Journal of Pest Science

, Volume 90, Issue 4, pp 1119–1125 | Cite as

Possible coexistence of native and exotic parasitoids and their impact on control of Halyomorpha halys

  • J. K. KonopkaEmail author
  • T. Haye
  • T. D. Gariepy
  • J. N. McNeil
Original Paper


Introduction of exotic natural enemies for biological control of invasive pests may disrupt existing ecological interactions, which may influence the outcome of biological control introductions. The interactions between Asian egg parasitoids, proposed as classical biological control agents of the highly polyphagous invasive pest Halyomorpha halys (Stål), and parasitoids native to the introduced area are largely unknown. Therefore, adult and larval interspecific competition between the exotic Trissolcus japonicus (Ashmead) and the European Anastatus bifasciatus (Geoffroy) was assessed (1) by observing aggressive interactions between adults of the two species following parasitization and (2) by providing each parasitoid species with previously parasitized H. halys egg masses at various time intervals. The results suggest that T. japonicus and A. bifasciatus engage in counterbalance competition, with the former being a superior extrinsic competitor (egg guarding and aggressiveness) and the latter being a superior intrinsic competitor (successful development from multiparasitized eggs of all ages). We suggest that the presence of T. japonicus is unlikely to have a negative impact on A. bifasciatus, and that those two species can coexist and potentially act synergistically in the biological control of H. halys.


Anastatus bifasciatus Trissolcus japonicus Larval competition Biological control Brown marmorated stink bug 



This work was funded by NSERC PGS Scholarship and ESC Research Travel Scholarship to JKK, and Agriculture and Agri-Food Canada A-base funds to TDG. We would like to thank Elijah Talamas (Smithsonian Institution, Washington, DC, USA) and Lucian Fusu (University of Iasi, Romania) for the identification of the parasitoids from our laboratory colonies. The authors are grateful to Serge Fischer (Agroscope Changins-Wädenswil) for providing the original A. bifasciatus colony.

Compliance with ethical standards

Conflict of interest

The authors have declared that no conflict of interest exists.

Research involving human participants and/or animals

This article does not contain any studies with human participants or animals (vertebrates) performed by any of the authors.


  1. Abram PK, Gariepy TD, Boivin G, Brodeur J (2014) An invasive stink bug as an evolutionary trap for an indigenous egg parasitoid. Biol Invasions 16:1387–1395CrossRefGoogle Scholar
  2. Alalouni U, Schädler M, Brandl R (2013) Natural enemies and environmental factors affecting the population dynamics of the gypsy moth. J Appl Entomol 137:721–738CrossRefGoogle Scholar
  3. Arakawa R, Namura Y (2002) Effects of temperature on development of three Trissolcus spp. (Hymenoptera: Scelionidae), egg parasitoids of the brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae). Entomol Sci 5:215–218Google Scholar
  4. Beasley TM, Schumacker RE (1995) Multiple regression approach to analysing contingency tables: post hoc and planned comparison procedures. J Exp Educ 64:79–93CrossRefGoogle Scholar
  5. Berthon K (2015) How do native species respond to invaders? Mechanistic and trait-based perspectives. Biol Invasions 17:2199–2211CrossRefGoogle Scholar
  6. Choi M-Y, Yang Z-Q, Wang X-Y, Tang Y-L, Hou Z-R, Kim JH, Byeon YW (2014) Parasitism rate of egg parasitoid Anastatus orientalis (Hymenoptera: Eupelmidae) on Lycorma delicatula (Hemiptera: Fulgoridae) in China. Korean J Appl Entomol 53:135–139CrossRefGoogle Scholar
  7. Clarke A, Clarke A (1990) The control of Nezara viridula L. with introduced egg parasitoids in Australia. A review of a “landmark” example of classical biological control. Aust J Agric Res 41:1127CrossRefGoogle Scholar
  8. Clausen CP (1940) Entomophagous insects. McGraw-Hill, New YorkGoogle Scholar
  9. Cusumano A, Peri E, Amodeo V, McNeil JN, Colazza S (2013) Intraguild interactions between egg parasitoids: window of opportunity and fitness costs for a facultative hyperparasitoid. PLoS ONE 8:e64768CrossRefPubMedPubMedCentralGoogle Scholar
  10. Cusumano A, Peri E, Colazza S (2016) Interspecific competition/facilitation among insect parasitoids. Curr Opin Insect Sci 14:12–16CrossRefPubMedGoogle Scholar
  11. Dahlman DL (1991) Teratocytes and host/parasitoid interactions. Biol Control 1:118–126CrossRefGoogle Scholar
  12. De Moraes CM, Cortesero AM, Stapel JO, Lewis WJ (1999) Intrinsic and extrinsic competitive interactions between two larval parasitoids of Heliothis virescens. Ecol Entomol 24:402–410CrossRefGoogle Scholar
  13. Didham RK, Tylianakis JM, Hutchison MA et al (2005) Are invasive species the drivers of ecological change? Trends Ecol Evol 20:470–474CrossRefPubMedGoogle Scholar
  14. Doury G, Bigot Y, Periquet G (1997) Physiological and biochemical analysis of factors in the female venom gland and larval salivary secretions of the ectoparasitoid wasp Eupelmus orientalis. J Insect Physiol 43:69–81CrossRefPubMedGoogle Scholar
  15. Ellers J, Sevenster JG, Driessen G (2000) Egg load evolution in parasitoids. Am Nat 156:650–665CrossRefGoogle Scholar
  16. Garcia-Pérez MA, Nunez-Anton V (2003) Cellwise residual analysis in two-way contingency tables. Educ Psychol Meas 63:825–839CrossRefGoogle Scholar
  17. Haye T, Fischer S, Zhang J, Gariepy T (2015a) Can native egg parasitoids adopt the invasive brown marmorated stink bug, Halyomorpha halys (Heteroptera: Pentatomidae), in Europe? J Pest Sci 88:693–705CrossRefGoogle Scholar
  18. Haye T, Gariepy T, Hoelmer K, Rossi J-P, Streito J-C, Tassus X, Desneux N (2015b) Range expansion of the invasive brown marmorated stinkbug, Halyomorpha halys: an increasing threat to field, fruit and vegetable crops worldwide. J Pest Sci 88:665–673CrossRefGoogle Scholar
  19. Hoebeke E, Carter ME (2003) Halyomopha halys (Stal)(Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. Proc Entomol Soc Wash 105:225–237Google Scholar
  20. Hoffmann M, Davidson N (1991) Imported wasp helps control southern green stink bug. Calif Agric 45:20–22Google Scholar
  21. Hou Z, Liang H, Qian C et al (2009) Application of Anastatus sp. against Halyomorpha halys. For Pest Dis 28:39–43Google Scholar
  22. Jones AL, Jennings DE, Hooks CRR, Shrewsbury PM (2014) Sentinel eggs underestimate rates of parasitism of the exotic brown marmorated stink bug, Halyomorpha halys. Biol Control 78:61–66CrossRefGoogle Scholar
  23. Kalina V (1981) The Palaearctic species of the genus Anastatus Motschulsky, 1860 (Hymenoptera, Chalcidoidea, Eupelmidae) with descriptions of new species. Silvaecultura Tropica et Subtropica 8:3–25Google Scholar
  24. Konopka JK, Haye T, Gariepy T, Mason P, Gillespie D, McNeil JN (2017) An exotic parasitoid provides an invasional lifeline for native parasitoids. Ecol Evol 7:277–284CrossRefPubMedGoogle Scholar
  25. Koppel AL, Herbert DA, Westbrook EW (2011) Using microscopy to assess chorion structural integrity and parasitoid oviposition sites on stink bug (Hemiptera: Pentatomidae) eggs. Microsc Microanal 17:114–117CrossRefPubMedGoogle Scholar
  26. Lee D-H, Short BD, Joseph SV, Bergh JC, Leskey TC (2013a) Review of the biology, ecology, and management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan, and the Republic of Korea. Environ Entomol 42:627–641CrossRefPubMedGoogle Scholar
  27. Lee D-H, Wright SE, Leskey TC (2013b) Impact of insecticide residue exposure on the invasive pest, Halyomorpha halys (Hemiptera: Pentatomidae): analysis of adult mobility. J Econ Entomol 106:150–158CrossRefPubMedGoogle Scholar
  28. Leskey TC, Lee D-H, Short BD, Wright SE (2012) Impact of insecticides on the invasive Halyomorpha halys (Hemiptera: Pentatomidae): analysis of insecticide lethality. J Econ Entomol 105:1726–1735CrossRefPubMedGoogle Scholar
  29. Milnes JM, Wiman NG, Talamas EJ, Brunner JF, Hoelmer KA, Buffington ML, Beers EH (2016) Discovery of an exotic egg parasitoid of the brown marmorated stink bug, Halyomorpha halys (Stål) in the Pacific Northwest. Proc Entomol Soc Wash 118:466–470CrossRefGoogle Scholar
  30. Mooney HA, Cleland EE (2001) The evolutionary impact of invasive species. Proc Natl Acad Sci USA 98:5446–5451CrossRefPubMedPubMedCentralGoogle Scholar
  31. Nakamatsu Y, Tanaka T (2003) Venom of ectoparasitoid, Euplectrus sp. near plathypenae (Hymenoptera: Eulophidae) regulates the physiological state of Pseudaletia separata (Lepidoptera: Noctuidae) host as a food resource. J Insect Physiol 49:149–159CrossRefPubMedGoogle Scholar
  32. Noyes JS (2016) Universal Chalcidoidea Database. World Wide Web electronic publication Accessed 1 Sep 2016
  33. Orr D (1988) Scelionid wasps as biological control agents: a review. Florida Entomol 71:506–528CrossRefGoogle Scholar
  34. Piek T (1986) Venoms of the Hymenoptera: biochemical, pharmacological and behavioural aspects. Academic Press, TorontoGoogle Scholar
  35. Rice KB, Bergh CJ, Bergmann EJ, Biddinger DJ, Dieckhoff C, Dively G, Fraser H, Gariepy T, Hamilton G, Haye T, Herbert A, Hoelmer K, Hooks CR, Jones A, Krawczyk G, Kuhar T, Martinson H, Mitchell W, Nielsen AL, Pfeiffer DG, Raupp MJ, Rodriguez-Saona C, Shearer P, Shrewsbury P, Venugopal PD, Whalen J, Wiman NG, Leskey TC, Tooker JF (2014) Biology, ecology, and management of brown marmorated stink bug (Hemiptera: Pentatomidae). J Integr Pest Manag 5:1–13CrossRefGoogle Scholar
  36. Rodriguez LF (2006) Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biol Invasions 8:927–939CrossRefGoogle Scholar
  37. Rosenheim J, Rosen D (1991) Foraging and oviposition decisions in the parasitoid Aphytis lingnanensis: distinguishing the influences of egg load and experience. J Anim Ecol 60:873–893CrossRefGoogle Scholar
  38. Schulthess F, Chabi-Olaye A, Goergen G (2001) Seasonal fluctuations of noctuid stemborer egg parasitism in Southern Benin with special reference to Sesamia calamistis Hampson (Lepidoptera: Noctuidae) and Telenomus spp. (Hymenoptera: Scelionidae) on maize. Biocontrol Sci Technol 11:745–757CrossRefGoogle Scholar
  39. Slansky F (1986) Nutritional ecology of endoparasitic insects and their hosts: an overview. J Insect Physiol 32:255–261CrossRefGoogle Scholar
  40. Talamas E, Johnson N, Buffington M (2015a) Key to Nearctic species of Trissolcus Ashmead (Hymenoptera, Scelionidae), natural enemies of native and invasive stink bugs (Hemiptera, Pentatomidae). J Hymenopt Res 43:45–110CrossRefGoogle Scholar
  41. Talamas EJ, Herlihy MV, Dieckhoff C, Hoelmer KA, Buffington M, Bon M-C, Weber DC (2015b) Trissolcus japonicus (Ashmead) (Hymenoptera, Scelionidae) emerges in North America. J Hymenopt Res 43:119–128CrossRefGoogle Scholar
  42. Tiberi R, Roversi P, Bin F (1991) Egg parasitoids of pine processionary caterpillars in central Italy. Redia 74:249–250Google Scholar
  43. Volkoff N, Colazza S (1992) Growth patterns of teratocytes in the immature stages of Trissolcus basalis (Woll.) (Hymenoptera: Scelionidae), an egg parasitoid of Nezara viridula (L.) (Heteroptera: Pentatomidae). Int J Insect Morphol Embryol 21:323–336CrossRefGoogle Scholar
  44. Yang Z-Q, Yao Y-X, Qiu L-F, Li Z-X (2009) A new species of Trissolcus (Hymenoptera: Scelionidae) parasitizing eggs of Halyomorpha halys (Heteroptera: Pentatomidae) in China with comments on its biology. Ann Entomol Soc Am 102:39–47. doi: 10.1603/008.102.0104 CrossRefGoogle Scholar
  45. Zwölfer H (1971) The structure and effects of parasite complexes attacking phytophagous host insects. In: den Boer PJ, Gradwell GR (eds) Dynamics of Populations: proceedings of the advanced study institute on “dynamics and numbers in populations”. Centre for Agricultural Publishing and Documentation, Waganingen, pp 405–418Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of BiologyWestern UniversityLondonCanada
  2. 2.CABI SwitzerlandDelémontSwitzerland
  3. 3.London Research and Development CentreAgriculture and Agri-Food CanadaLondonCanada

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