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Effects of superparasitism on immature and adult stages of Diachasmimorpha longicaudata Ashmead (Hymenoptera: Braconidae) reared on Ceratitis capitata Wiedemann (Diptera: Tephritidae)

Published online by Cambridge University Press:  06 April 2017

F. Devescovi ,
G.E. Bachmann ,
A.L. Nussenbaum ,
M.M. Viscarret ,
J.L. Cladera  and
D.F. Segura
F. Devescovi*
Affiliation:
Laboratorio de Genética de Insectos de Importancia Económica, IGEAF, CICVyA, INTA, Hurlingham, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina
G.E. Bachmann
Affiliation:
Laboratorio de Genética de Insectos de Importancia Económica, IGEAF, CICVyA, INTA, Hurlingham, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina
A.L. Nussenbaum
Affiliation:
Laboratorio de Genética de Insectos de Importancia Económica, IGEAF, CICVyA, INTA, Hurlingham, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina
M.M. Viscarret
Affiliation:
Insectario de Investigaciones para Lucha Biológica, IMyZA, CICVyA, INTA, Hurlingham, Argentina
J.L. Cladera
Affiliation:
Laboratorio de Genética de Insectos de Importancia Económica, IGEAF, CICVyA, INTA, Hurlingham, Argentina
D.F. Segura
Affiliation:
Laboratorio de Genética de Insectos de Importancia Económica, IGEAF, CICVyA, INTA, Hurlingham, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina
*
*Author for correspondence Phone: +(54 11) 4450 0805 ext. 111 Fax: +(54 11) 4450 1876 E-mail: frandevescovi00@hotmail.com
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Abstract

The optimal use of available host by parasitoid insects should be favoured by natural selection. For solitary parasitoids, superparasitism (i.e. the egg-laying of several eggs/host) may represent a detrimental phenomenon both in a biological and an applied sense, but under certain circumstances it may be adaptive. Here, we studied the effects of increasing levels of superparasitism (LSPs, number of parasitoid larvae/host) on fitness-related parameters of the immature and adult stages of Diachasmimorpha longicaudata, a solitary endoparasitoid parasitizing Ceratitis capitata. We investigated the moment when supernumerary parasitoid larvae are eliminated and the effects produced by this process, together with its repercussion on female fecundity, parasitism rate, sex ratio, adult survival, flight ability and body size. Complete elimination of competitors occurred soon after larval hatching, before reaching the second larval stage. Elimination process took longer at higher LSPs, although a normal developmental (egg–adult) time was achieved. For LSPs 1, 2, 3 and 5 the effects on parasitoid emergence were mild, but LSP 10 led to the death of all developing parasitoids. Aside from this, to develop in superparasitized hosts did not significantly affect any of the evaluated parameters, and only a female-biased sex ratio was observed at higher LSPs. However, the effects of superparasitism on the adults may have a different outcome under more variable conditions in the field, once they are released for biological control purposes.

Keywords

biological controlbraconid parasitoidforaging behaviourintraspecific larval competitiontephritidae fruit fly
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 107 , Issue 6 , December 2017 , pp. 756 - 767
Copyright
Copyright © Cambridge University Press 2017 

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References

Bai, B. & Mackauer, M. (1992) Influence of superparasitism on development rate and adult size in a solitary parasitoid Aphidius ervi. Functional Ecology 6, 302–307.Google Scholar
Bakker, K., van Alphen, J.J.M., van Batenberg, F.H.D., van der Hoeven, N., Nell, H.W., van Strien-van Liempt, W.T.F.H. & Turlings, T.C.J. (1985) The function of host discrimination and superparasitization in parasitoids. Oecologia 67, 572–576.Google Scholar
Böckmann, E.A., Tormos, J., Beitia, F. & Fischer, K. (2012) Offspring production and selfsuperparasitism in the solitary ectoparasitoid Spalangia cameroni (Hymenoptera: Pteromalidae) in relation to host abundance. Bulletin of Entomological Research 102, 131–137.Google Scholar
Brodeur, J. & Boivin, G. (2004) Functional ecology of immature parasitoids. Annual Reviews in Entomology 49, 27–49.Google Scholar
Cancino, J., Cancino, J.L., Martínez, M. & Liedo, P. (2002) Quality control parameters of wild and mass reared Diachasmimorpha longicaudata (Ashmead), a fruit fly parasitoid. p. 84 in Leppla, N.C., Bloem, K.A. & Luck, R.F. (Eds) Quality Control for Mass-Reared Arthropods, Proceedings of the Eighth and Ninth Workshops of the IOBC Working Group on Quality Control of Mass-Reared Arthropods. University of Florida, USA.Google Scholar
Chau, N.N.B. & Maeto, K. (2008) Intraspecific larval competition in Meteorus pulchricornis (Hymenoptera: Braconidae), a solitary endoparasitoid of lepidopteran larvae. Applied Entomology and Zoology 43, 159–165.Google Scholar
Chow, F.J. & Mackauer, M. (1986) Host discrimination and larval competition in the aphid parasite Ephedrus californicus. Entomologia Experimentalis et Applicata 41, 243–254.Google Scholar
Clausen, C.P., Clancy, D.W. & Chock, Q.C. (1965) Biological control of the oriental fruit fly (Dacus dorsalis Hendel) and other fruit flies in Hawaii (No. 1322). Agricultural Research Service. US Dept. of Agriculture; for sale by the Supt. of Docs., US Govt. Print. Off.Google 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, 279–285.Google Scholar
Eller, F.J., Tumlinson, J.H. & Lewis, W.J. (1990) Intraspecific competition in Microplitis croceipes (Hymenoptera: Braconidae), a parasitoid of Heliothis species (Lepidoptera: Noctuidae). Annals of the Entomological Society of America 83, 504–508.Google Scholar
Fisher, R.C. (1961) A study in insect multiparasitism II. The mechanism and control of competition for possession of the host. Journal of Experimental Biology 38, 605–629.Google Scholar
Fisher, R.C. (1971) Aspects of the physiology of endoparasitic Hymenoptera. Biological Reviews 46, 243–278.Google Scholar
Godfray, H.C.J. (1994) Parasitoids Behavioural and Evolutionary Ecology. 1st edn. 473 p. Princeton, New Jersey, Princeton University Press.Google 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, 320–326.Google Scholar
Gross, P. (1993) Insect behavioral and morphological defenses against parasitoids. Annual Review of Entomology 38, 251–73.Google Scholar
Harvey, J.A., Jervis, M.A., Gols, R., Jiang, N. & Vet, L.E. (1999) Development of the parasitoid, Cotesia rubecula (Hymenoptera: Braconidae) in Pieris rapae and Pieris brassicae (Lepidoptera: Pieridae): evidence for host regulation. Journal of Insect Physiology 45, 173–182.Google Scholar
Heimpel, G.E. & Lundgren, J.G. (2000) Sex ratios of commercially reared biological control agents. Biological Control 19, 77–93.Google Scholar
Hoffmeister, T.S. & Roitberg, B.D. (1997) To mark the host or the patch: decisions of a parasitoid searching for concealed host larvae. Evolutionary Ecology 11, 145–168.Google Scholar
King, B.H. (1987) Offspring sex ratios in parasitoid wasps. Quarterly Review of Biology 62, 367–396.Google Scholar
King, B.H. (1993) Sex ratio manipulation by parasitoid wasps. pp. 418–441 in Wrensch, D.L. & Ebbert, M. (Eds) Evolution and Diversity of Sex Ratio in Insects and Mites. Chapman & Hall, New York.Google Scholar
Lawrence, P.O. (1988) Intraspecific competition among first instars of the parasitic wasp Biosteres longicaudatus. Oecologia 74, 607–611.Google Scholar
Lebreton, S., Chevrier, C. & Darrouzet, E. (2010) Sex allocation strategies in response to conspecifics offspring sex ratio in solitary parasitoids. Behavioral Ecology 21, 107–112.Google Scholar
López, O.P., Hénaut, Y., Cancino, J., Lambin, M., Cruz-López, L. & Rojas, J.C. (2009) Is host size an indicator of quality in the mass-reared parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae)? Florida Entomologist 92, 441–449.Google Scholar
Mackauer, M. (1990) Host discrimination and larval competition in solitary endoparasitoids. pp. 41–62 in Mackauer, M. & Ehler, L.E. (Eds) Critical Issues in Biological Control. Intercept Ltd, Andover, Hants.Google Scholar
Mackauer, M. & Chau, A. (2001) Adaptive self superparasitism in a solitary parasitoid wasp: the influence of clutch size on offspring size. Functional Ecology 15, 335–343.Google 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, 131–141.Google Scholar
Meirelles, R.N., Redaelli, L.R. & Ourique, C. B. (2013) Comparative biology of Diachasmimorpha longicaudata (Hymenoptera: Braconidae) reared on Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae). Florida Entomologist 96, 412–418.Google Scholar
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 flies (Diptera: Tephritidae). Annals of the Entomological Society of America 93, 47–54.Google Scholar
Montoya, P., Cancino, J., Pérez-Lachaud, G. & Liedo, P. (2011) Host size, superparasitism and sex ratio in mass-reared Diachasmimorpha longicaudata, a fruit fly parasitoid. BioControl 56, 11–17.Google Scholar
Montoya, P., Pérez-Lachaud, G. & Liedo, P. (2012) Superparasitism in the fruit fly parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae) and the implications for mass rearing and augmentative release. Insects 3, 900–911.Google Scholar
Ovruski, S.M., Colin, C., Soria, A., Oroño, L.E. & Schliserman, P. (2003) Introducción y producción en laboratorio de Diachasmimorpha tryoni y Diachasmimorpha longicaudata (Hymenoptera: Braconidae) para el control biológico de Ceratitis capitata (Diptera: Tephritidae) en la Argentina. Revista de la Sociedad Entomológica Argentina 62, 49–59.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, 466–474.Google Scholar
Rosenheim, J.A. & Hongkham, D. (1996) Clutch size in an obligately siblicidal parasitoid wasp. Animal Behaviour 51, 841–852.Google Scholar
Rosenheim, J.A. & Mangel, M. (1994) Patch-leaving rules for parasitoids with imperfect host discrimination. Ecological Entomology 19, 374–380.Google Scholar
Salt, G. (1934) Experimental Studies in Insect Parasitism. II. Superparasitism. Proceedings of the Royal Society of London. Series B, Containing Papers of a Biological Character 114, 455–476.Google Scholar
Salt, G. (1936) Experimental studies in insect parasitism IV. The effect of superparasitism on populations of Trichogramma evanescens. Journal of Experimental Biology 13, 363–362.Google Scholar
Salt, G. (1961) Competition among insect parasitoids. Symposia of the Society for Experimental Biology 15, 119.Google Scholar
Santolamazza-Carbone, S. & Cordero-Rivera, A. (2003) Superparasitism and sex ratio adjustment in a wasp parasitoid: results at variance with Local Mate Competition? Oecologia 136, 365–73.Google Scholar
Segura, D.F., Nussenbaum, A.L., Viscarret, MM, Devescovi, F., Bachmann, G.E., Corley, J.C., Ovruski, S.M. & Cladera, J.L. (2016) Innate host habitat preference in the parasitoid Diachasmimorpha longicaudata: functional significance and modifications through learning. PLoS ONE 11(3), e0152222. doi: 10.1371/journal.pone.0152222.Google Scholar
Sequeira, R. & Mackauer, M. (1992) Nutritional ecology of an insect host-parasitoid association: the pea-aphid Aphidus ervi system. Ecology 73, 183–189.Google Scholar
Simmonds, F.J. (1943) The occurrence of superparasitism in Nemeritis canescens Grav. Revue canadienne de biologie expérimentale 2, 15–58.Google Scholar
Terán, H. (1977) Comportamiento alimentario y su correlación a la reproducción en hembras de Ceratitis capitata Wied. Revista Agronómica del NOA 14, 17–34.Google Scholar
Tunca, H. & Kilincer, N. (2009) Effect of superparasitism on the development of the solitary parasitoid Chelonus oculator Panzer (Hymenoptera: Braconidae). Turkish Journal of Agriculture and Forestry 33, 463–468.Google Scholar
van Alphen, J.J.M. & Visser, M.E. (1990) Superparasitism as an adaptive strategy for insect parasitoids. Annual Review of Entomology 35, 59–79.Google Scholar
van Baaren, J., Landry, B.L. & Boivin, G. (1999) Sex allocation and larval competition in a superparasitizing solitary egg parasitoid: competing strategies for an optimal sex ratio. Functional Ecology 13, 66–71.Google Scholar
van Dijken, M.J. & Waage, J.K. (1987) Self and conspecific superparasitism by the egg parasitoid Trichogramma evanescens. Entomologia Experimentalis et Applicata 43, 183–192.Google Scholar
van Lenteren, J.C. (1981) Host discrimination by parasitoids. pp. 153–179 in Nordlund, N. (Ed.) Semiochemicals: Their Role in Pest Control. Wiley, New York.Google Scholar
Varaldi, J., Fouillet, P., Ravallec, M., López-Ferber, M., Boulétreau, M. & Fleury, F. (2003) Infectious behavior in a parasitoid. Science 302, 1930–1930.Google Scholar
Varaldi, J., Ravallec, M., Labrosse, C., Lopez-Ferber, M., Boulétreau, M. & Fleury, F. (2006) Artifical transfer and morphological description of virus particles associated with superparasitism behaviour in a parasitoid wasp. Journal of Insect Physiology 52, 1202–1212.Google Scholar
Vinson, S.B. & Iwantsch, G.F. (1980) Host suitability for insect parasitoids. Annual Review of Entomology 25, 397–419.Google Scholar
Vinson, S.B. & Hegazi, E.M. (1998) A possible mechanism for the physiological suppression of conspecific eggs and larvae following superparasitism by solitary endoparasitoids. Journal of Insect Physiology 44, 703–712.Google Scholar
Viscarret, M.M., La Rossa, R., Segura, D.F., Ovruski, S.M. & Cladera, J.L. (2006) Evaluation of the parasitoid Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae) reared on a genetic sexing strain of Ceratitis capitata (Wied.) (Diptera: Tephritidae). Biological Control 36, 147–153.Google Scholar
Wang, X.G. & Messing, R.H. (2003) Intra- and interspecific competition by Fopius arisanus and Diachasmimorpha tryoni (Hymenoptera: Braconidae), parasitoids of tephritid fruit flies. Biological Control 27, 251–259.Google Scholar
Wharton, R.A. & Gilstrap, F.E. (1983) Key to and status of Opiinae Braconid (Hymenoptera) parasitoids used in biological control of Ceratitis and Dacus S. L. (Diptera: Tephritidae). Annals of the Entomological Society of America 76, 721–742.Google Scholar
Wylie, H.G. (1965) Discrimination between parasitized and unparasitized house fly pupae by females of Nasonia vitripennis (Walk.) (Hymenoptera: Pteromalidae). The Canadian Entomologist 97, 279–286.Google Scholar
Wylie, H.G. (1983) Delayed development of Microctonus vittatae (Hymenoptera: Braconidae) in superparasitized adults of Phyllotreta cruciferae (Coleoptera: Chrysomelidae). The Canadian Entomologist 115, 441–422.Google Scholar
Zar, J. H. (1996) Biostatistical Analysis. 3rd edn. 863 p. Upper Saddle River, New Jersey, Prentice Hall.Google Scholar