Oviposition Experience of Parasitoid Wasps with Nonhost Larvae Affects their Olfactory and Contact-Behavioral Responses toward Host- and Nonhost-Infested Plants

Journal of Chemical Ecology volume 45, pages402–409(2019)Cite this article

Abstract

In nature, parasitoid wasps encounter and sometimes show oviposition behavior to nonhost species. However, little is known about the effect of such negative incidences on their subsequent host-searching behavior. We tested this effect in a tritrophic system of maize plants (Zea mays), common armyworms (hosts), tobacco cutworms (nonhosts), and parasitoid wasps, Cotesia kariyai. We used oviposition inexperienced C. kariyai and negative-experienced individuals that had expressed oviposition behavior toward nonhosts on nonhost-infested maize leaves. We first observed the olfactory behavior of C. kariyai to volatiles from host-infested plants or nonhost-infested plants in a wind tunnel. Negative-experienced wasps showed significantly lower rates of taking-off behavior (Step-1), significantly longer duration until landing (Step-2), and lower rates of landing behavior (Step-3) toward nonhost-infested plants than inexperienced wasps. However, the negative-experience did not affect these three steps toward host-infested plants. A negative experience appears to have negatively affected the olfactory responses to nonhost-infested plants. The chemical analyses suggested that the wasps associated (Z)-3-hexenyl acetate, a compound that was emitted more in nonhost-infested plants, with the negative experience, and reduced their response to nonhost-infested plants. Furthermore, we observed that the searching duration of wasps on either nonhost- or host-infested plants (Step-4) was reduced on both plant types after the negative experiences. Therefore, the negative experience in Step-4 would be nonadaptive for wasps on host-infested plants. Our study indicated that the density (i.e., possible encounters) of nonhost species as well as that of host species in the field should be considered when assessing the host-searching behavior of parasitoid wasps.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  1. Arimura G, Köpke S, Kunert M, Volpe V, David A, Brand P, Dabrowska P, Maffei ME, Boland W (2008) Effects of feeding Spodoptera littoralis on lima bean leaves: IV. Diurnal and nocturnal damage differentially initiate plant volatile emission. Plant Physiol 146:965–973. https://doi.org/10.1104/pp.107.111088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Arimura G, Matsui K, Takabayashi J (2009) Chemical and molecular ecology of herbivore-induced plant volatiles: proximate factors and their ultimate functions. Plant Cell Physiol 50:911–923. https://doi.org/10.1093/pcp/pcp030

    Article  CAS  PubMed  Google Scholar 

  3. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting Linear Mixed-Effects Models using lme4. J Stat Softw 67:1–48

  4. Choh Y, Ozawa R, Takabayashi J (2013) Do plants use airborne cues to recognize herbivores on their neighbours? Exp Appl Acarol 59:263–273. https://doi.org/10.1007/s10493-012-9616-z

    Article  CAS  PubMed  Google Scholar 

  5. Costa A, Ricard I, Divison AC, Turlings TCJ (2010) Effects of rewarding and unrewarding experiences on the response to host-induced plant odors of the generalist parasitoid Cotesia marginiventris (Hymenoptera: Braconidae). J Insect Behav 23:303–318. https://doi.org/10.1007/s10905-010-9215-y

    Article  Google Scholar 

  6. 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. https://doi.org/10.1023/A:1014548213671

    Article  CAS  PubMed  Google Scholar 

  7. Geervliet JBF, Vet LEM, Dicke M (1996) Innate responses of the parasitoids Cotesia glomerata and C. rubecula (Hymenoptera: Braconidae) to volatiles from different plant-herbivore complexes. J Insect Behav 9:525–538. https://doi.org/10.1007/BF02213877

    Article  Google Scholar 

  8. Hare JD (2011) Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annu Rev Entomol 56:161–180. https://doi.org/10.1146/annurev-ento-120709-144753

    Article  CAS  PubMed  Google Scholar 

  9. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Statist 6:65–70

  10. Matsui K (2006) Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. Curr Opin Plant Biol 9:274–280. https://doi.org/10.1016/j.pbi.2006.03.002

    Article  CAS  PubMed  Google Scholar 

  11. McCormick AC, Unsicker SB, Gershenzon J (2012) The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci 964:1–8. https://doi.org/10.1016/j.tplants.2012.03.012

    CAS  Article  Google Scholar 

  12. R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL: http://www.R-project.org/

  13. SAS Institute (2013) JMP ver. 11.2.1. SAS Institute, Inc., Cary

  14. Sato Y, Tanaka T, Imafuku M, Hidaka T (1983) How does diurnal Apanteles kariyai parasitize and egress from a nocturnal host larva? Kontyu 51:128–139

    Google Scholar 

  15. Shiojiri K, Takabayashi J, Yano S, Takafuji A (2000) Flight response of parasitoids towards plant-herbivore complexes: a comparative study of two parasitoid-herbivore systems on cabbage plants. Appl Entomol Zool 35:87–92. https://doi.org/10.1303/aez.2000.87

    Article  Google Scholar 

  16. Takabayashi J, Takahashi S (1986a) Effect of kairomones in the host searching behavior of Apanteles kariyai Watanabe (Hymenoptera: Braconidae), a parasitoid of the common armyworm Pseudaletia separata Walker (Lepidoptera: Noctuidae). II. Isolation and identification of arrestants produced by the host larvae. Appl Entomol Zool 21:114–118. https://doi.org/10.1303/aez.21.114

    Article  CAS  Google Scholar 

  17. Takabayashi J, Takahashi S (1986b) Effect of kairomones in the host searching behavior of Apanteles kariyai Watanabe (Hymenoptera: Braconidae), a parasitoid of the common armyworm Pseudaletia separata Walker (Lepidoptera: Noctuidae). III. Synthesis and bioassay of arrestants and related compounds. Appl Entomol Zool 21:519–524. https://doi.org/10.1303/aez.21.519

    Article  CAS  Google Scholar 

  18. Takabayashi J, Takahashi S (1990) An allelochemical elicits arrestment in Apanteles kariyai in frass of nonhost larvae Acantholeucania loreyi. J Chem Ecol 16:2009–2017. https://doi.org/10.1007/BF01020512

    Article  CAS  PubMed  Google Scholar 

  19. Takabayashi J, Noda T, Takahashi S (1985) Effect of kairomones in the host searching behavior of Apanteles kariyai Watanabe (Hymenoptera: Braconidae), a parasitoid of the common armyworm Pseudaletia separata Walker (Lepidoptera: Noctuidae). I. Presence of arresting stimulants produced by the host larvae. Appl Entomol Zool 20:484–489

  20. Takabayashi J, Noda T, Takahashi S (1991) Plants produce attractants for Apanteles Kariyai, a parasitoid of Pseudaletia separata; cases of 'communication' and 'misunderstanding' in parasitoid-plant interactions. Appl Entomol Zool 26:237–243. https://doi.org/10.1303/aez.26.237

    Article  Google Scholar 

  21. Takabayashi J, Takahashi S, Dicke M, Posthumus MA (1995) Developmental stage of herbivore Pseudaletia separata affects production of herbivore-induced synomone by corn plants. J Chem Ecol 21:273–287. https://doi.org/10.1007/BF02036717

    Article  CAS  PubMed  Google Scholar 

  22. Takasu K, Lewis WJ (2003) Learning of host searching cues by the larval parasitoid Microplitis croceipes. Entomol Exp Appl 108:77–86. https://doi.org/10.1046/j.1570-7458.2003.00070.x

    Article  Google Scholar 

  23. Takemoto H, Powell W, Pickett JA, Kainoh Y, Takabayashi J (2012) Two-step learning involved in acquiring olfactory preferences for plant volatiles by parasitic wasps. Anim Behav 83:1491–1496. https://doi.org/10.1016/j.anbehav.2012.03.023

    Article  Google Scholar 

  24. 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. https://doi.org/10.1146/annurev-ento-020117-043507

    Article  CAS  PubMed  Google Scholar 

  25. Uefune M, Kugimiya S, Ozawa R, Takabayashi J (2013) Parasitic wasp females are attracted to blends of host-induced plant volatiles: do qualitative and quantitative differences in the blend matter? F1000Research 2:57. https://doi.org/10.12688/f1000research.2-57.v2

    Article  PubMed  PubMed Central  Google Scholar 

  26. van Oudenhove L, Mailleret L, Fauvergue X (2017) Infochemical use and dietary specialization in parasitoids: a meta-analysis. Ecol Evol 7:4804–4811. https://doi.org/10.1002/ece3.2888

    Article  PubMed  PubMed Central  Google Scholar 

  27. Yoneya K, Uefune M, Takabayashi J (2018) Parasitoid wasps’ exposure to host-infested plant volatiles affects their olfactory cognition of host-infested plants. Anim Cogn 21:79–86. https://doi.org/10.1007/s10071-017-1141-3

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to Prof. DeMar Taylor for reviewing the final version of the manuscript and to the Japan Ministry of Education, Culture, Sports and Technology (MEXT) for giving SS a Scholarship (period: Oct 2011 to March 2013) during his stay as a student of the Teacher Training Program. This study was supported in part by grants for scientific research (A) from MEXT.

Author information

Affiliations

  1. Master’s Program in Education, University of Tsukuba, Tsukuba, Ibaraki, 305-8572, Japan

    Saw Steven

  2. Department Agrobiological Resources, Faculty of Agriculture, Meijo University, Nagoya, Aichi, 468-8502, Japan

    Masayoshi Uefune

  3. Center for Ecological Research, Kyoto University, Otsu, Shiga, 520-2113, Japan

    Rika Ozawa & Junji Takabayashi

  4. Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, 305-8572, Japan

    Yooichi Kainoh

Authors
  1. Saw Steven
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masayoshi Uefune
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rika Ozawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Junji Takabayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yooichi Kainoh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yooichi Kainoh.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Steven, S., Uefune, M., Ozawa, R. et al. Oviposition Experience of Parasitoid Wasps with Nonhost Larvae Affects their Olfactory and Contact-Behavioral Responses toward Host- and Nonhost-Infested Plants. J Chem Ecol 45, 402–409 (2019). https://doi.org/10.1007/s10886-019-01064-6

Download citation

Keywords

  • Tritrophic interaction
  • Negative experience
  • Host-finding behavior
  • (Z)-3-hexenyl acetate