Individual species provide multifaceted contributions to the stability of ecosystems

Abstract

Exploration of the relationship between species diversity and ecological stability has occupied a prominent place in ecological research for decades. Yet, a key component of this puzzle—the contributions of individual species to the overall stability of ecosystems—remains largely unknown. Here, we show that individual species simultaneously stabilize and destabilize ecosystems along different dimensions of stability, and also that their contributions to functional (biomass) and compositional stability are largely independent. By simulating experimentally the extinction of three consumer species (the limpet Patella, the periwinkle Littorina and the topshell Gibbula) from a coastal rocky shore, we found that the capacity to predict the combined contribution of species to stability from the sum of their individual contributions varied among stability dimensions. This implies that the nature of the diversity–stability relationship depends upon the dimension of stability under consideration, and may be additive, synergistic or antagonistic. We conclude that, although the profoundly multifaceted and context-dependent consequences of species loss pose a significant challenge, the predictability of cumulative species contributions to some dimensions of stability provide a way forward for ecologists trying to conserve ecosystems and manage their stability under global change.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Quantification of species contributions to multiple dimensions of ecological stability.
Fig. 2: Relative responses of macroalgal communities to our experimental pulse perturbation over time.
Fig. 3: Species contributions to multiple components of ecological stability.
Fig. 4: Comparison of observed combined contributions of multiple grazer species to stability to those predicted from the additive combination of individual taxa.

Data availability

The data supporting the findings of this study are available in the Zonodo digital repository69.

References

  1. 1.

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

    CAS  Article  Google Scholar 

  2. 2.

    Hooper, D. U. et al. A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486, 105–108 (2012).

    CAS  PubMed  Article  Google Scholar 

  3. 3.

    Naeem, S., Duffy, J. E. & Zavaleta, E. The functions of biological diversity in an age of extinction. Science 336, 1401–1406 (2012).

    CAS  PubMed  Article  Google Scholar 

  4. 4.

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

    CAS  PubMed  Article  Google Scholar 

  5. 5.

    Pimm, S. L. et al. The biodiversity of species and their rates of extinction, distribution, and protection. Science 344, 1246752 (2014).

    CAS  PubMed  Article  Google Scholar 

  6. 6.

    Ceballos, G., Ehrlich, P. R. & Raven, P. H. Vertebrates on the brink as indicators of biological annihilation and the sixth mass extinction. Proc. Natl Acad. Sci. USA 117, 13596–13602 (2020).

    CAS  PubMed  Article  Google Scholar 

  7. 7.

    Loreau, M. et al. Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294, 804–808 (2001).

    CAS  Article  Google Scholar 

  8. 8.

    Lefcheck, J. S. et al. Biodiversity enhances ecosystem multifunctionality across trophic levels and habitats. Nat. Commun. 6, 6936 (2015).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  9. 9.

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

    PubMed  Article  Google Scholar 

  10. 10.

    Macdougall, A. S., McCann, K. S., Gellner, G. & Turkington, R. Diversity loss with persistent human disturbance increases vulnerability to ecosystem collapse. Nature 494, 86–89 (2013).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  11. 11.

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  12. 12.

    Kéfi, S. et al. Advancing our understanding of ecological stability. Ecol. Lett. 22, 1349–1356 (2019).

    PubMed  Article  PubMed Central  Google Scholar 

  13. 13.

    Donohue, I. et al. Loss of predator species, not intermediate consumers, triggers rapid and dramatic extinction cascades. Glob. Change Biol. 23, 2962–2972 (2017).

    Article  Google Scholar 

  14. 14.

    Sanders, D., Thébault, E., Kehoe, R. & Frank van Veen, F. J. Trophic redundancy reduces vulnerability to extinction cascades. Proc. Natl Acad. Sci. USA 115, 2419–2424 (2018).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  15. 15.

    O’Connor, N. E., Bracken, M. E., Crowe, T. P. & Donohue, I. Nutrient enrichment alters the consequences of species loss. J. Ecol. 103, 862–870 (2015).

    Article  Google Scholar 

  16. 16.

    O’Connor, N. E. & Donohue, I. Environmental context determines multi-trophic effects of consumer species loss. Glob. Change Biol. 19, 431–440 (2013).

    Article  Google Scholar 

  17. 17.

    O’Connor, N. E. & Crowe, T. P. Biodiversity loss and ecosystem functioning: distinguishing between number and identity of species. Ecology 86, 1783–1796 (2005).

    Article  Google Scholar 

  18. 18.

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  19. 19.

    Loreau, M. & Hector, A. Partitioning selection and complementarity in biodiversity experiments. Nature 412, 72–76 (2001).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  20. 20.

    Tilman, D., Isbell, F. & Cowles, J. M. Biodiversity and ecosystem functioning. Annu. Rev. Ecol. Evol. Syst. 45, 471–493 (2014).

    Article  Google Scholar 

  21. 21.

    O’Gorman, E. J. & Emmerson, M. C. Perturbations to trophic interactions and the stability of complex food webs. Proc. Natl Acad. Sci. USA 106, 13393–13398 (2009).

    PubMed  Article  PubMed Central  Google Scholar 

  22. 22.

    May, R. M. Will a large complex system be stable? Nature 238, 413–414 (1972).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  23. 23.

    May, R. M. Stability and Complexity in Model Ecosystems (Princeton Univ. Press, 1973).

  24. 24.

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

    CAS  Article  Google Scholar 

  25. 25.

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  26. 26.

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  27. 27.

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

    PubMed  Article  PubMed Central  Google Scholar 

  28. 28.

    Pennekamp, F. et al. Biodiversity increases and decreases ecosystem stability. Nature 563, 109–112 (2018).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  29. 29.

    Paine, R. T. Food web complexity and species diversity. Am. Nat. 100, 65–75 (1966).

    Article  Google Scholar 

  30. 30.

    Terborgh, J. et al. Ecological meltdown in predator-free forest fragments. Science 294, 1923–1927 (2001).

    CAS  PubMed  Article  Google Scholar 

  31. 31.

    Díaz, S., Symstad, A. J., Chapin, F. S., Wardle, D. A. & Huenneke, L. F. Functional diversity revealed by removal experiments. Trends Ecol. Evol. 18, 140–146 (2003).

    Article  Google Scholar 

  32. 32.

    Borrvall, C. & Ebenman, B. Early onset of secondary extinctions in ecological communities following the loss of top predators. Ecol. Lett. 9, 435–442 (2006).

    PubMed  Article  Google Scholar 

  33. 33.

    Petchey, O. L., Eklöf, A., Borrvall, C. & Ebenman, B. Trophically unique species are vulnerable to cascading extinction. Am. Nat. 171, 568–579 (2008).

    PubMed  Article  Google Scholar 

  34. 34.

    Kardol, P., Fanin, N. & Wardle, D. A. Long-term effects of species loss on community properties across contrasting ecosystems. Nature 557, 710–713 (2018).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  35. 35.

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

    PubMed  Article  Google Scholar 

  36. 36.

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

    Article  Google Scholar 

  37. 37.

    de Mazancourt, C. et al. Predicting ecosystem stability from community composition and biodiversity. Ecol. Lett. 16, 617–625 (2013).

    PubMed  Article  PubMed Central  Google Scholar 

  38. 38.

    Neubert, M. & Caswell, H. Alternatives to resilience for measuring the responses of ecological systems to perturbations. Ecology 78, 653–665 (2012).

    Article  Google Scholar 

  39. 39.

    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).

    PubMed  Article  PubMed Central  Google Scholar 

  40. 40.

    Naeem, S. Advancing realism in biodiversity research. Trends Ecol. Evol. 23, 414–416 (2008).

    PubMed  Article  PubMed Central  Google Scholar 

  41. 41.

    Mrowicki, R. J., Maggs, C. A. & O’Connor, N. E. Consistent effects of consumer species loss across different habitats. Oikos 124, 1555–1563 (2015).

    Article  Google Scholar 

  42. 42.

    Hillebrand, H. et al. Decomposing multiple dimensions of stability in global change experiments. Ecol. Lett. 21, 21–30 (2018).

    PubMed  Article  PubMed Central  Google Scholar 

  43. 43.

    Hillebrand, H. & Kunze, C. Meta-analysis on pulse disturbances reveals differences in functional and compositional recovery across ecosystems. Ecol. Lett. 23, 575–585 (2020).

    PubMed  Article  PubMed Central  Google Scholar 

  44. 44.

    Hoover, D. L., Knapp, A. K. & Smith, M. D. Resistance and resilience of a grassland ecosystem to climate extremes. Ecology 95, 2646–2656 (2014).

    Article  Google Scholar 

  45. 45.

    Johns, K. A., Osborne, K. O. & Logan, M. Contrasting rates of coral recovery and reassembly in coral communities on the Great Barrier Reef. Coral Reefs 33, 553–563 (2014).

    Article  Google Scholar 

  46. 46.

    Gülzow, N., Muijsers, F., Ptacnik, R. & Hillebrand, H. Functional and structural stability are linked in phytoplankton metacommunities of different connectivity. Ecography 40, 719–732 (2016).

    Article  Google Scholar 

  47. 47.

    Garnier, A., Pennekamp, F., Lemoine, M. & Petchey, O. L. Temporal scale dependent interactions between multiple environmental disturbances in microcosm ecosystems. Glob. Change Biol. 23, 5237–5248 (2017).

    Article  Google Scholar 

  48. 48.

    Yang, Q., Fowler, M. S., Jackson, A. L. & Donohue, I. The predictability of ecological stability in a noisy world. Nat. Ecol. Evol. 3, 251–259 (2019).

    PubMed  Article  Google Scholar 

  49. 49.

    Pimm, S. L., Donohue, I., Montoya, J. M. & Loreau, M. Measuring resilience is essential to understand it. Nat. Sustain. 2, 895–897 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  50. 50.

    Cardinale, B. J. et al. Impacts of plant diversity on biomass production increase through time because of species complementarity. Proc. Natl Acad. Sci. USA 104, 18123–18128 (2007).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  51. 51.

    Mrowicki, R. J., O’Connor, N. E. & Donohue, I. Temporal variability of a single population can determine the vulnerability of communities to perturbations. J. Ecol. 104, 887–897 (2016).

    Article  Google Scholar 

  52. 52.

    Griffin, J. N. et al. Spatial heterogeneity increases the importance of species richness for an ecosystem process. Oikos 118, 1335–1342 (2009).

    Article  Google Scholar 

  53. 53.

    Emmerson, M. C., Solan, M., Emes, C., Paterson, D. M. & Raffaelli, D. Consistent patterns and the idiosyncstatic effects of biodiversity in marine ecosystems. Nature 411, 73–77 (2001).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  54. 54.

    Baert, J. M., Eisenhauer, N., Janssen, C. R. & de Laender, F. Biodiversity effects on ecosystem functioning respond unimodally to environmental stress. Ecol. Lett. 21, 1191–1199 (2018).

    PubMed  Article  PubMed Central  Google Scholar 

  55. 55.

    Vye, S., Dick, J. T. A., Emmerson, M. C. & O’Connor, N. E. Cumulative effects of an invasive species and nutrient enrichment on rock pool communities. Mar. Ecol. Prog. Ser. 594, 39–50 (2018).

    CAS  Article  Google Scholar 

  56. 56.

    Thiébaut, E. et al. Changes in a benthic system exposed to multiple stressors: a 40-year time-series in the English Channel. PeerJ Prepr. 6, e26745v1 (2018).

    Google Scholar 

  57. 57.

    Houbin, C., Thiébaut, E. & Hoebeke, M. Study of specific diversity of macrobenthic communities in the ‘Pierre Noire’ site: Dataset/Sampling event (Station Biologique de Roscoff - Sorbonne Université-CNRS, 2018); https://doi.org/10.21411/kfms-pq29

  58. 58.

    O’Connor, N. E., Donohue, I., Crowe, T. P. & Emmerson, M. C. Importance of consumers on exposed and sheltered rocky shores. Mar. Ecol. Prog. Ser. 443, 65–75 (2011).

    Article  Google Scholar 

  59. 59.

    O’Connor, N. E., Emmerson, M. C., Crowe, T. P. & Donohue, I. Distinguishing between direct and indirect effects of predators in complex ecosystems. J. Anim. Ecol. 82, 438–448 (2013).

    PubMed  Article  PubMed Central  Google Scholar 

  60. 60.

    Byrnes, J. E. & Stachowicz, J. J. The consequences of consumer diversity loss: different answers from different experimental designs. Ecology 90, 2879–2888 (2009).

    PubMed  Article  PubMed Central  Google Scholar 

  61. 61.

    Firth, L. B. & Crowe, T. P. Competition and habitat suitability: small-scale segregation underpins large-scale coexistence of key species on temperate rocky shores. Oecologia 162, 163–174 (2010).

    PubMed  Article  PubMed Central  Google Scholar 

  62. 62.

    Crowe, T. P. et al. Large-scale variation in combined impacts of canopy loss and disturbance on community structure and ecosystem functioning. PLoS ONE 8, e66238 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  63. 63.

    Benedetti-Cecchi, L., Tamburello, L., Maggi, E. & Bulleri, F. Experimental perturbations modify the performance of early warning indicators of regime shift. Curr. Biol. 25, 1867–1872 (2015).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  64. 64.

    Griffin, J. N. et al. Consumer effects on ecosystem functioning in rock pools: roles of species richness and composition. Mar. Ecol. Prog. Ser. 420, 45–56 (2010).

    Article  Google Scholar 

  65. 65.

    Griffin, J. N., Méndez, V., Johnson, A. F., Jenkins, S. R. & Foggo, A. Functional diversity predicts overyielding effect of species combination on primary productivity. Oikos 118, 37–44 (2009).

    Article  Google Scholar 

  66. 66.

    Anderson, M. J. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26, 32–46 (2001).

    Google Scholar 

  67. 67.

    McArdle, B. H. & Anderson, M. J. Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82, 290–297 (2001).

    Article  Google Scholar 

  68. 68.

    Clarke, K. R. Non‐parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18, 117–143 (1993).

    Article  Google Scholar 

  69. 69.

    White, L., O’Connor, N., Yang, Q., Emmerson, M. & Donohue, I. Individual species provide multifaceted contributions to the stability of ecosystems_Dataset (Version 1). Zenodo https://doi.org/10.5281/zenodo.3974299 (2020).

  70. 70.

    Tilman, D., Reich, P. B. & Knops, J. M. H. Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature 441, 629–632 (2006).

    CAS  PubMed  Article  Google Scholar 

  71. 71.

    Whittaker, F. Evolution and measurement of species diversity. Taxon 21, 213–251 (1972).

    Article  Google Scholar 

  72. 72.

    Lande, R. Statistics and partitioning of species diversity, and similarity among multiple communities. Oikos 76, 5–13 (1996).

    Article  Google Scholar 

  73. 73.

    Olden, J. D., Poff, N. L. R., Douglas, M. R., Douglas, M. E. & Fausch, K. D. Ecological and evolutionary consequences of biotic homogenization. Trends Ecol. Evol. 19, 18–24 (2004).

    PubMed  Article  Google Scholar 

  74. 74.

    France, K. E. & Duffy, J. E. Diversity and dispersal interactively affect predictability of ecosystem function. Nature 441, 1139–1143 (2006).

    CAS  PubMed  Article  Google Scholar 

  75. 75.

    Wang, S. et al. An invariability-area relationship sheds new light on the spatial scaling of ecological stability. Nat. Commun. 8, 15211 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  76. 76.

    Wang, S. & Loreau, M. Biodiversity and ecosystem stability across scales in metacommunities. Ecol. Lett. 19, 510–518 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  77. 77.

    Gravel, D., Massol, F. & Leibold, M. A. Stability and complexity in model meta-ecosystems. Nat. Commun. 7, 12457 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Contributions

L.W., N.E.O’C. and I.D. designed the research. L.W. performed the experiment and analysed the data. L.W. and I.D. led the writing, with contributions from N.E.O’C., Q.Y. and M.C.E.

Corresponding author

Correspondence to Ian Donohue.

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

Extended Data Fig. 1 Functional and compositional stability responses of macroalgal assemblages in our different grazer loss treatments.

Box and whisker plots (n = 4, for all measures except spatial variability, for which, n = 11) of (a, b) spatial and (c, d) temporal variability of macroalgal communities in unperturbed plots and (e, f) resistance, (g, h) reactivity, (i, j) resilience and (k, l) recovery time of macroalgal communities in response to our experimentally-imposed pulse perturbation. The centre line indicates the median, the bottom and top hinges of the box and whiskers plot correspond to the 25th and 75th percentiles, and the bottom and top whiskers extend from the hinge to the lowest and highest value, respectively (maximum 1.5× interquartile range from the hinge). Outlying points are plotted individually. Functional stability responses (a, c, e, g, i, k) were based on total macroalgal cover, whereas compositional stability responses (b, d, f, h, j, l) were based on macroalgal community composition. Stability increases from the bottom to the top of the y-axis in every case. A strong destabilising effect of the pulse perturbation in plots from which a species was removed compared to those in which it was present implies that the species contributes strongly to that component of ecological stability. Letters indicate treatments that are statistically indistinguishable from each other based on SNK tests (P > 0.05).

Extended Data Fig. 2 Relationships between functional and compositional stability properties of macroalgal assemblages.

Analyses were pooled across grazer loss treatments (n = 20), with each point representing a single replicate plot. Significant (P < 0.05) relationships are indicated by the presence of a reduced major axis regression line, with associated 95% confidence intervals.

Extended Data Fig. 3 Responses of macroalgal communities to our experimental pulse perturbation over time in uncaged plots and caged plots from which no species were removed.

Mean (± s.e.m., n = 4) log response ratios (LRRs), overlain with raw data points, of the (a) functional (total cover) and (b) compositional responses of macroalgal assemblages to our experimental pulse perturbation (that is, LRRs of perturbed compared to equivalent unperturbed plots within caged and uncaged treatments) in plots from caged plots with no grazer removals (black line) and open uncaged control plots (grey line) over the duration of the experiment. Thick lines indicate significant (P < 0.05) effects of the perturbation, based on two-sample t-tests and PERMANOVAs for, respectively, functional and compositional responses.

Supplementary information

Supplementary Information

Supplementary Tables 1–4.

Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

White, L., O’Connor, N.E., Yang, Q. et al. Individual species provide multifaceted contributions to the stability of ecosystems. Nat Ecol Evol (2020). https://doi.org/10.1038/s41559-020-01315-w

Download citation

Search

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