Rare Species Support Vulnerable Functions in High-Diversity Ecosystems
Identifieur interne : 001286 ( Ncbi/Merge ); précédent : 001285; suivant : 001287Rare Species Support Vulnerable Functions in High-Diversity Ecosystems
Auteurs : David Mouillot [France, Australie] ; David R. Bellwood [Australie] ; Christopher Baraloto [France, États-Unis] ; Jerome Chave [France] ; Rene Galzin [France] ; Mireille Harmelin-Vivien [France] ; Michel Kulbicki [France] ; Sebastien Lavergne [France] ; Sandra Lavorel [France] ; Nicolas Mouquet [France] ; C. E. Timothy Paine [Royaume-Uni] ; Julien Renaud [France] ; Wilfried Thuiller [France]Source :
- PLoS Biology [ 1544-9173 ] ; 2013.
Abstract
The most unusual, and thus irreplaceable, functions performed by species in three different species-rich ecosystems are fulfilled by only the rare species in these ecosystems.
Url:
DOI: 10.1371/journal.pbio.1001569
PubMed: 23723735
PubMed Central: 3665844
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<author><name sortKey="Renaud, Julien" sort="Renaud, Julien" uniqKey="Renaud J" first="Julien" last="Renaud">Julien Renaud</name>
<affiliation wicri:level="4"><nlm:aff id="aff10"><addr-line>Laboratoire d'Ecologie Alpine, UMR CNRS 5553, Université Joseph Fourier, BP53, Grenoble, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Laboratoire d'Ecologie Alpine, UMR CNRS 5553, Université Joseph Fourier, BP53, Grenoble</wicri:regionArea>
<placeName><region type="region">Auvergne-Rhône-Alpes</region>
<region type="old region">Rhône-Alpes</region>
<settlement type="city">Grenoble</settlement>
<settlement type="city">Grenoble</settlement>
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<orgName type="university">Université Joseph Fourier</orgName>
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</author>
<author><name sortKey="Thuiller, Wilfried" sort="Thuiller, Wilfried" uniqKey="Thuiller W" first="Wilfried" last="Thuiller">Wilfried Thuiller</name>
<affiliation wicri:level="4"><nlm:aff id="aff10"><addr-line>Laboratoire d'Ecologie Alpine, UMR CNRS 5553, Université Joseph Fourier, BP53, Grenoble, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Laboratoire d'Ecologie Alpine, UMR CNRS 5553, Université Joseph Fourier, BP53, Grenoble</wicri:regionArea>
<placeName><region type="region">Auvergne-Rhône-Alpes</region>
<region type="old region">Rhône-Alpes</region>
<settlement type="city">Grenoble</settlement>
<settlement type="city">Grenoble</settlement>
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<orgName type="university">Université Joseph Fourier</orgName>
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</analytic>
<series><title level="j">PLoS Biology</title>
<idno type="ISSN">1544-9173</idno>
<idno type="eISSN">1545-7885</idno>
<imprint><date when="2013">2013</date>
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<front><div type="abstract" xml:lang="en"><p>The most unusual, and thus irreplaceable, functions performed by species in three different species-rich ecosystems are fulfilled by only the rare species in these ecosystems.</p>
</div>
</front>
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</author>
<author><name sortKey="Villeger, S" uniqKey="Villeger S">S Villeger</name>
</author>
<author><name sortKey="Mason, Nwh" uniqKey="Mason N">NWH Mason</name>
</author>
<author><name sortKey="Tomasini, Ja" uniqKey="Tomasini J">JA Tomasini</name>
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</author>
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<author><name sortKey="Collen, B" uniqKey="Collen B">B Collen</name>
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<author><name sortKey="Baillie, Jem" uniqKey="Baillie J">JEM Baillie</name>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS Biol</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS Biol</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plosbiol</journal-id>
<journal-title-group><journal-title>PLoS Biology</journal-title>
</journal-title-group>
<issn pub-type="ppub">1544-9173</issn>
<issn pub-type="epub">1545-7885</issn>
<publisher><publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">23723735</article-id>
<article-id pub-id-type="pmc">3665844</article-id>
<article-id pub-id-type="publisher-id">PBIOLOGY-D-12-01899</article-id>
<article-id pub-id-type="doi">10.1371/journal.pbio.1001569</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline-v2"><subject>Biology</subject>
<subj-group><subject>Ecology</subject>
</subj-group>
<subj-group><subject>Marine Biology</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Rare Species Support Vulnerable Functions in High-Diversity Ecosystems</article-title>
<alt-title alt-title-type="running-head">Rare Species Support Vulnerable Functions</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Mouillot</surname>
<given-names>David</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>*</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bellwood</surname>
<given-names>David R.</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Baraloto</surname>
<given-names>Christopher</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
<xref ref-type="aff" rid="aff5"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Chave</surname>
<given-names>Jerome</given-names>
</name>
<xref ref-type="aff" rid="aff6"><sup>6</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Galzin</surname>
<given-names>Rene</given-names>
</name>
<xref ref-type="aff" rid="aff7"><sup>7</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Harmelin-Vivien</surname>
<given-names>Mireille</given-names>
</name>
<xref ref-type="aff" rid="aff8"><sup>8</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kulbicki</surname>
<given-names>Michel</given-names>
</name>
<xref ref-type="aff" rid="aff9"><sup>9</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lavergne</surname>
<given-names>Sebastien</given-names>
</name>
<xref ref-type="aff" rid="aff10"><sup>10</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lavorel</surname>
<given-names>Sandra</given-names>
</name>
<xref ref-type="aff" rid="aff10"><sup>10</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Mouquet</surname>
<given-names>Nicolas</given-names>
</name>
<xref ref-type="aff" rid="aff11"><sup>11</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Paine</surname>
<given-names>C. E. Timothy</given-names>
</name>
<xref ref-type="aff" rid="aff12"><sup>12</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Renaud</surname>
<given-names>Julien</given-names>
</name>
<xref ref-type="aff" rid="aff10"><sup>10</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Thuiller</surname>
<given-names>Wilfried</given-names>
</name>
<xref ref-type="aff" rid="aff10"><sup>10</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>1</label>
<addr-line>Unité Mixte de Recherche (UMR) Centre National de la Recherche Scientifique (CNRS)–UM2– Institut français de recherche pour l'exploitation de la mer (IFREMER)–Institute for Research and Development (IRD) 5119 ECOSYM, Université Montpellier 2 cc 093, Montpellier, France</addr-line>
</aff>
<aff id="aff2"><label>2</label>
<addr-line>ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Australia</addr-line>
</aff>
<aff id="aff3"><label>3</label>
<addr-line>School of Marine and Tropical Biology, James Cook University, Townsville, Australia</addr-line>
</aff>
<aff id="aff4"><label>4</label>
<addr-line>Institut National de la Recherche Agronomique, UMR Ecologie des Forêts de Guyane, 97387, Kourou, French Guiana, France</addr-line>
</aff>
<aff id="aff5"><label>5</label>
<addr-line>Department of Biology, University of Florida, Gainesville, Florida, United States of America</addr-line>
</aff>
<aff id="aff6"><label>6</label>
<addr-line>Université Paul Sabatier, CNRS, Laboratoire Evolution et Diversité Biologique UMR 5174, Toulouse, France</addr-line>
</aff>
<aff id="aff7"><label>7</label>
<addr-line>Laboratoire d'Excellence “Corail” USR 3278 CNRS-EPHE, BP 1013, Moorea, Polynésie Française, France</addr-line>
</aff>
<aff id="aff8"><label>8</label>
<addr-line>Aix-Marseille Université, Institut Méditerranéen d'Océanologie (MIO), UMR CNRS 7294, Marseille, France</addr-line>
</aff>
<aff id="aff9"><label>9</label>
<addr-line>Laboratoire d'Excellence “Corail” IRD, Laboratoire Arago, Banyuls/mer, France</addr-line>
</aff>
<aff id="aff10"><label>10</label>
<addr-line>Laboratoire d'Ecologie Alpine, UMR CNRS 5553, Université Joseph Fourier, BP53, Grenoble, France</addr-line>
</aff>
<aff id="aff11"><label>11</label>
<addr-line>Institut des Sciences de l'Evolution, UMR CNRS–UM2, 5554, Université Montpellier 2, Montpellier, France</addr-line>
</aff>
<aff id="aff12"><label>12</label>
<addr-line>Biological and Environmental Sciences, University of Stirling, Stirling, United Kingdom</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Mace</surname>
<given-names>Georgina M.</given-names>
</name>
<role>Academic Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1"><addr-line>University College London, United Kingdom</addr-line>
</aff>
<author-notes><corresp id="cor1">* E-mail: <email>david.mouillot@univ-montp2.fr</email>
</corresp>
<fn fn-type="COI-statement"><p>The authors have declared that no competing interests exist.</p>
</fn>
<fn fn-type="con"><p>The author(s) have made the following declarations about their contributions: Conceived and designed the experiments: D. Mouillot, D.R. Bellwood, N. Mouquet, W. Thuiller, C. Baraloto. Performed the experiments: C. Baraloto, J. Chave, R. Galzin, M. Harmelin-Vivien, M. Kulbicki, S. Lavergne, S. Lavorel, C.E.T. Paine W. Thuiller. Analyzed the data: D. Mouillot, D.R. Bellwood, C. Baraloto, J. Chave, M. Kulbicki, S. Lavergne, C.E.T. Paine, J. Renaud, W. Thuiller. Contributed reagents/materials/analysis tools: D. Mouillot, D.R. Bellwood, C. Baraloto, J. Chave, M. Kulbicki, S. Lavergne, C.E.T. Paine, N. Mouquet, J. Renaud, W. Thuiller. Wrote the paper: D. Mouillot, D.R. Bellwood, C. Baraloto, J. Chave, M. Kulbicki, S. Lavergne, S. Lavorel, C.E.T. Paine, N. Mouquet, W. Thuiller.</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><month>5</month>
<year>2013</year>
</pub-date>
<pub-date pub-type="epub"><day>28</day>
<month>5</month>
<year>2013</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>28</day>
<month>5</month>
<year>2013</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the . </pmc-comment>
<volume>11</volume>
<issue>5</issue>
<elocation-id>e1001569</elocation-id>
<history><date date-type="received"><day>16</day>
<month>5</month>
<year>2012</year>
</date>
<date date-type="accepted"><day>17</day>
<month>4</month>
<year>2013</year>
</date>
</history>
<permissions><copyright-statement>© 2013 Mouillot et al</copyright-statement>
<copyright-year>2013</copyright-year>
<copyright-holder>Mouillot et al</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.</license-p>
</license>
</permissions>
<related-article id="RA1" related-article-type="companion" vol="" page="e1001573" ext-link-type="pmc"><pmc-comment>related-article was converted to @ext-link-type="pmc" and original @xlink:href value
was info:doi/10.1371/journal.pbio.1001573</pmc-comment>
<article-title>An Inordinate Fondness of Rarity</article-title>
</related-article>
<abstract abstract-type="toc"><p>The most unusual, and thus irreplaceable, functions performed by species in three different species-rich ecosystems are fulfilled by only the rare species in these ecosystems.</p>
</abstract>
<abstract><p>Around the world, the human-induced collapses of populations and species have triggered a sixth mass extinction crisis, with rare species often being the first to disappear. Although the role of species diversity in the maintenance of ecosystem processes has been widely investigated, the role of rare species remains controversial. A critical issue is whether common species insure against the loss of functions supported by rare species. This issue is even more critical in species-rich ecosystems where high functional redundancy among species is likely and where it is thus often assumed that ecosystem functioning is buffered against species loss. Here, using extensive datasets of species occurrences and functional traits from three highly diverse ecosystems (846 coral reef fishes, 2,979 alpine plants, and 662 tropical trees), we demonstrate that the most distinct combinations of traits are supported predominantly by rare species both in terms of local abundance and regional occupancy. Moreover, species that have low functional redundancy and are likely to support the most vulnerable functions, with no other species carrying similar combinations of traits, are rarer than expected by chance in all three ecosystems. For instance, 63% and 98% of fish species that are likely to support highly vulnerable functions in coral reef ecosystems are locally and regionally rare, respectively. For alpine plants, 32% and 89% of such species are locally and regionally rare, respectively. Remarkably, 47% of fish species and 55% of tropical tree species that are likely to support highly vulnerable functions have only one individual per sample on average. Our results emphasize the importance of rare species conservation, even in highly diverse ecosystems, which are thought to exhibit high functional redundancy. Rare species offer more than aesthetic, cultural, or taxonomic diversity value; they disproportionately increase the potential breadth of functions provided by ecosystems across spatial scales. As such, they are likely to insure against future uncertainty arising from climate change and the ever-increasing anthropogenic pressures on ecosystems. Our results call for a more detailed understanding of the role of rarity and functional vulnerability in ecosystem functioning.</p>
</abstract>
<abstract abstract-type="summary"><title>Author Summary</title>
<p>In ecological systems most species are rare—that is, represented by only a few individuals or restricted to particular habitats—and are vulnerable to being lost. Yet the ecological consequences of such biodiversity loss are often overlooked and remain controversial. In the best-case scenario, the functions that these rare species provide to their ecosystems might be insured by more common species, which share combinations of functional traits with the rare species, thereby helping to maintain ecosystem functioning despite rare species loss. In the worst-case scenario, rare species would have functional traits that are distinct from those of common species; thus, the functions they support would also be vulnerable to extinction. We examined three highly diverse ecosystems (coral reefs, alpine meadows, and tropical forests) and addressed whether common species would insure against the loss of functions carried by rare species. We demonstrate that highly distinct combinations of traits are supported predominantly by rare species. It is thus not only the quantity but also the quality of biodiversity that matters. Thus, our findings highlight that we need to change how we think about biodiversity in general, and about conservation strategies in particular, by moving beyond the protection of biodiversity per se and beyond focusing on iconic, charismatic, or phylogenetically distinct species, to protecting species that support irreplaceable functional roles and associated services.</p>
</abstract>
<funding-group><funding-statement>The research leading to this article had received funding from the Marie Curie International Outgoing Fellowship (FISHECO) with agreement number IOF-GA-2009-236316. W. Thuiller and S. Lavergne received funding from the European Research Council under the European Community's Seven Framework Programme FP7/2007-2013 Grant Agreement no. 281422 (TEEMBIO). We also acknowledge support from the ANR DIVERSITALP (ANR-07-BDIV-014), the ECOCHANGE project, funded by the Sixth European Framework Programme (GOCE-CT-2007-036866), the ANR 3Worlds (ANR-07-CIS7-001), the 6e extinction ANR-09-PEXT-01102 “EVORANGE”, the FRB project CESAB-GASPAR, and the Australian Research Council. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement>
</funding-group>
<counts><page-count count="11"></page-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>Australie</li>
<li>France</li>
<li>Royaume-Uni</li>
<li>États-Unis</li>
</country>
<region><li>Auvergne-Rhône-Alpes</li>
<li>Floride</li>
<li>Languedoc-Roussillon</li>
<li>Midi-Pyrénées</li>
<li>Occitanie (région administrative)</li>
<li>Provence-Alpes-Côte d'Azur</li>
<li>Rhône-Alpes</li>
</region>
<settlement><li>Grenoble</li>
<li>Marseille</li>
<li>Montpellier</li>
<li>Toulouse</li>
</settlement>
<orgName><li>Université Joseph Fourier</li>
<li>Université Montpellier 2</li>
<li>Université Toulouse III - Paul Sabatier</li>
<li>Université d'Aix-Marseille</li>
</orgName>
</list>
<tree><country name="France"><region name="Occitanie (région administrative)"><name sortKey="Mouillot, David" sort="Mouillot, David" uniqKey="Mouillot D" first="David" last="Mouillot">David Mouillot</name>
</region>
<name sortKey="Baraloto, Christopher" sort="Baraloto, Christopher" uniqKey="Baraloto C" first="Christopher" last="Baraloto">Christopher Baraloto</name>
<name sortKey="Chave, Jerome" sort="Chave, Jerome" uniqKey="Chave J" first="Jerome" last="Chave">Jerome Chave</name>
<name sortKey="Galzin, Rene" sort="Galzin, Rene" uniqKey="Galzin R" first="Rene" last="Galzin">Rene Galzin</name>
<name sortKey="Harmelin Vivien, Mireille" sort="Harmelin Vivien, Mireille" uniqKey="Harmelin Vivien M" first="Mireille" last="Harmelin-Vivien">Mireille Harmelin-Vivien</name>
<name sortKey="Kulbicki, Michel" sort="Kulbicki, Michel" uniqKey="Kulbicki M" first="Michel" last="Kulbicki">Michel Kulbicki</name>
<name sortKey="Lavergne, Sebastien" sort="Lavergne, Sebastien" uniqKey="Lavergne S" first="Sebastien" last="Lavergne">Sebastien Lavergne</name>
<name sortKey="Lavorel, Sandra" sort="Lavorel, Sandra" uniqKey="Lavorel S" first="Sandra" last="Lavorel">Sandra Lavorel</name>
<name sortKey="Mouquet, Nicolas" sort="Mouquet, Nicolas" uniqKey="Mouquet N" first="Nicolas" last="Mouquet">Nicolas Mouquet</name>
<name sortKey="Renaud, Julien" sort="Renaud, Julien" uniqKey="Renaud J" first="Julien" last="Renaud">Julien Renaud</name>
<name sortKey="Thuiller, Wilfried" sort="Thuiller, Wilfried" uniqKey="Thuiller W" first="Wilfried" last="Thuiller">Wilfried Thuiller</name>
</country>
<country name="Australie"><noRegion><name sortKey="Mouillot, David" sort="Mouillot, David" uniqKey="Mouillot D" first="David" last="Mouillot">David Mouillot</name>
</noRegion>
<name sortKey="Bellwood, David R" sort="Bellwood, David R" uniqKey="Bellwood D" first="David R." last="Bellwood">David R. Bellwood</name>
<name sortKey="Bellwood, David R" sort="Bellwood, David R" uniqKey="Bellwood D" first="David R." last="Bellwood">David R. Bellwood</name>
</country>
<country name="États-Unis"><region name="Floride"><name sortKey="Baraloto, Christopher" sort="Baraloto, Christopher" uniqKey="Baraloto C" first="Christopher" last="Baraloto">Christopher Baraloto</name>
</region>
</country>
<country name="Royaume-Uni"><noRegion><name sortKey="Paine, C E Timothy" sort="Paine, C E Timothy" uniqKey="Paine C" first="C. E. Timothy" last="Paine">C. E. Timothy Paine</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>
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