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

Journal name:
Nature
Volume:
466,
Pages:
752–755
Date published:
DOI:
doi:10.1038/nature09273
Received
Accepted
Published online

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.

At a glance

Figures

  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 1: Strengths of negative plant–soil feedback measured in the shade-house experiment are correlated with adult tree species abundance of the BCI forest.

    a, Variation in the strength of negative feedback mediated by soil biota among the six seedling species. Ba, Brosimum alicastrum; Bp, Beilschmiedia pendula; En, Eugenia nesiotica; Lp, Lacmellea panamensis; Tp, Tetragastris panamensis; Vs, Virola surinamensis. Bars indicate standard errors, and means that differ from zero are indicated by asterisks (*P<0.05; **P<0.01; ***P<0.001). Number of seedlings analysed = 349. b, Seedling response (averaged across seedling species) varied across live inocula (ANCOVA: F5,408 = 5.31, P<0.0001) but not across sterile inocula (ANCOVA: F5,408 = 0.15, P = 0.981). Bars indicate standard errors. c, Tree species that exhibited stronger negative feedback were less common as adults in the BCI 50-ha plot. DBH, diameter at breast height.

  2. Strengths of negative feedback measured in the field experiment are correlated with adult tree species abundance of the Gigante forest.
    Figure 2: Strengths of negative feedback measured in the field experiment are correlated with adult tree species abundance of the Gigante forest.

    a, Variation in the strength of negative feedback among the five seedling species. Species abbreviations are the same as those in Fig. 1, except for: Aa, Apeiba aspera; Sa, Simarouba amara. Bars indicate standard errors, and means that differ from zero are indicated by asterisks (*P<0.05; **P<0.01; ***P<0.001). Number of seedlings analysed = 945. b, Tree species that exhibited stronger negative feedback were less common as adults in the forest of the Gigante Peninsula than those species exhibiting weaker negative feedback. c, Proportional contribution of foliar insect herbivory, foliar pathogens and other causes to observed patterns of negative feedback.

  3. Simulations indicate that variation in feedback strength predicts tree species abundance.
    Figure 3: Simulations indicate that variation in feedback strength predicts tree species abundance.

    ac, Species abundance generated using simulations including shade-house plant response data (a), field-collected plant response data (b) and randomly generated feedback data (c). All simulations demonstrate that stronger negative feedback leads to lower species abundance. Each circle falling at the same location of the x axis in panels a and b indicates simulated abundance for each of 10 runs. Regression lines per run are plotted in panel c.

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Author information

Affiliations

  1. Department of Biological Sciences, University of Wisconsin–Milwaukee, Wisconsin 53201, USA

    • Scott A. Mangan &
    • Stefan A. Schnitzer
  2. Smithsonian Tropical Research Institute, MRC 0580-06, Unit 9100 Box 0948, DPO AA 34002-9998, USA

    • Scott A. Mangan,
    • Stefan A. Schnitzer,
    • Edward A. Herre &
    • Evelyn I. Sanchez
  3. Department of Biology, Indiana University, Bloomington, Indiana 47405, USA

    • Keenan M. L. Mack &
    • James D. Bever
  4. Department of Biological Sciences, University of Illinois–Chicago, Chicago, Illinois 60607, USA

    • Mariana C. Valencia

Contributions

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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The authors declare no competing financial interests.

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  1. Supplementary Information (0.26M)

    This file contains Supplementary Tables 1-3, Supplementary Figures 1-2 with legends, a Supplementary Discussion, and Supplementary Equations.

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