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.

Negative density dependence mediates biodiversity–productivity relationships across scales


Regional species diversity generally increases with primary productivity whereas local diversity–productivity relationships are highly variable. This scale-dependence of the biodiversity–productivity relationship highlights the importance of understanding the mechanisms that govern variation in species composition among local communities, which is known as β-diversity. Hypotheses to explain changes in β-diversity with productivity invoke multiple mechanisms operating at local and regional scales, but the relative importance of these mechanisms is unknown. Here we show that changes in the strength of local density-dependent interactions within and among tree species explain changes in β-diversity across a subcontinental-productivity gradient. Stronger conspecific relative to heterospecific negative density dependence in more productive regions was associated with higher local diversity, weaker habitat partitioning (less species sorting), and homogenization of community composition among sites (lower β-diversity). Regional processes associated with changes in species pools had limited effects on β-diversity. Our study suggests that systematic shifts in the strength of local interactions within and among species might generally contribute to some of the most prominent but poorly understood gradients in global biodiversity.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: Hypothesized influences of regional and local processes on patterns of biodiversity across regions that vary in primary productivity.
Figure 2: Study area in western North America and changes in tree species richness and composition with NPP.
Figure 3: Relationships between β-diversity, environmental heterogeneity and NPP.
Figure 4: Conspecific and heterospecific negative density dependence (CNDD and HNDD), NPP, and effects on β-diversity.


  1. 1.

    Hutchinson, G. E. Homage to Santa Rosalia or why are there so many kinds of animals? Am. Nat. 93, 145–159 (1959).

    Article  Google Scholar 

  2. 2.

    Mittelbach, G. G. et al. What is the observed relationship between species richness and productivity? Ecology 82, 2381–2396 (2001).

    Article  Google Scholar 

  3. 3.

    Chase, J. M. & Leibold, M. A. Spatial scale dictates the productivity–biodiversity relationship. Nature 416, 427–430 (2002).

    CAS  Article  PubMed  Google Scholar 

  4. 4.

    Chase, J. M. Stochastic community assembly causes higher biodiversity in more productive environments. Science 328, 1388–1391 (2010).

    CAS  Article  PubMed  Google Scholar 

  5. 5.

    Adler, P. B. et al. Productivity is a poor predictor of plant species richness. Science 333, 1750–1753 (2011).

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    Fraser, L. H. et al. Worldwide evidence of a unimodal relationship between productivity and plant species richness. Science 349, 302–305 (2015).

    CAS  Article  PubMed  Google Scholar 

  7. 7.

    Currie, D. J. & Paquin, V. Large-scale biogeographical patterns of species richness of trees. Nature 329, 326–327 (1987).

    Article  Google Scholar 

  8. 8.

    Gaston, K. J. Global patterns in biodiversity. Nature 405, 220–227 (2000).

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Abramsky, Z. & Rosenzweig, M. L. Tilman’s predicted productivity–diversity relationship shown by desert rodents. Nature 309, 150–151 (1984).

    CAS  Article  PubMed  Google Scholar 

  10. 10.

    Abrams, P. A. Monotonic or unimodal diversity–productivity gradients: what does competition theory predict? Ecology 76, 2019–2027 (1995).

    Article  Google Scholar 

  11. 11.

    Harrison, S., Davies, K. F., Safford, H. D. & Viers, J. H. Beta diversity and the scale-dependence of the productivity–diversity relationship: a test in the Californian serpentine flora. J. Ecol. 94, 110–117 (2006).

    Article  Google Scholar 

  12. 12.

    He, K. & Zhang, J. Testing the correlation between beta diversity and differences in productivity among global ecoregions, biomes, and biogeographical realms. Ecol. Inform. 4, 93–98 (2009).

    Article  Google Scholar 

  13. 13.

    Harrison, S., Vellend, M. & Damschen, E. I. ‘Structured’ beta diversity increases with climatic productivity in a classic dataset. Ecosphere 2, 1–13 (2011).

    Article  Google Scholar 

  14. 14.

    Andrew, M. E., Wulder, M. A., Coops, N. C. & Baillargeon, G. Beta-diversity gradients of butterflies along productivity axes. Global Ecol. Biogeogr. 21, 352–364 (2012).

    Article  Google Scholar 

  15. 15.

    Bonn, A., Storch, D. & Gaston, K. J. Structure of the species–energy relationship. Proc. R. Soc. Lond. B 271, 1685–1691 (2004).

    Article  Google Scholar 

  16. 16.

    Chalcraft, D. R., Williams, J. W., Smith, M. D. & Willig, M. R. Scale dependence in the species-richness–productivity relationship: the role of species turnover. Ecology 85, 2701–2708 (2004).

    Article  Google Scholar 

  17. 17.

    Gaston, K. J. et al. Spatial turnover in the global avifauna. Proc. R. Soc. B. 274, 1567–1574 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  18. 18.

    Chalcraft, D. R. et al. Scale-dependent responses of plant biodiversity to nitrogen enrichment. Ecology 89, 2165–2171 (2008).

    Article  PubMed  Google Scholar 

  19. 19.

    Stegen, J. C. et al. Stochastic and deterministic drivers of spatial and temporal turnover in breeding bird communities. Glob. Ecol. Biogeogr. 22, 202–212 (2013).

    Article  Google Scholar 

  20. 20.

    Melillo, J. M. et al. Global climate change and terrestrial net primary production. Nature 363, 234–240 (1993).

    CAS  Article  Google Scholar 

  21. 21.

    Cardinale, B. J. et al. Biodiversity loss and its impact on humanity. Nature 486, 59–67 (2012).

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Kraft, N. J. et al. Disentangling the drivers of β diversity along latitudinal and elevational gradients. Science 333, 1755–1758 (2011).

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    Ricklefs, R. E. Environmental heterogeneity and plant species diversity: a hypothesis. Am. Nat. 111, 376–381 (1977).

    Article  Google Scholar 

  24. 24.

    Pastor, J., Downing, A. & Erickson, H. E. Species–area curves and diversity–productivity relationships in beaver meadows of Voyageurs National Park, Minnesota, USA. Oikos 77, 399–406 (1996).

    Article  Google Scholar 

  25. 25.

    Veech, J. A. & Crist, T. O. Habitat and climate heterogeneity maintain beta-diversity of birds among landscapes within ecoregions. Glob. Ecol. Biogeogr. 16, 650–656 (2007).

    Article  Google Scholar 

  26. 26.

    MacArthur, R. & Levins, R. The limiting similarity, convergence, and divergence of coexisting species. Am. Nat. 101, 377–385 (1967).

    Article  Google Scholar 

  27. 27.

    Holt, R. D. Spatial heterogeneity, indirect interactions, and the coexistence of prey species. Am. Nat. 124, 377–406 (1984).

    Article  Google Scholar 

  28. 28.

    Tilman, D. & Pacala, S. in Species Diversity in Ecological Communities (eds Ricklefs, R. E. & Schluter, D.) Ch. 2 (Univ. Chicago Press, 1993).

  29. 29.

    Loreau, M. Are communities saturated? On the relationship between α, β and γ diversity. Ecol. Lett. 3, 73–76 (2000).

    Article  Google Scholar 

  30. 30.

    Terborgh, J. W. Toward a trophic theory of species diversity. Proc. Natl Acad. Sci. USA 112, 11415–11422 (2015).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Al-Mufti, M. M., Sydes, C. L., Furness, S. B., Grime, J. P. & Band, S. R. A quantitative analysis of shoot phenology and dominance in herbaceous vegetation. J. Ecol. 65, 759–791 (1977).

    Article  Google Scholar 

  32. 32.

    Stevens, C. J., Dise, N. B., Mountford, J. O. & Gowing, D. J. Impact of nitrogen deposition on the species richness of grasslands. Science 303, 1876–1879 (2004).

    CAS  Article  PubMed  Google Scholar 

  33. 33.

    Suding, K. N. et al. Functional- and abundance-based mechanisms explain diversity loss due to N fertilization. Proc. Natl Acad. Sci. USA 102, 4387–4392 (2005).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. 34.

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

    CAS  Article  PubMed  Google Scholar 

  35. 35.

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

    CAS  Article  PubMed  Google Scholar 

  36. 36.

    Comita, L. S. et al. Testing predictions of the Janzen–Connell hypothesis: a meta-analysis of experimental evidence for distance- and density-dependent seed and seedling survival. J. Ecol. 102, 845–856 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Bever, J. D., Mangan, S. A. & Alexander, H. M. Maintenance of plant species diversity by pathogens. Annu. Rev. Ecol. Evol. Syst. 46, 305–325 (2015).

    Article  Google Scholar 

  38. 38.

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

    Article  Google Scholar 

  39. 39.

    Connell, J. H. in Dynamics of Populations (eds den Boer, P. J. & Gradwell, G. R.) 298–312 (Centre for Agricultural Publishing and Documentation, Wageningen, The Netherlands, 1971).

  40. 40.

    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).

    CAS  Article  PubMed  Google Scholar 

  41. 41.

    Johnson, D. J., Beaulieu, W. T., Bever, J. D. & Clay, K. Conspecific negative density dependence and forest diversity. Science 336, 904–907 (2012).

    CAS  Article  PubMed  Google Scholar 

  42. 42.

    LaManna, J. A., Walton, M. L., Turner, B. L. & Myers, J. A. Negative density dependence is stronger in resource-rich environments and diversifies communities when stronger for common but not rare species. Ecol. Lett. 19, 657–667 (2016).

    Article  PubMed  Google Scholar 

  43. 43.

    Givnish, T. J. On the causes of gradients in tropical tree diversity. J. Ecol. 87, 193–210 (1999).

    Article  Google Scholar 

  44. 44.

    O’Connell, B. M. et al. The Forest Inventory and Analysis Database: Database Description and User Guide for Phase 2 version 6.0.2 (USDA Forest Service, 2015).

  45. 45.

    Qian, H. & Ricklefs, R. E. A latitudinal gradient in large-scale beta diversity for vascular plants in North America. Ecol. Lett. 10, 737–744 (2007).

    Article  PubMed  Google Scholar 

  46. 46.

    Chase, J. M. & Knight, T. M. Scale-dependent effect sizes of ecological drivers on biodiversity: why standardised sampling is not enough. Ecol. Lett. 16, 17–26 (2013).

    Article  PubMed  Google Scholar 

  47. 47.

    Fine, P. V., Mesones, I. & Coley, P. D. Herbivores promote habitat specialization by trees in Amazonian forests. Science 305, 663–665 (2004).

    CAS  Article  PubMed  Google Scholar 

  48. 48.

    Ricklefs, R. E. Intrinsic dynamics of the regional community. Ecol. Lett. 18, 497–503 (2015).

    Article  PubMed  Google Scholar 

  49. 49.

    Ricklefs, R. E. & He, F. Region effects influence local tree species diversity. Proc. Natl Acad. Sci. USA 113, 674–679 (2016).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. 50.

    Burkle, L. A., Myers, J. A. & Belote, R. T. Wildfire disturbance and productivity as drivers of plant species diversity across spatial scales. Ecosphere 6, 1–14 (2015).

    Article  Google Scholar 

  51. 51.

    Comes, H. P. & Kadereit, J. W. The effect of Quaternary climatic changes on plant distribution and evolution. Trends Plant Sci. 3, 432–438 (1998).

    Article  Google Scholar 

  52. 52.

    Jaramillo-Correa, J. P., Beaulieu, J., Khasa, D. P. & Bousquet, J. Inferring the past from the present phylogeographic structure of North American forest trees: seeing the forest for the genes. Can. J. For. Res. 39, 286–307 (2009).

    Article  Google Scholar 

  53. 53.

    McNab, W. H. et al. Description of Ecological Subregions: Sections of the Conterminous United States (US Department of Agriculture, Forest Service, 2007).

  54. 54.

    Amundsen, R., Harden, J. & Singer, M. (eds) Factors of Soil Formation: a Fiftieth Anniversary Perspective (Soil Science Society of America, 1994).

  55. 55.

    Zhao, M. & Running, S. W. Drought-induced reduction in global terrestrial net primary production from 2000 through 2009. Science 329, 940–943 (2010).

    CAS  Article  PubMed  Google Scholar 

  56. 56.

    Wang, T., Hamann, A., Spittlehouse, D. & Carroll, C. Locally downscaled and spatially customizable climate data for historical and future periods for North America. PloS ONE 11, e0156720 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  57. 57.

    Zhu, K., Woodall, C. W., Monteiro, J. V. & Clark, J. S. Prevalence and strength of density-dependent tree recruitment. Ecology 96, 2319–2327 (2015).

    Article  PubMed  Google Scholar 

  58. 58.

    Magurran, A. E. Measuring Biological Diversity (Blackwell, 2004).

  59. 59.

    R Core Team. R: A language and environment for statistical computing version 3.2.0 (2015).

  60. 60.

    Oksanen, J. et al. Vegan: Community Ecology Package. R package version 2.2-1 (2015).

  61. 61.

    Anderson, M. J. et al. Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist. Ecol. Lett. 14, 19–28 (2011).

    Article  PubMed  Google Scholar 

  62. 62.

    Eskelinen, A. & Harrison, S. Erosion of beta diversity under interacting global change impacts in a semi-arid grassland. J. Ecol. 103, 397–407 (2015).

    Article  Google Scholar 

  63. 63.

    Jost, L. Partitioning diversity into independent alpha and beta components. Ecology 88, 2427–2439 (2007).

    Article  PubMed  Google Scholar 

  64. 64.

    Myers, J. A. et al. Beta-diversity in temperate and tropical forests reflects dissimilar mechanisms of community assembly. Ecol. Lett. 16, 151–157 (2013).

    Article  PubMed  Google Scholar 

  65. 65.

    Tucker, C. M., Shoemaker, L. G., Davies, K. F., Nemergut, D. R. & Melbourne, B. A. Differentiating between niche and neutral assembly in metacommunities using null models of β-diversity. Oikos 125,, 778–789 (2016).

    Article  Google Scholar 

  66. 66.

    Dolédec, S., Chessel, D. & Gimaret-Carpentier, C. Niche separation in community analysis: a new method. Ecology 81, 2914–2927 (2000).

    Article  Google Scholar 

  67. 67.

    Schielzeth, H. & Forstmeier, W. Conclusions beyond support: overconfident estimates in mixed models. Behav. Ecol. 20, 416–420 (2009).

    Article  PubMed  Google Scholar 

  68. 68.

    Barr, D. J., Levy, R., Scheepers, C. & Tily, H. J. Random effects structure for confirmatory hypothesis testing: keep it maximal. J. Mem. Lang. 68, 255–278 (2013).

    Article  Google Scholar 

  69. 69.

    Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

    Article  Google Scholar 

  70. 70.

    Wright, J. S. Plant diversity in tropical forests: a review of mechanisms of species coexistence. Oecologia 130, 1–14 (2002).

    Article  PubMed  Google Scholar 

  71. 71.

    Paine, C. E. T., Harms, K. E., Schnitzer, S. A. & Carson, W. P. Weak competition among tropical tree seedlings: implications for species coexistence. Biotropica 40, 432–440 (2008).

    Article  Google Scholar 

  72. 72.

    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 

  73. 73.

    Johnson, D. J. et al. Conspecific negative density-dependent mortality and the structure of temperate forests. Ecology 95, 2493–2503 (2014).

    Article  Google Scholar 

Download references


We thank I. Jiménez, S. Tello and D. Vela for helpful comments; and the Forest Inventory and Analysis project. This work was supported by National Science Foundation grants DEB 1256788 and 1557094 (to J.A.M.) and DEB 1256819 (to L.A.B. and R.T.B.).

Author information




J.A.L., J.A.M., L.A.B. and R.T.B. conceived the study. J.A.M., L.A.B. and R.T.B. obtained the funding. J.A.L. executed the statistical analyses and wrote the first draft of the manuscript, and J.A.L., J.A.M., R.T.B., L.A.B. and C.P.C. contributed to revisions.

Corresponding author

Correspondence to Joseph A. LaManna.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

NATECOLEVOL-16080479 Supplementary Information

Supplementary Tables 1–3, Supplementary Figures 1–7

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

LaManna, J.A., Belote, R.T., Burkle, L.A. et al. Negative density dependence mediates biodiversity–productivity relationships across scales. Nat Ecol Evol 1, 1107–1115 (2017).

Download citation

Further reading


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