Reproductive success is energetically linked to foraging efficiency in Antarctic fur seals
Identifieur interne : 002824 ( Pmc/Curation ); précédent : 002823; suivant : 002825Reproductive success is energetically linked to foraging efficiency in Antarctic fur seals
Auteurs : Tiphaine Jeanniard-Du-Dot [Canada, France] ; Andrew W. Trites [Canada] ; John P. Y. Arnould [Australie] ; Christophe Guinet [France]Source :
- PLoS ONE [ 1932-6203 ] ; 2017.
Abstract
The efficiency with which individuals extract energy from their environment defines their survival and reproductive success, and thus their selective contribution to the population. Individuals that forage more efficiently (i.e., when energy gained exceeds energy expended) are likely to be more successful at raising viable offspring than individuals that forage less efficiently. Our goal was to test this prediction in large long-lived mammals under free-ranging conditions. To do so, we equipped 20 lactating Antarctic fur seals (
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DOI: 10.1371/journal.pone.0174001
PubMed: 28453563
PubMed Central: 5409505
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Trites</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Marine Mammal Research Unit, Institute for the Oceans and Fisheries, University of British Columbia, Vancouver, BC, Canada</addr-line></nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea>Marine Mammal Research Unit, Institute for the Oceans and Fisheries, University of British Columbia, Vancouver, BC</wicri:regionArea></affiliation></author><author><name sortKey="Arnould, John P Y" sort="Arnould, John P Y" uniqKey="Arnould J" first="John P. Y." last="Arnould">John P. Y. Arnould</name><affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>School of Life and Environmental Sciences, Deakin University, Burwood, VIC, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>School of Life and Environmental Sciences, Deakin University, Burwood, VIC</wicri:regionArea></affiliation></author><author><name sortKey="Guinet, Christophe" sort="Guinet, Christophe" uniqKey="Guinet C" first="Christophe" last="Guinet">Christophe Guinet</name><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Centre d’Etudes Biologiques de Chizé, CNRS, Villiers en Bois, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre d’Etudes Biologiques de Chizé, CNRS, Villiers en Bois</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">28453563</idno><idno type="pmc">5409505</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5409505</idno><idno type="RBID">PMC:5409505</idno><idno type="doi">10.1371/journal.pone.0174001</idno><date when="2017">2017</date><idno type="wicri:Area/Pmc/Corpus">002974</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">002974</idno><idno type="wicri:Area/Pmc/Curation">002824</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">002824</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Reproductive success is energetically linked to foraging efficiency in Antarctic fur seals</title><author><name sortKey="Jeanniard Du Dot, Tiphaine" sort="Jeanniard Du Dot, Tiphaine" uniqKey="Jeanniard Du Dot T" first="Tiphaine" last="Jeanniard-Du-Dot">Tiphaine Jeanniard-Du-Dot</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Marine Mammal Research Unit, Institute for the Oceans and Fisheries, University of British Columbia, Vancouver, BC, Canada</addr-line></nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea>Marine Mammal Research Unit, Institute for the Oceans and Fisheries, University of British Columbia, Vancouver, BC</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Centre d’Etudes Biologiques de Chizé, CNRS, Villiers en Bois, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre d’Etudes Biologiques de Chizé, CNRS, Villiers en Bois</wicri:regionArea></affiliation></author><author><name sortKey="Trites, Andrew W" sort="Trites, Andrew W" uniqKey="Trites A" first="Andrew W." last="Trites">Andrew W. Trites</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Marine Mammal Research Unit, Institute for the Oceans and Fisheries, University of British Columbia, Vancouver, BC, Canada</addr-line></nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea>Marine Mammal Research Unit, Institute for the Oceans and Fisheries, University of British Columbia, Vancouver, BC</wicri:regionArea></affiliation></author><author><name sortKey="Arnould, John P Y" sort="Arnould, John P Y" uniqKey="Arnould J" first="John P. Y." last="Arnould">John P. Y. Arnould</name><affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>School of Life and Environmental Sciences, Deakin University, Burwood, VIC, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>School of Life and Environmental Sciences, Deakin University, Burwood, VIC</wicri:regionArea></affiliation></author><author><name sortKey="Guinet, Christophe" sort="Guinet, Christophe" uniqKey="Guinet C" first="Christophe" last="Guinet">Christophe Guinet</name><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Centre d’Etudes Biologiques de Chizé, CNRS, Villiers en Bois, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre d’Etudes Biologiques de Chizé, CNRS, Villiers en Bois</wicri:regionArea></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The efficiency with which individuals extract energy from their environment defines their survival and reproductive success, and thus their selective contribution to the population. Individuals that forage more efficiently (i.e., when energy gained exceeds energy expended) are likely to be more successful at raising viable offspring than individuals that forage less efficiently. Our goal was to test this prediction in large long-lived mammals under free-ranging conditions. To do so, we equipped 20 lactating Antarctic fur seals (<italic>Arctocephalus gazella</italic>) breeding on Kerguelen Island in the Southern Ocean with tags that recorded GPS locations, depth and tri-axial acceleration to determine at-sea behaviours and detailed time-activity budgets during their foraging trips. We also simultaneously measured energy spent at sea using the doubly-labeled water (DLW) method, and estimated the energy acquired while foraging from 1) type and energy content of prey species present in scat remains, and 2) numbers of prey capture attempts determined from head acceleration. Finally, we followed the growth of 36 pups from birth until weaning (of which 20 were the offspring of our 20 tracked mothers), and used the relative differences in body mass of pups at weaning as an index of first year survival and thus the reproductive success of their mothers. Our results show that females with greater foraging efficiencies produced relatively bigger pups at weaning. These mothers achieved greater foraging efficiency by extracting more energy per minute of diving rather than by reducing energy expenditure. This strategy also resulted in the females spending less time diving and less time overall at sea, which allowed them to deliver higher quality milk to their pups, or allowed their pups to suckle more frequently, or both. The linkage we demonstrate between reproductive success and the quality of individuals as foragers provides an individual-based quantitative framework to investigate how changes in the availability and accessibility of prey can affect fitness of animals.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Stephens, Dw" uniqKey="Stephens D">DW Stephens</name></author><author><name sortKey="Krebs, Jr" uniqKey="Krebs J">JR Krebs</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Pyke, Gh" uniqKey="Pyke G">GH Pyke</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Macarthur, Rh" uniqKey="Macarthur R">RH MacArthur</name></author><author><name sortKey="Pianka, Er" uniqKey="Pianka E">ER Pianka</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Boggs, Cl" uniqKey="Boggs C">CL 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id><journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosone</journal-id><journal-title-group><journal-title>PLoS ONE</journal-title></journal-title-group><issn pub-type="epub">1932-6203</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, CA USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">28453563</article-id><article-id pub-id-type="pmc">5409505</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0174001</article-id><article-id pub-id-type="publisher-id">PONE-D-16-48266</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Behavior</subject><subj-group><subject>Animal Behavior</subject><subj-group><subject>Foraging</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Zoology</subject><subj-group><subject>Animal Behavior</subject><subj-group><subject>Foraging</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Animals</subject><subj-group><subject>Vertebrates</subject><subj-group><subject>Amniotes</subject><subj-group><subject>Mammals</subject><subj-group><subject>Marine Mammals</subject><subj-group><subject>Seals</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Marine Biology</subject><subj-group><subject>Marine Mammals</subject><subj-group><subject>Seals</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Earth Sciences</subject><subj-group><subject>Marine and Aquatic Sciences</subject><subj-group><subject>Marine Biology</subject><subj-group><subject>Marine Mammals</subject><subj-group><subject>Seals</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Ecology</subject><subj-group><subject>Community Ecology</subject><subj-group><subject>Trophic Interactions</subject><subj-group><subject>Predation</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Ecology and Environmental Sciences</subject><subj-group><subject>Ecology</subject><subj-group><subject>Community Ecology</subject><subj-group><subject>Trophic Interactions</subject><subj-group><subject>Predation</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Bioenergetics</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Ecology</subject><subj-group><subject>Community Ecology</subject><subj-group><subject>Trophic Interactions</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Ecology and Environmental Sciences</subject><subj-group><subject>Ecology</subject><subj-group><subject>Community Ecology</subject><subj-group><subject>Trophic Interactions</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>People and Places</subject><subj-group><subject>Geographical Locations</subject><subj-group><subject>Antarctica</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Evolutionary Biology</subject><subj-group><subject>Evolutionary Processes</subject><subj-group><subject>Natural Selection</subject><subj-group><subject>Reproductive Success</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Engineering and Technology</subject><subj-group><subject>Electronics</subject><subj-group><subject>Accelerometers</subject></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Reproductive success is energetically linked to foraging efficiency in Antarctic fur seals</article-title><alt-title alt-title-type="running-head">Reproductive success linked to foraging efficiency in fur seals</alt-title></title-group><contrib-group><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-1985-8325</contrib-id><name><surname>Jeanniard-du-Dot</surname><given-names>Tiphaine</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="author-notes" rid="econtrib001"><sup>‡</sup></xref><xref ref-type="corresp" rid="cor001">*</xref></contrib><contrib contrib-type="author" equal-contrib="yes"><name><surname>Trites</surname><given-names>Andrew W.</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author" equal-contrib="yes"><name><surname>Arnould</surname><given-names>John P. Y.</given-names></name><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author" equal-contrib="yes"><name><surname>Guinet</surname><given-names>Christophe</given-names></name><xref ref-type="aff" rid="aff002"><sup>2</sup></xref></contrib></contrib-group><aff id="aff001"><label>1</label><addr-line>Marine Mammal Research Unit, Institute for the Oceans and Fisheries, University of British Columbia, Vancouver, BC, Canada</addr-line></aff><aff id="aff002"><label>2</label><addr-line>Centre d’Etudes Biologiques de Chizé, CNRS, Villiers en Bois, France</addr-line></aff><aff id="aff003"><label>3</label><addr-line>School of Life and Environmental Sciences, Deakin University, Burwood, VIC, Australia</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Wang</surname><given-names>De-Hua</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Institute of Zoology, CHINA</addr-line></aff><author-notes><fn fn-type="COI-statement" id="coi001"><p><bold>Competing Interests: </bold>The authors have declared that no competing interests exist.</p></fn><fn fn-type="con"><p><list list-type="simple"><list-item><p><bold>Conceptualization:</bold> TJDD AWT CG JPYA.</p></list-item><list-item><p><bold>Data curation:</bold> TJDD.</p></list-item><list-item><p><bold>Formal analysis:</bold> TJDD.</p></list-item><list-item><p><bold>Funding acquisition:</bold> TJDD AWT CG JPYA.</p></list-item><list-item><p><bold>Investigation:</bold> TJDD.</p></list-item><list-item><p><bold>Methodology:</bold> TJDD.</p></list-item><list-item><p><bold>Project administration:</bold> TJDD CG.</p></list-item><list-item><p><bold>Resources:</bold> TJDD AWT CG JPYA.</p></list-item><list-item><p><bold>Software:</bold> TJDD.</p></list-item><list-item><p><bold>Supervision:</bold> TJDD AWT CG JPYA.</p></list-item><list-item><p><bold>Validation:</bold> TJDD.</p></list-item><list-item><p><bold>Visualization:</bold> TJDD.</p></list-item><list-item><p><bold>Writing – original draft:</bold> TJDD.</p></list-item><list-item><p><bold>Writing – review & editing:</bold> TJDD AWT CG JPYA.</p></list-item></list></p></fn><fn fn-type="other" id="econtrib001"><p>‡ This author is the first author and main contributor on this work. [for the first author only]</p></fn><corresp id="cor001">* E-mail: <email>tiphainejdd@gmail.com</email></corresp></author-notes><pub-date pub-type="epub"><day>28</day><month>4</month><year>2017</year></pub-date><pub-date pub-type="collection"><year>2017</year></pub-date><volume>12</volume><issue>4</issue><elocation-id>e0174001</elocation-id><history><date date-type="received"><day>6</day><month>12</month><year>2016</year></date><date date-type="accepted"><day>1</day><month>3</month><year>2017</year></date></history><permissions><copyright-statement>© 2017 Jeanniard-du-Dot et al</copyright-statement><copyright-year>2017</copyright-year><copyright-holder>Jeanniard-du-Dot 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 <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="pone.0174001.pdf"></self-uri><abstract><p>The efficiency with which individuals extract energy from their environment defines their survival and reproductive success, and thus their selective contribution to the population. Individuals that forage more efficiently (i.e., when energy gained exceeds energy expended) are likely to be more successful at raising viable offspring than individuals that forage less efficiently. Our goal was to test this prediction in large long-lived mammals under free-ranging conditions. To do so, we equipped 20 lactating Antarctic fur seals (<italic>Arctocephalus gazella</italic>) breeding on Kerguelen Island in the Southern Ocean with tags that recorded GPS locations, depth and tri-axial acceleration to determine at-sea behaviours and detailed time-activity budgets during their foraging trips. We also simultaneously measured energy spent at sea using the doubly-labeled water (DLW) method, and estimated the energy acquired while foraging from 1) type and energy content of prey species present in scat remains, and 2) numbers of prey capture attempts determined from head acceleration. Finally, we followed the growth of 36 pups from birth until weaning (of which 20 were the offspring of our 20 tracked mothers), and used the relative differences in body mass of pups at weaning as an index of first year survival and thus the reproductive success of their mothers. Our results show that females with greater foraging efficiencies produced relatively bigger pups at weaning. These mothers achieved greater foraging efficiency by extracting more energy per minute of diving rather than by reducing energy expenditure. This strategy also resulted in the females spending less time diving and less time overall at sea, which allowed them to deliver higher quality milk to their pups, or allowed their pups to suckle more frequently, or both. The linkage we demonstrate between reproductive success and the quality of individuals as foragers provides an individual-based quantitative framework to investigate how changes in the availability and accessibility of prey can affect fitness of animals.</p></abstract><funding-group><award-group id="award001"><funding-source><institution>North Pacific Reserch Board</institution></funding-source><award-id>F4112-00</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-1985-8325</contrib-id><name><surname>Jeanniard-du-Dot</surname><given-names>Tiphaine</given-names></name></principal-award-recipient></award-group><award-group id="award002"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/501100002790</institution-id><institution>Canadian Network for Research and Innovation in Machining Technology, Natural Sciences and Engineering Research Council of Canada</institution></institution-wrap></funding-source><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-1985-8325</contrib-id><name><surname>Jeanniard-du-Dot</surname><given-names>Tiphaine</given-names></name></principal-award-recipient></award-group><funding-statement>The Natural Sciences and Engineering Research Council of Canada (<ext-link ext-link-type="uri" xlink:href="http://www.nserc-crsng.gc.ca/index_eng.asp">http://www.nserc-crsng.gc.ca/index_eng.asp</ext-link>) and the Institut Polaire Francais Paul-Emile Victor (<ext-link ext-link-type="uri" xlink:href="http://www.institut-polaire.fr/language/en/">http://www.institut-polaire.fr/language/en/</ext-link>) help fund this project. 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><fig-count count="4"></fig-count><table-count count="3"></table-count><page-count count="19"></page-count></counts><custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name><meta-value>Data are deposited on the Dryad Digital Repository and available at <ext-link ext-link-type="uri" xlink:href="http://dx.doi.org/10.5061/dryad.269qr">http://dx.doi.org/10.5061/dryad.269qr</ext-link>.</meta-value></custom-meta></custom-meta-group></article-meta><notes><title>Data Availability</title><p>Data are deposited on the Dryad Digital Repository and available at <ext-link ext-link-type="uri" xlink:href="http://dx.doi.org/10.5061/dryad.269qr">http://dx.doi.org/10.5061/dryad.269qr</ext-link>.</p></notes></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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