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Courtship sequence and evidence of volatile pheromones in Phasgonophora sulcata (Hymenoptera: Chalcididae), a North American parasitoid of the invasive Agrilus planipennis (Coleoptera: Buprestidae)

Published online by Cambridge University Press:  02 September 2015

Lucas E. Roscoe*
Forest Protection Limited, c/o Natural Resources Canada, Atlantic Forestry Centre, P.O. Box 4000, 1350 Regent Street, Fredericton, New Brunswick, Canada E3B 5P7
D. Barry Lyons
Natural Resources Canada, Canadian Forest Service, Great Lakes Forestry Centre, 1219 Queen Street East, Sault Ste. Marie, Ontario, Canada P6A 2E5
Krista L. Ryall
Natural Resources Canada, Canadian Forest Service, Great Lakes Forestry Centre, 1219 Queen Street East, Sault Ste. Marie, Ontario, Canada P6A 2E5
Sandy M. Smith
Faculty of Forestry, University of Toronto, 33 Willcocks Street, Toronto, Ontario, Canada M5S 3B3
1Corresponding author (e-mail:


Phasgonophora sulcata Westwood (Hymenoptera: Chalcididae) is a North American parasitoid now using Agrilus planipennis Fairmaire (Coleoptera: Buprestidae) as a novel host, and may prove useful in biocontrol. Unfortunately, information is lacking regarding mating and the presence of pheromones, which may be important when attempting to exploit this parasitoid within a management context. Herein we used olfactometer assays and behavioural observations to determine the courtship and mating sequences of P. sulcata. A significantly higher proportion of males oriented towards females over the control arm containing filtered air in an olfactometer regardless of the age classes of females or males examined. We also observed four pre-copulatory behaviours that were consistent in all mating pairs. Our results indicate that courtship may be mediated by male perception of female-produced pheromones. Understanding the courtship sequence may be useful in rearing laboratory populations, while the putative pheromones may be useful in detection and retention of P. sulcata populations.

Behaviour & Ecology
© Entomological Society of Canada 2015 

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Subject editor: Deepa Pureswaran


Abdurahiman, U., Mohamed, U., and Remadevi, O. 1983. Studies on the biology of Antrocephalus hakonensis (Hymenoptera: Chalcididae) a pupal parasitoid of Opisina arenosella the coconut caterpillar. Cocos, 1: 1116.Google Scholar
Abell, K.J., Bauer, L.S., Duan, J.J., and Van Driesche, R. 2014. Long-term monitoring of the introduced emerald ash borer (Coleoptera: Buprestidae) egg parasitoid, Oobius agrili (Hymenoptera: Encyrtidae), in Michigan, USA and evaluation of a newly developed monitoring technique. Biological Control, 79: 3642.Google Scholar
Alcock, J. 1994. Body size and its effect on male-male competition in Hylaeus alcyoneus (Hymenoptera: Colletidae). Journal of Insect Behavior, 8: 149159.Google Scholar
Barras, R. 1960. The courtship behaviour of Mormoniella vitripennis Walk. (Hymenoptera, Pteromalidae). Behaviour, 15: 185209.Google Scholar
Bauer, L.S., Liu, H., Miller, D., and Gould, J. 2008. Developing a classical biological control program for Agrilus planipennis (Coleoptera: Buprestidae), an invasive ash pest in North America. Newsletter of the Michigan Entomological Society, 53: 3839.Google Scholar
Benelli, G., Bonsignori, G., Stefanini, C., and Canale, A. 2012. Courtship and mating behaviour in the fruit fly parasitoid Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae): the role of wing fanning. Journal of Pest Science, 85: 5563.Google Scholar
Bin, F., Wäckers, F., Romani, R., and Isidoro, N. 1999. Tyloids in Pimpla turionellae (L.) are release structures of male antennal glands involved in courtship behaviour (Hymenoptera: Ichneumonidae). International Journal of Insect Morphology and Embryology, 28: 6168.CrossRefGoogle Scholar
Bouček, Z.K. 1988. Australasian Chalcidoidea (Hymenoptera). A biosystematic revision of genera of fourteen families, with a reclassification of species. CABI, Wallingford, United Kingdom.Google Scholar
Bouček, Z.K. 1992. The new world genera of Chalcididae. Memoirs of the American Entomological Institute, 53: 49118.Google Scholar
Canale, A., Benelli, G., and Lucchi, A. 2013. Female‐borne cues affecting Psyttalia concolor (Hymenoptera: Braconidae) male behavior during courtship and mating. Insect Science, 20: 379384.Google Scholar
Cappaert, D. and McCullough, D.G. 2009. Occurrence and seasonal abundance of Atanycolus cappaerti (Hymenoptera: Braconidae) a native parasitoid of emerald ash borer, Agrilus planipennis (Coleoptera: Buprestidae). Great Lakes Entomologist, 42: 1629.Google Scholar
Cappaert, D., McCullough, D.G., Poland, T.M., and Siegert, N.W. 2005. Emerald ash borer in North America: a research and regulatory challenge. American Entomologist, 51: 152165.Google Scholar
Collatz, J., Tolasch, T., and Steidle, J.L. 2009. Mate finding in the parasitic wasp Cephalonomia tarsalis (Ashmead): more than one way to a female’s heart. Journal of Chemical Ecology, 35: 761768.Google Scholar
Cossé, A.A., Petroski, R.J., Zilkowski, B.W., Vermillion, K., Lelito, J.P., Cooperband, M.F., et al. 2012. Male-produced pheromone of Spathius agrili, a parasitoid introduced for the biological control of the invasive emerald ash borer, Agrilus planipennis . Journal of Chemical Ecology, 38: 389399.CrossRefGoogle ScholarPubMed
Danci, A., Gries, R., Schaefer, P.W., and Gries, G. 2006. Evidence for four-component close-range sex pheromone in the parasitic wasp Glyptapanteles flavicoxis . Journal of Chemical Ecology, 32: 15391554.Google Scholar
Duan, J.J., Bauer, L.S., Abell, K.J., Lelito, J.P., and Driesche, R.V. 2013. Establishment and abundance of Tetrastichus planipennisi (Hymenoptera: Eulophidae) in Michigan: potential for success in classical biocontrol of the invasive emerald ash borer (Coleoptera: Buprestidae). Journal of Economic Entomology, 106: 11451154.Google Scholar
Duan, J.J., Ulyshen, M.D., Bauer, L.S., Gould, J., and Driesche, R.V. 2010. Measuring the impact of biotic factors on populations of immature emerald ash borers (Coleoptera: Buprestidae). Environmental Entomology, 39: 15131522.CrossRefGoogle ScholarPubMed
Eller, F., Bartelt, R., Jones, R., and Kulman, H. 1984. Ethyl (Z)-9-hexadecenoate a sex pheromone of Syndipnus rubiginosus, a sawfly parasitoid. Journal of Chemical Ecology, 10: 291300.Google Scholar
Fauvergue, X., Hopper, K.R., and Antolin, M.F. 1995. Mate finding via a trail sex pheromone by a parasitoid wasp. Proceedings of the National Academy of Sciences, 92: 900904.Google Scholar
Field, S.A. and Keller, M.A. 1993. Courtship and intersexual signaling in the parasitic wasp Cotesia rubecula (Hymenoptera: Braconidae). Journal of Insect Behavior, 6: 737750.CrossRefGoogle Scholar
Gandhi, K.J.K. and Herms, D.A. 2010. North American arthropods at risk due to widespread Fraxinus mortality caused by the alien emerald ash borer. Biological Invasions, 12: 18391846.Google Scholar
Gandhi, K.J.K., Smith, A., Hartzler, D.M., and Herms, D.A. 2014. Indirect effects of emerald ash borer-induced ash mortality and canopy gap formation on epigaeic beetles. Environmental Entomology, 43: 546555.Google Scholar
González, J.M. and Matthews, R.W. 2005. Courtship of the two female morphs of Melittobia digitata (Hymenoptera: Eulophidae). Florida Entomologist, 88: 258267.CrossRefGoogle Scholar
Haack, R.A. and Benjamin, D.M. 1982. The biology and ecology of the twolined chestnut borer, Agrilus bilineatus (Coleoptera: Buprestidae), on oaks, Quercus spp., in Wisconsin. The Canadian Entomologist, 114: 385396.Google Scholar
Haack, R., Benjamin, D., and Schuh, B. 1981. Observations on the biology of Phasgonophora sulcata (Hymenoptera: Chalcididae), a larval parasitoid of the twolined chestnut borer, Agrilus bilineatus (Coleoptera: Buprestidae), in Wisconsin. Great Lakes Entomologist, 14: 113116.Google Scholar
Hansen, J.D. 1980. The life history and behavior of Spilochalcis albifrons (Hymenoptera: Chalcididae), a parasite of the larch casebearer, Coleophora laricella (Lepidoptera: Coleophoridae). Journal of the Kansas Entomological Society, 53: 553566.Google Scholar
Herms, D.A. and McCullough, D.G. 2014. Emerald ash borer invasion of North America: history, biology, ecology, impacts, and management. Annual Review of Entomology, 59: 1330.Google Scholar
Isidoro, N. and Bin, F. 1995. Male antennal gland of Amitus spiniferus (Brethes) (Hymenoptera: Platygastridae), likely involved in courtship behavior. International Journal of Insect Morphology and Embryology, 24: 365373.CrossRefGoogle Scholar
Isidoro, N., Bin, F., Colazza, S., and Vinson, S. 1996. Morphology of antennal gustatory sensilla and glands in some parasitoid Hymenoptera with hypothesis on their role in sex and host recognition. Journal of Hymenoptera Research, 5: 206239.Google Scholar
Jewett, D.K. and Carpenter, J.E. 2001. Seasonal abundance of a pupal parasitoid Diapetimorpha introita (Hymenoptera: Ichneumonidae). Florida Entomologist, 84: 5054.Google Scholar
Kainoh, Y. 1986. Mating behavior of Ascogaster reticulatus Watanabe (Hymenoptera: Braconidae), an egg-larval parasitoid of the smaller tea tortrix moth, Adoxophyes sp. (Lepidoptera: Tortricidae) I. Diel patterns of emergence and mating, and some conditions for mating. Japanese Society of Applied Entomology and Zoology, 21: 17.Google Scholar
Kainoh, Y. 1999. Parasitoids. In Pheromones of non-lepidopteran insects associated with agricultural plants. Edited by J. Hardie and A.K. Minks. CABI, Wallingford, United Kingdom. Pp. 383404.Google Scholar
Kainoh, Y. and Oishi, Y. 1993. Source of sex pheromone of the egg-larval parasitoid, Ascogaster reticulatus Watanabe (Hymenoptera: Braconidae). Journal of Chemical Ecology, 19: 963969.Google Scholar
Kovacs, K.F., Haight, R.G., McCullough, D.G., Mercader, R.J., Siegert, N.W., and Liebhold, A.M. 2010. Cost of potential emerald ash borer damage in US communities, 2009–2019. Ecological Economics, 69: 569578.CrossRefGoogle Scholar
Leonard, S.H. and Ringo, J.M. 1978. Analysis of male courtship patterns and mating behavior of Brachymeria intermedia . Annals of the Entomological Society of America, 71: 817826.CrossRefGoogle Scholar
Lewis, W.J., Snow, W.J., and Jones, R.L. 1971. A pheromone trap for studying populations of Cardiochiles nigriceps, a parasite of Heliothis virescens . Journal of Economic Entomology, 64: 14171421.CrossRefGoogle Scholar
Liu, H., Bauer, L.S., Gao, R., Zhao, T., Petrice, T.R., and Haack, R.A. 2003. Exploratory survey for the emerald ash borer, Agrilus planipennis (Coleoptera: Buprestidae), and its natural enemies in China. Great Lakes Entomologist, 36: 191204.Google Scholar
Loerch, C.R. and Cameron, E. 1983. Natural enemies of immature stages of the bronze birch borer, Agrilus anxius (Coleoptera: Buprestidae), in Pennsylvania. Environmental Entomology, 12: 17981801.Google Scholar
Loerch, C.R. and Cameron, E.A. 1984. Within-tree distributions and seasonality of immature stages of the bronze birch borer, Agrilus anxius (Coleoptera: Buprestidae). The Canadian Entomologist, 116: 147152.Google Scholar
Lyons, D.B. 2010. Biological control of emerald ash borer. In Workshop proceedings: guiding principles for managing the emerald ash borer in urban environments. Edited by D.B. Lyons and T.A. Scarr. Ontario Ministry of Natural Resources and Natural Resources Canada, Canadian Forest Service, Sault Ste, Marie, Ontario, Canada. Pp. 2934.Google Scholar
Matthews, R.W., Yukawa, J., and Gonzalez, J.M. 1985. Sex pheromones in male Melittobia parasitic wasps: female response to conspecific and congeneric males of 3 species. Journal of Ethology, 3: 5962.CrossRefGoogle Scholar
McClure, M., Whistlecraft, J., and McNeil, J.N. 2007. Courtship behavior in relation to the female sex pheromone in the parasitoid, Aphidius ervi (Hymenoptera: Braconidae). Journal of Chemical Ecology, 33: 19461959.Google Scholar
McCullough, D.G. and Mercader, R.J. 2012. Evaluation of potential strategies to SLow Ash Mortality (SLAM) caused by emerald ash borer (Agrilus planipennis): SLAM in an urban forest. International Journal of Pest Management, 58: 923.Google Scholar
McKenney, D.W., Pedlar, J.H., Yemshanov, D., Lyons, D.B., Campbell, K.L., and Lawrence, K. 2012. Estimates of the potential cost of emerald ash borer (Agrilus planipennis Fairmaire) in Canadian municipalities. Arboriculture and Urban Forestry, 38: 8191.Google Scholar
McNeil, J.N. and Brodeur, J. 1995. Pheromone-mediated mating in the aphid parasitoid, Aphidius nigripes (Hymenoptera: Aphididae). Journal of Chemical Ecology, 21: 959972.Google Scholar
Nichols, W.J., Cossé, A.A., Bartelt, R.J., and King, B.H. 2010. Methyl 6-methylsalicylate: a female-produced pheromone component of the parasitoid wasp Spalangia endius . Journal of Chemical Ecology, 36: 11401147.Google Scholar
Onagbola, E.O. and Fadamiro, H.Y. 2011. Electroantennogram and behavioral responses of Pteromalus cerealellae to odor stimuli associated with its host, Callosobruchus maculatus . Journal of Stored Products Research, 47: 123129.Google Scholar
Poland, T.M. and McCullough, D.G. 2006. Emerald ash borer: invasion of the urban forest and the threat to North America’s ash resource. Journal of Forestry, 104: 118124.Google Scholar
Quicke, D.L. 1997. Parasitic wasps. Chapman & Hall Ltd, London, United Kingdom.Google Scholar
Ramadan, M.M., Wong, T.T., and Wong, M.A. 1991. Influence of parasitoid size and age on male mating success of Opiinae (Hymenoptera: Braconidae), larval parasitoids of fruit flies (Diptera: Tephritidae). Biological Control, 1: 248255.Google Scholar
Roscoe, L.E. 2014. Phasgonophora sulcata Westwood (Hymenoptera: Chalcididae): a potential augmentative biological control agent for the invasive Agrilus planipennis Fairmaire (Coleoptera: Buprestidae) in Canada. Ph.D. thesis. University of Toronto, Toronto, Ontario, Canada.Google Scholar
Ruther, J., Homann, M., and Steidle, J.L. 2000. Female derived sex pheromone mediates courtship behaviour in the parasitoid Lariophagus distinguendus . Entomologia Experimentalis et Applicata, 96: 265274.CrossRefGoogle Scholar
Schwörer, U., Völkl, W., and Hoffmann, K.H. 1999. Foraging for mates in the hyperparasitic wasp, Dendrocerus carpenteri: impact of unfavourable weather conditions and parasitoid age. Oecologia, 119: 7380.Google Scholar
Shu, S. and Jones, R.L. 1993. Evidence for a multicomponent sex pheromone Eriborus terebrans (Gravenhorst) (HYM.: Ichneumonidae), a larval parasitoid of the European corn borer. Journal of Chemical Ecology, 19: 25632576.Google Scholar
Siegert, N.W., McCullough, D.G., Liebhold, A.M., and Telewski, F.W. 2014. Dendrochronological reconstruction of the epicentre and early spread of emerald ash borer in North America. Diversity and Distributions, 20: 847858.CrossRefGoogle Scholar
Stiling, P. 1993. Why do natural enemies fail in classical biological control programs? American Entomologist, 39: 3137.Google Scholar
Sullivan, B.T. 2002. Evidence for a sex pheromone in bark beetle parasitoid Roptrocerus xylophagorum . Journal of Chemical Ecology, 28: 10451063.CrossRefGoogle ScholarPubMed
Tagawa, J., Asano, M., Ohtsubo, T., Kamomae, M., and Gotoh, T. 1985. Influence of age on the mating behaviour of the braconid wasp, Apanteles glomeratus L. Japanese Society of Applied Entomology and Zoology, 20: 227230.Google Scholar
United States Department of Agriculture-Animal and Plant Health Inspection Service. 2014. Questions and answers: USDA’s emerald ash borer biocontrol program. Available from [accessed 22 October 2014].Google Scholar
van den Assem, J. 1986. Mating behavior in parasitic wasps. In Insect parasitoids: 13th symposium of the Royal Entomological Society of London, 18–19 September 1985. Edited by J. Waage and D. Greathead. Academic Press, London, United Kingdom. Pp. 137167.Google Scholar
van den Assem, J. and Vernel, C. 1979. Courtship behaviour of Nasonia vitripennis (Hym.: Pteromalidae): observations and experiments on male readiness to assume copulatory behaviour. Behaviour, 68: 118135.Google Scholar
van den Assem, J. and Werren, J. 1994. A comparison of the courtship and mating behavior of three species of Nasonia (Hymenoptera: Pteromalidae). Journal of Insect Behavior, 7: 5366.Google Scholar
Vinson, S.B. 1972. Courtship behavior and evidence for a sex pheromone in the parasitoid Campoletis sonorensis (Hymenoptera: Ichneumonidae). Environmental Entomology, 1: 409414.Google Scholar
Völkl, W., Hübner, G., and Dettner, K. 1994. Interactions between Alloxysta brevis (Hymenoptera, Cynipoidea, Alloxystidae) and honeydew-collecting ants: how an aphid hyperparasitoid overcomes ant aggression by chemical defense. Journal of Chemical Ecology, 20: 29012915.Google Scholar
Wigglesworth, V.B. 1950. The principles of insect physiology. Chapman and Hall, London, United Kingdom.Google Scholar
Yang, Z.-Q., Strazanac, J.S., Marsh, P.M., Van Achterberg, C., and Choi, W.Y. 2005. First recorded parasitoid from China of Agrilus plainpennis: a new species of Spathius (Hymenoptera: Braconidae, Doryctinae). Annals of the Entomological Society of America, 98: 636642.Google Scholar