Skip to main content

Advertisement

SpringerLink
Log in

Evidence for Four-Component Close-Range Sex Pheromone in the Parasitic Wasp Glyptapanteles flavicoxis

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Females of the parasitic wasp Glyptapanteles flavicoxis (Hymenoptera: Braconidae) deposit a close-range sex pheromone from their abdominal tip that attracts conspecific males and elicits wing-fanning behavior. In this study, we isolated the pheromone components and determined their role in the males' behavior. In coupled gas chromatographic–electroantennographic detection (GC-EAD) analyses of the females' body extract, four components (below GC detection) elicited strong responses from male antennae. Monitored by GC-EAD, the components were separated by flash silica gel and high-performance liquid chromatography. Y-tube olfactometer experiments with one or more components revealed that all are necessary to elicit short-range attraction and wing-fanning responses by males. These components remained below detection threshold of the mass spectrometer (∼10 pg) even when 4500 female equivalents were analyzed in a single injection, which attests to the potency of the pheromone and the insects' sensitivity to it.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Arn, H., Städler, E., and Rauscher, S. 1975. The electroantennographic detector—A selective and sensitive tool in the gas chromatographic analysis of insect pheromones. Z. Naturforsch. 30c:722–725.

    CAS  Google Scholar 

  • Bell, R. A., Owens, C. D., Shapiro, M., and Tardif, J. R. 1981. Mass rearing and virus production, pp. 599–655, in C. C. Doane and M. L. McManus (eds.). The gypsy moth: Research toward integrated pest management. U.S. Dept. Agric. Tech. Bull. 1584, p. 757.

  • Bjostad, L. B., Jewett, D. K., and Brigham, D. L. 1996. Sex pheromone of caddisfly Hesperophylax occidentalis (Banks) (Trichoptera: Limnephilidae). J. Chem. Ecol. 22:103–121.

    Article  CAS  Google Scholar 

  • Boush, G. M. and Baerwald, R. J. 1967. Courtship behavior and evidence for a sex pheromone in the apple maggot parasite, Opius alloeus (Hymenoptera: Braconidae). Ann. Entomol. Soc. Am. 60:865–866.

    Google Scholar 

  • Cole, L. R. 1970. Observations on the finding of mates by male Phaeogenes invisor and Apanteles medicaginis (Hymenoptera: Ichenumonidea). Anim. Behav. 18:184–189.

    Article  Google Scholar 

  • Corey, E. J. and Suggs, J. W. 1975. Pyridinium chlorochromate. An efficient reagent for oxidation of primary and secondary alcohols to carbonyl compounds. Tetrahedron Lett. 31:2647–2650.

    Article  Google Scholar 

  • Delury, N. C., Gries, G., Gries, R., Judd, G. J. R., and Brown, J. J. 1999. Sex pheromone of Ascogaster quadridentata, a parasitoid of Cydia pomonella. J. Chem. Ecol. 25:2229–2245.

    Article  CAS  Google Scholar 

  • Eller, F. J., Bartelt, R. J., Jones, R. L., and Kulman, H. M. 1984. Ethyl (Z)-9-hexadecenoate: A sex pheromone of Syndipnus rubiginosus, Hymenoptera, Ichneumonidae a sawfly parasitoid. J. Chem. Ecol. 10:291–300.

    Article  CAS  Google Scholar 

  • Fauvergue, X., Hopper, K. R., and Antolin, M. F. 1995. Mate finding via a trail sex pheromone by a parasitoid wasp. Proc. Natl. Acad. Sci. USA 92:900–904.

    Article  PubMed  CAS  Google Scholar 

  • Field, S. A. and Keller, M. A. 1994. Localization of the female pheromone gland in Cotesia rubecula Marshall (Hymenoptera: Braconidae). J. Hymenopt. Res. 3:151–156.

    Google Scholar 

  • Fuester, R. W., Taylor, P. B., and Groce, J. C. Jr. 1987. Reproductive response of Glyptapanteles flavicoxis (Hymenoptera: Braconidae) to various densities and instars of the gypsy moth, Lymantria dispar (Lepidoptera: Lymantriidae). Ann. Entomol. Soc. Am. 80:750–757.

    Google Scholar 

  • Gries, R., Khaskin, G., Gries, G., Bennett, R. G., King, S. G. G., Morewood, P., Slessor, K. N., and Morewood, W. D. 2002. (Z,Z)-4,7-Tridecadien-(S)-2-yl acetate: Sex pheromone of Douglas-fir cone gall midge, Contarinia oregonensis. J. Chem. Ecol. 11:2283–2297.

    Article  Google Scholar 

  • Hu, C., Barbosa, P., and Martinat, P. 1986. Influence of rearing conditions on the survival and reproduction of Glyptapanteles flavicoxis (Marsh). J. Appl. Ent. 101:525–531.

    Article  Google Scholar 

  • Huwyler, S. 1972. Ultramikromethoden. Acetylierung von Alkoholen. Experientia 28:718–719.

    Article  PubMed  CAS  Google Scholar 

  • Kainoh, Y. 1999. Parasitoids, pp. 383–404, in J. Hardie and A. K. Minks (eds.). Pheromones of Non-lepidopteran Insects Associated with Agricultural Plants, Oxford University Press, Oxford, p. 480.

    Google Scholar 

  • Kainoh, Y., Nemoto, T., Shimizu, K., Tatsuki, S., Kusano, T., and Kuwahara, Y. 1991. Mating behavior of Ascogaster reticulatus Watanabe (Hymenoptera: Braconidae), an egg–larval parasitoid of the smaller tea tortrix, Adoxophyes sp. (Lepidoptera: Tortricidae). III. Identification of a sex pheromone. Appl. Entomol. Zool. 26:543–549.

    CAS  Google Scholar 

  • Kamano, Y., Shimizu, K., Kainoh, Y., and Tatsuki, S. 1989. Mating behavior of Ascogaster reticulatus Watanabe (Hymenoptera: Braconidae), an egg–larval parasitoid of the smaller tea tortrix, Adoxophyes sp. (Lepidoptera: Tortricidae). II Behavioral sequence and a role of sex pheromone. Appl. Entomol. Zool. 24:372–378.

    Google Scholar 

  • Kimani, S. W. and Overholt, W. A. 1995. Biosystematics of the Cotesia flavipes complex (Hymenoptera, Braconidae)—Interspecific hybridization, sex-pheromone and mating behavior studies. Bull. Entomol. Res. 85:379–386.

    Article  Google Scholar 

  • Krause, S. C., Fuester, R. W., and Burbutis, P. P. 1990. Competitive interactions between Cotesia melanoscelus and Glyptapanteles flavicoxis (Hymenoptera: Braconidae): Implications for biological control of gypsy moth (Lepidoptera: Lymantriidae). Environ. Entomol. 19:1543–1546.

    Google Scholar 

  • Marchand, D. and McNeil, J. N. 2000. Effects of wind speed and atmospheric pressure on the mate searching behavior in the aphid parasitoid Aphidius nigripes (Hymenoptera: Aphidiidae). J. Insect Behav. 13:187–199.

    Article  Google Scholar 

  • Marsh, P. M. 1979. The braconid (Hymenoptera) parasites of the gypsy moth, Lymantria dispar (Lepidoptera: Lymantriidae). Ann. Entomol. Soc. Am. 72:794–810.

    Google Scholar 

  • McNeil, J. N. and Brodeur, J. 1995. Pheromone-mediated mating in the aphid parasitoid, Aphidius nigripes (Hymenoptera: Aphididae). J. Chem. Ecol. 21:959–972.

    Article  CAS  Google Scholar 

  • Millar, J. G. and Haynes, F. K. 1998. Methods in Chemical Ecology, Vol. 1. Kluwer Academic Publishers, Dordrecht.

    Google Scholar 

  • Nazzi, F., Powell, W., Wadhams, L. J., and Woodcock, C. M. 1996. Sex pheromone of aphid parasitoid Praon volucre (Hymenoptera, Braconidae). J. Chem. Ecol. 22:1169–1175.

    Article  CAS  Google Scholar 

  • Obara, M. and Kitano, H. 1974. Studies on the courtship behavior of Apalanteles glomeratus L. I. Experimental studies on releaser of wing-vibrating behavior in the male. Kontyu 42:208–214.

    Google Scholar 

  • Pompanon, F., Deschepper, B., Mourer, Y., Fouillet, P., and Bouletreau, M. 1997. Evidence for a substrate-borne sex pheromone in the parasitoid wasp Trichogramma brassicae. J. Chem. Ecol. 23:1349–1360.

    Article  CAS  Google Scholar 

  • Quimio, G. M. and Walter, G. H. 2000. Swarming, delayed sexual maturation of males and mating behavior of Fopius arisanus (Sonan) (Hymenoptera: Braconidae). J. Insect Behav. 13:797–813.

    Article  Google Scholar 

  • Robacker, D. C. and Hendry, L. B. 1977. Neral and geranial: components of the sex pheromone of the parasitic wasp, Itoplectis conquisitor. J. Chem. Ecol. 3:563–577.

    Article  CAS  Google Scholar 

  • Shu, S. and Jones, R. L. 1993. Evidence for a multicomponent sex pheromone in Eriborus terebrans (Gravenhorst) (Hymenoptera: Ichneumonidae), a larval parasitoid of the European corn borer. J. Chem. Ecol. 19:2563–2576.

    Article  CAS  Google Scholar 

  • Sivinski, J. and Webb, J. C. 1989. Acoustic signals produced during courtship in Diachasmimorpha (= Biosteres) longicaudata (Hymenoptera: Braconidae) and other Braconidae. Ann. Entomol. Soc. Am. 82:116–120.

    Google Scholar 

  • Staddon, B. W. and Everton, I. J. 1980. Haemolymph of the milkweed bug Oncopeltus fasciatus (Heteroptera; Lygaeidae): inorganic constituents and amino acids. Comp. Biochem. Physiol. 64A:371–374.

    Article  Google Scholar 

  • Stanley, G. 1979. Reaction gas chromatography in sealed glass capillaries. Dehydration, reduction and oxidation reactions, and the synthesis of reference compounds. J. Chromatogr. 178:487–493.

    Article  CAS  Google Scholar 

  • Swedenborg, P. D. and Jones, R. L. 1992a. Multicomponent sex pheromone in Macrocentrus grandii Goidanich (Hymenoptera: Braconidae). J. Chem. Ecol. 18:1901–1912.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Swedenborg, P. D., Jones, R. L., Liu, H., and Krick, T. P. 1993. (3R,5S,6R)-3,5-Dimethyl-6-(methylethyl)-3,4,5,6-tetrahydropyran-2-one, a third sex pheromone component for Macrocentrus grandii Goidanich (Hymenoptera: Braconidae) and evidence for its utility at eclosion. J. Chem. Ecol. 19:485–502.

    Article  CAS  Google Scholar 

  • Syvertsen, T. C., Jackson, L. L., Blomquist, G. J., and Vinson, S. B. 1995. Alkadienes mediating courtship in the parasitoid Cardiochiles nigriceps (Hymenoptera: Braconidae). J. Chem. Ecol. 21:1971–1989.

    Article  CAS  Google Scholar 

  • Tagawa, J. 1977. Localization and histology of the female sex pheromone-producing gland in the parasitic wasp, Apanteles glomeratus. J. Insect Physiol. 23:49–56.

    Article  PubMed  CAS  Google Scholar 

  • Tagawa, J. 1983. Female sex pheromone glands in the parasitic wasps, genus Apanteles. Appl. Entomol. Zool. 18:416–427.

    Google Scholar 

  • Van den Dool, H. and Kratz, P. D. 1963. A generalization of the retention index system including linear temperature programmed gas–liquid partition chromatography. J. Chromatogr. 2:463–471.

    Article  Google Scholar 

  • 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 

  • Weseloh, R. M. 1976. Dufour's gland: source of sex pheromone in a hymenopterous parasitoid. Science 193:695–697.

    Article  PubMed  CAS  Google Scholar 

  • Weseloh, R. M. 1980. Sex pheromone gland of the gypsy moth parasitoid, Apanteles melanoscelus: Revaluation and ultrastructural survey. Ann. Entomol. Soc. Am. 73:576–580.

    Google Scholar 

  • Zar, J. H. 1996. Biostatistical Analysis. Prentice-Hall, Upper Saddle River, NJ.

    Google Scholar 

Download references

Acknowledgments

We thank Carl Lowenberger for review of the manuscript, Susan Barth, Kenneth Swan, Philip Taylor, and Roger Fuester for supplying experimental insects, Bob Birtch for graphical illustrations, and two anonymous reviewers and Jeremy McNeil for constructive comments. This research was supported, in part, by a graduate fellowship from Simon Fraser University to A.D. and by a Discovery Grant and Industrial Research Chair from the Natural Sciences and Engineering Research Council of Canada (NSERC) to G.G., with Phero Tech. Inc., SC Johnson Canada, and Global Forest as industrial sponsors. Experimental insects were maintained in SFU's Global Forest Quarantine Facility, construction of which was completed through financial support from Global Forest (GF-18-2000-SFU-8).

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, Canada, V5A 1S6

    Adela Danci, Regine Gries & Gerhard Gries

  2. United States Department of Agriculture, Agricultural Research Service, Beneficial Insects Introduction Research Laboratory, Newark, DE, 19713, USA

    Paul W. Schaefer

Authors
  1. Adela Danci
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Regine Gries
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paul W. Schaefer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gerhard Gries
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gerhard Gries.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Danci, A., Gries, R., Schaefer, P.W. et al. Evidence for Four-Component Close-Range Sex Pheromone in the Parasitic Wasp Glyptapanteles flavicoxis . J Chem Ecol 32, 1539–1554 (2006). https://doi.org/10.1007/s10886-006-9068-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-006-9068-1

Keywords

Search

Navigation