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Research Article

Discontinuity in the responses of ecosystem processes and multifunctionality to altered soil community composition

Mark A. Bradford, Stephen A. Wood, Richard D. Bardgett, Helaina I. J. Black, Michael Bonkowski, Till Eggers, Susan J. Grayston, Ellen Kandeler, Peter Manning, Heikki Setälä, and T. Hefin Jones
  1. aSchool of Forestry and Environmental Studies, Yale University, New Haven, CT 06511;
  2. bDepartment of Ecology, Evolution, and Environmental Biology, Columbia University, New York, NY 10027;
  3. cFaculty of Life Sciences, The University of Manchester, Manchester M13 9PT, United Kingdom;
  4. dThe James Hutton Institute, Aberdeen AB15 8QH, Scotland, United Kingdom;
  5. eZoologisches Institut, University of Cologne, D-50674 Köln, Germany;
  6. fCentre for Population Biology, Department of Biological Sciences, Imperial College at Silwood Park, Berkshire SL5 7PY, United Kingdom;
  7. gDepartment of Forest Sciences, University of British Columbia, Vancouver, BC, Canada V6T 1Z4;
  8. hInstitute of Soil Science and Land Evaluation, University of Hohenheim, D-70593 Stuttgart, Germany;
  9. iInstitute of Plant Sciences, University of Bern, CH-3013 Bern, Switzerland;
  10. jDepartment of Environmental Sciences, University of Helsinki, Helsinki 00014, Finland; and
  11. kSchool of Biosciences, Cardiff University, Cardiff CF10 3AX, United Kingdom

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PNAS first published September 22, 2014; https://doi.org/10.1073/pnas.1413707111
Mark A. Bradford
aSchool of Forestry and Environmental Studies, Yale University, New Haven, CT 06511;
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  • For correspondence: mark.bradford@yale.edu
Stephen A. Wood
bDepartment of Ecology, Evolution, and Environmental Biology, Columbia University, New York, NY 10027;
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Richard D. Bardgett
cFaculty of Life Sciences, The University of Manchester, Manchester M13 9PT, United Kingdom;
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Helaina I. J. Black
dThe James Hutton Institute, Aberdeen AB15 8QH, Scotland, United Kingdom;
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Michael Bonkowski
eZoologisches Institut, University of Cologne, D-50674 Köln, Germany;
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Till Eggers
fCentre for Population Biology, Department of Biological Sciences, Imperial College at Silwood Park, Berkshire SL5 7PY, United Kingdom;
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Susan J. Grayston
gDepartment of Forest Sciences, University of British Columbia, Vancouver, BC, Canada V6T 1Z4;
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Ellen Kandeler
hInstitute of Soil Science and Land Evaluation, University of Hohenheim, D-70593 Stuttgart, Germany;
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Peter Manning
iInstitute of Plant Sciences, University of Bern, CH-3013 Bern, Switzerland;
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Heikki Setälä
jDepartment of Environmental Sciences, University of Helsinki, Helsinki 00014, Finland; and
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T. Hefin Jones
kSchool of Biosciences, Cardiff University, Cardiff CF10 3AX, United Kingdom
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  1. Edited by David Schimel, Jet Propulsion Laboratory, Pasadena, CA, and accepted by the Editorial Board August 28, 2014 (received for review July 18, 2014)

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Significance

Ecosystem functioning is more strongly affected by biodiversity loss when multiple functions are considered because different species affect different functions. To quantify these biodiversity-functioning relationships, the emerging multifunctionality framework advocates calculation of indices that aggregate responses of individual functions. Data aggregation, however, is notorious for providing misleading information by obscuring true relationships between explanatory and response variables. We test the ability of common multifunctionality indices to reveal effects on key ecosystem functions of changes in soil communities. The multifunctionality indices all decrease with soil animal loss, but the responses of individual functions diverge markedly from these aggregated metrics. Application of the multifunctionality framework for landscape provision of multiple ecosystem services should therefore emphasize understanding relationships between communities and individual functions.

Abstract

Ecosystem management policies increasingly emphasize provision of multiple, as opposed to single, ecosystem services. Management for such “multifunctionality” has stimulated research into the role that biodiversity plays in providing desired rates of multiple ecosystem processes. Positive effects of biodiversity on indices of multifunctionality are consistently found, primarily because species that are redundant for one ecosystem process under a given set of environmental conditions play a distinct role under different conditions or in the provision of another ecosystem process. Here we show that the positive effects of diversity (specifically community composition) on multifunctionality indices can also arise from a statistical fallacy analogous to Simpson’s paradox (where aggregating data obscures causal relationships). We manipulated soil faunal community composition in combination with nitrogen fertilization of model grassland ecosystems and repeatedly measured five ecosystem processes related to plant productivity, carbon storage, and nutrient turnover. We calculated three common multifunctionality indices based on these processes and found that the functional complexity of the soil communities had a consistent positive effect on the indices. However, only two of the five ecosystem processes also responded positively to increasing complexity, whereas the other three responded neutrally or negatively. Furthermore, none of the individual processes responded to both the complexity and the nitrogen manipulations in a manner consistent with the indices. Our data show that multifunctionality indices can obscure relationships that exist between communities and key ecosystem processes, leading us to question their use in advancing theoretical understanding—and in management decisions—about how biodiversity is related to the provision of multiple ecosystem services.

  • aboveground–belowground interactions
  • ecosystem functioning
  • plant-soil feedbacks
  • soil biodiversity
  • soil fauna

Footnotes

  • ↵1To whom correspondence should be addressed. Email: mark.bradford{at}yale.edu.
  • Author contributions: M.A.B., R.D.B., T.E., H.S., and T.H.J. designed research; M.A.B., R.D.B., H.I.J.B., M.B., T.E., S.J.G., E.K., P.M., and T.H.J. performed research; M.A.B., S.A.W., T.E., P.M., and T.H.J. analyzed data; and M.A.B., S.A.W., R.D.B., H.I.J.B., M.B., T.E., S.J.G., E.K., P.M., H.S., and T.H.J. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission. D.S. is a Guest Editor invited by the Editorial Board.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1413707111/-/DCSupplemental.

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Soil communities and ecosystem multifunctionality
Mark A. Bradford, Stephen A. Wood, Richard D. Bardgett, Helaina I. J. Black, Michael Bonkowski, Till Eggers, Susan J. Grayston, Ellen Kandeler, Peter Manning, Heikki Setälä, T. Hefin Jones
Proceedings of the National Academy of Sciences Sep 2014, 201413707; DOI: 10.1073/pnas.1413707111

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Soil communities and ecosystem multifunctionality
Mark A. Bradford, Stephen A. Wood, Richard D. Bardgett, Helaina I. J. Black, Michael Bonkowski, Till Eggers, Susan J. Grayston, Ellen Kandeler, Peter Manning, Heikki Setälä, T. Hefin Jones
Proceedings of the National Academy of Sciences Sep 2014, 201413707; DOI: 10.1073/pnas.1413707111
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This article has a Letter. Please see:

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Proceedings of the National Academy of Sciences: 118 (14)
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