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Superparasitism in Laboratory rearing of Spalangia cameroni (Hymenoptera: Pteromalidae), a parasitoid of medfly (Diptera: Tephritidae)

Published online by Cambridge University Press:  15 August 2011

J. Tormos*
Affiliation:
Área de Zoología, Facultad de Biología, Universidad de Salamanca, 37071-Salamanca, Spain
J. Asís
Affiliation:
Área de Zoología, Facultad de Biología, Universidad de Salamanca, 37071-Salamanca, Spain
B. Sabater-Muñoz
Affiliation:
Instituto Valenciano de Investigaciones Agrarias, Unidad Asociada de Entomología IVIA/CIB-CSIC, Apartado Oficial, 46113-Montcada, Valencia, Spain
L. Baños
Affiliation:
Área de Zoología, Facultad de Biología, Universidad de Salamanca, 37071-Salamanca, Spain
S.F. Gayubo
Affiliation:
Área de Zoología, Facultad de Biología, Universidad de Salamanca, 37071-Salamanca, Spain
F. Beitia
Affiliation:
Instituto Valenciano de Investigaciones Agrarias, Unidad Asociada de Entomología IVIA/CIB-CSIC, Apartado Oficial, 46113-Montcada, Valencia, Spain
*
*Author for correspondence Fax: 34 923294515 E-mail: [email protected]

Abstract

The frequency of superparasitism and its effects on the quality of laboratory-reared Spalangia cameroni (Hymenoptera: Pteromalidae) parasitoids were investigated under laboratory conditions. Numerous variables were measured, such as the number of ‘ovip holes’ per host as a measure of superparasitism. Adult emergence and sex ratio, as well as female size, emergence ability from soil and longevity were also measured. Finally, an assessment was made of fertility and survival of adult parasitoids emerging from the medfly Ceratitis capitata (Diptera: Tephritidae) pupae with different levels of superparasitism. A high frequency and prevalence of superparasitism under laboratory rearing conditions was observed. The number of ‘ovip holes’ per host ranged from one to 17, with an average (±SD) of 2.8±3.4. Sex ratios became increasingly female-biased with increasing levels of superparasitism, although overall levels of wasp emergence (male, female) declined. Nevertheless, no relationship was discerned between female size and level of superparasitism. The ‘emergence ability from the soil’ was higher in those parasitoids that emerged from strongly superparasitized hosts, but not related to the type of substrate in which the host pupae were buried. The level of superparasitism did not have a significant effect on the longevity, fertility and survival of female parasitoids. Our results support the hypothesis that superparasitism in S. cameroni might be adaptive, since attributes such as ‘emergence ability from the soil’, longevity, fertility and survival were not affected by the level of superparasitism or the presumably detrimental effects derived from physical combats among conspecific larvae. Our findings are relevant to recommendations for rearing S. cameroni for biological control releases, as well as shedding light on superparasitism under both laboratory and field conditions.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2011

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References

Alonso, M. (2009) Nuevo método de cría de Spalangia cameroni (Hymenoptera, Pteromalidae), calcidoideo utilizado en el control biológico de Ceratitis capitata (Diptera, Tephritidae). Tesis de Licenciatura (Master's thesis). Universidad de Salamanca, Salamanca, Spain.Google Scholar
Bakker, T., Peulet, P.H. & Visser, M.E. (1990) The ability to distinguish between hosts containing different numbers of parasitoid eggs by the solitary parasitoid Leptopilina heterotoma (Thomson) (Hym., Cynip.). Netherlands Journal of Zoology 40, 514520.CrossRefGoogle Scholar
Charnov, E.L., Los Den Hartogh, R.L., Jones, W.T. & van dem Assem, J. (1981) Sex ratio evolution in a variable environment. Nature 289, 2733.CrossRefGoogle Scholar
Cranshaw, W., Sclar, D.C. & Cooper, D. (1996) A review of 1994 pricing and marketing by suppliers of organisms for biological control of arthropods in the United States. Biological Control 6, 291296.CrossRefGoogle Scholar
Cullen, D., Sherratt, T.N. & Hubbard, S.F. (1991) Parasitoid diets: Does superparasitism pay? Tree 6, 2225.Google Scholar
Darrouzet, E., Imbert, E. & Chevrier, C. (2003) Self-superparasitism consequences for offspring sex ratio in the solitary ectoparasitoid Eupelmus vuilleti. Entomologia Experimentalis et Applicata 109, 167171.CrossRefGoogle Scholar
Darrouzet, E., Bignon, L. & Chevrier, C. (2007) Impact of mating status on egg-laying and superparasitism behaviour in a parasitoid wasp. Entomologia Experimentalis et Applicata 123, 279285.CrossRefGoogle Scholar
Docavo, I., Tormos, J. & Fischer, M. (2007) Bracónidos de España (Hym., Braconidae). Síntesis general dela familia. Subfamilia Alysiinae. Valencia, Spain, Patronato Valenciano de Zoología ‘Ignacio Docavo’.Google Scholar
Falcó, J.V., Garzón-Luque, E., Pérez-Hinarejos, M., Tarazona, I., Malagón, J. & Beitia, F. (2006) Two native pupal parasitoids of Ceratitis capitata (Diptera, Tephritidae) found in Spain. IOBC/WPRS Bulletin 29, 7174.Google Scholar
Galloway, K.S. & Grant, B. (1989) Reverse sex ratio adjustment in an apparently outbreeding wasp, Bracon hebetor. Evolution 43, 465468.CrossRefGoogle Scholar
Geden, C.J. & Hogsette, J.A. (2006) Suppression of house flies (Diptera: Muscidae) in Florida poultry houses by sustained releases of Muscidifurax raptorellus and Spalangia cameroni (Hymenoptera: Pteromalidae). Environmental Entomology 35, 7582.CrossRefGoogle Scholar
Gerling, D. & Legner, E.F. (1968) Developmental history and reproduction of Spalangia cameroni, parasite of synanthropic flies. Annals of the Entomological Society of America 61, 14361443.CrossRefGoogle Scholar
Godfray, H.C.J. (1994) Parasitoids: Behavioral and Evolutionary Ecology. Princenton, NJ, USA, Princeton University Press.CrossRefGoogle Scholar
González, P.I., Montoya, P., Perez-Lachaud, G., Cancino, J. & Liedo, P. (2007) Superparasitism in mass reared Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae), a parasitoid of fruit flies (Diptera: Tephritidae). Biological Control 40, 320326.CrossRefGoogle Scholar
Hamilton, W.D. (1979) Wingless and fighting males in fig wasps and other insects. pp 167220in Blum, M.S. & Blum, N.A. (Eds) Sexual Selection and Reproductive Competition in Insects. New York, USA, Academic Press.Google Scholar
Heimpel, G.E. & Lundgren, J.G. (2000) Sex ratios of commercially reared biological control agents. Biological Control 19, 7793.CrossRefGoogle Scholar
Hurlbutt, B.L. (1987) Sex ratio in a parasitoid wasp Spalangia cameroni (Hymenoptera:Pteromalidae). PhD thesis, Purdue University, West Lafayette, IN, USA.Google Scholar
King, B.H. (1987) Offspring sex ratios in parasitoid wasps. Quarterly Review of Biology 62, 367396.CrossRefGoogle Scholar
King, B.H. (1988) Sex-ratio manipulation in response to host size by the parasitoid wasp Spalangia cameroni: a laboratory study. Evolution 42, 11901198.Google ScholarPubMed
King, B.H. (1989) A test of local mate competition theory with a parasitoid wasp, Spalangia cameroni. Oikos 55, 5054.CrossRefGoogle Scholar
King, B.H. (1990) Sex ratio manipulation by the parasitoid wasp Spalangia cameroni in response to host age: a test of the host-size model. Evolutionary Ecology 4, 149156.CrossRefGoogle Scholar
King, B.H. (1993) Sex ratio manipulation by parasitoid wasps. pp. 418441in Wrensch, D.L. & Ebbert, M. (Eds) Evolution and Diversity of Sex Ratio in Insects and Mites. New York, USA, Chapman and Hall.CrossRefGoogle Scholar
King, B.H. (1994a) Effects of host size experience on sex ratios in the parasitoid wasp Spalangia cameroni. Animal Behaviour 47, 815820.CrossRefGoogle Scholar
King, B.H. (1994b) How do female parasitoid wasps assess host size during sex-ratio manipulation? Animal Behaviour 48, 511518.CrossRefGoogle Scholar
King, B.H. (1996) Fitness effects of sex ratio response to host quality and size in the parasitoid wasp Spalangia cameroni. Behavioral Ecology 7, 3542.CrossRefGoogle Scholar
King, B.H. (1998) Host Age Response in the Parasitoid Wasp Spalangia cameroni (Hymenoptera: Pteromalidae). Journal of Insect Behavior 11, 101117.Google Scholar
King, B.H. (2002a) Offspring sex ratio and number in response to proportion of host sizes and ages in the parasitoid wasp Spalangia cameroni (Hymenoptera: Pteromalidae). Environmental Entomology 31, 505508.CrossRefGoogle Scholar
King, B.H. (2002b) Breeding strategies in females of the parasitoid wasp Spalangia endius: effects of mating status and body size. Journal of Insect Behavior 15, 181193.CrossRefGoogle Scholar
King, B.H. & King, R.B. (1994) Sex ratio manipulation in response to host size in the parasitoid wasp Spalangia cameroni: is it adaptive? Behavioral Ecology 5, 448454.CrossRefGoogle Scholar
King, B.H. & Lee, H.E. (1994) Test of the adaptiveness of sex ratio manipulation in a parasitoid wasp. Behavioral Ecology and Sociobiology 35, 437443.CrossRefGoogle Scholar
Lebreton, S., Labarussias, M., Chevrier, C. & Darrouzet, E. (2009) Discrimination of the age of conspecific eggs by an ovipositing female wasp. Entomologia Experimentalis et Applicata 130, 2834.CrossRefGoogle Scholar
Lebreton, S., Christidès, J.P., Bagnères, A.-G., Chevrier, C. & Darrouzet, E. (2010a) Modifications of the chemical profile of hosts after parasitism allow parasitoid females to assess the time elapsed since the first attack. Journal of Chemical Ecology 36, 513521.CrossRefGoogle ScholarPubMed
Lebreton, S., Chevrier, C. & Darrouzet, E. (2010b) Sex allocation strategies in response to conspecifics offspring sex ratio in solitary parasitoids. Behavioral Ecology 21, 107112.CrossRefGoogle Scholar
Lebreton, S., Chevrier, C. & Darrouzet, E. (2010c) Sex allocation strategies in response to conspecifics offspring sex ratio in solitary parasitoids. Behavioral Ecology 21, 107112.CrossRefGoogle Scholar
Mayhew, P.J. & van Alphen, J.J.M. (1999) Gregarious development in alysiine parasitoids evolved through a reduction in larval aggression. Animal Behaviour 58, 131141.CrossRefGoogle ScholarPubMed
Montoya, P., Liedo, P., Benrey, B., Barrera, J.F., Cancino, J. & Aluja, M. (2000) Functional response and superparasitism by Diachasmimorpha longicaudata (Hymenoptera: Braconidae), a parasitoid of fruit fies (Diptera:Tephritidae). Annals of the Entomological Society of America 93, 4754.CrossRefGoogle Scholar
Mousseau, T.A. & Fox, C.W. (1998) The adaptive significance of maternal effects. Tree 13, 403407.Google ScholarPubMed
Noyes, J.S. (2005) Chalcidoidea 2001. in Dicky, S.Y. (Ed.) Taxapad 2005. Available online at www.taxapad.com.Google Scholar
Pérez-Hinarejos, M. & Beitia, F. (2008) Parasitism of Spalangia cameroni (Hymenoptera, Pteromalidae), an idiobiont parasitoid on pupae of Ceratitis capitata (Diptera, Tephritidae). IOBC/wprs Bulletin 38, 130133.Google Scholar
Rivers, D.B. (1996) Changes in oviposition behavior of the ectoparasitoids Nasonia vitripennis and Muscidifurax zaraptor (Hymenoptera: Pteromalidae) when using different species of fly hosts, prior oviposition experience, and allospecific competition. Annals of the Entomological Society of America 89, 466474.CrossRefGoogle Scholar
Rosenheim, J.A. & Hongkham, D. (1996) Clutch size in an obligately siblicidal parasitoid wasp. Animal Behaviour 51, 841852.CrossRefGoogle Scholar
Rueda, L.M. & Axtell, R.C. (1985) Guide to common species of pupal parasites (Hymenoptera: Pteromalidae) of house fly and other Muscoid flies associated with poultry and livestock manure. Technical Bulletin 278, 289.Google Scholar
Salt, G. (1961) Competition among insect parasitoids. Symposium of the Society for Experimental Biology 15, 96119.Google Scholar
Steenberg, T., Skovgàrd, H. & Kalsbeek, A. (2001) Microbial and biological control of flies in stables. DJF Rapport Markbrug 49, 9194.Google Scholar
Tormos, J., Beitia, F., Böckmann, E.A. & Asís, J.D. (2009) The preimaginal stages and development of Spalangia cameroni Perkins (Hymenoptera: Pteromalidae) on Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). Micron 40, 646658.CrossRefGoogle ScholarPubMed
van Alphen, J.J.M. & Jervis, M.A. (1996) Foraging behaviour: host discrimination. pp. 3236in Jervis, M.A. & Kidd, N. (Eds) Insect Natural Enemies: A Practical Approach to their Study and Evaluation. London, UK, Chapman & Hall.Google Scholar
van Alphen, J.J.M. & Nell, H.W. (1982) Superparasitism and host discrimination by Asobara tabida Nees (Braconidae: Alysiinae), a larval parasitoid of Drosophilidae. Netherlands Journal of Zoology 32, 232260.CrossRefGoogle Scholar
van Alphen, J.J.M. & Visser, M.E. (1990) Superparasitism as an adaptive strategy for insect parasitoids. Annual Review of Entomology 35, 5979.CrossRefGoogle ScholarPubMed
van Dijken, M.J. & Waage, J.K. (1987) Self and conspecific superparasitism by the egg parasitoid Trichogramma evanescens. Entomologia Experimentalis et Applicata 43, 183192.CrossRefGoogle Scholar
van Lenteren, J.C. (1981) Host discrimination by parasitoids. pp. 153180in Nordlund, D.A., Jones, R.L. & Lewis, W.J. (Eds) Semiochemicals: Their Role in Pest Control. New York, USA, John Wiley.Google Scholar
Visser, M.E., van Alphen, J.J.M. & Hemerik, L. (1992) Adaptive superparasitism and patch time allocation in solitary parasitoids: an ESS model. Journal of Animal Ecology 61, 93101.CrossRefGoogle Scholar
Waage, J.K. (1986) Family planning in parasitoids: adaptive patterns of progeny and sex allocation. pp. 6395in Waage, J.K. & Greathead, D. (Eds) Insect Parasitoids. London, UK, Academic Press.Google Scholar
Waage, J.K., Carl, K.P., Mills, N.J. & Greathead, D.J. (1985) Rearing entomophagous insects. pp. 4566in Singh, P. & Moore, R.F. (Eds) Handbook of Insect Rearing. Amsterdam, Netherlands, Elsevier.Google Scholar
Werren, J.H. (1984) Brood size and sex ratio regulation in the parasitic wasp Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae). Netherlands Journal of Zoology 34, 123143.CrossRefGoogle Scholar
Wylie, H.G. (1965) Discrimination between parasitized and unparasitized house fly pupae by females of Nasonia vitripennis (Walk.) (Hymenoptera: Pteromalidae). Canadian Entomologist 97, 279286.CrossRefGoogle Scholar
Wylie, H.G. (1972) Oviposition retraint of Spalangia cameroni (Hymenoptera: Pteromalidae) on parasitized housefly pupae. Canadian Entomologist 104, 209214.CrossRefGoogle Scholar