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<title xml:lang="en">Thieving rodents as substitute dispersers of megafaunal seeds</title>
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43210;</nlm:aff>
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, 78315 Radolfzell,
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<institution>Department of Forestry and Environmental Resources, North Carolina State University</institution>
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<title xml:lang="en" level="a" type="main">Thieving rodents as substitute dispersers of megafaunal seeds</title>
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<nlm:aff id="aff1">
<institution>Center for Tropical Forest Science, Smithsonian</institution>
<institution> Tropical Research Institute</institution>
, Balboa Ancón, Republic of Panamá;</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="aff2">
<institution>Department of Environmental Sciences, Wageningen University</institution>
, 6700 AA Wageningen,
<country>The Netherlands</country>
;</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="aff3">Center for Ecological and Evolutionary Studies,
<institution>Faculty of Mathematics and Natural Sciences, University of Groningen</institution>
, 9700 CC Groningen,
<country>The Netherlands</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Hirsch, Ben T" sort="Hirsch, Ben T" uniqKey="Hirsch B" first="Ben T." last="Hirsch">Ben T. Hirsch</name>
<affiliation>
<nlm:aff id="aff1">
<institution>Center for Tropical Forest Science, Smithsonian</institution>
<institution> Tropical Research Institute</institution>
, Balboa Ancón, Republic of Panamá;</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="aff4">School of Environment and Natural Resources,
<institution>Ohio State University</institution>
, Columbus,
<addr-line>OH</addr-line>
43210;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Emsens, Willem Jan" sort="Emsens, Willem Jan" uniqKey="Emsens W" first="Willem-Jan" last="Emsens">Willem-Jan Emsens</name>
<affiliation>
<nlm:aff id="aff2">
<institution>Department of Environmental Sciences, Wageningen University</institution>
, 6700 AA Wageningen,
<country>The Netherlands</country>
;</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="aff5">Ecosystem Management Research Group, Department of Biology,
<institution>University of Antwerp</institution>
, B-2610 Antwerp,
<country>Belgium</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Zamora Gutierrez, Veronica" sort="Zamora Gutierrez, Veronica" uniqKey="Zamora Gutierrez V" first="Veronica" last="Zamora-Gutierrez">Veronica Zamora-Gutierrez</name>
<affiliation>
<nlm:aff id="aff2">
<institution>Department of Environmental Sciences, Wageningen University</institution>
, 6700 AA Wageningen,
<country>The Netherlands</country>
;</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="aff6">Conservation Science Group, Department of Zoology,
<institution>University of Cambridge</institution>
, Cambridge CB2 3EJ,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Wikelski, Martin" sort="Wikelski, Martin" uniqKey="Wikelski M" first="Martin" last="Wikelski">Martin Wikelski</name>
<affiliation>
<nlm:aff id="aff1">
<institution>Center for Tropical Forest Science, Smithsonian</institution>
<institution> Tropical Research Institute</institution>
, Balboa Ancón, Republic of Panamá;</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="aff7">
<institution>Max Planck Institute for Ornithology</institution>
, 78315 Radolfzell,
<country>Germany</country>
;</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="aff8">Department of Ornithology,
<institution>University of Konstanz</institution>
, 78543 Konstanz,
<country>Germany</country>
;</nlm:aff>
</affiliation>
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<author>
<name sortKey="Kays, Roland" sort="Kays, Roland" uniqKey="Kays R" first="Roland" last="Kays">Roland Kays</name>
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<nlm:aff id="aff1">
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<institution> Tropical Research Institute</institution>
, Balboa Ancón, Republic of Panamá;</nlm:aff>
</affiliation>
<affiliation>
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<institution>Department of Forestry and Environmental Resources, North Carolina State University</institution>
, Raleigh,
<addr-line>NC</addr-line>
27695</nlm:aff>
</affiliation>
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<title level="j">Proceedings of the National Academy of Sciences of the United States of America</title>
<idno type="ISSN">0027-8424</idno>
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<div type="abstract" xml:lang="en">
<p>The Neotropics have many plant species that seem to be adapted for seed dispersal by megafauna that went extinct in the late Pleistocene. Given the crucial importance of seed dispersal for plant persistence, it remains a mystery how these plants have survived more than 10,000 y without their mutualist dispersers. Here we present support for the hypothesis that secondary seed dispersal by scatter-hoarding rodents has facilitated the persistence of these large-seeded species. We used miniature radio transmitters to track the dispersal of reputedly megafaunal seeds by Central American agoutis, which scatter-hoard seeds in shallow caches in the soil throughout the forest. We found that seeds were initially cached at mostly short distances and then quickly dug up again. However, rather than eating the recovered seeds, agoutis continued to move and recache the seeds, up to 36 times. Agoutis dispersed an estimated 35% of seeds for >100 m. An estimated 14% of the cached seeds survived to the next year, when a new fruit crop became available to the rodents. Serial video-monitoring of cached seeds revealed that the stepwise dispersal was caused by agoutis repeatedly stealing and recaching each other’s buried seeds. Although previous studies suggest that rodents are poor dispersers, we demonstrate that communities of rodents can in fact provide highly effective long-distance seed dispersal. Our findings suggest that thieving scatter-hoarding rodents could substitute for extinct megafaunal seed dispersers of tropical large-seeded trees.</p>
</div>
</front>
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<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Proc Natl Acad Sci U S A</journal-id>
<journal-id journal-id-type="iso-abbrev">Proc. Natl. Acad. Sci. U.S.A</journal-id>
<journal-id journal-id-type="hwp">pnas</journal-id>
<journal-id journal-id-type="pmc">pnas</journal-id>
<journal-id journal-id-type="publisher-id">PNAS</journal-id>
<journal-title-group>
<journal-title>Proceedings of the National Academy of Sciences of the United States of America</journal-title>
</journal-title-group>
<issn pub-type="ppub">0027-8424</issn>
<issn pub-type="epub">1091-6490</issn>
<publisher>
<publisher-name>National Academy of Sciences</publisher-name>
</publisher>
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<article-id pub-id-type="pmid">22802644</article-id>
<article-id pub-id-type="pmc">3412018</article-id>
<article-id pub-id-type="publisher-id">201205184</article-id>
<article-id pub-id-type="doi">10.1073/pnas.1205184109</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Biological Sciences</subject>
<subj-group>
<subject>Ecology</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Thieving rodents as substitute dispersers of megafaunal seeds</article-title>
<alt-title alt-title-type="short">Rodents as dispersers of megafaunal seeds</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Jansen</surname>
<given-names>Patrick A.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
<xref ref-type="aff" rid="aff3">
<sup>c</sup>
</xref>
<xref ref-type="corresp" rid="cor1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Hirsch</surname>
<given-names>Ben T.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff4">
<sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Emsens</surname>
<given-names>Willem-Jan</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
<xref ref-type="aff" rid="aff5">
<sup>e</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Zamora-Gutierrez</surname>
<given-names>Veronica</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
<xref ref-type="aff" rid="aff6">
<sup>f</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Wikelski</surname>
<given-names>Martin</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff7">
<sup>g</sup>
</xref>
<xref ref-type="aff" rid="aff8">
<sup>h</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Kays</surname>
<given-names>Roland</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff9">
<sup>i</sup>
</xref>
<xref ref-type="aff" rid="aff10">
<sup>j</sup>
</xref>
</contrib>
<aff id="aff1">
<sup>a</sup>
<institution>Center for Tropical Forest Science, Smithsonian</institution>
<institution> Tropical Research Institute</institution>
, Balboa Ancón, Republic of Panamá;</aff>
<aff id="aff2">
<sup>b</sup>
<institution>Department of Environmental Sciences, Wageningen University</institution>
, 6700 AA Wageningen,
<country>The Netherlands</country>
;</aff>
<aff id="aff3">
<sup>c</sup>
Center for Ecological and Evolutionary Studies,
<institution>Faculty of Mathematics and Natural Sciences, University of Groningen</institution>
, 9700 CC Groningen,
<country>The Netherlands</country>
;</aff>
<aff id="aff4">
<sup>d</sup>
School of Environment and Natural Resources,
<institution>Ohio State University</institution>
, Columbus,
<addr-line>OH</addr-line>
43210;</aff>
<aff id="aff5">
<sup>e</sup>
Ecosystem Management Research Group, Department of Biology,
<institution>University of Antwerp</institution>
, B-2610 Antwerp,
<country>Belgium</country>
;</aff>
<aff id="aff6">
<sup>f</sup>
Conservation Science Group, Department of Zoology,
<institution>University of Cambridge</institution>
, Cambridge CB2 3EJ,
<country>United Kingdom</country>
;</aff>
<aff id="aff7">
<sup>g</sup>
<institution>Max Planck Institute for Ornithology</institution>
, 78315 Radolfzell,
<country>Germany</country>
;</aff>
<aff id="aff8">
<sup>h</sup>
Department of Ornithology,
<institution>University of Konstanz</institution>
, 78543 Konstanz,
<country>Germany</country>
;</aff>
<aff id="aff9">
<sup>i</sup>
<institution>Department of Forestry and Environmental Resources, North Carolina State University</institution>
, Raleigh,
<addr-line>NC</addr-line>
27695; and</aff>
<aff id="aff10">
<sup>j</sup>
Nature Research Center, North Carolina Museum of Natural Sciences, Raleigh, NC 27601</aff>
</contrib-group>
<author-notes>
<corresp id="cor1">
<sup>1</sup>
To whom correspondence should be addressed. E-mail:
<email>patrick.jansen@wur.nl</email>
.</corresp>
<fn fn-type="edited-by">
<p>Edited
<xref ref-type="fn" rid="fn1">*</xref>
by John W. Terborgh, Duke University, Durham, NC, and approved June 14, 2012 (received for review April 3, 2012)</p>
</fn>
<fn fn-type="con">
<p>Author contributions: P.A.J., B.T.H., V.Z.-G., M.W., and R.K. designed research; P.A.J., B.T.H., W.-J.E., V.Z.-G., and R.K. performed research; P.A.J., B.T.H., W.-J.E., V.Z.-G., and R.K. analyzed data; and P.A.J., B.T.H., W.-J.E., V.Z.-G., M.W., and R.K. wrote the paper.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub">
<day>31</day>
<month>7</month>
<year>2012</year>
</pub-date>
<pub-date pub-type="epub">
<day>16</day>
<month>7</month>
<year>2012</year>
</pub-date>
<pub-date pub-type="pmc-release">
<day>16</day>
<month>7</month>
<year>2012</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the . </pmc-comment>
<volume>109</volume>
<issue>31</issue>
<fpage>12610</fpage>
<lpage>12615</lpage>
<permissions>
<license license-type="open-access">
<license-p>Freely available online through the PNAS open access option.</license-p>
</license>
</permissions>
<self-uri xlink:title="pdf" xlink:type="simple" xlink:href="pnas.201205184.pdf"></self-uri>
<abstract>
<p>The Neotropics have many plant species that seem to be adapted for seed dispersal by megafauna that went extinct in the late Pleistocene. Given the crucial importance of seed dispersal for plant persistence, it remains a mystery how these plants have survived more than 10,000 y without their mutualist dispersers. Here we present support for the hypothesis that secondary seed dispersal by scatter-hoarding rodents has facilitated the persistence of these large-seeded species. We used miniature radio transmitters to track the dispersal of reputedly megafaunal seeds by Central American agoutis, which scatter-hoard seeds in shallow caches in the soil throughout the forest. We found that seeds were initially cached at mostly short distances and then quickly dug up again. However, rather than eating the recovered seeds, agoutis continued to move and recache the seeds, up to 36 times. Agoutis dispersed an estimated 35% of seeds for >100 m. An estimated 14% of the cached seeds survived to the next year, when a new fruit crop became available to the rodents. Serial video-monitoring of cached seeds revealed that the stepwise dispersal was caused by agoutis repeatedly stealing and recaching each other’s buried seeds. Although previous studies suggest that rodents are poor dispersers, we demonstrate that communities of rodents can in fact provide highly effective long-distance seed dispersal. Our findings suggest that thieving scatter-hoarding rodents could substitute for extinct megafaunal seed dispersers of tropical large-seeded trees.</p>
</abstract>
<kwd-group>
<kwd>Pleistocene extinctions</kwd>
<kwd>seed predation</kwd>
<kwd>cache pilferage</kwd>
<kwd>telemetry</kwd>
</kwd-group>
</article-meta>
</front>
</pmc>
</record>

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