Journal of Pest Science

, Volume 88, Issue 4, pp 693–705 | Cite as

Can native egg parasitoids adopt the invasive brown marmorated stink bug, Halyomorpha halys (Heteroptera: Pentatomidae), in Europe?

  • T. Haye
  • S. Fischer
  • J. Zhang
  • T. Gariepy
Original Paper


Halyomorpha halys was accidentally introduced into Switzerland around 2004 and has recently spread to several additional areas in Europe, with established populations documented in France, Italy, Greece and Hungary. To test whether generalist egg parasitoids of European Pentatomidae have the potential to control H. halys, and whether these could be as effective as their related Asian species, sentinel egg masses of H. halys and six native European pentatomids were exposed in two regions of Switzerland. Freeze-killed sentinel egg masses of H. halys were attacked by the platygastrid Trissolcus cultratus and the eupelmid Anastatus bifasciatus, whereas fresh egg masses of native Pentatomidae occassionally yielded four Scelionidae species: Trissolcus semistriatus, T. scutellaris, T. cultratus and Telenomus chloropus. In no-choice tests, T. chloropus and T. semistratus produced no offspring from fresh H. halys eggs, whereas T. cultratus and T. scutellaris were sporadically able to complete development. Stopping embryogenesis by freezing egg masses of H. halys at -80 °C enabled T. cultratus and T. semistriatus to produce a high number of offspring without influencing the behaviour of the parasitoids. In contrast to European platygastrids, the Asian parasitoids Trissolcus japonicus and T. cultratus (Chinese strain) caused significantly higher parasitism of fresh H. halys eggs. Differences in developmental success may be related to less efficient venom of European scelionids injected during oviposition. To date, A. bifasciatus is the only potential candidate for augmentaive biological control of H. halys in Europe as it was the only European parasitoid capable of consistent, successful development on fresh H. halys eggs.


Halyomorpha halys Egg parasitoids Biological control Platygastridae Eupelmidae Trissolcus Anastatus Telenomus 



The authors are grateful to all Swiss homeowners and farmers who kindly allowed us to collect stink bugs on their property. We would like to thank Alyson Carter, Léna Durocher-Granger, Dennis Quach and Sara Abdallah for technical assistance in the field and in the laboratory. We would like to thank Paul Abram for useful comments and suggestions on our manuscript. We appreciate the taxonomic guidance offered by Lubomir Masner (Canadian National Collection of Insects, Arachnids and Nematodes, Ottawa) and Elijah Talamas (Smithsonian Institution, Washington DC, USA).

Conflict of interest

The authors have declared that no conflict of interest exists.

Informed consent

Informed consent was obtained from all individual participants included in the study.

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. Abdel-Latief M, Hilker M (2008) Innate immunity: eggs of Manduca sexta are able to respond to parasitism by Trichogramma evanescens. Insect Biochem Mol 38:136–145CrossRefGoogle Scholar
  2. Abram PK, Gariepy TD, Boivin G, Brodeur J (2014a) An invasive stink bug as an evolutionary trap for an indigenous egg parasitoid. Biol Invasions 16:1387–1395CrossRefGoogle Scholar
  3. Abram PK, Doyonal J, Brodeur J, Gariepy TD, Boivin G (2014b) Susceptibility of Halyomorpha halys (Hemiptera: Pentatomidae) eggs to different life stages of three generalist predators. Can Entomol. doi: 10.4039/tce.2014.41 Google Scholar
  4. Arnold K (2009) Halyomorpha halys (Stål, 1855), eine für die europäische Fauna neu nachgewiesene Wanzenart (Insecta: Heteroptera: Pentatomidae: Cappaeini). Mitt Thürin Entomol 16:19Google Scholar
  5. Artem’ev VP, Oleshchenko IN, Gaidarov PG (1971) The effect of sterilization of the noxious Pentatomid on its natural enemies. Zashchita Rast 16:24–25Google Scholar
  6. Callot H, Brua C (2013) Halyomorpha halys (Stål, 1855), la Punaise diabolique, nouvelle espèce pour la faune de France (Heteroptera Pentatomidae). L’Entomologiste 69:69–71Google Scholar
  7. Cantón-Ramos JM, Callejón-Ferre AJ (2010) Raising Trissolcus basalis for the biological control of Nezara viridula in greenhouses of Almería (Spain). Afr J Agric Res 5:3207–3212Google Scholar
  8. Cesari M, Maistrello L, Ganzerli F, Dioli P, Rebecchi L, Guidetti R (2015) A pest alien invasion in progress: potential pathways of origin of the brown marmorated stink bug Halyomorpha halys populations in Italy. J Pest Sci 88:1–7CrossRefGoogle Scholar
  9. Clarke AR (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 Agr Res 41:1127–1146CrossRefGoogle Scholar
  10. Colazza S, Rosi MC, Sebastiani P, Ursini M (1996) Host acceptance behaviour in the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae). Acta Oecol 17:109–125Google Scholar
  11. Cornell HV, Hawkins BA (1993) Accumulation of native parasitoid species on introduced herbivores-a comparison of hosts as natives and hosts as invaders. Am Nat 141:847–865CrossRefPubMedGoogle Scholar
  12. Drooz AT, Bustillo AE, Fedde GF, Fedde VH (1977) North American egg parasite successfully controls a different host genus in South America. Science 197:390–391CrossRefPubMedGoogle Scholar
  13. Egwuata RI, Taylor TA (1977) Development of Gryon gnidus (Nixon) (Hymenoptera: Scelionidae) in eggs of Acnthomia tomntosicollis (Stål) (Hemiptera: Coreidae) killed either by gamma irradiation or by freezing. B Entomol Res 67:31–33CrossRefGoogle Scholar
  14. Field SA (1998) Patch exploitation, patch leaving and pre-emptive patch defence in the parasitoid wasp Trissolcus basalis (Hymenoptera: Scelionidae). Ethology 104:323–338CrossRefGoogle Scholar
  15. Fogain R, Graff S (2011) First records of the invasive pest, Halyomorpha halys (Hemiptera: Pentatomidae), in Ontario and Quebec. J Entomol Soc Ontario 142:45–48Google Scholar
  16. Gariepy TD, Haye T, Zhang J (2013) Occurrence, genetic diversity, and potential pathways of entry of Halyomorpha halys in newly-invaded areas of Canada and Switzerland. J Pest Sci 87:17–28CrossRefGoogle Scholar
  17. Genduso P (1977) Difesa del nocciolo dagli artropodi dannosi. IX. Osservazioni sulla morfologia degli stadi preimmaginali e notizie bio-etologiche dell’ Anastatus bifasciatus (Geoffroy). Bollettino dell’Istituto di Entomologia Agraria e dell’Osservatorio di Fitopatologia di Palermo 9:1–22Google Scholar
  18. Godfray HCJ (1994) Parasitoids: behaviroal and evolutionary ecology. Princeton University Press, PrincetonGoogle Scholar
  19. Greathead DJ (1986) Parasitoids in classical biological control. In: Waage J, Greathead D (eds) Insect parasitoids. Academic Press, London, pp 289–318Google Scholar
  20. Hawkins BA, Cornell HV (1994) Patterns of parasitoid accumulation on introduced herbivores. In: Hawkins BA, Sheehan W (eds) Parasitoid community ecology. Oxford University Press, New York, pp 77–90Google Scholar
  21. Haye T, Abdallah S, Gariepy T, Wyniger D (2014a) Phenology, life table analysis, and temperature requirements of the invasive brown marmorated stink bug, Halyomorpha halys in Europe. J Pest Sci 87(3):407–418CrossRefGoogle Scholar
  22. Haye T, Wyniger D, Gariepy T (2014b) Recent range expansion of brown marmorated stink bug in Europe. In: Müller G, Pospischi R, Robinson WH (eds). Proceedings of the 8th International Conference on Urban Pests, Zurich, 20–23 July, p 309–314Google Scholar
  23. Herting, B. (1971) A catalog of parasites and predators of terrestrial arthropods. Section A-Host or prey/enemy. Vol. I-Arachnida to Heteroptera. Commonwealth Agricultural Bureaux, SloughGoogle Scholar
  24. Hoebeke ER, Carter ME (2003) Halyomorpha halys (Stål) (Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. P Entomol Soc Wash 105:225–237Google Scholar
  25. Holt RD (1977) Predation, apparent competition and the structure of prey communities. Theor Popul Biol 12:197–229CrossRefPubMedGoogle Scholar
  26. Hou Z, Liang H, Chen Q, Hu Y, Tian H (2009) Application of Anastatus sp. against Halyomorpha halys. For Pest Dis 28:39–43Google Scholar
  27. Huang MD, Mai H, Wu WN, Poo CL (1974) The bionomics of Anastatus sp. and its utilisation for control of Tessaratoma papillosa Drury. Acta Entomol Sin 17:362–375Google Scholar
  28. Jones WA (1988) World review of the parasitoids of the southern green stink bug, Nezara viridula (L.) (Heteroptera: Pentatomidae). Ann Entomol Soc Am 81:262–273CrossRefGoogle Scholar
  29. 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
  30. Kenis M, Auger-Rozenberg M, Roques A, Timms L, Péré C, Cock MJW, Settele J, Augustin S, Lopez-Caamonde C (2009) Ecological effects of invasive alien insects. Biol Invasions 11:21–45CrossRefGoogle Scholar
  31. Kivan M, Kilic N (2005) Effects of storage at low-temperature of various heteropteran host eggs on the egg parasitoid, Trissolcus semistriatus. Biocontrol 50:589–600CrossRefGoogle Scholar
  32. Lee DH, Short BD, Joseph SV, Bergh JC, Leskey TC (2013) 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
  33. Leskey TC, Hamilton GC, Nielsen AL et al (2012a) Pest status of the brown marmorated stink bug, Halyomorpha halys in the USA. Outlooks Pest Manag 23:218–226CrossRefGoogle Scholar
  34. Leskey TC, Lee DH, Short BD, Wright SE (2012b) Impact of insecticides on the invasive Halyomorpha halys (Hemiptera: Pentatomidae): analysis of insecticide lethality. J Econ Entomol 105:1726–1735CrossRefPubMedGoogle Scholar
  35. Leskey TC, Short BD, Butler BR, Wright SE (2012c) Impact of the invasive brown marmorated stink bug, Halyomorpha halys (Stål), in mid-atlantic tree fruit orchards in the United States: case studies of commercial management. Psyche 2012:1–14CrossRefGoogle Scholar
  36. Leskey TC, Wright SE, Short BD, Khrimian A (2012d) Development of behaviorally based monitoring tools for the brown marmorated stink bug, Halyomorpha halys (Stål)(Heteroptera: Pentatomidae) in commercial tree fruit orchards. J Entomol Sci 47:76–85Google Scholar
  37. Luck RF (1981) Parasitic insects introduced as biological control agents for arthropod pests. In: Pimentel D (ed) Handbook of pest management in agriculture. CRC, Boca Raton, pp 125–184Google Scholar
  38. Mahmoud AMA, Lim UT (2007) Evaluation of cold-stored eggs of Dolycoris baccarum (Hemiptera: Pentatomidae) for parasitization by Trissolcus nigripedius (Hymenoptera: Scelionidae). Biol Control 43:287–293CrossRefGoogle Scholar
  39. Maistrello L, Dioli P, Vaccari G, Nannini P, Bortolotti S, Caruso S, Costi E, Montermini A, Casoli L, Bariselli M (2014) Primi rinvenimenti in Italia della cimice esotica Halyomorpha halys, una nuova minaccia per la frutticoltura. Atti Giornate Fitopatol 1(2014):283–288Google Scholar
  40. Martin HE, Javahery M, Radjabi G (1969) Note sur la punaise des Céréales Eurygaster integriceps Put. et de ses parasites du genre Asolcus en Iran. Entomol Phytoptah Appl 28:38–46Google Scholar
  41. Milonas PG, Partsinevelos GK (2014) First report of brown marmorated stink bug Halyomorpha halys Stål (Hemiptera: Pentatomidae) in Greece. EPPO Bull 44:183–186CrossRefGoogle Scholar
  42. Mineo G, Lucido G (1977) Difesa del nocciolo dagli artropodi dannosi. XI Prove di controllo biologico del Gonocerus acuteangulatus (Goeze) con lanci inoculativi di alcuni suoi parassitoidi: Gryon muscaeformis (Nees), Trissolcus flavipes (Thoms.), Ooencyrtus gonoceri Vigg. Bollettino dell’Istituto di Entomologia Agraria e dell’Osservatorio di Fitopatologia di Palermo 9:109–128Google Scholar
  43. Noyes JS (2014) Universal Chalcidoidea Database. World Wide Web electronic publication. Accessed February 2015
  44. Northeastern IPM Center (2014) Host Plants of the brown marmorated stink bug in the U.S. Accessed Feb 27 2015
  45. Orr DB (1988) Scelionid wasps as biological control agents: a review. Fla Entomol 71:501–506CrossRefGoogle Scholar
  46. Pansa MG, Asteggiano L, Costamagna C, Vittone G, Tavella L (2013) First discovery of Halyomorpha halys in peach orchards in Piedmont. L’Inf Agrario 69:60–61Google Scholar
  47. Piek T (ed) (1986) Venoms of hymenoptera. Academic Press, LondonGoogle Scholar
  48. Reed DA, Luhring KA, Stafford CA, Hansen AK, Millar JG, Hanks LM, Paine TD (2007) Host defensive response against an egg parasitoid involves cellular encapsulation and melanisation. Biol Control 41:214–222CrossRefGoogle Scholar
  49. Rice K, Bergh C, Bergman E, Biddinger D, Dieckhoff C, Dively G, Fraser H, Gariepy T, Hamilton G, Haye T, Herbert A, Hoelmer K, Hooks C, Jones A, Krawczyk G, Kuhar T, Mitchell W, Nielsen A, Pfeiffer D, Raupp M, Rodriguez-Saona C, Shearer P, Shrewsbury P, Venugopal PD, Whalen J, Wiman N, Leskey T, Tooker J (2014) Biology, ecology, and management of brown marmorated stink bug (Halyomorpha halys). J Integr Pest Manag. doi: 10.1603/IPM14002 Google Scholar
  50. Rider DA (2014) Hymenoptera parasitoid records-list by parasitoid species ( Accessed 16 Feb 2015
  51. Strand MR, Quarles JM, Meola SM, Vinson SB (1985) Cultivation of teratocytes of the egg parasitoid Telenomus heliothidis (Hymenoptera: Scelionidae). In Vitro Cell Dev Biol 21:361–367CrossRefGoogle Scholar
  52. Strand MR, Meola SM, Vinson SB (1986) Correlating pathological symptoms in Heliothis virescens eggs with development of the parasitoid Telenomus heliothidis. J Insect Physiol 32:389–402CrossRefGoogle Scholar
  53. Talamas EJ, Buffington M, Hoelmer K (2013) New synonymy of Trissolcus halyomorphae Yang. J Hymenopt Res 33:113–117CrossRefGoogle Scholar
  54. Talamas EJ, Johnson NF, Buffington ML (2015) Key to Nearctic species of Trissolcus Ashmead, natural enemies of native and invasive stink bugs (Pentatomidae). J Hymenopt Res 43:119–128CrossRefGoogle Scholar
  55. Thompson W. R. (1944) A catalogue of the parasites and predators of insect pests. Section I. Parasite host catalogue. Part 3. Parasites of the Hemiptera. Imperial Agriculture of Bureau Institute Entomologist Parasite Service, OntarioGoogle Scholar
  56. Toepfer S, Kuhlmann U (2004) Survey for natural enemies of the invasive alien chrysomelid, Diabrotica virgifera virgifera, in Central Europe. Biocontrol 49:385–395CrossRefGoogle Scholar
  57. United States Apple Association (2010) Asian pest inflicting substantial losses, raising alarm in eastern apple orchards. Apple News 41:488Google Scholar
  58. van Lenteren JC, Bale J, Bigler F, Hokkanen HMT, Loomans AJM (2006) Assessing risks of releasing exotic biological control agents of arthropods pests. Annu Rev Entomol 51:609–634Google Scholar
  59. Vétek G, Papp V, Haltrich A, Redei D (2014) First record of the brown marmorated stink bug, Halyomorpha halys (Hemiptera: Heteroptera: Pentatomidae), in Hungary, with description of the genitalia of both sexes. Zootaxa 3780:194–200Google Scholar
  60. Vindstad OPL, Schott T, Hagen SB, Jepsen JU, Kapari L, Ims RA (2013) How rapidly do invasive birch forest geometrids recruit larval parasitoids? Insights from comparison with a sympatric native geometrid. Biol Invasions 15:1573–1589CrossRefGoogle Scholar
  61. Vinson SB (1990) How parasitoids deal with the immune system of their host: an overview. Arch Insect Biochem 13:3–27CrossRefGoogle Scholar
  62. Yang ZQ, Yao YX, Qiu LF, Li ZF (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 102:39–47CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.CABIDelémontSwitzerland
  2. 2.Agroscope Changins-WädenswilNyonSwitzerland
  3. 3.MoA-CABI Joint Laboratory for BiosafetyBeijingChina
  4. 4.Southern Crop Protection and Food Research Centre Agriculture and Agri-Food CanadaLondonCanada

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