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

Paul K. Abram, 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 HedstromMegan 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. Morrison, 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

Research output: Contribution to journalReview article

44 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)1009-1020
Number of pages12
JournalJournal of Pest Science
Volume90
Issue number4
DOIs
StatePublished - Sep 1 2017

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Halyomorpha halys
natural enemies
arthropods
predators
biological control
habitats
arthropod communities
Pentatomidae
mastication
egg masses
nymphs
Hemiptera
parasitism
pests
predation
crops

All Science Journal Classification (ASJC) codes

  • Agronomy and Crop Science

Cite this

Abram, P. K., Hoelmer, K. A., Acebes-Doria, A., Andrews, H., Beers, E. H., Bergh, J. C., ... Wiman, N. G. (2017). Indigenous arthropod natural enemies of the invasive brown marmorated stink bug in North America and Europe. Journal of Pest Science, 90(4), 1009-1020. https://doi.org/10.1007/s10340-017-0891-7
Abram, Paul K. ; Hoelmer, Kim A. ; Acebes-Doria, Angelita ; Andrews, Heather ; Beers, Elizabeth H. ; Bergh, J. Christopher ; Bessin, Ric ; Biddinger, David ; Botch, Paul ; Buffington, Matthew L. ; Cornelius, Mary L. ; Costi, Elena ; Delfosse, Ernest S. ; Dieckhoff, Christine ; Dobson, Rachelyn ; Donais, Zachary ; Grieshop, Matthew ; Hamilton, George ; Haye, Tim ; Hedstrom, Christopher ; Herlihy, Megan V. ; Hoddle, Mark S. ; Hooks, Cerruti R.R. ; Jentsch, Peter ; Joshi, Neelendra K. ; Kuhar, Thomas P. ; Lara, Jesus ; Lee, Jana C. ; Legrand, Ana ; Leskey, Tracy C. ; Lowenstein, David ; Maistrello, Lara ; Mathews, Clarissa R. ; Milnes, Joshua M. ; Morrison, William R. ; Nielsen, Anne L. ; Ogburn, Emily C. ; Pickett, Charles H. ; Poley, Kristin ; Pote, John ; Radl, James ; Shrewsbury, Paula M. ; Talamas, Elijah ; Tavella, Luciana ; Walgenbach, James F. ; Waterworth, Rebeccah ; Weber, Donald C. ; Welty, Celeste ; Wiman, Nik G. / Indigenous arthropod natural enemies of the invasive brown marmorated stink bug in North America and Europe. In: Journal of Pest Science. 2017 ; Vol. 90, No. 4. pp. 1009-1020.
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abstract = "Since the establishment of the brown marmorated stink bug, Halyomorpha halys (St{\aa}l) (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.",
author = "Abram, {Paul K.} and Hoelmer, {Kim A.} and Angelita Acebes-Doria and Heather Andrews and Beers, {Elizabeth H.} and Bergh, {J. Christopher} and Ric Bessin and David Biddinger and Paul Botch and Buffington, {Matthew L.} and Cornelius, {Mary L.} and Elena Costi and Delfosse, {Ernest S.} and Christine Dieckhoff and Rachelyn Dobson and Zachary Donais and Matthew Grieshop and George Hamilton and Tim Haye and Christopher Hedstrom and Herlihy, {Megan V.} and Hoddle, {Mark S.} and Hooks, {Cerruti R.R.} and Peter Jentsch and Joshi, {Neelendra K.} and Kuhar, {Thomas P.} and Jesus Lara and Lee, {Jana C.} and Ana Legrand and Leskey, {Tracy C.} and David Lowenstein and Lara Maistrello and Mathews, {Clarissa R.} and Milnes, {Joshua M.} and Morrison, {William R.} and Nielsen, {Anne L.} and Ogburn, {Emily C.} and Pickett, {Charles H.} and Kristin Poley and John Pote and James Radl and Shrewsbury, {Paula M.} and Elijah Talamas and Luciana Tavella and Walgenbach, {James F.} and Rebeccah Waterworth and Weber, {Donald C.} and Celeste Welty and Wiman, {Nik G.}",
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Abram, PK, Hoelmer, KA, Acebes-Doria, A, Andrews, H, Beers, EH, Bergh, JC, Bessin, R, Biddinger, D, Botch, P, Buffington, ML, Cornelius, ML, Costi, E, Delfosse, ES, Dieckhoff, C, Dobson, R, Donais, Z, Grieshop, M, Hamilton, G, Haye, T, Hedstrom, C, Herlihy, MV, Hoddle, MS, Hooks, CRR, Jentsch, P, Joshi, NK, Kuhar, TP, Lara, J, Lee, JC, Legrand, A, Leskey, TC, Lowenstein, D, Maistrello, L, Mathews, CR, Milnes, JM, Morrison, WR, Nielsen, AL, Ogburn, EC, Pickett, CH, Poley, K, Pote, J, Radl, J, Shrewsbury, PM, Talamas, E, Tavella, L, Walgenbach, JF, Waterworth, R, Weber, DC, Welty, C & Wiman, NG 2017, 'Indigenous arthropod natural enemies of the invasive brown marmorated stink bug in North America and Europe', Journal of Pest Science, vol. 90, no. 4, pp. 1009-1020. https://doi.org/10.1007/s10340-017-0891-7

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

In: Journal of Pest Science, Vol. 90, No. 4, 01.09.2017, p. 1009-1020.

Research output: Contribution to journalReview article

TY - JOUR

T1 - Indigenous arthropod natural enemies of the invasive brown marmorated stink bug in North America and Europe

AU - Abram, Paul K.

AU - Hoelmer, Kim A.

AU - Acebes-Doria, Angelita

AU - Andrews, Heather

AU - Beers, Elizabeth H.

AU - Bergh, J. Christopher

AU - Bessin, Ric

AU - Biddinger, David

AU - Botch, Paul

AU - Buffington, Matthew L.

AU - Cornelius, Mary L.

AU - Costi, Elena

AU - Delfosse, Ernest S.

AU - Dieckhoff, Christine

AU - Dobson, Rachelyn

AU - Donais, Zachary

AU - Grieshop, Matthew

AU - Hamilton, George

AU - Haye, Tim

AU - Hedstrom, Christopher

AU - Herlihy, Megan V.

AU - Hoddle, Mark S.

AU - Hooks, Cerruti R.R.

AU - Jentsch, Peter

AU - Joshi, Neelendra K.

AU - Kuhar, Thomas P.

AU - Lara, Jesus

AU - Lee, Jana C.

AU - Legrand, Ana

AU - Leskey, Tracy C.

AU - Lowenstein, David

AU - Maistrello, Lara

AU - Mathews, Clarissa R.

AU - Milnes, Joshua M.

AU - Morrison, William R.

AU - Nielsen, Anne L.

AU - Ogburn, Emily C.

AU - Pickett, Charles H.

AU - Poley, Kristin

AU - Pote, John

AU - Radl, James

AU - Shrewsbury, Paula M.

AU - Talamas, Elijah

AU - Tavella, Luciana

AU - Walgenbach, James F.

AU - Waterworth, Rebeccah

AU - Weber, Donald C.

AU - Welty, Celeste

AU - Wiman, Nik G.

PY - 2017/9/1

Y1 - 2017/9/1

N2 - 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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