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Oviposition strategy for superparasitism in the gregarious parasitoid Oomyzus sokolowskii (Hymenoptera: Eulophidae)

Published online by Cambridge University Press:  03 July 2018

X. Li
Affiliation:
School of Plant Protection, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China College of Agriculture, Shanxi Agricultural University, Taigu, Shanxi 030801, China
B. Li
Affiliation:
School of Plant Protection, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China
L. Meng*
Affiliation:
School of Plant Protection, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China
*
*Author for correspondence Tel/Fax: (86)(25)-84396394 E-mail: ml@njau.edu.cn

Abstract

Superparasitism is an adaptive strategy in solitary parasitoids, yet insufficient evidence confirms this in gregarious ones. We here ask whether the gregarious parasitoid Oomyzus sokolowskii is able to discriminate in attack and progeny allocation between parasitized and unparasitized Plutella xylostella larvae, and how the parasitoid allocates brood size and sex to superparasitized hosts due to some circumstances. We found that female parasitoids preferred unparasitized to parasitized host larvae, and allocated a smaller brood with more males in the later than in the former host. Brood size and sex ratio decreased from superparasitized hosts with a 48 h interval since a previous attack compared with one without an interval; they also declined from the host superparasitized by the parasitoid with oviposition experience compared with one without it. Brood size and sex ratio did not differ between the host superparasitized by the same parasitoid as in the first attack and that by a different one. Our findings suggest that O. sokolowskii females may adjust their oviposition decisions on progeny allocation in response to parasitized P. xylostella larvae to maximize their fitness gains from superparasitism.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2018 

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References

Baaren, J.V. & Nénon, J.P. (1996) Intraspecific larval competition in two solitary parasitoids, Apoanagyrus (Epidinocarsis) lopezi and Leptomastix dactylopii. Entomologia Experimentalis et Applicata 81, 325333.Google Scholar
Charnov, E.L., Los-den Hartogh, R.L., Jones, W.T. & Assem, J.V.D. (1981) Sex ratio evolution in a variable environment. Nature 289, 2733.Google Scholar
Dijken, M.J.V. & Waage, J.K. (1987) Self and conspecific superparasitism by the egg parasitoid Trichogramma evanescens. Entomologia Experimentalis et Applicata 43, 183192.Google Scholar
Dijken, M.J.V., van Stratum, P. & van Alphen, J.J.M. (1992) Recognition of individual-specific marked parasitized hosts by the solitary parasitoid Epidinocarsis lopezi. Behavioral Ecology and Sociobiology 30, 7782.Google Scholar
Dorn, S. & Beckage, N.E. (2007) Superparasitism in gregarious hymenopteran parasitoids: ecological, behavioural and physiological perspectives. Physiological Entomology 32, 199211.Google Scholar
Flanagan, K.E., West, S.A. & Godfray, H.C.J. (1998) Local mate competition, variable fecundity and information use in a parasitoid. Animal Behaviour 56, 191198.Google Scholar
Furlong, M.J. & Zalucki, M.P. (2007) Parasitoid complex of diamondback moth in south-east Queensland: first records of Oomyzus sokolowskii (Hymenoptera: Eulophidae) in Australia. Australian Journal of Entomology 46, 167175.Google Scholar
Furlong, M.J., Wright, D.J. & Dosdall, L.M. (2013) Diamondback moth ecology and management: problems, progress, and prospects. Annual Review of Entomology 58, 517541.Google Scholar
Gauthier, N., Monge, J.J. & Huignard, J. (1996) Superparasitism and host discrimination in the solitary ectoparasitoid Dinarmus basalis. Entomologia Experimentalis et Applicata 79, 9199.Google Scholar
Gelman, A. & Hill, J. (2007) Data analysis using regression and multilevel/hierarchical models. pp. 114116, UK, Cambridge University Press.Google Scholar
Godfray, H.C.J. (1994) Parasitoids: Behavioural and Evolutionary Ecology. Princeton, New Jersey, Princeton University Press.Google Scholar
Gu, H.N., Wang, Q. & Dorn, S. (2003) Superparasitism in Cotesia glomerata: response of hosts and consequences for parasitoids. Ecological Entomology 28, 422431.Google Scholar
Hamilton, W.D. (1967) Extraordinary sex ratios. Science 156, 477488.Google Scholar
Hardy, I.C.W., Griffiths, N.T. & Godfray, H.C.J. (1992) Clutch size in a parasitoid wasp – a manipulation experiment. Journal of Animal Ecology 61, 121129.Google Scholar
Henneman, M.L., Papaj, D.R., Figueredo, A.J. & Vet, L.E.M. (1995) Egg-laying experience and acceptance of parasitized hosts by the parasitoid, Leptopilina heterotoma (Hymenoptera: Eucoilidae). Journal of Insect Behavior 8, 331342.Google Scholar
Ikawa, T. & Suzuki, Y. (1982) Ovipositional experience of the gregarious parasitoid, Apanteles glomeratus (Hymenoptera: Braconidae), influencing her discrimination of the host larvae, Pieris rapae crucivora. Applied Entomology and Zoology 17, 119126.Google Scholar
Ito, E. & Yamada, Y.Y. (2014) Self-/conspecific discrimination and superparasitism strategy in the ovicidal parasitoid Echthrodelphax fairchildii (Hymenoptera: Dryinidae). Insect Science 21, 741749.Google Scholar
King, B.H. (1992) Sex ratios of the wasp Nasonia vitripennis from self – versus conspecifically – parasitized hosts: local mate competition versus host quality models. Journal of Evolutionary Biology 5, 445455.Google Scholar
King, B.H. (1993) Sex ratio manipulation by parasitoid wasps. pp. 225264 in Wrensch, D.L. & Ebert, M. A. (Eds) Evolution and Diversity of sex Ratio in Insect and Mites. New York, Chapman & Hall.Google Scholar
Koppik, M., Thiel, A. & Hoffmeister, T.S. (2014) Adaptive decision making or differential mortality: what causes offspring emergence in a gregarious parasitoid?. Entomologia Experimentalis et Applicata 150, 208216.Google Scholar
Lebreton, S., Labarussias, M., Chevrier, C. & Darrouzet, E. (2009) Discrimination of the age of conspecific eggs by an ovipositing ectoparasitic wasp. Entomologia Experimentalis et Applicata 130, 2834.Google Scholar
Li, X., Zhu, L., Meng, L. & Li, B. (2017) Brood size and sex ratio in response to host quality and wasp traits in the gregarious parasitoid Oomyzus sokolowskii (Hymneoptera: Eulophidae). PeerJ 5, e2919.Google Scholar
Masurier, L.A.D. (1991) Effect of host size on clutch size in Cotesia glomerata. Journal of Animal Ecology 60, 107118.Google Scholar
Mushtaque, M. (1990) Some studies on Tetrastichus sokolowskii Kurd (Eulophidae: Hymenoptera), a parasitoid of diamondback moth in Pakistan. Pakistan Journal of Zoology 22, 3743.Google Scholar
Nakamura, A. & Noda, T. (2001) Host-age effects on oviposition behavior and development of Oomyzus sokolowskii (Hymenoptera: Eulophidae), a larval-pupal parasitoid of Plutella xylostella (Lepidoptera: Yponomeutidae). Applied Entomology and Zoology 36, 367372.Google Scholar
Nakamura, A. & Noda, T. (2002) Effects of host age and size on clutch size and sex ratio of Oomyzus sokolowskii (Hymenoptera: Eulophidae), a larval-pupal parasitoid of Plutella xylostella (Lepidoptera: Yponomeutidae). Applied Entomology and Zoology 37, 319322.Google Scholar
Parker, G.A. & Courtney, S.P. (1984) Models of clutch size in insect oviposition. Theoretical Population Biology 26, 2748.Google Scholar
Rabinovich, J.E., Jorda, M.T. & Bernstein, C. (2000) Local mate competition and precise sex ratios in Telenomus fariai (Hymenoptera: Scelionidae), a parasitoid of triatomine eggs. Behavioral Ecology and Sociobiology 48, 308315.Google Scholar
R Development Core Team. (2014). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/.Google Scholar
Rosenheim, J.A. & Rosen, D. (1991) Foraging and oviposition decisions in the parasitoid Aphytis lingnanensis: distinguishing the influences of egg load and experience. Journal of Animal Ecology 60, 873893.Google Scholar
Sarfraz, M., Keddie, A.B. & Dosdall, L.M. (2005) Biological control of the diamondback moth, Plutella xylostella: a review. Biocontrol Science and Technology 15, 763789.Google Scholar
Shuker, D.M. & West, S.A. (2004) Information constraints and the precision of adaptation: sex ratio manipulation in wasps. Proceedings of the National Academy of Sciences of the USA 101, 1036310367.Google Scholar
Silva-Torres, C.S.A., Filho, I.T.R., Torres, J.B. & Barros, R. (2009) Superparasitism and host size effects in Oomyzus sokolowskii, a parasitoid of diamondback moth. Entomologia Experimentalis et Applicata 133, 6573.Google Scholar
Sow, G., Arvanitakis, L., Niassy, S., Diarra, K. & Bordat, D. (2013) Life history traits of Oomyzus sokolowskii Kurdjumov (Hymenoptera: Eulophidae), a parasitoid of the diamondback moth. African Entomology 21, 231238.Google Scholar
Strand, M.R. & Godfray, H.C.J. (1989) Superparasitism and ovicide in parasitic hymenoptera: theory and a case study of the ectoparasitoids Bracon hebetor. Behavioral Ecology & Sociobiology 24, 421432.Google Scholar
Suzuki, Y. & Iwasa, Y. (1980) A sex ratio theory of gregarious parasitoids. Researches on Population Ecology 22, 366382.Google Scholar
Suzuki, Y., Tsuji, H. & Sasakawa, M. (1984) Sex allocation and effects of superparasitism on secondary sex ratios in the gregarious parasitoid, Trichogramma chilonis (Hymenoptera: Trichogrammatidae). Animal Behaviour 32, 478484.Google Scholar
Talekar, N.S. & Hu, W.J. (1996) Characteristics of parasitism of Plutella xylostella (Lep., Plutellidae) by Oomyzus sokolowskii (Hym., Eulophidae). BioControl 41, 4552.Google Scholar
Talekar, N.S. & Shelton, A.M. (1993) Biology, ecology and management of the diamondback moth. Annual Review of Entomology 38, 275301.Google Scholar
Turlings, T.C.J., Wackers, F., Vet, L.E.M., Lewis, J. & Tumlinson, J.H. (1993) Learning of host location cues by insect parasitoids. pp. 5157 in Papaj, D.R. & Lewis, A.C. (Eds) Insect Learning: Ecological and Evolutionary Perspectives. New York, Chapman and Hall.Google Scholar
Ueno, T. & Tanaka, T. (1994) Can a female parasitoid recognize a previously rejected host? Animal Behaviour 47, 988990.Google Scholar
van Alphen, J.J.M. & Visser, M.E. (1990) Superparasitism as an adaptive strategy for insect parasitoids. Annual Review of Entomology 35, 5779.Google Scholar
van Alphen, J.J.M., Visser, M.E. & Nell, H.W. (1992) Adaptive superparasitism and patch time allocation in solitary parasitoids: the influence of pre-patch experience. Functional Ecology 6, 528535.Google Scholar
Vet, L.E.M., Datema, A., Janssen, A. & Snellen, H. (1994) Clutch size in a larval pupal endoparasitoid – consequences for fitness. Journal of Animal Ecology 63, 807815.Google Scholar
Visser, M.E. (1993) Adaptive self- and conspecific superparasitism in the solitary parasitoid Leptopilina heterotoma (Hymenoptera: Eucoilidae). Behavioral Ecology 4, 2228.Google Scholar
Visser, M.E., Luyckx, B., Nell, H.W. & Boskamp, G.J.F. (1992a) Adaptive superparasitism in solitary parasitoids: marking of parasitized hosts in relation to the pay-off from superparasitism. Ecological Entomology 17, 7682.Google Scholar
Visser, M.E., van Alphen, J.J.M. & Hemerik, L. (1992b) Adaptive super-parasitism and patch time allocation in solitary parasitoids: an ESS model. Journal of Animal Ecology 61, 93101.Google Scholar
Visser, M.E., van Alphen, J.J.M. & Nell, H.W. (1992c) Adaptive superparasitism and patch time allocation in solitary parasitoids: the influence of pre-patch experience. Behavioral Ecology and Sociobiology 31, 163171.Google Scholar
Wang, X.G., Liu, S.S., Guo, S.J. & Lin, W.C. (1999) Effects of host stages and temperature on population parameters of Oomyzus sokolowskii, a larval-pupal parasitoid of Plutella xylostella. BioControl 44, 391402.Google Scholar
Werren, J.H. (1980) Sex ratio adaptations to local mate competition in a parasite wasp. Science 208, 11571160.Google Scholar
Werren, J.H. (1984) A model for sex ratio selection in parasitic wasps: local mate competition and host quality effects. Netherlands Journal of Zoology 34, 123143.Google Scholar
West, S. (2009) Sex Allocation. Princeton, NJ, USA, Princeton University Press.Google Scholar
Wylie, H.G. (1965) Some factors that reduce the reproductive rate of Nasonia vitripennis (Walker) at high adult population densities. Canadian Entomologist 97, 970977.Google Scholar
Yazdani, M., Glatz, R. & Keller, M. (2015) Host discrimination by the solitary endoparasitoid Dolichogenidea tasmanica (Hymenopotera: Braconidae). Biocontrol Science and Technology 25, 155162.Google Scholar
Zalucki, M.P., Shabbir, A., Silva, R., Adamson, D., Liu, S.S. & Furlong, M.J. (2012) Estimating the economic cost of one of the world's major insect pests, Plutella xylostella (Lepidoptera: Plutellidae): just how long is a piece of string?. Journal of Economic Entomology 105, 11151129.Google Scholar
Zaviezo, T. & Mills, N. (2000) Factors influencing the evolution of clutch size in a gregarious insect parasitoid. Journal of Animal Ecology 69, 10471057.Google Scholar