Skip to main content

Thank you for visiting nature.com. 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.

Biodiversity increases and decreases ecosystem stability

Abstract

Losses and gains in species diversity affect ecological stability1,2,3,4,5,6,7 and the sustainability of ecosystem functions and services8,9,10,11,12,13. Experiments and models have revealed positive, negative and no effects of diversity on individual components of stability, such as temporal variability, resistance and resilience2,3,6,11,12,14. How these stability components covary remains poorly understood15. Similarly, the effects of diversity on overall ecosystem stability16, which is conceptually akin to ecosystem multifunctionality17,18, remain unknown. Here we studied communities of aquatic ciliates to understand how temporal variability, resistance and overall ecosystem stability responded to diversity (that is, species richness) in a large experiment involving 690 micro-ecosystems sampled 19 times over 40 days, resulting in 12,939 samplings. Species richness increased temporal stability but decreased resistance to warming. Thus, two stability components covaried negatively along the diversity gradient. Previous biodiversity manipulation studies rarely reported such negative covariation despite general predictions of the negative effects of diversity on individual stability components3. Integrating our findings with the ecosystem multifunctionality concept revealed hump- and U-shaped effects of diversity on overall ecosystem stability. That is, biodiversity can increase overall ecosystem stability when biodiversity is low, and decrease it when biodiversity is high, or the opposite with a U-shaped relationship. The effects of diversity on ecosystem multifunctionality would also be hump- or U-shaped if diversity had positive effects on some functions and negative effects on others. Linking the ecosystem multifunctionality concept and ecosystem stability can transform the perceived effects of diversity on ecological stability and may help to translate this science into policy-relevant information.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Biomass and stability in experimental microbial communities.
Fig. 2: Positive, negative and neutral relationships among resistance, resilience and temporal variability in empirical studies with diversity manipulation.
Fig. 3: Hump- and U-shaped diversity–stability relationships.

Data availability

The experimental data that support the findings of this study are available at Github (https://github.com/pennekampster/Code_and_data_OverallEcosystemStability) with the identifier (https://doi.org/10.5281/zenodo.1345557). Source Data for Figs. 13 are provided in the online version of the paper.

References

  1. Pimm, S. L. The complexity and stability of ecosystems. Nature 307, 321–326 (1984).

    Article  ADS  Google Scholar 

  2. McCann, K. S. The diversity–stability debate. Nature 405, 228–233 (2000).

    Article  CAS  Google Scholar 

  3. Ives, A. R. & Carpenter, S. R. Stability and diversity of ecosystems. Science 317, 58–62 (2007).

    Article  ADS  CAS  Google Scholar 

  4. Allesina, S. & Tang, S. Stability criteria for complex ecosystems. Nature 483, 205–208 (2012).

    Article  ADS  CAS  Google Scholar 

  5. Mougi, A. & Kondoh, M. Diversity of interaction types and ecological community stability. Science 337, 349–351 (2012).

    Article  ADS  MathSciNet  CAS  Google Scholar 

  6. Loreau, M. & de Mazancourt, C. Biodiversity and ecosystem stability: a synthesis of underlying mechanisms. Ecol. Lett. 16, 106–115 (2013).

    Article  Google Scholar 

  7. Grilli, J., Barabás, G., Michalska-Smith, M. J. & Allesina, S. Higher-order interactions stabilize dynamics in competitive network models. Nature 548, 210–213 (2017).

    Article  ADS  CAS  Google Scholar 

  8. Tilman, D. & Downing, J. A. Biodiversity and stability in grasslands. Nature 367, 363–365 (1994).

    Article  ADS  Google Scholar 

  9. Pfisterer, A. B. & Schmid, B. Diversity-dependent production can decrease the stability of ecosystem functioning. Nature 416, 84–86 (2002).

    Article  ADS  CAS  Google Scholar 

  10. Worm, B. et al. Impacts of biodiversity loss on ocean ecosystem services. Science 314, 787–790 (2006).

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  12. Wright, A. J. et al. Flooding disturbances increase resource availability and productivity but reduce stability in diverse plant communities. Nat. Commun. 6, 6092 (2015).

    Article  ADS  CAS  Google Scholar 

  13. Isbell, F. et al. Biodiversity increases the resistance of ecosystem productivity to climate extremes. Nature 526, 574–577 (2015).

    Article  ADS  CAS  Google Scholar 

  14. Isbell, F. I., Polley, H. W. & Wilsey, B. J. Biodiversity, productivity and the temporal stability of productivity: patterns and processes. Ecol. Lett. 12, 443–451 (2009).

    Article  Google Scholar 

  15. Donohue, I. et al. On the dimensionality of ecological stability. Ecol. Lett. 16, 421–429 (2013).

    Article  Google Scholar 

  16. Donohue, I. et al. Navigating the complexity of ecological stability. Ecol. Lett. 19, 1172–1185 (2016).

    Article  Google Scholar 

  17. Duffy, J. E., Richardson, J. P. & Canuel, E. A. Grazer diversity effects on ecosystem functioning in seagrass beds. Ecol. Lett. 6, 637–645 (2003).

    Article  Google Scholar 

  18. Hector, A. & Bagchi, R. Biodiversity and ecosystem multifunctionality. Nature 448, 188–190 (2007).

    Article  ADS  CAS  Google Scholar 

  19. Balvanera, P. et al. Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol. Lett. 9, 1146–1156 (2006).

    Article  Google Scholar 

  20. Zhang, Q.-G. & Zhang, D.-Y. Resource availability and biodiversity effects on the productivity, temporal variability and resistance of experimental algal communities. Oikos 114, 385–396 (2006).

    Article  Google Scholar 

  21. Baert, J. M., De Laender, F., Sabbe, K. & Janssen, C. R. Biodiversity increases functional and compositional resistance, but decreases resilience in phytoplankton communities. Ecology 97, 3433–3440 (2016).

    Article  Google Scholar 

  22. Arnoldi, J.-F., Loreau, M. & Haegeman, B. Resilience, reactivity and variability: a mathematical comparison of ecological stability measures. J. Theor. Biol. 389, 47–59 (2016).

    Article  MathSciNet  Google Scholar 

  23. Suding, K. N. et al. Scaling environmental change through the community-level: a trait-based response-and-effect framework for plants. Glob. Change Biol. 14, 1125–1140 (2008).

    Article  ADS  Google Scholar 

  24. Mori, A. S., Furukawa, T. & Sasaki, T. Response diversity determines the resilience of ecosystems to environmental change. Biol. Rev. Camb. Philos. Soc. 88, 349–364 (2013).

    Article  Google Scholar 

  25. Maestre, F. T. et al. Plant species richness and ecosystem multifunctionality in global drylands. Science 335, 214–218 (2012).

    Article  ADS  CAS  Google Scholar 

  26. Slade, E. M. et al. The importance of species identity and interactions for multifunctionality depends on how ecosystem functions are valued. Ecology 98, 2626–2639 (2017).

    Article  Google Scholar 

  27. Gamfeldt, L. & Roger, F. Revisiting the biodiversity–ecosystem multifunctionality relationship. Nat. Ecol. Evol. 1, 0168 (2017).

    Article  Google Scholar 

  28. Manning, P. et al. Redefining ecosystem multifunctionality. Nat. Ecol. Evol. 2, 427–436 (2018).

    Article  Google Scholar 

  29. Armsworth, P. R. & Roughgarden, J. E. The economic value of ecological stability. Proc. Natl Acad. Sci. USA 100, 7147–7151 (2003).

    Article  ADS  CAS  Google Scholar 

  30. Cottingham, K. L., Lennon, J. T. & Brown, B. L. Knowing when to draw the line: designing more informative ecological experiments. Front. Ecol. Environ. 3, 145–152 (2005).

    Article  Google Scholar 

  31. Leary, D. J. & Petchey, O. L. Testing a biological mechanism of the insurance hypothesis in experimental aquatic communities. J. Anim. Ecol. 78, 1143–1151 (2009).

    Article  Google Scholar 

  32. Altermatt, F. et al. Big answers from small worlds: a user’s guide for protist microcosms as a model system in ecology and evolution. Methods Ecol. Evol. 6, 218–231 (2015).

    Article  Google Scholar 

  33. Pennekamp, F. et al. Dynamic species classification of microorganisms across time, abiotic and biotic environments—a sliding window approach. PLoS ONE 12, e0176682 (2017).

    Article  Google Scholar 

  34. Pennekamp, F., Schtickzelle, N. & Petchey, O. L. BEMOVI, software for extracting behavior and morphology from videos, illustrated with analyses of microbes. Ecol. Evol. 5, 2584–2595 (2015).

    Article  Google Scholar 

  35. May, R. M. Stability and complexity in model ecosystems. Monogr. Popul. Biol. 6, 1–235 (1973).

    CAS  PubMed  Google Scholar 

  36. Tilman, D., Lehman, C. L. & Bristow, C. E. Diversity–stability relationships: statistical inevitability or ecological consequence? Am. Nat. 151, 277–282 (1998).

    Article  CAS  Google Scholar 

  37. Gross, K. et al. Species richness and the temporal stability of biomass production: a new analysis of recent biodiversity experiments. Am. Nat. 183, 1–12 (2014).

    Article  Google Scholar 

  38. Hallett, L. M. et al. codyn: an R package of community dynamics metrics. Methods Ecol. Evol. 7, 1146–1151 (2016).

    Article  Google Scholar 

  39. Schmid, B., Baruffol, M., Wang, Z. & Niklaus, P. A. A guide to analyzing biodiversity experiments. J. Plant Ecol. 10, 91–110 (2017).

    Article  Google Scholar 

  40. Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & R Core Team. nlme: Linear and Nonlinear Mixed Effects Models R package version 3.1.137 https://CRAN.R-project.org/package=nlme (2018).

  41. Legendre, P. lmodel2: Model II Regression R package version 1.7.3 https://CRAN.R-project.org/package=lmodel2 (2018).

  42. R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2018).

    Google Scholar 

  43. Caldeira, M. C., Hector, A., Loreau, M. & Pereira, J. S. Species richness, temporal variability and resistance of biomass production in a Mediterranean grassland. Oikos 110, 115–123 (2005).

    Article  Google Scholar 

  44. Zhang, Q.-G. & Zhang, D.-Y. Species richness destabilizes ecosystem functioning in experimental aquatic microcosms. Oikos 112, 218–226 (2006).

    Article  Google Scholar 

  45. van Ruijven, J. & Berendse, F. Diversity enhances community recovery, but not resistance, after drought. J. Ecol. 98, 81–86 (2010).

    Article  Google Scholar 

  46. Griffiths, B. S. et al. Ecosystem Response of pasture soil communities to fumigation-induced microbial diversity reductions: an examination of the biodiversity–ecosystem function relationship. Oikos 90, 279–294 (2000).

    Article  Google Scholar 

  47. Wardle, D. A., Bonner, K. I. & Barker, G. M. Stability of ecosystem properties in response to above-ground functional group richness and composition. Oikos 89, 11–23 (2000).

    Article  Google Scholar 

  48. Hughes, A. R. & Stachowicz, J. J. Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proc. Natl Acad. Sci. USA 101, 8998–9002 (2004).

    Article  ADS  CAS  Google Scholar 

  49. Vogel, A., Scherer-Lorenzen, M. & Weigelt, A. Grassland resistance and resilience after drought depends on management intensity and species richness. PLoS ONE 7, e36992 (2012).

    Article  ADS  CAS  Google Scholar 

  50. Wertz, S. et al. Decline of soil microbial diversity does not influence the resistance and resilience of key soil microbial functional groups following a model disturbance. Environ. Microbiol. 9, 2211–2219 (2007).

    Article  Google Scholar 

  51. Wagg, C. et al. Plant diversity maintains long-term ecosystem productivity under frequent drought by increasing short-term variation. Ecology 98, 2952–2961 (2017).

    Article  Google Scholar 

  52. Tilman, D. Biodiversity: population versus ecosystem stability. Ecology 77, 350–363 (1996).

    Article  Google Scholar 

  53. Byrnes, J. E. K. et al. Investigating the relationship between biodiversity and ecosystem multifunctionality: challenges and solutions. Methods Ecol. Evol. 5, 111–124 (2014).

    Article  Google Scholar 

  54. Antiqueira, P. A. P., Petchey, O. L. & Romero, G. Q. Warming and top predator loss drive ecosystem multifunctionality. Ecol. Lett. 21, 72–82 (2018).

    Article  Google Scholar 

  55. Gamfeldt, L., Hillebrand, H. & Jonsson, P. R. Multiple functions increase the importance of biodiversity for overall ecosystem functioning. Ecology 89, 1223–1231 (2008).

    Article  Google Scholar 

Download references

Acknowledgements

F. De Laender and B. Schmid provided feedback on previous drafts of the Letter; I. Donohue provided the list of publications from his 2016 review paper. The University of Zurich Research Priority Programme on Global Change and Biodiversity supported this research. In addition, funding came from the Swiss National Science Foundation (grant PP00P3_150698 to F.A. and 31003A_159498 to O.L.P.). This is publication ISEM 2018-171 of the Institut des Sciences de l’Evolution, Montpellier.

Reviewer information

Nature thanks T. Bell, P. J. Morin and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Author information

Authors and Affiliations

Authors

Contributions

O.L.P., F.P. and F.A. conceived the study. O.L.P., F.P., M.S., E.A.F., F.A., G.-M.P., T.M.M. and M.P. designed the experiment. F.P. coordinated and led the experiment. The experimental sampling was performed by all authors, except J.G. and A.T. F.P., O.L.P. and J.G. prepared the data for analysis. F.P., O.L.P., M.P., A.T. and M.S. analysed the dataset. The first draft was written by F.P. and O.L.P. All authors contributed to revisions of the manuscript.

Corresponding author

Correspondence to Frank Pennekamp.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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

Extended data figures and tables

Extended Data Fig. 1 Richness increased temporal stability across temperatures.

a, The stabilizing effect of richness was present across all temperatures, although temperature had a negative effect on mean stability. The inverse coefficient of variation (ICV) is calculated as the mean biomass divided by the standard deviation of biomass. b, Results of the linear mixed-effects model of log richness, temperature and their interaction on temporal stability supporting the positive effects of richness and the negative effect of temperature on temporal stability (n = 681 independent microcosms). c, Results of the same analysis as in b but without the monocultures. Results are qualitatively the same, indicating that the relationship between richness and temporal stability is not driven only by the monocultures (n = 580 independent microcosms). CI, 95% confidence interval; DF, degrees of freedom; Std.Error, standard error of the estimate.

Extended Data Fig. 2 The effect of richness on absolute and proportional resistance.

a, c, Richness decreased resistance, regardless of whether it was measured on an absolute or proportional scale. b, d, Results of linear mixed-effects models of richness, temperature and their interaction on absolute and proportional richness (n = 567 independent microcosms).

Extended Data Fig. 3 Niche complementarity and low response diversity probably caused the negative covariance of stability components.

Niche complementarity and the resulting increase in total biomass with richness tended to increase temporal stability (Fig. 1). a, b, We found little evidence for an effect of population asynchrony on temporal stability (linear mixed-effects model with composition as random effect and log richness and temperature as fixed effects; n = 681 independent microcosms). c, d, By contrast, statistical averaging contributed to stabilization (linear regression between mean species biomass and the variance of species biomass; n = 2,077 species mean–variance biomass observations). e, Low response diversity was inferred because the biomass of most species decreased or was unaffected by temperature (linear regression between temperature and species biomass; n = 972 species biomass × temperature observations). Consequently, when there were more species, there was greater total biomass and greater temporal stability, but a greater biomass loss, with temperature increase. Therefore, niche complementarity (that is, effect diversity) probably not only caused a positive effect of diversity on temporal stability but also had a negative effect of diversity on resistance in the absence of high response diversity. However, this explanation cannot apply within richness levels, for which positive covariance among stability components was found.

Extended Data Fig. 4 Overview of terms and the concept of overall ecosystem stability.

Measured ecosystem functions (left-most top box) can each have multiple components of stability (for example, temporal variability, resistance and resilience of biomass production), each of which can be combined into a measure of overall stability. When—as in our study—there is only one ecosystem function, this overall stability of a specific function is also the overall ecosystem stability. In studies of more than one ecosystem function, the overall stability of several functions could be combined to give overall ecosystem stability. Alternatively, one could first calculate ecosystem multifunctionality and then measure its stability components.

Extended Data Fig. 5 The effect of aggregating more than two stability components into overall ecosystem stability.

The fraction of stability components with a negative sign influences whether or not a unimodal pattern will result for a total of 100 stability components. a, A unimodal relationship between diversity and OES will result if at least one stability component is negative. b, However, the strength of the pattern depends on the relative balance of positive and negative relationships.

Extended Data Table 1 Richness increased, whereas temperature decreased, biomass production
Extended Data Table 2 Positive temporal stability–resistance relationships within richness levels
Extended Data Table 3 Overview of studies used for literature survey
Extended Data Table 4 Putative mechanisms and type of evidence for bivariate diversity–stability relationships

Supplementary information

Source data

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pennekamp, F., Pontarp, M., Tabi, A. et al. Biodiversity increases and decreases ecosystem stability. Nature 563, 109–112 (2018). https://doi.org/10.1038/s41586-018-0627-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41586-018-0627-8

Keywords

This article is cited by

Comments

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.

Search

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