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Long-term effects of species loss on community properties across contrasting ecosystems

Abstract

Biodiversity loss can heavily affect the functioning of ecosystems, and improving our understanding of how ecosystems respond to biodiversity decline is one of the main challenges in ecology1,2,3,4. Several important aspects of the longer-term effects of biodiversity loss on ecosystems remain unresolved, including how these effects depend on environmental context5,6,7. Here we analyse data from an across-ecosystem biodiversity manipulation experiment that, to our knowledge, represents the world’s longest-running experiment of this type. This experiment has been set up on 30 lake islands in Sweden that vary considerably in productivity and soil fertility owing to differences in fire history8,9. We tested the effects of environmental context on how plant species loss affected two fundamental community attributes—plant community biomass and temporal variability—over 20 years. In contrast to findings from artificially assembled communities10,11,12, we found that the effects of species loss on community biomass decreased over time; this decrease was strongest on the least productive and least fertile islands. Species loss generally also increased temporal variability, and these effects were greatest on the most productive and most fertile islands. Our findings highlight that the ecosystem-level consequences of biodiversity loss are not constant across ecosystems and that understanding and forecasting these consequences necessitates taking into account the overarching role of environmental context.

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Fig. 1: Effects of plant species removal on temporal plant biomass patterns.
Fig. 2: Effects of species richness on plant biomass decreases over time.
Fig. 3: Effects of species removal and species richness on temporal biomass invariability.

References

  1. 1.

    Hector, A. et al. Plant diversity and productivity experiments in European grasslands. Science 286, 1123–1127 (1999).

    Article  PubMed  CAS  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).

    ADS  Article  PubMed  CAS  Google Scholar 

  3. 3.

    Isbell, F. et al. Linking the influence and dependence of people on biodiversity across scales. Nature 546, 65–72 (2017).

    ADS  Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. 4.

    Duffy, J. E., Godwin, C. M. & Cardinale, B. J. Biodiversity effects in the wild are common and as strong as key drivers of productivity. Nature 549, 261–264 (2017).

    ADS  Article  PubMed  CAS  Google Scholar 

  5. 5.

    Craven, D. et al. Plant diversity effects on grassland productivity are robust to both nutrient enrichment and drought. Phil. Trans. R. Soc. Lond. B 371, 20150277 (2016).

    Article  Google Scholar 

  6. 6.

    Fridley, J. D. Resource availability dominates and alters the relationship between species diversity and ecosystem productivity in experimental plant communities. Oecologia 132, 271–277 (2002).

    ADS  Article  PubMed  Google Scholar 

  7. 7.

    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  PubMed  Google Scholar 

  8. 8.

    Wardle, D. A., Hörnberg, G., Zackrisson, O., Kalela-Brundin, M. & Coomes, D. A. Long-term effects of wildfire on ecosystem properties across an island area gradient. Science 300, 972–975 (2003).

    ADS  Article  PubMed  CAS  Google Scholar 

  9. 9.

    Wardle, D. A. & Zackrisson, O. Effects of species and functional group loss on island ecosystem properties. Nature 435, 806–810 (2005).

    ADS  Article  PubMed  CAS  Google Scholar 

  10. 10.

    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).

    ADS  Article  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Guerrero-Ramírez, N. R. et al. Diversity-dependent temporal divergence of ecosystem functioning in experimental ecosystems. Nat. Ecol. Evol. 1, 1639–1642 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Reich, P. B. et al. Impacts of biodiversity loss escalate through time as redundancy fades. Science 336, 589–592 (2012).

    ADS  Article  PubMed  CAS  Google Scholar 

  13. 13.

    Reich, P. B. et al. Plant diversity enhances ecosystem responses to elevated CO2 and nitrogen deposition. Nature 410, 809–812 (2001).

    ADS  Article  PubMed  CAS  Google Scholar 

  14. 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  PubMed  Google Scholar 

  15. 15.

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

    ADS  Article  PubMed  CAS  Google Scholar 

  16. 16.

    Bezemer, T. M. & van der Putten, W. H. Diversity and stability in plant communities. Nature 446, E6–E7 (2007).

    ADS  Article  CAS  Google Scholar 

  17. 17.

    Cardinale, B. J. et al. Biodiversity simultaneously enhances the production and stability of community biomass, but the effects are independent. Ecology 94, 1697–1707 (2013).

    Article  PubMed  Google Scholar 

  18. 18.

    Morin, X., Fahse, L., de Mazancourt, C., Scherer-Lorenzen, M. & Bugmann, H. Temporal stability in forest productivity increases with tree diversity due to asynchrony in species dynamics. Ecol. Lett. 17, 1526–1535 (2014).

    Article  PubMed  Google Scholar 

  19. 19.

    van Ruijven, J. & Berendse, F. Contrasting effects of diversity on the temporal stability of plant populations. Oikos 116, 1323–1330 (2007).

    Article  Google Scholar 

  20. 20.

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

    Article  PubMed  Google Scholar 

  21. 21.

    Hautier, Y. et al. Eutrophication weakens stabilizing effects of diversity in natural grasslands. Nature 508, 521–525 (2014).

    ADS  Article  PubMed  CAS  Google Scholar 

  22. 22.

    Wardle, D. A. et al. Linking vegetation change, carbon sequestration and biodiversity: insights from island ecosystems in a long-term natural experiment. J. Ecol. 100, 16–30 (2012).

    Article  Google Scholar 

  23. 23.

    Huston, M. A. & DeAngelis, D. L. Competition and coexistence: the effects of resource transport and supply rates. Am. Nat. 144, 954–977 (1994).

    Article  Google Scholar 

  24. 24.

    Gundale, M. J., Hyodo, F., Nilsson, M. C. & Wardle, D. A. Nitrogen niches revealed through species and functional group removal in a boreal shrub community. Ecology 93, 1695–1706 (2012).

    Article  PubMed  Google Scholar 

  25. 25.

    Fargione, J. et al. From selection to complementarity: shifts in the causes of biodiversity–productivity relationships in a long-term biodiversity experiment. Proc. R. Soc. Lond. B 274, 871–876 (2007).

    Article  Google Scholar 

  26. 26.

    Symstad, A. J. & Tilman, D. Diversity loss, recruitment limitation, and ecosystem functioning: lessons learned from a removal experiment. Oikos 92, 424–435 (2001).

    Article  Google Scholar 

  27. 27.

    Loreau, M. Biodiversity and ecosystem functioning: recent theoretical advances. Oikos 91, 3–17 (2000).

    Article  Google Scholar 

  28. 28.

    Fowler, M. S. et al. Species dynamics alter community diversity–biomass stability relationships. Ecol. Lett. 15, 1387–1396 (2012).

    Article  PubMed  Google Scholar 

  29. 29.

    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).

    ADS  Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. 30.

    Wardle, D. A., Zackrisson, O., Hörnberg, G. & Gallet, C. The influence of island area on ecosystem properties. Science 277, 1296–1299 (1997).

    Article  CAS  Google Scholar 

  31. 31.

    Wardle, D. A., Walker, L. R. & Bardgett, R. D. Ecosystem properties and forest decline in contrasting long-term chronosequences. Science 305, 509–513 (2004).

    ADS  Article  PubMed  CAS  Google Scholar 

  32. 32.

    Clemmensen, K. E. et al. Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339, 1615–1618 (2013).

    ADS  Article  PubMed  CAS  Google Scholar 

  33. 33.

    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 

  34. 34.

    Coomes, D. A. & Grubb, P. J. Impacts of root competition in forests and woodlands: a theoretical framework and review of experiments. Ecol. Monogr. 70, 171–207 (2000).

    Article  Google Scholar 

  35. 35.

    McGrady-Steed, J., Harris, P. M. & Morin, P. J. Biodiversity regulates ecosystem predictability. Nature 390, 162–165 (1997).

    ADS  Article  CAS  Google Scholar 

  36. 36.

    Wardle, D. A. & Jonsson, M. Long-term resilience of above- and below ground ecosystem components among contrasting ecosystems. Ecology 95, 1836–1849 (2014).

    Article  PubMed  Google Scholar 

  37. 37.

    .Flower-Ellis, J. G. K. Age Structure and Dynamics in Stands of Bilberry (Vaccinium myrtillus L.) (Department of Forest Ecology and Forest Soils, Royal College of Forestry, Stockholm, 1971).

  38. 38.

    Wardle, D. A. et al. Drivers of inter-year variability of plant production and decomposers across contrasting island ecosystems. Ecology 93, 521–531 (2012).

    Article  PubMed  Google Scholar 

  39. 39.

    Nakagawa, S. & Schielzeth, H. A general and simple method for obtaining R 2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4, 133–142 (2013).

    Article  Google Scholar 

  40. 40.

    Roscher, C. et al. Overyielding in experimental grassland communities – irrespective of species pool or spatial scale. Ecol. Lett. 8, 419–429 (2005).

    Article  Google Scholar 

  41. 41.

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

    ADS  Article  PubMed  CAS  Google Scholar 

  42. 42.

    Hector, A. The effect of diversity on productivity: detecting the role of species complementarity. Oikos 82, 597–599 (1998).

    Article  Google Scholar 

  43. 43.

    Loreau, M. Separating sampling and other effects in biodiversity experiments. Oikos 82, 600–602 (1998).

    Article  Google Scholar 

  44. 44.

    Hoaglin, D. C. & Iglewicz, B. Fine-tuning some resistant rules for outlier labeling. J. Am. Stat. Assoc. 82, 1147–1149 (1987).

    Article  Google Scholar 

  45. 45.

    Lagerström, A., Esberg, C., Wardle, D. A. & Giesler, R. Soil phosphorus and microbial response to a long-term wildfire chronosequence in northern Sweden. Biogeochemistry 95, 199–213 (2009).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank numerous assistants for help in the field. This work was supported by grants to D.A.W. from the Swedish Research Council (Vetenskapsrådet) and a Wallenberg Scholars award.

Reviewer information

Nature thanks Y. Hautier, P. Morin and F. van der Plas for their contribution to the peer review of this work.

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Authors

Contributions

D.A.W. acquired the necessary funding, designed the experiment and collected the data. N.F. and P.K. analysed the data in close consultation with D.A.W. P.K. wrote the first draft of the manuscript, and all authors contributed to manuscript completion and revision.

Corresponding author

Correspondence to Paul Kardol.

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The authors declare no competing interests.

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Extended data figures and tables

Extended Data Fig. 1 Effects of plant species removal on temporal biomass patterns (1999–2016, years 3–20) of individual species biomass.

ai, Data show individual species biomass (g per m2) for V. myrtillus (ac), V. vitis-idaea (df) and E. hermaphroditum (gi) for large, medium and small islands. Species codes (M, V, E) refer to the plant species remaining after removal. Thick dark-coloured lines show mean values per treatment (n = 10 islands per size class, except for E treatments on large islands (n = 8), E treatments on medium islands (n = 5), M + E treatments on medium islands (n = 8), E treatments on small islands (n = 9), M treatments on small islands (n = 8) and M + E treatments on small islands (n = 9). Thin light-coloured lines show values for individual plots. Within island size classes, removal treatments with the same letters are not significantly different across years through the duration of the study. Treatment effects were tested using linear mixed models fitted by a restricted maximum likelihood method, and we used contrast analyses to test across-year differences between removal treatments (see Methods for details).

Extended Data Fig. 2 Temporal patterns (1999–2016; years 3–20) of the proportion of variance in total plant biomass explained by the species-removal treatment for large, medium and small islands.

The proportion of variance explained (also called the effect size) was calculated using marginal R2 values (R2GLMM(m)) for linear mixed models (n = 10 islands per size class). Linear regressions were fit for each island size class (dotted lines). We used linear mixed models to test how R2GLMM(m) changed over time with island size class and year as fixed factors and year as a continuous variable. Contrasts on the interaction between island size class and year were used to test if the slopes of regressions between year and R2GLMM(m) differed between island size classes. Significant differences in slopes among island size classes at α = 0.05 are indicated in the panel.

Extended Data Table 1 Effects of species removal, island size and their interactions on total and species-specific plant biomass
Extended Data Table 2 Effects of species removal, island size and their interactions on the amount of variance explained (R2GLMM(m)) by species removal treatment and by realized species richness
Extended Data Table 3 Effects of species removal or realized species richness, and island size, and their interactions on temporal invariability
Extended Data Table 4 Selected ecosystem properties across the island size gradient

Supplementary information

Supplementary Information

This file contains 10 tables, 12 figures, and supplementary discussion. Together, these items provide essential background information and additional analyses further exploring the role of plant species identity, relative yield total and transgressive over-yielding, and non-linear patterns of effects of species loss

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Kardol, P., Fanin, N. & Wardle, D.A. Long-term effects of species loss on community properties across contrasting ecosystems. Nature 557, 710–713 (2018). https://doi.org/10.1038/s41586-018-0138-7

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