Abstract
Plant bugs belonging to the genus Lygus Hahn (Hemiptera: Miridae) are important pests of a wide variety of North American crops. Efforts to use biological control as one strategy in an integrated pest management approach have been impeded by a poor understanding of the endoparasitoids, particularly species of the genera Leiophron Nees and Peristenus Foerster (Hymenoptera: Braconidae) many of which parasitize the nymphal stages of Lygus, among other Miridae. The taxonomy of Leiophron and Peristenus species associated with agricultural habitats is reviewed based on reared material contributed by numerous researchers. Sixteen species of the two genera were found parasitizing Lygus nymphs, including the following eight species described as new, Leiophron australis Goulet, L. simoni Goulet, Peristenus braunae Goulet, P. broadbenti Goulet, P. carcamoi Goulet, P. dayi Goulet, P. gillespiei Goulet and P. otaniae Goulet. The species are differentiated in a key, described and illustrated. Two names are newly placed in synonymy, L. trigonotylidis Loan, 1974 under Leiophron lygivorus (Loan 1970) and Brachistes nocturnus Viereck, 1905 under P. mellipes (Cresson 1872). Euphorus mellipes Cresson is removed from synonymy with P. pallipes (Curtis). Most of the endoparasitoid species are known to be associated only with Lygus spp. and appear to be distinct in their distribution and their biology. Analysis of the endoparasitoid complex in southern Quebec shows that of the six species that occur in alfalfa and hay fields, four species use Lygus lineolaris (Palisot) as the main host. The introduced Peristenus digoneutis Loan has recently established in southern Quebec and although its numbers have increased substantially it has not yet had an evident impact on reducing L. lineolaris population levels.
References
Allen, R.T. & Ball G.E. (1979) Synopsis of Mexican taxa of the Loxandrus series (Coleoptera: Carabidae: Pterostichini). Transactions of the American Entomological Society, 105(4), 481-575.
Ashfaq, M., Braun, L., Hegedus, D. & Erlandson, M. (2004) Estimating parasitism levels in Lygus spp. (Hemiptera: Miridae) field populations using standard and molecular techniques. Biocontrol Science and Technology, 14, 731–735.
Ball, J., Pickett, C.H., Kuhlmann, U., Coutinot, D., Hoelmer, K. & Ertle, L. (2000) Production of two plant bug parasitoids from Europe, Peristenus digoneutis and P. stygicus, and field release in California in 1999. In: Woods, D.M. (Ed.) Biological Control Program Annual Summary, 1999. California Department of Food and Agriculture, Plant Health and Pest Prevention Services, Sacramento, California, U.S.A., pp. 7–8.
Bilewciz-Pawinska, T. (1974) Larvae of Peristenus Foerster (Hym., Braconidae) parasitic on Lygus rugulipennis Popp. (Heteroptera: Miridae). [in Polish]. Polskie Pismo Entomologiczne, 44, 759–764.
Braun, L., Erlandson, M., Baldwin, D., Soroka, J., Mason, P.G., Foottit, R. & Hegedus, D. (2001) Seasonal occurrence, species composition, and parasitism of Lygus spp. in alfalfa, canola, and mustard. The Canadian Entomologist, 133, 565–577.
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, 109–111.
Carigan, S., Boivin, G. & Stewart, R.K. (1995) Developmental biology and morphology of Peristenus digoneutis Loan (Hymenoptera: Braconidae: Euphorinae). Biological Control, 5, 553–560.
Cresson, E.T. (1872) Descriptions of North American Hymenoptera, No. 4. The Canadian Entomologist, 4, 226–235.
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). Biological Control, 25, 512–518.
Day, W.H. (1999) Host preferences of introduced and native parasites (Hymenoptera: Braconidae) of phytophagous plant bugs (Hemiptera: Miridae) in alfalfa-grass fields in the northeastern USA. BioControl, 44, 249–261.
Day, W.H., Baird, C.R. & Shaw, S.R. (1999) New, native species of Peristenus (Hymenoptera: Braconidae) parasitizing Lygus hesperus (Hemiptera: Miridae) in Idaho: biology, importance, and description. Annals of the Entomological Society of America, 92, 370–375.
Day, W.H., Eaton, A.T., Romig, R.F., Tilmon, K.J., Mayer, M. & Dorsey, T. (2003) Peristenus digoneutis (Hymenoptera: Braconidae), a parasite of Lygus lineolaris (Hemiptera: Miridae) in Northeastern United States alfalfa, and the need for research in other crops. Entomological News, 114, 105–111.
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, 1528–1533.
Day, W.D., Marsh, P.M., Fuester, R.W., Hoyer, H. & Dysart, R.J. (1992) Biology, initial effect, and description of a new species of Peristenus (Hymenoptera: Braconidae), a parasite of the alfalfa plant bug (Hemiptera: Miridae), recently established in the United Sates. Annals of the Entomological Society of America, 85, 482–488.
Day, W.H. & Saunders, LB. (1990) Abundance of the garden fleahopper (Hemiptera: Miridae) on alfalfa and parasitism by Leiophron uniformis (Gahan) (Hymenoptera: Braconidae). Journal of Economic Entomology, 83, 101–106.
Day, W.H., Tilmon, K.J., Romig, R.F., Eaton, A.T. & Murray, K.D. (2000) Recent range expansions of Peristenus digoneutis (Hymenoptera: Braconidae), a parasite of the tarnished plant bug (Hemiptera: Miridae), and high temperatures limiting its geographical distribution in North America. Journal of the New York Entomological Society, 180, 326–331.
Day, W.H., Tropp, J.M., Eaton, A.T., Romig, R.F., Van Driesche, R.G. & Chianese, R.J. (1998) Geographic distributions of Peristenus conradi and P. digoneutis (Hymenoptera: Braconidae), parasites of the alfalfa plant bug and the tarnished plant bug (Hemiptera: Miridae) in the northeastern United States. Journal of the New York Entomological Society, 106, 69–75.
Gahan, A.B. (1913) New Hymenoptera from North America. Proceedings of the United States National Museum, 46, 431–443.
Gariepy, T.D., Kuhlmann, U., Haye, T., Gillott, C. & Erlandson, M. (2005) A single-step multiplex PCR assay for the detection of European Peristenus spp., parasitoids of Lygus spp. Biocontrol Science and Technology, 15, 481–495.
Gibson, G.A.P. (1990) Revision of the genus Macroneura Walker in America north of Mexico (Hymenoptera: Eupelmidae). The Canadian Entomologist, 122, 837–873.
Goulet, H. (1986) The genera and species of the Nearctic Dolerini (Symphyta: Tenthredinidae: Selandriinae): classification and phylogeny. Memoirs of the Entomological Society of Canada, 135, 208 pp.
Huber, J.T. & Sharkey, M.J. (1993). Chapter 3 Structure. In: Goulet, H. & Huber, J.T. (Eds.) Hymenoptera of the world: an identification guide to families. Publication 1894/E, Research Branch, Agriculture Canada. Pp. 13-33.
Haye, T., Goulet, H., Mason, P.G. & Kuhlmann, U. (2005) Does fundamental host range match ecological host range? A retrospective case study of a Lygus plant bug parasitoid. Biological Control, 35, 55–67.
Haye, T., Kuhlmann, U., Goulet, H. & Mason, P.G. (2006) Controlling Lygus plant bugs with European Peristenus relictus (Hymenoptera: Braconidae) in Canada—Risky or Not? Bulletin of Entomological Research, 96, 187–196.
Hung, A.C.F., Day, W.H. & Hedlund, R.C. (1988) Genetic variability in arrhenotokous and thelytokous forms of Mesochorus nigripes (Hym: Ichneumonidae). Entomophaga, 33, 7–15.
Lachance, S., Broadbent, A.B. & Sears, M.K. (2001) In-host compatibility and in-host competition of exotic and native parasitoids of the tarnished plant bug (Heteroptera: Miridae). Environmental Entomology, 30, 1158–1163.
Lim, K.P. & Stewart, R.K. (1976) Parasitism of the tarnished plant bug, Lygus lineolaris (Hemiptera: Miridae), by Peristenus pallipes and P. pseudopallipes (Hymenoptera: Braconidae). The Canadian Entomologist, 108, 601–608.
Loan, C.C. (1965) Life cycle and development of Leiophron pallipes Curtis (Hymenoptera: Braconidae: Euphorinae) in five mirid hosts in the Belleville district. Proceedings of the Entomological Society of Ontario, 95, 115–121.
Loan, C.C. (1970) Two new parasites of the tarnished plant bug in Ontario: Leiophron pseudopallipes and Euphoriana lygivora (Hymenoptera: Braconidae, Euphorinae). Proceedings of the Entomological Society of Ontario, 100, 188–195.
Loan, C.C. (1974a) The North American species of Leiophron Nees, 1818 and Peristenus Foerster, 1862 (Hymenoptera: Braconidae, Euphorinae) including the description of 31 new species. Le Naturaliste Canadien, 101, 821–860.
Loan, C.C. (1974b) The European species of Leiophron Nees and Peristenus Foerster (Hymenoptera: Braconidae, Euphorinae). Transactions of the Royal Entomological Society of London, 126, 207–238.
Loan, C.C. (1980) Plant bug hosts (Heteroptera: Miridae) of some Euphorine parasites (Hymenoptera: Braconidae) near Belleville, Ontario, Canada. Le Naturaliste Canadien, 107, 87–93.
Loan, C. C. & Bilewicz-Pawinska, T. (1973) Systematic and biology of four Polish species of Peristenus Foerster (Hymenoptera: Braconidae, Euphorinae). Environmental Entomology, 2, 271–277.
Loan, C.C. & Craig, C.H. (1976) Euphorine parasitism of Lygus spp. in alfalfa in Western Canada (Hymenoptera: Braconidae; Heteroptera: Miridae). Le Naturaliste Canadien, 103, 497–500.
Loan, C.C. & Shaw, S.R. (1987) Euphorine parasites of Lygus and Adelphocoris (Hymenoptera: Braconidae and Heteroptera: Miridae). In: Hedlund, R. C. & Graham, H.M. (Eds.) Economic importance and biological control of Lygus and Adelphocoris in North America. U. S. Department of Agriculture, Agricultural Research Service, ARS–64, pp. 60–74.
Marsh, P.M. (1979) Family Braconidae. In: Krombien, K.V., Hurd, P.D., Smith, D.R. & Burks, B.D. (Eds.) Catalog of Hymenoptera in America North of Mexico. Volume I. Smithsonian Institution Press, Washington, D. C. pp. 144–294.
Mowry, T.M. & Barbour, J.D. (2004) Distinguishing the parasitic wasp, Peristenus howardi, from its congeners using polymerase chain reaction and restriction endonuclease digestion. Journal of Insect Science, 25, pp. 1–7.
Muesebeck, C.F.W. (1936) The genera of parasitic wasps of the braconid subfamily Euphorinae, with a review of the Nearctic species. Miscellaneous Publication United States Department of Agriculture, no 241. Washington, D.C. 36 pp.
Muesebeck, C.F.W & Walkley, L.M. (1951) Braconidae. In: Muesebeck, C.F.W., Krombien, K.V. and Townes, H.K. (Eds.) Hymenoptera of North America north of Mexico. Synoptic catalog. United States Government Printing Office, Washington, p. 103.
Pickett, C.H., Ball, J.C., Kuhlmann, U., Coutinot, D., Ertle, L., Tilmon, K. & Schmidth, L. (1998) Importation of Peristenus stygicus for the biological control of Lygus hesperus. In: Woods, D.M. (Ed.) Biological Control Program Annual Report 1997. California Department of Food and Agriculture, Plant Health and Pest Prevention Services, Sacramento, California, U.S.A., pp. 3–4.
Pickett, C.H., Ball, J.C., Mayhew, D.A., Casanave, K., Kuhlmann, U., Coutinot, D., Ertle, L. & Hoelmer, K.A. (2000) Importation and establishment of nymphal parasites of Lygus hesperus. In: Woods, D.M. (Ed.) Biological Control Program Annual Report 1999, California Department of Food and Agriculture, Plant Health and Pest Prevention Services, Sacramento, California, U.S.A., pp.9–10.
Pickett, C.H., Ball, J.C., Mayhew, D.A., Casanave, K., Kuhlmann, U., Coutinot, D., Ertle, L. & Hoelmer, K.A. (2001) Colonization of Lygus nymphal parasitoids in California. In: Woods, D.M. (Ed.) Biological Control Program Annual Summary, 2000. California Department of Food and Agriculture, Plant Health and Pest Prevention Services, Sacramento, California, U.S.A., pp. 9–10.
Pickett, C.H., Coutinot, D., Hoelmer, K.A., Goulet, H., Brown, J. & Lawson, M. (2005) Colonization of Lygus nymphal parasitoids in California. In: Woods, D.M. (Ed.) Biological Control Program Annual Summary, 2004. California Department of Food and Agriculture, Plant Health and Pest Prevention Services, Sacramento, California, U.S.A., pp. 19–20.
Pickett, C.H., Godfrey, K., Mayhew, D.A., Casanave, K., Rodriguez, R., Coutinot, D., Ertle, L. & Hoelmer, K.A. (2002). Importation and establishment of Lygus hesperus nymphal parasitoids. In: Woods, D.M. (Ed.) Biological Control Program Annual Report 2001. California Department
of Food and Agriculture, Plant Health and Pest Prevention Services, Sacramento, California, U.S.A., pp. 7–10.
Pickett, C.H., Godfrey, K., Mayhew, D.A., Casanave, K., Rodriguez, R., Coutinot, D., Ertle, L. & Hoelmer, K.A. (2003) Colonization of Lygus nymphal parasitoids in California. In: Woods, D.M. (Ed.) Biological Control Program Annual Summary, 2002. California Department of Food and Agriculture, Plant Health and Pest Prevention Services, Sacramento, California, U.S.A., pp. 7–10.
Richards, O.W. (1967) Some British species of Leiophron Nees (Hymenoptera: Braconidae, Euphorinae) with descriptions of two new species. Transactions of the Royal Entomological Society of London, 119, 171–186.
Ruthe, J.F. (1856) Prodomus einer Monographie der Gattung “Microctonus Wesmael”. Stettiner entomologische Zeitung, 17, 289–308.
Shenefelt, R.D. (1969). Braconidae 1. Hybrizoninae, Euphorinae, Cosmophorinae, Neoneurinae, Macrocentrinae. In: Ferrière, C. & van der Vetcht, J. (Eds.) Hymenopterorum Catalogus. Pars 4. Uitgeverij Dr. W. Junk N. V. ‚ Gravenhage, 176 pp.
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). Memoirs on Entomology, International, Volume 10. Associated Publishers, Gainesville, Florida, vii + 428 pp.
Shaw, S.R. (1997) Subfamily Euphorinae. In: Wharton, R. A., Marsh, P. M., Sharkey, M. J. (Eds.) Manual of the New World genera of the family Braconidae (Hymenoptera) The International Society of Hymenopterists, Washington, DC., pp. 232–254.
Tilmon, K.J., Danforth, B.N., Day, W.H. & Hoffman, M.P. (2000) Determining parasitoid species composition in a host population: A molecular approach. Annals of the Entomological Society of America, 93, 640–647.
Thomson, C.G. (1891) Bidrag till Braconidernes kannedom. Opuscula Entomologica, 16, 1659–1751.
Varis, A.-L. & van Achterberg, C. (2001) Peristenus varisae spec. nov. (Hymenoptera: Braconidae) parasitising the European tarnished plant bug. Lygus rugulipennis Poppius (Heteroptera: Miridae). Zoologisch mededeelingen, 75, 371–379.
Viereck, H.L. (1905) Notes and descriptions of Hymenoptera from the Western United States in the collection of the University of Kansas. Transactions of the Kansas Academy of Sciences, 19, 264–281.
Whistlecraft, J., Broadbent, B. & Lachance, S. (1999). Laboratory rearing of braconid parasitoids of Lygus lineolaris In: Foottit, R. & Mason, P. (Eds.). Proceedings of the Lygus Working Group Meeting, September 26, 1999, Saskatoon, Saskatchewan. Agriculture and Agri-Food Canada, Miscellaneous Publication, pp. 35–39.