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:

Release of invasive plants from fungal and viral pathogens

Nature volume 421, pages 625–627 (2003)Cite this article

Abstract

Invasive plant species both threaten native biodiversity and are economically costly1,2,3,4,5, but only a few naturalized species become pests2,4. Here we report broad, quantitative support for two long-standing hypotheses that explain why only some naturalized species have large impacts. The enemy release hypothesis argues that invaders' impacts result from reduced natural enemy attack2,4,6,7,8,9,10. The biotic resistance hypothesis argues that interactions with native species, including natural enemies, limit invaders' impacts6,7,8. We tested these hypotheses for viruses and for rust, smut and powdery mildew fungi that infect 473 plant species naturalized to the United States from Europe. On average, 84% fewer fungi and 24% fewer virus species infect each plant species in its naturalized range than in its native range. In addition, invasive plant species that are more completely released from pathogens are more widely reported as harmful invaders of both agricultural and natural ecosystems. Together, these results strongly support the enemy release hypothesis. Among noxious agricultural weeds, species accumulating more pathogens in their naturalized range are less widely noxious, supporting the biotic resistance hypothesis. Our results indicate that invasive plants' impacts may be a function of both release from and accumulation of natural enemies, including pathogens.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: Net release of introduced plant species from fungal and viral pathogens.
Figure 2
Figure 3: More complete release from pathogens increases the degree of noxiousness and invasiveness in the naturalized range.
Figure 4: Decomposition of the effect of net release on noxiousness into the effects of escape from pathogens and accumulation of pathogens native to each plant's naturalized range.

Similar content being viewed by others

References

  1. US Congress Office of Technology Assessment Harmful Non-Indigenous Species in the United States Report No. OTA-F-565 (US Government Printing Office, Washington DC, 1993)

    Google Scholar 

  2. Williamson, M. Biological Invasions (Chapman & Hall, London, 1996)

    Google Scholar 

  3. Wilcove, D. S., Rothstein, D., Dubow, J., Phillips, A. & Losos, E. Quantifying threats to imperiled species in the United States. BioScience 48, 607–615 (1998)

    Article  Google Scholar 

  4. Mack, R. N. et al. Biotic invasions: causes, epidemiology, global consequences, and control. Ecol. Appl. 10, 689–710 (2000)

    Article  Google Scholar 

  5. Pimentel, D. (ed) Biological Invasions: Economic and Environmental Costs of Alien Plant, Animal, and Microbe Species (CRC, Boca Raton, Florida, 2002)

  6. Darwin, C. On the Origin of Species by Means of Natural Selection (John Murray, London, 1859)

    Google Scholar 

  7. Elton, C. S. The Ecology of Invasions by Animals and Plants (Methuen, London, 1958)

    Book  Google Scholar 

  8. Maron, J. L. & Vila, M. When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95, 361–373 (2001)

    Article  Google Scholar 

  9. Keane, R. M. & Crawley, M. J. Exotic plant invasions and the enemy release hypothesis. Trends Ecol. Evol. 17, 164–170 (2002)

    Article  Google Scholar 

  10. Van der Putten, W. H. How to be invasive. Nature 417, 32–33 (2002)

    Article  ADS  CAS  Google Scholar 

  11. Clay, K. Correlates of pathogen species richness in the grass family. Can. J. Bot. 73, S42–S49 (1995)

    Article  Google Scholar 

  12. Hokkanen, H. Exploiter–victim relationships of major plant diseases: implications for biological weed control. Agric. Ecosys. Environ. 14, 63–76 (1985)

    Article  Google Scholar 

  13. Anderson, R. M. & May, R. M. Population biology of infectious diseases: Part I. Nature 280, 361–367 (1979)

    Article  ADS  CAS  Google Scholar 

  14. Packer, A. & Clay, K. Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404, 278–281 (2000)

    Article  ADS  CAS  Google Scholar 

  15. Klironomos, J. N. Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417, 67–70 (2002)

    Article  ADS  CAS  Google Scholar 

  16. Agrios, G. N. Plant Pathology (Academic, San Diego, 1997)

    Google Scholar 

  17. Parker, I. M. et al. Impact: toward a framework for understanding the ecological effects of invaders. Biol. Invasions 1, 3–19 (1999)

    Article  Google Scholar 

  18. Julien, M. H. & Griffiths, M. W. (eds) Biological Control of Weeds: A World Catalogue of Agents and their Target Weeds (CABI, New York, 1998)

  19. Charudattan, R. Biological control of weeds by means of plant pathogens: Significance for integrated weed management in modern agro-ecology. BioControl 46, 229–260 (2001)

    Article  Google Scholar 

  20. Liebman, M. in Ecological Management of Agricultural Weeds (eds Liebman, M., Mohler, C. L. & Staver, C. P.) 375–408 (Cambridge Univ. Press, Cambridge, 2001)

    Google Scholar 

  21. Naylor, R. L. & Ehrlich, P. R. in Nature's Services: Societal Dependence on Natural Ecosystems (ed. Daily, G. C.) 151–174 (Island, Washington DC, 1997)

    Google Scholar 

  22. Torchin, M. E., Lafferty, K. D., Dobson, A. P., McKenzie, V. J. & Kuris, A. M. Introduced species and their missing parasites. Nature (in the press)

  23. Tutin, T. G. et al. (eds) Flora Europaea (Cambridge Univ. Press, Cambridge, 1964–1980)

  24. Mabberly, D. J. The Plant-Book: A Portable Dictionary of the Vascular Plants (Cambridge Univ. Press, Cambridge, 1997)

    Google Scholar 

  25. Vánky, K. European Smut Fungi (G. Fischer, Suttgart, 1994)

    Google Scholar 

  26. Farr, D. F., Bills, G. F., Chamuris, G. P. & Rossman, A. Y. Fungi on Plants and Plant Products in the United States (APS, St Paul, Minnesota, 1989)

    Google Scholar 

  27. Braun, U. The Powdery Mildews (Erysiphales) of Europe (G. Fischer, Jena, Germany, 1995)

    Google Scholar 

  28. Gaumann, E. A. Die Rostpilze Mitteleuropas mit besonderer Berücksichtigung der Schweiz (Buchdruckerei Büchler, Bern, 1959)

    Google Scholar 

  29. Wilson, M. & Henderson, D. M. British Rust Fungi (Cambridge Univ. Press, Cambridge, 1966)

    Google Scholar 

  30. Holm, L. G., Plucknett, D. L., Pancho, J. V. & Herberger, J. P. The World's Worst Weeds: Distribution and Biology (Univ. Hawaii, Honolulu, 1977)

    Google Scholar 

Download references

Acknowledgements

We thank B. Blossey, A. Dobson, A. Kuris, K. Lafferty, J. Maron, A. Rossman and M. Torchin for discussions; J. Gardell and B. Youn for assistance; and L. Aldrich-Wolfe, R. Allen, K. Blaisdell, G. Hall, K. Howe, G. Knight and S. Travers for manuscript reviews. This work resulted from the Disease and Conservation working group at the National Center for Ecological Analysis and Synthesis, which is supported by the US National Science Foundation (NSF), the State of California and the University of California Santa Barbara. Cornell University, the USDA and a postdoctoral research fellowship in microbial biology from the NSF also supported this work.

Author information

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York, 14853, USA

    Charles E. Mitchell & Alison G. Power

Authors
  1. Charles E. Mitchell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alison G. Power
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Charles E. Mitchell.

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

Mitchell, C., Power, A. Release of invasive plants from fungal and viral pathogens. Nature 421, 625–627 (2003). https://doi.org/10.1038/nature01317

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01317

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

Advanced 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