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Delayed Response after Learning Associated with Oviposition Experience in the Larval Parasitoid, Cotesia kariyai (Hymenoptera: Braconidae)

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Abstract

The ability of female parasitoid wasps, Cotesia kariyai (Hymenoptera: Braconidae), to learn to recognize plant volatiles associated with an oviposition experience was investigated. First, we observed oviposition behavior of female wasps when encountering host larvae (Mythimna separata, Lepidoptera: Noctuidae). On their first encounters with host larvae, 96% of inexperienced female wasps showed oviposition behavior. Immediately afterward, and for 2 h after the first oviposition, wasp oviposition behavior was suppressed. Only 20–30% of wasps showed a second oviposition response, even after several encounters with a new host. Then, oviposition behavior gradually recovered 6 to 24 h after the first oviposition. At 6 h after the first oviposition experience, more than 80% of the wasps showed a second oviposition response when encountering a new host. Next, in a wind tunnel, we investigated the effect of time since first oviposition on wasp responses to host-infested plant volatiles. Female landings in response to volatiles of host-infested maize plants, Zea mays, showed a bell-shaped curve from 0 to 48 h after first oviposition. Eight hours after the first oviposition, the rate of landing by wasps was significantly higher than that of oviposition-inexperienced wasps. The ecological strategy explaining the effect of oviposition experience on olfactory responses of C. kariyai to host-infested plant volatiles is discussed.

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References

  • Afsheen S, Wang X, Li R, Zhu C, Lou Y (2008) Differential attraction of parasitoids in relation to specificity of kairomones from herbivores and their by-products. Insect Sci 15:381–397

    Article  Google Scholar 

  • Collett TS, Collett M (2002) Memory use in insect visual navigation. Nat Rev Neurosci 3:542–552

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Dukas R (2013) Effects of learning on evolution: robustness, innovation and speciation. Anim Behav 85:1023–1030

    Article  Google Scholar 

  • Dutton A, Mattiacci L, Dorn S (2000) Learning used as a strategy for host stage location in an endophytic host-parasitoid system. Entomol Exp Appl 94:123–132

    Article  Google Scholar 

  • Fukushima J, Kainoh Y, Honda H, Takabayashi J (2001) Learning of host-infested plant volatiles in the larval parasitoid Cotesia kariyai. Entomol Exp Appl 99:341–346

    Article  Google Scholar 

  • Fukushima J, Kainoh Y, Honda H, Takabayashi J (2002) Learning of herbivore-induced and nonspecific plant volatiles by a parasitoid, Cotesia kariyai. J Chem Ecol 28:579–586

    Article  CAS  Google Scholar 

  • Girling RD, Hassall M, Turner JG, Poppy GM (2006) Behavioural responses of the aphid parasitoid Diaeretiella rapae to volatiles from Arabidopsis thaliana induced by Myzus persicae. Entomol Exp Appl 120:1–9

    Article  Google Scholar 

  • Giunti G, Canale A, Messing RH, Donati E, Stefanini C, Michaud JP, Benelli G (2015) Parasitoid learning: current knowledge and implications for biological control. Biol Control 90:208–219

    Article  Google Scholar 

  • Godfray HCJ (1994) Parasitoids behavioral and evolutionary ecology. Princeton University Press, Princeton

    Book  Google Scholar 

  • Hirai K (1984) Notes on Apanteles kariyai Watanabe (Hymenoptera: Braconidae), a parasitoid of the armyworm Pseudaletia separata Walker. Ann Rep Plant Prot North Jpn 35:154–156

    Google Scholar 

  • Kaiser L, Pérez-Maluf R, Sandoz JC, Pham-Delègue MH (2003) Dynamics of odour learning in Leptopilina boulardi, a hymenopterous parasitoid. Anim Behav 66:1077–1084

    Article  Google Scholar 

  • Kanda K (1988) Hatching time of eggs and dispersal time of resultant hatching of the army-worm, Pseudaletia separata Walker. Jap J Appl Entomol Zool 32:85–87 (in Japanese with an English summary)

    Article  Google Scholar 

  • Kanda K (1991) Rearing method of armyworm. In: Yushima K, Kamano S, Tamaki Y (eds) Rearing method of insects. Japan Plant Protection Association, Tokyo, pp 206–209 (in Japanese)

    Google Scholar 

  • Kanda K, Naito A (1979) Behavior of oriental armyworm moth, Leucania separata Walker, from emergence to oviposition. Jap J Appl Entomol Zool 23:69–77 (in Japanese with an English summary)

    Article  Google Scholar 

  • Lewis WJ, Martin WR (1990) Semiochemicals for use with parasitoids: status and future. J Chem Ecol 16:3067–3089

    Article  CAS  Google Scholar 

  • Mangel M (1993) Motivation, learning and motivated learning. In: Papaj DR, Lewis AC (eds) Insect learning - ecological and evolutionary perspectives. Chapman& Hall, London, pp 158–173

    Google Scholar 

  • Nealis VG (1986) Responses to host kairomones and foraging behavior of the insect parasite Cotesia rubecula (Hymenoptera: Braconidae). Can J Zool 64:2393–2398

    Article  Google Scholar 

  • Quicke DLJ (2015) Host location, associative learning and host assessment. In: Quicke DLJ (ed) The braconid and ichneumonid parasitoid wasps: biology, systematics, evolution and ecology. John Wiley & Sons, Chichester

    Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria http://www.R-proje

    Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

  • Sato Y, Tanaka T (1984) Effect of the number of parasitoid (Apanteles kariyai) eggs (Hym.: Braconidae) on the growth of host (Leucania separata) larvae (Lep.: Noctuidae). Entomophaga 29:21–28

    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. P Roy Soc B: Biol Sci 274:1539–1546

    Google Scholar 

  • Takabayashi J, Shiojiri K (2019) Multifunctionality of herbivory-induced plant volatiles in chemical communication in tritrophic interactions. Curr Opin Insect Sci 32:110–117

    Article  Google Scholar 

  • Takasu K, Lewis WJ (1996) The role of learning in adult food location by the larval parasitoid, Microplitis croceipes (Hymenoptera: Braconidae). J Insect Behav 9:265–281

    Article  Google Scholar 

  • Takemoto H, Powell W, Pickett J, Kainoh Y, Takabayashi J (2009) Learning is involved in the response of parasitic wasps Aphidius ervi (Haliday) (Hymenoptera: Braconidae) to volatiles from a broad bean plant, Vicia faba (Fabaceae), infested by aphids Acyrthosiphon pisum (Harris) (Homoptera: Aphididae). Appl Entomol Zool 44:23–28

    Article  Google Scholar 

  • Takemoto H, Powell W, Pickett J, Kainoh Y, Takabayashi J (2012) Two-step learning involved in acquiring olfactory preferences for plant volatiles by parasitic wasps. Anim Behav 83:1491–1496

    Article  Google Scholar 

  • Tanaka A (1976) Population dynamics in Mythimna separata (Walker). Plant Prot 30:431–437 (in Japanese)

    Google Scholar 

  • Tanaka T, Agui N, Hiruma K (1987) The parasitoid Apanteles kariyai inhibits pupation of its host, Pseudaletia separata, via disruption of prothoracicotropic hormone release. Gen Comp Endocrinol 67:364–374

    Article  CAS  Google Scholar 

  • Tanaka T, Matsumoto H, Hayakawa Y (2002) Analysis in the course of polydnavirus replication in ovarian calyx cells of the parasitoid wasp, Cotesia kariyai (Hymenoptera: Braconidae). Appl Entomol Zool 37:323–328

    Article  Google Scholar 

  • Tempel BL, Bonini N, Dawson DR, Quinn WG (1983) Reward learning in normal and mutant Drosophila. Proc Natl Acad Sci U S A 80:1482–1486

    Article  CAS  Google Scholar 

  • Turlings TCJ, Erb M (2018) Tritrophic interactions mediated by herbivore-induced plant volatiles: mechanisms, ecological relevance, and application potential. Annu Rev Entomol 63:433–452

    Article  CAS  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 perspective. Chapman and Hall, New York, pp 51–78

    Chapter  Google Scholar 

  • Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in tritrophic context. Annu Rev Entomol 37:141–172

    Article  Google Scholar 

  • Vet LEM, Lewis WJ, Cardé RT (1995) Parasitoid foraging and learning. In: Cardé RT, Bell WJ (eds) Chemical ecology of insects 2. Chapman and Hall, New York, pp 65–101

    Chapter  Google Scholar 

  • Villar ME, Marchal P, Viola H, Giurfa M (2020) Redefining single-trial memories in the honeybee. Cell Rep 30:2603–2613

    Article  CAS  Google Scholar 

  • Vos M, Vet LEM (2004) Geographic variation in host acceptance by an insect parasitoid: genotype versus experience. Evol Ecol Res 6:1021–1035

  • Wäschke N, Meiners T, Rostas M (2013) Foraging strategies of parasitoids in complex chemical environments. In: Wajnberg E, Colazza S (eds) Chemical ecology of insect parasitoids. Wiley-Blackwell, Chichester, pp 37–63

    Chapter  Google Scholar 

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Acknowledgements

We thank Prof. DeMar Taylor, Faculty of Life and Environmental Sciences, University of Tsukuba, for his comments on the early version of the manuscript.

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Authors and Affiliations

  1. Graduate School of Environmental Sciences, University of Tsukuba, Tennodai 1-1-1, Tsukuba, Ibaraki, 305-8572, Japan

    Junji Fukushima

  2. Faculty of Life and Environmental Sciences, University of Tsukuba, Tennodai 1-1-1, Tsukuba, Ibaraki, 305-8572, Japan

    Kazumu Kuramitsu & Yooichi Kainoh

  3. Japan Society for the Promotion of Science, 5-3-1 Kojimachi, Chiyoda-ku, Tokyo, 102-0083, Japan

    Kazumu Kuramitsu

  4. Center for Ecological Research, Kyoto University, 2-509-3 Hirano, Otsu, Shiga, 520-2113, Japan

    Junji Takabayashi

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  1. Junji Fukushima
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  2. Kazumu Kuramitsu
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  4. Yooichi Kainoh
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Correspondence to Yooichi Kainoh.

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Fukushima, J., Kuramitsu, K., Takabayashi, J. et al. Delayed Response after Learning Associated with Oviposition Experience in the Larval Parasitoid, Cotesia kariyai (Hymenoptera: Braconidae). J Insect Behav 34, 264–270 (2021). https://doi.org/10.1007/s10905-021-09786-w

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  • DOI: https://doi.org/10.1007/s10905-021-09786-w

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