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Different patterns of oviposition learning in two closely related ectoparasitoid wasps with contrasting reproductive strategies

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Abstract

Many parasitoid wasps learn host-associated cues and use them in subsequent host-searching behavior. This associative learning, namely “oviposition learning,” has been investigated in many studies. However, few studies have compared multiple species, and no comparative study has previously been conducted on ectoparasitoid species. We compared the effects of oviposition learning on host preference and offspring sex ratio in two closely related ectoparasitoid wasps with contrasting reproductive strategies, Anisopteromalus calandrae (r-strategist) and its sibling species (K-strategist). Using two bruchine hosts, Callosobruchus chinensis and Callosobruchus maculatus larvae infesting the cowpea Vigna unguiculata, oviposition choice experiments were performed at high and low host densities. In both species, no conspicuous effect on the offspring sex ratio was detected, but effects on host preference were found to differ between the species. In A. calandrae, the effects were detected only at high host density, suggesting that oviposition learning plays a role in host discrimination from a short distance but not from a long distance. In the sibling species, those effects were not detected in any of the cases, suggesting the absence of oviposition learning. These results are compatible with those of previous comparative studies of endoparasitoid wasps in that few lifetime oviposition experiences and/or low reward per foraging decision result in low or absent oviposition learning ability. This finding may indicate that ecological traits contributing to learning ability are similar between endoparasitoid and ectoparasitoid wasps. Thus, our species comparison of ectoparasitoids provides another model system for investigating learning and memory dynamics in parasitoid wasps.

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References

  • Ahmed KS (1996) Studies on the ectoparasitoid, Anisopteromalus calandrae How. (Hymenoptera: Pteromalidae) as a biological agent against the lesser grain borer, Rhyzopertha dominica (Fab.) in Saudi Arabia. J Stored Prod Res 32:137–140

    Article  Google Scholar 

  • Arthur AP (1966) Associative learning in Itoplectis conquisitor (Say) (Hymenoptera: Ichneumonidae). Can Entomol 98:213–223

    Article  Google Scholar 

  • Bjorksten TA, Hoffmann AA (1998) Persistence of experience effects in the parasitoid Trichogramma nr. brassicae. Ecol Entomol 23:110–117

    Article  Google Scholar 

  • De Jong R, Kaiser L (1991) Odor learning by Leptopilina boulardi, a specialist parasitoid (Hymenoptera: Eucoilidae). J Insect Behav 4:743–750

    Article  Google Scholar 

  • Dukas R (2008) Evolutionary biology of insect learning. Annu Rev Entomol 53:145–160

    Article  PubMed  CAS  Google Scholar 

  • Gandolfi M, Mattiacci L, Dorn S (2003) Preimaginal learning determines adult response to chemical stimuli in a parasitic wasp. Proc R Soc B 270:2623–2629

    Article  PubMed  Google Scholar 

  • Geervliet JBF, Vreugdenhil AI, Dicke M, Vet LEM (1998) Learning to discriminate between infochemicals from different plant-host complexes by the parasitoids Cotesia glomerata and C. rubecula. Entomol Exp Appl 86:241–252

    Article  CAS  Google Scholar 

  • Ghimire MN, Phillips TW (2007) Suitability of five species of stored-product insects as hosts for development and reproduction of the parasitoid Anisopteromalus calandrae (Hymenoptera: Pteromalidae). J Econ Entomol 100:1732–1739

    Article  PubMed  Google Scholar 

  • Ghimire MN, Phillips TW (2008) Effects of prior experience on host selection and host utilization by two populations of Anisopteromalus calandrae (Hymenoptera: Pteromalidae). Environ Entomol 37:1300–1306

    Article  PubMed  Google Scholar 

  • Gokhman VE, Timokhov AV, Fedina TY (1998) First evidence for sibling species in Anisopteromalus calandrae (Hymenoptera: Pteromalidae). Russian Entomol J 7:157–162

    Google Scholar 

  • Gokhman VE, Fedina TY, Timokhov AV (1999) Life-history strategies in parasitic wasps of the Anisopteromalus calandrae complex (Hymenoptera: Pteromalidae). Russian Entomol J 8:201–211

    Google Scholar 

  • Gullan PJ, Cranston PS (2010) The insects: An outline of entomology, 4th edn. Wiley-Blackwell, Oxford

    Google Scholar 

  • Hoedjes KM, Kruidhof HM, Huigens ME, Dicke M, Vet LEM, Smid HM (2011) Natural variation in learning rate and memory dynamics in parasitoid wasps: opportunities for converging ecology and neuroscience. Proc R Soc B 278:889–897

    Article  PubMed  Google Scholar 

  • Huigens ME, Pashalidou FG, Qian M, Bukovinszky T, Smid HM, van Loon JJA, Dicke M, Fatouros NE (2009) Hitch-hiking parasitic wasp learns to exploit butterfly anti-aphrodisiac. Proc Natl Acad Sci USA 106:820–825

    Article  PubMed  CAS  Google Scholar 

  • Ishii Y (2008) Coexistence mediated by a common predator in three species host-parasitoid experimental systems. PhD thesis, The University of Tokyo

  • Ishii Y, Shimada M (2012) Learning predator promotes coexistence of prey species in host–parasitoid systems. Proc Natl Acad Sci USA 109:5116–5120

    Article  PubMed  CAS  Google Scholar 

  • Kaiser L, Pham-Delegue MH, Masson C (1989) Behavioural study of plasticity in host preference of Trichogramma maidis (Hym.: Trichogrammatidae). Physiol Entomol 14:53–60

    Article  Google Scholar 

  • Langley SA, Tilmon KJ, Cardinale BJ, Ives AR (2006) Learning by the parasitoid wasp, Aphidius ervi (Hymenoptera: Braconidae), alters individual fixed preferences for pea aphid color morphs. Oecologia 150:172–179

    Article  PubMed  Google Scholar 

  • Lewis WJ, Tumlinson JH (1988) Host detection by chemically mediated associative learning in a parasitic wasp. Nature 331:257–259

    Article  Google Scholar 

  • Mandeville JD, Mullens BA (1990) Host preference and learning in Muscidifurax zaraptor (Hymenoptera: Pteromalidae). Ann Entomol Soc Am 83:1203–1209

    Google Scholar 

  • Papaj DR, Vet LEM (1990) Odor learning and foraging success in the parasitoid, Leptopilina heterotoma. J Chem Ecol 16:3137–3150

    Article  Google Scholar 

  • Poolman Simons MTT, Suverkropp BP, Vet LEM, de Moed G (1992) Comparison of learning in related generalist and specialist eucoilid parasitoids. Entomol Exp Appl 64:117–124

    Article  Google Scholar 

  • Potting RPJ, Otten H, Vet LEM (1997) Absence of odour learning in the stemborer parasitoid Cotesia flavipes. Anim Behav 53:1211–1223

    Article  PubMed  Google Scholar 

  • R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • Sasakawa K, Satô M, Shimada M (2012) Additional notes on Anisopteromalus sp. (Hymenoptera: Pteromalidae), the sibling species of a parasitic wasp of stored-product pests, Anisopteromalus calandrae (Howard): a new alternative host, an eye color mutant and DNA barcodes. Entomol Sci 15:349–351

    Article  Google Scholar 

  • Smid HM, Wang G, Bukovinszky T, Steidle JLM, Bleeker MAK, van Loon JJA, Vet LEM (2007) Species-specific acquisition and consolidation of long-term memory in parasitic wasps. Proc R Soc B 274:1539–1546

    Article  PubMed  Google Scholar 

  • Steiner S, Steidle JLM, Ruther J (2007) Host-associated kairomones used for habitat orientation in the parasitoid Lariophagus distinguendus (Hymenoptera: Pteromalidae). J Stored Prod Res 43:587–593

    Article  CAS  Google Scholar 

  • Takasu K, Lewis WJ (2003) Learning of host searching cues by the larval parasitoid Microplitis croceipes. Entomol Exp Appl 108:77–86

    Article  Google Scholar 

  • Timokhov AV, Gokhman VE (2003) Host preferences of parasitic wasps of the Anisopteromalus calandrae species complex (Hymenoptera: Pteromalidae). Acta Soc Zoo Bohem 67:35–39

    Google Scholar 

  • Turlings TCJ, Tumlinson JH, Lewis WJ, Vet LEM (1989) Beneficial arthropod behavior mediated by airborne semiochemicals. VIII. Learning of host-related odors induced by a brief contact experience with host by-products in Cotesia marginiventris (Cresson), a generalist larval parasitoid. J Insect Behav 2:217–225

    Article  Google Scholar 

  • Turlings TCJ, Wäckers FL, Vet LEM, Lewis WJ, Tumlinson JH (1993) Learning of host-finding cues by hymenopterous parasitoids. In: Papaj DR, Lewis AC (eds) Insect learning: Ecological and evolutionary perspectives. Chapman & Hall, New York, pp 51–78

    Chapter  Google Scholar 

  • van den Berg M, Duivenvoorde L, Wang GH, 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

    Article  Google Scholar 

  • Vet LEM (1983) Host-habitat location through olfactory cues by Leptopilina clavipes (Hartig) (Hym.: Eucoilidae), a parasitoid of fungivorous Drosophila: the influence of conditioning. Neth J Zool 33:225–248

    Article  Google Scholar 

  • Vet LEM, van Opzeeland K (1984) The influence of conditioning on olfactory microhabitat and host location in Asobara tabida (Nees) and A. rufescens (Foerster) (Braconidae, Alysiinae) larval parasitoids of Drosophilidae. Oecologia 63:171–177

    Article  Google Scholar 

  • Wardle AR, Borden JH (1985) Learning of host microhabitat form by Exeristes roborator (F.) (Hymenoptera: Ichneumonidae). J Insect Behav 3:251–263

    Article  Google Scholar 

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Acknowledgments

We thank four anonymous reviewers for their helpful comments. This study was partly supported by the Japan Society for the Promotion of Science (JSPS) to MS (nos. 20370008 and 23370009).

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Correspondence to Kôji Sasakawa.

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Communicated by: Sven Thatje

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Sasakawa, K., Uchijima, K., Shibao, H. et al. Different patterns of oviposition learning in two closely related ectoparasitoid wasps with contrasting reproductive strategies. Naturwissenschaften 100, 117–124 (2013). https://doi.org/10.1007/s00114-012-1001-6

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  • DOI: https://doi.org/10.1007/s00114-012-1001-6

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