Caterpillar-induced nocturnal plant volatiles repel conspecific females

Abstract

Plants respond to insect herbivory by synthesizing and releasing complex blends of volatile compounds, which provide important host-location cues for insects that are natural enemies of herbivores1,2,3. The effects of these volatile blends on herbivore behaviour have been investigated to only a limited extent4,5, in part because of the assumption that herbivore-induced volatile emissions occur mainly during the light phase of the photoperiod6,7. Because many moths—whose larvae are some of the most important insect herbivores—are nocturnal, herbivore-induced plant volatiles have not hitherto been considered to be temporally available as host-location cues for ovipositing females. Here we present chemical and behavioural assays showing that tobacco plants (Nicotiana tabacum) release herbivore-induced volatiles during both night and day. Moreover, several volatile compounds are released exclusively at night and are highly repellent to female moths (Heliothis virescens). The demonstration that tobacco plants release temporally different volatile blends and that lepidopteran herbivores use induced plant signals released during the dark phase to choose sites for oviposition adds a new dimension to our understanding of the role of chemical cues in mediating tritrophic interactions.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Gas chromatographic analysis of induced plant volatiles.
Figure 2: Response of female moths to plant volatiles.

References

  1. 1

    Dicke, M. Local and systemic production of volatile herbivore-induced terpenoids: their role in plant-carnivore mutualism. J. Plant Physiol. 143, 465–472 (1994).

    CAS  Article  Google Scholar 

  2. 2

    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).

    ADS  CAS  Article  Google Scholar 

  3. 3

    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. Insect Behav. 6, 625–639 (1993).

    Article  Google Scholar 

  4. 4

    Pallini, A., Jansen, A. & Sabelis, M. Odour-mediated responses of phytophagous mites to conspecific and heterospecific competitors. Oecologia 110, 179–185 (1997).

    ADS  CAS  Article  Google Scholar 

  5. 5

    Karban, R. & Baldwin, I. T. Induced Responses to Herbivory (Univ. Chicago Press, Chicago, Illinois, 1997).

    Google Scholar 

  6. 6

    Paré, P. W. & Tumlinson, J. H. Induced synthesis of plant volatiles. Nature 385, 30–31 (1997).

    ADS  Article  Google Scholar 

  7. 7

    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).

    Article  Google Scholar 

  8. 8

    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).

    ADS  CAS  Article  Google Scholar 

  9. 9

    Karban, R. Resistance against spider mites in cotton induced by mechanical abrasion. Entomol. Exp. Appl. 37, 137–141 (1985).

    Article  Google Scholar 

  10. 10

    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).

    CAS  Article  Google Scholar 

  11. 11

    Mattiacci, L., Dicke, M. & Posthumus, M. A. Induction of parasitoid attracting synomone in brussels sprouts plants by feeding of Pieris brassicae larvae: Role of mechanical damage and herbivore elicitor. J. Chem. Ecol. 20, 2229–2247 (1994).

    CAS  Article  Google Scholar 

  12. 12

    Alborn, H. T. et al. An elicitor of plant volatiles from beet armyworm oral secretion. Science 276, 945–948 (1997).

    CAS  Article  Google Scholar 

  13. 13

    De Moraes, C. M. et al. Herbivore-infested plants selectively attract parasitoids. Nature 393, 570–573 (1998).

    ADS  CAS  Article  Google Scholar 

  14. 14

    Dicke, M. Volatile spider-mite pheromone and host plant kairomone, involved in spaced-out gregariousness in spider mite Tetranychus urticae. Physiol. Entomol. 11, 251–262 (1986).

    Article  Google Scholar 

  15. 15

    Schultz, S. et al. Host plant selection of the Colorado Potato Beetle as influenced by damage induced volatiles of the potato plant. Naturwissenschaften 84, 212–217 (1997).

    ADS  Article  Google Scholar 

  16. 16

    Harari, A. R., Ben-Yakir, D. & Rosen, D. Mechanisms of aggregation behavior in Maladera matrida Argaman (Coleoptera: Scarabeidae). J. Chem. Ecol. 20, 361–371 (1994).

    CAS  Article  Google Scholar 

  17. 17

    Landolt, P. J., Tumlinson, J. H. & Alborn, D. H. Attraction of Colorado potato beetle (Coleoptera : Chrysomelidae) to damaged and chemically induced potato plants. Environ. Entomol. 28, 973–978 (1999).

    Article  Google Scholar 

  18. 18

    Landolt, P. J. Effects of host plant leaf damage on cabbage looper moth attraction and oviposition. Entomol. Exp. Appl. 67, 79–85 (1993).

    Article  Google Scholar 

  19. 19

    Heath, R. R. & Tumlinson, J. H. Prediction of release ratios of multicomponent pheromones from rubber septa. J. Chem. Ecol. 12, 2081–2088 (1986).

    CAS  Article  Google Scholar 

  20. 20

    Heath, R. R., Teal, P. E. A., Tumlinson, J. H. & Mengelkoch, L. J. Correlation of retention times on liquid crystal capillary column with reported vapor pressures and half-lives of compounds used in pheromone formulations. J. Chem. Ecol. 12, 2133–2143 (1986).

    CAS  Article  Google Scholar 

  21. 21

    Thaler, J. S. Jasmonate-inducible plant defenses cause increased parasitism of herbivores. Nature 399, 686–588 (1999).

    ADS  CAS  Article  Google Scholar 

  22. 22

    Agrawal, A. A. Induced responses to herbivory and increased plant performance. Science 279, 1201–1202 (1998).

    ADS  CAS  Article  Google Scholar 

  23. 23

    Coley, P. D., Bryant, J. P. & Chapin, F. S. Resource availability and plant antiherbivore defense. Science 230, 895–899 (1985).

    ADS  CAS  Article  Google Scholar 

  24. 24

    Heath, R. R. & Manukian, A. An automated-system for use in collecting volatile chemicals released from plants. J. Chem. Ecol. 20, 593–608 (1994).

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank G. W. G. De Moraes for discussions; H. T. Alborn, J. G. Hildebrand, P. J. Landolt, W. J. Lewis, K. G. Ross and J. R. Ruberson for comments on the manuscript; and B. Dueben and M. Sammons for technical assistance.

Author information

Affiliations

Authors

Corresponding author

Correspondence to James H. Tumlinson.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

De Moraes, C., Mescher, M. & Tumlinson, J. Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410, 577–580 (2001). https://doi.org/10.1038/35069058

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing