Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-14T05:59:47.077Z Has data issue: false hasContentIssue false
  • English
  • Français

Impact and oviposition behaviour of Ageniaspis fuscicollis (Hymenoptera: Encyrtidae), a polyembryonic parasitoid of the apple ermine moth, Yponomeuta malinellus (Lepidoptera: Yponomeutidae)

Published online by Cambridge University Press:  10 July 2009

U. Kuhlmann ,
D. Babendreier ,
T.S. Hoffmeister  and
N.J. Mills
U. Kuhlmann*
Affiliation:
CABI Bioscience Centre, 1 Rue des Grillons, CH-2800 Delémont, Switzerland
D. Babendreier
Affiliation:
CABI Bioscience Centre, 1 Rue des Grillons, CH-2800 Delémont, Switzerland
T.S. Hoffmeister
Affiliation:
Zoologisches Institut der Universität Kiel - Ökologie, Germany
N.J. Mills
Affiliation:
Center for Biological Control, University of California at Berkeley, USA
*
*Fax: +41 32 422 48 24 E-mail: u.kuhlmann@cabi.org
Get access Rights & Permissions [Opens in a new window]

Abstract

The distribution and extent of parasitism of the apple ermine moth Yponomeuta malinellus Zeller by the polyembyronic encyrtid parasitoid Ageniaspis fuscicollis (Dalman) were examined in a three year field study and related to oviposition behaviour in the laboratory. Ageniaspis fuscicollis attacks egg batches of its host and kills the final instar larvae, which feed gregariously from within tents. Host population densities in the field were low, from 1.5 to 2.2 tents per 100 leaf clusters, and parasitism increased from 7.8% to 18% over the three year period. Parasitism was independent of host density at the whole tree scale, but at the individual tent scale, the probability of a tent containing parasitized host larvae increased and percent parasitism decreased with the number of host larvae per tent. Observations on the oviposition behaviour of A. fuscicollis in the laboratory revealed that parasitoids distributed their eggs randomly within host egg batches. On average, they spent almost two hours on an egg batch and laid 44% of their egg load of 132 eggs into the first egg batch visited, leading to a mean of 1.4 eggs laid per host egg through frequent self-superparasitism of hosts. The percentage of eggs receiving one or more ovipositions was independent of the size of an egg batch, contradicting our field observations of inverse density dependence. Factors that might account for the differences in rates of parasitism and attack distributions between laboratory and field data are discussed.

Type
Original Articles
Information
Bulletin of Entomological Research , Volume 88 , Issue 6 , December 1998 , pp. 617 - 625
Copyright
Copyright © Cambridge University Press 1998

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.)

References

Affolter, F. & Carl, K.P. (1986) The natural enemies of the apple ermine moth, Yponomeuta mahnellus, in Europe: a literature review. 29 pp. Report of the Commonwealth Institute of Biological Control, Delemont, Switzerland.Google Scholar
Aleksidze, G.N. & Abashidze, E.D. (1983) Forecasting the harmfulness of the apple moth. Zashchita Rastenii 6, 27–28 (in Russian, English abstract).Google Scholar
Baggiolini, ML., Keller, E., Milaire, H.G. & Steiner, H. (1980) Visuelle Kontrollen xm Apfelanbau. 3. Aufl. 104 pp. France, Generalsekretariat IOBC/WPRS.Google Scholar
Bakker, K., van Alphen, J.J.M., van Batenburg, F.H.D., van der Hoeven, N., Nell, H.W., van Strien-van Liempt, W.T.F.H. & Turlings, T.C. (1985) The function of host discrimination and superparasitism in parasitoids. Oecologia 67, 572–576.CrossRefGoogle ScholarPubMed
Blackman, R.L. (1965) A review of the literature on Ageniaspis fuscicollis (Dalm.). 10 pp. Report of the Commonwealth Institute of Biological Control, Delemont, Switzerland.Google Scholar
Bouskila, A., Robertson, I.C., Robinson, M.E., Roitberg, B.D., Tenhumberg, B., Tyre, A.J. & van Randen, E. (1995) Submaximal oviposition rates in a mymarid parasitoid: choosiness should not be ignored. Ecology 76, 1990–1993.CrossRefGoogle Scholar
Braune, H.J. (1982) Einfluss der Gelegestruktur des Wirtes auf die Wirksamkeit ernes Eiparasiten von Spodoptera litura (F.) (Lepidoptera). Drosera 1982, 7–16.Google Scholar
Charnov, E.L. (1976) Optimal foraging, the marginal value theorem. Theoretical Population Biology 9, 129–136.CrossRefGoogle ScholarPubMed
Charnov, E.L. & Skinner, S.W. (1984) Evolution of host selection and clutch size in parasitoid wasps. Florida Entomologist 67, 5–21.CrossRefGoogle Scholar
Clausen, C.P. (1940) Entomophagous insects. 688 pp. New York, McGraw-Hill Book Co.Google Scholar
Comins, H.N. & Hassell, M.P. (1979) The dynamics of optimally foraging predators and parasitoids. Journal of Animal Ecology 48, 335–351.CrossRefGoogle Scholar
Corbett, A. & Rosenheim, J.A. (1996) Quantifying movement of a minute parasitoid, Anagrus epos (Hymenoptera: Mymaridae), using fluorescent dust marking and recapture. Biological Control 6, 35–44.CrossRefGoogle Scholar
Cronin, J.T & Strong, D.R. (1990) Density-independent parasitism among host patches by Anagrus delicatus (Hymenoptera: Mymaridae): experimental manipulation of hosts. Journal of Animal Ecology 59, 1019–1026.CrossRefGoogle Scholar
Cronin, J.T. & Strong, D.R. (1993) Substantially submaximal oviposition rates by a mymarid egg parasitoid in the laboratory and field. Ecology 74, 1813–1825.CrossRefGoogle Scholar
Dijkerman, J.M., de Groot, J.M.B. &Herrebout, W.M. (1986) The parasitoids of the genus Yponomeuta Latreille (Lepidoptera, Yponomeutidae) in the Netherlands. Proceedings of the Koninklijke Nederlandse Akademie van Wettenschappen Series C 89, 379–398.Google Scholar
Elliot, J.M. (1983) Some methods for the statistical analysis of samples of benthic invertebrates. Freshwater Biologists Association Publication 25, 2nd edn, 3rd. impr., Kendal, Titus Wilson.Google Scholar
Godfray, H.C.J. (1994) Parasitoids – behavioural and evolutionary ecology, 473 pp. Princeton, New Jersey, Princeton University Press.CrossRefGoogle Scholar
Hawkins, B.A. & Cornell, H.V. (1994) Maximum parasitism rates and successful biological control. Science 266, 1886.CrossRefGoogle ScholarPubMed
Hawkins, B.A., Thomas, M.B. & Hochberg, M.E. (1993) Refuge theory and biological control. Science 262, 1429–1432.CrossRefGoogle ScholarPubMed
Iwasa, Y., Suzuki, Y. & Matsuda, H. (1984) Theory of oviposition strategy of parasitoids, I. Effect of mortality and limited egg number. Theoretical Population Biology 26, 205–227.CrossRefGoogle ScholarPubMed
Junnikkala, E. (1960) Life history and insect enemies of Hyponomeuta mahnellus Zell. in Finland. Annales Zoologici Societatis Zoologicae Botamcae Fenmcae “Vanamo” 21, 3–44.Google Scholar
Kot, J. (1964) Experiments on the use of parasitic Hymenoptera for the control of Hyponomeuta malinellus L. (Lep.Hyponomeutidae). Polskie Pismo Entmologwzne 32, 35–36 (in Polish, English abstract).Google Scholar
Kuhlmann, U., Carl, K.P. & Mills, N.J. (1998) Quantifying the impact of insect predators and parasitoids on populations of the apple ermine moth, Yponomeuta malinellus (Lepidoptera: Yponomeutidae), in Europe. Bulletin of Entomological Research 88, 165–175.CrossRefGoogle Scholar
Lessells, C.M. (1985) Parasitoid foraging: should parasitism be density dependent? Journal of Animal Ecology 54, 27–41.CrossRefGoogle Scholar
Mamedov, Z.M. (1977) Intra-area colonisation of Ageniaspis. Zashchita Rastenu 4, 54 (in Russian, English abstract).Google Scholar
Marshal, P. (1904) Recherches sur la biologie et le dévelopment des hyménopteres parasites. 1. La polyembryonie specifique ou germinogonie. Archives de Zoology Expérimentalis et Générale 2, 257–335.Google Scholar
Martin, F. (1914) Zur Entwicklungsgeschichte des polyembryonalen Chalcidiers Ageniaspis (Encyrtus) fuscicollis. Zeitschrift f˙r Wissenschafthche Zoologie 110, 419–479.Google Scholar
Mills, N.J. & Getz, W.M. (1996) Modelling the biological control of insect pests: a review of host-parasitoid models. Ecological Modelling 92, 121–143.CrossRefGoogle Scholar
Murdoch, W.W. (1990) The relevance of pest-enemy models to biological control, pp 1–24 in Mackauer, M., Ehler, L.E. & Roland, J. (Eds) Critical issues in biological control. Andover, UK, Intercept.Google Scholar
Murdoch, W.W. & Briggs, C.J. (1996) Theory for biological control: recent developments. Ecology 77, 2001–2013.CrossRefGoogle Scholar
Nenon, J.P. & de Merleire, H. (1972) L'Hyponomeuta du pommier et son parasite Encyrtus fuscicollis. Phytoma 24, 24–26.Google Scholar
Ode, P.J. & Strand, M.R. (1995) Progeny and sex allocation decisions of the polyembryonie wasp Copidosoma flondanum. Journal of Animal Ecology 64, 213–224.CrossRefGoogle Scholar
Pacala, S. & Hassell, M.P. (1991) The persistence of host-parasitoid associations in patchy environments. II. Evaluation of field data. American Naturalist 138, 584–605.CrossRefGoogle Scholar
Puttler, B. (1974) Hypera postica and Bathyplectes curulionis: Encapsulation of parasite eggs by host larvae in Missouri and Arkansas. Environmental Entomology 3, 881–882.CrossRefGoogle Scholar
Rosenheim, J.A. & Mangel, M. (1994) Patch–leaving rules for parasitoids with imperfect host discrimination. Ecological Entomology 19, 374–380.CrossRefGoogle Scholar
Salt, G. (1961) Competition among insect parasitoids. Symposium of the Society of Experimental Biology 15, 96–119.Google Scholar
Sitenko, L.S. (1962) The biology of Ageniaspis fuscicollis Dalm. and measures to increase its efficiency in the area of Primorsk. Biologitshesky method borby s vrediteljami i boleznjami selskochoz. kultur Moskva 1, 114–137 (in Russian, English abstract).Google Scholar
Speirs, D.C., Sherratt, T.N. & Hubbard, S.F. (1991) Parasitoid diets: does superparasitism pay? Trends in Ecology and Evolution 6, 22–25.CrossRefGoogle ScholarPubMed
Strand, M.R. (1989a) Clutch size, sex ratio and mating by the polyembronic encyrtid Copidosoma flondanum (Hymenoptera: Encyrtidae). Florida Entomologist 72, 32–42.CrossRefGoogle Scholar
Strand, M.R. (1989b) Oviposition behaviour and progeny allocation of the polyembryonie wasp Copidosoma floridanum (Hymenoptera: Encyrtidae). Journal of Insect Behaviour 2, 355–369.CrossRefGoogle Scholar
Unruh, T.R., Congdon, B.D. & LaGasa, E. (1993) Yponomeuta malinellus Zeller (Lepidoptera: Yponomeutidae), a new immigrant pest of apples in the Northwest: phenology and distribution expansion, with notes on efficacy of natural enemies. Pan-Pacific Entomologist 69, 57–70.Google Scholar
van Alphen, J.J.M. & Nell, H.W. (1982) Superparasitism and host discrimination by Asobara tabida Nees (Braconidae: Alysiinae) and Leptopilina heterotoma (Cynipoidea: Eucoilidae). Netherlands Journal of Zoology 33, 497–514.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
van der Hoeven, N. & Hemerik, L. (1990) Superparasitism as an ESS: to reject or not to reject, that is the question. Journal of Theoretical Biology 146, 467–482.CrossRefGoogle ScholarPubMed
van Driesche, R.G. & Bellows, T.S. Jr (1996) Biological control. 539 pp. New York, Chapman & Hall.CrossRefGoogle Scholar
van Lenteren, J.C. (1981) Host discrimination by parasitoids. pp. 153–179 in Nordlund, D.A., Jones, R.L. & Lewis, W.J. (Eds) Semiochemicals. Their role in pest control. New York, John Wiley & Sons.Google Scholar
Visser, M.E. (1993) Adaptive self- and conspecific superparasitism in the solitary parasitoid Leptopilina heterotoma (Hymenoptera: Eucoilidae). Behavioural Ecology 4, 22–28.CrossRefGoogle Scholar
Visser, M.E., van Alphen, J.J.M. & Nell, H.W. (1992a) Adaptive superparasitism and patch time allocation in solitary parasitoids: the influence of pre-patch experience. Behavioural Ecology and Sociobiology 31, 163–171.CrossRefGoogle Scholar
Visser, M.E., van Alphen, J.J.M. & Hemerik, L. (1992b) Adaptive superparasitism and patch time allocation in solitary parasitoids: an ESS model. Journal of Animal Ecology 61, 93–101.CrossRefGoogle Scholar
Waage, J.K. & Mills, N.J. (1992) Biological control, pp. 412–30 in Crawley, M.J. (Ed.) Natural enemies: the population biology of predators, parasites and diseases. Oxford, Blackwell Scientific Publications.CrossRefGoogle Scholar
Waage, J.K. (1990) Ecological theory and the selection of biological control agents. pp. 135–157 in Mackauer, M., Ehler, L.E. & Roland, J. (Eds) Critical issues in biological control. Andover, Hampshire, Intercept.Google Scholar
Walde, S.J. & Murdoch, W.W. (1988) Spatial density dependence in parasitoids. Annual Review of Entomology 33, 441–466.CrossRefGoogle Scholar
Weisser, W.W. & Houston, A.I. (1993) Host discrimination in parasitic wasps: when is it advantageous? Functional Ecology 7, 27–39.CrossRefGoogle Scholar