Skip to main content
SpringerLink
Log in

Exposure of Lima Bean Leaves to Volatiles from Herbivore-Induced Conspecific Plants Results in Emission of Carnivore Attractants: Active or Passive Process?

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

There is increasing evidence that volatiles emitted by herbivore-damaged plants can cause responses in downwind undamaged neighboring plants, such as the attraction of carnivorous enemies of herbivores. One of the open questions is whether this involves an active (production of volatiles) or passive (adsorption of volatiles) response of the uninfested downwind plant. This issue is addressed in the present study. Uninfested lima bean leaves that were exposed to volatiles from conspecific leaves infested with the spider mite Tetranychus urticae, emitted very similar blends of volatiles to those emitted from infested leaves themselves. Treating leaves with a protein-synthesis inhibitor prior to infesting them with spider mites completely suppressed the production of herbivore-induced volatiles in the infested leaves. Conversely, inhibitor treatment to uninfested leaves prior to exposure to volatiles from infested leaves did not affect the emission of volatiles from the exposed, uninfested leaves. This evidence supports the hypothesis that response of the exposed downwind plant is passive. T. urticae-infested leaves that had been previously exposed to volatiles from infested leaves emitted more herbivore-induced volatiles than T. urticae-infested leaves previously exposed to volatiles from uninfested leaves. The former leaves were also more attractive to the predatory mite, Phytoseiulus persimilis, than the latter. This shows that previous exposure of plants to volatiles from herbivore-infested neighbors results in a stronger response of plants in terms of predator attraction when herbivores damage the plant. This supports the hypothesis that the downwind uninfested plant is actively involved. Both adsorption and production of volatiles can mediate the attraction of carnivorous mites to plants that have been exposed to volatiles from infested neighbors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  • ABRAMS, P. A., MENGE, B. A., and MITTELBACH, G. G. 1996. The role of indirect effects in food webs, pp. 371–395, inG. A. POLIS and K. O. WINEMILLER (eds.). Food Webs: Integration of Patterns and Dynamics. Chapman & Hall, New York.

    Google Scholar 

  • ARIMURA, G., OZAWA, R., HORIUCHI, J., NISHIOKA, T., and TAKABAYASHI, J. 2001. Plant-plant interactions mediated by volatiles emitted from plants infested by spider mites. Biochem. Syst. Ecol.29:1049–1061.

    Google Scholar 

  • ARIMURA, G., OZAWA, R., SHIMODA, T., NISHIOKA, T., BOLAND, W., and TAKABAYASHI, J. 2000a. Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature406:512–515.

    Google Scholar 

  • ARIMURA, G., TASHIRO, K., KUHARA, S., NISHIOKA, T., and TAKABAYASHI, J. 2000b. Gene responses in bean leaves induced by herbivory and by herbivore-induced volatiles. Biochem. Biophys. Res. Commun.277:305–310.

    Google Scholar 

  • BERNASCONI, M. L., TURLINGS, T. C. J., AMBROSETTI, L., BASSETTI, P., and DORN, S. 1998. Herbivoreinduced emissions of maize volatiles repel the corn leaf aphid, Rhopalosiphum maidis. Entomol. Exp. Appl.87:133–142.

    Google Scholar 

  • BRUIN, J., SABELIS, M. W., and DICKE, M. 1995. Do plants tap SOS signals from their infested neighbours? Trends Ecol. Evol.10:167–170.

    Google Scholar 

  • DICKE, M. 1986. Volatile spider-mite pheromone and host-plant kairomone, involved in spaced-out gregariousness in the spider mite Tetranychus urticae. Physiol. Entomol.11:251–262.

    Google Scholar 

  • DICKE, M. 1999. Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods? Entomol. Exp. Appl.92:131–142.

    Google Scholar 

  • DICKE, M. and BRUIN, J. 2001. Chemical information transfer between plants: Back to the future. Biochem. Syst. Ecol.29:981–994.

    Google Scholar 

  • DICKE, M., GOLS, R., LUDEKING, D., and POSTHUMUS, M. A. 1999. Jasmonic acid and herbivory differentially induce carnivore-attracting plant volatiles in lima bean plants. J. Chem. Ecol.25:1907–1922.

    Google Scholar 

  • DICKE, M. and SABELIS, M. W. 1988. Does it pay plants to advertise for bodyguards? Towards a cost-benefit analysis of induced synomone production, pp. 341–358, inH. LAMBERS, M. L. CAMBRIDGE, H. KONINGS, and T. L. PONS (eds.). Causes and Consequences of Variation in Growth Rate and Productivity of Higher Plants. SPB, The Hague, The Netherlands.

    Google Scholar 

  • DICKE, M., SABELIS, M.W., TAKABAYASHI, J., BRUIN, J., and POSTHUMUS, M.A. 1990. Plant strategies of manipulating predator-prey interactions through allelochemicals: Prospects for application in pest control. J. Chem. Ecol.16:3091–3118.

    Google Scholar 

  • DICKE, M. and VAN LOON, J. J. A. 2000. Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomol. Exp. Appl.97:237–249.

    Google Scholar 

  • DICKE, M., VAN POECKE, R. M. P., and DE BOER, J. G. 2003. Inducible indirect defence of plants: From mechanisms to ecological functions. Basic Appl. Ecol.4:27–42.

    Google Scholar 

  • ENGELBERTH, J., ALBORN, H. T., SCMELZ, E. A., and TUMLINSON, J. H. 2004. Airborne signals prime plants against insect herbivore attack. Proc. Natl. Acad. Sci. U.S.A.101:1781–1785.

    Google Scholar 

  • HOBALLAH-FRITZSCHE, M. E. and TURLINGS, T. C. J. 2001. Experimental evidence that plants under caterpillar attack may benefit from attracting parasitoids. Evol. Ecol. Res.3:553–565.

    Google Scholar 

  • HORIUCHI, J., ARIMURA, G., OZAWA, R., SHIMODA, T., TAKABAYASHI, J., and NISHIOKA, T. 2002. A comparison of the responses of Tetranychus ruticae(Acari: Tetranychidae) and Phytoseiulus persimilis(Acari: Phytoseiidae) to volatiles emitted from lima bean leaves with different levels of damage made by T. urticaeor Spodoptera exigua(Lepidoptera: Noctuidae). Appl. Entomol. Zool. 38:109–116.

    Google Scholar 

  • LANDOLT, P. J., TUMLINSON, J. H., and ALBORN, H. T. 1999. Attraction of Colorado potato beetle (Coleoptera: Chrysomelidae) to damaged and chemically induced potato plants. Environ. Entomol. 28:973–978.

    Google Scholar 

  • MAEDA, T. and TAKABAYASHI, J. 2001. Production of herbivore-induced plant volatiles and their attractiveness to Phytoseiulus persimilis(Acari: Phytoseiidae) with the change of Tetranychus urticae(Acari: Tetranychidae) density on a plant. Appl. Entomol. Zool.36:47–52.

    Google Scholar 

  • MAEDA, T., TAKABAYASHI, J., YANO, S., and TAKAFUJI, A. 1999. Response of the predatory mites. Amblyseius womersleyi(Acari: Phytoseiidae), toward herbivore-induced plant volatiles: Variation in response between two local populations. Appl. Entomol. Zool.34:449–454.

    Google Scholar 

  • MATTIACCI, L., RUDELLI, S., ROCCA, A., GENINI, S., and DORN, S. 2001. Systemically-induced response of cabbage plants against a specialist herbivore Pieris brassicae. Chemoecology11:167–173.

    Google Scholar 

  • POLIS, G. A. and STRONG, D. R. 1996. Food web complexity and community dynamics. Am. Nat. 147:814–846.

    Google Scholar 

  • PRICE, P. W., BOUTON, C. E., GROSS, P., MCPHERON, B. A., THOMPSON, J. N., and WEIS, A. E. 1980. Interaction among three trophic levels: Influence of plants on interactions between insect herbivores and natural enemies. Annu. Rev. Ecol. Syst.11:41–65.

    Google Scholar 

  • SABELIS, M. W., VAN BAALEN, M., BAKKER, F. M., BRUIN, J., DRUKKER, B., EGAS, M., JANSSEN, A. R. M., LESNA, I. K., PELS, B., VAN RIJN, P., and SCUTAREANU, P. 1999. The evolution of direct and indirect plant defence against herbivorous arthropods, pp. 109–166, inH. OLFF, V. K. BROWN, and R. H. DRENT (eds.). Herbivores: Between Plants and Predators. Blackwell Science, Oxford.

    Google Scholar 

  • SHIMODA, T., OZAWA, R., ARIMURA, G., TAKABAYASHI, J., and NISHIOKA, T. 2002. Olfactory response of two specialist insect predators of spider mites toward plant volatiles from lima bean leaves induced by jasmonic and/or methyl salicylate. Appl. Entomol. Zool.37:535–541.

    Google Scholar 

  • SHIMODA, T. and TAKABAYASHI, J. 2001. Response of Oligota kashmirica benefica, a specialist insect predator of spider mites, to volatiles from prey-infested leaves under both laboratory and field conditions. Entomol. Exp. Appl.101:41–47.

    Google Scholar 

  • SHIMODA, T., TAKABAYASHI, J., ASHIHARA, A., and TAKAFUJI, A. 1997. Response of predatory insect Scolothrips takahasiitoward herbivore-induced plant volatiles under laboratory and field conditions. J. Chem. Ecol.23:2033–2048.

    Google Scholar 

  • TAKABAYASHI, J. and DICKE, M. 1992. Response of predatory mites with different rearing histories to volatiles of uninfested plants. Entomol. Exp. Appl.64:187–193.

    Google Scholar 

  • TAKABAYASHI, J. and DICKE,M. 1996. Plant-carnivore mutualism through herbivore-induced carnivore attractants. Trends Plant Sci.1:109–113.

    Google Scholar 

  • TURLINGS, T. C. J., LOUGHRIN, J. H., MCCALL, P., J., ROSE, U. S. R., LEWIS, W. J., and TUMLINSON, J. H. 1995. Howcaterpillar-damaged plants protect themselves by attracting parasiticwasps. Proc. Natl. Acad. Sci. U.S.A.92:4169–4174.

    Google Scholar 

  • 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, inD. R. PAPAI and A. C. LEWIS (eds.). Insect Learning: Ecological and Evolutionary Perspectives. Chapman & Hall, New York.

    Google Scholar 

  • VAN LOON, J. J. A., DE BOER, J. G., and DICKE,M. 2000. Parasitoid-plant mutualism: Parasitoid attack of herbivore increases plant reproduction. Entomol. Exp. Appl.97:219–227.

    Google Scholar 

  • VET, L. E. M. and DICKE, M. 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol.37:141–172.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Center for Ecological Research, Kyoto University, Otsuka 509-3, Hirano, Kamitanakami, Otsu, 520-2113, Japan

    Yasuyuki Choh & Rika Ozawa

  2. Insect Biocontrol Laboratory, Department of Entomology and Nematology, National Agricultural Research Center, Ibaraki, 305-8666, Japan

    Takeshi Shimoda

  3. Laboratory of Entomology, Wageningen University, P. O. Box 8031, 6700EH, Wageningen, The Netherlands

    Marcel Dicke & Junji Takabayashi

  4. Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Corporation, Japan

    Junji Takabayashi

Authors
  1. Yasuyuki Choh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Takeshi Shimoda
    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. Marcel Dicke
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Junji Takabayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Choh, Y., Shimoda, T., Ozawa, R. et al. Exposure of Lima Bean Leaves to Volatiles from Herbivore-Induced Conspecific Plants Results in Emission of Carnivore Attractants: Active or Passive Process?. J Chem Ecol 30, 1305–1317 (2004). https://doi.org/10.1023/B:JOEC.0000037741.13402.19

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:JOEC.0000037741.13402.19

Search

Navigation