Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-24T01:19:16.369Z Has data issue: false hasContentIssue false

INVITATION PAPER: C.P. Alexander Fund: HOST CHOICE BY APHIDIID PARASITOIDS (HYMENOPTERA: APHIDIIDAE): HOST RECOGNITION, HOST QUALITY, AND HOST VALUE

Published online by Cambridge University Press:  31 May 2012

M. Mackauer*
Affiliation:
Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, Canada V5A 1S6
J.P. Michaud
Affiliation:
Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, Canada V5A 1S6
W. Völkl
Affiliation:
Department of Animal Ecology I, University of Bayreuth, D-95440 Bayreuth, Germany
*
1 Author to whom reprint requests should be sent.

Abstract

Species in the family Aphidiidae (Hymenoptera) parasitize exclusively ovoviviparous aphids. Females use a variety of information to detect and evaluate suitable hosts. Olfactory cues associated with aphids, or the aphids’ host plant, are important for host location. Visual cues including aphid colour, shape, and movement can be evaluated from a distance without physical contact; aphid movement may act as a releasing stimulus for attack. Contact chemosensory cues (gustatory cues) are evaluated by antennation of the host cuticle and during ovipositor probing. A potential host must conform to the wasp’s response profile and satisfy minimum physiological and dietary requirements for immature development and growth. Host quality is determined in part by attributes specific to each aphid species and in part by each aphid’s individual-specific growth potential. Host quality for male and female progeny may vary as a result of different patterns of resource allocation and sexual size dimorphism. For an encountered aphid to be accepted as a host, its perceived value must exceed the wasp’s response threshold for oviposition. Host value, as opposed to host quality, varies dynamically with parasitoid state variables such as age, egg load, and prior experience. A conceptual model of host choice by aphidiid wasps is presented.

Résumé

Les espèces de la famille des Aphidiidae (Hymenoptera) parasitent exclusivement les pucerons ovovivipares. Les femelles utilisent un grand nombre d’indices pour détecter et évaluer les hôtes acceptables. Les indices olfactifs associés aux pucerons, ou à la plante hôte des pucerons, jouent un rôle important dans la détection des hôtes. Les indices visuels, couleur, forme et déplacements des pucerons, peuvent servir même à distance, sans qu’il y ait contact physique avec les hôtes; les déplacements des pucerons peuvent agir comme stimuli déclencheurs de l’attaque des hôtes. Les indices chimiosensoriels de contact (indices gustatifs) sont évalués par contact des antennes avec la cuticule de l’hôte et par sondage au moyen de l’oviscapte. L’hôte potentiel doit correspondre au profil de réaction de la guêpe et satisfaire un minimum de conditions physiologiques et alimentaires nécessaires au développement et à la croissance des larves. La qualité des hôtes est déterminée en partie par les caractéristiques spécifiques à chaque espèce de puceron et en partie par le potentiel de croissance spécifique à chaque individu. La qualité de l’hôte comme support de la progéniture mâle et femelle peut varier selon les différents modes d’allocation des ressources et le dimorphisme sexuel de la taille. Pour qu’un puceron soit accepté comme hôte, sa valeur perçue doit excéder le seuil de réaction de ponte de la guêpe. La valeur de l’hôte, contrairement à la qualité de l’hôte, varient de façon dynamique en fonction des variables reliées à la condition, à l’âge, à la quantité d’oeufs, à l’expérience préalable. Un modèle conceptuel du choix d’un hôte par les guêpes aphidiidées est présenté.

[Traduit par la Rédaction]

Type
Articles
Copyright
Copyright © Entomological Society of Canada 1996

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

Antolin, M.F. 1989. Genetic considerations in the study of attack behavior of parasitoids, with reference to Muscidifurax raptor (Hymenoptera: Pteromalidae). Florida Entomologist 72: 1532.CrossRefGoogle Scholar
Bai, B., and Mackauer, M.. 1992. Influence of superparasitism on development rate and adult size in a solitary parasitoid wasp, Aphidius ervi. Functional Ecology 6: 302307.CrossRefGoogle Scholar
Battaglia, D., Pennacchio, F., Marincola, G., and Tranfaglia, A.. 1993. Cornicle secretion of Acyrthosiphon pisum (Homoptera: Aphididae) as a contact kairomone for the parasitoid Aphidius ervi (Hymenoptera: Braconidae). European Journal of Entomology 90: 423428.Google Scholar
Battaglia, D., Pennacchio, F., Romano, A., and Tranfaglia, A.. 1995. The role of physical cues in the regulation of host recognition and acceptance behavior of Aphidius ervi Haliday (Hymenoptera: Braconidae). Journal of Insect Behavior 8: 739750.CrossRefGoogle Scholar
Bell, W.J. 1991. Searching Behaviour. The Behavioural Ecology of Finding Resources. Chapman and Hall, London. 358 pp.Google Scholar
Bouchard, Y., and Cloutier, C.. 1984. Honeydew as a source of host-searching kairomones for the aphid parasitoid Aphidius nigripes (Hymenoptera: Aphidiidae). Canadian Journal of Zoology 62: 15131520.CrossRefGoogle Scholar
Bouchard, Y., and Cloutier, C.. 1985. Role of olfaction in host finding by aphid parasitoid Aphidius nigripes (Hymenoptera: Aphidiidae). Journal of Chemical Ecology 11: 801808.CrossRefGoogle Scholar
Braimah, H., and van Emden, H.F.. 1994. The role of the plant in host acceptance by the parasitoid Aphidius rhopalosiphi (Hymenoptera: Braconidae). Bulletin of Entomological Research 84: 303306.CrossRefGoogle Scholar
Budenberg, W.J. 1990. Honeydew as a contact kairomone for aphid parasitoids. Entomologia Experimentalis et Applicata 55: 139148.CrossRefGoogle Scholar
Budenberg, W.J., Powell, W., and Clark, S.J.. 1992. The influence of aphids and honeydew on the leaving rate of searching aphid parasitoids from wheat plants. Entomologia Experimentalis et Applicata 63: 259264.CrossRefGoogle Scholar
Calvert, D.J. 1973. Experimental host preferences of Monoctonus paulensis (Hymenoptera: Braconidae), including a hypothetical scheme of host selection. Annals of the Entomological Society of America 66: 2833.CrossRefGoogle Scholar
Calvert, D.J., and van den Bosch, R.. 1972. Behavior and biology of Monoctonus paulensis (Hymenoptera: Braconidae), a parasite of dactynotine aphids. Annals of the Entomological Society of America 65: 773779.CrossRefGoogle Scholar
Charnov, E.L., Los-den-Hartogh, R.L., Jones, W.T., and van den Assem, J.. 1981. Sex ratio evolution in a variable environment. Nature (London) 289: 2733.CrossRefGoogle Scholar
Chow, A., and Mackauer, M.. 1991. Patterns of host selection by four species of aphidiid (Hymenoptera) parasitoids: Influence of host switching. Ecological Entomology 16: 403410.CrossRefGoogle Scholar
Chow, A., and Mackauer, M.. 1992. The influence of prior ovipositional experience on host selection in four species of aphidiid wasps (Hymenoptera: Aphidiidae). Journal of Insect Behavior 5: 99108.CrossRefGoogle Scholar
Chow, F.J., and Mackauer, M.. 1986. Host discrimination and larval competition in the aphid parasite Ephedrus californicus Baker. Entomologia Experimentalis et Applicata 41: 243254.CrossRefGoogle Scholar
Cloutier, C., and Bauduin, F.. 1990. Searching behavior of the aphid parasitoid Aphidius nigripes (Hymenoptera: Aphidiidae) foraging on potato plants. Environmental Entomology 19: 222228.CrossRefGoogle Scholar
Cloutier, C., Dohse, L.A., and Bauduin, F.. 1984. Host discrimination in the aphid parasitoid Aphidius nigripes. Canadian Journal of Zoology 62: 13671372.CrossRefGoogle Scholar
Cloutier, C., Lévesque, C.A., Eaves, D.M., and Mackauer, M.. 1991. Maternal adjustment of sex ratio in response to host size in the aphid parasitoid Ephedrus californicus. Canadian Journal of Zoology 69: 14891495.CrossRefGoogle Scholar
Cloutier, C., and Mackauer, M.. 1979. The effect of parasitism by Aphidius smithi (Hymenoptera: Aphidiidae) on the food budget of the pea aphid, Acyrthosiphon pisum (Homoptera: Aphididae). Canadian Journal of Zoology 57: 16051611.CrossRefGoogle Scholar
Cloutier, C., and Mackauer, M.. 1980. The effect of superparasitism by Aphidius smithi (Hymenoptera: Aphidiidae) on the food budget of the pea aphid, Acyrthosiphon pisum (Homoptera: Aphididae). Canadian Journal of Zoology 58: 241244.CrossRefGoogle Scholar
Collins, M.D., and Dixon, A.F.G.. 1986. The effect of egg depletion on the foraging behaviour of an aphid parasitoid. Journal of Applied Entomology 102: 342352.CrossRefGoogle Scholar
Courtney, S.P., Chen, G.K., and Gardner, A.. 1989. A general model for individual host selection. Oikos 55: 5565.CrossRefGoogle Scholar
Courtney, S.P., and Kibota, T.T.. 1990. Mother doesn't know best: Selection of hosts by ovipositing insects. pp. 161–188 in Bernays, E.A. (Ed.), Insect–Plant Interactions, Vol. II. CRC Press, Boca Raton, FL. 199 pp.Google Scholar
Danyk, T.P., and Mackauer, M.. 1993. Discrimination between self- and conspecific-parasitized hosts in the aphid parasitoid Praon pequodorum Viereck (Hymenoptera: Aphidiidae). The Canadian Entomologist 125: 957964.CrossRefGoogle Scholar
Donaldson, J.S., and Walter, G.H.. 1984. Sex ratios of Spalangia endius (Hymenoptera: Pteromalidae), in relation to current theory. Ecological Entomology 9: 395402.CrossRefGoogle Scholar
Doutt, R.L. 1959. The biology of parasitic Hymenoptera. Annual Review of Entomology 4: 161182.CrossRefGoogle Scholar
Evans, G.A., Polaszek, A., and Bennett, F.D.. 1995. The taxonomy of the Encarsia flavocsutellum species-group (Hymenoptera: Aphelinidae) parasitoids of Hormaphididae (Homoptera: Aphidoidea). Oriental Insects 29: 3345.CrossRefGoogle Scholar
Fletcher, J.P., Hughes, J.P., and Harvey, I.F.. 1994. Life expectancy and egg load affect oviposition decisions of a solitary parasitoid. Proceedings of the Royal Society (London), B 258: 163167.Google ScholarPubMed
Gardner, S.M., and Dixon, A.F.G.. 1985. Plant structure and the foraging success of Aphidius rhopalosiphi (Hymenoptera: Aphidiidae). Ecological Entomology 10: 171179.CrossRefGoogle Scholar
Gauld, I., and Bolton, B. (Eds.). 1988. The Hymenoptera. Oxford University Press, Oxford. 332 pp.Google Scholar
Gerling, D., Roitberg, B.D., and Mackauer, M.. 1990. Instar-specific defense of the pea aphid, Acyrthosiphon pisum: Influence on oviposition success of the parasite Aphelinus asychis (Hymenoptera: Aphelinidae). Journal of Insect Behavior 3: 501514.CrossRefGoogle Scholar
Godfray, H.C.J. 1994. Parasitoids. Behavioral and Evolutionary Ecology. Princeton University Press, Princeton, NJ. 473 pp.Google Scholar
Godfray, H.C.J., and Hardy, I.C.W.. 1993. Sex ratio and virginity in haplodiploid insects. pp. 402–417 in Wrensch, D.C., and Ebbert, M.A. (Eds.), Evolution and Diversity of Sex Ratio in Insects and Mites. Chapman and Hall, New York, NY. 630 pp.Google Scholar
Goff, A.M., and Nault, L.R.. 1984. Response of the pea aphid parasite Aphidius ervi Haliday (Hymenoptera: Aphidiidae) to transmitted light. Environmental Entomology 13: 595598.CrossRefGoogle Scholar
Grasswitz, T.R., and Paine, T.D.. 1992. Kairomonal effect of an aphid cornicle secretion on Lysiphlebus testaceipes (Cresson) (Hymenoptera: Aphidiidae). Journal of Insect Behavior 5: 447457.CrossRefGoogle Scholar
Cloutier, C., and Mackauer, M.. 1993 a. Influence of physiological state and experience on the responsiveness of Lysiphlebus testaceipes (Cresson) (Hymenoptera: Aphidiidae) to aphid honeydew and to host plants. Journal of Insect Behavior 6: 511528.Google Scholar
Cloutier, C., and Mackauer, M.. 1993 b. Effect of experience on in-flight orientation to host-associated cues in the generalist parasitoid Lysiphlebus testaceipes. Entomologia Experimentalis et Applicata 68: 219229.Google Scholar
Griffiths, D.C. 1960. The behaviour and specificity of Monoctonus paludum Marshall (Hym., Braconidae), a parasite of Nasonovia ribis-nigri (Mosley) on lettuce. Bulletin of Entomological Research 51: 303319.CrossRefGoogle Scholar
Griffiths, D.C. 1961. The development of Monoctonus paludum Marshall (Hym., Braconidae), a parasite of Nasonovia ribis-nigri (Mosley) on lettuce. Bulletin of Entomological Research 52: 147163.CrossRefGoogle Scholar
Guerrieri, E., Pennacchio, F., and Tremblay, E.. 1993. Flight behaviour of the aphid parasitoid Aphidius ervi (Hymenoptera: Braconidae) in response to plant and host volatiles. European Journal of Entomology 90: 415421.Google Scholar
Hacker, S.D., and Bertness, M.D.. 1994. A herbivore paradox: Why salt marsh aphids live on poor-quality plants. American Naturalist 145: 192210.CrossRefGoogle Scholar
Hagvar, E.B., and Hofsvang, T.. 1989. Effect of honeydew on plant colonization by the aphid parasitoid Ephedrus cerasicola. Entomophaga 34: 495501.CrossRefGoogle Scholar
Hardie, J., Hick, A.J., Höller, C., Mann, J., Merritt, L., Nottingham, S.F., Powell, W., Wadhams, L.J., Witthinrich, J., and Wright, A.F.. 1994. The response of Praon spp. parasitoids to aphid sex pheromone components in the field. Entomologia Experimentalis et Applicata 71: 9599.CrossRefGoogle Scholar
Hardie, J., Nottingham, S.F., Powell, W., and Wadhams, L.J.. 1991. Synthetic aphid sex pheromone lures female parasitoids. Entomologia Experimentalis et Applicata 61: 9799.CrossRefGoogle Scholar
Heie, O.E. 1987. Palaeontology and phylogeny. pp. 367–391 in Minks, A.K., and Harrewijn, P. (Eds.), Aphids, their Biology, Natural Enemies and Control. World Crop Pests, Vol. 2A. Elsevier, Amsterdam. 450 pp.Google Scholar
Hille Ris Lambers, D. 1966. Polymorphism in Aphididae. Annual Review of Entomology 11: 4778.CrossRefGoogle Scholar
Hofsvang, T. 1988. Mechanisms of host discrimination and intraspecific competition in the aphid parasitoid Ephedrus cerasicola. Entomologia Experimentalis et Applicata 48: 233239.CrossRefGoogle Scholar
Höller, C., Borgemeister, C., Haardt, H., and Powell, W.. 1993. The relationship between primary parasitoids and hyperparasitoids of cereal aphids: An analysis of field data. Journal of Animal Ecology 62: 1221.CrossRefGoogle Scholar
Horn, D.J. 1984. Vegetational complexity and parasitism of green peach aphids (Myzus persicae (Sulzer) (Homoptera: Aphididae)) on collards. Journal of the New York Entomological Society 92: 1926.Google Scholar
Iwasa, Y., Suzuki, Y., and Matsuda, H.. 1984. Theory of oviposition strategy of parasitoids. I. Effect of mortality and limited egg number. Theoretical Population Biology 26: 205227.CrossRefGoogle ScholarPubMed
Kindlmann, P., and Ruzicka, Z.. 1992. Possible consequences of a specific interaction between predators and parasites of aphids. Ecological Modelling 61: 253265.CrossRefGoogle Scholar
Klingauf, F. 1967. Abwehr- und Meidereaktionen von Blattläusen (Aphididae) bei Bedrohung durch Räuber und Parasiten. Zeitschrift für Angewandte Entomologie 60: 269317.CrossRefGoogle Scholar
Kouamé, K.L., and Mackauer, M.. 1991. Influence of aphid size, age and behaviour on host choice by the parasitoid wasp Ephedrus californicus: A test of host-size models. Oecologia 88: 197203.CrossRefGoogle ScholarPubMed
Kouamé, K.L., and Mackauer, M.. 1992. Influence of starvation on development and reproduction in apterous virginoparae of the pea aphid, Acyrthosiphon pisum. The Canadian Entomologist 124: 8795.CrossRefGoogle Scholar
Lewis, T., and Taylor, L.R.. 1965. Diurnal periodicity of flight by insects. Transactions of the Royal Entomological Society (London) 116: 393479.CrossRefGoogle Scholar
Lewis, W.J., and Tumlinson, J.H.. 1988. Host detection by chemically mediated associative learning in a parasitic wasp. Nature (London) 331: 257259.CrossRefGoogle Scholar
Lewis, W.J., Tumlinson, J.H., and Krasnoff, S.. 1991. Chemically mediated associative learning: An important function in the foraging behavior of Microplitis croceipes (Cresson). Journal of Chemical Ecology 17: 13091325.CrossRefGoogle Scholar
Lewis, W.J., Vet, L.E.M., Tumlinson, J.H., van Lenteren, J.C., and Papaj, D.R.. 1990. Variations in parasitoid foraging behavior: Essential element of a sound biological control theory. Environmental Entomology 19: 11831193.CrossRefGoogle Scholar
Li, C., Roitberg, B.D., and Mackauer, M.. 1992. The search pattern of a parasitoid wasp, Aphelinus asychis, for its host. Oikos 65: 207212.CrossRefGoogle Scholar
Li, C., Roitberg, B.D., and Mackauer, M.. 1993. Patch residence time and parasitism of Aphelinus asychis: A simulation model. Ecological Modelling 69: 227241.CrossRefGoogle Scholar
Liepert, C., and Dettner, K.. 1993. Recognition of aphid parasitoids by honeydew-collecting ants: The role of cuticular lipids in a chemical mimicry system. Journal of Chemical Ecology 19: 21432153.CrossRefGoogle Scholar
Liu, S.S., Morton, R., and Hughes, R.D.. 1984. Oviposition preferences of a hymenopterous parasite for certain instars of its aphid host. Entomologia Experimentalis et Applicata 35: 249254.Google Scholar
Lopez, E.R., Van Driesche, R.G., and Elkinton, J.S.. 1990. Rates of parasitism by Diaeretiella rapae (Hymenoptera: Braconidae) for cabbage aphids (Homoptera: Aphididae) in and outside of colonies: Why do they differ? Journal of the Kansas Entomological Society 63: 158165.Google Scholar
Luck, R.F., Stouthamer, R., and Nunney, E.P.. 1993. Sex determination and sex ratio patterns in parasitic Hymenoptera. pp. 442–476 in Wrensch, D.C., and Ebbert, M.A. (Eds.), Evolution and Diversity of Sex Ratio in Insects and Mites. Chapman and Hall, New York, NY. 630 pp.Google Scholar
Mackauer, M. 1965. Parasitological data as an aid in aphid classification. The Canadian Entomologist 97: 10161024.CrossRefGoogle Scholar
Mackauer, M. 1976. The sex ratio in field populations of some aphid parasites. Annals of the Entomological Society of America 69: 453456.CrossRefGoogle Scholar
Mackauer, M. 1990. Host discrimination and larval competition in solitary endoparasitoids. pp. 41–62 in Mackauer, M., Ehler, L.E., and Roland, J. (Eds.), Critical Issues in Biological Control. Intercept, Andover, Hants. 330 pp.Google Scholar
Mackauer, M. 1996. Sexual size dimorphism in solitary parasitoid wasps: Influence of host quality. Oikos 76: 265272.CrossRefGoogle Scholar
Mackauer, M., Bai, B., Chow, A., and Danyk, T.. 1992. Asymmetric larval competition between two species of solitary parasitoid wasps: The influence of superparasitism. Ecological Entomology 17: 233236.CrossRefGoogle Scholar
Mackauer, M., and Chow, F.J.. 1986. Parasites and parasite impact on aphid populations. pp. 95–117 in McLean, G.D., Garret, R.G., and Ruesink, W.G. (Eds.), Plant Virus Epidemics: Monitoring, Modelling and Predicting Outbreaks. Academic Press, Sydney. 550 pp.Google Scholar
Mackauer, M., and Foottit, R.. 1979. A gall midge, Endaphis sp. (Diptera: Cecidomyiidae), as a gregarious aphid parasite. The Canadian Entomologist 111: 615620.CrossRefGoogle Scholar
Mackauer, M., and Kambhampati, S.. 1988. Parasitism of aphid embryos by Aphidius smithi: Some effects of extremely small host size. Entomologia Experimentalis et Applicata 49: 167173.CrossRefGoogle Scholar
Mackauer, M., and Sequeira, R.. 1993. Patterns of development in insect parasites. pp. 1–23 in Beckage, N.E., Thompson, S.N., and Federici, B.A. (Eds.), Parasites and Pathogens of Insects, Vol. 1: Parasites. Academic Press, Orlando, FL. 364 pp.Google Scholar
Mackauer, M., Sequeira, R., and Otto, M.. 1997. Growth and development in parasitoid wasps: Adaptation to variable host resources. In Dettner, K., Bauer, G., and Völkl, W. (Eds.), Vertical Food Web Interactions: Evolutionary Patterns and Driving Forces. Ecological Studies, Springer-Verlag, Heidelberg. In press.Google Scholar
Mackauer, M., and Starý, P.. 1967. World Aphidiidae (Hym. Ichneumonoidea). Le François, Paris. 195 pp.Google Scholar
Mackauer, M., and Völkl, W.. 1993. Regulation of aphid populations by aphidiid wasps: Does parasitoid foraging behaviour or hyperparasitism limit impact? Oecologia 94: 339350.CrossRefGoogle ScholarPubMed
Mangel, M. 1989. Evolution of host selection in parasitoids: Does the state of the parasitoid matter? American Naturalist 133: 688705.CrossRefGoogle Scholar
Mangel, M., and Clark, C.W.. 1988. Dynamic Modeling in Behavioral Ecology. Princeton University Press, Princeton, NJ. 308 pp.Google Scholar
McBrien, H., and Mackauer, M.. 1990. Heterospecific larval competition and host discrimination in two species of aphid parasitoids: Aphidius ervi and Aphidius smithi. Entomologia Experimentalis et Applicata 56: 145153.CrossRefGoogle Scholar
McBrien, H., and Mackauer, M.. 1991. Decision to superparasitize based on larval survival: Competition between aphid parasitoids Aphidius ervi and Aphidius smithi. Entomologia Experimentalis et Applicata 59: 145150.CrossRefGoogle Scholar
McGregor, R., and Mackauer, M.. 1989. Toxicity of carbaryl to the pea-aphid parasite Aphidius smithi: Influence of behaviour on pesticide uptake. Crop Protection 8: 193196.CrossRefGoogle Scholar
Michaud, J.P. 1994. Differences in foraging behaviour between virgin and mated aphid parasitoids (Hymenoptera: Aphidiidae). Canadian Journal of Zoology 72: 15971602.CrossRefGoogle Scholar
Michaud, J.P. 1995. Static and Dynamic Criteria in Host Evaluation by Aphid Parasitoids (Hymenoptera: Aphidiidae). Ph.D. thesis, Simon Fraser University, Burnaby, British Columbia. 150 pp.Google Scholar
Michaud, J.P. 1996. The oviposition behavior of Aphidius ervi and Monoctonus paulensis (Hymenoptera: Aphidiidae) encountering different host species (Homoptera: Aphididae) in sequential patches. Journal of Insect Behavior. In press.CrossRefGoogle Scholar
Michaud, J.P., and Mackauer, M.. 1994. The use of visual cues in host evaluation by aphidiid wasps. I. Comparison between three Aphidius parasitoids of the pea aphid. Entomologia Experimentalis et Applicata 70: 273283.CrossRefGoogle Scholar
Michaud, J.P., and Mackauer, M.. 1995 a. The use of visual cues in host evaluation by aphidiid wasps. II. Comparison between Ephedrus californicus, Monoctonus paulensis, and Praon pequodorum. Entomologia Experimentalis et Applicata 74: 267275.CrossRefGoogle Scholar
Michaud, J.P., and Mackauer, M.. 1995 b. Oviposition behavior of Monoctonus paulensis (Hymenoptera: Aphidiidae): Factors influencing reproductive allocation to hosts and host patches. Annals of the Entomological Society of America 88: 220226.CrossRefGoogle Scholar
Miller, J.R., and Strickler, K.. 1984. Finding and accepting host plants. pp. 127–157 in Bell, W.J., and Cardé, R.T. (Eds.), Chemical Ecology of Insects. Sinauer Associates, Sunderland, MA. 524 pp.Google Scholar
Miyazaki, M. 1987. Forms and morphs of aphids. pp. 27–50 in Minks, A.K., and Harrewijn, P. (Eds.), Aphids. Their Biology, Natural Enemies and Control. World Crop Pests, Vol. 2A. Elsevier, Amsterdam. 450 pp.Google Scholar
Ojayi, O., and Dewar, A.M.. 1982. The effect of barley yellow dwarf virus on honeydew production by the cereal aphids, Sitobion avenae and Metopolophium dirhodum. Annals of Applied Biology 100: 203212.CrossRefGoogle Scholar
Papaj, D.R., and Vet, L.E.M.. 1990. Odor learning and foraging success in the parasitoid, Leptopilina heterotoma. Journal of Chemical Ecology 16: 31373150.CrossRefGoogle ScholarPubMed
Polgár, L., Mackauer, M., and Völkl, W.. 1991. Diapause induction in two species of aphid parasitoids: The influence of aphid morph. Journal of Insect Physiology 37: 699702.CrossRefGoogle Scholar
Powell, W., and Wright, A.F.. 1992. The influence of host food plants on host recognition by four aphidiine parasitoids (Hymenoptera: Braconidae). Bulletin of Entomological Research 81: 449453.CrossRefGoogle Scholar
Powell, W., and Zhang, Z.L.. 1983. The reactions of two cereal aphid parasitoids, Aphidius uzbekistanicus and A. ervi, to host aphids and their food plants. Physiological Entomology 8: 439443.CrossRefGoogle Scholar
Pungerl, N. 1984. Host preferences of Aphidius (Hymenoptera: Aphidiidae) populations parasitising pea and cereal aphids (Hemiptera: Aphididae). Bulletin of Entomological Research 74: 153161.CrossRefGoogle Scholar
Read, D.P., Feeny, P.P., and Root, R.B.. 1970. Habitat selection by the aphid parasite Diaeretiella rapae (Hymenoptera: Braconidae) and hyperparasite Charips hrassicae (Hymenoptera: Cynipidae). The Canadian Entomologist 102: 15671578.CrossRefGoogle Scholar
Roitberg, B.D. 1990. Variation in behaviour of individual parasitic insects: Bane or boon? pp. 25–39 in Mackauer, M., Ehler, L.E., and Roland, J. (Eds.), Critical Issues in Biological Control. Intercept, Andover, Hants. 330 pp.Google Scholar
Rosenheim, J.A., Kaya, H.K., Ehler, L.E., Marois, J.A., and Jaffee, B.A.. 1995. Intraguild predation among biological-control agents: Theory and evidence. Biological Control 5: 303335.CrossRefGoogle Scholar
Saxena, K.N., and Khattar, P.. 1977. Orientation of Papilio demoleus larvae in relation to size, distance, and combination patterns of visual stimuli. Proceedings of the Royal Society (London), B 122: 5775.Google Scholar
Sequeira, R., and Mackauer, M.. 1987. Host instar preference of the aphid parasite Praon pequodorum (Hymenoptera: Aphidiidae). Entomologia Generalis 12: 259265.CrossRefGoogle Scholar
Sequeira, R., and Mackauer, M.. 1992 a. Nutritional ecology of an insect host–parasitoid association: The pea aphid – Aphidius ervi system. Ecology 73: 183189.CrossRefGoogle Scholar
Sequeira, R., and Mackauer, M.. 1992 b. Covariance of adult size and development time in the parasitoid wasp Aphidius ervi in relation to the size of its host, Acyrthosiphon pisum. Evolutionary Ecology 6: 3444.CrossRefGoogle Scholar
Sequeira, R., and Mackauer, M.. 1993 a. The nutritional ecology of a parasitoid wasp, Ephedrus californicus Baker (Hymenoptera: Aphidiidae). The Canadian Entomologist 125: 423430.CrossRefGoogle Scholar
Sequeira, R., and Mackauer, M.. 1993 b. Seasonal variation in body size and offspring sex ratio in field populations of the parasitoid wasp, Aphidius ervi (Hymenoptera: Aphidiidae). Oikos 68: 340346.CrossRefGoogle Scholar
Sequeira, R., and Mackauer, M.. 1994. Variation in selected life-history parameters of the parasitoid wasp, Aphidius ervi: Influence of host developmental stage. Entomologia Experimentalis et Applicata 71: 1522.CrossRefGoogle Scholar
Shaw, M.R. 1994. Parasitoid host ranges. pp. 111–144 in Hawkins, B.A., and Sheehan, W. (Eds.), Parasitoid Community Ecology. Oxford University Press, Oxford. 516 pp.Google Scholar
Singh, R., and Sinha, T.B.. 1980. Bionomics of Trioxys (Binodoxys) indicus Subba Rao & Sharma, an aphidiid parasitoid of Aphis craccivora. VII. Sex ratio of the parasitoid in field populations. Entomon 4: 269275.Google Scholar
Singh, R., and Sinha, T.B.. 1982. Bionomics of Trioxys (Binodoxys) indicus Subba Rao & Sharma, an aphidiid parasitoid of Aphis craccivora. XIII. Host selection by the parasitoid. Zeitschrift für Angewandte Entomologie 93: 6475.CrossRefGoogle Scholar
Singh, R., and Srivastava, M.. 1987. Bionomics of Trioxys indicus Subba Rao & Sharma, an aphidiid parasitoid of Aphis craccivora Koch. 25. The role of host haemolymph in the host stage preference by the parasitoid. Giornale Italiana di Entomologia 3: 409412.Google Scholar
Srivastava, M., and Singh, R.. 1988. Bionomics of Trioxys indicus, an aphidiid parasitoid of Aphis craccivora. 26. Impact of host extract on the oviposition response of the parasitoid. Biology, Agriculture and Horticulture 5: 169176.CrossRefGoogle Scholar
Stadler, B., and Mackauer, M.. 1996. Influence of plant quality on interactions between the aphid parasitoid Ephedrus californicus (Hymenoptera: Aphidiidae) and its host, Acyrthosiphon pisum (Homoptera: Aphididae). The Canadian Entomologist 128: 2739.CrossRefGoogle Scholar
Stadler, B., and Völkl, W.. 1991. Foraging patterns of two aphid parasitoids, Lysiphlebus testaceipes and Aphidius colemani on banana. Entomologia Experimentalis et Applicata 58: 221229.CrossRefGoogle Scholar
Starý, P. 1970. Biology of Aphid Parasites. Series Entomologica, Vol. 6. Dr. W. Junk, The Hague. 643 pp.Google Scholar
Starý, P. 1988 a. Aphidiidae. pp. 171 – 184 in Minks, A.K., and Harrewijn, P. (Eds.), Aphids. Their Biology, Natural Enemies and Control. World Crop Pests, Vol. 2B. Elsevier, Amsterdam. 364 pp.Google Scholar
Starý, P. 1988 b. Aphelinidae. pp. 185–188 in Minks, A.K., and Harrewijn, P. (Eds.), Aphids. Their Biology, Natural Enemies and Control. World Crop Pests, Vol. 2B. Elsevier, Amsterdam. 364 pp.Google Scholar
Stechmann, D.H., Völkl, W., and Starý, P.. 1996. Ant-attendance as a critical factor in the biological control of the banana aphid Pentalonia nigronervosa Coq. (Hom. Aphididae) in Oceania. Journal of Applied Entomology 120: 119123.CrossRefGoogle Scholar
Stephens, D.W., and Krebs, J.R.. 1986. Foraging Theory. Princeton University Press, Princeton, NJ. 247 pp.Google Scholar
Sullivan, D.J. 1988. Hyperparasites. pp. 189–203 in Minks, A.K., and Harrewijn, P. (Eds.), Aphids. Their Biology, Natural Enemies and Control. World Crop Pests, Vol. 2B. Elsevier, Amsterdam. 364 pp.Google Scholar
Tagawa, J. 1987. Post-mating changes in the oviposition tactics of the parasitic wasp, Apanteles glomeratus L. (Hymenoptera: Braconidae). Applied Entomology and Zoology 22: 537542.CrossRefGoogle Scholar
Takada, H., and Hashimoto, Y.. 1985. Association of the root aphid parasitoids Aclitus sappaphis and Paralipsis eikoae (Hymenoptera, Aphidiidae) with the aphid-attending ants Pheidole fervida and Lasius niger (Hymenoptera, Formicidae). Kontu 53: 150160.Google Scholar
Tamaki, G., Annis, B., and Weiss, M.. 1981. Response of natural enemies to the green peach aphid in different plant cultures. Environmental Entomology 10: 375378.CrossRefGoogle Scholar
Tang, Y.Q., Yokomi, R.K., and Gagné, R.J.. 1994. Life history and description of Endaphis maculans (Diptera: Cecidomyiidae), an endoparasitoid of aphids in Florida and the Caribbean Basin. Annals of the Entomological Society of America 87: 523531.CrossRefGoogle Scholar
Tardieux, I., and Rabasse, J.M.. 1986. Host–parasite interrelationships in the case of Aphidius colemani. pp. 125–130 in Hodek, I. (Ed.), Ecology of Aphidophaga 2. Academia, Prague. 562 pp.Google Scholar
Thompson, J.N. 1988. Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomologia Experimentalis et Applicata 47: 314.CrossRefGoogle Scholar
Turlings, T.C.J., Scheepmaker, J.W.A., Vet, L.E.M., Tumlinson, J.H., and Lewis, W.J.. 1990. How contact foraging experiences affect preferences for host-related odors in the larval parasitoid Cotesia marginiventris (Cresson) (Hymenoptera: Braconidae). Journal of Chemical Ecology 16: 15771589.CrossRefGoogle Scholar
van Emden, H.F. 1995. Host plant – aphidophaga interactions. Agriculture, Ecosystems & Environment 52: 311.CrossRefGoogle Scholar
Vater, G. 1971. Über Ausbreitung und Orientierung von Diaeretiella rapae (Hymenoptera, Aphidiidae) unter Berücksichtigung der Hyperparasiten von Brevicoryne brassicae (Homoptera, Aphididae). Zeitschrift für Angewandte Entomologie 68: 187225.CrossRefGoogle Scholar
Vet, L.E.M., Lewis, W.J., Papaj, D.R., and van Lenteren, J.C.. 1990. A variable response model for parasitoid foraging behavior. Journal of Insect Behavior 3: 471490.CrossRefGoogle Scholar
Vinson, S.B. 1976. Host selection by insect parasitoids. Annual Revue of Entomology 21: 109133.CrossRefGoogle Scholar
Vinson, S.B., and Iwantsch, G.F.. 1980 a. Host regulation by insect parasitoids. Quarterly Review of Biology 55: 145165.CrossRefGoogle Scholar
Vinson, S.B., and Iwantsch, G.F.. 1980 b. Host suitability for insect parasitoids. Annual Review of Entomology 25: 397419.CrossRefGoogle Scholar
Völkl, W. 1991. Species-specific larval instar preferences and aphid defense behaviour in three parasitoids of Aphis fabae. pp. 73–78 in Polgár, L., Chambers, R.J., Dixon, A.F.G., and Hodek, I. (Eds.), Behaviour and Impact of Aphidophaga. SPB Academic, The Hague. 350 pp.Google Scholar
Völkl, W. 1992. Aphids or their parasitoids: Who actually benefits from ant-attendance? Journal of Animal Ecology 61: 273281.CrossRefGoogle Scholar
Völkl, W. 1994 a. Searching at different spatial scales: The foraging behaviour of the aphid parasitoid Aphidius rosae in rose bushes. Oecologia 100: 177183.CrossRefGoogle ScholarPubMed
Völkl, W. 1994 b. The effect of ant-attendance on the foraging behaviour of the aphid parasitoid Lysiphlebus cardui. Oikos 70: 149155.CrossRefGoogle Scholar
Völkl, W., and Kraus, W.. 1996. Foraging behaviour and resource utilization of the aphid parasitoid Pauesia unilachni: Adaptation to host distribution and mortality risk. Entomologia Experimentalis et Applicata 79: 101109.CrossRefGoogle Scholar
Völkl, W., Liepert, C., Birnbach, R., Hübner, G., and Dettner, K.. 1996. Chemical and tactile communication by the root aphid parasitoid Paralipsis enervis and trophobiotic ants: Consequences for parasitoid survival. Experientia 52: 731738.CrossRefGoogle Scholar
Völkl, W., and Mackauer, M.. 1990. Age-specific pattern of host discrimination by the aphid parasitoid Ephedrus californicus Baker (Hymenoptera: Aphidiidae). The Canadian Entomologist 122: 349361.CrossRefGoogle Scholar
Völkl, W., and Mackauer, M.. 1993. Interactions between ants and parasitoid wasps foraging for Aphis fabae ssp. cirsiiacanthoidis on thistles. Journal of Insect Behavior 6: 301312.CrossRefGoogle Scholar
Völkl, W., and Stadler, B.. 1996. Colony orientation and successful defense behaviour in the conifer aphid, Schizolachnus pineti. Entomologia Experimentalis et Applicata 78: 197200.CrossRefGoogle Scholar
Waage, J.K. 1986. Family planning in parasitoids: Adaptive patterns of progeny and sex allocation. pp. 63–95 in Waage, J., and Greathead, D. (Eds.), Insect Parasitoids. Academic Press, London. 389 pp.Google Scholar
Weisser, W.W. 1994. Age-dependent foraging behaviour and host-instar preference of the aphid parasitoid Lysiphlebus cardui. Entomologia Experimentalis et Applicata 70: 110.CrossRefGoogle Scholar
Weisser, W.W. 1995. Within-patch foraging behaviour of the aphid parasitoid Aphidius funebris: Plant architecture, host behaviour, and individual variation. Entomologia Experimentalis et Applicata 76: 133141.CrossRefGoogle Scholar
Weisser, W.W., and Houston, A.I.. 1993. Host discrimination in parasitic wasps: When is it advantageous? Functional Ecology 7: 2739.CrossRefGoogle Scholar
Weisser, W.W., Houston, A.I., and Voelkl, W.. 1994. Foraging strategies in solitary parasitoids: The trade-off between female and offspring mortality risks. Evolutionary Ecology 8: 587597.CrossRefGoogle Scholar
Wellings, P.W. 1993. Foraging behaviour in aphid parasitoids: Spatial scale and resource assessment. European Journal of Entomology 90: 377382.Google Scholar
Wickremasinghe, M.G.V., and van Emden, H.F.. 1992. Reactions of adult female parasitoids, particularly Aphidius rhopalosiphi, to volatile chemical cues from the host plants of their aphid prey. Physiological Entomology 17: 297304.CrossRefGoogle Scholar