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Irradiation-induced sterility in an egg parasitoid and possible implications for the use of biological control in insect eradication

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  • 1.

    DeBach, P. & Rosen, D. Biological Control by Natural Enemies (Cambridge University Press, 1991).

    Google Scholar 

  • 2.

    Naranjo, S. E., Ellsworth, P. C. & Frisvold, G. B. Economic value of biological control in integrated pest management of managed plant systems. Annu. Rev. Entomol. 60, 621–645 (2015).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 3.

    Walker, J. T. S., Suckling, D. M. & Wearing, C. H. Past, present, and future of integrated control of apple pests: The New Zealand experience. Annu. Rev. Entomol. 62, 231–248 (2017).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 4.

    van Lenteren, J. C., Bale, J., Bigler, F., Hokkanen, H. M. T. & Loomans, A. J. M. Assessing risks of releasing exotic biological control agents of arthropod pests. Annu. Rev. Entomol. 51, 609–634 (2006).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 5.

    Bale, J. S., van Lenteren, J. C. & Bigler, F. Biological control and sustainable food production. Phil. Trans. R. Soc. Lond. B 363, 761–776 (2008).

    Article 
    CAS 

    Google Scholar 

  • 6.

    Sheppard, A. W. et al. A global review of risk-benefit-cost analysis for the introduction of classical biological control agents against weeds: A crisis in the making?. Biocontrol News Inf. 24, 91N-108N (2003).

    Google Scholar 

  • 7.

    Barratt, B. I. P., Blossey, B. & Hokkanen, H. M. Post-release evaluation of non-target effects of biological control agents. In Environmental Impact of Invertebrates for Biological Control of Arthropods: Methods and Risk Assessment (eds Bigler, F. et al.) 166–186 (CABI Publishing, 2006).

    Chapter 

    Google Scholar 

  • 8.

    Barratt, B. I. P., Moeed, A. & Malone, L. A. Biosafety assessment protocols for new organisms in New Zealand: Can they apply internationally to emerging technologies?. Environ. Impact Assess. Rev. 26, 339–358 (2006).

    Article 

    Google Scholar 

  • 9.

    Klassen, W. & Curtis, C. F. History of the sterile insect technique. In Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management (eds Dyck, V. A. et al.) 3–38 (Springer, 2021).

    Google Scholar 

  • 10.

    Hendrichs, J., Kenmore, P., Robinson, A. S. & Vreyson, M. J. B. Area-wide integrated pest management (AW-IPM): principles, practice and prospects. In Area-Wide Control of Insect Pests (eds Vreysen, M. J. B. et al.) 3–34 (Springer, 2007).

    Google Scholar 

  • 11.

    Knipling, E. F. Possibilities of insect control or eradication through the use of sexually sterile males. J. Econ. Entomol. 48, 459–462 (1955).

    Article 

    Google Scholar 

  • 12.

    Brockerhoff, E. G., Liebhold, A. M., Richardson, B. & Suckling, D. M. Eradication of invasive forest insects: Concepts, methods, costs and benefits. NZ J. For. Sci. 40, S117–S135 (2010).

    Google Scholar 

  • 13.

    Suckling, D. M., Tobin, P. C., McCullough, D. G. & Herms, D. A. Combining tactics to exploit Allee effects for eradication of alien insect populations. J. Econ. Entomol. 105, 1–13 (2012).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 14.

    Hendrichs, J., Enkerlin, W. R. & Pereira, R. Invasive insect pests: challenges and the role of the sterile insect technique in their prevention, containment, and eradication. In Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management 885–922 (Springer, 2021).

    Chapter 

    Google Scholar 

  • 15.

    Nagel, P. & Peveling, R. Environment and the sterile insect technique. In Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management (eds Dyck, V. A. et al.) 499–519 (Springer, 2021).

    Google Scholar 

  • 16.

    Knipling, E. F. The Basic Principles of Insect Population Suppression and Management (U.S. Department of Agriculture, 1979).

    Google Scholar 

  • 17.

    Barclay, H. J. Models for pest control: Complementary effects of periodic releases of sterile pests and parasitoids. Theor. Popul. Biol. 32, 76–89 (1987).

    Article 

    Google Scholar 

  • 18.

    Soller, M. & Lanzrein, B. Polydnavirus and venom of the egg-larval parasitoid Chelonus inanitus (Braconidae) induce developmental arrest in the prepupa of its host Spodoptera littoralis (Noctuidae). J. Insect Physiol. 42, 471–481 (1996).

    Article 
    CAS 

    Google Scholar 

  • 19.

    Tillinger, N. A., Hoch, G. & Schopf, A. Effects of parasitoid associated factors of the endoparasitoid Glyptapanteles liparidis (Hymenoptera: Braconidae). Eur. J. Entomol. 101, 243–249 (2004).

    Article 

    Google Scholar 

  • 20.

    Tunçbilek, A. S., Canpolat, U. & Ayvaz, A. Effects of gamma radiation on suitability of stored cereal pest eggs and the reproductive capability of the egg parasitoid Trichogramma evanescens (Trichogrammatidae: Hymenoptera). Biocontrol Sci. Techn. 19, 179–191 (2009).

    Article 

    Google Scholar 

  • 21.

    Lynch, L. D. et al. Insect biological control and non-target effects: a European perspective. In Evaluating Indirect Ecological Effects of Biological Control (eds Wajnberg, E. et al.) 99–126 (Springer, 2001).

    Google Scholar 

  • 22.

    van Lenteren, J. C. V. et al. Environmental risk assessment of exotic natural enemies used in inundative biological control. Biocontrol 48, 3–38 (2003).

    Article 

    Google Scholar 

  • 23.

    Horrocks, K. J., Avila, G. A., Holwell, G. I. & Suckling, D. M. Integrating sterile insect technique with the release of sterile classical biocontrol agents for eradication: Is the Kamikaze Wasp Technique feasible?. Biocontrol 65, 257–271 (2020).

    Article 

    Google Scholar 

  • 24.

    Welsh, T. J., Stringer, L. D., Caldwell, R., Carpenter, J. E. & Suckling, D. M. Irradiation biology of male brown marmorated stink bugs: Is there scope for the sterile insect technique?. Int. J. Radiat. Biol. 93, 1357–1363 (2017).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 25.

    Suckling, D. M. et al. The competitive mating of irradiated brown marmorated stink bugs, Halyomorpha halys, for the sterile insect technique. Insects 10, 411 (2019).

    PubMed Central 
    Article 

    Google Scholar 

  • 26.

    Larivière, M.-C. Fauna of New Zealand (Manaaki Whenua Press, 1995).

    Google Scholar 

  • 27.

    Martin, N. A. Green vegetable bug – Nezara viridula. Interesting insects and other invertebrates. New Zealand arthropod factsheet number 47 https://nzacfactsheets.landcareresearch.co.nz/factsheet/InterestingInsects/Green-vegetable-bug—Nezara-viridula.html (2018). Accessed 16 Sept 2020.

  • 28.

    Powell, J. E. & Shepard, M. Biology of Australian and United States strains of Trissolcus basalis, a parasitoid of the green vegetable bug Nezara viridula. Austr. Ecol. 7, 181–186 (1982).

    Article 

    Google Scholar 

  • 29.

    Cantón-Ramos, J. M. & Callejón-Ferre, Á. J. Raising Trissolcus basalis for the biological control of Nezara viridula in greenhouses of Almería (Spain). Afr. J. Agric. Res. 5, 3207–3212 (2010).

    Google Scholar 

  • 30.

    Loch, A. D. & Walter, G. H. Mating behavior of Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae): Potential for outbreeding in a predominantly inbreeding species. J. Insect Behav. 11, 2 (2002).

    Google Scholar 

  • 31.

    Johns, H. F. & Cunningham, J. R. The interaction of single beams of x and gamma rays with a scattering medium. In The Physics of Radiology 349–350 (Charles C Thomas, 1983).

    Google Scholar 

  • 32.

    Bin, F., Vinson, S. B., Strand, M. R., Colazza, S. & Jones, W. A. Source of an egg kairomone for Trissolcus basalis, a parasitoid of Nezara viridula. Physiol. Entomol. 18, 7–15 (1993).

    Article 

    Google Scholar 

  • 33.

    Mahmoud, A. M. A. & Lim, U. T. Evaluation of cold-stored eggs of Dolycoris baccarum (Hemiptera: Pentatomidae) for parasitization by Trissolcus nigripedius (Hymenoptera: Scelionidae). Biol. Control 43, 287–293 (2007).

    Article 

    Google Scholar 

  • 34.

    Haye, T. et al. Fundamental host range of Trissolcus japonicus in Europe. J. Pest Sci. 93, 171–182 (2020).

    Article 

    Google Scholar 

  • 35.

    Cusumano, A. et al. First extensive characterization of the venom gland from an egg parasitoid: Structure, transcriptome and functional role. J. Insect Physiol. 107, 68–80 (2018).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • 36.

    Bundy, C. S. & McPherson, R. M. Morphological examination of stink bug (Heteroptera: Pentatomidae) eggs on cotton and soybeans, with a key to genera. Ann. Entomol. Soc. Am. 93, 616–624 (2000).

    Article 

    Google Scholar 

  • 37.

    Favetti, B. M., Butnariu, A. R. & Doetzer, A. K. Storage of Euschistus heros eggs (Fabricius) (Hemiptera: Pentatomidae) in liquid nitrogen for parasitization by Telenomus podisi Ashmead (Hymenoptera: Platygastridae). Neotrop. Entomol. 43, 291–293 (2014).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • 38.

    Kazmer, D. J. & Luck, R. F. Field tests of the size-fitness hypothesis in the egg parasitoid Trichogramma pretiosum. Ecology 76, 412–425 (1995).

    Article 

    Google Scholar 

  • 39.

    Wickham, H. Ggplot2: Elegant Graphics for Data Analysis (Springer, 2016).

    MATH 
    Book 

    Google Scholar 

  • 40.

    Bates, D., Machler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

    Article 

    Google Scholar 

  • 41.

    Chapman, T., Miyatake, T., Smith, H. K. & Partridge, L. Interactions of mating, egg production and death rates in females of the Mediterranean fruit fly, Ceratitis capitata. Proc. R. Soc. Lond. B 265, 1879–1894 (1998).

    Article 
    CAS 

    Google Scholar 

  • 42.

    Grosch, D. S. & Sullivan, R. L. The quantitative aspects of permanent and temporary sterility induced in female Habrobracon by x-rays and β radiation. Radiat. Res. 1, 294–320 (1954).

    ADS 
    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 43.

    Colazza, S. & Wajnberg, E. Effects of host egg mass size on sex ratio and oviposition sequence of Trissolcus basalis (Hymenoptera: Scelionidae). Environ. Entomol. 27, 329–336 (1998).

    Article 

    Google Scholar 

  • 44.

    Rosi, M. C., Isidoro, N., Colazza, S. & Bin, F. Source of the host marking pheromone in the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae). J. Insect Physiol. 47, 989–995 (2001).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 45.

    Abram, P. K., Brodeur, J., Burte, V. & Boivin, G. Parasitoid-induced host egg abortion: An underappreciated component of biological control services provided by egg parasitoids. Biol. Control 98, 52–60 (2016).

    Article 

    Google Scholar 

  • 46.

    Kuske, S. et al. Dispersal and persistence of mass released Trichogramma brassicae (Hymenoptera: Trichogrammatidae) in non-target habitats. Biol. Control 27, 181–193 (2003).

    Article 

    Google Scholar 

  • 47.

    Draz, K. A., Tabikha, R. M., El-Aw, M. A. & Darwish, H. F. Impact of gamma radiation doses on sperm competitiveness, fecundity and morphometric characters of peach fruit fly Bactrocera zonata (Saunders) (Diptera: Tephiritidae). J. Radiat. Res. Appl. Sci. 9, 352–362 (2016).

    Article 
    CAS 

    Google Scholar 

  • 48.

    Ali, A., Rashid, M. A., Huang, Q. Y. & Lei, C.-L. Effect of UV-A radiation as an environmental stress on the development, longevity, and reproduction of the oriental armyworm, Mythimna separata (Lepidoptera: Noctuidae). Environ. Sci. Pollut. Res. 23, 17002–17007 (2016).

    Article 
    CAS 

    Google Scholar 

  • 49.

    Liebhold, A. M. et al. Eradication of invading insect populations: From concepts to applications. Annu. Rev. Entomol. 61, 335–352 (2016).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 50.

    Tobin, P. C. et al. Determinants of successful arthropod eradication programs. Biol. Invasions 16, 401–414 (2014).

    Article 

    Google Scholar 

  • 51.

    Pluess, T. et al. Which factors affect the success or failure of eradication campaigns against alien species?. PLoS ONE 7, e48157 (2012).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 52.

    Colunga-Garcia, M., Magarey, R. A., Haack, R. A., Gage, S. H. & Qi, J. Enhancing early detection of exotic pests in agricultural and forest ecosystems using an urban-gradient framework. Ecol. Appl. 20, 303–310 (2010).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 53.

    Myers, J. H., Savoie, A. & van Randen, E. Eradication and pest management. Annu. Rev. Entomol. 43, 471–491 (1998).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 54.

    Lance, D. R. & McInnis, D. O. Biological basis of the sterile insect technique. In Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management (eds Dyck, V. A. et al.) 69–94 (Springer, 2021).

    Google Scholar 

  • 55.

    Godfray, H. C. J. Oviposition behaviour. In Parasitoids: Behavioural and Evolutionary Ecology Vol. 67 83–150 (Princeton University Press, 1994).

    Chapter 

    Google Scholar 

  • 56.

    Ravuiwasa, K. T., Lu, K.-H., Shen, T.-C. & Hwang, S.-Y. Effects of irradiation on Planococcus minor (Hemiptera: Pseudococcidae). J. Econ. Entomol. 102, 1774–1780 (2009).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 57.

    Bloem, S., Bloem, K. A. & Knight, A. L. Oviposition by sterile codling moths, Cydia pomonella (Lepidoptera: Tortricidae) and control of wild populations with combined releases of sterile moths and egg parasitoids. J. Entomol. Soc. 95, 99–109 (1998).

    Google Scholar 

  • 58.

    Hasaballah, A. I. Impact of gamma irradiation on the development and reproduction of Culex pipiens (Diptera; Culicidae). Int. J. Radiat. Biol. 94, 844–849 (2018).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 59.

    Sagarra, L. A., Vincent, C. & Stewart, R. K. Body size as an indicator of parasitoid quality in male and female Anagyrus kamali (Hymenoptera: Encyrtidae). Bull. Entomol. Res. 91, 363–367 (2001).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 60.

    Bertin, A., Pavinato, V. A. C. & Parra, J. R. P. Effects of intraspecific hybridization on the fitness of the egg parasitoid Trichogramma galloi. Biocontrol 63, 555–563 (2018).

    Article 

    Google Scholar 

  • 61.

    Bloem, S., Bloem, K. A., Carpenter, J. E. & Calkins, C. O. Inherited sterility in codling moth (Lepidoptera: Tortricidae): Effect of substerilizing doses of radiation on insect fecundity, fertility, and control. Ann. Entomol. Soc. Am. 92, 222–229 (1999).

    Article 

    Google Scholar 

  • 62.

    Bloem, S., Carpenter, J. E. & Hofmeyr, J. H. Radiation biology and inherited sterility in false codling moth (Lepidoptera:Tortricidae). J. Econ. Entomol. 96, 1724–1731 (2003).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 63.

    El-Kholy, E. M. S. Biological and biochemical effects of vitamin ‘c’ on the normal and irradiated mediterranean fruit fly, Ceratitis capitata (wied). J. Radiat. Res. Appl. Sci. 2, 197–212 (2009).

    Google Scholar 

  • 64.

    Rempoulakis, P., Castro, R., Nemny-Lavy, E. & Nestel, D. Effects of radiation on the fertility of the Ethiopian fruit fly, Dacus ciliatus. Entomol. Exp. Appl. 155, 117–122 (2015).

    Article 

    Google Scholar 

  • 65.

    Würgler, F. E. & Lütolf, H.-U. Radiosensitivity of oocytes of Drosophila I. sensitivity of class-a oocytes of triploid and diploid females. Int. J. Radiat. Biol. 21, 455–463 (1972).

    Google Scholar 

  • 66.

    Field, S. A. Patch exploitation, patch-leaving and pre-emptive patch defence in the parasitoid wasp Trissolcus basalis (Insecta: Scelionidae). Ethology 104, 323–338 (1998).

    Article 

    Google Scholar 

  • 67.

    Sked, S. L. & Calvin, D. D. Temporal synchrony between Macrocentrus cingulum (Hymenoptera: Braconidae) with its preferred host, Ostrinia nubilalis (Lepidoptera: Crambidae). Environ. Entomol. 34, 344–352 (2005).

    Article 

    Google Scholar 

  • 68.

    Jiang, N., Zhou, G., Overholt, W. A., Muchugu, E. & Schulthess, F. The temporal correlation and spatial synchrony in the stemborer and parasitoid system of Coast Kenya with climate effects. Ann. Soc. Entomol. Fr. 42, 381–387 (2006).

    Article 

    Google Scholar 

  • 69.

    Whitten, M. & Mahon, R. Misconceptions and constraints. In Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management (eds Dyck, V. A. et al.) 601–626 (Springer, 2021).

    Google Scholar 

  • 70.

    Lee, Y. J. & Ducoff, H. S. Radiation-enhanced resistance to oxygen: A possible relationship to radiation-enhanced longevity. Mech. Ageing Dev. 27, 101–109 (1984).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 71.

    Suckling, D. M., Wee, S. L. & Pedley, R. Assessing competitive fitness of irradiated painted apple moth Teia anartoides (Lepidoptera: Lymantriidae). N.Z. Plant Prot. 57, 171–176 (2004).

    Google Scholar 

  • 72.

    Wee, S. L. et al. Effects of substerilizing doses of gamma radiation on adult longevity and level of inherited sterility in Teia anartoides (Lepidoptera: Lymantriidae). J. Econ. Entomol. 98, 732–738 (2005).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 73.

    Vilca Mallqui, K. S., Vieira, J. L., Guedes, R. N. C. & Gontijo, L. M. Azadirachtin-induced hormesis mediating shift in fecundity-longevity trade-off in the Mexican bean weevil (Chrysomelidae: Bruchinae). J. Econ. Entomol. 107, 860–866 (2014).

    Article 

    Google Scholar 

  • 74.

    Monroy Kuhn, J. M. & Korb, J. Editorial overview: Social insects: Aging and the re-shaping of the fecundity/longevity trade-off with sociality. Curr. Opin. Insect Sci. 16, 7–10 (2016).

    Google Scholar 

  • 75.

    Blacher, P., Huggins, T. J. & Bourke, A. F. G. Evolution of ageing, costs of reproduction and the fecundity–longevity trade-off in eusocial insects. Proc. R. Soc. B-Biol. Sci. 284, 20170380 (2017).

    Article 

    Google Scholar 

  • 76.

    Flatt, T. Survival costs of reproduction in Drosophila. Exp. Gerontol. 46, 369–375 (2011).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 77.

    Vogt, E. & Nechols, J. R. The influence of host deprivation and host source on the reproductive biology and longevity of the squash bug egg parasitoid Gryon penssylvanicum (Ashmead) (Hymenoptera: Scelionidae). Biol. Control 3, 148–154 (1993).

    Article 

    Google Scholar 

  • 78.

    Ramesh, B. & Manickavasagam, S. Tradeoff between longevity and fecundity in relation to host availability in a thelytokous oophagous parasitoid, Trichogramma brasiliensis Ashmead (Trichogrammatidae: Hymenoptera). Int. J. Trop. Insect Sci. 23, 207–210 (2003).

    Article 

    Google Scholar 

  • 79.

    Gurr, G. M. & Kvedaras, O. L. Synergizing biological control: scope for sterile insect technique, induced plant defences and cultural techniques to enhance natural enemy impact. Biol. Control 52, 198–207 (2010).

    Article 

    Google Scholar 

  • 80.

    Knipling, E. F. Principles of Insect Parasitism Analyzed from New Perspectives: Practical Implications for Regulating Insect Populations by Biological Means (United States Department of Agriculture, 1992).

    Google Scholar 

  • 81.

    Orozco, D., Domínguez, J., Reyes, J., Villaseñor, A. & Gutiérrez, J. M. SIT and biological control of Anastrepha fruit flies in Mexico. in Proceedings of the 6th International Fruit Fly Symposium 245–249 (Isteg Scientific Publications, 2002).

  • 82.

    Wong, T. T. Y., Ramadan, M. M., Herr, J. C. & McInnis, D. O. Suppression of a Mediterranean fruit fly (Diptera: Tephritidae) population with concurrent parasitoid and sterile fly releases in Kula, Maui, Hawaii. J. Econ. Entomol. 85, 1671–1681 (1992).

    Article 

    Google Scholar 

  • 83.

    Cossentine, J. E. & Jensen, L. B. M. Releases of Trichogramma platneri (Hymenoptera: Trichogrammatidae) in apple orchards under a sterile codling moth release program. Biol. Control 18, 179–186 (2000).

    Article 

    Google Scholar 

  • 84.

    Carpenter, J. E., Bloem, S. & Hofmeyr, J. H. Acceptability and suitability of eggs of false codling moth (Lepidoptera: Tortricidae) from irradiated parents to parasitism by Trichogrammatoidea cryptophlebiae (Hymenoptera: Trichogrammatidae). Biol. Control 30, 351–359 (2004).

    Article 

    Google Scholar 

  • 85.

    Carpenter, J. E., Bloem, S. & Hofmeyr, J. H. Area-wide control tactics for the false codling moth Thaumatotibia leucotreta in South Africa: a potential invasive species. In Area-Wide Control of Insect Pests (eds Vreysen, M. J. B. et al.) 351–359 (Springer, 2007).

    Google Scholar 

  • 86.

    Faúndez, E. I. & Rider, D. A. The brown marmorated stink bug Halyomorpha halys (Stål, 1855) (Heteroptera: Pentatomidae) in Chile. Arquivos Entomol. 17, 305–307 (2017).

    Google Scholar 

  • 87.

    Kriticos, D. J. et al. The potential global distribution of the brown marmorated stink bug, Halyomorpha halys, a critical threat to plant biosecurity. J. Pest Sci. 90, 1033–1043 (2017).

    Article 

    Google Scholar 

  • 88.

    Kiwifruit Vine Health. KVH information sheet: BMSB risk update January 2019 (Kiwifruit Vine Health, 2019).

  • 89.

    Vandervoet, T. F., Bellamy, D. E., Anderson, D. & MacLellan, R. Trapping for early detection of the brown marmorated stink bug, Halyomorpha halys New Zealand. N.Z. Plant Prot. 72, 36–43 (2019).

    Google Scholar 

  • 90.

    Laing, K., Belton, D. & Taylor, J. Decision on releasing Trissolcus japonicus from containment. (Environmental Protection Authority, 2018).

  • 91.

    Charles, J. G. 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).

    Article 
    CAS 

    Google Scholar 


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