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

  • Saw Steven
  • Masayoshi Uefune
  • Rika Ozawa
  • Junji Takabayashi
  • Yooichi KainohEmail author
Article
  • 67 Downloads

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.

Keywords

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

Notes

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.

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 CrossRefPubMedPubMedCentralGoogle 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 CrossRefPubMedGoogle Scholar
  3. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting Linear Mixed-Effects Models using lme4. J Stat Softw 67:1–48Google Scholar
  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 CrossRefPubMedGoogle 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 CrossRefGoogle 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 CrossRefPubMedGoogle 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 CrossRefGoogle 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 CrossRefPubMedGoogle Scholar
  9. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Statist 6:65–70Google Scholar
  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 CrossRefPubMedGoogle 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 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., CaryGoogle Scholar
  14. Sato Y, Tanaka T, Imafuku M, Hidaka T (1983) How does diurnal Apanteles kariyai parasitize and egress from a nocturnal host larva? Kontyu 51:128–139Google 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 CrossRefGoogle 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 CrossRefGoogle 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 CrossRefGoogle 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 CrossRefPubMedGoogle 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 20:484–489Google Scholar
  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 CrossRefGoogle 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 CrossRefPubMedGoogle 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 CrossRefGoogle 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 CrossRefGoogle 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 CrossRefPubMedGoogle 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 CrossRefPubMedPubMedCentralGoogle 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 CrossRefPubMedPubMedCentralGoogle 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 CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Master’s Program in EducationUniversity of TsukubaTsukubaJapan
  2. 2.Department Agrobiological Resources, Faculty of AgricultureMeijo UniversityNagoyaJapan
  3. 3.Center for Ecological ResearchKyoto UniversityOtsuJapan
  4. 4.Faculty of Life and Environmental SciencesUniversity of TsukubaTsukubaJapan

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