Skip to main content
SpringerLink
Log in

Dolichodial: A New Aphid Sex Pheromone Component?

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

Abstract

The sex pheromones of many aphid species from the subfamily Aphididae comprise a mixture of the iridoids (cyclopentanoids) (1R,4aS,7S,7aR)-nepetalactol and (4aS,7S,7aR)-nepetalactone. In this paper, we investigate whether other chemicals, in addition to nepetalactol and nepetalactone, are released from Dysaphis plantaginea (rosy apple aphid) oviparae as part of their sex pheromone. Four compounds present in an air entrainment sample collected from D. plantaginea oviparae feeding on apple (Malus silvestris c.v. Braburn) elicited electrophysiological responses from male D. plantaginea. Active peaks were tentatively identified by gas chromatography (GC) coupled with mass spectrometry, with identification confirmed by peak enhancement with authentic compounds on GC columns of different polarities. The electroantennography-active chemicals were (1R,4aS,7S,7aR)-nepetalactol, (4aS,7S,7aR)-nepetalactone, (1S,2R,3S)-dolichodial, and phenylacetonitrile. (1S,2R,3S)-Dolichodial elicited a behavioral response from male D. plantaginea and naïve-mated female parasitoids, Aphidius ervi. This is the first report of electrophysiological and behavioral responses from any aphid morph to (1S,2R,3S)-dolichodial. Whether or not (1S,2R,3S)-dolichodial is a third component of the aphid sex pheromone is discussed.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Bartlet, E., Blight, M. M., Lane, P., and Williams, I. H. 1997. The responses of the cabbage seed weevil Ceutorhynchus assimilis to volatile compounds from oilseed rape in a linear track olfactometer. Entomol. Exp. Appl. 85:257–262.

    Article  Google Scholar 

  • Bellesia, F., Pagnoni, U. M., Pinetti, A., and Trave, R. 1983a. Teucrein, a new iridolactol from Teucrium marum, and its biosynthetic relationship with dolichodial. J. Chem. Res. Synop. 12:328–329.

    Google Scholar 

  • Bellesia, F., Pagnoni, U. M., Pinetti, A., and Trave, R. 1983b. The biosynthesis of dolichodial in Teucrium marum. Phytochemistry 22:2197–2201.

    Article  CAS  Google Scholar 

  • Bellesia, F., Grandi, R., Pagnoni, U. M., Pinetti, A., and Trave, R. 1984. Biosynthesis of nepetalactone in Nepeta cataria. Phytochemistry 23:83–87.

    Article  CAS  Google Scholar 

  • Birkett, M. A., and Pickett, J. A. 2003. Aphid sex pheromones: from discovery to commercial production. Phytochemistry 62:651–656.

    Article  PubMed  CAS  Google Scholar 

  • Blackman, R. L., and Eastop, V. F. 2000. Aphids on the Worlds Crops. 2nd edn. p. 414. Wiley, Chichester.

    Google Scholar 

  • Blommers, L. H. M., Helsen, H. H. M., and Vaal, F. W. N. M. 2004. Life history data of the rosy apple aphid Dysaphis plantaginea (Pass.) (Homoptera: Aphididae) on plantain and as migrant to apple. J. Pest Sci. 77:155–163.

    Article  Google Scholar 

  • Boeve, J. L., Lengwiler, U. B., Tollsten, L., Dorn, S., and Turlings, T. C. J. 1996. Volatiles emitted by apple fruitlets infested by larvae of the European apple sawfly. Phytochemistry 42:373–381.

    Article  CAS  Google Scholar 

  • Boo, K. S., Choi, M. Y., Chung, I. B., Eastop, V. F., Pickett, J. A., Wadhams, L. J., and Woodcock, C. M. 2000. Sex pheromone of the peach aphid, Tuberocephalus momonis and optimal blends for trapping males and females in the field. J. Chem. Ecol. 26:601–609.

    Article  CAS  Google Scholar 

  • Campbell, C. A. M., Dawson, G. W., Griffiths, D. C., Pettersson, J., Pickett, J. A., Wadhams, L. J., and Woodcock, C. M. 1990. Sex attractant pheromone of damson-hop aphid Phorodon humuli (Homoptera: Aphididae). J. Chem. Ecol. 16:3455–3465.

    Article  CAS  Google Scholar 

  • Cavill, G. W. K., and Hinterberger, H. 1960. The chemistry of ants. IV. Terpenoid constituents of some Dolichoderus and Iridomyrmex species. Aust. J. Chem. 13:514–519.

    CAS  Google Scholar 

  • Cavill, G. W. K., and Houghton, E. 1974. Volatile constituents of argentine ant, Iridomyrmex humilis. J. Insect Physiol. 20:2049–2059.

    Article  PubMed  CAS  Google Scholar 

  • Cavill, G. W. K., Robertson, P. L., Brophy, J. J., Clark, D. V., Duke, R., Orton, C. J., and Plant, W. D. 1982. Defensive and other secretions of the Australian cocktail ant, Iridomyrmex nitidiceps. Tetrahedron 38:1931–1938.

    Article  CAS  Google Scholar 

  • Dawson, G. W., Griffiths, D. C., Janes, N. F., Mudd, A., Pickett, J. A., Wadhams, L. J., and Woodcock, C. M. 1987. Identification of an aphid sex-pheromone. Nature 325:614–616.

    Article  CAS  Google Scholar 

  • Dawson, G. W., Griffiths, D. C., Merritt, L. A., Mudd, A., Pickett, J. A., Wadhams, L. J., and Woodcock, C. M. 1990. Aphid semiochemicals: a review, and recent advances on the sex-pheromone. J. Chem. Ecol. 16:3019–3030.

    Article  CAS  Google Scholar 

  • Dawson, G. W., Pickett, J. A., and Smiley, D. W. M. 1996. The aphid sex pheromone cyclopentanoids: synthesis in the elucidation of structure and biosynthetic pathways. Bioorg. Med. Chem. 4:351–361.

    Article  PubMed  CAS  Google Scholar 

  • De Berardinis, E., Baronio, P., and Baumgartner, J. 1994. The effect of aphid (Dysaphis plantaginea Pass., Homoptera: Aphididae) feeding on apple fruit-growth. Ecol. Model. 72:115–127.

    Article  Google Scholar 

  • Douloumpaka, S., and Van Emden, H. F. 2003. A maternal influence on the conditioning to plant cues of Aphidius colemani Viereck, parasitizing the aphid Myzus persicae Sulzer. Physiol. Entomol. 28:108–113.

    Article  Google Scholar 

  • Forrest, J. M. S., and Dixon, A. F. G. 1975. The induction of leaf-roll galls by the apple aphids Dysaphis devecta and D. plantaginea. Ann. Appl. Biol. 81:281–288.

    Article  Google Scholar 

  • Glinwood, R. T. 1998. Response of aphid parasitoids to aphid sex pheromones: laboratory and field studies, Ph.D. Thesis. The University of Nottingham.

  • Goldansaz, S. H., Dewhirst, S. Y., Birkett, M. A., Hooper, A. M., Smiley, D. W. M., Pickett, J. A., Wadhams, L. J., and McNeil, J. N. 2004. Identification of two sex pheromone components of the potato aphid, Macrosiphum euphorbiae (Thomas). J. Chem. Ecol. 30:819–834.

    Article  PubMed  CAS  Google Scholar 

  • Gomez, K. A. 1984. Statistical Procedures for Agricultural Research. p. 680. Wiley, New York.

    Google Scholar 

  • Graf, B. 1999. Optimising the control of rosy apple aphid Dysaphis plantaginea (Pass.) (Homoptera: Aphididae). IOBC/WPRS Bull. 22:71–76.

    Google Scholar 

  • Guldemond, J. A., Dixon, A. F. G., Pickett, J. A., Wadhams, L. J., and Woodcock, C. M. 1992. The role of host plant odour and sex pheromones in mate recognition in the aphid Cryptomyzus. Proceedings of the 8th International Symposium of Insect-Plant Relationships, 119–121.

  • Guldemond, J. A., Dixon, A. F. G., Pickett, J. A., Wadhams, L. J., and Woodcock, C. M. 1993. Specificity of sex-pheromones, the role of host-plant odor in the olfactory attraction of males, and mate recognition in the aphid Cryptomyzus. Physiol. Entomol. 18:137–143.

    Article  CAS  Google Scholar 

  • Hardie, J., Holyoak, M., Nicholas, J., Nottingham, S. F., Pickett, J. A., Wadhams, L. J., and Woodcock, C. M. 1990. Aphid sex pheromone components: age-dependent release by females and species-specific male response. Chemoecology 1:63–68.

    Article  CAS  Google Scholar 

  • Hardie, J., Visser, J. H., and Piron, P. G. M. 1994. Perception of volatiles associated with sex and food by different adult forms of the black bean aphid, Aphis fabae. Physiol. Entomol. 19:278–284.

    Article  CAS  Google Scholar 

  • Knudsen, J. T., Tollsten, L., and Bergstrom, L. G. 1993. Floral scents—a checklist of volatile compounds isolated by headspace techniques. Phytochemistry 33:253–280.

    Article  CAS  Google Scholar 

  • Leal, W. S., Ono, M., Hasegawa, M., and Sawada, M. 1994. Kairomone from dandelion, Taraxacum officinale, attractant for scarab beetle Anomala octiescostata. J. Chem. Ecol. 20:1697–1704.

    Article  CAS  Google Scholar 

  • Lilley, R., and Hardie, J. 1996. Cereal aphid responses to sex pheromones and host-plant odours in the laboratory. Physiol. Entomol. 21:304–308.

    Article  CAS  Google Scholar 

  • Lösel, P. M., Lindemann, M., Scherkenbeck, J., Maier, J., Engelhard, B., Campbell, C. A. M., Hardie, J., Pickett, J. A., Wadhams, L. J., Elbert, A., and Thielking, G. 1996. The potential of semiochemicals for control of Phorodon humuli (Homoptera: Aphididae). J. Pest Sci. 48:293–303.

    Article  Google Scholar 

  • Loughrin, J. H., Potter, D. A., and Hamilton-Kemp, T. R. 1995. Volative compounds induced by herbivory act as aggregation kairomones for the Japanese beetle (Popillia japonica Newman). J. Chem. Ecol. 21:1457–1467.

    Article  CAS  Google Scholar 

  • MacLeod, A. J., Pieris, N. M., and Gil, V. 1981. Volatile components of sugar beet leaves. Phytochemistry 20:2292–2295.

    Article  CAS  Google Scholar 

  • Maddrell, S. H. 1969. Secretion by malpighian tubules of Rhodnius: movements of ions and water. J. Exp. Biol. 51:71–97.

    CAS  Google Scholar 

  • Marsh, D. 1972. Sex pheromone in the aphid Megoura viciae. Nature 238:31–32.

    Article  CAS  Google Scholar 

  • Marsh, D. 1975. Responses of male aphids to female sex pheromone in Megoura viciae Buckton. J. Entomol. Ser. A. Physiol. Behav. 50:43–64.

    Google Scholar 

  • Meinwald, J., Chadha, M. S., Hurst, J. J., and Eisner, T. 1962. Defense mechanisms of arthropods. 9. Anisomorphal, the secretion of a phasmid insect. Tetrahedron 1:29–33.

    Google Scholar 

  • Montgomery, D. C. 1997. Design and Analysis of Experiments. 4th edn. p. 704. Wiley, New York.

    Google Scholar 

  • Norris, M. J., and Pener, M. P. 1965. A inhibitory effect of allatectomized males and females on the sexual maturation of young male adults of Schistocerca gregaria (Forskal) (Orthoptera: Acrididae). Nature 208:1122.

    Article  Google Scholar 

  • Obeng-Ofori, D., Torto, B., and Hassanali, A. 1993. Evidence for mediation of two releaser pheromones in the aggregation behavior of the gregarious desert locust, Schistocerca gregaria (Forskal) (Orthoptera, Acrididae). J. Chem. Ecol. 19:1665–1676.

    Article  Google Scholar 

  • Pagnoni, U. M., Pinetti, A., Trave, R., and Garanti, L. 1976. Monoterpenes of Teucrium marum. Aust. J. Chem. 29:1375–1381.

    Article  CAS  Google Scholar 

  • Park, K. C., Elias, D., Donato, B., and Hardie, J. 2000. Electroantennogram and behavioural responses of different forms of the bird cherry-oat aphid, Rhopalosiphum padi, to sex pheromone and a plant volatile. J. Insect Physiol. 46:597–604.

    Article  PubMed  CAS  Google Scholar 

  • Payne, R. W., Murray, D. A., Harding, S. A., Baird, D. B., and Soutar, D. M. 2005. GenStat® for Windows®—Introduction. 8th edn. p. 359. VSN International, Hemel Hempstead.

    Google Scholar 

  • Pettersson, J. 1970. An aphid sex attractant I. Biological studies. Entomol. Scan. 1:63–73.

    Google Scholar 

  • Powell, G., and Hardie, J. 2001. The chemical ecology of aphid host alternation: how do return migrants find the primary host plant? Appl. Entomol. Zoolog. 36:259–267.

    Article  Google Scholar 

  • Rawlings, J. O., Pantula, S. G., and Dickey, D. A. 1998. Applied Regression Analysis: A Research Tool. p. 657. Springer, New York.

    Google Scholar 

  • Stewart-Jones, A., Dewhirst, S. Y., Durrant, L., Fitzgerald, J. D., Hardie, J., Hooper, A. M., Pickett, J. A., and Poppy, G. M. 2007. Structure, ratios and patterns of release in the sex pheromone of an aphid, Dysaphis plantaginea. J. Exp. Biol. 210:4335–4344.

    Article  PubMed  CAS  Google Scholar 

  • Tatsuka, K., Suekane, S., Sakai, Y., and Sumitani, H. 1990. Volatile constituents of kiwi fruit flowers: simultaneous distillation and extraction versus headspace sampling. J. Agric. Food Chem. 38:2176–2180.

    Article  CAS  Google Scholar 

  • Torto, B., Obeng-Ofori, D., Njagi, P. G. N., Hassanali, A., and Amiani, H. 1994. Aggregation pheromone system of adult gregarious desert locust Schistocerca gregaria (Forskal). J. Chem. Ecol. 20:1749–1762.

    Article  CAS  Google Scholar 

  • Vamvatsikos, P. G. 2006. Olfactory behaviours associated with host-aphid location in a generalist parasitoid wasp, PhD. University of London.

  • Wyss, E., Villiger, M., Hemptinne, J. L., and Scharer, H. M. 1999. Effects of augumentative release of eggs and larvae of the ladybird beetle, Adalia bipuncata, on the abundance of the rosy apple aphid, Dysaphis plantaginea, in organic apple orchards. Entomol. Exp. Appl. 90:167–173.

    Article  Google Scholar 

  • Zhu, J. W., Zhang, A. J., Park, K. C., Baker, T. C., Lang, B., Jurenka, R., Obrycki, J. J., Graves, W. R., Pickett, J. A., Smiley, D., Chauhan, K. R., and Klun, J. A. 2006. Sex pheromone of the soybean aphid, Aphis glycines Matsumura, and its potential use in semiochemical-based control. Environ. Entomol. 35:249–257.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Rothamsted Research receives grant-aided support from the Biotechnology and Biological Sciences Research Council (BBSRC) of the UK. This work was supported by funds from the UK Department for Environment, Food and Rural Affairs. Rothamsted Research receives grant-aided support from the UK. Many thanks to Dr Salvador Gezan who provided statistical guidance and Tom Palmer, manager of the Leckford Estate Fruit Farm, for permission to use the apple orchards.

Author information

Authors and Affiliations

  1. Biological Chemistry Department, Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK

    Sarah Y. Dewhirst, Michael A. Birkett, Lester J. Wadhams, Christine M. Woodcock & John A. Pickett

  2. East Malling Research, New Road, East Malling, Kent, ME19 6BJ, UK

    Jean D. Fitzgerald

  3. School of Biological Sciences, University of Southampton, Bassett Crescent East, Southampton, SO16 7PX, UK

    Alex Stewart-Jones

  4. Department of Life Sciences, Imperial College London, Silwood Park campus, Ascot, Berkshire, SL5 7PY, UK

    Jim Hardie

Authors
  1. Sarah Y. Dewhirst
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael A. Birkett
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jean D. Fitzgerald
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alex Stewart-Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lester J. Wadhams
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Christine M. Woodcock
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jim Hardie
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. John A. Pickett
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sarah Y. Dewhirst.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dewhirst, S.Y., Birkett, M.A., Fitzgerald, J.D. et al. Dolichodial: A New Aphid Sex Pheromone Component?. J Chem Ecol 34, 1575–1583 (2008). https://doi.org/10.1007/s10886-008-9561-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-008-9561-9

Keywords

Search

Navigation