshop & Kristin Poley

  9. Systematic Entomology Laboratory, USDA Agricultural Research Service, Washington, DC, USA

    Matthew L. Buffington & Elijah Talamas

  10. Invasive Insect Biocontrol and Behavior Laboratory, USDA Agricultural Research Service, Beltsville, MD, USA

    Mary L. Cornelius, Megan V. Herlihy & Donald C. Weber

  11. Department of Life Sciences, University of Modena and Reggio Emilia, Modena, Italy

    Elena Costi & Lara Maistrello

  12. Department of Entomology and Wildlife Ecology, University of Delaware, Newark, DE, USA

    Christine Dieckhoff

  13. Department of Plant Science and Landscape Architecture, University of Connecticut, Storrs, CT, USA

    Zachary Donais & Ana Legrand

  14. Department of Entomology, Rutgers University, New Brunswick, NJ, USA

    George Hamilton

  15. CABI, Delémont, Switzerland

    Tim Haye

  16. Oregon Department of Agriculture, Insect Pest Prevention & Management, Salem, OR, USA

    Christopher Hedstrom

  17. Department of Entomology, University of California, Riverside, CA, USA

    Mark S. Hoddle & Jesus Lara

  18. Department of Entomology, University of Maryland, College Park, MD, USA

    Cerruti R. R. Hooks, Paula M. Shrewsbury & Rebeccah Waterworth

  19. Hudson Valley Research Laboratory, Cornell University, Highland, NY, USA

    Peter Jentsch

  20. Department of Entomology, University of Arkansas, Fayetteville, AR, USA

    Neelendra K. Joshi

  21. Department of Entomology, Virginia Tech, Blacksburg, VA, USA

    Thomas P. Kuhar

  22. Horticultural Crops Research Unit, USDA Agricultural Research Service, Corvallis, OR, USA

    Jana C. Lee

  23. Appalachian Fruit Research Station, USDA Agricultural Research Service, Kearneysville, WV, USA

    Tracy C. Leskey

  24. Inst. Environmental & Physical Sciences, Shepherd University, Shepherdstown, WV, USA

    Clarissa R. Mathews

  25. Center for Grain and Animal Health Research, USDA Agricultural Research Service, Manhattan, KS, USA

    William R. Morrison III

  26. Rutgers Agricultural Research & Extension Center, Bridgeton, NJ, USA

    Anne L. Nielsen & John Pote

  27. Mountain Horticulture Research and Extension Center, North Carolina State University, Mills River, NC, USA

    Emily C. Ogburn & James F. Walgenbach

  28. California Department of Food and Agriculture, Sacramento, CA, USA

    Charles H. Pickett

  29. Department of Entomology, Ohio State University, Columbus, OH, USA

    James Radl & Celeste Welty

  30. Florida Department of Agriculture and Consumer Services, Division of Plant Industry/Entomology, Gainesville, FL, USA

    Elijah Talamas

  31. Department of Agricultural, Forest and Food Sciences, University of Turin, Turin, Italy

    Luciana Tavella

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  1. Paul K. Abram
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Corresponding author

Correspondence to Paul K. Abram.

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The authors have declared that no conflict of interest exists.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

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Communicated by M. Traugott.

Special Issue: The brown marmorated stink bug Halyomorpha halys an emerging pest of global concern.

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Abram, P.K., Hoelmer, K.A., Acebes-Doria, A. et al. Indigenous arthropod natural enemies of the invasive brown marmorated stink bug in North America and Europe. J Pest Sci 90, 1009–1020 (2017). https://doi.org/10.1007/s10340-017-0891-7

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