This article has been updated

Abstract

Many experiments have shown that loss of biodiversity reduces the capacity of ecosystems to provide the multiple services on which humans depend1,2. However, experiments necessarily simplify the complexity of natural ecosystems and will normally control for other important drivers of ecosystem functioning, such as the environment or land use. In addition, existing studies typically focus on the diversity of single trophic groups, neglecting the fact that biodiversity loss occurs across many taxa3,4 and that the functional effects of any trophic group may depend on the abundance and diversity of others5,6. Here we report analysis of the relationships between the species richness and abundance of nine trophic groups, including 4,600 above- and below-ground taxa, and 14 ecosystem services and functions and with their simultaneous provision (or multifunctionality) in 150 grasslands. We show that high species richness in multiple trophic groups (multitrophic richness) had stronger positive effects on ecosystem services than richness in any individual trophic group; this includes plant species richness, the most widely used measure of biodiversity. On average, three trophic groups influenced each ecosystem service, with each trophic group influencing at least one service. Multitrophic richness was particularly beneficial for ‘regulating’ and ‘cultural’ services, and for multifunctionality, whereas a change in the total abundance of species or biomass in multiple trophic groups (the multitrophic abundance) positively affected supporting services. Multitrophic richness and abundance drove ecosystem functioning as strongly as abiotic conditions and land-use intensity, extending previous experimental results7,8 to real-world ecosystems. Primary producers, herbivorous insects and microbial decomposers seem to be particularly important drivers of ecosystem functioning, as shown by the strong and frequent positive associations of their richness or abundance with multiple ecosystem services. Our results show that multitrophic richness and abundance support ecosystem functioning, and demonstrate that a focus on single groups has led to researchers to greatly underestimate the functional importance of biodiversity.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Change history

  • 22 August 2016

    Figure 1 has been corrected to fix incorrect hatching in panels e, f, g and h.

References

  1. 1.

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

  2. 2.

    , & The functions of biological diversity in an age of extinction. Science 336, 1401–1406 (2012)

  3. 3.

    et al. Interannual variation in land-use intensity enhances grassland multidiversity. Proc. Natl Acad. Sci. USA 111, 308–313 (2014)

  4. 4.

    et al. Global effects of land use on local terrestrial biodiversity. Nature 520, 45–50 (2015)

  5. 5.

    , & Producer-decomposer co-dependency influences biodiversity effects. Nature 403, 762–764 (2000)

  6. 6.

    et al. Linking biodiversity and ecosystem services: current uncertainties and the necessary next steps. Bioscience 64, 49–57 (2014)

  7. 7.

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

  8. 8.

    , & Biodiversity impacts ecosystem productivity as much as resources, disturbance, or herbivory. Proc. Natl Acad. Sci. USA 109, 10394–10397 (2012)

  9. 9.

    , , & Environmental warming alters food-web structure and ecosystem function. Nature 402, 69–72 (1999)

  10. 10.

    et al. The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecol. Lett. 10, 522–538 (2007)

  11. 11.

    et al. The links between ecosystem multifunctionality and above- and belowground biodiversity are mediated by climate. Nat. Commun. 6, 8159 (2015)

  12. 12.

    , & Herbivore and predator diversity interactively affect ecosystem properties in an experimental marine community. Ecol. Lett. 11, 598–608 (2008)

  13. 13.

    , , , & Functional trait diversity across trophic levels determines herbivore impact on plant community biomass. Ecol. Lett. 18, 1346–1355 (2015)

  14. 14.

    et al. Consequences of biodiversity loss for litter decomposition across biomes. Nature 509, 218–221 (2014)

  15. 15.

    et al. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat. Commun. 7, 10541 (2016)

  16. 16.

    et al. Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339, 1608–1611 (2013)

  17. 17.

    , & Biodiversity regulates ecosystem predictability. Nature 390, 162–165 (1997)

  18. 18.

    Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J. Ecol. 86, 902–910 (1998)

  19. 19.

    , & Consequences of dominance: a review of evenness effects on local and regional ecosystem processes. Ecology 89, 1510–1520 (2008)

  20. 20.

    et al. Locally rare species influence grassland ecosystem multifunctionality. Phil. Trans. R. Soc. B 371, 20150269 (2016)

  21. 21.

    et al. Integrative modelling reveals mechanisms linking productivity and plant species richness. Nature 529, 390–393 (2016)

  22. 22.

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

  23. 23.

    Millennium Ecosystem Assessment. Ecosystems and Human Well-Being 1–86 World Resources Institute (2005)

  24. 24.

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

  25. 25.

    & Biodiversity and ecosystem multifunctionality. Nature 448, 188–190 (2007)

  26. 26.

    , , & Relative and interactive effects of plant and grazer richness in a benthic marine community. Ecology 89, 2518–2528 (2008)

  27. 27.

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

  28. 28.

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

  29. 29.

    , , , & Declining biodiversity can alter the performance of ecosystems. Nature 368, 734–737 (1994)

  30. 30.

    et al. Grassland management intensification weakens the associations among the diversities of multiple plant and animal taxa. Ecology 96, 1492–1501 (2015)

  31. 31.

    et al. Implementing large-scale and long-term functional biodiversity research: The Biodiversity Exploratories. Basic Appl. Ecol. 6, 473–485 (2010)

  32. 32.

    et al. A quantitative index of land-use intensity in grasslands: integrating mowing, grazing and fertilization. Basic Appl. Ecol. 13, 207–220 (2012)

  33. 33.

    , , & Sustaining multiple ecosystem functions in grassland communities requires higher biodiversity. Proc. Natl Acad. Sci. USA 107, 1443–1446 (2010)

  34. 34.

    et al. Land use intensification alters ecosystem multifunctionality via loss of biodiversity and changes to functional composition. Ecol. Lett. 18, 834–843 (2015)

  35. 35.

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

  36. 36.

    , & Multiple functions increase the importance of biodiversity for overall ecosystem functioning. Ecology 89, 1223–1231 (2008)

  37. 37.

    et al. Higher levels of multiple ecosystem services are found in forests with more tree species. Nat. Commun. 4, 1340 (2013)

  38. 38.

    et al. Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443, 989–992 (2006)

  39. 39.

    Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100, 403–405 (2003)

  40. 40.

    et al. Resource heterogeneity moderates the biodiversity-function relationship in real world ecosystems. PLoS Biol. 6, e122 (2008)

  41. 41.

    R Development Core Team. R: A Language And Environment For Statistical Computing (R Foundation For Statistical Computing, 2014)

  42. 42.

    , & Partialling out the spatial component of ecological variation. Ecology 73, 1045–1055 (1992)

  43. 43.

    , , & Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87, 2614–2625 (2006)

  44. 44.

    & eulerAPE: drawing area-proportional 3-Venn diagrams using ellipses. PLoS One 9, e101717 (2014)

  45. 45.

    & Biodiversity, productivity and stability in real food webs. Trends Ecol. Evol. 18, 628–632 (2003)

Download references

Acknowledgements

We thank B. Schmid, F. T. Maestre and S. Kéfi for comments that helped improve this manuscript. W. Ulrich and N. J. Gotelli provided statistical advice. We thank the people who maintain the Biodiversity Exploratories program: A. Hemp, K. Wells, S. Gockel, K. Wiesner and M. Gorke (local management team); S. Pfeiffer and C. Fischer (central office), B. König-Ries and M. Owonibi (central database management); and E. Linsenmair, D. Hessenmöller, J. Nieschulze, E.-D. Schulze and the late E. Kalko for their role in setting up the project. This work was funded by the Deutsche Forschungsgemeinschaft Priority Program 1374 ‘Infrastructure-Biodiversity Exploratories’. Fieldwork permits were given by the responsible state environmental offices of Baden-Württemberg, Thüringen and Brandenburg (according to §72 BbgNatSchG). Figure icons were created by R. D. Manzanedo.

Author information

Affiliations

  1. Institute of Plant Sciences, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland

    • Santiago Soliveres
    • , Fons van der Plas
    • , Peter Manning
    • , Daniel Prati
    • , Stefan Blaser
    • , Steffen Boch
    • , Barbara Schmitt
    • , Markus Fischer
    •  & Eric Allan
  2. Senckenberg Gesellschaft für Naturforschung, Biodiversity and Climate Research Centre BIK-F, Senckenberganlage 25, 60325 Frankfurt, Germany

    • Fons van der Plas
    • , Peter Manning
    •  & Markus Fischer
  3. Institute of Ecology, Friedrich-Schiller-University Jena, Dornburger Straße 159, D-07743 Jena, Germany

    • Martin M. Gossner
    • , Markus Lange
    • , Esther Pašalić
    • , Ingo Schöning
    • , Manfred Türke
    •  & Wolfgang W. Weisser
  4. Technische Universität München, Terrestrial Ecology Research Group, Department of Ecology and Ecosystem Management, School of Life Sciences Weihenstephan, Hans-Carl-von-Carlowitz-Platz 2, 85354 Freising, Germany

    • Martin M. Gossner
    • , Markus Lange
    • , Esther Pašalić
    • , Manfred Türke
    •  & Wolfgang W. Weisser
  5. Institute of Zoology, University of Natural Resources and Life Science, Gregor-Mendel-Straße 33, 1180 Vienna, Austria

    • Swen C. Renner
    •  & Stefan Böhm
  6. Smithsonian Conservation Biology Institute, National Zoological Park, 1500 Remount Road, Front Royal, Virginia 22630, USA

    • Swen C. Renner
  7. Geocology, University of Tuebingen, Ruemelinstr. 19-23, 72070 Tuebingen, Germany

    • Fabian Alt
    • , Yvonne Oelmann
    •  & Elisabeth Sorkau
  8. University of Cologne, Institute for Zoology, Zülpicher Str. 47b, 50674 Cologne, Germany

    • Hartmut Arndt
    •  & Paul C. Venter
  9. Leibniz Institute DSMZ German Collection of Microorganisms and Cell Cultures, Inhoffenstr. 7B, 38124 Braunschweig, Germany

    • Vanessa Baumgartner
    • , Jörg Overmann
    •  & Johannes Sikorski
  10. Chair of Nature Conservation and Landscape Ecology, Faculty of Environment and Natural Resources, University of Freiburg, Tennenbacher Straße 4, 79106 Freiburg, Germany

    • Julia Binkenstein
  11. Department of Biology, Lund University, Sölvegatan 35, 22362 Lund, Germany

    • Klaus Birkhofer
  12. Ecological Networks, Biology, Technische Universität Darmstadt, Schnittspahnstr. 3, 64287 Darmstadt, Germany

    • Nico Blüthgen
    •  & Christiane N. Weiner
  13. Botanical Garden, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland

    • Steffen Boch
    •  & Markus Fischer
  14. Agroecology, Department of Crop Sciences, Georg-August University of Göttingen, Grisebachstr. 6, D-37077, Göttingen, Germany

    • Carmen Börschig
    •  & Catrin Westphal
  15. UFZ-Helmholtz Centre for Environmental Research, Department of Soil Ecology, Theodor-Lieser-Straße 4, 06120 Halle (Saale), Germany

    • Francois Buscot
    • , Sandra Klemmer
    •  & Tesfaye Wubet
  16. German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, D-04103 Leipzig, Germany

    • Francois Buscot
    • , Manfred Türke
    •  & Tesfaye Wubet
  17. Department of Landscape Ecology, Kiel University, Olshausenstr. 75, D-24118 Kiel, Germany

    • Tim Diekötter
  18. Biodiversity Research/Systematic Botany, University of Potsdam, Maulbeerallee 1, D-14469 Potsdam, Germany

    • Johannes Heinze
    •  & Jörg Müller
  19. Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), D-14195 Berlin, Germany

    • Johannes Heinze
    •  & Matthias C. Rillig
  20. Institute of Landscape Ecology, University of Münster, Heisenbergstr. 2, 48149 Münster, Germany

    • Norbert Hölzel
    • , Valentin H. Klaus
    •  & Till Kleinebecker
  21. Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Albert-Einstein-Allee 11, 89069 Ulm, Germany

    • Kirsten Jung
    •  & Marco Tschapka
  22. Department of Animal Ecology and Tropical Biology, Biocentre, University of Würzburg, Am Hubland, D-97074 Würzburg, Germany

    • Jochen Krauss
    • , Juliane Steckel
    • , Ingolf Steffan-Dewenter
    •  & Michael Werner
  23. Max-Planck Institute for Biogeochemistry, Hans-Knoell-Str. 10, 07745 Jena, Germany

    • Markus Lange
    • , Ingo Schöning
    • , Marion Schrumpf
    •  & Emily F. Solly
  24. Xavier University, Department of Biology, 3800 Victory Parkway, Cincinnati, Ohio 45207, USA

    • E. Kathryn Morris
  25. Plant Ecology, Institut für Biologie, Freie Universität Berlin, Altensteinstr. 6, D-14195 Berlin, Germany

    • E. Kathryn Morris
    •  & Matthias C. Rillig
  26. Department of Ecology and Evolutionary Biology, Faculty of Biology, University of Freiburg, Hauptstraße 1, 79104 Freiburg i. Br., Germany

    • H. Martin Schaefer
  27. Research Unit for Environmental Genomics; Helmholtz Zentrum München, Ingolstädter Landstr. 1, 85758 Oberschleissheim, Germany

    • Michael Schloter
    •  & Barbara Stempfhuber
  28. Department of Ecology and Evolution, Universität Salzburg, Hellbrunnerstrasse 34, 5020 Salzburg, Austria

    • Stephanie A. Socher
  29. Swiss Federal Institute for Forest, Snow and Landscape Research WSL, Zürcherstrasse 111, 8903 Birmensdorf, Switzerland

    • Emily F. Solly
  30. Functional Biodiversity, Institute of Biology, Freie Universität Berlin. Königin-Luise-Str. 1-3. D-14195 Berlin, Germany

    • Ilja Sonnemann
    •  & Susanne Wurst
  31. Smithsonian Tropical Research Institute, Balboa, Panama

    • Marco Tschapka
  32. Institute for Biology, Leipzig University, Johannisallee 21, D-04103 Leipzig, Germany

    • Manfred Türke
  33. Institute of Geography and Geoecology, Karlsruhe Institute of Technology (KIT), Reinhard-Baumeister-Platz 1, 76131 Karlsruhe, Germany

    • Wolfgang Wilcke
  34. Department of Animal Ecology, Justus Liebig University Giessen, Heinrich-Buff-Ring 26-32, D-35392 Giessen, Germany

    • Volkmar Wolters
  35. Centre for Development and Environment, University of Bern, Hallerstrasse, 10, 3012 Bern, Switzerland

    • Eric Allan

Authors

  1. Search for Santiago Soliveres in:

  2. Search for Fons van der Plas in:

  3. Search for Peter Manning in:

  4. Search for Daniel Prati in:

  5. Search for Martin M. Gossner in:

  6. Search for Swen C. Renner in:

  7. Search for Fabian Alt in:

  8. Search for Hartmut Arndt in:

  9. Search for Vanessa Baumgartner in:

  10. Search for Julia Binkenstein in:

  11. Search for Klaus Birkhofer in:

  12. Search for Stefan Blaser in:

  13. Search for Nico Blüthgen in:

  14. Search for Steffen Boch in:

  15. Search for Stefan Böhm in:

  16. Search for Carmen Börschig in:

  17. Search for Francois Buscot in:

  18. Search for Tim Diekötter in:

  19. Search for Johannes Heinze in:

  20. Search for Norbert Hölzel in:

  21. Search for Kirsten Jung in:

  22. Search for Valentin H. Klaus in:

  23. Search for Till Kleinebecker in:

  24. Search for Sandra Klemmer in:

  25. Search for Jochen Krauss in:

  26. Search for Markus Lange in:

  27. Search for E. Kathryn Morris in:

  28. Search for Jörg Müller in:

  29. Search for Yvonne Oelmann in:

  30. Search for Jörg Overmann in:

  31. Search for Esther Pašalić in:

  32. Search for Matthias C. Rillig in:

  33. Search for H. Martin Schaefer in:

  34. Search for Michael Schloter in:

  35. Search for Barbara Schmitt in:

  36. Search for Ingo Schöning in:

  37. Search for Marion Schrumpf in:

  38. Search for Johannes Sikorski in:

  39. Search for Stephanie A. Socher in:

  40. Search for Emily F. Solly in:

  41. Search for Ilja Sonnemann in:

  42. Search for Elisabeth Sorkau in:

  43. Search for Juliane Steckel in:

  44. Search for Ingolf Steffan-Dewenter in:

  45. Search for Barbara Stempfhuber in:

  46. Search for Marco Tschapka in:

  47. Search for Manfred Türke in:

  48. Search for Paul C. Venter in:

  49. Search for Christiane N. Weiner in:

  50. Search for Wolfgang W. Weisser in:

  51. Search for Michael Werner in:

  52. Search for Catrin Westphal in:

  53. Search for Wolfgang Wilcke in:

  54. Search for Volkmar Wolters in:

  55. Search for Tesfaye Wubet in:

  56. Search for Susanne Wurst in:

  57. Search for Markus Fischer in:

  58. Search for Eric Allan in:

Contributions

S.S. and E.A. conceived the idea of this study. M.F. initiated the Biodiversity Exploratories project aimed at measuring multiple diversities and functions in the field sites. All authors but S.S., E.A. and F.V.D.P. contributed data. S.S. and F.V.D.P. performed the analyses. S.S. and S.C.R. performed the literature search. S.S. wrote the first draft of the manuscript and all the authors (especially E.A., P.M., F.D.V.P., M.M.G. and D.P.) contributed substantially to the revisions.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Santiago Soliveres.

Reviewer Information

Nature thanks Y. Hautier, F. Isbell and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Extended data

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature19092

Further reading

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.