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Research Article

Functional rarity and evenness are key facets of biodiversity to boost multifunctionality

Yoann Le Bagousse-Pinguet, View ORCID ProfileNicolas Gross, View ORCID ProfileHugo Saiz, Fernando T. Maestre, Sonia Ruiz, View ORCID ProfileMarina Dacal, View ORCID ProfileSergio Asensio, View ORCID ProfileVictoria Ochoa, View ORCID ProfileBeatriz Gozalo, View ORCID ProfileJohannes H. C. Cornelissen, View ORCID ProfileLucas Deschamps, View ORCID ProfileCarlos García, Vincent Maire, View ORCID ProfileRubén Milla, View ORCID ProfileNorma Salinas, View ORCID ProfileJuntao Wang, View ORCID ProfileBrajesh K. Singh, and View ORCID ProfilePablo García-Palacios
  1. aAix Marseille Univ, CNRS, Avignon Université, Institut de Recherche pour le Développement (IRD), Institut Méditerranéen de la Biodiversité et d’Ecologie marine et continentale (IMBE), Technopôle Arbois-Méditerranée Bât. Villemin – BP 80, F-13545 Aix-en-Provence cedex 04, France;
  2. bDepartamento de Biología y Geología, Física y Química Inorgánica y Analítica, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos, 28933 Móstoles, Spain;
  3. cUniversité Clermont-Auvergne, Institut national de recherche pour l’agriculture, l’alimentation et l’environnement (INRAE), VetAgro Sup, UMR Ecosystème Prairial, 63000 Clermont-Ferrand, France;
  4. dInstitute of Plant Sciences, University of Bern, 3013 Bern, Switzerland;
  5. eDepartamento de Ecología, Universidad de Alicante, Carretera de San Vicente del Raspeig s/n, 03690 San Vicente del Raspeig, Alicante, Spain;
  6. fInstituto Multidisciplinar para el Estudio del Medio “Ramón Margalef”, Universidad de Alicante, Carretera de San Vicente del Raspeig s/n, 03690 San Vicente del Raspeig, Alicante, Spain;
  7. gSystems Ecology, Department of Ecological Science, Vrije Universiteit, 1081 HV Amsterdam, The Netherlands;
  8. hDépartement des sciences de l’environnement, Université du Quebec à Trois-Rivières, 3351, boul. des Forges, Trois-Rivières, QC G8Z 4M3, Canada;
  9. iCentro de Edafología y Biología Aplicada del Segura, Consejo Superior de Investigaciones Científicas, Campus Universitario de Espinardo, 30100, Murcia, Spain;
  10. jInstitute for the Sciences of Nature, Earth, and Energy (INTE-PUCP), Pontifical Catholic University of Peru, Lima 15088, Peru;
  11. kHawkesbury Institute for the Environment, Western Sydney University, Penrith, NSW 2751, Australia;
  12. lGlobal Centre for Land-Based Innovation, Western Sydney University, Penrith South DC, NSW 2751, Australia;
  13. mInstituto de Ciencias Agrarias, Consejo Superior de Investigaciones Científicas, 28006 Madrid, Spain

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PNAS February 16, 2021 118 (7) e2019355118; https://doi.org/10.1073/pnas.2019355118
Yoann Le Bagousse-Pinguet
aAix Marseille Univ, CNRS, Avignon Université, Institut de Recherche pour le Développement (IRD), Institut Méditerranéen de la Biodiversité et d’Ecologie marine et continentale (IMBE), Technopôle Arbois-Méditerranée Bât. Villemin – BP 80, F-13545 Aix-en-Provence cedex 04, France;
bDepartamento de Biología y Geología, Física y Química Inorgánica y Analítica, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos, 28933 Móstoles, Spain;
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  • For correspondence: yoann.pinguet@imbe.fr pablo.garcia@ica.csic.es
Nicolas Gross
bDepartamento de Biología y Geología, Física y Química Inorgánica y Analítica, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos, 28933 Móstoles, Spain;
cUniversité Clermont-Auvergne, Institut national de recherche pour l’agriculture, l’alimentation et l’environnement (INRAE), VetAgro Sup, UMR Ecosystème Prairial, 63000 Clermont-Ferrand, France;
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Hugo Saiz
bDepartamento de Biología y Geología, Física y Química Inorgánica y Analítica, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos, 28933 Móstoles, Spain;
dInstitute of Plant Sciences, University of Bern, 3013 Bern, Switzerland;
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Fernando T. Maestre
eDepartamento de Ecología, Universidad de Alicante, Carretera de San Vicente del Raspeig s/n, 03690 San Vicente del Raspeig, Alicante, Spain;
fInstituto Multidisciplinar para el Estudio del Medio “Ramón Margalef”, Universidad de Alicante, Carretera de San Vicente del Raspeig s/n, 03690 San Vicente del Raspeig, Alicante, Spain;
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Sonia Ruiz
bDepartamento de Biología y Geología, Física y Química Inorgánica y Analítica, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos, 28933 Móstoles, Spain;
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Marina Dacal
bDepartamento de Biología y Geología, Física y Química Inorgánica y Analítica, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos, 28933 Móstoles, Spain;
fInstituto Multidisciplinar para el Estudio del Medio “Ramón Margalef”, Universidad de Alicante, Carretera de San Vicente del Raspeig s/n, 03690 San Vicente del Raspeig, Alicante, Spain;
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  • ORCID record for Marina Dacal
Sergio Asensio
fInstituto Multidisciplinar para el Estudio del Medio “Ramón Margalef”, Universidad de Alicante, Carretera de San Vicente del Raspeig s/n, 03690 San Vicente del Raspeig, Alicante, Spain;
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Victoria Ochoa
fInstituto Multidisciplinar para el Estudio del Medio “Ramón Margalef”, Universidad de Alicante, Carretera de San Vicente del Raspeig s/n, 03690 San Vicente del Raspeig, Alicante, Spain;
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  • ORCID record for Victoria Ochoa
Beatriz Gozalo
fInstituto Multidisciplinar para el Estudio del Medio “Ramón Margalef”, Universidad de Alicante, Carretera de San Vicente del Raspeig s/n, 03690 San Vicente del Raspeig, Alicante, Spain;
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Johannes H. C. Cornelissen
gSystems Ecology, Department of Ecological Science, Vrije Universiteit, 1081 HV Amsterdam, The Netherlands;
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  • ORCID record for Johannes H. C. Cornelissen
Lucas Deschamps
hDépartement des sciences de l’environnement, Université du Quebec à Trois-Rivières, 3351, boul. des Forges, Trois-Rivières, QC G8Z 4M3, Canada;
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Carlos García
iCentro de Edafología y Biología Aplicada del Segura, Consejo Superior de Investigaciones Científicas, Campus Universitario de Espinardo, 30100, Murcia, Spain;
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Vincent Maire
hDépartement des sciences de l’environnement, Université du Quebec à Trois-Rivières, 3351, boul. des Forges, Trois-Rivières, QC G8Z 4M3, Canada;
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Rubén Milla
bDepartamento de Biología y Geología, Física y Química Inorgánica y Analítica, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos, 28933 Móstoles, Spain;
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Norma Salinas
jInstitute for the Sciences of Nature, Earth, and Energy (INTE-PUCP), Pontifical Catholic University of Peru, Lima 15088, Peru;
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Juntao Wang
kHawkesbury Institute for the Environment, Western Sydney University, Penrith, NSW 2751, Australia;
lGlobal Centre for Land-Based Innovation, Western Sydney University, Penrith South DC, NSW 2751, Australia;
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Brajesh K. Singh
kHawkesbury Institute for the Environment, Western Sydney University, Penrith, NSW 2751, Australia;
lGlobal Centre for Land-Based Innovation, Western Sydney University, Penrith South DC, NSW 2751, Australia;
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Pablo García-Palacios
bDepartamento de Biología y Geología, Física y Química Inorgánica y Analítica, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos, 28933 Móstoles, Spain;
mInstituto de Ciencias Agrarias, Consejo Superior de Investigaciones Científicas, 28006 Madrid, Spain
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  • For correspondence: yoann.pinguet@imbe.fr pablo.garcia@ica.csic.es
  1. Edited by Nils Chr. Stenseth, University of Oslo, Oslo, Norway, and approved January 15, 2021 (received for review September 14, 2020)

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Significance

Identifying species assemblages that boost the provision of multiple ecosystem functions simultaneously (multifunctionality) is crucial to undertake effective restoration actions aiming at simultaneously promoting biodiversity and high multifunctionality in a changing world. By disentangling the effect of multiple traits on multifunctionality in a litter decomposition experiment, we show that it is possible to identify the assemblages that boost multifunctionality across multiple species mixtures originating from six biomes. We found that higher evenness among dissimilar species and the functional attributes of rare species as key biodiversity attributes to enhance multifunctionality and to reduce the abundance of plant pathogens. Our study identifies those species assemblages needed to simultaneously maximize multifunctionality and limit plant disease risks in natural and managed ecosystems.

Abstract

The functional traits of organisms within multispecies assemblages regulate biodiversity effects on ecosystem functioning. Yet how traits should assemble to boost multiple ecosystem functions simultaneously (multifunctionality) remains poorly explored. In a multibiome litter experiment covering most of the global variation in leaf trait spectra, we showed that three dimensions of functional diversity (dispersion, rarity, and evenness) explained up to 66% of variations in multifunctionality, although the dominant species and their traits remained an important predictor. While high dispersion impeded multifunctionality, increasing the evenness among functionally dissimilar species was a key dimension to promote higher multifunctionality and to reduce the abundance of plant pathogens. Because too-dissimilar species could have negative effects on ecosystems, our results highlight the need for not only diverse but also functionally even assemblages to promote multifunctionality. The effect of functionally rare species strongly shifted from positive to negative depending on their trait differences with the dominant species. Simultaneously managing the dispersion, evenness, and rarity in multispecies assemblages could be used to design assemblages aimed at maximizing multifunctionality independently of the biome, the identity of dominant species, or the range of trait values considered. Functional evenness and rarity offer promise to improve the management of terrestrial ecosystems and to limit plant disease risks.

  • complex species assemblages
  • litter decomposition
  • nutrient cycling
  • plant pathogens
  • trait distributions

Footnotes

  • ↵1Y.L.B.-P., N.G., H.S., and P.G.-P. contributed equally to this work.

  • ↵2To whom correspondence may be addressed. Email: yoann.pinguet{at}imbe.fr or pablo.garcia{at}ica.csic.es.
  • Author contributions: Y.L.B.-P., N.G., H.S., F.T.M., and P.G.-P. designed research; Y.L.B.-P., N.G., H.S., S.R., M.D., S.A., V.O., B.G., and P.G.-P. performed research; Y.L.B.-P., N.G., H.S., J.W., and P.G.-P. analyzed data; Y.L.B.-P., N.G., H.S., F.T.M., J.H.C.C., L.D., C.G., V.M., R.M., N.S., B.K.S., and P.G.-P. wrote the paper; N.G., J.H.C.C., L.D., C.G., V.M., R.M., N.S., and P.G.-P. provided biological material; and F.T.M. provided fundings.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2019355118/-/DCSupplemental.

Data Availability.

All data and R codes are available on Figshare: https://figshare.com/s/a73f2c4106b33f32e9c0.

Published under the PNAS license.

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Functional rarity and evenness are key facets of biodiversity to boost multifunctionality
Yoann Le Bagousse-Pinguet, Nicolas Gross, Hugo Saiz, Fernando T. Maestre, Sonia Ruiz, Marina Dacal, Sergio Asensio, Victoria Ochoa, Beatriz Gozalo, Johannes H. C. Cornelissen, Lucas Deschamps, Carlos García, Vincent Maire, Rubén Milla, Norma Salinas, Juntao Wang, Brajesh K. Singh, Pablo García-Palacios
Proceedings of the National Academy of Sciences Feb 2021, 118 (7) e2019355118; DOI: 10.1073/pnas.2019355118

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Functional rarity and evenness are key facets of biodiversity to boost multifunctionality
Yoann Le Bagousse-Pinguet, Nicolas Gross, Hugo Saiz, Fernando T. Maestre, Sonia Ruiz, Marina Dacal, Sergio Asensio, Victoria Ochoa, Beatriz Gozalo, Johannes H. C. Cornelissen, Lucas Deschamps, Carlos García, Vincent Maire, Rubén Milla, Norma Salinas, Juntao Wang, Brajesh K. Singh, Pablo García-Palacios
Proceedings of the National Academy of Sciences Feb 2021, 118 (7) e2019355118; DOI: 10.1073/pnas.2019355118
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Proceedings of the National Academy of Sciences: 118 (7)
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