Skip to main content
SpringerLink
Log in

Fungal Infection Reduces Herbivore-Induced Plant Volatiles of Maize but does not Affect Naïve Parasitoids

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

Abstract

Plants attacked by insects release volatile compounds that attract the herbivores' natural enemies. This so-called indirect defense is plastic and may be affected by an array of biotic and abiotic factors. We investigated the effect of fungal infection as a biotic stress agent on the emission of herbivore-induced volatiles and the possible consequences for the attraction of two parasitoid species. Maize seedlings that were simultaneously attacked by the fungus Setosphaeria turcica and larvae of Spodoptera littoralis emitted a blend of volatiles that was qualitatively similar to the blend emitted by maize that was damaged by only the herbivore, but there was a clear quantitative difference. When simultaneously challenged by fungus and herbivore, the maize plants emitted in total 47% less of the volatiles. Emissions of green leaf volatiles were unaffected. In a six-arm olfactometer, the parasitoids Cotesia marginiventris and Microplitis rufiventris responded equally well to odors of herbivore-damaged and fungus- and herbivore-damaged maize plants. Healthy and fungus-infected plants were not attractive. An additional experiment showed that the performance of S. littoralis caterpillars was not affected by the presence of the pathogen, nor was there an effect on larvae of M. rufiventris developing inside the caterpillars. Our results confirm previous indications that naïve wasps may respond primarily to the green leaf volatiles.

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

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Agrawal, A. A., Tuzun, S., and Bent, E. (eds.). 1999. Induced Plant Defenses against Pathogens and Herbivores. The American Phytopathological Society.

  • Alborn, H. T., Turlings, T. C. J., Jones, T. H., Stenhagen, G., Loughrin, J. H., and Tumlinson, J. H. 1997. An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–949.

    Article  CAS  Google Scholar 

  • Borchardt, D. S., Welz, H. G., and Geiger, H. H. 1998. Molecular marker analysis of European Setosphaeria turcica populations. Eur. J. Plant Pathol. 104:611–617.

    Article  CAS  Google Scholar 

  • CAB International. 1988. Distribution maps of plant diseases. Map No. 257, ISSN 0012-396X.

  • Cardoza, Y. J., Alborn, H. T., and Tumlinson, J. H. 2002. In vivo volatile emissions from peanut plants induced by simultaneous fungal infection and insect damage. J. Chem. Ecol. 28:161–174.

    Article  PubMed  CAS  Google Scholar 

  • Cardoza, Y. J., Lait, C. G., Schmelz, E. A., Huang, J., and Tumlinson, J. H. 2003a. Fungus-induced biochemical changes in peanut plants and their effect on development of beet armyworm, Spodoptera exigua Hubner (Lepidoptera: Noctuidae) larvae. Environ. Entomol. 32:220–228.

    Article  CAS  Google Scholar 

  • Cardoza, Y. J., Teal, P. E. A., and Tumlinson, J. H. 2003b. Effect of peanut plant fungal infection on oviposition preference by Spodoptera exigua and on host-searching behavior by Cotesia marginiventris. Environ. Entomol. 32:970–976.

    Google Scholar 

  • D'Alessandro, M. and Turlings, T. C. J. (2005). In situ modification of herbivore-induced plant odours: A novel approach to study the attractiveness of volatile organic compounds to parasitoids. Chem. Senses 30:739–753.

    Article  PubMed  Google Scholar 

  • De Boer, J. G. and Dicke, M. 2004. Experience with methyl salicylate affects behavioural responses of a predatory mite to blends of herbivore-induced plant volatiles. Entomol. Exp. Appl. 110:181–189.

    Article  Google Scholar 

  • De Moraes, C. M., Lewis, W. J., Pare, P. W., Alborn, H. T., and Tumlinson, J. H 1998. Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573.

    Article  Google Scholar 

  • Devoto, A. and Turner, J. G. 2003. Regulation of jasmonate-mediated plant responses in Arabidopsis. Ann. Bot. 92:329–337.

    Article  PubMed  CAS  Google Scholar 

  • Dicke, M. 1999. Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods? Entomol. Exp. Appl. 91:131–142.

    Article  CAS  Google Scholar 

  • Dicke, M. and Sabelis, M. W. 1988. How plants obtain predatory mites as bodyguards. Neth. J. Zool. 38:148–165.

    Article  Google Scholar 

  • Felton, G. W. and Korth, K. L. 2000. Trade-offs between pathogen and herbivore resistance. Curr. Opin. Plant Biol. 3:309–314.

    Article  PubMed  CAS  Google Scholar 

  • Fidantsef, A. L., Stout M. J., Thaler, J. S., Duffey, S. S., and Bostock, R. M. 1999. Signal interactions in pathogen and insect attack: Expression of lipoxygenase, proteinase inhibitor II, and patho genesis-related protein P4 in the tomato, Lycopersicon esculentum. Physiol. Mol. Plant Pathol. 54:97–114.

    Article  CAS  Google Scholar 

  • Gerling, D. 1969. The parasites of Spodoptera littoralis (Boisd.) (Lepidoptera; Noctuidae) eggs and larvae in Israel. Isr. J. Entomol. 4:73–81.

    Google Scholar 

  • Gouinguené, S. P. and Turlings, T. C. J. 2002. The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiol. 129:1296–1307.

    Article  PubMed  CAS  Google Scholar 

  • Gouinguené, S., Degen, T., and Turlings, T. C. J. 2001. Variability in herbivore-induced odour emissions among maize cultivars and their wild ancestors (teosinte). Chemoecology 11:9–16.

    Article  Google Scholar 

  • Guerrieri, E., Poppy, G. M., Powell, W., Tremblay, E., and Pennacchio, F. 1999. Induction and systemic release of herbivore-induced plant volatiles mediating in-flight orientation of Aphidius ervi. J. Chem. Ecol. 25:1247–1261.

    Article  CAS  Google Scholar 

  • Hatcher, P. E. 1995. Three-way interactions between plant pathogenic fungi, herbivorous insects and their host plants. Biol. Rev. 70:639–694.

    Article  Google Scholar 

  • Heath, R. R. and Manukian, A. 1992. Development and evaluation of systems to collect volatile semiochemicals from insects and plants using a charcoal-infused medium for air purification. J. Chem. Ecol. 18:1209–1226.

    Article  CAS  Google Scholar 

  • Hegazi, E. M. 1977. Further studies on certain natural enemies attacking the cotton leafworm in Alexandria region. PhD thesis. University of Alexandria, Egypt.

  • Hilker, M. and Meiners, T. 2002. Induction of plant responses to oviposition and feeding by herbivorous arthropods: A comparison. Entomol. Exp. Appl. 104:181–192.

    Article  CAS  Google Scholar 

  • Hoballah, M. E. F. 2001. Benefits, costs and exploitation of caterpillar-induced odor emissions in maize plants. Ph.D. thesis, University of Neuchâtel, Switzerland.

  • Hoballah, M. E. F. 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 

  • Hoballah, M. E. F., Tamo, C., and Turlings, T. C. J. 2002. Differential attractiveness of induced odors emitted by eight maize varieties for the parasitoid Cotesia marginiventris: Is quality or quantity important? J. Chem. Ecol. 28:951–968.

    Article  PubMed  CAS  Google Scholar 

  • James, D. G. 2003a. Field evaluation of herbivore-induced plant volatiles as attractants for beneficial insects: Methyl salicylate and the green lacewing, Chrysopa nigricornis. J. Chem. Ecol. 29:1601–1609.

    Article  PubMed  CAS  Google Scholar 

  • James, D. G. 2003b. Synthetic herbivore-induced plant volatiles as field attractants for beneficial insects. Environ. Entomol. 32:977–982.

    CAS  Google Scholar 

  • Karban, R. and Baldwin, I. T. 1997. Induced Responses to Herbivory. University of Chicago Press, Chicago.

    Google Scholar 

  • Loughrin, J. H., Manukian, A., Heath, R. R., and Tumlinson, J. H. 1995. Volatiles emitted by different cotton varieties damaged by feeding beet armyworm larvae. J. Chem. Ecol. 21:1217–1227.

    Article  CAS  Google Scholar 

  • Molina-Ochoa, J., Carpenter, J. E., Heinrichs, E. A., and Foster, J. E. 2003. Parasitoids and parasites of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas and Caribbean Basin: An inventory. Fla. Entomol. 86:254–289.

    Article  Google Scholar 

  • Peacock, L., Lewis, M., and Powers, S. 2001. Volatile compounds from Salix spp. varieties differing in susceptibility to three willow beetle species. J. Chem. Ecol. 27:1943–1951.

    Article  PubMed  CAS  Google Scholar 

  • Preston, C. A., Lewandowski, C., Enyedi, A. J., and Baldwin, I. T. 1999. Tobacco mosaic virus inoculation inhibits wound-induced jasmonic acid-mediated responses within but not between plants. Planta 209:87–95.

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Saona, C., Crafts-Brandner, S. J., and Canas, L. A. 2003. Volatile emissions triggered by multiple herbivore damage: Beet armyworm and whitefly feeding on cotton plants. J. Chem. Ecol. 29:2539–2550.

    Article  PubMed  CAS  Google Scholar 

  • Rostás, M., Simon, M., and Hilker, M. 2003. Ecological cross-effects of induced plant responses towards herbivores and phytopathogenic fungi. Basic Appl. Ecol. 4:43–62.

    Article  Google Scholar 

  • Ruther, J. and Kleier, S. 2005. Plant–plant signaling: Ethylene synergizes volatile emission in Zea mays induced by exposure to (Z)-3-hexen-1-ol. J. Chem. Ecol. 31:2217–2222.

    Article  PubMed  CAS  Google Scholar 

  • Schmelz, E. A., Alborn, H. T., Banchio, E., and Tumlinson, J. H. 2003a. Quantitative relationships between induced jasmonic acid levels and volatile emission in Zea mays during Spodoptera exigua herbivory. Planta 216:665–673.

    PubMed  CAS  Google Scholar 

  • Schmelz, E. A., Alborn, H. T., and Tumlinson, J. H. 2003b. Synergistic interactions between volicitin, jasmonic acid and ethylene mediate insect-induced volatile emission in Zea mays. Physiol. Plantarum 117:403–412.

    Article  CAS  Google Scholar 

  • Takabayashi, J., Takahashi, S., Dicke, M., and Posthumus, M. A. 1995. Developmental stage of herbivore Pseudaletia separata affects production of herbivore-induced synomone by corn plants. J. Chem. Ecol. 21:273–287.

    Article  CAS  Google Scholar 

  • Thaler, J. S., Karban, R., Ullman, D. E., Boege, K., and Bostock, R. M. 2002. Cross-talk between jasmonate and salicylate plant defense pathways: Effects on several plant parasites. Oecologia 131:227–235.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Turlings, T. C. J., Loughrin, J. H., McCall, P. J., Rose, U. S. R., Lewis, W. J., and Tumlinson, J. H. 1995. How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc. Natl. Acad. Sci. U.S.A. 92:4169–4174.

    Article  PubMed  CAS  Google Scholar 

  • Turlings, T. C. J., Gouinguene, S., Degen, T., and Fritsche-Hoballah, M. E. 2002. The chemical ecology of plant–caterpillar–parasitoid interactions, pp. 148–173, in T. Tscharntke and B. Hawkins (eds.). Multitrophic Level Interactions. Cambridge University Press, Cambridge.

    Google Scholar 

  • Turlings, T. C. J., Davison, A. C., and Tamo, C. 2004. A six-arm olfactometer permitting simultaneous observation of insect attraction and odour trapping. Physiol. Entomol. 29:45–55.

    Article  Google Scholar 

  • Van Poecke, R. M. P. and Dicke, M. 2004. Indirect defence of plants against herbivores: Using Arabidopsis thaliana as a model plant. Plant Biol. 6:387–401.

    Article  PubMed  CAS  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.

    Article  Google Scholar 

  • Walling, L. L. 2000. The myriad plant responses to herbivores. J. Plant Growth Regul. 19:195–216.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We wish to thank Cristina Faria, Cristina Tamò, Marco d'Alessandro, and Matthias Held for discussions and technical assistance. We also thank Syngenta for supplying us with eggs of S. littoralis. This work was supported by the Deutsche Forschungsgemeinschaft (grant to Michael Rostás, Ro2409/1-1) and the Swiss National Centre of Competence in Research “Plant Survival.” All experiments complied with current laws in Switzerland.

Author information

Author notes

  1. Michael Rostás

    Present address: Lehrstuhl für Botanik II, Julius-von-Sachs-Platz-3, Universität Würzburg, 97082, Würzburg, Germany

Authors and Affiliations

  1. Laboratoire d’Ecologie Animale et d’Entomologie, Rue Emile-Argand 11, Université de Neuchâtel, 2007, Neuchâtel, Switzerland

    Michael Rostás & Ted C. J. Turlings

  2. Laboratoire de Biochimie et Biologie Moléculaire, Rue Emile-Argand 11, Université de Neuchâtel, 2007, Neuchâtel, Switzerland

    Jurriaan Ton & Brigitte Mauch-Mani

Authors
  1. Michael Rostás
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jurriaan Ton
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Brigitte Mauch-Mani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ted C. J. Turlings
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael Rostás.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rostás, M., Ton, J., Mauch-Mani, B. et al. Fungal Infection Reduces Herbivore-Induced Plant Volatiles of Maize but does not Affect Naïve Parasitoids. J Chem Ecol 32, 1897–1909 (2006). https://doi.org/10.1007/s10886-006-9147-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-006-9147-3

Keywords

Search

Navigation