Journal of Chemical Ecology

, Volume 24, Issue 10, pp 1595–1610 | Cite as

Effect of Female Age on Daily Cycle of Sexual Pheromone Emission in Gregarious Egg Parasitoid Anaphes listronoti

  • Daniel Cormier
  • Lucie Royer
  • Clément Vigneault
  • Bernard Panneton
  • Guy Boivin


The temporal pattern of pheromone emission by Anaphes listronoti females was established in a four-arm olfactometer by observing, at 2-hr intervals, the response of <2-hr-old males to odor produced by individual virgin females of <1, 1, and 2 days of age. This is the first evidence of a sexual pheromone in a Mymaridae. Under a 16L:8D photoperiod and 24°C constant temperature, the responsiveness of males to females of different ages varied significantly during the photophase. When <1-day-old females were used, males made significantly more final choices in the pheromone field than odorless fields at 4 and 6 hr after the onset of the photophase, and their walking speed was significantly higher from 4 to 12 hr, suggesting that females began to release a long-range pheromone during this period. Final choices and high walking speed were observed earlier with 1- and 2-day-old females than with <1-day-old females, and there was a significant decrease in male responses at 6 hr after the onset of the photophase, suggesting a bimodal temporal pattern of sexual pheromone emission.

Sexual pheromone daily cycle male attraction female age olfactometer egg parasitoid Hymenoptera Mymaridae Anaphes listronoti 


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  1. Assem, J., van den. 1986. Mating behaviour in parasitic wasps, pp. 137–167, in J. Waage and D. Greathead (eds.). Insect Parasitoids. Academic Press, Orlando, Florida.Google Scholar
  2. Assem, J. van den, and Jachmann, F. 1982. The coevolution of receptivity signalling and body size dimorphism in the Chalcidoidea. Behaviour 80:96–105.Google Scholar
  3. Assem, J. van den, and Putters, F. A. 1980. Patterns of sound produced by courting chalcidoid males and its biological significance. Entomol. Exp. Appl. 27:293–302.Google Scholar
  4. Baker, T. C., Meyer, W., and Roelofs, W. L. 1981. Sex pheromone dosage and blend specificity of response by oriental fruit moth males. Entomol. Exp. Appl. 30:269–279.Google Scholar
  5. Bakkendorf, O. 1934. Biological investigations on some Danish hymenopterous egg-parasites, especially in homopterous and heteropterous eggs, with taxonomic remarks and descriptions of new species. Entomol. Medd. 19:1–134.Google Scholar
  6. Bartelt, R. J., Jones, R. L., and Kulman, H. M. 1982. Hydrocarbon components of the yellow-headed spruce sawfly sex pheromone: A series of (Z,Z)-9, 19-dienes. J. Chem. Ecol. 8:95–114.Google Scholar
  7. Berry, J. S., and Holtzer, T. O. 1990. Ambulatory dispersal behavior of Neoseiulus fallacis (Acarina: Phytoseiidae) in relation to prey density and temperature. Exp. Appl. Acarol. 8:253–274.Google Scholar
  8. Bigler, F., Bieri, M., Fritschy, A., and Seidel, K. 1988. Variation in locomotion between laboratory strains of Trichogramma maidis and its impact on parasitism of eggs of Ostrinia nubilalis in the field. Entomol. Exp. Appl. 49:283–290.Google Scholar
  9. Boivin, G. 1988. Laboratory rearing of Anaphes soridatus (Hym.: Mymaridae) on carrot weevil eggs (Col.: Curculionidae). Entomophaga 33:245–248.Google Scholar
  10. Brodeur, J., and McNeil, J. N. 1994. Seasonal ecology of Aphidius nigripes (Hymenoptera: Aphidiidae), a parasitoid of Macrosiphum euphorbiae (Homoptera: Aphididae). Environ. Entomol. 23:292–298.Google Scholar
  11. Clausen, C. P. 1940. Entomophagous Insects. McGraw-Hill, New York.Google Scholar
  12. Collins, R. D. 1982. The biology of Patasson sp. near sordidatus (Hymenoptera: Mymaridae) and its impact on the carrot weevil. MS thesis. Michigan State University, East Lansing.Google Scholar
  13. Collins, R. D., and Grafius, E. 1986a. Biology and life cycle of Anaphes sordidatus (Hymenoptera: Mymaridae), an egg parasitoid of the carrot weevil (Coleoptera: Curculionidae). Environ. Entomol. 15:100–105.Google Scholar
  14. Collins, R. D., and Grafius, E. 1986b. Impact of the egg parasitoid, Anaphes sordidatus (Hymenoptera: Mymaridae), on the carrot weevil (Coleoptera: Curculionidae). Environ. Entomol. 15:469–475.Google Scholar
  15. Collins, R. D., and Grafius, E. 1986c. Courtship and mating behavior of Anaphes sordidatus (Hymenoptera: Mymaridae), a parasitoid of the carrot weevil (Coleoptera: Curculionidae). Ann. Entomol. Soc. Am. 79:31–33.Google Scholar
  16. Cormier, D., Stevenson, A. B., and Boivin, G. 1996. Seasonal ecology and geographical distribution of Anaphes listronoti and A. victus (Hymenoptera: Mymaridae), egg parasitoids of the carrot weevil (Coleoptera: Curculionidae) in central Ontario. Environ. Entomol. 25:1376–1382.Google Scholar
  17. Daniel, W. W. 1990. Applied Nonparametric Statistics. PWS-Kent Publishing, Boston.Google Scholar
  18. Decker, U. M., Powell, W., and Clark, S. J. 1993. Sex pheromones in the cereal aphid parasitoids Praon volucre and Aphidius rhopalosiphi. Entomol. Exp. Appl. 69:33–39.Google Scholar
  19. Doutt, R. L. 1959. The biology of parasitic hymenoptera. Annu. Rev. Entomol. 4:161–182.Google Scholar
  20. Giles, D. K., Heinz, K. M., and Parrella, M. P. 1996. Quantitative assessment of insect olfactometer performance by experimental flow analysis. Biol. Control 7:44–47.Google Scholar
  21. Godray, H. C. J. 1994. Parasitoids: Behavioral and Evolutionary Ecology. Princeton University Press, Princeton, New Jersey.Google Scholar
  22. Gordh, G., and DeBach, P. 1978. Courtship behavior in the Aphytis lingnanensis group, its potential usefulness in taxonomy, and a review of sexual behavior in the parasitic Hymenoptera (Chalcidoidea: Aphelinidae). Hilgardia 46:37–75.Google Scholar
  23. Haynes, K. F., Gaston, L. K., Pope, M. M., and Baker, T. C. 1983. Rate and periodicity of pheromone release from individual female artichoke plume moths, Platyptilia carduidactyla (Lepidoptera: Pterophoridae). Environ. Entomol. 12:1597–1600.Google Scholar
  24. Kimani, S. W., and Overholt, W. A. 1995. Biosystematics of the Cotesia flavipes complex (Hymenoptera: Braconidae): Interspecific hybridization, sex pheromone and mating behaviour studies. Bull. Entomol. Res. 85:379–386.Google Scholar
  25. Leonard, S. H., and Ringo, J. M. 1978. Analysis of male courtship patterns and mating behavior of Brachymeria intermedia. Ann. Entomol. Soc. Am. 71:817–826.Google Scholar
  26. Martel, P., Svec, H. J., and Harris, C. R. 1975. Mass rearing of the carrot weevil, Listronotus oregonensis (Coleoptera: Curculionidae), under controlled environmental conditions. Can. Entomol. 107:95–98.Google Scholar
  27. McNeil, J. N., and Brodeur, J. 1995. Pheromone-mediated mating in the aphid parasitoid, Aphidius nigripes (Hymenoptera: Aphididae). J. Chem. Ecol. 21:959–972.Google Scholar
  28. Pettersson, J. 1970. An aphid sex attractant. I. Biological studies. Entomol. Scand. 1:63–73.Google Scholar
  29. Pintureau, B., and Toonders, T. 1983. Quelques résultats concernant l'étude de l'attraction des mâles par les femelles vierges chez Trichogramma maidis (Hym. Trichogrammatidae). Bull. Soc. Linn. Lyon 52:81–87.Google Scholar
  30. Pittara, I. S., and Katsoyannos, B. I. 1985. Male attraction to virgin females in the almond seed wasp, Eurytoma amygdali Enderlein (Hymenoptera, Eurytomidae). Entomol. Hell. 3:43–46.Google Scholar
  31. Raina, A. K., Klun, J. A., and Stadelbacher, E. A. 1986. Diel periodicity and effect of age and mating on female sex pheromone titer in Heliothis zea (Lepidoptera: Noctuidae). Ann. Entomol. Soc. Am. 79:128–131.Google Scholar
  32. Rao, S. V., and DeBach, P. 1969. Experimental studies on hybridization and sexual isolation between some Aphytis species (Hymenoptera: Aphelinidae). I. Experimental hybridization and an interpretation of evolutionary relationships among the species. Hilgardia 39:515–553.Google Scholar
  33. Read, D. P., Feeny, P. P., and Root, R. B. 1970. Habitat selection by the aphid parasite Diaeretiella rapae (Hymenoptera: Braconidae) and hyperparasite Charips brassicae (Hymenoptera: Cynipidae). Can. Entomol. 102:1567–1578.Google Scholar
  34. Reed, H. C., Tan, S., Reed, D. K., Elliott, N. C., Burd, J. D., and Walker, T. 1994. Evidence for a sex attractant in Aphidius colemani Viereck with potential use in field studies. Southwest Entomol. 19:273–278.Google Scholar
  35. Robacker, D. C., Weaver, K. M., and Hendry, L. B. 1976. Sexual communication and associative learning in the parasitic wasp Itoplectis conquisitor (Say). J. Chem. Ecol. 2:39–48.Google Scholar
  36. SAS Institute. 1988. SAS/STAT User's Guide, Release 6.03 ed. SAS Institute, Cary, North Carolina.Google Scholar
  37. Schwartz, A., and Gerling, D. 1974. Adult biology of Telenomus remus (Hymenoptera: Scelionidae) under laboratory conditions. Entomophaga 19:483–492.Google Scholar
  38. Steel, R. G. D., and Torrie, J. H. 1980. Principles and Procedures of Statistics: A Biometrical Approach. McGraw-Hill, New York.Google Scholar
  39. Swedenborg, P. D., and Jones, R. L. 1992a. Multicomponent sex pheromone in Macrocentrus grandii Goidanich (Hymenoptera: Braconidae). J. Chem. Ecol. 18:1901–1912.Google Scholar
  40. Swedenborg, P. D., and Jones, R. L. 1992b. (Z)-4-Tridecenal, a pheromonally active air oxidation product from a series of (Z,Z)-9,13 dienes in Macrocentrus grandii Goidanich (Hymenoptera: Braconidae). J. Chem. Ecol. 18:1913–1931.Google Scholar
  41. Swedenborg, P. D., Jones, R. L., Liu, H.-W., and Krick, T. P. 1993. (3R*,5S*,6R*s*)-3,5-Dimethyl-6-(methylethyl)-3,4,5,6-tetrahydropyran-2-one, third sex pheromone component for Macrocentrus grandii (Goidanich) (Hymenoptera: Braconidae) and evidence for its utility at eclosion. J. Chem. Ecol. 19:485–502.Google Scholar
  42. Swier, S. R., Rings, R. W., and Musick, G. J. 1977. Age-related calling behavior of the black cutworm, Agrotis ipsilon. Ann. Entomol. Soc. Am. 70:919–924.Google Scholar
  43. Takahashi, S., and Sugai, T. 1982. Mating behavior of the parasitoid wasp Tetrastichus hagenowii (Hymenoptera: Eulophidae). Entomol. Gen. 7:287–293.Google Scholar
  44. Tripathi, R. N., and Singh, R. 1990. Mating behaviour of Lysiphlebia mirzai Shuja-Uddin (Hymenoptera: Aphidiidae), a parasitoid of Rhopalosiphum maidis (Fitch) (Hemiptera: Aphididae). Entomon 15:21–25.Google Scholar
  45. Vet, L. E. M., van Lenteren, J. C., Heymans, M., and Meelis, E. 1983. An airflow olfactometer for measuring olfactory responses of hymenopterous parasitoids and other small insects. Physiol. Entomol. 8:97–106.Google Scholar
  46. Vigneault, C., Panneton, B., Cormier, D., and Boivin, G. 1997. Automated system to quantify the behavior of small insects in a four-pointed star olfactometer. Appl. Eng. Agric. 13:545–550.Google Scholar
  47. Vinson, S. B. 1972. Courtship behavior and evidence for a sex pheromone in the parasitoid Campoletis sonorensis (Hymenoptera: Ichneumonidae). Environ. Entomol. 1:409–414.Google Scholar
  48. Whitcomb, W. D. 1965. The carrot weevil in Massachusetts; biology and control. Agriculture Experiment Station, University of Massachusetts Bulletin No. 550.Google Scholar
  49. Yoshida, S. 1978. Behaviour of males in relation to the female sex pheromone in the parasitoid wasp, Anisopteromalus calandrae (Hymenoptera: Pteromalidae). Entomol. Exp. Appl. 23:152–162.Google Scholar
  50. Yoshida, S., and Hidaka, T. 1979. Determination of the position of courtship display of the young unmated male Anisopteromalus calandrae. Entomol. Exp. Appl. 26:115–120.Google Scholar

Copyright information

© Plenum Publishing Corporation 1998

Authors and Affiliations

  • Daniel Cormier
    • 1
  • Lucie Royer
    • 1
  • Clément Vigneault
    • 2
  • Bernard Panneton
    • 2
  • Guy Boivin
    • 2
  1. 1.Department of Natural Resource SciencesMacdonald campus of McGill UniversitySainte-Anne-de-BellevueCanada
  2. 2.Horticultural Research and Development CentreAgriculture and Agri-Food CanadaSaint-Jean-sur-RichelieuCanada

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