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Pathogens and insect herbivores drive rainforest plant diversity and composition

Nature volume 506, pages 85–88 (2014)Cite this article

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Abstract

Tropical forests are important reservoirs of biodiversity1, but the processes that maintain this diversity remain poorly understood2. The Janzen–Connell hypothesis3,4 suggests that specialized natural enemies such as insect herbivores and fungal pathogens maintain high diversity by elevating mortality when plant species occur at high density (negative density dependence; NDD). NDD has been detected widely in tropical forests5,6,7,8,9, but the prediction that NDD caused by insects and pathogens has a community-wide role in maintaining tropical plant diversity remains untested. We show experimentally that changes in plant diversity and species composition are caused by fungal pathogens and insect herbivores. Effective plant species richness increased across the seed-to-seedling transition, corresponding to large changes in species composition5. Treating seeds and young seedlings with fungicides significantly reduced the diversity of the seedling assemblage, consistent with the Janzen–Connell hypothesis. Although suppressing insect herbivores using insecticides did not alter species diversity, it greatly increased seedling recruitment and caused a marked shift in seedling species composition. Overall, seedling recruitment was significantly reduced at high conspecific seed densities and this NDD was greatest for the species that were most abundant as seeds. Suppressing fungi reduced the negative effects of density on recruitment, confirming that the diversity-enhancing effect of fungi is mediated by NDD. Our study provides an overall test of the Janzen–Connell hypothesis and demonstrates the crucial role that insects and pathogens have both in structuring tropical plant communities and in maintaining their remarkable diversity.

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Figure 1: Suppression of insects and pathogens alters seedling community composition and diversity, respectively.
Figure 2: Recruitment across the seed-to-seedling transition showed NDD in the control, but spraying with the fungicide Amistar removed this NDD.
Figure 3: Negative density dependence is strongest in species that are most abundant as seeds.
Figure 4: Including NDD in model simulations reproduces the observed diversity patterns, whereas excluding NDD underestimates diversity in the control and insecticide treatments.

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Acknowledgements

Permission to undertake research in the Chiquibul Forest Reserve was granted by the Ministry of Natural Resources, Belize under Scientific Collection/Research Permit CD/60/3/07(20). We thank the staff at the Las Cuevas Research Station (the late N. Bol, C. Bol, M. Bol and J. Boucher) for their help; and R. Cocomb, E. Miles, C. Rasell, M. Senior, T. Swinfield and O. Theisinger provided field assistance. H. Rue provided advice on implementing measurement error models in INLA. This research was funded by the Natural Environment Research Council (NERC; standard grant NE/DO10721/1) and S.G. was funded by grant 126296 from the Academy of Finland.

Author information

Authors and Affiliations

  1. Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK,

    Robert Bagchi, Rachel E. Gallery, Sofia Gripenberg, Lakshmi Narayan, Claire E. Addis & Owen T. Lewis

  2. Ecosystem Management Group, Institute of Terrestrial Ecosystems, ETH Zürich, Universitätstrasse 16, 8092 Zürich, Switzerland ,

    Robert Bagchi

  3. School of Natural Resources and the Environment, University of Arizona, Tucson, 85721, Arizona, USA

    Rachel E. Gallery

  4. Department of Biology, Section of Biodiversity and Environmental Research, University of Turku, 20014 Turku, Finland,

    Sofia Gripenberg

  5. Department of BioSciences, Geoffrey Pope Building, University of Exeter, Exeter EX4 4QD, UK,

    Sarah J. Gurr

  6. Department of Plant Sciences, University of Oxford, South Parks Road, Oxford OX1 3RB, UK,

    Sarah J. Gurr

  7. Department of Animal and Plant Science, University of Sheffield, Western Bank, Sheffield S10 2TN, UK,

    Robert P. Freckleton

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  1. Robert Bagchi
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Contributions

O.T.L., R.P.F. and S.J.G. conceived the project and obtained funding. R.B., R.E.G., S.G., O.T.L., L.N. and C.E.A. established fieldwork design and protocols, and carried out the fieldwork with advice from R.P.F. and S.J.G. Data analysis was carried out by R.B. with input from R.P.F. and O.T.L. R.B. wrote the first draft of the manuscript and all authors contributed to discussing the results and editing the manuscript.

Corresponding author

Correspondence to Owen T. Lewis.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 The mean abundance-weighted Morisita–Horn dissimilarity in species composition (and 95% confidence intervals), comparing seedlings recruiting in the control plots with seedlings in the pesticide treatments and with seeds falling into seed traps.

Extended Data Figure 2 A comparison of the observed seedling communities (observed survival) with those simulated either fixing survival to the mean for each species in each treatment (mean density survival) or allowing survival to be negatively density dependent (NDD survival).

The simulated values are means and 95% confidence intervals based on 1,000 simulations for effective number of species, total abundance and community dissimilarity to seeds falling in adjacent traps.

Extended Data Table 1 Coefficients from the model relating the strength of NDD to treatment, log total seed abundance, and their interaction
Full size table
Extended Data Table 2 Coefficients from the negative binomial model fitted to the shadehouse and field trials of effects of the insecticide Engeo on seedling survival
Full size table
Extended Data Table 3 Tests of pesticide effects on seedling species diversity using different diversity indices
Full size table
Extended Data Table 4 Tests of pesticide effects on dissimilarity in species composition, comparing assemblages of seedlings germinating in plots to those of seeds falling in adjacent seed traps
Full size table

Supplementary information

Supplementary Table 1

This file shows the model coefficients (± standard deviation) for each species, which relate the numbers of seedlings to the number of seeds for each pesticide treatment. The parameters are described in equation 2 of the Methods. (PDF 202 kb)

Supplementary Data 1

This file includes the data, which is analysed in the main paper and associated with the R code supplied in Supplementary Notes 1. (XLS 580 kb)

Supplementary Notes 1

This document includes R code used to analyse the data supplied in Supplementary Data 1. (TXT 49 kb)

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Bagchi, R., Gallery, R., Gripenberg, S. et al. Pathogens and insect herbivores drive rainforest plant diversity and composition. Nature 506, 85–88 (2014). https://doi.org/10.1038/nature12911

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