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:

Soil biota and exotic plant invasion

Abstract

Invasive plants are an economic problem and a threat to the conservation of natural systems. Escape from natural enemies might contribute to successful invasion1, with most work emphasizing the role of insect herbivores2,3,4; however, microbial pathogens are attracting increased attention5. Soil biota in some invaded ecosystems may promote ‘exotic’ invasion6,7,8,9, and plant–soil feedback processes are also important. Thus, relatively rare species native to North America consistently demonstrate negative feedbacks with soil microbes that promote biological diversity10, whereas abundant exotic and native species demonstrate positive feedbacks that reduce biological diversity10. Here we report that soil microbes from the home range of the invasive exotic plant Centaurea maculosa L. have stronger inhibitory effects on its growth than soil microbes from where the weed has invaded in North America. Centaurea and soil microbes participate in different plant–soil feedback processes at home compared with outside Centaurea's home range. In native European soils, Centaurea cultivates soil biota with increasingly negative effects on the weed's growth, possibly leading to its control. But in soils from North America, Centaurea cultivates soil biota with increasingly positive effects on itself, which may contribute to the success of this exotic species in North America.

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

Access options

Buy this article

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

Figure 1: Total biomass of C. maculosa plants grown in non-sterilized and sterilized soil collected from European (n = 4) and North American (n = 6) populations of C. maculosa.
Figure 2: Total biomass of C. maculosa plants grown alone in European soil (Central Massif population) and North American soil (Missoula population) that had been pre-cultured by either C. maculosa or a Festuca species native to the place of soil origin.

Similar content being viewed by others

References

  1. Crawley, M. J. Natural Enemies: the Population Biology of Predators, Parasites, and Diseases (Blackwell Science, Oxford, UK, 1992)

    Book  Google Scholar 

  2. Louda, S. M., Pemberton, R. W., Johnson, M. T. & Follet, P. A. Non-target effects: the Achilles heel of biological control? Annu. Rev. Entomol. 48, 365–396 (2003)

    Article  CAS  Google Scholar 

  3. Goeden, R. D. & Andres, L. A. Handbook of Biological Control (eds Bellows, T. S. & Fisher, T. W.) Ch. 34 (Academic, New York, 1999)

    Google Scholar 

  4. McEvoy, P. & Coombs, E. M. Biological control of plant invaders: regional patterns, field experiments, and structured population models. Ecol. Appl. 9, 387–401 (1999)

    Article  Google Scholar 

  5. Mitchell, C. G. & Power, A. G. Release of invasive plants from fungal and viral pathogens. Nature 421, 625–627 (2003)

    Article  ADS  CAS  Google Scholar 

  6. Richardson, D. M., Allsopp, N., D'Antonio, C. M., Milton, S. J. & Rejmánek, M. Plant invasions—the role of mutualisms. Biol. Rev. 75, 65–93 (2000)

    Article  CAS  Google Scholar 

  7. Simberloff, D. & Von Holle, B. Positive interactions of nonindigenous species: invasional meltdown? Biol. Invas. 1, 21–31 (1999)

    Article  Google Scholar 

  8. Marler, M. M., Zabinski, C. A. & Callaway, R. M. Mycorrhizae indirectly enhance competitive effects of an invasive forb on a native bunchgrass. Ecology 80, 1180–1186 (1999)

    Article  Google Scholar 

  9. Callaway, R. M., Newingham, B., Zabinski, C. A. & Mahall, B. E. Compensatory growth and competitive ability of an invasive weed are enhanced by soil fungi and native neighbors. Ecol. Lett. 4, 1–5 (2001)

    Article  Google Scholar 

  10. Klironomos, J. Feedback with soil b iota contributes to plant rarity and invasiveness in communities. Nature 417, 67–70 (2002)

    Article  ADS  CAS  Google Scholar 

  11. Packer, A. & Clay, K. Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 440, 278–281 (2000)

    Article  ADS  Google Scholar 

  12. Burdon, J. J. The structure of pathogen populations in natural plant communities. Annu. Rev. Phytopathol. 31, 305–348 (1993)

    Article  Google Scholar 

  13. Van der Putten, W. H., Vet, L. E. M., Harvey, J. A. & Wäckers, F. L. Linking above and belowground multitrophic interactions of plants, herbivores, pathogens and their antagonists. Trends Ecol. Evol. 16, 547–551 (2001)

    Article  Google Scholar 

  14. Holah, J. C. & Alexander, H. M. Soil pathogenic fungi have the potential to affect the coexistence of two tall-grass prairie species. J. Ecol. 87, 598–606 (1999)

    Article  Google Scholar 

  15. Brundrett, M. Mycorrhizas in natural ecosystems. Adv. Ecol. Res. 21, 171–313 (1991)

    Article  Google Scholar 

  16. Crowley, D. E., Yant, Y. C., Reid, C. P. P. & Szaniszlo, P. J. Mechanisms of iron acquisition from siderophores by microorganisms and plants. Plant Soil 130, 179–198 (1991)

    Article  CAS  Google Scholar 

  17. Newsham, K. K., Fitter, A. H. & Watkinson, A. R. Root pathogenic and arbuscular mycorrhizal fungi determine fecundity of asymptomatic plants in the field. J. Ecol. 82, 805–814 (1994)

    Article  Google Scholar 

  18. Bever, J. D., Westover, K. M. & Antonovics, J. Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J. Ecol. 85, 561–573 (1997)

    Article  Google Scholar 

  19. Bever, J. D. Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit. Proc. R. Soc. Lond. B 269, 2595–2601 (2002)

    Article  Google Scholar 

  20. Van der Putten, W. H., Van Dijk, C. & Peters, B. A. M. Plant-specific soil-borne diseases contribute to succession in foredune vegetation. Nature 362, 53–56 (1993)

    Article  ADS  Google Scholar 

  21. Bever, J. D. Feedback between plants and their soil communities in an old field community. Ecology 75, 1965–1977 (1994)

    Article  Google Scholar 

  22. Van der Putten, W. H. & Peters, B. A. M. How soil-borne pathogens may affect plant competition. Ecology 78, 1785–1795 (1997)

    Article  Google Scholar 

  23. Bais, H. P., Walker, T. S., Stermitz, F. R., Hufbauer, R. S. & Vivanco, J. M. Enantiomeric-dependent phytotoxic and antimicrobial activity of (± )-catechin. A rhizosecreted racemic mixture from spotted knapweed. Plant Physiol. 128, 1173–1177 (2002)

    Article  CAS  Google Scholar 

  24. Angspurger, C. K. Pests, Pathogens, and Plant Communities (eds Burdon, J. J. & Leather, S. R.) Ch. 3 (Blackwell Scientific, Oxford, 1990)

    Google Scholar 

  25. Streitwolf-Engel, R., Boller, R., Weimken, A. & Sanders, I. R. Clonal growth traits of two Prunellax species are determined by co-occurring arbuscular mycorrhizal fungi from a calcareous grassland. J. Ecol. 85, 181–191 (1997)

    Article  Google Scholar 

  26. Young, N. R. & Mytton, L. R. The response of white clover to different strains of Rhizobium trifolii in hill land reseeding. Grass Forage Sci. 38, 13–39 (1983)

    Article  Google Scholar 

  27. Eom, A. & Hartnett, D. C. Host plant species effects on arbuscular mycorrhizal fungal communities in tallgrass prairie. Oecologia 122, 435–444 (2000)

    Article  ADS  Google Scholar 

  28. 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 

Download references

Acknowledgements

We thank E. Corcket and R. Michalet for assistance with locating and identifying C. maculosa populations in Europe, and K. Feris for assistance with denaturing gradient gel electrophoresis data analysis. Our research on soil microbes and plant invasion is supported by NSF, USDA, the Andrew W. Mellon Foundation and The University of Montana.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ragan M. Callaway.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Information

Supplementary figures and methods for DGGE analysis. (PDF 65 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Callaway, R., Thelen, G., Rodriguez, A. et al. Soil biota and exotic plant invasion. Nature 427, 731–733 (2004). https://doi.org/10.1038/nature02322

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature02322

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