Hostname: page-component-7bb8b95d7b-qxsvm Total loading time: 0 Render date: 2024-09-24T01:09:00.070Z Has data issue: false hasContentIssue false
  • English
  • Français

Olfactory conditioning in mate searching by the parasitoid Aphidius ervi (Hymenoptera: Braconidae)

Published online by Cambridge University Press:  25 February 2008

C.A. Villagra ,
R.A. Vásquez  and
H.M. Niemeyer
C.A. Villagra*
Affiliation:
Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile
R.A. Vásquez
Affiliation:
Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile Instituto de Ecología y Biodiversidad, Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile
H.M. Niemeyer
Affiliation:
Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile
*
*Author for correspondence Fax: 1 (607) 254 1303 E-mail: cavillagra@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Despite the fact that insect learning capacity has been broadly demonstrated, the role that this process plays during mate searching has been scarcely explored. We studied whether the sexual behaviour of a male parasitic wasp can be conditioned to the odours from two alternative host plant complexes (HPCs) present during its first copulation. The experimental subjects were newly emerged males of the aphid parasitoid, Aphidius ervi, and two alternative HPCs (alfalfa or wheat). In the training protocol, copulation experience corresponded to an unconditioning stimulus and HPC odours to the conditioning stimuli. The initial (just after eclosion) and trained responses were assessed in a glass Y-olfactometer. The results showed that neither alfalfa HPC nor wheat HPC stimuli elicited sexual-related behaviours in initial male responses. Conversely, both HPCs triggered strong attraction and wing fanning courtship behaviour in trained responses when the male was exposed to a female plus HPC during training. In males trained with females plus a given HPC but tested with the alternative HPC in the olfactometer, trained response showed a similar trend to the non-associative treatments. Hence, through learning, the olfactory stimulus context present during copulation could become a predictive cue for further mate searching. These results are discussed in terms of parasitic wasp ecology and host fidelity.

Keywords

insect sexual learningconditioned place preferencehost fidelity
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 98 , Issue 4 , August 2008 , pp. 371 - 377
Copyright
Copyright © 2008 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.)

References

Assem, J. van den (1986) Mating behavior in parasitc wasps. pp. 125–157in Waage, J.D. (Ed.) Insect Parasitoids. New York, USA, Academic Press.Google Scholar
Atanassova, P., Brookes, C.P., Loxdale, H.D. & Powell, W. (1998) Electrophoretic study of five aphid parasitoid species of the genus Aphidius (Hymenoptera: Braconidae), including evidence for reproductively isolated sympatric populations and cryptic species. Bulletin of Entomological Research 88, 3–13.CrossRefGoogle Scholar
Battaglia, D., Isidoro, N., Romani, R., Bin, F. & Pennacchio, F. (2002) Mating behaviour of Aphidius ervi (Hymenoptera: Braconidae): the role of antennae. European Journal of Entomology 99, 451–456.CrossRefGoogle Scholar
Blumstein, D.T., Evans, C.S. & Daniel, J.C. (2000) JWatcher 0.9. An Introductory User′s Guide. Animal Behaviour Laboratory, Macquarie University, Australia. http://galliform.psy.mq.edu.au/jwatcher/.Google Scholar
Bush, G.L. (1968) Sympatric host race formation and speciation in frugivorous flies of the genus Rhagoletis (Diptera: Tephritidae). Evolution 23, 237–251.CrossRefGoogle Scholar
Bush, G.L. (1994) Sympatric speciation in animals – new wine in old bottles. Trends in Ecology and Evolution 9, 285–288.Google ScholarPubMed
Butlin, R.K. (1990) Divergence in emergence time of host races due to differential gene flow. Heredity 65, 47–50.CrossRefGoogle ScholarPubMed
Cameron, P.J., Powell, W. & Loxdale, D.H. (1984) Reservoirs for Aphidius ervi Haliday (Hymenoptera: Aphidiidae), a polyphagous parasitoid of cereal aphids (Hemiptera, Aphididae). Bulletin of Entomological Research 74, 647–656.CrossRefGoogle Scholar
Colwell, R.K. (1986) Population structure and sexual selection for host fidelity in the speciation of hummingbird flower mites. pp. 475–495in Karlin, S. & Nevo, E. (Eds) Evolutionary Process and Theory. London, UK, Academic Press.CrossRefGoogle Scholar
Conover, W.J. & Iman, R.L. (1982) Analysis of covariance using the rank transformation. Biometrics 38, 715–724.CrossRefGoogle ScholarPubMed
Coria-Avila, G.A., Ouimet, A.J., Pacheco, P., Manzo, J. & Pfaus, J.G. (2005) Olfactory conditioned partner preference in the female rat. Behavioral Neuroscience 119, 716–725.CrossRefGoogle ScholarPubMed
Dicke, M. & van Loon, J.J.A. (2000) Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomologia Experimentalis et Applicata 97, 237–249.CrossRefGoogle Scholar
Dieckmann, U. & Doebeli, M. (1999) On the origin of species by sympatric speciation. Nature 400, 354–357.CrossRefGoogle ScholarPubMed
Du, Y.J., Poppy, G.M., Powell, W. & Wadhams, L.J. (1997) Chemically mediated associative learning in the host foraging behavior of the aphid parasitoid Aphidius ervi (Hymenoptera: Braconidae). Journal of Insect Behavior 10, 509–522.CrossRefGoogle Scholar
Dukas, R. (2005) Learning affects mate choice in female fruit flies. Behavioral Ecology 16, 800–804.CrossRefGoogle Scholar
Everitt, B.J. (1990) Sexual motivation: a neural and behavioral analysis of the mechanisms underlying appetitive and copulatory responses of male rats. Neuroscience and Biobehavioral Reviews 14, 217–232.CrossRefGoogle ScholarPubMed
Frías, D. (1988) Tiempos y modos de especiación. pp. 158–171in Santibáñez-Lara, I. (Ed.) Manejo del Tiempo en Biología y Algunas de Sus Ingeniosas Maneras de Estudiarlo. Santiago, Chile, Facultad de Medicina, Universidad de Chile.Google Scholar
Glinwood, R.T., Du, Y.J. & Powell, W. (1999) Responses to aphid sex pheromones by the pea aphid parasitoids Aphidius ervi and Aphidius eadyi. Entomological Experimentalis et Applicata 92, 227–232.CrossRefGoogle Scholar
He, X.Z. & Teulon, D.A.J. (2004) Emergence, sexual maturation and oviposition of Aphidius ervi (Hymenoptera: Aphidiidae). New Zealand Plant Protection 57, 214–220.CrossRefGoogle Scholar
Hirsch, H.V.B. (1994) The flexible fly: experience-dependent development of complex behaviors in Drosophila melanogaster. Journal of Experimental Biology 195, 1–18.CrossRefGoogle ScholarPubMed
Hoffmann, H., Janssen, E. & Turner, S.L. (2004) Classical conditioning of sexual arousal in women and men: effects of varying awareness and biological relevance of the conditioned stimulus. Archives of Sexual Behavior 33, 43–53.CrossRefGoogle ScholarPubMed
Immelman, K. (1975) Ecological significance of imprinting and early learning. Annual Review of Ecology and Systematics 6, 15–37.CrossRefGoogle Scholar
Kateri, M., Papaioannu, T. & Dellaportas, P. (2001) Bayesian analysis of correlated proportions. Sankhya: The Indian Journal of Statistics 63, 270–285.Google Scholar
Landolt, P.L. & Phillips, T.W. (1997) Host plant influences on sex pheromone behaviour of phytophagous insects. Annual Review of Entomology 42, 371–391.CrossRefGoogle ScholarPubMed
Lewis, W.J. & Tumlinson, J.H. (1988) Host detection by chemically mediated associative learning in a parasitic wasp. Nature 331, 257–259.CrossRefGoogle Scholar
Mackauer, M. (1969) Sexual behaviour of and hybridization between three species of Aphidius Nees parasitic on the pea aphid. Proceedings of the Entomological Society of Washington 71, 339–351.Google Scholar
Mackauer, M. & Finlayson, T. (1967) The hymenopterous parasites (Hymenoptera: Aphidiidae et Aphelinidae) of the pea aphid in eastern North America. Canadian Entomologist 99, 1051–1082.CrossRefGoogle Scholar
Maturana, H.R. & Mpodozis, J.M. (2000) The origin of species by means of natural drift. Revista Chilena de Historia Natural 73, 262–310.Google Scholar
McNemar, Q. (1947) Note on the sampling error of the difference between correlated proportions or percentages. Psychometrika 12, 153–157.CrossRefGoogle ScholarPubMed
Němec, V. & Starý, P. (1985) Genetic diversity of the parasitoid Aphidius ervi on the pea aphid, Acyrthosiphon pisum in Czechoslovakia (Hymenoptera: Aphidiidae; Homoptera, Aphididae). Acta Entomologica Bohemoslovaca 82, 88–94.Google Scholar
O'Donohue, W. & Plaud, J.J. (1994) The conditioning of human sexual arousal. Archives of Sexual Behavior 23, 321–344.CrossRefGoogle ScholarPubMed
Olson, D.M., Rains, G.C., Meiners, T., Takasu, K., Tertuliano, M., Tumlinson, J.H., Wäckers, F.L. & Lewis, W.J. (2003) Parasitic wasps learn and report diverse chemicals with unique conditionable behaviors. Chemical Senses 28, 545–549.CrossRefGoogle ScholarPubMed
Pfaus, J.G., Kippin, T.E. & Centeno, S. (2001) Conditioning and sexual behavior: a review. Hormones and Behavior 40, 291–321.CrossRefGoogle ScholarPubMed
Quicke, D.L.J. (1997) Parasitic Wasps. 470 pp. London, UK, Chapman & Hall.Google Scholar
Ramírez, C.C., Fuentes-Contreras, E., Rodríguez, L.C. & Niemeyer, H.M. (2000) Pseudoreplication and its frequency in olfactometric laboratory studies. Journal of Chemical Ecology 26, 1426–1431.CrossRefGoogle Scholar
Rice, W.R. & Hostert, E.E. (1993) Laboratory experiments on speciation – what have we learned in 40 years? Evolution 47, 1637–1653.CrossRefGoogle Scholar
Robacker, D.C. & Hendry, L.B. (1977) Neral and geranial: components of the sex pheromone of the parasitic wasp Itoplectis conquistor. Journal of Chemical Ecology 3, 563–577.CrossRefGoogle Scholar
Robacker, D.C., Weaver, K.M. & Hendry, L.B. (1976) Sexual communication and associative learning in the parasitic wasp Itoplectis conquistor. Journal of Chemical Ecology 2, 39–48.CrossRefGoogle Scholar
Scheiner, S.M. (1993) MANOVA: Multiple response variables and multispecies interactions. pp. 94–112in Scheiner, S.M. & Gurevitch, J. (Eds) Design and Analysis of Ecological Experiments. New York, USA, Chapman & Hall.Google Scholar
Starý, P., Gerding, M., Norambuena, H. & Remaudière, G. (1993) Environmental research on aphid parasitoid biocontrol agents in Chile (Hym: Aphidiidae, Hom: Aphidoidea). Journal of Applied Entomology 115, 292–306.CrossRefGoogle Scholar
Steiner, S. (2007) Courtship pheromones in parasitic wasps: comparison of bioactive and inactive hydrocarbon profiles by multivariate statistical methods. Journal of Chemical Ecology 33, 825–838.CrossRefGoogle ScholarPubMed
Sumana, A. & Starks, P.T. (2004) Grooming patterns in the primitively eusocial wasp Polistes dominulus. Ethology 110, 825–833.CrossRefGoogle Scholar
Takada, H. & Tada, E. (2000) A comparison between two strains from Japan and Europe of Aphidius ervi. Entomologia Experimentalis et Applicata 97, 11–20.CrossRefGoogle Scholar
Tremblay, E. & Pennacchio, F. (1988) Speciation in Aphidiine Hymenoptera (Hymenoptera: Aphidiidae). pp. 139–146in Gupta, V.K. (Ed.) Advances in Parasitic Hymenoptera Research. Leiden, The Netherlands, E.J. Brill.Google Scholar
Unruh, T.R., White, W., Gonzáles, D. & Luck, R.F. (1983) Heterozygosity and effective size in laboratory populations of Aphidius ervi (Hym: Aphidiidae). Entomophaga 28, 245–258.CrossRefGoogle Scholar
Villagra, C.A., Vásquez, R.A. & Niemeyer, H.M. (2005) Associative odour learning affects mating behaviour in Aphidius ervi males (Hymenoptera: Braconidae). European Journal of Entomology 102, 557–559.CrossRefGoogle Scholar
Walsh, B.D. (1864) On phytophagic varieties and phytophagic species. Proceedings of the Entomological Society of Philadelphia 3, 403–431.Google Scholar
Wcislo, W.T. (1987) The role of learning in the mating biology of a sweat bee Lasioglossum zephyrum (Hymenoptera: Halictidae). Behavioral Ecology and Sociobiology 20, 179–189.CrossRefGoogle Scholar
Wcislo, W.T. (1992) Attraction and learning in mate-finding by solitary bees, Lasioglossum (Dialictus) figueresi Wcislo and Nomia triangulifera Vachal (Hymenoptera: Halictidae). Behavioral Ecology and Sociobiology 31, 139–148.CrossRefGoogle Scholar
Wuellner, C.T., Porter, S.D. & Gilbert, L.E. (2002) Eclosion, mating, and grooming behavior of the parasitoid fly Pseudacteon curvatus (Diptera: Phoridae). Florida Entomologist 85, 563–566.CrossRefGoogle Scholar
Zúñiga, E. (1990) Biological control of cereal aphids in the southern cone of South America. pp. 362–367in Burnett, P.A. (Ed.) World Perspectives on Barley Yellow Dwarf. Mexico, DF, CIMMYT.Google Scholar