Physiological host range of Trissolcus japonicus in relation to Halyomorpha halys and other pentatomids from California

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Brown marmorated stinkbug (BMSB), Halyomorpha halys Stål (Hemiptera: Pentatomidae), is native to Asia and an invasive urban and agricultural pest in the US. In California (CA), BMSB has been recorded attacking specialty crops such as almonds and peaches. The egg parasitoid Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae), a key BMSB natural enemy native to Asia, is a candidate for classical biological control efforts targeting BMSB in CA and other parts of the US Trissolcus japonicus cannot be introduced deliberately into CA for BMSB control without US federal regulatory agency approval which is contingent on better understanding of its host range and specificity. Consequently, the host specificity and physiological host range of T. japonicus was evaluated under laboratory quarantine conditions by exposing eggs of BMSB and non-target pentatomid hosts (native and other exotic species) found in CA to T. japonicus. No-choice and binary-choice experiments provided female T. japonicus with equal unrestricted access to eggs of BMSB and non-target pentatomids. In addition to BMSB, eggs from six of ten resident pentatomid species found in CA were parasitized by T. japonicus. However, T. japonicus attack and emergence rates were consistently higher on BMSB when compared to non-target species. These results suggest that T. japonicus is oligophagous, but BMSB is a superior reproductive host compared to non-target pentatomid species that were evaluated. The implications of these findings for classical biological control efforts targeting BMSB in CA are discussed.

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  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 16:1387–1395

  2. Abram PK, Brodeur J, Burte V, Boivin G (2016) Parasitoid-induced host egg abortion: an underapparent component of biological control services provided by egg parasitoids. Biol Control 98:52–60

  3. Abram PK, Brodeur J, Urbaneja A, Tena A (2019a) Nonreproductive effects of insect parasitoids on their hosts. Annu Rev Entomol 64:259–276

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

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

  6. Avila GA, Charles JG (2018b) Species of pentatomidae present in New Zealand, including a summary of T. japonicus host testing and analysis. In: Application form to obtain approval to release new organisms (through importing for release or releasing from containment). New Zealand Government Environmental Protection Authority. Accessed 09 Jan 2019

  7. Bon MC, Lesieur V (2016) Update on the genetic characterization of west coast populations of Halyomorpha halys and adventive populations of its egg parasitoid Trissolcus japonicus. Accessed 21 Dec 2018

  8. Botch PS, Delfosse ES (2018) Host-acceptance behavior of Trissolcus japonicus (Hymenoptera: Scelionidae) reared on the invasive Halyomorpha halys (Heteroptera: Pentatomidae) and nontarget species. Environ Entomol 47:403–411

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

  10. Cornelius ML, Dieckhoff C, Hoelmer KA, Olsen RT, Weber DC, Herlihy MV, Talamas EJ, Vinyard BT, Greenstone MH (2016) Biological control of sentinel egg masses of the exotic invasive stink bug Halyomorpha halys (Stål) in Mid-Atlantic USA ornamental landscapes. Biol Control 103:11–20

  11. Delfosse ES (2005) Risk and ethics in biological control. Biol Control 35:319–329

  12. Dieckhoff C, Tatman KM, Hoelmer KA (2017) Natural biological control of Halymorpha halys by native egg parasitoids: a multi-year survey in northern Delaware. J Pest Sci 90:1143–1158

  13. Froeschner RC (1988) Family Pentatomidae Leach, 1815. In: Henry TJ, Froeschner RC (eds) Catalog of the heteroptera, or true bugs of Canada and the Continental United States. EJ Brill, New York, pp 544–597

  14. Gariepy TD, Bruin A, Konopka J, Scott-Dupree C, Fraser H, Bon M-C, Talamas E (2018) A modified DNA barcode approach to define trophic interactions between native and exotic pentatomids and their parasitoids. Mol Ecol 28:456–470

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

  16. 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

  17. Herlihy MV, Talamas EJ, Weber DC (2016) Attack and success of native and exotic parasitoids on eggs of Halyomorpha halys in three Maryland habitats. PLoS ONE 11(3):e0150275

  18. Hoelmer K (2017) Distribution and impact of Trissolcus japonicus and status of petition to release quarantined populations. Accessed 13 Dec 2018

  19. Jones AL, Jennings DE, Hooks CRR, Shrewsbury PM (2017) Field surveys of egg mortality and indigenous egg parasitoids of the brown marmorated stink bug, Halyomorpha halys, in ornamental nurseries in the mid-Atlantic region of the USA. J Pest Sci 90:1159–1168

  20. Kaser JM, Nielsen AL, Abram PK (2018) Biological control effects of non-reproductive host mortality caused by insect parasitoids. Ecol Appl 28:1081–1092

  21. Konopka JK, Gariepy TD, Haye T, Zhang J, Rubin BD, McNeil JN (2019) Exploitation of pentatomids by native egg parasitoids in the native and introduced ranges of Halyomorpha halys: a molecular approach using sentinel egg mass. J Pest Sci 92:609–619

  22. 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

  23. Lanfen Q (2007) Studies on biology of the brown marmorated stink bug Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), an important pest for pome trees in China and its biological control. Ph.D. dissertation, Chinese Academy of Forestry, Beijing

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

  25. Lara JR, Kamiyama MT, Hernandez G, Nay J, Hoddle MS (2017) Assessment of feeding acceptance and injury of Kerman pistachios, Pistacia vera, by brown marmorated stink bug (Hemiptera: Pentatomidae). J Insect Sci 17:106

  26. Lara JR, Pickett C, Hannon E, Gonzalez L, Figueroa S, Romo M, Cabanas C, Bazurto V, Strode V, Briseno K, Lewis M, Atkinson M, Hoddle M (2018a) Trouble comes in pairs: invasive stink bugs in California. CAPCA Advis 21:62–72

  27. Lara JR, Kamiyama M, Hernandez G, Lewis M, Hoddle MS (2018b) Laboratory assessment of feeding injury and preference of brown marmorated stink bug, Halyomorpha halys Stål (Hemiptera: Pentatomidae), for Actinidia chinensis var. deliciosa ‘Hayward’ (Zespri® Green) and Actinidia chinensis var. chinensis ‘Zesy002’ (Zespri® SunGold). NZ Entomol 41:12–24

  28. 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

  29. Leskey TC, Short BD, Butler BR, Wright SE (2012) 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 2012:535062

  30. 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

  31. [NIC] Northeastern IPM Center (2017) Samurai wasp (Trissolcus japonicus). Accessed 02 Jan 2019

  32. O’Neil RJ (1997) Functional response and search strategy of Podisus maculiventris (Heteroptera: Pentatomidae) attacking colorado potato beetle (Coleoptera: Chrysomelidae). Environ Entomol 26:1183–1190

  33. Pickett C, Lara R, Hoddle M (2015) Brown marmorated stink bug in California. BMSB national working group meeting. Accessed 02 May 2019

  34. 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, Rodiguez-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:A1–A13

  35. Rijal J, Duncan R (2017) Brown marmorated stink bug spread to peach growing areas in the Northern San Joaquin Valley. CAPCA Advis 20:32–35

  36. Rijal J, Gyawaly S (2018) Characterizing brown marmorated stink bug injury in almond, a new host crop in California. Insects 9:126

  37. SAS Institute Inc. (2011) SAS 9.3. Cary, NC, USA

  38. Tognon R, Santana J, Zhang Q-H, Millar JC, Aldrich JR, Zalom FG (2016) Volatiles mediating parasitism of Euschistus conspersus and Halyomorpha halys eggs by Telenomus podisi and Trissolcus erugatus. J Chem Ecol 42:1016–1027

  39. [USDA-APHIS] United States Department of Agriculture, Animal and Plant Health Inspection Services (2018) Biological control organism permits. Accessed 10 Jan 2019

  40. Valentin RE, Nielsen AL, Wiman NG, Lee D-H, Fonseca DM (2017) Global invasion network of the brown marmorated stink bug, Halyomorpha halys. Sci Rep 7:9866

  41. 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

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This project was supported, in part, by the US Department of Agriculture’s (USDA) Agricultural Marketing Service through Grant 16-SCBGP-CA-0035, USDA Farm Bill 16-8130-0359-CA, USDA-NIFA SCRI 2016-51181-25409, California Pistachio Research Board Grant CPRB-16101166, and Consolidated Central Valley Table Grape Pest and Disease Control District Grant CCVTGP-15004. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the USDA and the other funding agencies. Special thanks to Sarah Ocampo, Jenny Nguyen, Jose Alvarado Rojas, Brett Birdwell, Ruth Amrich and Andrea Rios for their assistance with parasitoid and stink bug rearing. We also thank Chris Borkent for customizing the BMSB distribution map. We are greatly indebted to Kim Hoelmer, Kathy Tatman, and Christine Dieckhoff for providing starter colony specimens of Trissolcus japonicus and assistance with the design of safety testing protocols.

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Correspondence to Jesús R. Lara.

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Handling Editor: Stefano Colazza

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Lara, J.R., Pickett, C.H., Kamiyama, M.T. et al. Physiological host range of Trissolcus japonicus in relation to Halyomorpha halys and other pentatomids from California. BioControl 64, 513–528 (2019) doi:10.1007/s10526-019-09950-4

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  • Classical biological control
  • Invasive species
  • Non-target species
  • Pentatomidae
  • Host-range
  • Scelionidae