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Symbiotic fungal endophytes control insect host–parasite interaction webs

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Abstract

Symbiotic microorganisms that live intimately associated with terrestrial plants affect both the quantity and quality of resources1,2, and thus the energy supply to consumer populations at higher levels in the food chain. Empirical evidence on resource limitation of food webs points to primary productivity as a major determinant of consumer abundance and trophic structure3,4,5,6. Prey quality plays a critical role in community regulation7,8. Plants infected by endophytic fungi are known to be chemically protected against herbivore consumption9,10,11. However, the influence of this microbe–plant association on multi-trophic interactions remains largely unexplored. Here we present the effects of fungal endophytes on insect food webs that reflect limited energy transfer to consumers as a result of low plant quality, rather than low productivity. Herbivore–parasite webs on endophyte-free grasses show enhanced insect abundance at alternate trophic levels, higher rates of parasitism, and increased dominance by a few trophic links. These results mirror predicted effects of increased productivity on food-web dynamics12. Thus ‘hidden’ microbial symbionts can have community-wide impacts on the pattern and strength of resource–consumer interactions.

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Figure 1: Response of insects to the grass-endophyte association.
Figure 2: Aphid–parasite interaction webs established on Lolium multiflorum monocultures.

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References

  1. Gehring, C. A. & Whitham, T. G. Interactions between aboveground herbivores and mycorrhyzal mutualists of plants. Trends Ecol. Evol. 9, 251–255 (1994).

    Article  CAS  Google Scholar 

  2. van der Heijden, M. G. A. et al. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396, 69–72 (1998).

    Article  ADS  CAS  Google Scholar 

  3. Wootton, J. T. & Power, M. E. Productivity, consumers, and the structure of a river food chain. Proc. Natl Acad. Sci. USA 90, 1384–1387 (1993).

    Article  ADS  CAS  Google Scholar 

  4. Kaunzinger, C. M. K. & Morin, P. J. Productivity controls food-chain properties in microbial communities. Nature 395, 495–497 (1998).

    Article  ADS  CAS  Google Scholar 

  5. Mikola, J. & Setälä, H. Productivity and trophic-level biomasses in a microbial-based solid food web. Oikos 82, 158–168 (1998).

    Article  Google Scholar 

  6. Hulot, F. D., Lacroix, G., Lescher-Moutoué, F. & Loreau, M. Functional diversity governs ecosystem response to nutrient enrichment. Nature 405, 340–344 (2000).

    Article  ADS  CAS  Google Scholar 

  7. Leibold, M. A., Chase, J. M., Schurin, J. B. & Downing, A. L. Species turnover and the regulation of trophic structure. Annu. Rev. Ecol. Syst. 28, 467–494 (1997).

    Article  Google Scholar 

  8. Abrams, P. A. Effects of increased productivity on the abundance of trophic levels. Am. Nat. 141, 351–371 (1993).

    Article  Google Scholar 

  9. Clay, K. Fungal endophytes of grasses. Annu. Rev. Ecol. Syst. 21, 275–297 (1990).

    Article  Google Scholar 

  10. Dahlman, D. L., Eichenseer, H. & Siegel, M. R. in Microbial Mediation of Plant-Herbivore Interactions (eds Barbosa, P., Krischik, V. A. & Jones, C. G.) 227–252 (John Wiley, New York, 1991).

    Google Scholar 

  11. Breen, J. P. Acremonium endophyte interactions with enhanced plant resistance to insects. Annu. Rev. Entomol. 39, 401–423 (1994).

    Article  Google Scholar 

  12. Oksanen, L., Fretwell, S. D., Arruda, J. & Niemelä, P. Exploitation ecosystems in gradients of primary productivity. Am. Nat. 118, 240–261 (1981).

    Article  Google Scholar 

  13. Hairston, N. G., Smith, F. E. & Slobotkin, L. B. Community structure, population control, and competition. Am. Nat. 94, 421–425 (1960).

    Article  Google Scholar 

  14. Price, P. W. et al. Interaction among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu. Rev. Ecol. Syst. 11, 41–65 (1980).

    Article  Google Scholar 

  15. Hunter, M. D. & Price, P. W. Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73, 724–732 (1992).

    Google Scholar 

  16. Osenberg, C. W. & Mittelbach, G. G. in Food Webs: Integration of Patterns and Dynamics (eds Polis, G. & Winemiller, K. O.) 134–148 (Chapman & Hall, New York, 1996).

    Book  Google Scholar 

  17. DeAngelis, D. L. Dynamics of Nutrient Cycling and Food Webs (Chapman & Hall, London, 1992).

    Book  Google Scholar 

  18. Müller, C. B., Adriaanse, I. C. T., Belshaw, R. & Godfray, H. C. J. The structure of an aphid-parasitoid community. J. Anim. Ecol. 68, 346–370 (1999).

    Article  Google Scholar 

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

    Article  MathSciNet  CAS  Google Scholar 

  20. 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 

  21. Chaneton, E. J. & Bonsall, M. B. Enemy-mediated apparent competition: empirical patterns and the evidence. Oikos 88, 380–394 (2000).

    Article  Google Scholar 

  22. McCann, K., Hastings, A. & Huxel, G. Weak trophic interactions and the balance of nature. Nature 395, 794–798 (1998).

    Article  ADS  CAS  Google Scholar 

  23. Barker, G. M. & Addison, P. J. Influence of Clavicipitaceous endophyte infection in ryegrass on development of the parasitoid Microctonus hyperodae Loan (Hymenoptera: Braconidae) in Listronotus bonariensis (Kuschel) (Coleoptera: Curculionidae). Biol. Contr. 7, 281–287 (1996).

    Article  Google Scholar 

  24. Bultman, T. L., Borowicz, K. L., Schneble, R. M., Coudron, T. A. & Bush, L. P. Effect of a fungal endophyte on the growth and survival of two Euplectrus parasitoids. Oikos 78, 170–176 (1997).

    Article  Google Scholar 

  25. Dobson, A. P. & Crawley, M. J. Pathogens and the structure of plant communities. Trends Ecol. Evol. 9, 393–398 (1994).

    Article  CAS  Google Scholar 

  26. Grime, J. P., MacKey, J. M. L., Hillier, S. H. & Read, D. J. Floristic diversity in a model system using experimental microcosms. Nature 328, 420–422 (1987).

    Article  ADS  Google Scholar 

  27. Clay, K. & Holah, J. Fungal endophyte symbiosis and plant diversity in successional fields. Science 285, 1742–1744 (1999).

    Article  CAS  Google Scholar 

  28. Latch, G. C. M., Christensen, M. J. & Hickson, R. E. Endophytes of annual and hybrid ryegrasses. New Zeal. J. Agr. Res. 31, 57–63 (1988).

    Article  Google Scholar 

  29. Alatalo, R. V. Problems in the measurement of evenness in ecology. Oikos 37, 199–204 (1981).

    Article  Google Scholar 

  30. Magurran, A. E. Ecological Diversity and its Measurement (Princeton Univ. Press, New Jersey, 1988).

    Book  Google Scholar 

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Acknowledgements

We thank A. Austin, M. Bonsall, A. Bourke, C. Godfray, D. Golombek, T. H. Jones, N. Mazía, R. Pettifor, S. Power, P. Roset, S. Semple and M. Vila-Aiub for comments on the manuscript; E. Demartin, P. Gundel and M. Rabadan for field assistance; R. Belshaw and F. van Veen for helping with parasitoid identification; and C. Godfray for constructing the web diagrams. This study was funded by grants from the Agencia Nacional de Promoción Cientifica y Tecnológica of Argentina and Fundación Antorchas.

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Authors and Affiliations

  1. IFEVA-Departamento de Recursos Naturales y Ambiente, Facultad de Agronomia, Universidad de Buenos Aires, Av. San Martin 4453, Buenos Aires, 1417, Argentina

    Marina Omacini, Enrique J. Chaneton & Claudio M. Ghersa

  2. Department of Biology and NERC Centre for Population Biology, Imperial College at Silwood Park, Ascot, SL5 7PY, Berkshire, UK

    Christine B. Müller

  3. The Zoological Society of London, Institute of Zoology, Regent's Park, London, NW1 4RY, UK

    Christine B. Müller

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  1. Marina Omacini
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  2. Enrique J. Chaneton
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  3. Claudio M. Ghersa
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  4. Christine B. Müller
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Correspondence to Marina Omacini or Christine B. Müller.

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Omacini, M., Chaneton, E., Ghersa, C. et al. Symbiotic fungal endophytes control insect host–parasite interaction webs. Nature 409, 78–81 (2001). https://doi.org/10.1038/35051070

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