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Experimental assessment of the biosafety of Trissolcus japonicus in New Zealand, prior to the anticipated arrival of the invasive pest Halyomorpha halys

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Abstract

Despite numerous interceptions at the border, the brown marmorated stink bug (BMSB), Halyomorpha halys Stål (Hemiptera: Pentatomidae), is not yet established in New Zealand. Nevertheless, a classical biocontrol programme using the egg parasitoid Trissolcus japonicus Ashmead (Hymenoptera: Scelionidae) has been initiated in anticipation of its likely arrival. The potential host range of the parasitoid in New Zealand was investigated by importing parasitised BMSB eggs into quarantine from Newark, DE, USA. Egg masses of seven species of Pentatomidae, including one sub-species, were individually exposed to naïve mated female T. japonicus in no-choice laboratory experiments. The results showed that predatory Cermatulus nasalis nasalis, C. nasalis hudsoni and Oechalia schellenbergii, and the phytophagous Monteithiella humeralis, Dictyotus caenosus, Glaucias amyoti, and Cuspicona simplex are all within the physiological host range of T. japonicus, although not all appeared to be equally susceptible to parasitism. No development or emergence of T. japonicus from eggs of the cosmopolitan pentatomid plant pest Nezara viridula were observed. The likely ecological consequences of releasing T. japonicus in New Zealand are discussed, as is the subsequent decision of New Zealand’s Environmental Protection Authority to approve release of the parasitoid once BMSB arrives in New Zealand.

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References

  • 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. J Pest Sci 90:1009–1020

    Article  Google Scholar 

  • Abram PK, Talamas EJ, Acheampong S, Mason PG, Gariepy TD (2019) First detection of the samurai wasp, Trissolcus japonicus (Ashmead) (Hymenoptera, Scelionidae), in Canada. J Hymenopt Res 68:29–36

    Article  Google Scholar 

  • Avila GA, Charles JG (2018) Modelling the potential geographic distribution of Trissolcus japonicus: a biological control agent of the brown marmorated stink bug, Halyomorpha halys. BioControl 63:505–518

    Article  Google Scholar 

  • Avila GA, Withers TM, Holwell GI (2016) Laboratory odour-specificity testing of Cotesia urabae to assess potential risks to non-target species. BioControl 61:365–377

    Article  Google Scholar 

  • Barratt BIP, Evans AA, Ferguson CM, Barker GM, McNeill MR, Phillips CB (1997) Laboratory nontarget host range of the introduced parasitoids Microctonus aethiopoides and M. hyperodae (Hymenoptera: Braconidae) compared with field parasitism in New Zealand. Entomol Soc Am 26:694–702

    Google Scholar 

  • Barratt BIP, Berndt LA, Dodd SL, Ferguson CM, Hill RL, Kean JM, Teulon DAJ, Withers TM (2007) BIREA—Biocontrol Information Resource for EPA applicants. http://www.b3nz.org/birea/. Accessed 2 Oct 2017

  • Buffington M, Talamas EJ, Hoelmer KA (2018) Team Trissolcus: integrating taxonomy and biological control to combat the brown marmorated stink bug. Am Entomol 64:224–232

    Article  Google Scholar 

  • Conti E, Salerno G, Bin F, Vinson SB (2004) The role of host semiochemicals in parasitoid specificity: a case study with Trissolcus brochymenae and Trissolcus simoni on pentatomid bugs. Biol Control 29:435–444

    Article  CAS  Google Scholar 

  • Dieckhoff C, Tatman K, Hoelmer KA (2017) Natural biological control of Halyomorpha halys (Hemiptera: Pentatomidae) by native egg parasitoids—a multi-year survey in northern Delaware. J Pest Sci 90:1143–1158

    Article  Google Scholar 

  • Duthie C (2012) Risk analysis of Halyomorpha halys (brown marmorated stinkbug) on all pathways. Ministry for primary industries. https://mpi.govt.nz/dmsdocument/2909-halyomorpha-halys-brown-marmorated-stink-bug-riskanalysis-november-2012. Accessed 02 Feb 2017

  • EPA (2018) Application and approval to release Trissolcus japonicus into New Zealand. https://www.epa.govt.nz/search/SearchForm?Search=Trissolcus+japonicus. Accessed March 2019

  • Faúndez EI, Rider DA (2017) The brown marmorated stink bug Halyomorpha halys (Stål 1885) (Heteroptera: Pentatomidae) in Chile. Arquivos Entomol 17:305–330

    Google Scholar 

  • Ferro J (2017) Stink bug killers: Scientists to release Samurai wasps. Discovery of wasps in Ulster County is likely to speed process across New York. http://www.stopbmsb.org/more-resources/bmsb-in-the-news/stink-bug-killers-scientists-to-release-samurai-wasps/. Accessed 10 May 2017

  • Gapon D (2016) First records of the brown marmorated stink bug Halyomorpha halys (Stål, 1855) (Heteroptera, Pentatomidae) in Russia, Abkhazia, and Georgia. Entomol Rev 96:1086–1088

    Article  Google Scholar 

  • Haye T, Goulet H, Mason P, Kuhlmann U (2005) Does fundamental host range match ecological host range? A retrospective case study of a Lygus plant bug parasitoid. Biol Control 35:55–67

    Article  Google Scholar 

  • Haye T, Gariepy T, Hoelmer K, Rossi J-P, Streito J-C, Tassus X, Desneux N (2015a) Range expansion of the invasive brown marmorated stinkbug, Halyomorpha halys: an increasing threat to field, fruit and vegetable crops worldwide. J Pest Sci 88:665–673

    Article  Google Scholar 

  • Haye T, Fischer S, Zhang J, Gariepy T (2015b) Can native egg parasitoids adopt the invasive brown marmorated stink bug, Halyomorpha halys (Heteroptera: Pentatomidae), in Europe. J Pest Sci 88:693–705

    Article  Google Scholar 

  • Haye T, Moraglio ST, Stahl J, Visentin S, Grogorio T, Tavella L (2019) Fundamental host range of Trissolcus japonicus in Europe. J Pest Sci. https://doi.org/10.1007/s10340-019-01127-3

    Article  Google Scholar 

  • Hedstrom C, Lowenstein D, Andrews H, Bai B, Wiman N (2017) Pentatomid host suitability and the discovery of introduced populations of Trissolcus japonicus in Oregon. J Pest Sci 90:1169–1179

    Article  Google Scholar 

  • Jentsch P (2016) BMSB News: The invasive parasitic wasp, Trissolcus japonicus, recently found in New York State. https://blogs.cornell.edu/jentsch/2016/09/19/bmsb-news-the-invasive-parasitic-wasp-trissolcus-japonicus-recently-found-in-new-york-state/. Accessed 26 April 2017

  • Kim KY, Choi D-S, Choi J-Y, Hong K-J (2017) Host records of Trissolcus (Hymenoptera: Platygasteridae: Telenominae) parasitizing eggs of stink bugs in Korea. Korean J Appl Entomol 56:87–92

    Article  Google Scholar 

  • Kriticos DJ, Kean JM, Phillips CB, Senay SD, Acosta H, Haye T (2017) The potential global distribution of the brown marmorated stink bug, Halyomorpha halys, a critical threat to plant biosecurity. J Pest Sci 90:1033–1043

    Article  Google Scholar 

  • Lara J, Pickett C, Ingels C, Haviland D, Grafton-Cardwell E, Doll D, Bethke J, Dara S, Hoddle M (2016) Biological control program is being developed for brown marmorated stink bug. Calif Agric 70:15–23

    Article  Google Scholar 

  • Larivière M-C (1995) Cydnidae, Acanthosomatidae, and Pentatomidae (Insecta: Heteroptera): systematics, geographical distribution, and bioecology. Fauna of New Zealand 35. Whenua Press, Lincoln

    Google Scholar 

  • Lee D-H (2015) Current status of research progress on the biology and management of Halyomorpha halys (Hemiptera: Pentatomidae) as an invasive species. Appl Entomol Zool 50:277–290

    Article  CAS  Google Scholar 

  • Lee D-H, Short BD, Leskey TC, Joseph SV, Bergh JC (2013) Review of the biology, ecology, and management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan, and the Republic of Korea. Environ Entomol 42:627–641

    Article  Google Scholar 

  • Leskey TC, Nielsen AL (2018) Impact of the invasive brown marmorated stink bug in North America and Europe: history, biology, ecology, and management. Ann Rev Entomol 63:599–618

    Article  CAS  Google Scholar 

  • Liebhold AM, Berec L, Brockerhoff EG, Epanchin-Niell RS, Hastings A, Herms DA, Kean JM, McCullough DG, Suckling DM, Tobin PC, Yamanaka T (2016) Eradication of invading insect populations: from concepts to applications. Annu Rev Entomol 61:335–352

    Article  CAS  Google Scholar 

  • Medal J, Smith T, Fox A, Santa Cruz A, Poplin A, Hodges A (2012) Rearing the brown marmorated stink bug Halyomorpha halys. Flo Entomol 95:800–802

    Article  Google Scholar 

  • Milnes JN, 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 118:466–470

    Article  Google Scholar 

  • Morrison WR III, Blaauw BR, Nielsen AL, Talamas E, Leskey TC (2018) Predation and parasitism by native and exotic natural enemies of Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) eggs augmented with semiochemicals and differing host stimuli. Biol Control 121:140–150

    Article  Google Scholar 

  • Nystrom Santacruz E, Venette R, Dieckhoff C, Hoelmer K, Koch RL (2017) Cold tolerance of Trissolcus japonicus and T. cultratus, potential biological control agents of Halyomorpha halys, the brown marmorated stink bug. Biol Control 107:11–20

    Article  Google Scholar 

  • Ogburn E, Bessin R, Dieckhoff C, Dobson R, Grieshop M, Hoelmer K, Mathews C, Moore J, Nielsen A, Poley K, Pote J, Rogers M, Welty C, Walgenbach J (2016) Natural enemy impact on eggs of the invasive brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), in organic agroecosystems: a regional assessment. Biol Control 101:39–51

    Article  Google Scholar 

  • Quinn NF, Talamas EJ, Acebes-Doria AL, Leskey TC, Bergh JC (2019) Vertical sampling in tree canopies for Halyomorpha halys (Hemiptera: Pentatomidae) life stages and its egg parasitoid, Trissolcus japonicus (Hymenoptera: Scelionidae). Environ Entomol 48:173–180

    Article  PubMed  Google Scholar 

  • Rice K, Bergh C, Bergmann 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, Martinson H, Mitchell W, Nielson A, Pfeiffer D, Raupp M, Rodriguez-Saona C, Shearer P, Shrewsbury P, Venugopal P, Whalen J, Wiman N, Leskey T, Tooker J (2014) Biology, ecology, and management of brown marmorated stink bug (Hemiptera: Pentatomidae). J Integr Pest Manag 5:1–13

    Article  Google Scholar 

  • Rider D (2015) Pentatomoidea home page. North Dakota State University. https://www.ndsu.edu/pubweb/~rider/Pentatomoidea/. Accessed 2 Oct 2017

  • Sabbatini Peverieri G, Talamas E, Bon MC, Marianelli L, Bernardinelli I, Malossini G, Benvenuto L, Roversi PF, Hoelmer K (2018) Two asian egg parasitoids emerge in Italy on Halyomorpha halys: Trissolcus mitsukurii (Ashmead) and Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae). J Hym Res 67:37–53

    Google Scholar 

  • Stahl J, Tortorici F, Pontini M, Bon MC, Hoelmer K, Marazzi C, Tavella L, Haye T (2019) First discovery of adventive populations of Trissolcus japonicus (Ashmead) in Europe. J Pest Sci 92:371–379

    Article  Google Scholar 

  • Taekul C, Valerio A, Austin A, Klompen H, Johnson N (2014) Molecular phylogeny of telenomine egg parasitoids (Hymenoptera: Platygastridae s.l.: Telenominae): evolution of host shifts and implications for classification. Syst Entomol 39:24–35

    Article  Google Scholar 

  • Talamas EJ, Buffington M, Hoelmer K (2013) New synonymy of Trissolcus halyomorphae (Yang). J Hymenopt Res 33:113–117

    Article  Google Scholar 

  • 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 43:45–110

    Article  Google Scholar 

  • Talamas EJ, Herlihy MV, Dieckhoff C, Hoelmer K, Buffington M, Bon M-C, Weber DC (2015b) Trissolcus japonicus (Ashmead) (Hymenoptera, Scelionidae) emerges in North America. J Hymenopt Res 43:119–128

    Article  Google Scholar 

  • Tobin PC, Kean JM, Suckling DM, McCullough DG, Herms DA, Stringer LD (2014) Determinants of successful arthropod eradication programs. Biol Invasions 16:401–414

    Article  Google Scholar 

  • van Driesche RG, Murray TJ (2004) Overview of testing schemes and designs used to estimate host ranges. In: van Driesche RG, Reardon R (eds) Assessing host ranges for parasitoids and predators used for classical biological control: a guide to best practice. Forest Health Technology Enterprise Team (FHTET), Morgantown, pp 68–89

    Google Scholar 

  • Williams DA (1982) Extra-binomial variation in logistic linear models. J R Stat Soc 31:144–148

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Zhang J, Zhang F, Gariepy T, Mason P, Gillespie D, Talamas E, Haye T (2017) Seasonal parasitism and host specificity of Trissolcus japonicus in northern China. J Pest Sci 90:1127–1141

    Article  Google Scholar 

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Acknowledgements

We wish to thank Dr Barbara Barratt (AgResearch), Dr Mark Hoddle (University of California, Riverside), Dr Cathy McKenna (Plant and Food Research), Dr David Teulon (Plant and Food Research), Graham Walker (Plant and Food Research) and Libby Burgess (Plant and Food Research) for their useful comments on draft versions of this manuscript. We thank Mark Wohlers (Plant and Food Research) for assistance in statistical analysis, and Dr N. A. Martin for collecting Pentatomidae from which laboratory cultures were initiated. We also thank Brian Patrick (Wildlands Consultants Ltd), and the AgResearch Invermay team for their efforts in support of this work. This work was funded by New Zealand’s Ministry of Science and Innovation, the Better Border Biosecurity (B3) (http://www.b3nz.org) research collaboration and The New Zealand Institute for Plant & Food Research Limited Strategic Science Investment Fund. Support for maintenance of T. japonicus cultures in the USA was provided to K. Hoelmer by USDA NIFA SCRI Grant 2011-51181-30937.

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Authors and Affiliations

  1. The New Zealand Institute for Plant & Food Research Limited, Mt Albert Research Centre, Private Bag 92169, Mt Albert, Auckland, 1142, New Zealand

    J. G. Charles, G. A. Avila, Sophie Hunt, Robin Gardner-Gee, Frances MacDonald & Vicky Davis

  2. Better Border Biosecurity, New Zealand http://www.b3nz.org

    J. G. Charles, G. A. Avila, Sophie Hunt, Frances MacDonald & Vicky Davis

  3. USDA/ARS, Beneficial Insects Introduction Research Unit, Newark, DE, 19713, USA

    Kim A. Hoelmer

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  1. J. G. Charles
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Correspondence to G. A. Avila.

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Charles, J.G., Avila, G.A., Hoelmer, K.A. et al. Experimental assessment of the biosafety of Trissolcus japonicus in New Zealand, prior to the anticipated arrival of the invasive pest Halyomorpha halys. BioControl 64, 367–379 (2019). https://doi.org/10.1007/s10526-019-09949-x

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