Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Experimental evidence for apparent competition in a tropical forest food web

Abstract

The herbivorous insects of tropical forests constitute some of the most diverse communities of living organisms1. For this reason it has been difficult to discover the degree to which these communities are structured, and by what processes. Interspecific competition for resources does occur, but its contemporary importance is limited because most pairs of potentially competing insects feed on different host plants2. An alternative way in which species can interact is through shared natural enemies, a process called apparent competition3. Despite extensive theoretical discussion there are few field demonstrations of apparent competition, and none in hyper-diverse tropical communities. Here, we experimentally removed two species of herbivore from a community of leaf-mining insects in a tropical forest. We predicted that other species that share natural enemies with the two removed species would experience lower parasitism and have higher population densities in treatment compared with control sites. In both cases (on removal of a dipteran and a coleopteran leaf-miner species) we found significantly lower parasitism, and in one case (removal of the dipteran) we found significantly higher abundance a year after the manipulation. Our results suggest that apparent competition may be important in structuring tropical insect communities.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Quantitative food web17 showing leaf-miner species (bottom bars), parasitoid species (top bars), trophic links among them, and the species predicted to be affected by the manipulation.
Figure 2: Effect of species removal on parasitism (a) and species abundances (b) 1 year after the manipulation.

Similar content being viewed by others

References

  1. Novotny, V. et al. Low host specificity of herbivorous insects in a tropical forest. Nature 416, 841–844 (2002)

    Article  ADS  CAS  Google Scholar 

  2. Strong, D. R., Lawton, J. H. & Southwood, T. R. E. Insects on Plants: Community Patterns and Mechanisms (Blackwell Science, Oxford, 1984)

    Google Scholar 

  3. Holt, R. D. Predation, apparent competition and the structure of prey communities. Theor. Popul. Biol. 12, 197–229 (1977)

    Article  MathSciNet  CAS  Google Scholar 

  4. Strauss, S. Y. Indirect effects in community ecology—their definition, study and importance. Trends Ecol. Evol. 6, 206–210 (1991)

    Article  CAS  Google Scholar 

  5. Wootton, J. T. The nature and consequences of indirect effects in ecological communities. Annu. Rev. Ecol. Syst. 25, 443–466 (1994)

    Article  Google Scholar 

  6. Abrams, P. A., Menge, B. A., Mittelback, G. G., Spiller, D. A. & Yodzis, P. Food Webs: Integration of Patterns and Dynamics. (eds Polis, G. & Winemiller, K. O.) 371–395 (Chapman & Hall, New York, 1995)

    Google Scholar 

  7. Holt, R. D. & Lawton, J. H. Apparent competition and enemy-free space in insect host-parasitoid communities. Am. Nat. 142, 623–645 (1993)

    Article  CAS  Google Scholar 

  8. Schmitt, R. J. Indirect interactions between prey: apparent competition, predator aggregation, and habitat segregation. Ecology 68, 1887–1897 (1987)

    Article  Google Scholar 

  9. Menge, B. A. Indirect effects in marine rocky intertidal interaction webs: Patterns and importance. Ecol. Monogr. 65, 21–74 (1995)

    Article  Google Scholar 

  10. Tomkins, D. M., Draycott, R. A. H. & Hudson, P. J. Field evidence for apparent competition mediated via the shared parasites of two gamebird species. Ecol. Lett. 3, 10–14 (2000)

    Article  Google Scholar 

  11. Muller, C. B. & Godfray, H. C. J. Apparent competition between two aphid species. J. Anim. Ecol. 66, 57–64 (1997)

    Article  Google Scholar 

  12. Morris, R. J., Müller, C. B. & Godfray, H. C. J. Field experiments testing for apparent competition between primary parasitoids mediated by secondary parasitoids. J. Anim. Ecol. 70, 301–309 (2001)

    Article  Google Scholar 

  13. Bonsall, M. B. & Hassell, M. P. Apparent competition structures ecological assemblages. Nature 338, 371–373 (1997)

    Article  ADS  Google Scholar 

  14. Settle, W. H. & Wilson, L. T. Invasion by the variegated leafhopper and biotic interactions: parasitism, competition and apparent competition. Ecology 71, 1461–1470 (1990)

    Article  Google Scholar 

  15. Janzen, D. H. Herbivores and the number of tree species in tropical forests. Am. Nat. 104, 501–528 (1970)

    Article  Google Scholar 

  16. Hespenheide, H. A. Bionomics of leaf-mining insects. Annu. Rev. Entomol. 36, 535–560 (1991)

    Article  Google Scholar 

  17. Lewis, O. T. et al. Structure of a diverse tropical forest insect-parasitoid community. J. Anim. Ecol. 71, 855–873 (2002)

    Article  Google Scholar 

  18. Holt, R. D. & Lawton, J. H. The ecological consequences of shared natural enemies. Annu. Rev. Ecol. Syst. 25, 495–520 (1994)

    Article  Google Scholar 

  19. Abrams, P. The theory of limiting similarity. Annu. Rev. Ecol. Syst. 14, 359–376 (1983)

    Article  Google Scholar 

  20. Jeffries, M. J. & Lawton, J. H. Enemy free space and the structure of ecological communities. Biol. J. Linn. Soc. 23, 269–286 (1984)

    Article  Google Scholar 

  21. Abrams, P. A. & Matsuda, H. Positive indirect effects between prey species that share predators. Ecology 77, 610–616 (1996)

    Article  Google Scholar 

  22. Bonsall, M. B. & Hassell, M. P. The effects of metapopulation structure on indirect interactions in host-parasitoid assemblages. Proc. R. Soc. Lond. B 267, 2207–2212 (2000)

    Article  CAS  Google Scholar 

  23. Bonsall, M. B. & Hassell, M. P. Parasitoid-mediated effects: apparent competition and the persistence of host-parasitoid assemblages. Res. Popul. Ecol. 41, 59–68 (1999)

    Article  Google Scholar 

  24. Turchin, P. Complex Population Dynamics: A Theoretical/Empirical Synthesis (Princeton Univ. Press, Princeton, New Jersey, 2003)

    MATH  Google Scholar 

  25. Power, M. E. et al. Challenges in the quest for keystones. Bioscience 46, 609–620 (1996)

    Article  Google Scholar 

  26. Howarth, F. G. Environmental impacts of classical biological control. Annu. Rev. Entomol. 36, 485–509 (1991)

    Article  Google Scholar 

  27. Simberloff, D. in Selection Criteria and Ecological Consequences of Importing Natural Enemies (eds Kauffman, W. C. & Nechols, J. R.) 103–117 (Entomological Society of America, Lanham, Maryland, 1992)

    Google Scholar 

  28. Henneman, M. L. & Memmott, J. Infiltration of a Hawaiian community by introduced biological control agents. Science 293, 1314–1316 (2001)

    Article  ADS  CAS  Google Scholar 

  29. Memmott, J. & Godfray, H. C. J. in Parasitoid Community Ecology (eds Hawkins, B. A. & Sheehan, W.) 300–318 (Oxford Univ. Press, Oxford, 1994)

    Google Scholar 

Download references

Acknowledgements

We are particularly grateful to A. Lord. We thank Ch. Bol, Ce. Bol, I. Bol, N. Coc, L. Davies and E. Saquil for support and assistance in the field, and our taxonomic collaborators, including J. LaSalle, D. Quicke and C. Whitefoord. Research permission was granted by the Ministry of Natural Resources in Belize, and we are grateful to the Natural History Museum London for allowing us to work at Las Cuevas, and the Natural Environment Research Council for financial support. O.T.L. is a Royal Society University Research Fellow.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rebecca J. Morris.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Morris, R., Lewis, O. & Godfray, H. Experimental evidence for apparent competition in a tropical forest food web. Nature 428, 310–313 (2004). https://doi.org/10.1038/nature02394

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature02394

This article is cited by

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