Hostname: page-component-cb9f654ff-lqqdg Total loading time: 0 Render date: 2025-08-09T11:58:55.467Z Has data issue: false hasContentIssue false
  • English
  • Français

Female-induced increase of host-plant volatiles enhance specific attraction of aphid male Dysaphis plantaginea (Homoptera: Aphididae) to the sex pheromone

Published online by Cambridge University Press:  19 February 2009

R.W.H.M. van Tol ,
H.H.M. Helsen ,
F.C. Griepink  and
W.J. de Kogel
R.W.H.M. van Tol*
Affiliation:
Plant Research International, Wageningen-UR, PO Box 69, 6700 AB Wageningen, The Netherlands
H.H.M. Helsen
Affiliation:
Applied Plant Research, Wageningen-UR, Lingewal 1, 6668 LA Randwijk, The Netherlands
F.C. Griepink
Affiliation:
Plant Research International, Wageningen-UR, PO Box 69, 6700 AB Wageningen, The Netherlands
W.J. de Kogel
Affiliation:
Plant Research International, Wageningen-UR, PO Box 69, 6700 AB Wageningen, The Netherlands
*
*Author for correspondence Fax: +31 317 418094 E-mail: rob.vantol@wur.nl
Get access Rights & Permissions [Opens in a new window]

Abstract

All aphid species studied so far share the same sex pheromone components, nepetalactol and nepetalactone. Variation by different enantiomers and blends of the two components released by different aphid species are limited and can only partially explain species-specific attraction of males to females. While some host-plant odours are known to enhance specific attraction of aphid species, herbivore-induced plant volatiles that synergise attractiveness to the sex pheromone are unknown. Here, we demonstrate that for the host-alternating rosy apple aphid (Dysaphis plantaginea (Passerini)) specificity of attraction of males to females is triggered by female-induced tree odours in combination with a 1:8 ratio of (4aS,7S,7aR)-nepetalactone and (1R,4aS,7S,7aR)-nepetalactol. Female aphid infestation induces increased release of four esters (hexyl butyrate, (E)-2-hexenyl butyrate, (Z)-3-hexenyl 3-methylbutyrate and hexyl 2-methylbutyrate) from apple leaves. Two different combinations of three esters applied in a 1:1:1 ratio increase the number of male D. plantaginea and decrease the number of other aphid species caught in water traps in the presence of the pheromone components. The ester blend alone was not attractive. Combination of the pheromone blend with each single ester was not increasing attraction of male D. plantaginea. The demonstration that sexual aphid species use herbivore-induced plant volatiles as a species-specific attractant for mate finding adds a new dimension to our understanding of insect species using or manipulating chemical cues of host plants for orientation.

Keywords

Dysaphis plantaginearosy apple aphidMalussexual kairomonepheromoneherbivore-induced plant volatiles

Information

Type
Research Paper
Information
Bulletin of Entomological Research , Volume 99 , Issue 6 , December 2009 , pp. 593 - 602
Copyright
Copyright © 2009 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Alford, D.V. (1984) A Colour Atlas of Fruit Pests. London, UK, Wolfe.Google Scholar
Bengtsson, M., Bäckman, A-C., Liblikas, I., Ramirez, M.I., Borg-Karlson, A-K., Ansebo, L., Anderson, P., Löfqvist, J. & Witzgall, P. (2001) Plant odor analysis of apple: antennal response of codling moth females to apple volatiles during phenological development. Journal of Agricultural and Food Chemistry 49, 3736–3741.CrossRefGoogle ScholarPubMed
Bernasconi, M.L., Turlings, T.C.J., Ambrosetti, L., Bassetti, P. & Dorn, S. (1998) Herbivore-induced emissions of maize volatiles repel the corn leaf aphid, Rhopalosiphum maidis. Entomologia Experimentalis et Applicata 87, 133–142.CrossRefGoogle Scholar
Blackman, R. & Eastop, V.F. (1984) Aphids on the World's Crops: An Identification and Information Guide. Chichester, UK, John Wiley & Sons Ltd.Google Scholar
Blommers, L.H.M., Helsen, H.H.M. & Vaal, F.W.N.M. (2004) Life history data of the rosy apple aphid Dysaphis plantaginea (Pass.) (Homopt., Aphididae) on plantain and as migrant to apple. Journal of Pesticide Science 77, 155–163.Google Scholar
Bonnemaison, L. (1959) Le puceron cendr‘e du pommier (Dysaphis plantaginea Pass.) – Morphologie et biologie – Methodes de lutte. Annales INRA, Série C Epiphytes 10, 257–329.Google Scholar
Campbell, C.A.M., Dawson, G.W., Griffiths, D.C., Pettersson, J., Pickett, J.A., Wadhams, L.J. & Woodcock, C.M. (1990) Sex attractant pheromone of the damson-hop aphid Phorodon humuli (Homoptera: Aphididae). Journal of Chemical Ecology 16, 3455–3465.CrossRefGoogle ScholarPubMed
Du, Y.J., Poppy, G.M., Powell, W., Pickett, J.A., Wadhams, L.J. & Woodcock, C.M. (1998) Identification of semiochemicals released during aphid feeding that attract parasitoid Aphidius ervi. Journal of Chemical Ecology 24, 1355–1368.CrossRefGoogle Scholar
Eisenbach, J. & Mittler, T.E. (1987) Sex pheromone discrimination by male aphids of a biotype of Schizaphis graminum. Entomologia Experimentalis et Applicata 36(43), 181–182.CrossRefGoogle Scholar
Fitzgerald, J.D., Pope, T.W., Solomon, M.G., Poppy, G.M., Jones, A.S. & Wadhams, L.J. (2005) The use of the aphid sex pheromone and plant volatiles to enhance control of Dysaphis plantaginea in apple. IOBC/WPRS Bulletin 28(7), 395–398.Google Scholar
Goldansaz, S.H., Dewhirst, S., Birkett, M.A., Hooper, A.M., Smiley, D.W.M., Pickett, J.A., Wadhams, L. & McNeil, J.N. (2004) Identification of two sex pheromone components of the potato aphid, Macrosiphum euphorbiae (Thomas). Journal of Chemical Ecology 30, 819–834.CrossRefGoogle ScholarPubMed
Goldansaz, S.H. & McNeil, J.N. (2006) Effect of wind speed on the pheromone-mediated behavior of sexual morphs of the potato aphid, Macrosiphum euphorbiae (Thomas) under laboratory and field conditions. Journal of Chemical Ecology 32, 1719–1729.CrossRefGoogle ScholarPubMed
Guerrieri, E., Pennacchio, F. & Tremblay, E. (1993) Flight behaviour of the aphid parasitoid Aphidius ervi (Hymenoptera: Braconidae) in response to plant and host volatiles. European Journal of Entomology 90, 415–421.Google Scholar
Guldemond, J.A. (1990a) Choice of host plant as a factor in reproductive isolation of the aphid genus Cryptomyzus (Homoptera, Aphididae). Ecological Entomology 15, 43–51.CrossRefGoogle Scholar
Guldemond, J.A. (1990b) Evolutionary genetics of the aphid Cryptomyzus, with a preliminary analysis of the inheritance of host preference, reproductive performance and host-alternation. Entomologia Experimentalis et Applicata 57, 65–76.CrossRefGoogle Scholar
Guldemond, J.A., Dixon, A.F.G., Pickett, J.A., Wadhams, L.J. & Woodcock, C.M. (1993) Specificity of sex pheromones, the role of host plant odour in the olfactory attraction of males, and mate recognition in the aphid Cryptomyzus. Physiological Entomology 18, 137–143.CrossRefGoogle Scholar
Guldemond, J.A. & Dixon, A.F.G. (1994) Specificity and daily cycle of release of sex pheromones in aphids: a case of reinforcement? Biological Journal of the Linnean Society 52, 287–303.CrossRefGoogle Scholar
Guldemond, J.A., Dixon, A.F.G. & Tigges, W.T. (1994) Mate recognition in Cryptomyzus aphids: copulation and insemination. Entomologia Experimentalis et Applicata 73, 67–75.CrossRefGoogle Scholar
Hardie, J., Pickett, J.A., Pow, E.M. & Smiley, D.W.M. (1999) Aphids. pp. 227–250in Hardie, J. & Minks, A.K. (Eds) Pheromones of Non-Lepidopteran Insects Associated with Agricultural Plants. Wallingford, UK, CAB International.CrossRefGoogle Scholar
Hardie, J., Storer, R., Nottingham, S.F., Peace, L., Harrington, R., Merritt, L.A., Wadhams, L.J. & Wood, D.K. (1994) The interaction of sex pheromone and plant volatiles for field attraction of male bird-cherry aphid, Rhopalosiphum padi. pp. 1223–1230 in Brighton Crop Protection Conference – Pests and Diseases, British Crop Protection Council, Thornton Heath, UK.Google Scholar
Hardie, J., Holyoak, M., Nicholas, J., Nottingham, S.F., Pickett, J.A., Wadhams, L.J. & Woodcock, C.M. (1990) Aphid sex pheromone components: Age-dependent release by females and species-specific male response. Chemoecology 1, 63–68.CrossRefGoogle Scholar
Hardie, L., Nottingham, S.F., Powell, W. & Wadhams, L.J. (1991) Synthetic aphid sex pheromone lures female parasitoids. Entomologia Experimentalis et Applicata 61, 97–99.CrossRefGoogle Scholar
Hardie, L., Nottingham, S.F., Dawson, G.W., Harrington, R., Pickett, J.A. & Wadhams, L.J. (1992) Attraction of field-flying aphid males to synthetic sex pheromone. Chemoecology 3, 113–117.CrossRefGoogle Scholar
Heie, O.E. (1982) Aphidoidae (Hemiptera) of Fennoscandia and Denmark. Fauna Entomologia Scandinavia 11, 57–92.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. & Thielking, G. (1996a) The potential of semiochemicals for control of Phorodon humuli (Homoptera: Aphididae). Pesticide Science 48, 293–303.3.0.CO;2-5>CrossRefGoogle Scholar
Lösel, P.M., Lindemann, M., Scherkenbeck, J., Campbell, C.A.M., Hardie, J., Pickett, J.A. & Wadhams, L.J. (1996b) Effect of primary-host kairomones on the attractiveness of the hop-aphid sex pheromone to Phorodon humuli males and gynoparae. Entomologia Experimentalis et Applicata 80, 79–82.CrossRefGoogle Scholar
Marsh, D. (1975) Responses of male aphids to the female sex pheromone in Megoura viciae Buckton. Journal of Entomology 50, 43–64.Google Scholar
Micha, S.G. & Wyss, U. (1995) The importance of plant odors for the host search of Aphidius uzbekistanicus (Hymenoptera, Aphidiidae), a parasitoid of the grain aphid (Sitobion avenae). Gesunde Pflanzen 47, 300–307.Google Scholar
Müller, F.P. (1982) Das Problem Aphis fabae. Zeitschrift für Angewandte Entomologie 94, 432–446.CrossRefGoogle Scholar
Müller, F.P. (1985) Genetric and evolutionary aspects of host choice in phytophagous insects, especially aphids. Biologisches Zentralblatt 104, 225–237.Google Scholar
Nottingham, S.F., Hardie, J., Dawson, G.W., Hick, A.J., Pickett, J.A., Wadhams, L.J. & Woodcock, C.M. (1991) Behavioral and electrophysiological responses of aphids to host and nonhost plant volatiles. Journal of Chemical Ecology 17, 1231–1242.CrossRefGoogle ScholarPubMed
Park, K.C., Elias, D., Donato, B. & Hardie, J. (2000) Electronantennogram and behavioural responses of different forms of the bird cherry-oat aphid, Rhopalosiphum padi, to sex pheromone and a plant volatile. Journal of Insect Physiology 46, 597–604.CrossRefGoogle Scholar
Pettersson, J. (1970a) An aphid sex attractant I. Biological studies. Entomologica Scandinavica 1, 63–73.CrossRefGoogle Scholar
Pettersson, J. (1970b) Studies on Rhopalosiphum padi (L.) I. Laboratory studies on olfactometric responses to the winter host, Prunus padus L. Lantbrukshoegskolans Annaler 36, 381–399.Google Scholar
Pope, T.W., Campbell, C.A.M., Hardie, J., Pickett, J.A. & Wadhams, L.J. (2007) Interactions between host-plant volatiles and the sex pheromones of the bird cherry-oat aphid, Rhopalosiphum padi and the damson-hop aphid, Phorodon humuli. Journal of Chemical Ecology 33, 157–165.CrossRefGoogle ScholarPubMed
Powell, G. & Hardie, J. (2001) The chemical ecology of aphid host alternation: How do return migrants find the primary host plant? Applied Entomology and Zoology 36, 259–267.CrossRefGoogle Scholar
Ruther, J., Reinecke, A. & Hilker, M. (2002) Plant volatiles in the sexual communication of Melolontha hippocastani: response towards time dependent bouquets and novel function of (Z)-3-hexen-1-ol as a sexual kairomone. Ecological Entomology 27, 76–83.CrossRefGoogle Scholar
Steffan, A.W. (1987) Fern- und Nahorientierung geflügelter Gynoparae und Sexualis-Männchen bei Blattläusen (Homoptera: Aphidinea: Aphididae). Entomologia Generalis 12, 235–258.CrossRefGoogle Scholar
Steffan, A.W. (1990) Courtship behaviour and possible pheromone spread by hindleg raising in sexual females of aphids (Homoptera: Aphidinea). Entomologia Generalis 15, 33–49.CrossRefGoogle Scholar
Stroyan, H.L.G. (1957) A revision of the British species of Sappaphis Matsamura. Part I. Introduction and subgenus Sappaphis sensu stricto. London, UK, Ministry of Agriculture, Fisheries and Food.Google Scholar
Stroyan, H.L.G. (1963) A revision of the British species of Dysaphis Börner. Part II. The subgenus Dysaphis sensu stricto. London, UK, Ministry of Agriculture, Fisheries and Food.Google Scholar
Thieme, T. (1988) Zur Biologie von Aphis fabae mordwilkowi Börner und Janisch, 1922 (Hom., Aphididae). Journal of Applied Entomology 105, 510–515.CrossRefGoogle Scholar
Thieme, T. & Dixon, A.F.G. (1996) Mate recognition in the Aphis fabae complex: daily rhythm of release and specificity of sex pheromones. Entomologia Experimentalis et Applicata 79, 85–89.CrossRefGoogle Scholar
Van Tol, R.W.H.M. & Visser, J.H. (2002) Olfactory antennal responses of the vine weevil Otiorhynchus sulcatus to plant volatiles. Entomologia Experimentalis et Applicata 102, 49–64.CrossRefGoogle Scholar
Visser, J.H. & Piron, P.G.M. (1995) Olfactory antennal responses to plant volatiles in apterous virginoparae of the vetch aphid Megoura viciae. Entomologia Experimentalis et Applicata 77, 37–46.CrossRefGoogle Scholar