Negative plant–soil feedback predicts tree-species relative abundance in a tropical forest

Abstract

The accumulation of species-specific enemies around adults is hypothesized to maintain plant diversity by limiting the recruitment of conspecific seedlings relative to heterospecific seedlings1,2,3,4,5,6. Although previous studies in forested ecosystems have documented patterns consistent with the process of negative feedback7,8,9,10,11,12,13,14,15,16, these studies are unable to address which classes of enemies (for example, pathogens, invertebrates, mammals) exhibit species-specific effects strong enough to generate negative feedback17, and whether negative feedback at the level of the individual tree is sufficient to influence community-wide forest composition. Here we use fully reciprocal shade-house and field experiments to test whether the performance of conspecific tree seedlings (relative to heterospecific seedlings) is reduced when grown in the presence of enemies associated with adult trees. Both experiments provide strong evidence for negative plant–soil feedback mediated by soil biota. In contrast, above-ground enemies (mammals, foliar herbivores and foliar pathogens) contributed little to negative feedback observed in the field. In both experiments, we found that tree species that showed stronger negative feedback were less common as adults in the forest community, indicating that susceptibility to soil biota may determine species relative abundance in these tropical forests. Finally, our simulation models confirm that the strength of local negative feedback that we measured is sufficient to produce the observed community-wide patterns in tree-species relative abundance. Our findings indicate that plant–soil feedback is an important mechanism that can maintain species diversity and explain patterns of tree-species relative abundance in tropical forests.

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Figure 1: Strengths of negative plant–soil feedback measured in the shade-house experiment are correlated with adult tree species abundance of the BCI forest.
Figure 2: Strengths of negative feedback measured in the field experiment are correlated with adult tree species abundance of the Gigante forest.
Figure 3: Simulations indicate that variation in feedback strength predicts tree species abundance.

References

  1. 1

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

    Article  Google Scholar 

  2. 2

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

    Google Scholar 

  3. 3

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

    Article  Google Scholar 

  4. 4

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

    ADS  CAS  Article  Google Scholar 

  5. 5

    Kulmatiski, A., Beard, K. H., Stevens, J. R. & Cobbold, S. M. Plant-soil feedback: a meta-analytical review. Ecol. Lett. 11, 980–992 (2008)

    Article  Google Scholar 

  6. 6

    Carson, W. P., Anderson, J. T., Leigh, E. G. & Schnitzer, S. A. in Tropical Forest Community Ecology (eds Carson, W. P. & Schnitzer, S. A.) 210–241 (Wiley-Blackwell, 2008)

    Google Scholar 

  7. 7

    Webb, C. O. & Peart, D. R. Seedling density dependence promotes coexistence of Bornean rain forest trees. Ecology 80, 2006–2017 (1999)

    Article  Google Scholar 

  8. 8

    Harms, K. E., Wright, S. J., Calderón, O., Hernández, A. & Herre, A. E. Pervasive density-dependent recruitment enhances seedling diversity in a tropical forest. Nature 404, 493–495 (2000)

    ADS  CAS  Article  Google Scholar 

  9. 9

    Lambers, H. R. L., Clark, J. S. & Beckage, B. Density-dependent mortality and the latitude gradient in species diversity. Nature 417, 732–735 (2002)

    ADS  Article  Google Scholar 

  10. 10

    Peters, H. A. Neighbour-regulated mortality: the influence of positive and negative density dependence on tree populations in species-rich tropical forests. Ecol. Lett. 6, 757–765 (2003)

    Article  Google Scholar 

  11. 11

    Wills, C. et al. Nonrandom processes maintain diversity in tropical forests. Science 311, 527–531 (2006)

    ADS  CAS  Article  Google Scholar 

  12. 12

    Comita, L. S. & Hubbell, S. P. Local neighborhood and species’ shade tolerance influence survival in a diverse seedling bank. Ecology 90, 328–334 (2009)

    Article  Google Scholar 

  13. 13

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

    ADS  CAS  Article  Google Scholar 

  14. 14

    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)

    ADS  Article  Google Scholar 

  15. 15

    Hood, L. A., Swaine, M. D. & Mason, P. A. The influence of spatial patterns of damping-off disease and arbuscular mycorrhizal colonization on tree seedling establishment in Ghanaian tropical forest soil. J. Ecol. 92, 816–823 (2004)

    Article  Google Scholar 

  16. 16

    Bell, T., Freckleton, R. P. & Lewis, O. T. Plant pathogens drive density-dependent seedling mortality in a tropical tree. Ecol. Lett. 9, 569–574 (2006)

    Article  Google Scholar 

  17. 17

    Bever, J. D., Kristi, M. W. & 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 

  18. 18

    Bever, J. D. Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol. 157, 465–473 (2003)

    Article  Google Scholar 

  19. 19

    Adler, R. A. & Muller-Landau, H. C. When do localized natural enemies increase species richness? Ecol. Lett. 8, 438–447 (2005)

    Article  Google Scholar 

  20. 20

    Petermann, J. S., Fergus, A. J. F., Turnbull, L. A. & Schmid, B. Janzen-Connell effects are widespread and strong enough to maintain diversity in grasslands. Ecology 89, 2399–2406 (2008)

    Article  Google Scholar 

  21. 21

    McCarthy-Neumann, S. & Kobe, R. K. Conspecific plant-soil feedbacks reduce survivorship and growth of tropical tree seedlings. J. Ecol. 98, 396–407 (2010)

    Article  Google Scholar 

  22. 22

    Hubbell, S. P., Ahumada, J. A., Condit, R. & Foster, R. B. Local neighborhood effects on long-term survival of individual trees in a neotropical forest. Ecol. Res. 16, 859–875 (2001)

    Article  Google Scholar 

  23. 23

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

    Article  Google Scholar 

  24. 24

    Kardol, P., Cornips, N. J., van Kempen, M. M. L., Bakx-Shotman, J. M. T. & van der Putten, W. H. Microbe-mediated plant-soil feedback causes historical contingency effects in plant community assembly. Ecol. Monogr. 77, 147–162 (2007)

    Article  Google Scholar 

  25. 25

    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 

  26. 26

    De Deyn, G. B. et al. Soil invertebrate fauna enhances grassland succession and diversity. Nature 442, 711–713 (2003)

    ADS  Article  Google Scholar 

  27. 27

    Comita, L. S., Muller-Landau, H. C., Aguilar, S. & Hubbell, S. P. Asymmetric density dependence shapes species abundances in a tropical tree community. Science 10.1126/science.1190772 (in the press)

  28. 28

    Hubbell, S. P. The Unified Neutral Theory of Biodiversity and Biogeography (Princeton Univ. Press, 2001)

    Google Scholar 

  29. 29

    Roesch, L. F. W. et al. Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J. 1, 283–290 (2007)

    CAS  Article  Google Scholar 

  30. 30

    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 

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Acknowledgements

We thank G. Adler, M. Kaspari, E. Leigh, T. Lambert, I. Rubinoff, E. Tanner, M. Tobin, B. Turner, S. Van Bael and N. Wurzburger for providing discussions and comments on the manuscript. R. Kolodziej, K. Meyer, K. McElligott and T. Shirshac provided greenhouse and field assistance. Logistical support was provided by the Smithsonian Tropical Research Institute. The Center of Tropical Forest Science provided BCI tree abundance data published online at https://ctfs.arnarb.harvard.edu/webatlas/datasets/bci/abundance. This study was supported by a Smithsonian Tropical Research Institute (STRI) postdoctoral fellowship to S.A.M., a University of Wisconsin–Milwaukee (UWM) Research Growth Initiative grant to S.A.S., a fellowship from the UWM Research Foundation, and a grant from the National Science Foundation to J.D.B. We thank I. Rubinoff for his support of the STRI Soil Initiative.

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S.A.M. designed and conducted the experiments, analysed the data and wrote the first draft. S.A.S., E.A.H. and J.D.B. provided important revisions. J.D.B. and K.M.L.M. developed the simulation. M.C.V. and E.I.S. provided essential field support.

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Correspondence to Scott A. Mangan.

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The authors declare no competing financial interests.

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This file contains Supplementary Tables 1-3, Supplementary Figures 1-2 with legends, a Supplementary Discussion, and Supplementary Equations. (PDF 256 kb)

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Mangan, S., Schnitzer, S., Herre, E. et al. Negative plant–soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466, 752–755 (2010). https://doi.org/10.1038/nature09273

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