Journal of Chemical Ecology

, Volume 36, Issue 6, pp 620–628 | Cite as

Present or Past Herbivory: A Screening of Volatiles Released from Brassica rapa Under Caterpillar Attacks as Attractants for the Solitary Parasitoid, Cotesia vestalis

  • Soichi Kugimiya
  • Takeshi Shimoda
  • Jun Tabata
  • Junji Takabayashi
Article
First Online:
Received:
Revised:
Accepted:

Abstract

Females of the solitary endoparasitoid Cotesia vestalis respond to a blend of volatile organic compounds (VOCs) released from plants infested with larvae of their host, the diamondback moth (Plutella xylostella), which is an important pest insect of cruciferous plants. We investigated the flight response of female parasitoids to the cruciferous plant Brassica rapa, using two-choice tests under laboratory conditions. The parasitoids were more attracted to plants that had been infested for at least 6 hr by the host larvae compared to intact plants, but they did not distinguish between plants infested for only 3 hr and intact plants. Although parasitoids preferred plants 1 and 2 days after herbivory (formerly infested plants) over intact plants they also preferred plants that had been infested for 24 hr over formerly infested plants. This suggests that parasitoids can distinguish between the VOC profiles of currently and formerly infested plants. We screened for differences in VOC emissions among the treatments and found that levels of benzyl cyanide and dimethyl trisulfide significantly decreased after removal of the host larvae, whereas terpenoids and their related compounds continued to be released at high levels. Benzyl cyanide and dimethyl trisulfide attracted parasitoids in a dose-dependent manner, whereas the other compounds were not attractive. These results suggest that nitrile and sulfide compounds temporarily released from plants under attack by host larvae are potentially more effective attractants for this parasitoid than other VOCs that are continuously released by host-damaged plants.

Key Words

Herbivore-induced plant volatiles Indirect defense Tritrophic interaction Brassica rapa Plutella xylostella Cotesia vestalis 
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Notes

Acknowledgements

We are grateful to Kimiko Kanbe and Yumiko Togashi (NARC) for their help in rearing insects and cultivating plants used in the experiments. This study was partly supported by a Grant-in-Aid for Young Scientists (B) [No. 21710241 for SK] and by a Grant-in-Aid for Scientific Research (B) [No. 19380188 for TS] from the Japan Society for the Promotion of Science (JSPS).

References

  1. Birkett, M. A., Chamberlain, K., Guerrieri, E., Pickett, J. A., Wadhams, L. J., and Yasuda, T. 2003. Volatiles from whitefly-infested plants elicit a host-locating response in the parasitoid, Encarsia formosa. J. Chem. Ecol. 29:1589–1600.CrossRefPubMedGoogle Scholar
  2. Bruinsma, M., POSTHUMUS, M. A., Mumm, R., Mueller, M. J., Van Loon, J. J. A., and Dicke, M. 2009. Jasmonic acid-induced volatiles of Brassica oleracea attract parasitoids: effects of time and dose, and comparison with induction by herbivores. J. Exp. Botany 60:2575–2587.CrossRefPubMedGoogle Scholar
  3. D’Auria, J. C., Pichersky, E., Schaub, A., Hansel, A., and Gershenzon, J. 2007. Characterization of a BAHD acyltransferase responsible for producing the green leaf volatile (Z)-3-hexen-1-yl acetate in Arabidopsis thaliana. Plant J. 49:194–207.CrossRefPubMedGoogle Scholar
  4. De Moraes, C. M., Mescher, M. C., and Tumlinson, J. H. 2001. Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410:577–580.CrossRefPubMedGoogle Scholar
  5. Dugravot, S., Thibout, E., Abo-Ghalia, A., and Huignard, J. 2004. How a specialist and a nonspecialist insect cope with the dimethyl disulfide produced by Allium porrum. Entomol. Exp. Appl. 113:173–179.CrossRefGoogle Scholar
  6. Fatouros, N. E., Huigens, M. E., Van Loon, J. J. A., Dicke, M., and Hilker, M. 2005. Chemical communication—Butterfly anti-aphrodisiac lures parasitic wasps. Nature 433:704.CrossRefPubMedGoogle Scholar
  7. Ferry, A., Dugravot, S., Delattre, T., Christides, J. -P., Auger, J., Bagnères, A. -G., Poinsot, D., and Cortesero, A. -M. 2007. Identification of a widespread monomolecular odor differentially attractive to several Delia radicum ground-dwelling predators in the field. J. Chem. Ecol. 33:2064–2077.CrossRefPubMedGoogle Scholar
  8. Geervliet, J. B. F., Posthumus, M. A., Vet, L. E. M., and Dicke, M. 1997. Comparative analysis of headspace volatiles from different caterpillar-infested or uninfested food plants of Pieris species. J. Chem. Ecol. 23:2935–2954.CrossRefGoogle Scholar
  9. Gouinguené, S., and Turlings, T. C. J. 2002. The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiol. 129:1296–1307.CrossRefPubMedGoogle Scholar
  10. Gouinguené, S., Pickett, J. A., Wadhams, L. J., Birkett, M. A., and Turlings, T. C. J. 2005. Antennal electrophysiological responses of three parasitic wasps to caterpillar-induced volatiles from maize (Zea mays), cotton (Gossypium herbaceum), and cowpea (Vigna unguiculata). J. Chem. Ecol. 31:1023–1038.CrossRefPubMedGoogle Scholar
  11. Herde, M., Gartner, K., Köllner, T. G., Fode, B., Boland, W., Gershenzon, J., Gatz, C., and Tholl, D. 2008. Identification and regulation of TPS04/GES, an Arabidopsis geranyllinalool synthase catalyzing the first step in the formation of the insect-induced volatile C16-homoterpene TMTT. Plant Cell 20:1152–1168.CrossRefPubMedGoogle Scholar
  12. Hoballah, M. E., and Turlings, T. C. J. 2005. The role of fresh versus old leaf damage in the attraction of parasitic wasps to herbivore-induced maize volatiles. J. Chem. Ecol. 31:2003–2018.CrossRefPubMedGoogle Scholar
  13. Ibrahim, M. A., Nissinen, A., and Holopainen, J. K. 2005. Response of Plutella xylostella and its parasitoid Cotesia plutellae to volatile compounds. J. Chem. Ecol. 31:1969–1984.CrossRefPubMedGoogle Scholar
  14. Karban, R., and Baldwin, I. T. 1997. Induced Responses to Herbivory. University of Chicago Press, Chicago.Google Scholar
  15. Loughrin, J. H., Manukian, A., Heath, R. R., Turlings, T. C. J., and Tumlinson, J. H. 1994. Diurnal cycle of emission of induced volatile terpenoids by herbivore-injured cotton plants. Proc. Natl. Acad. Sci. U. S. A. 91:11836–11840.CrossRefPubMedGoogle Scholar
  16. Maeda, T., Takabayashi, J., Yano, S., and Takafuji, A. 2000. Effects of light on the tritrophic interaction between kidney bean plants, two-spotted spider mites and predatory mites, Amblyseius womersleyi (Acari: Phytoseiidae). Exp. Appl. Acarol. 24:415–425.CrossRefPubMedGoogle Scholar
  17. Mattiacci, L., Dicke, M., and Posthumus, M. A. 1994. Induction of parasitoid attracting synomone in Brussels sprouts plants by feeding of Pieris brassicae larvae: Role of mechanical damage and herbivore damage. J. Chem. Ecol. 20:2229–2247.CrossRefGoogle Scholar
  18. Mattiacci, L., Dicke, M., and Posthumus, M. A. 1995. β-Glucosidase: an elicitor of herbivore-induced plant odor that attracts hosts-searching parasitic wasps. Proc. Natl. Acad. Sci. U. S. A. 92:2036–2040.CrossRefPubMedGoogle Scholar
  19. Mattiacci, L., Ambühl-Rocca, B., Scascighini, N., D’Alessandro, M., Hern, A., and Dorn, S. 2001. Systemically induced plant volatiles emitted at the time of “danger”. J. Chem. Ecol. 27:2233–2252.CrossRefPubMedGoogle Scholar
  20. Ratzka, A., Vogel, H., Kliebenstein, D. J., Mitchell-Olds, T., and Kroymann, J. 2002. Disarming the mustard oil bomb. Proc. Natl. Acad. Sci. U. S. A. 99:11223–11228.CrossRefPubMedGoogle Scholar
  21. Sabelis, M. W., Takabayashi, J., Janssen, A., Kant, M. R., Van Wijk, M., Sznajder, B., et al. 2007. Ecology meets plant physiology: herbivore-induced plant responses and their indirect effects on arthropod communities, pp. 188–217, in T. Ohgushi, T. P. Craig and P. W. Price (eds.). Ecological Communities: Plant Mediation in Indirect Interaction Webs. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
  22. Scascighini, N., Mattiacci, L., D’Alessandro, M., Hern, A., Rott A. S., and Dorn, S. 2005. New insights in analysing parasitoid attracting synomones: early volatile emission and use of stir bar sorptive extraction. Chemoecology 15:97–104.CrossRefGoogle Scholar
  23. Sgoutas, D. S., and Kummerow, F. A. 1967. Cis-trans isomerization of unsaturated fatty acid methyl esters without double bond migration. Lipids 4:283–287.CrossRefGoogle Scholar
  24. Shiojiri, K., and Takabayashi, J. 2005. Parasitoid preference for host-infested plants is affected by the risk of intraguild predation. J. Insect Behav. 18:567–576.CrossRefGoogle Scholar
  25. Shiojiri, K., Takabayashi, J., Yano, S., and Takafuji, A. 2000. Flight response of parasitoid toward plant-herbivore complexes: A comparative study of two parasitoid-herbivore systems on cabbage plants. Appl. Entomol. Zool. 35:87–92.CrossRefGoogle Scholar
  26. Shiojiri, K., Ozawa, R., and Takabayashi, J. 2006a. Plant volatiles, rather than light, determine the nocturnal behavior of a caterpillar. PloS Biol. 4:e164. doi: 10.1371/journal.pbio.0040164.CrossRefPubMedGoogle Scholar
  27. Shiojiri, K., Ozawa, R., Matsui, K., Kishimoto, K. Kugimiya, S., and Takabayashi, J. 2006b. Role of the lipoxygenase/lyase pathway of host-food plants in the host searching behavior of two parasitoid species, Cotesia glomerata and Cotesia plutellae. J. Chem. Ecol. 32:969–979.CrossRefPubMedGoogle Scholar
  28. Smid, H. M., Van Loon, J. J. A., Posthumus, M. A., and Vet, L. E. M. 2002. GC-EAG-analysis of volatiles from Brussels sprouts plants damaged by two species of Pieris caterpillars: olfactory receptive range of a specialist and a generalist parasitoid wasp species. Chemoecology 12:169–176.CrossRefGoogle Scholar
  29. Sokal, R. R., and Rohlf, F. J. 1995. Biometry: The Principles and Practice of Statistics in Biological Research (3rd ed.). W. H. Freeman and Company, New York.Google Scholar
  30. Takabayashi, J., and Dicke, M. 1996. Plant-carnivore mutualism through herbivore-induced carnivore attractants. Trends Plant Sci. 1:109–113.CrossRefGoogle Scholar
  31. Takabayashi, J., Dicke, M., and Posthumus, M. A. 1994. Volatile herbivore-induced terpenoids in plant-mite interactions: Variation caused by biotic and abiotic factors. J. Chem. Ecol. 20:1329–1354.CrossRefGoogle Scholar
  32. Tatemoto, S., and Shimoda, T. 2008. Olfactory responses of the predatory mites (Neoseiulus cucumeris) and insects (Orius strigicollis) to two different plant species infested with onion thrips (Thrips tabaci). J. Chem. Ecol. 34:605–613.CrossRefPubMedGoogle Scholar
  33. Turlings, T. C. J., Tumlinson, J. H., and Lewis, W. J. 1990. Exploitation of herbivore-induced plant odors by host seeking parasitic wasps. Science 250:1251–1253.CrossRefPubMedGoogle Scholar
  34. Turlings, T. C. J., Wäckers, F. L., Vet, L. E. M., Lewis, W. J., and Tumlinson, J. H. 1993. Learning of host-finding cues by hymenopterous parasitoids, pp. 51–78, in D. R. Papaj and A. C. Lewis (eds.). Insect Learning. Ecological and Evolutionary Perspectives. Chapman & Hall, New York.Google Scholar
  35. Turlings, T. C. J., Lengwiler, U. B., Bernasconi M. L., and Wechsler, D. 1998. Timing of induced volatile emissions in maize seedlings. Planta 207:146–152.CrossRefGoogle Scholar
  36. Van Poecke, R. M. P., and Dicke, M. 2002. Induced parasitoid attraction by Arabidopsis thaliana: involvement of the octadecanoid and the salicylic acid pathway. J. Exp. Botany 53:1793–1799.CrossRefGoogle Scholar
  37. Van Poecke, R. M. P., Posthumus, M. A., and Dicke, M. 2001. Herbivore-induced volatile production by Arabidopsis thaliana leads to attraction of the parasitoid Cotesia rubecula: chemical, behavioral and gene-expression analysis. J. Chem. Ecol. 27:1911–1928.CrossRefPubMedGoogle Scholar
  38. Vet, L. E. M., Lewis, W. J., and Cardé, R. T. 1995. Parasitoid foraging and learning, pp. 65–101, in R. T. Cardé and W. J. Bell (eds.). Chemical Ecology of Insects II. Chapman & Hall, New York.Google Scholar
  39. Whitman, D. W., and Eller, F. J. 1992. Orientation of Microplitis croceipes (Hymenoptera, Braconidae) to green leaf volatiles: Dose–response curves. J. Chem. Ecol. 18:1743–1753.CrossRefGoogle Scholar
  40. Wittstock, U., and Halkier, B. A. 2002. Glucosinolate research in the Arabidopsis era. Trends Plant Sci. 7: 263–270.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Soichi Kugimiya
    • 1
  • Takeshi Shimoda
    • 2
  • Jun Tabata
    • 1
  • Junji Takabayashi
    • 3
  1. 1.National Institute for Agro-Environmental SciencesTsukubaJapan
  2. 2.National Agricultural Research CenterTsukubaJapan
  3. 3.Center for Ecological ResearchKyoto UniversityOtsuJapan

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