Skip to main content
SpringerLink
Log in

Strong Attraction of the Parasitoid Cotesia marginiventris Towards Minor Volatile Compounds of Maize

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

Abstract

Plants infested with herbivorous arthropods emit complex blends of volatile compounds, which are used by several natural enemies as foraging cues. Despite detailed knowledge on the composition and amount of the emitted volatiles in many plant-herbivore systems, it remains largely unknown which compounds are essential for the attraction of natural enemies. In this study, we used a combination of different fractionation methods and olfactometer bioassays in order to examine the attractiveness of different compositions of volatile blends to females of the parasitoid Cotesia marginiventris. In a first step, we passed a volatile blend emitted by Spodoptera littoralis infested maize seedlings over a silica-containing filter tube and subsequently desorbed the volatiles that were retained by the silica filter (silica extract). The volatiles that broke through the silica filter were collected on and subsequently desorbed from a SuperQ filter (breakthrough). The silica extract was highly attractive to the wasps, whereas the breakthrough volatiles were not attractive. The silica extract was even more attractive than the extract that contained all herbivore-induced maize volatiles. Subsequently, we fractioned the silica extract by preparative gas-chromatography (GC) and by separating more polar from less polar compounds. In general, C. marginiventris preferred polar over non-polar compounds, but several fractions were attractive to the wasp, including one that contained compounds emitted in quantities below the detection threshold of the GC analysis. These results imply that the attractiveness of the volatile blend emitted by Spodoptera-infested maize seedlings to C. marginiventris females is determined by a specific combination of attractive and repellent/masking compounds, including some that are emitted in very small amounts. Manipulating the emission of such minor compounds has the potential to greatly improve the attraction of certain parasitoids and enhance biological control of specific insect pests.

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Angioy, A. M., Desogus, A., Barbarossa, I. T., Anderson P., and Hansson B. S. 2003. Extreme sensitivity in an olfactory system. Chem. Sens. 28:279–284.

    Article  Google Scholar 

  • Arimura, G., Matsui, K., and Takabayashi J. 2009. Chemical and molecular ecology of herbivore-induced plant volatiles: Proximate factors and their ultimate functions. Plant Cell Physiol. 50:911–923.

    Article  PubMed  CAS  Google Scholar 

  • Baldwin, I. T., Halitschke, R., Kessler, A., and Schittko, U. 2001. Merging molecular and ecological approaches in plant-insect interactions. Curr. Opin. Plant Biol. 4:351–358.

    Article  PubMed  CAS  Google Scholar 

  • D’alessandro, M., Held, M., Triponez, Y., and Turlings, T. C. J. 2006. The role of indole and other shikimic acid derived maize volatiles in the attraction of two parasitic wasps. J. Chem. Ecol. 32:2733–2748.

    Article  PubMed  Google Scholar 

  • D’alessandro, M. and Turlings, T. C. J. 2005. In situ modification of herbivore-induced plant odors: A novel approach to study the attractiveness of volatile organic compounds to parasitic wasps. Chem. Sens. 30:739–753.

    Article  Google Scholar 

  • D’alessandro, M. and Turlings, T. C. J. 2006. Advances and challenges in the identification of volatiles that mediate interactions among plants and arthropods. Analyst 131:24–32.

    Article  PubMed  Google Scholar 

  • De Boer, J. G., and Dicke M. 2004. The role of methyl salicylate in prey searching behavior of the predatory mite Phytoseiulus persimilis. J. Chem. Ecol. 30:255–271.

    Article  PubMed  CAS  Google Scholar 

  • Degen, T., Dillmann, C., Marion-Poll, F., and Turlings, T. C. J. 2004. High genetic variability of herbivore-induced volatile emission within a broad range of maize inbred lines. Plant Physiol. 135:1928–1938.

    Article  PubMed  CAS  Google Scholar 

  • Degenhardt, J., Hiltpold, I., Köllner, T. G., Frey, M., Gierl, A., Gershenzon, J., Hibbard, B. E., Ellersieck, M. R., and Turlings, T. C. J. 2009. Restoring a maize root signal that attracts insect-killing nematodes to control a major pest. Proc. Natl. Acad. Sci. USA 106:13213–13218.

    Article  PubMed  CAS  Google Scholar 

  • Dicke, M., 2009. Behavioural and community ecology of plants that cry for help. Plant Cell Environ. 32:654–665.

    Article  PubMed  CAS  Google Scholar 

  • Dicke, M., Van Loon, J. J. A., and Soler, R. 2009. Chemical complexity of volatiles from plants induced by multiple attack. Nat. Chem. Biol. 5:317–324.

    Article  PubMed  CAS  Google Scholar 

  • Dudareva, N., Negre, F., Nagegowda, D. A., and Orlova, I. 2006. Plant volatiles: Recent advances and future perspectives. Crit. Rev. Plant Sci. 25:417–440.

    Article  CAS  Google Scholar 

  • Fritzsche Hoballah, M. E., Tamò, 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  Google Scholar 

  • Frost, C. J., Mescher, M. C., Dervinis, C., Davis, J. M., Carlson, J. E., and De Moraes, C. M. 2008. Priming defense genes and metabolites in hybrid poplar by the green leaf volatile cis-3-hexenyl acetate. New Phytol. 180:722–733.

    Article  PubMed  CAS  Google Scholar 

  • Gaquerel, E., Weinhold, A., and Baldwin, I. T. 2009. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphigidae) and its natural host Nicotiana attenuata. VIII. An unbiased GCxGC-ToFMS analysis of the plant’s elicited volatile emissions. Plant Physiol. 149:1408–1423.

    Article  PubMed  CAS  Google Scholar 

  • 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 mays), cotton (Gossypium herbaceum), and cowpea (Vigna unguiculata). J. Chem. Ecol. 31:1023–1038.

    Article  PubMed  Google Scholar 

  • Heil, M. 2008. Indirect defence via tritrophic interactions. New Phytol. 178:41–61.

    Article  PubMed  CAS  Google Scholar 

  • Kappers, I. F., Aharoni, A., Van Herpen, T., Luckerhoff, L. L. P., Dicke, M., and Bouwmeester, H. J. 2005. Genetic engineering of terpenoid metabolism attracts, bodyguards to Arabidopsis. Science 309:2070–2072.

    Article  PubMed  CAS  Google Scholar 

  • Köllner, T. G., Schnee, C., Gershenzon, J., and Degenhardt, J. 2004. The sesquiterpene hydrocarbons of maize (Zea mays) form five groups with distinct developmental and organ-specific distribution. Phytochemistry 65:1895–1902.

    Article  PubMed  Google Scholar 

  • Loivamaki, M., Mumm, R., Dicke, M., and Schnitzler, J. P. 2008. Isoprene interferes with the attraction of bodyguards by herbaceous plants. Proc. Natl. Acad. Sci. USA 105:17430–17435.

    Article  PubMed  Google Scholar 

  • Mumm, R. and Hilker, M. 2005. The significance of background odour for an egg parasitoid to detect plants with host eggs. Chem. Sens. 30:337–343.

    Article  CAS  Google Scholar 

  • Ngumbi, E. N., Ngi-Song, A. J., Njagi, E. N. M., Torto, R., Wadhams, L. J., Birkett, M. A., Pickett, J. A., Overholt, W. A., and Torto, B. 2005. Responses of the stem borer larval endoparasitoid Cotesia flavipes (Hymenoptera: Braconidae) to plant derived synomones: Laboratory and field cage experiments. Biocontrol Sci. Techn. 15:271–279.

    Article  Google Scholar 

  • Niinemets, U., Loreto, F., and Reichstein, M. 2004. Physiological and physicochemical controls on foliar volatile organic compound emissions. Trends Plant Sci. 9:180–186.

    Article  PubMed  CAS  Google Scholar 

  • Paré, P. W. and Tumlinson, J. H. 1999. Plant volatiles as a defense against insect herbivores. Plant Physiol. 121:325–331.

    Article  PubMed  Google Scholar 

  • Pareja, M., Mohib, A., Birkett, M. A., Dufour, S., and Glinwood, R. T. 2009. Multivariate statistics coupled to generalized linear models reveal complex use of chemical cues by a parasitoid. Anim. Behav. 77:901–909.

    Article  Google Scholar 

  • Paschold, A., Halitschke. R., and Baldwin, I. T. 2006. Using ‘mute’ plants to translate volatile signals. Plant J. 45:275–291.

    Article  PubMed  CAS  Google Scholar 

  • Penuelas, J., Filella, I., Stefanescu, C., and Llusia, J. 2005. Caterpillars of Euphydryas aurinia (Lepidoptera: Nymphalidae) feeding on Succisa pratensis leaves induce large foliar emissions of methanol. New Phytol. 167:851–857.

    Article  PubMed  CAS  Google Scholar 

  • Pichersky, E., Noel, J. P., and Dudareva, N. 2006. Biosynthesis of plant volatiles: Nature’s diversity and ingenuity. Science 311:808–811.

    Article  PubMed  CAS  Google Scholar 

  • Rasmann, S. and Turlings, T. C. J. 2008. First insights into specificity of belowground tritrophic interactions. Oikos 117:362–369.

    Article  Google Scholar 

  • Schnee, C., Köllner, T. G., Held, M., Turlings, T. C. J., Gershenzon, J., and Degenhardt, J. 2006. The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. Proc. Natl. Acad. Sci. USA 103:1129–1134.

    Article  PubMed  CAS  Google Scholar 

  • Schröder, R. and Hilker, M. 2008. The relevance of background odor in resource location by insects: A behavioral approach. Bioscience 58:308–316.

    Article  Google Scholar 

  • Takács, S., Gries, G., and Gries, R. 1997. Semiochemical-mediated location of host habitat by Apanteles carpatus (Say) (Hymenoptera: Braconidae), a parasitoid of clothes moth larvae. J. Chem. Ecol. 23:459–472.

    Article  Google Scholar 

  • Tamò, C., Ricard, I., Held, M., Davison, A. C., and Turlings, T. C. J. 2006. A comparison of naive and conditioned responses of three generalist endoparasitoids of lepidopteran larvae to host-induced plant odours. Anim. Biol. 56:205–220.

    Article  Google Scholar 

  • Ton, J., D’alessandro, M., Jourdie, V., Jakab, G., Karlen, D., Held, M., Mauch-Mani, B., and Turlings, T. C. J. 2007. Priming by airborne signals boosts direct and indirect resistance in maize. Plant J. 49:16–26.

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Turlings, T. C. J., Tumlinson, J. H., Eller, F. J., and Lewis, W. J. 1991a. Larval-damaged plants—Source of volatile synomones that guide the parasitoid Cotesia marginiventris to the microhabitat of its hosts. Entomol. Exp. Appl. 58:75–82.

    Article  Google Scholar 

  • Turlings, T. C. J., Tumlinson, J. H., Heath, R. R., Proveaux, A. T., and Doolittle, R. E. 1991b. Isolation and identification of allelochemicals that attract the larval parasitoid, Cotesia marginiventris (Cresson), to the microhabitat of one of its hosts. J. Chem. Ecol. 17:2235–2251.

    Article  CAS  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. and Wäckers, F. 2004. Recruitment of predators and parasitoids by herbivore-injured plants, pp. 21–75, in R. T. Cardé and J. G. Millar (eds.). Advances in Insect Chemical Ecology. Cambridge University Press. Cambridge.

    Google Scholar 

  • Van Dam, N. M. and Poppy, G. M. 2008. Why plant volatile analysis needs bioinformatics—detecting signal from noise in increasingly complex profiles. Plant Biol. 10:29–37.

    PubMed  CAS  Google Scholar 

  • Von Dahl, C. C., Havecker, M., Schlogl, R., and Baldwin, I. T. 2006. Caterpillar-elicited methanol emission: a new signal in plant-herbivore interactions? Plant J. 46:948–960.

    Article  PubMed  CAS  Google Scholar 

  • Yan, Z. G. and Wang, C. Z. 2006. Identification of Mythmna separata-induced maize volatile synomones that attract the parasitoid Campoletis chlorideae. J. Appl. Entomol. 130:213–219.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank the members of the Laboratory of Fundamental and Applied Research in Chemical Ecology (FARCE) at the University of Neuchâtel for continuous support and stimulating discussions on behavioral and chemical aspects. We are grateful to Yves Borcard and students of the University of Neuchâtel for parasitoid rearing and Syngenta (Stein, Switzerland) for the weekly shipments of S. littoralis eggs. Statistical advice was provided by Ingrid Ricard and Anthony Davison (EPF Lausanne, Switzerland). This project was possible due to the Research Fellow Partnership Program of the North-South Centre at the ETH-Zurich (RFPP-fellowship) and funded by the Swiss Agency for Development and Cooperation (SDC).

Author information

Authors and Affiliations

  1. Laboratory of Fundamental and Applied Research in Chemical Ecology (FARCE), University of Neuchâtel, Institute of Biology, Case Postale 158, CH-2009, Neuchâtel, Switzerland

    Marco D’Alessandro, Virginie Brunner, Georg von Mérey & Ted C. J. Turlings

Authors
  1. Marco D’Alessandro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Virginie Brunner
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Georg von Mérey
    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 Marco D’Alessandro.

Rights and permissions

Reprints and permissions

About this article

Cite this article

D’Alessandro, M., Brunner, V., von Mérey, G. et al. Strong Attraction of the Parasitoid Cotesia marginiventris Towards Minor Volatile Compounds of Maize. J Chem Ecol 35, 999–1008 (2009). https://doi.org/10.1007/s10886-009-9692-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-009-9692-7

Keywords

Search

Navigation