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Journal of Pest Science

, Volume 90, Issue 4, pp 1009–1020 | Cite as

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

  • Paul K. AbramEmail author
  • Kim A. Hoelmer
  • Angelita Acebes-Doria
  • Heather Andrews
  • Elizabeth H. Beers
  • J. Christopher Bergh
  • Ric Bessin
  • David Biddinger
  • Paul Botch
  • Matthew L. Buffington
  • Mary L. Cornelius
  • Elena Costi
  • Ernest S. Delfosse
  • Christine Dieckhoff
  • Rachelyn Dobson
  • Zachary Donais
  • Matthew Grieshop
  • George Hamilton
  • Tim Haye
  • Christopher Hedstrom
  • Megan V. Herlihy
  • Mark S. Hoddle
  • Cerruti R. R. Hooks
  • Peter Jentsch
  • Neelendra K. Joshi
  • Thomas P. Kuhar
  • Jesus Lara
  • Jana C. Lee
  • Ana Legrand
  • Tracy C. Leskey
  • David Lowenstein
  • Lara Maistrello
  • Clarissa R. Mathews
  • Joshua M. Milnes
  • William R. MorrisonIII
  • Anne L. Nielsen
  • Emily C. Ogburn
  • Charles H. Pickett
  • Kristin Poley
  • John Pote
  • James Radl
  • Paula M. Shrewsbury
  • Elijah Talamas
  • Luciana Tavella
  • James F. Walgenbach
  • Rebeccah Waterworth
  • Donald C. Weber
  • Celeste Welty
  • Nik G. Wiman
Review

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.

Keywords

Invasive species Biological control Parasitoids Predators Pentatomidae Halyomorpha halys 

Notes

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.

Compliance with ethical standards

Conflict of interest

The authors have declared that no conflict of interest exists.

Ethical approval

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.

Supplementary material

10340_2017_891_MOESM1_ESM.xlsx (27 kb)
Supplementary material 1 (XLSX 27 kb)

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Copyright information

© Her Majesty the Queen in Right of Canada 2017

Authors and Affiliations

  • Paul K. Abram
    • 1
    Email author
  • Kim A. Hoelmer
    • 2
  • Angelita Acebes-Doria
    • 3
  • Heather Andrews
    • 4
  • Elizabeth H. Beers
    • 5
  • J. Christopher Bergh
    • 3
  • Ric Bessin
    • 6
  • David Biddinger
    • 7
  • Paul Botch
    • 8
  • Matthew L. Buffington
    • 9
  • Mary L. Cornelius
    • 10
  • Elena Costi
    • 11
  • Ernest S. Delfosse
    • 8
  • Christine Dieckhoff
    • 12
  • Rachelyn Dobson
    • 6
  • Zachary Donais
    • 13
  • Matthew Grieshop
    • 8
  • George Hamilton
    • 14
  • Tim Haye
    • 15
  • Christopher Hedstrom
    • 16
  • Megan V. Herlihy
    • 10
  • Mark S. Hoddle
    • 17
  • Cerruti R. R. Hooks
    • 18
  • Peter Jentsch
    • 19
  • Neelendra K. Joshi
    • 20
  • Thomas P. Kuhar
    • 21
  • Jesus Lara
    • 17
  • Jana C. Lee
    • 22
  • Ana Legrand
    • 13
  • Tracy C. Leskey
    • 23
  • David Lowenstein
    • 4
  • Lara Maistrello
    • 11
  • Clarissa R. Mathews
    • 24
  • Joshua M. Milnes
    • 5
  • William R. MorrisonIII
    • 25
  • Anne L. Nielsen
    • 26
  • Emily C. Ogburn
    • 27
  • Charles H. Pickett
    • 28
  • Kristin Poley
    • 8
  • John Pote
    • 26
  • James Radl
    • 29
  • Paula M. Shrewsbury
    • 18
  • Elijah Talamas
    • 9
    • 30
  • Luciana Tavella
    • 31
  • James F. Walgenbach
    • 27
  • Rebeccah Waterworth
    • 18
  • Donald C. Weber
    • 10
  • Celeste Welty
    • 29
  • Nik G. Wiman
    • 4
  1. 1.Agriculture and Agri-Food Canada, Agassiz Research and Development CentreAgassizCanada
  2. 2.Beneficial Insects Introduction Research UnitUSDA Agricultural Research ServiceNewarkUSA
  3. 3.Alson H. Smith Jr. Agricultural Research and Extension CenterVirginia TechWinchesterUSA
  4. 4.Department of HorticultureOregon State UniversityCorvallisUSA
  5. 5.Washington State University, Tree Fruit & Extension CenterWenatcheeUSA
  6. 6.Department of EntomologyUniversity of KentuckyLexingtonUSA
  7. 7.Pennsylvania State University, Fruit Research & Extension CenterBiglervilleUSA
  8. 8.Department of EntomologyMichigan State UniversityEast LansingUSA
  9. 9.Systematic Entomology LaboratoryUSDA Agricultural Research ServiceWashingtonUSA
  10. 10.Invasive Insect Biocontrol and Behavior LaboratoryUSDA Agricultural Research ServiceBeltsvilleUSA
  11. 11.Department of Life SciencesUniversity of Modena and Reggio EmiliaModenaItaly
  12. 12.Department of Entomology and Wildlife EcologyUniversity of DelawareNewarkUSA
  13. 13.Department of Plant Science and Landscape ArchitectureUniversity of ConnecticutStorrsUSA
  14. 14.Department of EntomologyRutgers UniversityNew BrunswickUSA
  15. 15.CABIDelémontSwitzerland
  16. 16.Oregon Department of Agriculture, Insect Pest Prevention & ManagementSalemUSA
  17. 17.Department of EntomologyUniversity of CaliforniaRiversideUSA
  18. 18.Department of EntomologyUniversity of MarylandCollege ParkUSA
  19. 19.Hudson Valley Research LaboratoryCornell UniversityHighlandUSA
  20. 20.Department of EntomologyUniversity of ArkansasFayettevilleUSA
  21. 21.Department of EntomologyVirginia TechBlacksburgUSA
  22. 22.Horticultural Crops Research UnitUSDA Agricultural Research ServiceCorvallisUSA
  23. 23.Appalachian Fruit Research StationUSDA Agricultural Research ServiceKearneysvilleUSA
  24. 24.Inst. Environmental & Physical SciencesShepherd UniversityShepherdstownUSA
  25. 25.Center for Grain and Animal Health ResearchUSDA Agricultural Research ServiceManhattanUSA
  26. 26.Rutgers Agricultural Research & Extension CenterBridgetonUSA
  27. 27.Mountain Horticulture Research and Extension CenterNorth Carolina State UniversityMills RiverUSA
  28. 28.California Department of Food and AgricultureSacramentoUSA
  29. 29.Department of EntomologyOhio State UniversityColumbusUSA
  30. 30.Florida Department of Agriculture and Consumer Services, Division of Plant Industry/EntomologyGainesvilleUSA
  31. 31.Department of Agricultural, Forest and Food SciencesUniversity of TurinTurinItaly

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