In response to insect herbivory, plants synthesize and emit blends of volatile compounds from their damaged and undamaged tissues, which act as important host-location cues for parasitic insects1,2,3. Here we use chemical and behavioural assays to show that these plant emissions can transmit herbivore-specific information that is detectable by parasitic wasps (parasitoids). Tobacco, cotton and maize plants each produce distinct volatile blends in response to damage by two closely related herbivore species, Heliothis virescens and Helicoverpa zea. The specialist parasitic wasp Cardiochiles nigriceps exploits these differences to distinguish infestation by its host, H. virescens, from that by H.zea. The production by phylogenetically diverse plant species and the exploitation by parasitoids of highly specific chemical signals, keyed to individual herbivore species, indicates that the interaction between plants and the natural enemies of the herbivores that attack them is more sophisticated than previously realized.
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Dicke, M. Local and systemic production of volatile herbivore-induced terpenoids: their role in plant-carnivore mutualism. J. Plant Physiol. 143, 465–472 (1994).
Turlings, T. C. J., Tumlinson, J. H. & Lewis, W. J. Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250, 1251–1253 (1990).
McCall, P. J., Turlings, T. C. J., Lewis, W. J. & Tumlinson, J. H. Role of plant volatiles in host location by the specialist parasitoid Microplitis croceipes Cresson (Braconidae:Hymenoptera). J. Ins. Behav. 6, 625–639 (1993).
Karban, R. Resistance against spider mites in cotton induced by mechanical abrasion. Entomol. Exp. appl. 37, 137–141 (1985).
Dicke, M.et al. Isolation and identification of volatile kairomone that affects acarine predator–prey interactions. Involvement of host plant in its production. J. Chem. Ecol. 16, 381–396 (1990).
Mattiacci, L., Dicke, M. & Posthumus, M. A. Induction of parasitoid attracting synomone in brussels sprouts plants by feeding of Pieres brassicae larvae: Role of mechanical damage and herbivore elicitor. J. Chem. Ecol. 20, 2229–2247 (1994).
Turlings, T. C. J.et al. How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc. Natl Acad. Sci. USA 92, 4169–4174 (1995).
Alborn, H. T.et al. An elicitor of plant volatiles from beet armyworm oral secretion. Science 276, 945–948 (1997).
Paré, P. W. & Tumlinson, J. H. Induced synthesis of plant volatiles. Nature 385, 30–31 (1997).
Udayagiri, S. & Jones, R. L. Role of plant odor in parasitism of European corn borer by braconid specialist Macrocentrus grandii Goidanich: Isolation and characterization of plant synomones eliciting arasitoid flight response. J. Chem. Ecol. 18, 1841–1855 (1992).
Turlings, T. C. J., Wäckers, F. L., Vet, L. E. M., Lewis, W. J. & Tumlinson, J. H. in Insect Learning (eds Papaj, D. R. & Lewis, A. C.) 51–78 (Chapman & Hall, New York, (1993).
Loughrin, J. H., Manukian, A., Heath, R. R. & Tumlinson, J. H. Diurnal cycle of emission of induced volatile terpenoids by herbivore-injured cotton plants. J. Chem. Ecol. 21, 1217–1227 (1994).
Takabayashi, J., Dicke, M. & Posthumus, M. A. Variation in composition of predator-attracting allelochemicals emitted by herbivore-infested plants: Relative influence of plant and herbivore. Chemoecology 2, 1–6 (1991).
Du, Y.-J., Poppy, G. M. & Powell, W. Relative importance of semiochemicals from first and second trophic levels in host foraging behavior of Aphidius ervi. J. Chem. Ecol. 22, 1591–1605 (1996).
Lewis, W. J. & Takasu, K. Use of learned odours by a parasitic wasp in accordance with host and food needs. Nature 348, 635–636 (1990).
Tumlinson, J. H., Lewis, W. J. & Vet, L. E. M. How parasitic wasps find their hosts. Sci. Am. 268, 100–106 (1993).
Bell, W. J., Kipp, L. R. & Collins, R. D. in Chemical Ecology of Insects 2 (eds Cardé, R. T. & Bell, W. J.) 105–154 (Chapman & Hall, New York, (1995).
Strand, M. R. & Obrycki, J. J. Host specificity of insect parasitoids and predators. BioScience 46, 422–429 (1996).
Futuyma, D. J. & Moreno, G. The evolution of ecological specialization. Annu. Rev. Ecol. Syst. 19, 207–233 (1988).
Thompson, J. N. The Coevolutionary Process (Univ. of Chicago Press, Chicago, (1994).
Röse, U. S. R., Manukian, A., Heath, R. R. & Tumlinson, J. H. Volatile semiochemicals released from undamaged cotton leaves: A systemic response of living plants to caterpillar damage. Plant Physiol. 111, 487–495 (1996).
Heath, R. R. & Manukian, A. J. Chem. Ecol. 20, 593–608 (1994).
We thank M. C. Mescher for assistance in preparing the manuscript; T. C. Turlings, P. J. Landolt, J. Garcia, B. Benrey, K. Ross, K. Korth and J. Ruberson for comments on the manuscript; A. T. Proveaux for assistance with mass spectrometric analysis; J. H. Loughrin for leaf measurement software; and T. Green for insect rearing. C.D.M. is recipient of fellowship from CAPES (Brazil).
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De Moraes, C., Lewis, W., Paré, P. et al. Herbivore-infested plants selectively attract parasitoids. Nature 393, 570–573 (1998). https://doi.org/10.1038/31219
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