A substantial body of evidence has demonstrated that biodiversity stabilizes ecosystem functioning over time in grassland ecosystems. However, the relative importance of different facets of biodiversity underlying the diversity–stability relationship remains unclear. Here we use data from 39 grassland biodiversity experiments and structural equation modelling to investigate the roles of species richness, phylogenetic diversity and both the diversity and community-weighted mean of functional traits representing the ‘fast–slow’ leaf economics spectrum in driving the diversity–stability relationship. We found that high species richness and phylogenetic diversity stabilize biomass production via enhanced asynchrony in the performance of co-occurring species. Contrary to expectations, low phylogenetic diversity enhances ecosystem stability directly, albeit weakly. While the diversity of fast–slow functional traits has a weak effect on ecosystem stability, communities dominated by slow species enhance ecosystem stability by increasing mean biomass production relative to the standard deviation of biomass over time. Our in-depth, integrative assessment of factors influencing the diversity–stability relationship demonstrates a more multicausal relationship than has been previously acknowledged.
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May, R. M. Stability and Complexity in Model Ecosystems 6 (Princeton Univ. Press, Princeton, NJ, 1973).
McNaughton, S. J. Stability and diversity of ecological communities. Nature 274, 251–253 (1978).
Tilman, D. & Downing, J. A. Biodiversity and stability in grasslands. Nature 367, 363–365 (1994).
Ives, A. R. & Carpenter, S. R. Stability and diversity of ecosystems. Science 317, 58–62 (2007).
Balvanera, P. et al. Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol. Lett. 9, 1146–1156 (2006).
Hautier, Y. et al. Anthropogenic environmental changes affect ecosystem stability via biodiversity. Science 348, 336–340 (2015).
Isbell, F., Tilman, D., Polasky, S. & Loreau, M. The biodiversity-dependent ecosystem service debt. Ecol. Lett. 18, 119–134 (2015).
Donohue, I. et al. Navigating the complexity of ecological stability. Ecol. Lett. 19, 1172–1185 (2016).
Tilman, D., Reich, P. B. & Knops, J. M. H. Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature 441, 629–632 (2006).
Jiang, L. & Pu, Z. Different effects of species diversity on temporal stability in single-trophic and multitrophic communities. Am. Nat. 174, 651–659 (2009).
Hector, A. et al. General stabilizing effects of plant diversity on grassland productivity through population asynchrony and overyielding. Ecology 91, 2213–2220 (2010).
Campbell, V., Murphy, G. & Romanuk, T. N. Experimental design and the outcome and interpretation of diversity–stability relations. Oikos 120, 399–408 (2011).
de Mazancourt, C. et al. Predicting ecosystem stability from community composition and biodiversity. Ecol. Lett. 16, 617–625 (2013).
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).
Aussenac, R. et al. Intraspecific variability in growth response to environmental fluctuations modulates the stabilizing effect of species diversity on forest growth. J. Ecol. 105, 1010–1020 (2017).
del Río, M. et al. Species interactions increase the temporal stability of community productivity in Pinus sylvestris–Fagus sylvatica mixtures across Europe. J. Ecol. 105, 1032–1043 (2017).
Oliver, T. H. et al. Biodiversity and resilience of ecosystem functions. Trends Ecol. Evol. 30, 673–684 (2015).
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).
Tilman, D. The ecological consequences of changes in biodiversity: a search for general principles. Ecology 80, 1455–1474 (1999).
van Ruijven, J. & Berendse, F. Diversity enhances community recovery, but not resistance, after drought. J. Ecol. 98, 81–86 (2010).
Isbell, F. et al. Biodiversity increases the resistance of ecosystem productivity to climate extremes. Nature 526, 574–577 (2015).
Yachi, S. & Loreau, M. Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc. Natl Acad. Sci. USA 96, 1463–1468 (1999).
Hautier, Y. et al. Eutrophication weakens stabilizing effects of diversity in natural grasslands. Nature 508, 521–525 (2014).
Lehman, C. L. & Tilman, D. Biodiversity, stability, and productivity in competitive communities. Am. Nat. 156, 534–552 (2000).
Maron, J. L., Marler, M., Klironomos, J. N. & Cleveland, C. C. Soil fungal pathogens and the relationship between plant diversity and productivity. Ecol. Lett. 14, 36–41 (2011).
Schnitzer, S. A. et al. Soil microbes drive the classic plant diversity–productivity pattern. Ecology 92, 296–303 (2011).
Tredennick, A. T., de Mazancourt, C., Loreau, M. & Adler, P. B. Environmental responses, not species interactions, determine synchrony of dominant species in semiarid grasslands. Ecology 98, 971–981 (2017).
Naeem, S. et al. Biodiversity as a multidimensional construct: a review, framework and case study of herbivory’s impact on plant biodiversity. Proc. R. Soc. B 283, 20153005 (2016).
Venail, P. et al. Species richness, but not phylogenetic diversity, influences community biomass production and temporal stability in a re-examination of 16 grassland biodiversity studies. Funct. Ecol. 29, 615–626 (2015).
Roscher, C. et al. Identifying population- and community-level mechanisms of diversity–stability relationships in experimental grasslands. J. Ecol. 99, 1460–1469 (2011).
Lepš, J., Májeková, M., Vítová, A., Doležal, J. & de Bello, F. Stabilizing effects in temporal fluctuations: management, traits, and species richness in high-diversity communities. Ecology 99, 360–371 (2018).
Cadotte, M. W., Dinnage, R. & Tilman, D. Phylogenetic diversity promotes ecosystem stability. Ecology 93, S223–S233 (2012).
Flynn, D. F. B., Mirotchnick, N., Jain, M., Palmer, M. I. & Naeem, S. Functional and phylogenetic diversity as predictors of biodiversity–ecosystem–function relationships. Ecology 92, 1573–1581 (2011).
Spasojevic, M. J. & Suding, K. N. Inferring community assembly mechanisms from functional diversity patterns: the importance of multiple assembly processes. J. Ecol. 100, 652–661 (2012).
Cadotte, M. W. Phylogenetic diversity and productivity: gauging interpretations from experiments that do not manipulate phylogenetic diversity. Funct. Ecol. 29, 1603–1606 (2015).
Díaz, S. & Cabido, M. Vive la différence: plant functional diversity matters to ecosystem processes. Trend Ecol. Evol. 16, 646–655 (2001).
Wright, I. J. et al. The worldwide leaf economics spectrum. Nature 428, 821–827 (2004).
Reich, P. B. The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto. J. Ecol. 102, 275–301 (2014).
Grime, J. P. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am. Nat. 111, 1169–1194 (1977).
Díaz, S. et al. The global spectrum of plant form and function. Nature 529, 167–171 (2016).
Polley, H. W., Isbell, F. I. & Wilsey, B. J. Plant functional traits improve diversity-based predictions of temporal stability of grassland productivity. Oikos 122, 1275–1282 (2013).
Májeková, M., de Bello, F., Doležal, J. & Lepš, J. Plant functional traits as determinants of population stability. Ecology 95, 2369–2374 (2014).
Gomez, J. M., Verdu, M. & Perfectti, F. Ecological interactions are evolutionarily conserved across the entire tree of life. Nature 465, 918–921 (2010).
Reinhart, K. O., Wilson, G. W. T. & Rinella, M. J. Predicting plant responses to mycorrhizae: integrating evolutionary history and plant traits. Ecol. Lett. 15, 689–695 (2012).
Gilbert, G. S., Magarey, R., Suiter, K. & Webb, C. O. Evolutionary tools for phytosanitary risk analysis: phylogenetic signal as a predictor of host range of plant pests and pathogens. Evol. Appl. 5, 869–878 (2012).
Parker, I. M. et al. Phylogenetic structure and host abundance drive disease pressure in communities. Nature 520, 542–544 (2015).
Pérez-Harguindeguy, N. et al. New handbook for standardised measurement of plant functional traits worldwide. Aust. J. Bot. 61, 167–234 (2013).
Hoover, D. L., Knapp, A. K. & Smith, M. D. Resistance and resilience of a grassland ecosystem to climate extremes. Ecology 95, 2646–2656 (2014).
O’Brien, M. J., Leuzinger, S., Philipson, C. D., Tay, J. & Hector, A. Drought survival of tropical tree seedlings enhanced by non-structural carbohydrate levels. Nat. Clim. Change 4, 710–714 (2014).
Weigelt, A., Schumacher, J., Roscher, C. & Schmid, B. Does biodiversity increase spatial stability in plant community biomass?. Ecol. Lett. 11, 338–347 (2008).
Fargione, J. & Tilman, D. Niche differences in phenology and rooting depth promote coexistence with a dominant C4 bunchgrass. Oecologia 143, 598–606 (2005).
Reich, P. B. et al. Impact of biodiversity loss escalate through time as redundancy fades. Science 336, 589–592 (2012).
Loreau, M. & Hector, A. Partitioning selection and complementarity in biodiversity experiments. Nature 412, 72–76 (2001).
Allan, E. et al. More diverse plant communities have higher functioning over time due to turnover in complementary dominant species. Proc. Natl Acad. Sci. USA 108, 17034–17039 (2011).
Isbell, F. et al. High plant diversity is needed to maintain ecosystem services. Nature 477, 199–202 (2011).
Turnbull, L. A., Isbell, F., Purves, D. W., Loreau, M. & Hector, A. Understanding the value of plant diversity for ecosystem functioning through niche theory. Proc. R. Soc. B 283, 20160536 (2016).
Edwards, E. J., Osborne, C. P., Strömberg, C. A. E. & Smith, S. A. The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science 328, 587–591 (2010).
Bartlett, M. K., Scoffoni, C. & Sack, L. The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta-analysis. Ecol. Lett. 15, 393–405 (2012).
Schroeder‐Georgi, T. et al. From pots to plots: hierarchical trait‐based prediction of plant performance in a mesic grassland. J. Ecol. 104, 206–218 (2016).
Iversen, C. M. et al. A global fine-root ecology database to address below-ground challenges in plant ecology. New Phytol. 215, 15–26 (2017).
Aubin, I. et al. Traits to stay, traits to move: a review of functional traits to assess sensitivity and adaptive capacity of temperate and boreal trees to climate change. Environ. Rev. 24, 164–186 (2016).
Hoover, D. L., Duniway, M. C. & Belnap, J. Pulse-drought atop press-drought: unexpected plant responses and implications for dryland ecosystems. Oecologia 179, 1211–1221 (2015).
Shi, Z. et al. Dual mechanisms regulate ecosystem stability under decade-long warming and hay harvest. Nat. Commun. 7, 11973 (2016).
Mitchell, C. E., Tilman, D. & Groth, J. V. Effects of grassland plant species diversity, abundance, and composition on foliar fungal disease. Ecology 83, 1713–1726 (2002).
Wilsey, B. J. & Polley, H. W. Realistically low species evenness does not alter grassland species–richness–productivity relationships. Ecology 85, 2693–2700 (2004).
Wilsey, B. J., Teaschner, T. B., Daneshgar, P. P., Isbell, F. I. & Polley, H. W. Biodiversity maintenance mechanisms differ between native and novel exotic-dominated communities. Ecol. Lett. 12, 432–442 (2009).
Hallett, L. M. et al. Biotic mechanisms of community stability shift along a precipitation gradient. Ecology 95, 1693–1700 (2014).
Guerrero-Ramírez, N. R. et al. Diversity-dependent temporal divergence of ecosystem functioning in experimental ecosystems. Nat. Ecol. Evol. 1, 1639–1642 (2017).
Craine, J. M. et al. Timing of climate variability and grassland productivity. Proc. Natl Acad. Sci. USA 109, 3401–3405 (2012).
Stuart-Haëntjens, E. et al. Mean annual precipitation predicts primary production resistance and resilience to extreme drought. Sci. Total Environ. 636, 360–366 (2018).
Xu, Z. et al. Environmental changes drive the temporal stability of semi-arid natural grasslands through altering species asynchrony. J. Ecol. 103, 1308–1316 (2015).
Yang, Z. et al. Daytime warming lowers community temporal stability by reducing the abundance of dominant, stable species. Glob. Change Biol. 23, 154–163 (2017).
Craven, D. et al. Plant diversity effects on grassland productivity are robust to both nutrient enrichment and drought. Phil. Trans. R. Soc. B 371, 20150277 (2016).
Isbell, F. et al. Linking the influence and dependence of people on biodiversity across scales. Nature 546, 65–72 (2017).
Borer, E. T. et al. Finding generality in ecology: a model for globally distributed experiments. Methods Ecol. Evol. 5, 65–73 (2014).
Eisenhauer, N. et al. Biodiversity–ecosystem function experiments reveal the mechanisms underlying the consequences of biodiversity change in real world ecosystems. J. Veg. Sci. 27, 1061–1070 (2016).
Goodess, C. M. How is the frequency, location and severity of extreme events likely to change up to 2060?. Environ. Sci. Policy 27, S4–S14 (2013).
Stott, P. How climate change affects extreme weather events. Science 352, 1517–1518 (2016).
Boyle, B. et al. The taxonomic name resolution service: an online tool for automated standardization of plant names. BMC Bioinform. 14, 16 (2013).
Loreau, M. & de Mazancourt, C. Species synchrony and its drivers: neutral and nonneutral community dynamics in fluctuating environments. Am. Nat. 172, E48–E66 (2008).
Kattge, J. et al. TRY - a global database of plant traits. Glob. Change Biol. 17, 2905–2935 (2011).
Grime, J. P. Plant strategy theories: a comment on Craine (2005). J. Ecol. 95, 227–230 (2007).
Wacker, L., Baudois, O., Eichenberger-Glinz, S. & Schmid, B. Diversity effects in early- and mid-successional species pools along a nitrogen gradient. Ecology 90, 637–648 (2009).
Roscher, C. et al. Using plant functional traits to explain diversity–productivity relationships. PLoS ONE 7, e36760 (2012).
Daneshgar, P. P., Polley, H. W. & Wilsey, B. J. Simple plant traits explain functional group diversity decline in novel grassland communities of Texas. Plant Ecol. 214, 231–241 (2013).
Roscher, C.et al. Origin context of trait data matters for predictions of community performance in a grassland biodiversity experiment. Ecology 99, 1214–1226 2018).
Kazakou, E. et al. Are trait-based species rankings consistent across data sets and spatial scales?. J. Veg. Sci. 25, 235–247 (2014).
Siefert, A. et al. A global meta-analysis of the relative extent of intraspecific trait variation in plant communities. Ecol. Lett. 18, 1406–1419 (2015).
Lê, S. et al. FactoMineR: an R package for multivariate analysis. J. Stat. Softw. 25, 1–18 (2008).
Laliberté, E. & Legendre, P. A distance-based framework for measuring functional diversity from multiple traits. Ecology 91, 299–305 (2010).
Zanne, A. E. et al. Three keys to the radiation of angiosperms into freezing environments. Nature 506, 89–92 (2014).
Zanne, A. et al. Data from: Three keys to the radiation of angiosperms into freezing environments (Dryad Digital Repository, 2013); https://doi.org/10.5061/dryad.63q27.2
Pearse, W. D. et al. pez: phylogenetics for the environmental sciences. Bioinformatics 31, 2888–2890 (2015).
Webb, C. O., Ackerly, D. D., McPeek, M. A. & Donoghue, M. J. Phylogenies and community ecology. Annu. Rev. Ecol. Syst. 33, 475–505 (2002).
Godoy, O., Kraft, N. J. B. & Levine, J. M. Phylogenetic relatedness and the determinants of competitive outcomes. Ecol. Lett. 17, 836–844 (2014).
Valencia-Gómez, E. et al. Functional diversity enhances the resistance of ecosystem multifunctionality to aridity in Mediterranean drylands. New Phytol. 206, 660–671 (2015).
Middleton, N. J. & Thomas, D. S. World Atlas of Desertification (United Nations Environment Programme/Edward Arnold, London, 1992).
Harris, I. C. & Jones, P. D. CRU TS4.01: Climatic Research Unit (CRU) Time-Series (TS) version 4.01 of high-resolution gridded data of month-by-month variation in climate (January 1901–December 2016). Centre for Environmental Data Analysis https://doi.org/10.5285/58a8802721c94c66ae45c3baa4d814d0 (2017).
Burnham, K. & Anderson, D. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach (Springer Science & Business Media, New York, NY, 2003).
Lefcheck, J. S. iecewiseSEM: Piecewise structural equation modelling in R for ecology, evolution, and systematics. Methods Ecol. Evol. 7, 573–579 (2016).
R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2018).
This paper is a product of the sTability group funded by sDiv (www.idiv.de/stability), the Synthesis Centre of the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig (DFG FZT 118). The Jena Experiment is funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation; FOR 1451) and the Swiss National Science Foundation. The Cedar Creek biodiversity experiments were supported by awards from the Andrew Mellon Foundation, the US National Science Foundation (NSF) Long-Term Ecological Research (grant numbers DEB-9411972, DEB-0080382, DEB-0620652 and DEB-1234162), Biocomplexity Coupled Biogeochemical Cycles (DEB-0322057), Long-Term Research in Environmental Biology (DEB-0716587, DEB-1242531) and Ecosystem Sciences (NSF DEB- 1120064) Programs, as well as the US Department of Energy Programs for Ecosystem Research (DE-FG02-96ER62291) and National Institute for Climatic Change Research (DE-FC02-06ER64158). The Texas MEND study was funded by US-NSF DEB-0639417 and USDA-NIFA-2014-67003-22067. The study has been supported by the TRY initiative on plant traits (http://www.try-db.org). TRY is currently supported by DIVERSITAS/Future Earth and the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig. V.O. received financial support from the Russian Science Foundation (14-50-00029). The authors would also like to thank J. Lefcheck for his help in revising the structural equation models.
D.C., N.E. and F.I. conceived the project. D.C., P.M., N.E., W.D.P., Y.H., C.R., F.I., A.E., J.N.G., J.H., A.J., N.L., S.T.M., J.v.R., A.W. and M.D.S. further developed the project in a workshop. N.E., C.R., F.I., M.B., C.Be., G.B., N.B., C.By., B.E.L.C., J.A.C., J.H.C.C., J.M.C., E.D.L., A.H., A.J., J.Ka., J.Kr., V.L., V.M., V.O., H.W.P., P.B.R., J.v.R., B.S., N.A.S., D.T., A.W. and B.W. contributed experimental and functional trait data. D.C. compiled data. D.C. analysed data with significant input from P.M., N.E., W.D.P. and Y.H. D.C. and P.M. wrote the first draft of the manuscript and all co-authors contributed substantially to revisions.
The authors declare no competing interests.
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Craven, D., Eisenhauer, N., Pearse, W.D. et al. Multiple facets of biodiversity drive the diversity–stability relationship. Nat Ecol Evol 2, 1579–1587 (2018). https://doi.org/10.1038/s41559-018-0647-7
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