Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-22T15:55:25.791Z Has data issue: false hasContentIssue false

Life history traits of Coccophagus gossypariae (Hymenoptera: Aphelinidae), a parasitoid of invasive Eriococcus spurius (Hemiptera: Eriococcidae) in field studies

Published online by Cambridge University Press:  28 February 2020

Caitlin Mader*
Affiliation:
Department of Renewable Resources, Faculty of Agriculture, Life & Environmental Sciences, 4-42 Earth Sciences Building, University of Alberta, Edmonton, Alberta, Canada, T6G 2E3
Jim Watts
Affiliation:
City of Calgary Urban Conservation Unit, Calgary, Alberta, Canada
Nadir Erbilgin
Affiliation:
Department of Renewable Resources, Faculty of Agriculture, Life & Environmental Sciences, 4-42 Earth Sciences Building, University of Alberta, Edmonton, Alberta, Canada, T6G 2E3
*
*Corresponding author. Email: [email protected]

Abstract

Eriococcus spurius (Modeer) (Hemiptera: Eriociccidae) is a pest of American elm (Ulmus americana Linnaeus; Ulmaceae) trees in western North America, but no effective biological control agent has been reported. This study took place in Calgary, Alberta, Canada, where urban American elms have been heavily and negatively impacted by E. spurius. Although the parasitoid Coccophagus gossypariae Gahan (Hymenoptera: Aphelinidae) was recovered from an E. spurius infested American elm in Calgary, little is known about its ecology. Prior to implementing biological control, the basic ecology of a candidate species must be understood. We documented the geographic establishment, sex ratios, and parasitism rate of C. gossyparaie on its host within the study area. Coccophagus gossypariae had established at 89% of study trees sampled and accounted for 98% of the parasitoids caught. They had a female-biased sex ratio of 13.7 females per male, and both males and females developed to maturity using the host. We found evidence of a highly consistent aversion to superparasitism by females in the field. This first investigation established a baseline of information on field populations of C. gossypariae that could lead to biological control of E. spurius.

Type
Research Papers
Copyright
© 2020 Entomological Society of Canada

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Subject editor: Roselyne Labbé

References

Bai, B. and Mackauer, M. 1990. Host discrimination by the aphid parasitoid Aphelinus asychis (Hymenoptera: Aphelinidae): when superparasitism is not adaptive. The Canadian Entomologist, 122: 363372.CrossRefGoogle Scholar
Batsankalashvili, M., Kaydan, M.B., Kirkitadze, G., and Japoshvili, G. 2017. Updated checklist of scale insects (Hemiptera: Coccoporpha) in Sakartvelo (Georgia). Annals of Agrarian Science, 15: 252268.CrossRefGoogle Scholar
Bey, C.F. 1990. Ulmus americana L. American elm. In Silvics of North America volume 2: hardwoods. Edited by Burns, R. and Honkala, B.. Agriculture Handbook 654. United States Department of Agriculture, Washington, District of Columbia, United States of America. Pp. 801807.Google Scholar
Blumberg, D. and Luck, R.F. 1990. Differences in the rates of superparasitism between two strains of Comperiella bifasciata (Howard) (Hymenoptera: Encyrtidae) parasitizing California red scale (Homoptera: Diaspididae): an adaptation to circumvent encapsulation? Annals of the Entomological Society of America, 83: 591597.CrossRefGoogle Scholar
Briggs, C.J., Nisbet, R.M., Murdoch, W.W., Collier, T.R., and Metz, J.A.J. 1995. Dynamical effects of host-feeding in parasitoids. Journal of Animal Ecology, 64: 403416.CrossRefGoogle Scholar
Bürgi, L.P. and Mills, N.J. 2013. Developmental strategy and life history traits of Meteorus ictericus, a successful resident parasitoid of the exotic light brown apple moth in California. Biological Control, 66: 173182. https://doi.org/10.1016/j.biocontrol.2013.05.006.CrossRefGoogle Scholar
Byrne, F.J. and Toscano, N.C. 2007. Lethal toxicity of systemic residues of imidacloprid against Homalodisca vitripennis (Homoptera: Cicadellidae) eggs and its parasitoid Gonatocerus ashmeadi (Hymenoptera: Mymaridae). Biological Control, 43: 130135. https://doi.org/10.1016/j.biocontrol.2007.05.007.CrossRefGoogle Scholar
Castelo, M.K., Corley, J.C., and Desouhant, E. 2003. Conspecific avoidance during foraging in Venturia canescens (Hymenoptera: Ichneumonidae): the roles of host presence and conspecific densities. Journal of Insect Behavior, 16: 307318.CrossRefGoogle Scholar
Chen, T.H., Li, M., Wang, J.H., Zhang, F., and Li, Y.X. 2013. Vulnerability window for laying male eggs and superparasitism in producing female offspring of Encarsia sophia on Bemisia tabaci B biotype. BioControl, 58: 2736. https://doi.org/10.1007/s10526-012-9469-8.CrossRefGoogle Scholar
Cohen, H., Horowitz, A. R., Nestel, D., and Rosen, D. 1996. Susceptibility of the woolly apple aphid parasitoid, Aphelinus mali (Hym.: Aphelinidae), to common pesticides used in apple orchards in Israel. Entomophaga, 41: 225233. https://doi.org/10.1007/BF02764248.CrossRefGoogle Scholar
Cowles, R.S. and Lagalante, A.F. 2009. Activity and persistence of systemic insecticides for managing hemlock woolly adelgids. In Proceedings, 20th US Department of Agriculture interagency research forum on invasive species 2009, Edited by McManus, K.A. and Gottschalk, K.W.. Northern Research Station, Forest Service, United States Department of Agriculture, Annapolis, Maryland, United States of America. Pp 1718Google Scholar
Dreistadt, S.H. and Hagen, K.S. 1994. European elm scale (Homoptera: Eriococcidae) abundance and parasitism in northern California. Pan-Pacific Entomologist, 70: 240252.Google Scholar
Duan, J.J., Bauer, L.S., van Driesche, R.G., and Gould, J.R. 2018. Progress and challenges of protecting North American ash trees from emerald ash borer using biological control. Forests, 9: article 142, 117. https://doi.org/10.3390/f9030142.CrossRefGoogle Scholar
Eliopoulos, P.A., Kapranas, A., Givropoulou, E.G., and Hardy, I.C. 2017. Reproductive efficiency of the bethylid wasp Cephalonomia tarsalis: the influences of spatial structure and host density. Bulletin of Entomological Research, 107: 19.CrossRefGoogle ScholarPubMed
Gahan, A. 1927. Miscellaneous descriptions of new parasitic Hymenoptera with some synonymical notes. Proceedings of the United States National Museum, 71: 139.CrossRefGoogle Scholar
Gertsson, C. 2013. A zoogeographical analysis of the scale insect (Hemiptera, Coccoidea) fauna of Fennoscandia and Denmark. Norweigan Journol of Entomology, 25: 8189.Google Scholar
González, P.I., Montoya, P., Perez-Lachaud, G., Cancino, J., and Liedo, P. 2007. Superparasitism in mass reared Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae), a parasitoid of fruit flies (Diptera: Tephritidae). Biological Control, 40: 320326. https://doi.org/10.1016/j.biocontrol.2006.11.009.CrossRefGoogle Scholar
Gordh, G. and Beardsley, J.W. 1999. Taxonomy and biological control. In Handbook of biological control. Edited by Bellows, T.S. and Fisher, T.W.. Academic Press, San Diego, California, United States of America. Pp. 4555.CrossRefGoogle Scholar
Greathead, D.J. 1972. Dispersal of the sugar-cane scale Aulacaspis tegalensis (Zhnt.) (Hem., Diaspididae) by air currents. Bulletin of Entomological Research, 61: 547558. https://doi.org/10.1017/S0007485300047404.CrossRefGoogle Scholar
Griswold, G.H. 1927. The development of Coccophagus gossypariae Gahan, a parasite of the European elm scale. Annals of the Entomological Society of America, 20: 553555.CrossRefGoogle Scholar
Gulick, J. 2014. Planning for urban forest resilience: managing invasive pests and diseases [online]. Available from http://www.treesintrouble.com/wp-content/uploads/2015/08/PAS-Memo-March-April-2014_cr.pdf [accessed 5 January 2020].Google Scholar
Hardy, I.C.W. 1994. Sex ratio and mating structure in the parasitoid Hymenoptera. Oikos, 72: 320.CrossRefGoogle Scholar
Hoddle, M.S., Van Driesche, R.G., and Sanderson, J.P. 1998. Biology and use of the whitefly parasitoid Encarsia formosa. Annual Review of Entomology, 43: 645669. https://doi.org/10.1146/annurev.ento.43.1.645.CrossRefGoogle ScholarPubMed
Japoshvili, G. and Celik, H. 2010. Fauna of Encyrtidae, parasitoids of coccids in Golcuk Natural Park. Entomologia Hellenica, 19: 132136. https://doi.org/10.12681/eh.11580.CrossRefGoogle Scholar
Japoshvili, G. and Kaydan, M.B. 2018. Parasitoid complex of Gossypariae spuria (Modeer) Hemitpera: Acathococcidae) from eastern Anatolia with new records for the Turkish fauna. Annals of Agrarian Science, 16: 3233. https://doi.org/10.1016/j.aasci.2018.01.001.CrossRefGoogle Scholar
Karimzadeh, R. and Iranipour, S. 2017. Spatial distribution and site-specific spraying of main sucking pests of elm trees. Neotropical Entomology, 46: 18. https://doi.org/10.1007/s13744-016-0453-3.CrossRefGoogle ScholarPubMed
Kozár, F., Samu, F., Szita, É., Konczné Benedicty, Z., Kiss, B., Botos, E., et al. 2009. New data to the scale insect (Hemiptera: Coccoidea) fauna of Mezőföld (Hungary). Acta Phytopathologica et Entomologica Hungarica, 44: 431442. https://doi.org/10.1556/APhyt.44.2009.2.19.CrossRefGoogle Scholar
Laćan, I. and McBride, J.R. 2008. Pest vulnerability matrix (PVM): a graphic model for assessing the interaction between tree species diversity and urban forest susceptibility to insects and diseases. Urban Forestry and Urban Greening, 7: 291300. https://doi.org/10.1016/j.ufug.2008.06.002.CrossRefGoogle Scholar
Latham, D.R. and Mills, N.J. 2010. Life history characteristics of Aphidius transcaspicus, a parasitoid of mealy aphids (Hyalopterus species). Biological Control, 54: 147157.CrossRefGoogle Scholar
Liang, Q., Jia, Y., and Liu, T., 2017. Self-and conspecific discrimination between unparasitized and parasitized green peach aphid (Hemiptera: Aphididae), by Aphelinus asychis (Hymenoptera: Aphelinidae). Journal of Economic Entomology, 110: 430437.Google Scholar
Mackauer, M. and Chow, A. 2016. Females of the parasitoid wasp, Dendrocerus carpenteri (Hymenoptera: Megaspilidae), adjust offspring sex allocation when competing for hosts. European Journal of Entomology, 113: 542550. https://doi.org/10.14411/eje.2016.074.CrossRefGoogle Scholar
Mills, N.J. and Gutierrez, A.P. 1996. Prospective modelling in biological control: an analysis of the dynamics of heteronomous hyperparasitism in a cotton-whitefly-parasitoid system. Journal of Applied Ecology, 33: 13791934.CrossRefGoogle Scholar
Mills, N.J. and Kean, J.M. 2010. Behavioral studies, molecular approaches, and modeling: methodological contributions to biological control success. Biological Control, 52: 255262. https://doi.org/10.1016/j.biocontrol.2009.03.018.CrossRefGoogle Scholar
Milonas, P., Kozár, F., and Kontodimas, D. 2008. List of scale insects of Greece. In Proceedings of the XI international symposium on scale insect studies, Oeiras, Portugal, 24–27 September 2007. Edited by Branco, M., Franco, J.C., and Hodgson, C.J.. Instituto Superior de Agronomia Press, Lisbon, Portugal. Pp. 2427.Google Scholar
Milosavljević, I., Schall, K., Hoddle, C., Morgan, D., and Hoddle, M. 2017. Biocontrol program targets Asian citrus psyllid in California’s urban areas. California Agriculture, 71: 169177. https://doi.org/10.3733/ca.2017a0027.CrossRefGoogle Scholar
Nufio, C.R. and Papaj, D.R. 2001. Host marking behavior in phytophagous insects and parasitoids. Entomologia Experimentalis et Applicata, 99: 273293.CrossRefGoogle Scholar
Outreman, Y., Le Ralec, A., Plantegenest, M., Chaubet, B., and Pierre, J.S. 2001. Superparasitism limitation in an aphid parasitoid: cornicle secretion avoidance and host discrimination ability. Journal of Insect Physiology, 47: 339348.CrossRefGoogle Scholar
Rogers, D. 1975. A model for avoidance of superparasitism by solitary insect parasitoids. Journal of Animal Ecology, 44: 623638.CrossRefGoogle Scholar
Rogers, M.E. and Potter, D. 2003. Effects of spring imidacloprid application for white grub control on parasitism of Japanese beetle (Coleoptera: Scarabaeidae) by Tiphia vernalis (Hymenoptera: Tiphiidae). Journal of Economic Entomology, 96: 14121419.CrossRefGoogle Scholar
Ruschioni, S., van Loon, J.J., Smid, H.M., and van Lenteren, J.C., 2015. Insects can count: sensory basis of host discrimination in parasitoid wasps revealed. Public Library of Science One, 10: e0138045.Google ScholarPubMed
Sclar, D.C. and Cranshaw, W.S. 1996. Evaluation of new systemic insecticides for elm insect pest control. Journal of Environmental Horticulture, 14: 2226.Google Scholar
Tanis, S.R., Cregg, B.M., Mota-Sanchez, D., McCullough, D.G., and Poland, T.M. 2012. Spatial and temporal distribution of trunk-injected 14C-imidacloprid in Fraxinus trees. Pest Management Science, 68: 529536.CrossRefGoogle Scholar
Tormos, J., Asís, J., Sabater-Muñoz, B., Baños, L., Gayubo, S.F., and Beitia, F. 2012. Superparasitism in laboratory rearing of Spalangia cameroni (Hymenoptera: Pteromalidae), a parasitoid of medfly (Diptera: Tephritidae). Bulletin of Entomological Research, 102: 5161. https://doi.org/10.1017/S0007485311000393.CrossRefGoogle Scholar
Tunca, H., Buradino, M., Colombel, E.A., and Tabone, E. 2016. Tendency and consequences of superparasitism for the parasitoid Ooencyrtus pityocampae (Hymenoptera: Encyrtidae) in parasitizing a new laboratory host, Philosamia ricini (Lepidoptera: Saturniidae). European Journal of Entomology, 113: 5159. https://doi.org/10.14411/eje.2016.006.CrossRefGoogle Scholar
van Alphen, J.J.M. and Visser, M.E. 1990. Superparasitism as an adaptive strategy for insect parasitoids. Annual Review of Entomology, 35: 5979. https://doi.org/10.1146/annurev.en.35.010190.000423.CrossRefGoogle ScholarPubMed
van Dijken, M.J., Van Stratum, P., and van Alphen, J.J. 1992. Recognition of individual-specific marked parasitized hosts by the solitary parasitoid Epidinocarsis lopezi. Behavioral Ecology and Sociobiology, 30: 7782.CrossRefGoogle Scholar
van Lenteren, J.C. 2012. The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. BioControl, 57: 120. https://doi.org/10.1007/s10526-011-9395-1.CrossRefGoogle Scholar
van Lenteren, J.C., Drost, Y.C., Van Roermund, H.J.W., and Posthuma-Doodeman, C.J.A.M., 1997. Aphelinid parasitoids as sustainable biological control agents in greenhouses. Journal of Applied Entomology, 121: 473485. https://doi.org/10.1111/j.1439-0418.1997.tb01437.x.CrossRefGoogle Scholar
Viggiani, G. 1998. Rediscription of Coccophagus gossypariae Gahan (Hymenoptera, Aphelinidae), with notes on the preimaginal stages. Phytophaga, 8: 3947.Google Scholar
Viggiani, G. 1999. Variations and biological traits of Coccophagus gossypariae Gahan (Hymenoptera: Aphelinidae). Biological Control, 16: 4346. https://doi.org/10.1006/bcon.1999.0735.CrossRefGoogle Scholar
Walter, G.H. 1983. “Divergent male ontogenies” in Aphelinidea (Hymenoptera: Chalcidoidea): a simple classification and suggested evolutionary sequence. Biological Journal of the Linnean Society, 19: 6382. https://doi.org/10.1111/j.1095-8312.1983.tb00777.x.CrossRefGoogle Scholar
Washburn, J.O. and Washburn, L. 1984. Active aerial dispersal of minute wingless arthropods: exploitation of boundary-layer velocity gradients. Science, 223: 10881090. https://doi.org/10.1126/science.223.4640.1088.CrossRefGoogle ScholarPubMed
Weisser, W.W. and Houston, A.I. 1993. Host discrimination in parasitic wasps: when is it advantageous? Functional Ecology, 7: 2739.CrossRefGoogle Scholar
West, S.A. and Rivero, A. 2000. Using sex ratios to estimate what limits reproduction in parasitoids. Ecology Letters, 3: 294299. https://doi.org/10.1046/j.1461-0248.2000.00153.x.CrossRefGoogle Scholar
Williams, D.J. 1985. The British and some other European Eriococcidae (Homoptera: Coccoidea). Bulletin of the British Museum (Natural History), Entomology, 51: 347393.Google Scholar