Understanding how loss of biodiversity affects ecosystem functioning, and thus the delivery of ecosystem goods and services, has become increasingly necessary in a changing world. Considerable recent attention has focused on predicting how biodiversity loss simultaneously impacts multiple ecosystem functions (that is, ecosystem multifunctionality), but the ways in which these effects vary across ecosystems remain unclear. Here, we report the results of two 19-year plant diversity manipulation experiments, each established across a strong environmental gradient. Although the effects of plant and associated fungal diversity loss on individual functions frequently differed among ecosystems, the consequences of biodiversity loss for multifunctionality were relatively invariant. However, the context-dependency of biodiversity effects also worked in opposing directions for different individual functions, meaning that similar multifunctionality values across contrasting ecosystems could potentially mask important differences in the effects of biodiversity on functioning among ecosystems. Our findings highlight that an understanding of the relative contribution of species or functional groups to individual ecosystem functions among contrasting ecosystems and their interactions (that is, complementarity versus competition) is critical for guiding management efforts aimed at maintaining ecosystem multifunctionality and the delivery of multiple ecosystem services.
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Duraiappah, A. K. et al. Ecosystems and Human Well-Being: Biodiversity Synthesis (World Resources Institute, Washington DC, 2005).
Isbell, F. et al. High plant diversity is needed to maintain ecosystem services. Nature 477, 199–202 (2011).
Cardinale, B. J. et al. Biodiversity loss and its impact on humanity. Nature 486, 59–67 (2012).
Emmett Duffy, J., Paul Richardson, J. & Canuel, E. A. Grazer diversity effects on ecosystem functioning in seagrass beds. Ecol. Lett. 6, 637–645 (2003).
Hector, A. & Bagchi, R. Biodiversity and ecosystem multifunctionality. Nature 448, 188–190 (2007).
Mori, A. S. et al. Low multifunctional redundancy of soil fungal diversity at multiple scales. Ecol. Lett. 19, 249–259 (2016).
Gamfeldt, L. & Roger, F. Revisiting the biodiversity–ecosystem multifunctionality relationship. Nat. Ecol. Evol. 1, 0168 (2017).
Byrnes, J. E. et al. Investigating the relationship between biodiversity and ecosystem multifunctionality: challenges and solutions. Methods Ecol. Evol. 5, 111–124 (2014).
Lefcheck, J. S. et al. Biodiversity enhances ecosystem multifunctionality across trophic levels and habitats. Nat. Commun. 6, 6936 (2015).
Loreau, M. & Hector, A. Partitioning selection and complementarity in biodiversity experiments. Nature 412, 72–76 (2001).
Hooper, D. U. et al. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol. Monogr. 75, 3–35 (2005).
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).
Symstad, A. J. & Tilman, D. Diversity loss, recruitment limitation, and ecosystem functioning: lessons learned from a removal experiment. Oikos 92, 424–435 (2001).
Flombaum, P. & Sala, O. E. Higher effect of plant species diversity on productivity in natural than artificial ecosystems. Proc. Natl Acad. Sci. USA 105, 6087–6090 (2008).
Tilman, D. et al. Diversity and productivity in a long-term grassland experiment. Science 294, 843–845 (2001).
Reich, P. B. et al. Impacts of biodiversity loss escalate through time as redundancy fades. Science 336, 589–592 (2012).
Wardle, D. A. Do experiments exploring plant diversity–ecosystem functioning relationships inform how biodiversity loss impacts natural ecosystems? J. Veg. Sci. 27, 646–653 (2016).
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).
Allan, E. et al. Land use intensification alters ecosystem multifunctionality via loss of biodiversity and changes to functional composition. Ecol. Lett. 18, 834–843 (2015).
Van der Plas, F. et al. Biotic homogenization can decrease landscape-scale forest multifunctionality. Proc. Natl Acad. Sci. USA 113, 3557–3562 (2016).
Gross, N. et al. Functional trait diversity maximizes ecosystem multifunctionality. Nat. Ecol. Evol. 1, 0132 (2017).
Ratcliffe, S. et al. Biodiversity and ecosystem functioning relations in European forests depend on environmental context. Ecol. Lett. 20, 1414–1426 (2017).
Wardle, D. A. & Zackrisson, O. Effects of species and functional group loss on island ecosystem properties. Nature 435, 806–810 (2005).
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).
Handa, I. T. et al. Consequences of biodiversity loss for litter decomposition across biomes. Nature 509, 218–221 (2014).
Zavaleta, E. S., Pasari, J. R., Hulvey, K. B. & Tilman, G. D. Sustaining multiple ecosystem functions in grassland communities requires higher biodiversity. Proc. Natl Acad. Sci. USA 107, 1443–1446 (2010).
Maestre, F. T. et al. Plant species richness and ecosystem multifunctionality in global drylands. Science 335, 214–218 (2012).
Bradford, M. A. et al. Discontinuity in the responses of ecosystem processes and multifunctionality to altered soil community composition. Proc. Natl Acad. Sci. USA 111, 14478–14483 (2014).
Delgado-Baquerizo, M. et al. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat. Commun. 7, 10541 (2016).
Soliveres, S. et al. Biodiversity at multiple trophic levels is needed for ecosystem multifunctionality. Nature 536, 456–459 (2016).
Clemmensen, K. et al. Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339, 1615–1618 (2013).
Clemmensen, K. E. et al. Carbon sequestration is related to mycorrhizal fungal community shifts during long‐term succession in boreal forests. New Phytol. 205, 1525–1536 (2015).
Averill, C. & Hawkes, C. V. Ectomycorrhizal fungi slow soil carbon cycling. Ecol. Lett. 19, 937–947 (2016).
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).
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).
Van der Plas, F. et al. Jack-of-all-trades effects drive biodiversity–ecosystem multifunctionality relationships in European forests. Nat. Commun. 7, 11109 (2016).
Leibold, M. A., Chase, J. M. & Ernest, S. Community assembly and the functioning of ecosystems: how metacommunity processes alter ecosystems attributes. Ecology 98, 909–919 (2017).
Isbell, F. et al. Biodiversity increases the resistance of ecosystem productivity to climate extremes. Nature 526, 574–577 (2015).
Meyer, S. T. et al. Biodiversity–multifunctionality relationships depend on identity and number of measured functions. Nat. Ecol. Evol. https://doi.org/10.1038/s41559-017-0391-4 (2017).
Chesson, P. Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst. 31, 343–366 (2000).
HilleRisLambers, J., Adler, P., Harpole, W., Levine, J. & Mayfield, M. Rethinking community assembly through the lens of coexistence theory. Annu. Rev. Ecol. Evol. Syst. 43, 227–248 (2012).
Kumordzi, B. B. et al. Linkage of plant trait space to successional age and species richness in boreal forest understorey vegetation. J. Ecol. 103, 1610–1620 (2015).
Scherber, C. et al. Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment. Nature 468, 553–556 (2010).
Kardol, P., Spitzer, C. M., Gundale, M. J., Nilsson, M. C. & Wardle, D. A. Trophic cascades in the bryosphere: the impact of global change factors on top‐down control of cyanobacterial N2‐fixation. Ecol. Lett. 19, 967–976 (2016).
Duffy, J. E. et al. The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecol. Lett. 10, 522–538 (2007).
Jing, X. et al. The links between ecosystem multifunctionality and above- and belowground biodiversity are mediated by climate. Nat. Commun. 6, 8159 (2015).
Taylor, D. L. et al. A first comprehensive census of fungi in soil reveals both hyperdiversity and fine‐scale niche partitioning. Ecol. Monogr. 84, 3–20 (2014).
Tiunov, A. V. & Scheu, S. Facilitative interactions rather than resource partitioning drive diversity‐functioning relationships in laboratory fungal communities. Ecol. Lett. 8, 618–625 (2005).
Hooper, D. U. et al. A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486, 105–108 (2012).
Isbell, F. et al. Linking the influence and dependence of people on biodiversity across scales. Nature 546, 65–72 (2017).
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).
Wardle, D. A., Zackrisson, O., Hörnberg, G. & Gallet, C. The influence of island area on ecosystem properties. Science 277, 1296–1299 (1997).
Lagerström, A., Nilsson, M. C., Zackrisson, O. & Wardle, D. Ecosystem input of nitrogen through biological fixation in feather mosses during ecosystem retrogression. Funct. Ecol. 21, 1027–1033 (2007).
Nilsson, M.-C. & Wardle, D. A. Understory vegetation as a forest ecosystem driver: evidence from the northern Swedish boreal forest. Front. Ecol. Environ. 3, 421–428 (2005).
Peltzer, D. A. et al. Understanding ecosystem retrogression. Ecol. Monogr. 80, 509–529 (2010).
Dıaz, 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).
Bardgett, R. D. & Wardle, D. A. Aboveground-Belowground Linkages: Biotic Interactions, Ecosystem Processes, and Global Change (Oxford Univ. Press, Oxford, 2010).
Wardle, D. A. et al. Ecological linkages between aboveground and belowground biota. Science 304, 1629–1633 (2004).
Wall, D. H. et al. Soil Ecology and Ecosystem Services (Oxford Univ. Press, Oxford, 2012).
Bardgett, R. D. & van der Putten, W. H. Belowground biodiversity and ecosystem functioning. Nature 515, 505–511 (2014).
Pasari, J. R., Levi, T., Zavaleta, E. S. & Tilman, D. Several scales of biodiversity affect ecosystem multifunctionality. Proc. Natl Acad. Sci. USA 110, 10219–10222 (2013).
Mouillot, D., Villéger, S., Scherer-Lorenzen, M. & Mason, N. W. Functional structure of biological communities predicts ecosystem multifunctionality. PLoS ONE 6, e17476 (2011).
Maestre, F. T., Castillo‐Monroy, A. P., Bowker, M. A. & Ochoa‐Hueso, R. Species richness effects on ecosystem multifunctionality depend on evenness, composition and spatial pattern. J. Ecol. 100, 317–330 (2012).
Hoaglin, D. C. & Iglewicz, B. Fine-tuning some resistant rules for outlier labeling. J. Am. Stat. Assoc. 82, 1147–1149 (1987).
Gotelli, N. J. & Colwell, R. K. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol. Lett. 4, 379–391 (2001).
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-Seq data with DESeq2. Genome Biol. 15, 550 (2014).
Witten, D. M. Classification and clustering of sequencing data using a Poisson model. Ann. Appl. Stat. 5, 2493–2518 (2011).
Verhoeven, K. J., Simonsen, K. L. & McIntyre, L. M. Implementing false discovery rate control: increasing your power. Oikos 108, 643–647 (2005).
Boström, B., Comstedt, D. & Ekblad, A. Isotope fractionation and 13C enrichment in soil profiles during the decomposition of soil organic matter. Oecologia 153, 89–98 (2007).
Hobbie, E. A. & Ouimette, A. P. Controls of nitrogen isotope patterns in soil profiles. Biogeochemistry 95, 355–371 (2009).
Gamfeldt, L. et al. Higher levels of multiple ecosystem services are found in forests with more tree species. Nat. Commun. 4, 1340 (2013).
Tremblay, A. & Ransijn, J. Model Selection and Post-Hoc Analysis for (G)LMER Models (R Foundation for Statistical Computing, Vienna, 2012).
We thank numerous assistants for help in the field and laboratory. We also thank B. Lindahl and K. Clemmensen for guidance on the fungal component of the work and helpful comments on earlier versions of the manuscript. This work was supported by grants to D.A.W. from the Swedish Research Council (Vetenskapsrådet) and a Wallenberg Scholars award.
The authors declare no competing financial interests.
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Fanin, N., Gundale, M.J., Farrell, M. et al. Consistent effects of biodiversity loss on multifunctionality across contrasting ecosystems. Nat Ecol Evol 2, 269–278 (2018). https://doi.org/10.1038/s41559-017-0415-0
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