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Parasitoid Foraging and Learning

  • Louise E. M. Vet
  • W. Joe Lewis
  • Ring T. Cardé

Abstract

The diminutive size of most parasitoids undoubtedly has limited their choice as subjects for behavioral study, despite their great diversity in lifestyles and reproductive strategies. The present chapter addresses their foraging behavior as influenced by learning. Most of their adult life female parasitoids search for host insects which, in turn, are under selection to avoid being found and devoured. This scenario sets the stage for the evolution of diverse hide-and-seek games played by parasitoids and their victims, most often herbivores. That parasitoids are successful in their quest for hosts is evidenced by the vast number of parasitoid species and their importance in insect management.

Keywords

Conditioned Stimulus Associative Learning Innate Response Larval Parasitoid Host Acceptance 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Alphen, J.J.M. van and Vet, L.E.M. (1986) An evolutionary approach to host finding and selection, in Insect Parasitoids, (eds J.K. Waage and D.J. Greathead), Acad. Press, London, pp. 23–61.Google Scholar
  2. Arthur, A.P. (1971) Associative learning by Nenteritis canescens (Hymenoptera: Ichneumonidae). Can. Entom. 103: 1137–1141.CrossRefGoogle Scholar
  3. Barton Browne, L. (1993) Physiologically induced changes in resource-oriented behavior. Annu. Rev. Entomol. 38: 1–25.CrossRefGoogle Scholar
  4. Bateson, P.P.G (1984) Genes, evolution and learning, in The Biology of Learning (eds P. Marler and H.S Terrace), Springer-Verlag, Berlin pp. 75–88.CrossRefGoogle Scholar
  5. Bell, W.J. (1990) Searching behavior patterns in insects. Annu. Rev. Entomol. 35: 447–467.CrossRefGoogle Scholar
  6. Bell, W.J. and Cardé, R.T. (eds) (1984) Chemical Ecology of Insects, Chapman & Hall, London.Google Scholar
  7. Carew, T.J., Abrams, T.W., Hawkins, R.D., and Kandel, E.R. (1984) in Primary Neural Substrates of Learning and Behavioural Change, (eds D.L. Alkon and J. Farley), Cambridge University Press, Cambridge, pp. 169–184.Google Scholar
  8. Clausen, C.P. (1976) Phoresy among entomophagous insects. Annu. Rev. Entomol. 21: 343–368.CrossRefGoogle Scholar
  9. Cornell, H. and Pimentel, D. (1978) Switching in the parasitoid Nasonia vitripennis and its effects on host competition. Ecology 59: 297–308.CrossRefGoogle Scholar
  10. De Jong, R. and Kaiser, L. (1991) Odor learning by Leptopilina boulardi, a specialist parasitoid (Hymenoptera: Eucoilidae). J. Insect Behav. 4: 743–750.CrossRefGoogle Scholar
  11. De Jong, R. and Kaiser, L. (1992) Odour preference of a parasitic wasp depends on order of learning. Experientia 48: 902–904.CrossRefGoogle Scholar
  12. Dicke, M. (1994) Local and systemic production of volatile herbivore-induced terpenoids: their role in plant-carnivore mutualism. J. Plant Physiol. 143: 465–472.CrossRefGoogle Scholar
  13. Dicke, M., Sabelis, M.W., Takabayashi, J., Bruin, J., Posthumus, M.A. (1990) Plant strategies of manipulating predator-prey interactions through allelochemicals: prospects for application in pest control. J. Chem. Ecol. 16: 3091–3118.CrossRefGoogle Scholar
  14. Dicke, M., Baarlen, P. van, Wessels, R., Dijkman, H. (1993) Herbivory induces systemic production of plant volatiles that attract herbivore predators: extraction of endogenous elicitor. J. Chem. Ecol. 19: 581–599.CrossRefGoogle Scholar
  15. Dicke, M. and Takabayashi, J. (1991) Specificity of induced indirect defence of plants against herbivores. Redia 74 (3) Append: 105–113.Google Scholar
  16. Driessen, G. and Hemerik, L. (1992) The time and egg budget of Leptopilina clavipes (Hartig), a larval parasitoid of Drosophila. Ecol. Entomol. 17: 17–27.CrossRefGoogle Scholar
  17. Drost, Y.C. and Cardé, R.T. (1990) Influence of experience on the sequential and temporal organization of host-acceptance behavior in Brachymeria intermedia (Chalcididae), an endoparasitoid of gypsy moth. J. Insect Behav. 3: 647–661.CrossRefGoogle Scholar
  18. Drost, Y.C. and Cardé, R.T. (1993a) Use of learned visual cues during habitat location by Brachymeria intermedia. Entomol. exp. appl. 64: 217–224.CrossRefGoogle Scholar
  19. Drost, Y.C. and Cardé, R.T. (1993b) Influence of host deprivation on egg load and oviposition behaviour of Brachymeria intermedia, a parasitoid of gypsy moth. Physiol. Entomol. 17: 230–234.CrossRefGoogle Scholar
  20. Drost, Y.C. and Cardé, R.T. (1993c) Host switching m Brachymeria intermedia (Hyme-noptera: Chalcididae), a pupal endoparasitoid of Lymantria dispar (Lepidoptera: Lyman-triidae). Environ. Entomol. 21: 760–766.Google Scholar
  21. Drost, Y.C., Lewis, W.J., Zanen, P.O., Keller, M. A. (1986) Beneficial arthropod behavior mediated by airborne semiochemicals. I. Flight behavior and influence of preflight handling of Microplitis croceipes (Cresson). J. Chem. Ecol. 12: 1247–1262.CrossRefGoogle Scholar
  22. Eller, F.J., Tumlinson, J.H., Lewis, W.J. (1992) Effect of host diet and preflight experience on the flight responses of Microplitis croceipes (Cresson). Physiol. Entomol. 17: 234–240.CrossRefGoogle Scholar
  23. Flanders, S.E. (1950) Regulation of ovulation and egg disposal in the parasitic Hymenoptera. Can. Entomol. 82: 134–140.CrossRefGoogle Scholar
  24. Garcia, J. and Garcia Y Robertson, R. (1985) The evolution of learning mechanisms. Amer. Psych. Assoc.: Master Lecture Series, 4: 191–243.Google Scholar
  25. Gardner, S.M. and Lenteren, J.C. van (1986) Characterisation of the arrestment responses of Trichogramma evanescens. Oecologia 68: 265–270.CrossRefGoogle Scholar
  26. Giessen van, W.A., Lewis, J., Vet, L.E.M., and Wäckers, F.L. (1993) The influence of host site experience on subsequent flight behaviour in Microplitis croceipes (Cresson) (Hymenoptera: Braconidae). Biol. Control 3: 75–79.CrossRefGoogle Scholar
  27. Godfray, H.C.J. (1987) The evolution of clutch size in invertebrates, in Oxford Surveys in Evolutionary Biology, 4, (eds. P. Harvey & L. Partridge), Oxford University Press, Oxford, pp. 117–154.Google Scholar
  28. Gould, J.L. (1993) Ethological and comparative perspectives on honey bee learning, in Insect Learning. Ecological and Evolutionary Aspects, (eds D.R. Papaj and A.C. Lewis), Chapman & Hall, New York, pp. 18–50.Google Scholar
  29. Gould J.L. and Marier, P. (1984) Ethology and the natural history of learning, in The Biology of Learning, (eds P. Marler and H.S. Terrace), Springer-Verlag, Berlin, pp. 47–74.CrossRefGoogle Scholar
  30. 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. J. Insect Behav. in press.Google Scholar
  31. Jaenike, J. and Papaj, D.R. (1992). Behavioral plasticity and patterns of host use by insects, in Insect Chemical Ecology, An Evolutionary Approach, (eds. B.D. Roitberg and M.B. Isman), Chapman & Hall, New York, pp. 245–264.Google Scholar
  32. Janssen, A. (1989) Optimal host selection by Drosophila parasitoids in the field. Func. Ecol. 3: 469–479.CrossRefGoogle Scholar
  33. Jervis, M.A., Kidd, N.A.C. (1986) Host-feeding strategies in Hymenopteran parasitoids. Biol. Rev. Camb. Phil. Soc. 61: 395–434.CrossRefGoogle Scholar
  34. Jones, R.L., Lewis, W.J., Beroza, M., Bierl, B.A., Sparks, A.N. (1973) Host seeking stimulants (kairomones) for the egg-parasite Trichogramma evanescens. Environ. Entomol. 2: 593–596.Google Scholar
  35. Jones, R.L., Lewis, W.J., Bowman, M.C., Beroza, M., Bierl, B.A. (1971) Host seeking stimulants for parasite of corn earworm: isolation, identification and synthesis. Science 173: 842–843.PubMedCrossRefGoogle Scholar
  36. Kaiser, L. and Cardé, R.T. (1992). In-flight orientation to volatiles from the plant host complex in Cotesia rubecula (Hym.: Braconidae): increased sensitivity through olfactory conditioning. Physiol. Entomol. 17: 62–67.CrossRefGoogle Scholar
  37. Kaiser, L., Pham-Delegue, M.H., Bakchine, E., Masson, C. (1989) Olfactory responses of Trichogramma maidis Pint, et Voeg.: effects of chemical cues and behavioral plasticity. J. Insect Behav. 2: 701–712.CrossRefGoogle Scholar
  38. Kaiser, L., Willis, M.A. and Cardé, R.T. (1994) Flight manoeuvers used by a parasitic wasp to locate host-infested plant. Entomol. exp. appl. 10: 285–294.CrossRefGoogle Scholar
  39. Kerguelen, V. and Cardé, R.T. (1995) Increased host acceptance in experienced females of the parasitoid Brachymeria intermedia: which oviposition behaviours contribute to experience, (unpublished study).Google Scholar
  40. Kester, K.M. and Barbosa, P. (1991) Behavioral and ecological constraints imposed by plants on insect parasitoids: implications for biological control. Biol. Control 1: 94–106.CrossRefGoogle Scholar
  41. Krebs, J.R. and Kacelnic, A. (1991) Decision-making, in Behavioural Ecology. An Evolutionary Approach, (eds J.R. Krebs and N.B. Davies), Blackwell Scientific Publications, Oxford, pp. 105–137.Google Scholar
  42. Lewis, W.J., Jones, R.L., Gross, H.R., Nordlund, D.A. (1976) The role of kairomones and other behavioral chemicals in host finding by parasitic insects. Behav. Biol. 16: 267–289.PubMedCrossRefGoogle Scholar
  43. Lewis, W.J., Jones, R.L., Sparks, A.N. (1972) A host seeking stimulant for the egg-parasite Trichogramma evanescens: its source and a demonstration of its laboratory and field activity. Ann. Entomol. Soc. Am. 65: 1087–1089.Google Scholar
  44. Lewis, W.J. and Martin, W.R. jr. (1990) Semiochemicals for use with parasitoids: status and future. J. Chem. Ecol. 16: 3067–3089.CrossRefGoogle Scholar
  45. Lewis, W.J., Nordlund, D.A., Gueldner, R.C., Teal, P.E.A., Tumlinson, J.H. (1982) Kairomones and their use for management of entomophagous insects. XIII. Kairomonal activity for Trichogramma spp. of abdominal tips, excretion, and a synthetic sex pheromone blend of Heliothis zea (Boddie) moths. J. Chem. Ecol. 8: 1323–1331.CrossRefGoogle Scholar
  46. Lewis, W.J. and Takasu, K. (1990) Use of learned odours by a parasitic wasp in accordance with host and food needs. Nature 348: 635–636.CrossRefGoogle Scholar
  47. Lewis, W.J. and Tumlinson, J.H. (1988) Host detection by chemically mediated associative learning in a parasitic wasp. Nature 331: 257–259.CrossRefGoogle Scholar
  48. Lewis, W.J., Tumlinson, J.H., Krasnoff, S. (1991) Chemically mediated associative learning: an important function in the foraging behavior of Microplitis croceipes (Cresson). J. Chem. Ecol. 17: 1309–1325.CrossRefGoogle Scholar
  49. Lewis, W.J., Vet, L.E.M., Tumlinson, J.H., Lenteren, J.C. van, Papaj, D.R. (1990) Variations in parasitoid foraging behavior: essential element of a sound biological control theory. Environ. Entomol. 19: 1183–1193.Google Scholar
  50. MacArthur, R.H. and Pianka, E.R. (1966) On optimal use of a patchy environment. Am. Nat. 916: 603–609.CrossRefGoogle Scholar
  51. Mandeville, J.D. and Mullens, B.A. (1990) Host species and size as factors in parasitism by Muscidifurax spp and Spalangia spp. (Hymenoptera: Pteromalidae) in the field. Ann. Entomol. Soc. Am. 83: 1074–1083.Google Scholar
  52. Mangel, M. (1992) Descriptions of superparasitism by optimal foraging theory, evolutionarily stable strategies and quantitative genetics. Evol. Ecol. 6: 152–169.CrossRefGoogle Scholar
  53. Mangel, M. (1993) Motivation, learning, and motivated learning, in Insect Learning. Ecological and Evolutionary Aspects, (eds D.R. Papaj and A.C. Lewis), Chapman & Hall, New York, pp. 158–173.Google Scholar
  54. Martin, W.R. and Lewis, W.J. (1995) Timing of host and host feces encounters: influence on learning and memory in the parasitoid Microplitis croceipes. (unpublished study).Google Scholar
  55. McAuslane, H.J., Vinson, S.B., Williams, H.J. (1991a). Influence of adult experience on host microhabitat location by the generalist parasitoid, Campoletis sonorensis (Hymenoptera: Ichneumonidae). J. Insect Behav., 4: 101–113.CrossRefGoogle Scholar
  56. McAuslane, H.J., Vinson, S.B., Williams, H.J. (1991b) Stimuli influencing host micro-habitat location in the parasitoid Campoletis sonorensis. Entomol. exp. appl. 58: 267–277.CrossRefGoogle Scholar
  57. Menzel, R., Greggers, U., Hammer, M. (1993) Functional organization of appetitive learning and memory in a generalist pollinator, the honey bee, in Insect Learning. Ecological and Evolutionary Aspects, (eds D.R. Papaj and A.C. Lewis), Chapman & Hall, New York, pp.79–125.Google Scholar
  58. Minkenberg, O., Tatar, M., Rosenheim, J.A. (1992) Egg load as a major source of variability in insect foraging and oviposition behavior. Oikos 65: 134–142.CrossRefGoogle Scholar
  59. Noldus, L.P.J.J. (1989) Semiochemicals, foraging behaviour and quality of entomophagous insects for biological control. J. Appl. Entomol. 108: 425–451.CrossRefGoogle Scholar
  60. Noldus, L.P.J.J. and Lenteren, J.C. van (1985) Kairomones for the egg parasite Trichogramma evanescens Westwood. II. Effect of contactchemicals produced by two of its hosts, Pieris brassicae L. and Pieris rapae L.. J. Chem. Ecol. 11: 793–800.CrossRefGoogle Scholar
  61. Noldus, L.P.J.J., Lenteren, J.C. van, Lewis, W.J. (1991) How Trichogramma parasitoids use moth sex pheromone as kairomone: orientation behaviour in a wind tunnel. Physiol. Entomol. 16: 313–327.CrossRefGoogle Scholar
  62. Nordlund, D.A., Lewis, W.J., Gueldner, R.C. (1983) Kairomones and their use for management of entomophagous insects. XIV. Response of Telenomus remus to abdominal tips of Spodoptera frugiperda, (Z)-9-tetradecene-1-ol acetate and (Z)-9-dodecene-1-ol acetate. J. Chem. Ecol. 9: 695–701.CrossRefGoogle Scholar
  63. Nordlund, D.A. and Sauls, C.E. (1981) Kairomones and their use for management of entomophagous insects. XI. Effect of host plants on kairomonal activity of frass from Heliothis zea larvae for the parasitoid Microplitis croceipes. J. Chem. Ecol. 7: 1057–1061.CrossRefGoogle Scholar
  64. Pak, G. A. and Jong, E.J. de (1987) Behavioural variations among strains of Trichogramma spp.: host recognition. Neth. J. Zool. 37: 137–166.CrossRefGoogle Scholar
  65. Papaj, D.R. (1993a) Automatic behavior and the evolution of instinct: lessons from learning in parasitoids, in Insect Learning. Ecological and Evolutionary Aspects, (eds D.R. Papaj and A.C. Lewis), Chapman & Hall, New York, pp.243–272.CrossRefGoogle Scholar
  66. Papaj, D.R. (1993b) Afterword: learning, adaptation, and the lessons of O, in Insect Learning. Ecological and Evolutionary Aspects, (eds D.R. Papaj and A.C. Lewis), Chapman & Hall, New York, pp.374–386.CrossRefGoogle Scholar
  67. Papaj, D.R. and Lewis, A.C. (eds) (1993) Insect Learning. Ecological and Evolutionary Perspectives, Chapman & Hall, New York.Google Scholar
  68. Papaj, D.R. and Prokopy, R.J. (1989) Ecological and evolutionary aspects of learning in phytophagous insects. Annu. Rev. Entomol. 34: 315–350.CrossRefGoogle Scholar
  69. Papaj, D.R., Snellen, H., Swaans, K. and Vet, L.E.M. (1994) Unrewarding experiences and their effect on foraging in parasitic wasps. J. Insect Behav. 7: 465–481.CrossRefGoogle Scholar
  70. Papaj, R.D. and Vet, L.E.M. (1990) Odor learning and foraging success in the parasitoid, Leptopilina heterotoma. J. Chem. Ecol. 16: 3137–3150.CrossRefGoogle Scholar
  71. Pavlov, I.P. (1941) Lectures on Conditioned Reflexes, 2 vols. International Publishers, New York.Google Scholar
  72. Poolman Simons, M.T.T., Suverkropp, B.P., Vet, L.E.M., Moed, G. de (1992) Comparison of learning in related generalist and specialist eucoilid parasitoids. Entomol. exp. appl. 64: 117–124.CrossRefGoogle Scholar
  73. Powell, W. and Wright, A.F. (1992) The influence of host food plants on host recognition by four aphidiine parasitoids (Hymenoptera: Braconidae). Bull. Entomol. Res. 81:449–453.CrossRefGoogle Scholar
  74. Price, P.W., Bouton, C.E., Gross, P., McPheron, B.A., Thompson, J.N., Weis, A.E. (1980) Interactions among three trophic levels: influence of plant on interactions between insect herbivores and natural enemies. Annu. Rev. Ecol. Syst. 11: 41–65.CrossRefGoogle Scholar
  75. Rescorla, R. A. (1988) Behavioral studies of Pavlovian conditioning. Annu. Rev. Neurosci. 11: 329–352.PubMedCrossRefGoogle Scholar
  76. Roitberg B.D., Reid, M.L., Li, C. (1993) Choosing hosts and mates: the value of learning, in Insect Learning. Ecological and Evolutionary Aspects, (eds D.R. Papaj and A.C. Lewis), Chapman & Hall, New York, pp. 174–194.Google Scholar
  77. Roper T.J. (1983) Learning as a biological phenomenon, in Genes, Development and Learning (eds T.R. Halliday and P.J.B. Slater), W.H. Freeman, New York, pp. 178–212.Google Scholar
  78. Smith, B.H. (1993) Merging mechanism and adaptation: an ethological approach to learning and generalization, in Insect Learning. Ecological and Evolutionary Aspects, (eds D.R. Papaj and A.C. Lewis), Chapman & Hall, New York, pp. 126–157.CrossRefGoogle Scholar
  79. Schmidt, J.M. and Smith, J.J.B. (1987) Short interval time measurement by a parasitoid wasp. Science 237: 903–905.PubMedCrossRefGoogle Scholar
  80. Schmidt, J., Cardé, R.T., Vet, L.E.M. (1993) Host recognition by Pimpla instigator F. (Hymenoptera: Ichneumonidae): preferences and learned responses. J. Insect Behav. 6: 1–11.CrossRefGoogle Scholar
  81. Sheehan, W. and Shelton, A.M. (1989) The role of experience in plant foraging by the aphid parasitoid Diaeretiella rapae (Hymenoptera:Aphidiidae). J. Insect Behav. 2: 743–759.CrossRefGoogle Scholar
  82. Sheehan, W., Wäckers, F.L., Lewis W.J. (1993) Discrimination of previously searched, host free sites by Microplitis croceipes (Hymenoptera: Braconidae). J. Insect Behav. 6: 323–331.CrossRefGoogle Scholar
  83. Shettleworth, S.J. (1984) Learning and behavioural ecology, in Behavioural Ecology. An evolutionary approach, (eds J.R. Krebs and N.B. Davies), Blackwell Scientific Publications, Oxford, pp. 170–194.Google Scholar
  84. Stephens, D.W. (1993) Learning and behavioral ecology: incomplete information and environmental predictability, in Insect Learning. Ecological and Evolutionary Aspects, (eds D.R. Papaj and A.C. Lewis), Chapman & Hall, New York, pp. 195–218.CrossRefGoogle Scholar
  85. Stephens, D.W. and Krebs, J.R. (1986) Foraging Theory, Princeton University Press, Princeton.Google Scholar
  86. Stamp, N.E. (1982) Behavioral interactions of parasitoids and Baltimore checkerspot caterpillars (Euphydrias phaeton). Environ. Entomol. 11: 100–104.Google Scholar
  87. Strand, M.R. and Vinson, S.B. (1982) Behavioral response of the parasitoid Cardiochiles nigriceps to a kairomone. Entomol. exp. appl. 31: 308–315.CrossRefGoogle Scholar
  88. Strand, M.R. and Vinson, S.B. (1983) Factors affecting host recognition and acceptance in the egg parasitoid Telenomus heliothidis (Hymenoptera: Scelionidae). Environ. Entomol. 12: 1114–1119.Google Scholar
  89. Takasu, K. and Lewis, W.J. (1993) Host- and food-foraging of the parasitoid Microplitis croceipes: learning and physiological state effects. Biol. Control 3: 70–74.CrossRefGoogle Scholar
  90. Takasu, K. and Lewis, W.J. (1995) Importance of adult food sources to host searching of the larval parasitoid Microplitis croceipes. Biol. Control 5: 25–30.CrossRefGoogle Scholar
  91. Thorpe, W.H. and Jones, F.G.W. (1937) Olfactory conditioning in a parasitic insect and its relation to the problem of host selection. Proc. R. Soc. Lond. B 124: 56–81.CrossRefGoogle Scholar
  92. Tierney, A.J. (1986) The evolution of learned and innate behavior: contributions from genetics and neurobiology to a theory of behavioral evolution. Anim. Learning Behav. 14: 339–348.CrossRefGoogle Scholar
  93. Tumlinson, J.H., Lewis W.J., Vet, L.E.M. (1993) Parasitic wasps, chemically guided intelligent foragers. Sci. Amer. 268: 100–106.CrossRefGoogle Scholar
  94. Turlings, T.C.J., Scheepmaker, J.W.A., Vet, L.E.M., Tumlinson, J.H., Lewis, W.J. (1990) How contact foraging experiences affect preferences for host-related odors in the larval parasitoid Cotesia marginiventris (Cresson) (Hymenoptera:Braconidae). J. Chem. Ecol. 16: 1577–1589.CrossRefGoogle Scholar
  95. Turlings, T.C.J, and Tumlinson, J.H., (1992) Systemic release of chemical signals by herbivore-injured corn. Proc. Natl. Acad. Sci. USA89: 8399–8402.PubMedCrossRefGoogle Scholar
  96. Turlings, T.C. J., Tumlinson, J.H., Lewis, W.J. (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250: 1251–1253.PubMedCrossRefGoogle Scholar
  97. Turlings, T.C.J., Tumlinson, J.H., Lewis, W.J., Vet, L.E.M. (1989) Beneficial arthropod behavior mediated by airborne semiochemicals. VIII. Learning of host-related odors induced by a brief contact experience with host by-products in Cotesia marginiventris (Cresson), a generalist larval parasitoid. J. Insect Behav. 2: 217–225.CrossRefGoogle Scholar
  98. Turlings, T.C.J., Wäckers, F.L., Vet, L.E.M., Lewis, W.J., Tumlinson, J.H. (1992) Learning of host-finding cues by hymenopterous parasitoids, in Insect Learning. Ecological and Evolutionary Aspects, (eds D.R. Papaj and A.C. Lewis), Chapman & Hall, New York, pp.51–78.Google Scholar
  99. Vet, L.E.M. (1988) The influence of learning on habitat location and acceptance by parasitoids. Les Colloq del’INRA 48: 29–34.Google Scholar
  100. Vet, L.E.M. and Dicke, M. (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol. 37: 141–172.CrossRefGoogle Scholar
  101. Vet, L.E.M. and Groenewold, A.W. (1990) Semiochemicals and learning in parasitoids. J. Chem. Ecol. 16: 3119–3135.CrossRefGoogle Scholar
  102. Vet, L.E.M. and Papaj, D.R. (1992) Effects of experience on parasitoid movement in odour plumes. Physiol. Entomol. 17: 90–96.CrossRefGoogle Scholar
  103. Vet, L.E.M., Lewis, W.J., Papaj, D.R., Lenteren, J.C. van (1990) A variable-response model for parasitoid foraging behavior. J. Insect Behav. 3: 471–490.CrossRefGoogle Scholar
  104. Vet, L.E.M. and Schoonman, G. (1988) The influence of previous foraging experience on microhabitat acceptance in Leptopilina heterotoma. J. Insect Behav. 1: 387–392.CrossRefGoogle Scholar
  105. Vet, L.E.M., Wäckers, F.L., Dicke, M. (1991) How to hunt for hiding hosts: the reliability-detectability problem in foraging parasitoids. Neth. J. Zool. 41: 202–213.CrossRefGoogle Scholar
  106. Vinson, S.B. (1984) Parasitoid-host relationships, in Chemical Ecology of Insects, (eds. W.J. Bell and R.T. Cardé), Chapman and Hall, London, pp. 205–233.Google Scholar
  107. Vinson, S.B., Barfield, C.S., Henson, R.D. (1977) Oviposition behaviour ofBracon mellitor, a parasitoid of the boll weevil (Anthonomus grandis). II. Associative learning. Physiol. Entomol. 2: 157–164.CrossRefGoogle Scholar
  108. Vinson, S.B. and Williams, H.J. (1991) Host selection behavior of Campoletis sonorensis: a model system. Biol. Control 1: 107–117.CrossRefGoogle Scholar
  109. Visser, J.H. (1986) Host odor perception by phytophagous insects. Annu. Rev. Entomol. 31: 121–144.CrossRefGoogle Scholar
  110. Visser, M.E., Alphen, J.J.M. van, Nell, H.W. (1992) Adaptive superparasitism and patch time allocation in solitary parasitoids: the influence of pre-patch experience. Behav. Ecol. Sociobiol. 31: 163–171.CrossRefGoogle Scholar
  111. Waage, J.K. (1978) Arrestment responses of the parasitoid, Nemeritis canescens, to a contact chemical produced by its host, Plodia interpunctella. Physiol. Entomol. 3: 135–146.CrossRefGoogle Scholar
  112. Waage, J.K. and Ng, S.M. (1984) The reproductive strategy of a parasitic wasp. I. Optimal progeny and sex allocation in Trichogramma evanescens. J. Anim. Ecol. 53: 401–415.CrossRefGoogle Scholar
  113. Wäckers, F.L. and Lewis, W.J. (1993) Olfactory and visual learning and their combined influence on host site location by Microplitis croceipes. Biol. Control, 4: 105–112.CrossRefGoogle Scholar
  114. Wardle, A.R. (1990) Learning of host microhabitat colour by Exeristes roborator (F.) (Hymenoptera: Ichneumonidae). Anim. Behav. 39: 914–923.CrossRefGoogle Scholar
  115. Wardle, A.R. and Borden, J.H. (1989) Learning of an olfactory stimulus associated with a host microhabitat by Exeristes roborator. Entomol. exp. appl. 52: 271–279.CrossRefGoogle Scholar
  116. Wardle, A.R. and Borden, J.H. (1990) Learning of host microhabitat form by Exeristes roborator (F.) (Hymenoptera: Ichneumonidae). J. Insect Behav. 3: 251–263.CrossRefGoogle Scholar
  117. Weseloh, R.M. (1981) Host location by parasitoids, in: Semiochemicals: their Role in Pest Control, (eds D.A. Nordlund, R.L. Jones and W.J. Lewis), Wiley, New York, pp. 79–95.Google Scholar
  118. Wiskerke, J.S.C., Dicke, M., Vet, L.E.M. (1993) Larval parasitoid uses aggregation pheromone of adult hosts in foraging behaviour: a solution to the reliability-detectability problem. Oecologia 93: 145–148.Google Scholar
  119. Zaborski, E., Teal, P.E.A., Laing, J.E. (1987) Kairomone-mediated host finding by the spruce budworm egg parasite, Trichogramma minutum. J. Chem. Ecol. 13: 113–122.CrossRefGoogle Scholar
  120. Zanen, P.O. and Cardé, R.T. (1991) Learning and the role of host-specific volatiles during in-flight host-finding in the specialist parasitoid Microplitis croceipes. Physiol. Entomol. 16: 381–389.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 1995

Authors and Affiliations

  • Louise E. M. Vet
    • 1
  • W. Joe Lewis
    • 2
  • Ring T. Cardé
    • 3
  1. 1.Department of EntomologyWageningen Agricultural UniversityNetherlands
  2. 2.Agricultural Research ServiceUnited States Department of AgricultureUSA
  3. 3.Department of EntomologyUniversity of MassachusettsUSA

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