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Biological Sciences

Functional over-redundancy and high functional vulnerability in global fish faunas on tropical reefs

David Mouillot, Sébastien Villéger, Valeriano Parravicini, Michel Kulbicki, Jesus Ernesto Arias-González, Mariana Bender, Pascale Chabanet, Sergio R. Floeter, Alan Friedlander, Laurent Vigliola, and David R. Bellwood
  1. aEcologie des Systèmes Marins Côtiers, Unité Mixte de Recherche 5119, Centre National de la Recherche Scientifique-Institut de Recherche pour le Développement-Université Montpellier 2-Institut Français de Recherche pour l'Exploitation de la Mer, Université Montpellier 2, 34095 Montpellier, France;
  2. bAustralian Research Council Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD 4811, Australia;
  3. cInstitut de Recherche pour le Développement, Unité de Recherche 227 Biocomplexité des écosystèmes coralliens de l'Indo-Pacifique, LABEX Corail, Laboratoire Arago, BP 44, 66651 Banyuls sur Mer, France;
  4. dCenter for Synthesis and Analysis of Biodiversity-Fondation pour la Recherche sur la Biodiversité Immeuble Henri Poincaré, Domaine du Petit Arbois, 13857 Aix-en-Provence Cedex 3, France;
  5. eLaboratorio de Ecología de Ecosistemas de Arrecifes Coralinos, Departamento de Recursos del Mar, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Unidad Mérida, 97310 Mérida, Yucatán, Mexico;
  6. fMarine Macroecology and Biogeography Laboratory, Universidade Federal de Santa Catarina, Florianópolis, 88040-900, Santa Catarina, Brazil;
  7. gInstitut de Recherche pour le Développement, Unité de Recherche 227 Biocomplexité des écosystèmes coralliens de l'Indo-Pacifique, LABEX Corail, BP 50172, 97492 Ste. Clotilde 18 Cedex, Reunion Island, France;
  8. hFisheries Ecology Research Laboratory, Department of Biology, University of Hawaii at Manoa, Honolulu, HI 96822;
  9. iInstitut de Recherche pour le Développement, Unité de Recherche 227 Biocomplexité des écosystèmes coralliens de l'Indo-Pacifique, LABEX Corail, 98848 Nouméa Cedex, New Caledonia, France; and
  10. jSchool of Marine and Tropical Biology, James Cook University, Townsville, QLD 4811, Australia

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PNAS September 23, 2014 111 (38) 13757-13762; first published September 15, 2014; https://doi.org/10.1073/pnas.1317625111
David Mouillot
aEcologie des Systèmes Marins Côtiers, Unité Mixte de Recherche 5119, Centre National de la Recherche Scientifique-Institut de Recherche pour le Développement-Université Montpellier 2-Institut Français de Recherche pour l'Exploitation de la Mer, Université Montpellier 2, 34095 Montpellier, France;
bAustralian Research Council Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD 4811, Australia;
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  • For correspondence: david.mouillot@univ-montp2.fr
Sébastien Villéger
aEcologie des Systèmes Marins Côtiers, Unité Mixte de Recherche 5119, Centre National de la Recherche Scientifique-Institut de Recherche pour le Développement-Université Montpellier 2-Institut Français de Recherche pour l'Exploitation de la Mer, Université Montpellier 2, 34095 Montpellier, France;
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Valeriano Parravicini
cInstitut de Recherche pour le Développement, Unité de Recherche 227 Biocomplexité des écosystèmes coralliens de l'Indo-Pacifique, LABEX Corail, Laboratoire Arago, BP 44, 66651 Banyuls sur Mer, France;
dCenter for Synthesis and Analysis of Biodiversity-Fondation pour la Recherche sur la Biodiversité Immeuble Henri Poincaré, Domaine du Petit Arbois, 13857 Aix-en-Provence Cedex 3, France;
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Michel Kulbicki
cInstitut de Recherche pour le Développement, Unité de Recherche 227 Biocomplexité des écosystèmes coralliens de l'Indo-Pacifique, LABEX Corail, Laboratoire Arago, BP 44, 66651 Banyuls sur Mer, France;
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Jesus Ernesto Arias-González
eLaboratorio de Ecología de Ecosistemas de Arrecifes Coralinos, Departamento de Recursos del Mar, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Unidad Mérida, 97310 Mérida, Yucatán, Mexico;
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Mariana Bender
aEcologie des Systèmes Marins Côtiers, Unité Mixte de Recherche 5119, Centre National de la Recherche Scientifique-Institut de Recherche pour le Développement-Université Montpellier 2-Institut Français de Recherche pour l'Exploitation de la Mer, Université Montpellier 2, 34095 Montpellier, France;
fMarine Macroecology and Biogeography Laboratory, Universidade Federal de Santa Catarina, Florianópolis, 88040-900, Santa Catarina, Brazil;
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Pascale Chabanet
gInstitut de Recherche pour le Développement, Unité de Recherche 227 Biocomplexité des écosystèmes coralliens de l'Indo-Pacifique, LABEX Corail, BP 50172, 97492 Ste. Clotilde 18 Cedex, Reunion Island, France;
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Sergio R. Floeter
fMarine Macroecology and Biogeography Laboratory, Universidade Federal de Santa Catarina, Florianópolis, 88040-900, Santa Catarina, Brazil;
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Alan Friedlander
hFisheries Ecology Research Laboratory, Department of Biology, University of Hawaii at Manoa, Honolulu, HI 96822;
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Laurent Vigliola
iInstitut de Recherche pour le Développement, Unité de Recherche 227 Biocomplexité des écosystèmes coralliens de l'Indo-Pacifique, LABEX Corail, 98848 Nouméa Cedex, New Caledonia, France; and
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David R. Bellwood
bAustralian Research Council Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD 4811, Australia;
jSchool of Marine and Tropical Biology, James Cook University, Townsville, QLD 4811, Australia
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  1. Edited by Cyrille Violle, Centre National de la Recherche Scientifique, Montpellier, France, and accepted by the Editorial Board January 28, 2014 (received for review September 18, 2013)

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Significance

Our results indicate that, even in highly diverse systems like coral reefs, we can no longer assume that the erosion of species diversity can be discounted by the high probability of functional redundancy: i.e., that several species can support the same function. Indeed, we show that fish species tend to disproportionately pack into a few particular functions while leaving many functions highly vulnerable, i.e., they are supported by just one species. Even the Coral Triangle, which has a high concentration of tropical-reef fishes, may experience a loss of functional diversity following fisheries pressure and local species extirpation. Our results suggest that the promised benefits of functional insurance from high species diversity may not be as strong as we once hoped.

Abstract

When tropical systems lose species, they are often assumed to be buffered against declines in functional diversity by the ability of the species-rich biota to display high functional redundancy: i.e., a high number of species performing similar functions. We tested this hypothesis using a ninefold richness gradient in global fish faunas on tropical reefs encompassing 6,316 species distributed among 646 functional entities (FEs): i.e., unique combinations of functional traits. We found that the highest functional redundancy is located in the Central Indo-Pacific with a mean of 7.9 species per FE. However, this overall level of redundancy is disproportionately packed into few FEs, a pattern termed functional over-redundancy (FOR). For instance, the most speciose FE in the Central Indo-Pacific contains 222 species (out of 3,689) whereas 38% of FEs (180 out of 468) have no functional insurance with only one species. Surprisingly, the level of FOR is consistent across the six fish faunas, meaning that, whatever the richness, over a third of the species may still be in overrepresented FEs whereas more than one third of the FEs are left without insurance, these levels all being significantly higher than expected by chance. Thus, our study shows that, even in high-diversity systems, such as tropical reefs, functional diversity remains highly vulnerable to species loss. Although further investigations are needed to specifically address the influence of redundant vs. vulnerable FEs on ecosystem functioning, our results suggest that the promised benefits from tropical biodiversity may not be as strong as previously thought.

  • fish ecology
  • coral reefs

Footnotes

  • ↵1D.M., S.V., and V.P. contributed equally to this work.

  • ↵2To whom correspondence should be addressed. Email: david.mouillot{at}univ-montp2.fr.
  • Author contributions: D.M., S.V., V.P., M.K., J.E.A.-G., M.B., P.C., S.R.F., A.F., L.V., and D.R.B. designed research, performed research, contributed new reagents/analytic tools, analyzed data, and wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission. C.V. 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.1317625111/-/DCSupplemental.

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Functional over-redundancy in fish faunas
David Mouillot, Sébastien Villéger, Valeriano Parravicini, Michel Kulbicki, Jesus Ernesto Arias-González, Mariana Bender, Pascale Chabanet, Sergio R. Floeter, Alan Friedlander, Laurent Vigliola, David R. Bellwood
Proceedings of the National Academy of Sciences Sep 2014, 111 (38) 13757-13762; DOI: 10.1073/pnas.1317625111

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Functional over-redundancy in fish faunas
David Mouillot, Sébastien Villéger, Valeriano Parravicini, Michel Kulbicki, Jesus Ernesto Arias-González, Mariana Bender, Pascale Chabanet, Sergio R. Floeter, Alan Friedlander, Laurent Vigliola, David R. Bellwood
Proceedings of the National Academy of Sciences Sep 2014, 111 (38) 13757-13762; DOI: 10.1073/pnas.1317625111
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