Integrative review of indigenous arthropod natural enemies of the invasive brown marmorated stink bug in North America and Europe

Authors: ABRAM, PAUL - Agriculture And Agri-Food Canada; Hoelmer, Kim; ACEBES-DORIA, ANGEL - Virginia Tech; ANDREWS, HEATHER - Oregon State University; BEERS, ELIZABETH - Washington State University; BERGH, CHRISTOPHER - Virginia Tech; BESSIN, RIC - University Of Kentucky; BIDDINGER, DAVID - Pennsylvania State University; BOTCH, PAUL - Michigan State University; Buffington, Matthew; Cornelius, Mary; COSTI, ELENA - University Of Modena And Reggio Emilia (UNIMORE); DELFOSSE, ERNEST - Michigan State University; DIECKHOFF, CHRISTINE - University Of Delaware; DOBSON, RACHELYN - University Of Kentucky; DONAIS, ZACHARY - University Of Connecticut; GRIESHOP, MATT - Michigan State University; HAMILTON, GEORGE - Rutgers University; HAYE, TIM - Commonwealth Agricultural Bureau International (CABI) - Switzerland; HEDSTROM, CHRIS - Oregon Department Of Agriculture; Herlihy-Adams, Megan; HODDLE, MARK - University Of California; HOOKS, CERRUTI - University Of Maryland; JENTSCH, PETER - Cornell University; NEELANDRA, JOSHI - Pennsylvania State University; KUHAR, THOMAS - Virginia Tech; LARA, JESUS - University Of California; LEGRAND, ANA - University Of Connecticut; Lee, Jana; Leskey, Tracy; LOWENSTEIN, DAVID - Oregon State University; MILNES, JOSH - Washington State University; MAISTRELLO, LARA - University Of Modena And Reggio Emilia (UNIMORE); Morrison, William - Rob; NIELSEN, ANNE - Rutgers University; OGBURN, EMILY - North Carolina State University; PICKETT, CHARLES - California Department Of Food And Agriculture; POLEY, KRISTIN - Michigan State University; POTE, JOHN - Rutgers University; JAMES, RADL - The Ohio State University; SHREWSBURY, PAULA - University Of Maryland; Talamas, Elijah; TAVELLA, LUCIANA - University Of Turin; WALGENBACH, JAMES - North Carolina State University; WATERWORTH, REBECCAH - University Of Maryland; Weber, Donald; WELTY, CELESTE - The Ohio State University; WIMAN, NIK - Oregon State University

Submitted to: Journal of Pest Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/5/2017
Publication Date: 6/8/2017
Citation: Abram, P.K., Hoelmer, K.A., Acebes-Doria, A., Andrews, H., Beers, E., Bergh, C.J., Bessin, R., Biddinger, D., Botch, P., Buffington, M.L., Cornelius, M.L., Costi, E., Delfosse, E., Dieckhoff, C., Dobson, R., Donais, Z., Grieshop, M., Hamilton, G., Haye, T., Hedstrom, C., Herlihy, M.V., Hoddle, M., Hooks, C., Jentsch, P., Neelandra, J., Kuhar, T., Lara, J., Legrand, A., Lee, J.C., Leskey, T.C., Lowenstein, D., Milnes, J., Maistrello, L., Morrison III, W.R., Nielsen, A.L., Ogburn, E., Pickett, C., Poley, K., Pote, J., James, R., Shrewsbury, P., Talamas, E.J., Tavella, L., Walgenbach, J., Waterworth, R., Weber, D.C., Welty, C., Wiman, N.G. 2017. Integrative review of indigenous arthropod natural enemies of the invasive brown marmorated stink bug in North America and Europe. Journal of Pest Science. 90(4):1009-1020.

Interpretive Summary: The establishment of the invasive Asian brown marmorated stink bug in the U.S. has caused significant crop losses and increased pest management costs in many fruit, vegetable, ornamental and field crops. We reviewed all available stink bug natural enemy studies spanning a variety of sampling methods, habitats, and geographic regions to identify patterns and trends, and identify gaps for future research. A majority of biological control research to date has focused on the stink bug egg stage to identify native parasitoid and predator communities and their contribution to stink bug egg mortality. Although egg parasitism and predation levels by indigenous natural enemies are typically less than ten percent, total egg mortality from natural enemies can sometimes be significant in certain habitats or crops. Predator species include a wide variety of chewing and sucking insects. There is less known about natural enemies that may attack stink bug nymphs and adults. Additional research on native natural enemies of stink bug should focus on: understanding the impact of biological control over the entire life cycle of stink bug; studying potential adaptation by native enemies to this stink bug over time; understanding the ecology and behavior of natural enemies and their influence on stink bug biocontrol; and augmenting the impact of biological control and integrating it with other components of stink bug management in crop systems.

Technical 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 integrative review, we combine 99 indigenous natural enemy (predator and/or parasitoid) datasets spanning a variety of sampling methods, habitats, and geographic areas to consolidate this information, evaluate qualitative trends, and identify gaps to guide future research. 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 5-25%; up to 83%) – even though these values were likely underestimated in most cases. 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 suggest that future research on native natural enemies of H. halys should focus on: (i) quantifying the population-level (generational) impact of biological control over the entire life cycle of H. halys; (ii) investigating the possibility of ongoing adaptation of indigenous natural enemies to H. halys over time in invaded areas; (iii) understanding the chemical ecology and intraguild interactions of natural enemies and the resulting effects on H. halys biocontrol; and (iv) finding ways of augmenting indigenous biological control impact and integrating it with other components of H. halys management in cropping systems.