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 pathogens and spatial patterns of seedling mortality in a temperate tree

Nature volume 404, pages 278–281 (2000)Cite this article

Abstract

The Janzen–Connell hypothesis1,2 proposes that host-specific, distance- and/or density-dependent predators and herbivores maintain high tree diversity in tropical forests. Negative feedback between plant and soil communities could be a more effective mechanism promoting species coexistence because soil pathogens can increase rapidly in the presence of their host3, causing conditions unfavourable for local conspecific recruitment4,5,6. Here we show that a soil pathogen leads to patterns of seedling mortality in a temperate tree (Prunus serotina) as predicted by the Janzen–Connell hypothesis. In the field, the mean distance to parent of seedling cohorts shifted away from maternal trees over a period of 3 years. Seedlings were grown in soil collected 0–5 m or 25–30 m from Prunus trees. Sterilization of soil collected beneath trees improved seedling survival relative to unsterilized soil, whereas sterilization of distant soil did not affect survival. Pythium spp., isolated from roots of dying seedlings and used to inoculate healthy seedlings, decreased survival by 65% relative to controls. Our results provide the most complete evidence that native pathogens influence tree distributions, as predicted by the Janzen–Connell hypothesis, and suggest that similar ecological mechanisms operate in tropical and temperate forests.

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: Relationship between distance to parent, initial seedling germination (filled triangles), and probability of seedling survival over time (dashed lines: open circles, after 4 months; open diamonds, after 16 months; open squares, after 28 months).
Figure 2: Logistic regression models of the probability of black cherry survival in relation to distance to parent and neighbourhood density.
Figure 3: Effect of distance, neighbourhood density and soil sterilization on black cherry seedling survival.
Figure 4: Black cherry seedling survival in control and pathogen inoculation treatments (n = 40 per treatment).

Similar content being viewed by others

References

  1. Janzen, D. H. Herbivores and the number of tree species in tropical forests. Am. Nat. 104, 501–508 ( 1970).

    Article  Google Scholar 

  2. Connell, J. H. in Dynamics in Populations (eds den Boer, P. J. & Gradwell, G. R.) 298–312 (Center for Agricultural Publishing and Documentation, Wageningen, 1971).

    Google Scholar 

  3. Burdon, J. J. Diseases and Plant Population Biology (Cambridge Univ. Press, Cambridge, 1987).

    Google Scholar 

  4. Florence, R. G. Decline of old-growth forests in relation to some soil microbiological processes. Ecology 46, 52–64 (1965).

    Article  Google Scholar 

  5. 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 

  6. Mills, K. E. & Bever, J. D. Maintenance of diversity within plant communities: soil pathogens as agents of negative feedback. Ecology 79, 1595–1601 ( 1998).

    Article  Google Scholar 

  7. Hubbell, S. P. Seed predation and the coexistence of tree species in tropical forests. Oikos 35, 214–229 ( 1980).

    Article  Google Scholar 

  8. Augspurger, C. K. Offspring recruitment around tropical trees: changes in cohort distance with time. Oikos 40, 189–196 (1983).

    Article  Google Scholar 

  9. Augspurger, C. K. & Kelly, C. K. Pathogen mortality of tropical tree seedlings: experimental studies of the effects of dispersal distance, seedling density, and light conditions. Oecologia 61, 211–217 (1984).

    Article  ADS  Google Scholar 

  10. Clark, D. A. & Clark, D. B. Spacing dynamics of a tropical rain forest tree: evaluation of the Janzen–Connell model. Am. Nat. 124, 769–788 ( 1984).

    Article  Google Scholar 

  11. Connell, J. H., Tracey, J. G. & Webb, L. J. Compensatory recruitment, growth and mortality as factors maintaining rain forest tree diversity. Ecol. Monogr. 54, 141–164 (1984).

    Article  Google Scholar 

  12. Becker, P., Lee, L. W., Rothman, E. D. & Hamilton, W. D. Seed predation and the coexistence of tree species: Hubbell's models revisited. Oikos 44, 382–390 (1985).

    Article  Google Scholar 

  13. Condit, R., Hubbell, S. P. & Foster, R. B. Recruitment of conspecific adults and the maintenance of tree and shrub diversity in a neotropical forest. Am. Nat. 140, 261–286 (1992).

    Article  CAS  Google Scholar 

  14. Gilbert, G. S., Hubbell, S. P. & Foster, R. B. Density and distance to adult effects of a canker disease of trees in a moist tropical forest. Oecologia 98, 100–108 (1994).

    Article  ADS  CAS  Google Scholar 

  15. Notman, E., Gorchov, D. L. & Cornejo, F. Effect of distance, aggregation, and habitat on levels of seed predation for two mammal-dispersed neotropical rain forest tree species. Oecologia 106, 221–227 (1996).

    Article  ADS  Google Scholar 

  16. Wills, C., Condit, R., Foster, R. B. & Hubbell, S. P. Strong density- and diversity-related effects help to maintain species diversity in a neotropical forest. Proc. Natl Acad. Sci. 94, 1252–1257 (1997).

    Article  ADS  CAS  Google Scholar 

  17. Schupp, E. W. The Janzen–Connell model for tropical tree diversity: population implications and the importance of spatial scale. Am. Nat. 140, 526–530 (1992).

    Article  CAS  Google Scholar 

  18. Burkey, T. V. Tropical tree species diversity: A test of the Janzen–Connell model. Oecologia 97, 533–540 (1994).

    Article  ADS  CAS  Google Scholar 

  19. Cintra, R. A test of the Janzen–Connell model with two common tree species in Amazonian forest. J. Trop. Ecol. 13, 641– 658 (1997).

    Article  Google Scholar 

  20. Burdon, J. J. & Chilvers, G. A. Host density as a factor in plant disease ecology. Annu. Rev. Phytopathol. 20, 143–166 (1982).

    Article  Google Scholar 

  21. Fox, J. F. Alternation and coexistence of tree species. Am. Nat. 111, 69–89 (1977).

    Article  Google Scholar 

  22. Woods, K. D. Reciprocal replacement and the maintenance of codominance in a beech maple forest. Oikos 33, 31–39 (1979).

    Article  Google Scholar 

  23. 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 

  24. 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 

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

    Article  Google Scholar 

  26. Chen, W., Schneider, R. W. & Hoy, J. W. Taxonomic and phylgenetic analyses of ten Pythium species using isozyme polymorphisms. Phytopathology 82, 1234–1244 (1992).

    Article  CAS  Google Scholar 

  27. Carlisle, M. J. & Watkinson, S. C. The Fungi (Academic, Harcourt Brace & Co., New York, 1994 ).

    Google Scholar 

  28. Barone, J. A. Host-specificity of folivorous insects in a moist tropical forest. J. Animal Ecol. 67, 400–409 (1998).

    Article  Google Scholar 

  29. May, R. M. How many species are there on Earth? Science 241, 1441–1449 (1988).

    Article  ADS  CAS  Google Scholar 

Download references

Acknowledgements

We thank C. Augspurger, G. Gilbert, J. Holah, P. Kover, C. Lively and J. Price for critical review of the manuscript. We also thank R. Wagner for assistance with fungal isolation and identification, and J. Berg, M. Hallinan, M. Hardesty, T. Levitt, A. Overgaard, M. Selby, L. Somers and members of the Clay lab for field assistance. This work was supported by grants to A.P. from the Indiana Academy of Sciences and Indiana University.

Author information

Authors and Affiliations

  1. Department of Biology, Indiana University, Bloomington , 47405, Indiana, USA

    Alissa Packer & Keith Clay

Authors
  1. Alissa Packer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Keith Clay
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Packer, A., Clay, K. Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404, 278–281 (2000). https://doi.org/10.1038/35005072

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35005072

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