Intra- and Interspecific Interactions among Parasitoids: Mechanisms, Outcomes and Biological Control

  • Guy Boivin
  • Jacques Brodeur


Insect parasitoids are a major mortality factor for their herbivore hosts. Parasitoids typically interact, within their guild and between trophic levels, with several organisms from their community. Both intra- and interspecific competitions occur and the intensity of this competition influences the population dynamics of parasitoids. A female parasitoid may face several types of competition from females of her own species or from different species or from either conspecific or heterospecific females. The strategies evolved by parasitoids to cope with competition have implications both for the population dynamics of these species and for their use as biological control agents. The response of parasitoids to the type and intensity of competition varies at the level of the species, population and individual. In addition, a female parasitoid may change her response to competition depending on the conditions under which she developed and the experience she gained.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. van Alphen, J. J. M., and Visser, M. E., 1990, Superparasitism as an adaptive strategy for insect parasitoids. Annu. Rev. Entomol. 35: 59-79.PubMedCrossRefGoogle Scholar
  2. Askary, H., and Brodeur, J., 1999, Susceptibility of larval stages of the aphid parasitoid Aphidius nigripes to the entomopathogenic fungus, Verticillium lecanii. J. Invert. Pathol. 73: 129-132.CrossRefGoogle Scholar
  3. Askew, R. R., and Shaw, M. R., 1986, Parasitoid communities: their size, structure and development. In: Insect Parasitoids, J. Waage, and D. Greathead, eds, , Academic Press, San Diego, pp. 225-264.Google Scholar
  4. van Baaren, J., and Boivin, G., 1998a, Genotypic and kin discrimination in a solitary Hymenopterous parasitoid: implications for speciation. Evol. Ecol. 12: 523-534.CrossRefGoogle Scholar
  5. van Baaren, J., and Boivin, G., 1998b, Learning affects host discrimination behavior in a parasitoid wasp. Behav. Ecol. Sociobiol. 42: 9-16.CrossRefGoogle Scholar
  6. van Baaren, J., Boivin, G., Le Lannic, J., and Nénon, J. P., 1997, The male and female first instar larvae of Anaphes victus and A. listronoti (Hymenoptera: Mymaridae). Zoomorphology 117: 189-197.CrossRefGoogle Scholar
  7. van Baaren, J., Boivin, G., and Nénon, J. P., 1994, Intra- and interspecific host discrimination in two closely related egg parasitoids. Oecologia 100: 325-330.CrossRefGoogle Scholar
  8. van Baaren, J., Boivin, G., and Nénon, J. P., 1995a, Intraspecific hyperparasitism in a primary hymenopteran parasitoid. Behav. Ecol. Sociobiol. 36: 237-242.Google Scholar
  9. van Baaren, J., Boivin, G., and Outreman, Y., 2005a, Patch exploitation strategy by an egg parasitoid in constant or variable environment. Ecol. Entomol. 30: 502-509.CrossRefGoogle Scholar
  10. van Baaren, J., Nénon, J. P., and Boivin, G., 1995b, Comparison of oviposition behavior of a solitary and a gregarious parasitoid (Hymenoptera: Mymaridae). J. Ins. Behav. 8: 671-686.CrossRefGoogle Scholar
  11. van Baaren, J., Outreman, Y., and Boivin, G., 2005b, Effect of low temperature exposure on oviposition behaviour and patch exploitation strategy in parasitic wasps. Anim. Behav. 70: 153-163.CrossRefGoogle Scholar
  12. Baker, D. A., Loxdale, H. D., and Edwards, O. R., 2003, Genetic variation and founder effects in the parasitoid wasp, Diaeretiella rapae (M’intosh) (Hymenoptera: Braconidae: Aphidiidae), affecting its potential as a biological control agent. Mol. Ecol. 12: 3303-3311.PubMedCrossRefGoogle Scholar
  13. Batchelor, T. P., Hardy, I. C. W., Barrera, J. F., and Pérez-Lachaud, G., 2005, Insect gladiators II: competitive interactions within and between bethylid parasitoid species of the coffe berry borer, Hypothenemus hampei (Coleoptera: Scolytidae). Biol. Contr. 33: 194-202.CrossRefGoogle Scholar
  14. Blumberg, D., and Luck, R. F., 1990, Differences in the rate of superparasitism between two strains of Comperiella bifasciata (Howard) (Hymenoptera: Encyrtidae) parasitizing California red scale (Homoptera: Diaspididae): an adaptation to circumvent encapsulation? Ann. Entomol. Soc. Am. 83: 591-597.Google Scholar
  15. Boivin, G. and van Baaren, J., 2000, The role of larval aggression and mobility in the transition between solitary and gregarious development in parasitoid wasps. Ecol. Lett. 3: 469-474.CrossRefGoogle Scholar
  16. Boivin, G., Fauvergue, X., and Wajnberg, E., 2004. Optimal patch residence time in egg parasitoids: innate versus learned estimate of patch quality. Oecologia 138: 640-647.PubMedCrossRefGoogle Scholar
  17. Boivin, G., and Lagacé, M., 1999, Effet de la taille sur la fitness de Trichogramma evanescens (Hymenoptera: Trichogrammatidae). Ann. Soc. Entomol. Fr. 35 (suppl.): 371-378.Google Scholar
  18. Briggs, C. J., 1993, Competition among parasitoid species on a stage-structured host and its effect on host suppression. Am. Nat. 141: 372-397..CrossRefGoogle Scholar
  19. Brodeur, J., 2000, Host specificity and trophic relationship of hyperparasitoids. In: Parasitoid Population Biology, M. E. Hochberg and A.R. Ives, eds, Princeton University Press, pp. 163-183.Google Scholar
  20. Brodeur, J., and Boivin, G., 2004, Functional ecology of immature parasitoids. Annu. Rev. Entomol. 49: 27-49.PubMedCrossRefGoogle Scholar
  21. Brodeur, J., and Rosenheim, J. A., 2000, Intraguild predation in aphid parasitoids: a review. Entomol. Exp. Appl. 97: 93-108.CrossRefGoogle Scholar
  22. Brooks, W.M., 1993, Host-parasitoid-pathogen interactions. In: Parasites and pathogens of insects, N.E. Beckage, S.N. Thompson and B.A. Federici, eds, Vol. 2, Academic Press, San Diego, pp. 231-272.Google Scholar
  23. Browning, H. W., and Oatman, E. R., 1984, Intra- and interspecific relationships among some parasites of Trichoplusia ni (Lepidoptera: Noctuidae). Environ. Entomol. 13: 551-556.Google Scholar
  24. Chassain, C., Boulétreau, M., and Fouillet, P., 1988, Host exploitation by parasitoids: local variations in foraging behaviour of females among populations of Trichogramma species. Entomol. Exp. Appl. 48: 195-202.CrossRefGoogle Scholar
  25. Chow, F. J., and Mackauer, M., 1986, Host discrimination and larval competition in the aphid parasite, Ephedrus californicus. Entomol. Exp. Appl. 41: 243-254.CrossRefGoogle Scholar
  26. Cormier, D., Royer, L., Vigneault, C., Panneton, B., and Boivin, G., 1998, Effect of female age on daily cycle of sexual pheromone emission in gregarious egg parasitoid Anaphes listronoti. J. Chem. Ecol. 24: 1595-1610.CrossRefGoogle Scholar
  27. Demoraes, C. M., Cortesero, A. M., Stapel, J. O., and Lewis, W. J., 1999, Intrinsic and extrinsic competitive interactions between two larval parasitoids of Heliothis virescens. Ecol. Entomol. 24: 402-410.CrossRefGoogle Scholar
  28. Duan, J. J., and Messing, R. H., 1999, Effect of origin and experience on patterns of host acceptance by the opiine parasitoid Diachasmimorpha tryoni. Ecol. Entomol. 24: 284-291.CrossRefGoogle Scholar
  29. Eichhorn, O., 1996, Experimental studies upon the parasitoid complex of the gypsy moth (Lymantria dispar L.) (Lep., Lymantriidae) in lower host populations in eastern Austria. J. Appl. Entomol. 120: 205-212.CrossRefGoogle Scholar
  30. Fauvergue, X., Fouillet, P., Mesquita, A. L. M., and Boulétreau, M., 1998, Male orientation to trail sex pheromones in parasitoid wasps: does the spatial distribution of virgin females matter? J. Ins. Physiol. 44: 667-675.CrossRefGoogle Scholar
  31. Feijen, H. R., and Schulten, G. G. M., 1981, Egg parasitoids (Hymenoptera: Trichogrammatidae) of Diopsis macrophthalma (Diptera: Diopsidae) in Malawi. Neth. J. Zool. 31: 381-417.Google Scholar
  32. Field, S. A., and Calbert, G., 1999, Don’t count your eggs before they’re parasitized: contest resolution and the trade-off during patch defense in a parasitoid wasp. Behav. Ecol. 10: 122-127.CrossRefGoogle Scholar
  33. Flexner, J. L., Lighthart, B., and Croft, B.A., 1986, The effects of microbial pesticides on non-target, beneficial arthropods. Agric. Ecosys. Environ. 16: 203-254.CrossRefGoogle Scholar
  34. Gandolfi, M., Mattiacci, L., and Dorn, S., 2003, Mechanisms of behavioral alterations of parasitoids reared in artificial systems. J. Chem. Ecol. 29: 1871-1887.PubMedCrossRefGoogle Scholar
  35. Godfray, H. C. J., 1994, Parasitoids: Behavioral and Evolutionary Ecology. Princeton University Press, Princeton.Google Scholar
  36. Godfray, H. C. J., and Shimada, M., 1999, Parasitoids: a model system to answer questions in behavioral, evolutionary and population ecology. Res. Popul. Ecol. 41: 3-10.CrossRefGoogle Scholar
  37. Goubault, M., 2003, Exploitation des hôtes chez un Hyménoptère parasitoïde solitaire: conséquences adaptatives de la compétition intraspécifique sur les stratégies comportementales des femelles. PhD Thesis, Université de Rennes 1, Rennes.Google Scholar
  38. Goubault, M., Krespi, L., Boivin, G., Poinsot, D., Nénon, J.-P., and Cortesero, A. M., 2004, Intraspecific variations in host discrimination behavior in the pupal parasitoid Pachycrepoideus vindemmiae Rondani (Hymenoptera: Pteromalidae). Environ. Entomol. 33: 362-369.CrossRefGoogle Scholar
  39. Goubault, M., Outreman, Y., Poinsot, D., and Cortesero, A. M., 2005, Patch exploitation strategies of parasitic wasps under intraspecific competition. Behav. Ecol. 16 693-701.CrossRefGoogle Scholar
  40. Grandgirard, J., Poinsot D., Krespi L., Nénon J.-P., and Cortesero, A. M., 2002, Costs of secondary parasitism in the facultative hyperparasitoid Pachycrepoideus dubius: does host size matter? Entomol. Exp. Appl. 103: 239-248.CrossRefGoogle Scholar
  41. Griffiths, N. T., and Godfray, H. C. J., 1988, Local mate competition, sex ratio and clutch size in bethylid wasps. Behav. Ecol. Sociobiol. 22: 211-217.CrossRefGoogle Scholar
  42. Hagvar, E. B., and Hofsvang, T., 1988, Interspecific competition between the aphid parasitoids Aphidius colemani Viereck and Ephedrus cerasicola Stary (Hymenoptera: Aphidiidae). Entomol. Exp. Appl. 59: 145-150.Google Scholar
  43. Hardy, I. C. W., and Blackburn, T. M., 1991, Brood guarding in a bethylid wasp. Ecol. Entomol. 16: 55-62.Google Scholar
  44. Hassan, S. A., 1994, Strategies to select Trichogramma species for use in biological control. In: Biological Control with Egg Parasitoids, E. Wajnberg and S. A. Hassan, eds, CAB International, Wallingford, pp. 55-71.Google Scholar
  45. Hassell, M.P., 2000, The Spatial and Temporal Dynamics of Host-Parasitoid Interactions. Oxford University Press, Oxford..Google Scholar
  46. Hawkins, B. A., 2000, Species coexistence in parasitoid communities: does competition matter? In: Parasitoid Population Biology, M. A. Hochberg and A. R. Ives, eds, Princeton University Press, Princeton, pp. 198-213.Google Scholar
  47. Hawkins, B.A., Cornell, H.V., and Hochberg, M.E., 1997, Predators, parasitoids, and pathogens as mortality agents in phytophagous insect populations. Ecology 78: 2145-2152.CrossRefGoogle Scholar
  48. Heslin, L. M., and Merritt, D.J., 2005, Cannibalistic feeding of larval Trichogramma carverae parasitoids in moth eggs. Naturwissenschaften 92: 435-439.PubMedCrossRefGoogle Scholar
  49. Hochberg, M.E., and Lawton, J. H., 1990, Competition between kingdoms. TREE 5: 367-371.Google Scholar
  50. Holt, R.D., and Lawton, J. H., 1994, The ecological consequences of shared natural enemies. Annu. Rev. Ecol. Syst. 25: 495-520.CrossRefGoogle Scholar
  51. Hughes, J. P., Harvey, I. F., and Hubbard, S. F., 1994, Host-searching behavior of Venturia canescens (Grav.) (Hymenoptera: Ichneumonidae): Interference- The effect of mature egg load and prior behavior. J. Ins. Behav. 7: 433-454.CrossRefGoogle Scholar
  52. Jaenike, J., and Papaj, D. R., 1992, Behavioral plasticity and patterns of host use by insects, In: Insect Chemical Ecology: an Evolutionary Approach, B. D. Roitberg and M. B. Isman, eds, Chapman & Hall, New York, pp. 245-264.Google Scholar
  53. Jarjees, E. A., and Merritt, D. J., 2002, Development of Trichogramma australicum Girault (Hymenoptera: Trichogrammatidae) in Helicoverpa (Lepidoptera: Noctuidae) host eggs. Austr. J. Entomol. 41: 310-315.CrossRefGoogle Scholar
  54. Kfir, R., and Rosen D., 1981, Biology of the hyperparasite Pachyneuron concolor (Förster) (Hymenoptera: Pteromalidae) reared on Microterys flavus (Howard) in brown soft scale. J. Entomol. Soc. South. Afric. 44: 151-163.Google Scholar
  55. Landry, B. S., Dextrase, L., and Boivin, G., 1993, Random amplified polymorphic DNA markers for DNA fingerprinting and genetic variability assessment of minute parasitic wasp species (Hymenoptera: Mymaridae and Trichogrammatidae) used in biological control programs of phytophagous insects. Genome 36: 580-587.PubMedGoogle Scholar
  56. Lawrence, P. O., 1981, Interference competition and optimal host selection in the parasitic wasp, Biosteres longicaudatus. Ann. Entomol. Soc. Am. 74: 540-544.Google Scholar
  57. 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. Environ. Entomol. 19: 1183-1193.Google Scholar
  58. Liu, F.-H., and Smith, S. M., 2000, Measurement and selection of parasitoid quality for mass-reared Trichogramma minutum Riley used in inundative release. Biocontr. Sci. Tech. 10: 3-13.CrossRefGoogle Scholar
  59. Luck, R. F., Messenger, P. S., and Barbieri, J. F., 1981, The influence of hyperparasitism on the performance of biological control agents. In D. Rosen, ed., The Role of Hyperparasitism in Biological Control: A Symposium, Berkeley, U.S.A.: Division of Agricultural Science, University of California, pp. 34-42..Google Scholar
  60. Mackauer, M., 1990, Host discrimination and larval competition in solitary endoparasitoids. In: Critical Issues in Biological Control, M. Mackauer, L. E. Ehler, and J. Roland, eds, Intercept/VCH, Andover, pp. 41-62.Google Scholar
  61. McBrien, H., and Mackauer, M., 1991, Decision to superparasitise based on larval survival: Competition between larval parasitoids Aphidius ervi and Aphidius smithi. Entomol. Exp. Appl. 59: 145-150.CrossRefGoogle Scholar
  62. Miller, J. C., 1982, Life history of insect parasitoids involved in successful multiparasitism. Oecologia 54: 8-9.CrossRefGoogle Scholar
  63. Mills, N. J., 1991, Searching strategies and attack rates of parasitoids of the ash bark beetle (Leperisinus varius) and its relevance to biological control. Entomol. Entomol. 16: 461-470.Google Scholar
  64. Morin, P.J. 1999, Community ecology. Blackwell Science, Malden..Google Scholar
  65. Müller, C. B., Adriaanse, I. C. T., Belshaw, R., and Godfray, H. C. J., 1999, The structure of an aphid-parasitoid community. J. Anim. Ecol. 68: 346-370.CrossRefGoogle Scholar
  66. van Nouhuys, S., and Hanski, I., 2000, Apparent competition between parasitoids mediated by a shared hyperparasitoid. Ecol. Lett. 3: 82-84.CrossRefGoogle Scholar
  67. Outreman, Y., Le Ralec, A., Wajnberg, E., and Pierre, J. S., 2001, Can imperfect host discrimination explain partial patch exploitation in parasitoids? Ecol. Entomol. 26: 271-280.CrossRefGoogle Scholar
  68. Pak, G. A., 1992, Inundative release of Trichogramma for the control of cruciferous Lepidoptera: preintroductory selection of an effective parasitoid. In: Diamondback moth and other crucifer pests, N. S. Talekar, eds, Asian Vegetable Research and Development Center, AVRDC Publication; v. No. 92-368, Tainan, Taiwan, pp. 297-308.Google Scholar
  69. Parker, G. A., and Courtney, S. P., 1984, Models of clutch size in insect oviposition. Theor. Popul. Biol. 26: 27-48.CrossRefGoogle Scholar
  70. Pedersen, B.S., and Mills, N.J., 2004, Single vs. multiple introduction in biological control : the roles of parasitoid efficiency, antagonism and niche overlap. J. Appl. Ecol. 41: 973-984.CrossRefGoogle Scholar
  71. Pérez-Lachaud, G., Bachelor, T. P., and Hardy, I. C. W., 2004, Wasp eat wasp: facultative hyperparasitism and intra-guild predation by bethylid wasps. Biol. Contr. 30: 149-155.CrossRefGoogle Scholar
  72. Pérez-Lachaud, G., Hardy, I. C. W., and Lachaud, J. P., 2002, Insect gladiators: competitive interactions between three species of bethylid wasps attacking the coffe berry borer, Hypothenemus hampei (Coleoptera: Scolytidae). Biol. Contr. 25: 231-238.CrossRefGoogle Scholar
  73. Petersen, G., and Hardy, I. C. W., 1996, The importance of being larger: parasitoid intruder-owner contests and their implications for clutch size. Anim. Behav. 51: 1363-1373.CrossRefGoogle Scholar
  74. Pigliucci, M., 2005, Evolution of phenotypic plasticity: where are we going now? TREE 20: 481-486.PubMedGoogle Scholar
  75. 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
  76. Prévost, G., and Lewis, W. J., 1990, Heritable differences in the response of the Braconid wasp, Microplitis croceipes to volatile allelochemicals. J. Ins. Behav. 3: 277-287.CrossRefGoogle Scholar
  77. Quicke, D. L. J., 1997, Parasitic Wasps. Chapman & Hall, London..Google Scholar
  78. Rosenheim, J.A., 1998, Higher-order predators and the regulation of insect herbivore populations. Annu. Rev. Entomol. 43: 421-447.PubMedCrossRefGoogle Scholar
  79. Rosenheim, J.A., Kaya, H. K., Ehler, L. E., Marois, J. J., and Jaffee, B. A., 1995, Intraguild predation among biological control agents: theory and evidence. Biol. Contr. 5: 303-335.CrossRefGoogle Scholar
  80. Stiling, P., 1993, Why do natural enemies fail in classical biological control programs? Am. Entomol. 39(1): 31-37.Google Scholar
  81. Stokkebo, S., and Hardy, I. C. W., 2000, The importance of being gravid: egg load and contest outcome in a parasitoid wasp. Anim. Behav. 59: 1111-1118.PubMedCrossRefGoogle Scholar
  82. Strand, M. R., 1986, The physiological interactions of parasitoids with their hosts and their influence on reproductive strategies, in: Insect Parasitoids, J. K. Waage and D. Greathead, eds., Academic Press, London, pp. 97-136.Google Scholar
  83. Strand, M. R., Johnson, J. A., and Culin, J. D., 1990, Intrinsic interspecific competition between the polyembryonic parasitoid Copidosoma floridanum and the solitary endoparasitoid Microplitis demolitor in Pseudoplusia includens. Entomol. Exp. Appl. 55: 275-284.Google Scholar
  84. van Strien-van Liempt, W. T. F. H., and van Alphen, J. J. M., 1981, The absence of interspecific host discrimination in Asobara tabida Nees and Leptopilina heterotoma (Thompson) coexisting larval parasitoids of Drosophila species. Neth. J. Zool. 31: 701-712.CrossRefGoogle Scholar
  85. Ueno, T., 1999, Host-size-dependent sex ratio in a parasitoid wasp. Res. Popul. Ecol. 41: 47-57.CrossRefGoogle Scholar
  86. Vinson, S. B., 1998, The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species. Biol. Contr. 11: 79-96.CrossRefGoogle Scholar
  87. Vinson, S. B., and Ables, J. R., 1980, Interspecific competition among endoparasitoids of tobacco budworm larvae (Lep.: Noctuidae). Entomophaga 25: 357-362.CrossRefGoogle Scholar
  88. Wajnberg, E., 1993, Genetic variation in sex allocation in a parasitic wasp: variation in sex pattern within sequences of oviposition. Entomol. Exp. Appl. 69: 221-229.CrossRefGoogle Scholar
  89. Wajnberg, E., Pizzol, J., and Babault, M., 1989, Genetic variation in progeny allocation in Trichogramma maidis. Entomol. Exp. Appl. 53:177-187.CrossRefGoogle Scholar
  90. Wajnberg, E., Rosi M. C., and Colazza, S., 1999, Genetic variation in patch time allocation in a parasitic wasp. J. Anim. Ecol. 68: 121-133.CrossRefGoogle Scholar
  91. Weber, C.A., Smilanik, I. M., Ehler, L. E., and Zalom, F. G., 1996, Ovipositional behavior and host discrimination in three scelionid egg parasitoids of stink bugs. Biol. Contr. 6: 245-252.CrossRefGoogle Scholar
  92. Wu, Z. X., Cohen, A. C., and Nordlund, D. A., 2000, The feeding behavior of Trichogramma brassicae: new evidence for selective ingestion of solid food. Entomol. Exp. Appl. 96: 1-8.CrossRefGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Guy Boivin
    • 1
  • Jacques Brodeur
    • 2
  1. 1.CRDH, Agriculture and Agrifood CanadaSaint-Jean-sur-RichelieuCanada
  2. 2.Institut de Recherche en Biologie Végétale, Université de MontréalMontréalCanada

Personalised recommendations