Skip to main content

Thank you for visiting 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:

Pathogens and insect herbivores drive rainforest plant diversity and composition


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.

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: 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.

Similar content being viewed by others


  1. Gibson, L. et al. Primary forests are irreplaceable for sustaining tropical biodiversity. Nature 478, 378–381 (2011)

    Article  CAS  ADS  Google Scholar 

  2. Wright, S. J. Plant diversity in tropical forests: a review of mechanisms of species coexistence. Oecologia 130, 1–14 (2001)

    Article  ADS  Google Scholar 

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

    Article  Google Scholar 

  4. Connell, J. H. in Dynamics of Numbers in Populations (eds den Boer, P. J. & Gradwell, G. R. ) 298–312 (PUDOC, 1971)

    Google Scholar 

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

    Article  CAS  ADS  Google Scholar 

  6. Metz, M. R., Sousa, W. & Valencia, R. Widespread density-dependent seedling mortality promotes species coexistence in a highly diverse Amazonian rain forest. Ecology 91, 3675–3685 (2010)

    Article  Google Scholar 

  7. Bagchi, R. et al. Testing the Janzen-Connell mechanism: pathogens cause overcompensating density dependence in a tropical tree. Ecol. Lett. 13, 1262–1269 (2010)

    Article  Google Scholar 

  8. 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 

  9. Terborgh, J. Enemies maintain hyperdiverse tropical forests. Am. Nat. 179, 303–314 (2012)

    Article  Google Scholar 

  10. Chesson, P. Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst. 31, 343–366 (2000)

    Google Scholar 

  11. Curran, L. M. et al. Lowland forest loss in protected areas of Indonesian Borneo. Science 303, 1000–1003 (2004)

    Article  CAS  ADS  Google Scholar 

  12. Achard, F. et al. Determination of deforestation rates of the world’s humid tropical forests. Science 297, 999–1002 (2002)

    Article  CAS  ADS  Google Scholar 

  13. Bonan, G. B. Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320, 1444–1449 (2008)

    Article  CAS  ADS  Google Scholar 

  14. 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 

  15. Mangan, S. A. et al. Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466, 752–755 (2010)

    Article  CAS  ADS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  ADS  Google Scholar 

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

    Article  Google Scholar 

  19. Theimer, T. C., Gehring, C. A., Green, P. T. & Connell, J. H. Terrestrial vertebrates alter seedling composition and richness but not diversity in an Australian tropical rain forest. Ecology 92, 1637–1647 (2011)

    Article  Google Scholar 

  20. Leigh, E. G., Wright, S. J., Herre, E. A. & Putz, F. E. The decline of tree diversity on newly isolated tropical islands: a test of a null hypothesis and some implications. Evol. Ecol. 7, 76–102 (1993)

    Article  Google Scholar 

  21. Terborgh, J. et al. Tree recruitment in an empty forest. Ecology 89, 1757–1768 (2008)

    Article  Google Scholar 

  22. Hammond, D. S. & Brown, V. K. in Dynamics of Tropical Communities (eds G. R. Newbery, D. M., Prins, H. H. T. & Brown, N. D. ) 51–78 (Blackwell, 1998)

    Google Scholar 

  23. Horn, H. S. Measurement of “overlap” in comparative ecological studies. Am. Nat. 100, 419–424 (1966)

    Article  Google Scholar 

  24. Comita, L. S., Muller-Landau, H. C., Aguilar, S. & Hubbell, S. P. Asymmetric density dependence shapes species abundances in a tropical tree community. Science 329, 330–332 (2010)

    Article  CAS  ADS  Google Scholar 

  25. Kobe, R. K. & Vriesendorp, C. F. Conspecific density dependence in seedlings varies with species shade tolerance in a wet tropical forest. Ecol. Lett. 14, 503–510 (2011)

    Article  Google Scholar 

  26. Bagchi, R. et al. Impacts of logging on density-dependent predation of dipterocarp seeds in a southeast Asian rainforest. Phil. Trans. R. Soc. B 366, 3246–3255 (2011)

    Article  Google Scholar 

  27. Paine, C. E. T. & Beck, H. Seed predation by neotropical rain forest mammals increases diversity in seedling recruitment. Ecology 88, 3076–3087 (2007)

    Article  Google Scholar 

  28. Norghauer, J. M., Malcolm, J., Zimmerman, B. & Felfili, J. An experimental test of density- and distant-dependent recruitment of mahogany (Swietenia macrophylla) in southeastern Amazonia. Oecologia 148, 437–446 (2006)

    Article  ADS  Google Scholar 

  29. Bridgewater, S. G. M. et al. A preliminary checklist of the vascular plants of the Chiquibul Forest, Belize. Edinb. J. Bot. 63, 269–321 (2006)

    Article  Google Scholar 

  30. Bridgewater, S. A Natural History of Belize (Univ. Texas Press, 2012)

    Google Scholar 

  31. Ford, K. A. et al. Neonicotinoid insecticides induce salicylate-associated plant defense responses. Proc. Natl Acad. Sci. USA 107, 17527–17532 (2010)

    Article  CAS  ADS  Google Scholar 

  32. Jost, L. Entropy and diversity. Oikos 113, 363–375 (2006)

    Article  Google Scholar 

  33. Oksanen, J. et al. vegan: community ecology package v.2.0-8 (R Foundation for Statistical Computing, 2013)

  34. R Development Core Team. R: a language and environment for statistical computing v.3.0.1 (R Foundation for Statistical Computing, 2013)

  35. Pinheiro, J. C. & Bates, D. M. Mixed-Effects Models in S and S-Plus (Springer, 2000)

    Book  Google Scholar 

  36. Carroll, R. J., Ruppert, D., Stefanski, L. A. & Crainiceanu, C. M. Measurement Error in Nonlinear Models: A Modern Perspective 2nd edn (Chapman & Hall/CRC, 2006)

    Book  Google Scholar 

  37. Rue, H., Martino, S. & Chopin, N. Approximate Bayesian inference for latent Gaussian models by using integrated nested Laplace approximations. J. R. Stat. Soc. Ser. B 71, 319–392 (2009)

    Article  MathSciNet  Google Scholar 

Download references


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



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.

Ethics declarations

Competing interests

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
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
Extended Data Table 3 Tests of pesticide effects on seedling species diversity using different diversity indices
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

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)

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bagchi, R., Gallery, R., Gripenberg, S. et al. Pathogens and insect herbivores drive rainforest plant diversity and composition. Nature 506, 85–88 (2014).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:

This article is cited by


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.


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