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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Gibson, L. et al. Primary forests are irreplaceable for sustaining tropical biodiversity. Nature 478, 378–381 (2011)
Wright, S. J. Plant diversity in tropical forests: a review of mechanisms of species coexistence. Oecologia 130, 1–14 (2001)
Janzen, D. H. Herbivores and the number of tree species in tropical forests. Am. Nat. 104, 501–528 (1970)
Connell, J. H. in Dynamics of Numbers in Populations (eds den Boer, P. J. & Gradwell, G. R. ) 298–312 (PUDOC, 1971)
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)
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)
Bagchi, R. et al. Testing the Janzen-Connell mechanism: pathogens cause overcompensating density dependence in a tropical tree. Ecol. Lett. 13, 1262–1269 (2010)
Comita, L. S. & Hubbell, S. P. Local neighborhood and species' shade tolerance influence survival in a diverse seedling bank. Ecology 90, 328–334 (2009)
Terborgh, J. Enemies maintain hyperdiverse tropical forests. Am. Nat. 179, 303–314 (2012)
Chesson, P. Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst. 31, 343–366 (2000)
Curran, L. M. et al. Lowland forest loss in protected areas of Indonesian Borneo. Science 303, 1000–1003 (2004)
Achard, F. et al. Determination of deforestation rates of the world’s humid tropical forests. Science 297, 999–1002 (2002)
Bonan, G. B. Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320, 1444–1449 (2008)
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)
Mangan, S. A. et al. Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466, 752–755 (2010)
Bever, J. D. Feedback between plants and their soil communities in an old field community. Ecology 75, 1965–1977 (1994)
Packer, A. & Clay, K. Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404, 278–281 (2000)
Webb, C. O. & Peart, D. R. Seedling density dependence promotes coexistence of Bornean rain forest trees. Ecology 80, 2006–2017 (1999)
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)
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)
Terborgh, J. et al. Tree recruitment in an empty forest. Ecology 89, 1757–1768 (2008)
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)
Horn, H. S. Measurement of “overlap” in comparative ecological studies. Am. Nat. 100, 419–424 (1966)
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)
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)
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)
Paine, C. E. T. & Beck, H. Seed predation by neotropical rain forest mammals increases diversity in seedling recruitment. Ecology 88, 3076–3087 (2007)
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)
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)
Bridgewater, S. A Natural History of Belize (Univ. Texas Press, 2012)
Ford, K. A. et al. Neonicotinoid insecticides induce salicylate-associated plant defense responses. Proc. Natl Acad. Sci. USA 107, 17527–17532 (2010)
Jost, L. Entropy and diversity. Oikos 113, 363–375 (2006)
Oksanen, J. et al. vegan: community ecology package v.2.0-8 (R Foundation for Statistical Computing, 2013)
R Development Core Team. R: a language and environment for statistical computing v.3.0.1 (R Foundation for Statistical Computing, 2013)
Pinheiro, J. C. & Bates, D. M. Mixed-Effects Models in S and S-Plus (Springer, 2000)
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)
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)
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.
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.
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)
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)
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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