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Controlling Lygus plant bugs (Heteroptera: Miridae) with European Peristenus relictus (Hymenoptera: Braconidae) in Canada – risky or not?

Published online by Cambridge University Press:  09 March 2007

T. Haye
Affiliation:
CABI Bioscience Switzerland Centre, Rue des Grillons 1, 2800 Delémont, Switzerland
U. Kuhlmann*
Affiliation:
CABI Bioscience Switzerland Centre, Rue des Grillons 1, 2800 Delémont, Switzerland
H. Goulet
Affiliation:
Agriculture and Agri-Food Canada, Research Centre, K.W. Neatby Building, Ottawa, Ontario, Canada, K1A 0C6
P.G. Mason
Affiliation:
Agriculture and Agri-Food Canada, Research Centre, K.W. Neatby Building, Ottawa, Ontario, Canada, K1A 0C6
*
*Fax: +41 32 421 4871 E-mail: u.kuhlmann@cabi.org

Abstract

The European Peristenus relictus Loan (syn. P. stygicus) has been considered for biological control of Lygus plant bugs native to Canada. Laboratory and field studies were conducted in the area of origin to evaluate the host specificity of P. relictus. Laboratory choice and no-choice tests demonstrated that P. relictus attacked all non-target species offered (fundamental host range). However, closely related non-target mirids (tribe Mirini) were generally well accepted by P. relictus, while hosts from the tribe Stenodemini were less frequently attacked and less suitable for parasitoid development. To validate the laboratory results, a thorough examination of the parasitoid complex of common mirids in Europe was conducted to determine which non-target species may serve as alternative hosts for P. relictus in a natural situation (ecological host range). When comparing both approaches, the fundamental host range of P. relictus matched its ecological host range. In addition to three Lygus species, the ecological host range of P. relictus in the area of Schleswig-Holstein, northern Germany, contains at least 16 non-target species, including hosts belonging to the subfamilies Mirinae, Phylinae and Bryocorinae. A broad ecological and fundamental host range suggests that P. relictus is a generalist; however, P. relictus was not the primary contributor to parasitism of most non-target hosts studied. Although P. relictus is assumed to be of minor importance for regulating non-target populations in the area of investigation, the results of the present study indicate that P. relictus has the potential to use non-target host populations for reproduction.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2006

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References

Afscharpour, F. (1960) Ökologische Untersuchungen über Wanzen und Zikaden auf Kulturfeldern in Schleswig-Holstein. Zeitschrift für Angewandte Zoologie 47, 257301.Google Scholar
Bigler, F., Babendreier, D. & Kuhlmann, U. (2006) Environmental impact of invertebrates for biological control of arthropods: methods and risk assessment. Wallingford, Oxon, CABI Publishing.Google Scholar
Bilewicz-Pawinska, T. (1977) Parasitism of Adelphocoris lineolatus Goeze and Lygus rugulipennis Popp. (Heteroptera) by braconids and their occurrence on alfalfa. Ekologia Polska 25, 539550.Google Scholar
Bilewicz-Pawinska, T. (1982) Plant bugs (Heteroptera: Miridae) and their parasitoids (Hymenoptera: Braconidae) on cereal crops. Polish Ecological Studies 8, 113191.Google Scholar
Braun, L., Erlandson, M., Baldwin, D., Soroka, J., Mason, P., Foottit, R. & Hegedus, D. (2001) Seasonal occurrence, species composition, and parasitism of Lygus spp. in alfalfa, canola, and mustard. Canadian Entomologist 133, 565577.CrossRefGoogle Scholar
Broadbent, A.B. (1976) Laboratory studies on the biology of Peristenus stygicus Loan (Hymenoptera: Braconidae), a parasitoid of Lygus lineolaris (P. de B.) (Hemiptera: Miridae). MSc thesis, McGill University, Montreal, Quebec, Canada.Google Scholar
Broadbent, A.B., Goulet, H., Whistlecraft, J.W., Lachance, S., Mason, P.G. (1999) First Canadian record of three parasitoid species (Hymenoptera: Braconidae: Euphorinae) of the tarnished plant bug, Lygus lineolaris (Hemiptera: Miridae). Proceedings of the Entomological Society of Ontario 130, 109111.Google Scholar
Broadbent, A.B., Mason, P.G., Lachance, S., Whistlecraft, J.W., Soroka, J.J. & Kuhlmann, U. (2002) Lygus pp., plant bugs (Hemiptera: Miridae) Biological control programmes in Canada, 19812000. 152 – 159 Mason, P.G., Huber, J.T.Wallingford: Oxon Published on behalf of The Nutrition Society by CABI Publishing.Google Scholar
Butts, R.A., Lamb, R.J. (1991) Pest status of Lygus bugs (Hemiptera: Miridae) in oilseed Brassica crops. Journal of Economic Entomology 84, 15911596.CrossRefGoogle Scholar
Carl, K.P., Mason, P.G. (1996) Overseas collection and importation of Lygus parasitoids. pp. 3033Soroka, J.J.Proceedings of the Lygus working Group Meeting, 11–12. April 1996, Winnipeg, Manitoba. Saskatoon, Saskatchewan, Agriculture and Agri-Food Canada, Research Branch.Google Scholar
Carlson, J.W. (1940) Lygus bug damage to alfalfa in relation to seed production. Journal of Agricultural Research 61, 791815.Google Scholar
Clancy, D.W., Pierce, H.D. (1966) Some natural enemies of some Lygus bugs. Journal of Economic Entomology 59, 853858.CrossRefGoogle Scholar
Condit, B.P., Cate, J.R. (1982) Determination of host range in relation to systematics for Peristenus stygicus (Hym.: Braconidae), a parasitoid of Miridae. Entomophaga 27, 203210.CrossRefGoogle Scholar
Coulson, J.R. (1987) Studies on the biological control of plant bugs (Heteroptera: Miridae): an introduction and history, 1961–1983. pp. 112 in Hedlund, R.C. & Graham, H.M.Economic importance and biological control of Lygus and Adelphocoris in North America. ARS-64, Springfield, Virginia United States Department of Agriculture, Agriculture Research Service.Google Scholar
Coutinot, D. & Hoelmer, K. (1999) Parasitoids of Lygus spp. in Europe and their potential for biological control of Lygus spp. in North America. pp. 641648 ANNP Fifth International Conference on Pests in Agriculture, 7–9 December 1999, Montpellier, FranceGoogle Scholar
Craig, C.H. & Loan, C.C. (1987) Biological control efforts on Miridae in Canada. pp. 4853Hedlund, R.C., Graham, H.M.Economic importance and biological control of Lygus and Adelphocoris in North America. ARS-64, Springfield, Virginia United States Department of Agriculture, Agriculture Research Service.Google Scholar
Day, W.H. (1987) Biological control efforts against Lygus and Adelphocoris spp. infesting alfalfa in the United States, with notes on other associated mirid species. pp. 2039Hedlund, R.C. & Graham, H.M.Economic importance and biological control of Lygus and Adelphocoris in North America. ARS-64, Springfield, Virginia United States Department of Agriculture, Agriculture Research Service.Google Scholar
Day, W.H. (1996) Evaluation of biological control of the tarnished plant bug (Hemiptera: Miridae) in alfalfa by the introduced parasite Peristenus digoneutis (Hymenoptera: Braconidae). Environmental Entomology 25, 512518.CrossRefGoogle Scholar
Day, W.H. (2005) Changes in abundance of native and introduced parasites (Hymenoptera: Braconidae), and of the target and non-target plant bug species (Hemiptera: Miridae), during two classical biological control programs in alfalfa. Biological Control 33, 368374.CrossRefGoogle Scholar
Day, W.H. & Fuester, R. (2003) ARS Project: classical biological control of insect pests of crops (407139)–2003 Annual Report. (http://www.ars.usda.gov/research/projects/projects.htmACCN_NO=407139 – showpars=true&fy =2003).Google Scholar
Day, W.H., Hedlund, R.C., Saunders, L.B. & Coutinot, D. (1990) Establishment of Peristenus digoneutis (Hymenoptera: Braconidae), a parasite of the tarnished plant bug (Hemiptera: Miridae), in the United States. Environmental Entomology 19, 15281533.CrossRefGoogle Scholar
De Nardo, E.A.B., Hopper, K.R. (2004) Using the literature to evaluate parasitoid host ranges: a case study of Macrocentrus grandii (Hymenoptera: Braconidaea) introduced into North America to control Ostrinia nubilalis (Lepidoptera: Crambidae). Biological Control 31, 280295.CrossRefGoogle Scholar
Drea, J.J., Dureseau, L. & Rivet, E. (1973) Biology of Peristenus stygicus from Turkey, a potential natural enemy of Lygus bugs in North America. Environmental Entomology 2, 278280.CrossRefGoogle Scholar
Elkinton, J.S., Boettner, G.H. (2004) The effects of Compsilura concinnata, an introduced generalist tachinid, on non-target species in North America: A cautionary tale Assessing host ranges for parasitoids and predators used for classical biological control: a guide to best practice 4 – 14 van Driesche R.G. Reardon R. Morgantown, West Virginia USDA, Forest Health Technology Enterprise TeamGoogle Scholar
Fuester, R.W., Kenis, M., Swan, K.S., Kingsley, P.C., Lopez-Vaamonde, C. & Herard, F. (2001) Host range of Aphantorhaphopsis samarensis (Diptera: Tachinidae), a larval parasite of the gypsy moth (Lepidoptera: Lymantriidae). Environmental Entomology 30, 605611.CrossRefGoogle Scholar
Gillespie, D. & Foottit, R. (1997) Lygus bugs in vegetable greenhouses in B.C Proceedings of the Lygus working Group Meeting, 11–12. April 1996, Winnipeg, Manitoba 7 – 9 Soroka J.J. Saskatoon Saskatchewan, Agriculture and Agri-Food Canada, Research BranchGoogle Scholar
Godfray, H.C.J. (1994) Parasitoids, behavioral and evolutionary ecology Princeton, New Jersey Princeton University PressCrossRefGoogle Scholar
Grafton-Cardwell, B., Goodell, P.B. & Montez, G. (2000) Trends in pesticide use and pesticide resistance in San Joaquin Valley cotton. California Cotton Review 56, 47.Google Scholar
Haye, T. & Kenis, M. (2004) Biology of Lilioceris spp. (Coleoptera: Chrysomelidae) and their parasitoids in Europe. Biological Control 29, 399408.CrossRefGoogle Scholar
Haye, T., Broadbent, A.B., Whistlecraft, J. & Kuhlmann, U. (2005a) Comparative analysis of the reproductive biology of two Peristenus species (Hymenoptera: Braconidae), biological control agents of Lygus plant bugs (Hemiptera: Miridae). Biological Control 32, 442449.CrossRefGoogle Scholar
Haye, T., Goulet, H., Mason, P.G. & Kuhlmann, U. (2005b) Does fundamental host range match ecological host range? A retrospective case study of a Lygus plant bug parasitoid. Biological Control 35, 5567.CrossRefGoogle Scholar
Henneman, M.L. & Memmott, J. (2001) Infiltration of a Hawaiian community by introduced biological control agents. Science 293 13141316CrossRefGoogle ScholarPubMed
Hoddle, M.S. (2004) Analysis of fauna in the receiving area for the purpose of identifying native species that exotic natural enemies may potentially attack. pp. 2439 in van Driesche, R.G. & Reardon, R. (Eds) Assessing host ranges for parasitoids and predators used for classical biological control: a guide to best practice. Morgantown, West Virginia USDA, Forest Health Technology Enterprise Team.Google Scholar
Kuhlmann, U. & Mason, P.G. (2003) Use of field host range surveys for selecting candidate non-target species for physiological host specificity testing of entomophagous biological control agents. pp. 370377 in Van Driesche, R.G. (ed). Proceedings of the 1st International Symposium on Biological Control of Arthropods, Honolulu, Hawaii, 14–18 January 2002, WV, FHTET-2033–05 Morgantown, United States Department of Agriculture, Forest Service.Google Scholar
Kuhlmann, U., Mason, P.G., Foottit, R.G. (2000) Host specificity assessment of European Peristenus parasitoids for classical biological control of native Lygus species in North America: use of field host surveys to predict natural enemy habitat and host ranges. pp. 8495 in van Driesche, R., Heard, T., McClay, A., Reardon, R. (Eds) Proceedings of Session: Host Specificity Testing of Exotic Arthropod Biological Control Agents – The Biological Basis for Improvement in Safety. Morgantown, West Virginia, USDA Forest Service.Google Scholar
Kuhlmann, U., Schaffner, U. & Mason, P.G. (2005) Selection of non-target species for host specificity testing of entomophagous biological control agents. pp. 566583 in Hoddle M.S. (compiler) Proceedings of the 2nd International Symposium on Biological Control of ArthropodsDavos, Switzerland12–16 September 2005WV, FHTET-2005–08. Morgantown, United States Department of Agriculture, Forest Service.Google Scholar
Lachance, S. (2000) Classical biological control of the tarnished plant bug, Lygus lineolaris, in Ontario, using imported braconid wasps, Peristenus spp. PhD thesis, University of Guelph, Canada.Google Scholar
Loan, C.C. (1980) Plant bug hosts (Heteroptera: Miridae) of some Euphorine parasites (Hymenoptera: Braconidae) near Belleville, Ontario, Canada. Naturaliste Canadien 107, 8793.Google Scholar
Loan, C.C., Bilewicz-Pawinska, T. (1973) Systematics and biology of four Polish species of Peristenus Foerster (Hymenoptera: Braconidae, Euphorinae). Environmental Entomology 2, 271278.CrossRefGoogle Scholar
Louda, S.M., Pemberton, R.W., Johnson, M.T., Follett, P.A. (2003a) Nontarget effects – the Achilles' heel of biological control? Retrospective analyses to reduce risk associated with biocontrol introductions. Annual Review of Entomology 48, 365396.CrossRefGoogle ScholarPubMed
Louda, S.M., Arnett, R.W., Rand, T.A., Russell, F.L. (2003b) Invasiveness of some biological control insects and adequacy of their ecological risk assessment and regulation. Conservation Biology 17, 7382.CrossRefGoogle Scholar
Maw, H.E.L., Foottit, R.G., Hamilton, K.G.A., Scudder, G.G.E. (2000) Checklist of the Hemiptera of Canada and Alaska Ottawa, National Research Council of Canada, NRC Research Press.Google Scholar
May, W.E., Soroka, J.J., Loeppky, H.A., Murrell, D.C. (2003) The effects of trichlorfon and deltamethrin on alfalfa plant bug and Lygus bug (Heteroptera: Miridae) populations in alfalfa grown in Canada. Crop Protection 22, 883889.CrossRefGoogle Scholar
McMahon, H., Arnason, A.P. (1947) Control of Lygus bugs in alfalfa seed fields in Saskatchewan. Division of Entomology Processed Publication 67, 13.Google Scholar
Messing, R.H. (2001) Centrifugal phylogeny as a basis for non-target host testing in biological control: is it relevant for parasitoids. Phytoparasitica 29, 187190.CrossRefGoogle Scholar
Nechols, J.R., Kauffman, W.C., Schaefer, P.W. (1992) Significance of host specificity in classical biological control. pp. 4152 in Kauffman, W.C., Nechols, J.R. (Eds) Selection criteria and ecological consequences of importing natural enemies. Lanham, Maryland, Entomological Society of America.Google Scholar
Obrycki, J.J., Elliott, N.C. & Glies, K.L. (2000) Coccinellid introductions: potential for and evaluation of non-target effects. pp. 127145 in Follett, P.A. & Duan, J.J. (Eds) Nontarget effects of biological control. Dordrecht, Kluwer.CrossRefGoogle Scholar
Onstad, D.W., McManus, M.L. (1996) Risks of host range expansion by parasites of insects. Bioscience 46, 430435.CrossRefGoogle Scholar
Pickett, C.H., Coutinout, D., Hoelmer, K.A. & Kuhlmann, U. (2005) Establishment of Peristenus spp. in Northern California for the control of Lygus spp. pp. 116125 in Hoddle, M.S. Proceedings of the 2nd International Symposium on Biological Control of Arthropods, Davos, Switzerland, 12–16 September 2005, WV, FHTET-2005–08. Morgantown, United States Department of Agriculture, Forest Service.Google Scholar
Porter, B.J. (1979) Host selection in Peristenus stygicus Loan (Hymenoptera: Braconidae); an approach to the evaluation of host range for parasitoids. MSc thesis, A and M University, Texas.Google Scholar
Sands, D.P.A. (1993) Effects of confinement on parasitoid/host interactions: interpretation and assessment for biological control of arthropod pests. pp. 196199 in Corey, S.A., Dall, D.J., Milne, W.M. (Eds) Pest control and sustainable agriculture. Canberra, CSIRO, Division of Entomology.Google Scholar
Sands, D.P.A., van Driesche, R.G. (2003) Host range testing techniques for parasitoids and predators. pp. 4153Van Driesche, R.G.Proceedings of the 1st International Symposium on Biological Control of Arthropods, Honolulu, Hawaii, 14–18 January 2002, FHTET-2033–05. Morgantown, West Virginia United States Department of Agriculture, Forest Service.Google Scholar
Sands, D.P.A., van Driesche, R.G. (2004) Using the scientific literature to estimate the host range of a biological control agent. pp. 1523 in van Driesche, R.G., Reardon, R. (Eds) Assessing host ranges for parasitoids and predators used for classical biological control: a guide to best practice. Morgantown, West Virginia USDA, Forest Health Technology Enterprise Team.Google Scholar
Schwartz, M.D., Foottit, R.G. (1998) Revision of the Nearctic species of the genus Lygus Hahn, with a review of the Palaearctic species (Heteroptera: Miridae) Gainesville, Florida Associated PublishersGoogle Scholar
Shahjahan, M. (1974) Erigeron flowers as a food and attractive odor source for Peristenus pseudopallipes, a braconid parasitoid of the tarnished plant bug. Environmental Entomology 3, 6972.CrossRefGoogle Scholar
Shaw, M.R. (1994) Parasitoid host ranges. pp. 111144 in Hawkins, B.A., Sheehan, W. (Eds) Parasitoid community ecology. Oxford, Oxford University Press.CrossRefGoogle Scholar
Shrimpton, G. (1985) Four insect pests of conifer nurseries in British Columbia. pp. 119121 Western Forest Nursery Council – Intermountain Nurseryman's Association, USDA Forest Service, General Technical Report INT–185.Google Scholar
Snodgrass, G.L., McWilliams, J.M. (1992) Rearing the tarnished plant bug (Heteroptera: Miridae) using a tissue paper oviposition site. Journal of Economic Entomology 85, 11621166.CrossRefGoogle Scholar
Soroka, J.J. (1997) Plant bugs in lucerne. pp. 46 in Soroka, J.J.Proceedings of the Lygus working Group Meeting, 11–12. April 1996, Winnipeg, Manitoba. Saskatoon, Saskatchewan Agriculture and Agri-Food Canada, Research Branch.Google Scholar
SPSS Inc. (1999) SPSS® Base 10.0 user's guide Chicago IllinoisGoogle Scholar
Stevenson, A.B., Roberts, M.D. (1973) Tarnished plant bug rearing on lettuce. Journal of Economic Entomology 66, 13541355.CrossRefGoogle Scholar
Stiling, P. (2004) Biological control not on target. Biological Invasions 6, 151159.CrossRefGoogle Scholar
Timlick, B.H., Turnock, W.J. & Wise, I. (1993) Distribution and abundance of Lygus spp. (Heteroptera: Miridae) on alfalfa and canola in Manitoba. Canadian Entomologist 125, 10331041.CrossRefGoogle Scholar
van Driesche, R.G., Murray, T.J. (2004) Overview of testing schemes and designs used to estimate host ranges. pp. 5667van Driesche, R.G., Reardon, R. (Eds) Assessing host ranges for parasitoids and predators used for classical biological control: a guide to best practice. Morgantown, West Virginia USDA, Forest Health Technology Enterprise Team.Google Scholar
van Driesche, R.G. & Reardon, R. (2004) Assessing host ranges for parasitoids and predators used for classical biological control: a guide to best practice Morgantown, West Virginia USDA, Forest Health Technology Enterprise TeamGoogle Scholar
van Lenteren, J.C., Babendreier, D., Bigler, F., Burgio, G., Hokkanen, H.M.T., Kuske, S., Loomans, A.J.M., Menzler-Hokkanen, H.M.T., van Rijn, P.C.J., Thomas, M.B., Tommasini, M.G., Zeng, Q.-Q. (2003) Environmental risk assessment of exotic natural enemies used in inundative biological control. BioControl 48, 338.CrossRefGoogle Scholar
Varis, A.-L., van Achterberg, C. (2001) Peristenus varisae spec. nov. (Hymenoptera: Braconidae) parasitizing the European tarnished plant bug, Lygus rugulipennis Poppius (Heteroptera: Miridae). Zoologische Mededelingen Leiden 75, 371379.Google Scholar
Withers, T.M., Browne, L.B. (2004) Behavioral and physiological processes affecting outcomes of host range testing. pp. 4055 in van Driesche, R.G., Reardon, R. (Eds) Assessing host ranges for parasitoids and predators used for classical biological control: a guide to best practice. USDA, Forest Health Technology Enterprise Team, Morgantown, West Virginia.Google Scholar