Abstract
Animals rely on associative learning for a wide range of purposes, including danger avoidance. This has been demonstrated for several insects, including cockroaches, mosquitoes, drosophilid flies, paper wasps, stingless bees, bumblebees and honeybees, but less is known for parasitic wasps. We tested the ability of Psyttalia concolor (Hymenoptera: Braconidae) females to associate different dosages of two innately attractive host-induced plant volatiles (HIPVs), ethyl octanoate and decanal, with danger (electric shocks). We conducted an associative treatment involving odours and shocks and two non-associative controls involving shocks but not odours and odours but not shocks. In shock-only and odour-only trained wasps, females preferred on HIPV-treated than on blank discs. In associative-trained wasps, however, P. concolor’s innate positive chemotaxis for HIPVs was nullified (lowest HIPV dosage tested) or reversed (highest HIPV dosage tested). This is the first report of associative learning of olfactory cues for danger avoidance in parasitic wasps, showing that the effects of learning can override innate positive chemotaxes.
References
Benelli G, Canale A (2012) Learning of visual cues in the fruit fly parasitoid Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae). BioControl 57:767–777
Benelli G, Canale A (2013) Male-male sexual behaviour in the parasitic wasp Psyttalia concolor. J Insect Sci 13:25
Benelli G, Gennari G, Francini A, Canale A (2013a) Longevity costs of same-sex interactions: first evidence from a parasitic wasp. Invert Biol 132:156–162
Benelli G, Revadi S, Carpita A, Giunti G, Raspi A, Anfora G, Canale A (2013b) Behavioral and electrophysiological responses of the parasitic wasp Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae) to Ceratitis capitata-induced fruit volatiles. Biol Control 64:116–124
Benelli G, Carpita A, Simoncini S, Raspi A, Canale A (2014) For sex and more: attraction of the tephritid parasitoid Psyttalia concolor (Hymenoptera: Braconidae) to male sex pheromone of the olive fruit fly, Bactrocera oleae. J Pest Sci. doi:10.1007/s10340-014-0595-1
Bleeker MAK, Smid HM, Steidle JLM, Kruidhof M, van Loon JJA, Vet LEM (2006) Differences in memory dynamics between two closely related parasitoid wasp species. Anim Behav 71:1343–1350
Canale A, Benelli G (2012) Impact of mass-rearing on the host-seeking behaviour and parasitism by the fruit fly parasitoid Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae). J Pest Sci 85:65–74
Carpita A, Canale A, Raffaelli A, Saba A, Benelli G, Raspi A (2012) (Z)-9-tricosene identified in rectal glands extracts of Bactrocera oleae males: first evidence of a male-produced female attractant in olive fruit fly. Naturwissenschaften 99:77–81
Craig CL (1994) Limits to learning: effects of predator pattern and colour on perception and avoidance-learning by prey. Anim Behav 47:1087–1099
Dukas R (2001) Effects of perceived danger on flower choice by bees. Ecol Lett 4:327–333
Dukas R (2013) Effects of learning on evolution: robustness, innovation and speciation. Anim Behav 85:1023–1030
Dukas R, Durisko Z, Dukas L (2012) Learning in the context of sexual behaviour and danger in female and male Drosophila pseudoobscura. Anim Behav 83:95–101
Ings TC, Chittka L (2009) Predator crypsis enhances behaviourally mediated indirect effects on plants by altering bumblebee foraging preferences. Proc R Soc B. doi:10.1098/rspb.2008.1748
Janssen A, van Alphen JJM, Sabelis MW, Bakker K (1995a) Odor-mediated avoidance of competition in Drosophila parasitoids—the ghost of competition. Oikos 73:356–366
Janssen A, van Alphen JJM, Sabelis MW, Bakker K (1995b) Specificity of odor mediated avoidance of competition in Drosophila parasitoids. Behav Ecol Sociobiol 36:229–235
McGuire TR, Tully T, Gelperin A (1990) Conditioning odor-shock associations in the black blowfly Phormia regina. J Insect Behav 3:49–60
Menda G, Uhr JH, Wyttenbach RA, Vermeylen FM, Smith DM, Harrington LC, Hoy RR (2013) Associative learning in the dengue vector mosquito, Aedes aegypti: avoidance of a previously attractive odor or surface color that is paired with an aversive stimulus. J Exp Biol 216:218–223
Ngumbi EN, Jordan M, Fadamiro HY (2012) Comparison of associative learning of host-related plant volatiles in two parasitoids with different degrees of host specificity, Cotesia marginiventris and Microplitis croceipes. Chemoecology 22:207–215
Oliai SE, King BH (2000) Associative learning in response to color in the parasitoid wasp Nasonia vitripennis (Hymenoptera: Pteromalidae). J Insect Behav 13:55–69
Pritchatt D (1968) Avoidance of electric shock by the cockroach Periplaneta americana. Anim Behav 16:178–185
Quinn WG, Harris WA, Benzer S (1974) Conditioned behavior in Drosophila melanogaster. Proc Natl Acad Sci U S A 3:708–712
Saleh N, Lars Chittka L (2006) The importance of experience in the interpretation of conspecific chemical signals. Behav Ecol Sociobiol 61:215–220
Segura DF, Viscarret MM, Carabajal Paladino LZ, Ovruski SM, Cladera JL (2007) Role of visual information and learning in habitat selection by a generalist parasitoid foraging for concealed hosts. Anim Behav 74:131–142
Sheehan MJ, Elizabeth A, Tibbetts EA (2011) Specialized face learning is associated with individual recognition in paper wasps. Science 334:1272–1275
Tully T, Quinn WG (1985) Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol A 157:263–277
Turner AM, Turner SE, Lappi HM (2006) Learning, memory and predator avoidance by freshwater snails: effects of experience on predator recognition and defensive strategy. Anim Behav 72:1443–1450
van den Berg M, Duivenvoorde L, Wang W, Tribuhl S, Bukovinszky T, Vet LEM, Dicke M, Smid HM (2011) Natural variation in learning and memory dynamics studied by artificial selection on learning rate in parasitic wasps. Anim Behav 81:325–333
Vergoz V, Roussel E, Sandoz JC, Giurfa M (2007) Aversive learning in honeybees revealed by the olfactory conditioning of the sting extension reflex. PLOS ONE 3:e288
Völkl W (2001) Parasitoid learning during interactions with ants: how to deal with an aggressive antagonist. Behav Ecol Sociobiol 49:135–144
Acknowledgments
We would like to thank Elisa Rigosi (CiMeC, Trento, Italy) and three anonymous reviewers for the comments on an earlier version of the manuscript. We are grateful to Donato Romano (University of Pisa) for the assistance during the experiments.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by: Sven Thatje
Rights and permissions
About this article
Cite this article
Benelli, G., Stefanini, C., Giunti, G. et al. Associative learning for danger avoidance nullifies innate positive chemotaxis to host olfactory stimuli in a parasitic wasp. Naturwissenschaften 101, 753–757 (2014). https://doi.org/10.1007/s00114-014-1210-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00114-014-1210-2