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<title xml:lang="en">Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution</title>
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<name sortKey="Feild, Taylor S" sort="Feild, Taylor S" uniqKey="Feild T" first="Taylor S." last="Feild">Taylor S. Feild</name>
<affiliation>
<nlm:aff id="aff1">Department of Ecology and Evolutionary Biology,
<institution>University of Tennessee</institution>
, Knoxville,
<country>TN 37996</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Brodribb, Timothy J" sort="Brodribb, Timothy J" uniqKey="Brodribb T" first="Timothy J." last="Brodribb">Timothy J. Brodribb</name>
<affiliation>
<nlm:aff id="aff2">Department of Plant Science,
<institution>University of Tasmania</institution>
, Hobart, 7001 Tasmania,
<country>Australia</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Iglesias, Ari" sort="Iglesias, Ari" uniqKey="Iglesias A" first="Ari" last="Iglesias">Ari Iglesias</name>
<affiliation>
<nlm:aff id="aff3">Facultad de Ciencias Naturales y Museo,
<institution>Universidad Nacional de La Plata</institution>
, 1900 La Plata,
<country>Argentina</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Chatelet, David S" sort="Chatelet, David S" uniqKey="Chatelet D" first="David S." last="Chatelet">David S. Chatelet</name>
<affiliation>
<nlm:aff id="aff4">Department of Ecology and Evolutionary Biology,
<institution>Brown University</institution>
, Providence, RI 02912;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Baresch, Andres" sort="Baresch, Andres" uniqKey="Baresch A" first="Andres" last="Baresch">Andres Baresch</name>
<affiliation>
<nlm:aff id="aff5">
<institution>Smithsonian Tropical Research Institute</institution>
, Balboa,
<country>Panama</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Upchurch, Garland R" sort="Upchurch, Garland R" uniqKey="Upchurch G" first="Garland R." last="Upchurch">Garland R. Upchurch</name>
<affiliation>
<nlm:aff id="aff6">Department of Biology,
<institution>Texas State University</institution>
, San Marcos, TX 78666;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Gomez, Bernard" sort="Gomez, Bernard" uniqKey="Gomez B" first="Bernard" last="Gomez">Bernard Gomez</name>
<affiliation>
<nlm:aff id="aff7">Université Lyon 1,
<institution>Centre National de la Recherche Scientifique-Unité Mixte de Recherche 5125</institution>
, Paléoenvironnements et Paléobiosphère, Villeurbanne,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Mohr, Barbara A R" sort="Mohr, Barbara A R" uniqKey="Mohr B" first="Barbara A. R." last="Mohr">Barbara A. R. Mohr</name>
<affiliation>
<nlm:aff wicri:cut="; and" id="aff8">Collections,
<institution>Museum of Natural History</institution>
, 10 115 Berlin,
<country>Germany</country>
</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Coiffard, Clement" sort="Coiffard, Clement" uniqKey="Coiffard C" first="Clement" last="Coiffard">Clement Coiffard</name>
<affiliation>
<nlm:aff wicri:cut="; and" id="aff8">Collections,
<institution>Museum of Natural History</institution>
, 10 115 Berlin,
<country>Germany</country>
</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Kvacek, Jiri" sort="Kvacek, Jiri" uniqKey="Kvacek J" first="Jiri" last="Kvacek">Jiri Kvacek</name>
<affiliation>
<nlm:aff id="aff9">National Museum, Prague,
<country>Czech Republic</country>
</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Jaramillo, Carlos" sort="Jaramillo, Carlos" uniqKey="Jaramillo C" first="Carlos" last="Jaramillo">Carlos Jaramillo</name>
<affiliation>
<nlm:aff id="aff5">
<institution>Smithsonian Tropical Research Institute</institution>
, Balboa,
<country>Panama</country>
;</nlm:aff>
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<idno type="doi">10.1073/pnas.1014456108</idno>
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<title xml:lang="en" level="a" type="main">Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution</title>
<author>
<name sortKey="Feild, Taylor S" sort="Feild, Taylor S" uniqKey="Feild T" first="Taylor S." last="Feild">Taylor S. Feild</name>
<affiliation>
<nlm:aff id="aff1">Department of Ecology and Evolutionary Biology,
<institution>University of Tennessee</institution>
, Knoxville,
<country>TN 37996</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Brodribb, Timothy J" sort="Brodribb, Timothy J" uniqKey="Brodribb T" first="Timothy J." last="Brodribb">Timothy J. Brodribb</name>
<affiliation>
<nlm:aff id="aff2">Department of Plant Science,
<institution>University of Tasmania</institution>
, Hobart, 7001 Tasmania,
<country>Australia</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Iglesias, Ari" sort="Iglesias, Ari" uniqKey="Iglesias A" first="Ari" last="Iglesias">Ari Iglesias</name>
<affiliation>
<nlm:aff id="aff3">Facultad de Ciencias Naturales y Museo,
<institution>Universidad Nacional de La Plata</institution>
, 1900 La Plata,
<country>Argentina</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Chatelet, David S" sort="Chatelet, David S" uniqKey="Chatelet D" first="David S." last="Chatelet">David S. Chatelet</name>
<affiliation>
<nlm:aff id="aff4">Department of Ecology and Evolutionary Biology,
<institution>Brown University</institution>
, Providence, RI 02912;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Baresch, Andres" sort="Baresch, Andres" uniqKey="Baresch A" first="Andres" last="Baresch">Andres Baresch</name>
<affiliation>
<nlm:aff id="aff5">
<institution>Smithsonian Tropical Research Institute</institution>
, Balboa,
<country>Panama</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Upchurch, Garland R" sort="Upchurch, Garland R" uniqKey="Upchurch G" first="Garland R." last="Upchurch">Garland R. Upchurch</name>
<affiliation>
<nlm:aff id="aff6">Department of Biology,
<institution>Texas State University</institution>
, San Marcos, TX 78666;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Gomez, Bernard" sort="Gomez, Bernard" uniqKey="Gomez B" first="Bernard" last="Gomez">Bernard Gomez</name>
<affiliation>
<nlm:aff id="aff7">Université Lyon 1,
<institution>Centre National de la Recherche Scientifique-Unité Mixte de Recherche 5125</institution>
, Paléoenvironnements et Paléobiosphère, Villeurbanne,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Mohr, Barbara A R" sort="Mohr, Barbara A R" uniqKey="Mohr B" first="Barbara A. R." last="Mohr">Barbara A. R. Mohr</name>
<affiliation>
<nlm:aff wicri:cut="; and" id="aff8">Collections,
<institution>Museum of Natural History</institution>
, 10 115 Berlin,
<country>Germany</country>
</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Coiffard, Clement" sort="Coiffard, Clement" uniqKey="Coiffard C" first="Clement" last="Coiffard">Clement Coiffard</name>
<affiliation>
<nlm:aff wicri:cut="; and" id="aff8">Collections,
<institution>Museum of Natural History</institution>
, 10 115 Berlin,
<country>Germany</country>
</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Kvacek, Jiri" sort="Kvacek, Jiri" uniqKey="Kvacek J" first="Jiri" last="Kvacek">Jiri Kvacek</name>
<affiliation>
<nlm:aff id="aff9">National Museum, Prague,
<country>Czech Republic</country>
</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Jaramillo, Carlos" sort="Jaramillo, Carlos" uniqKey="Jaramillo C" first="Carlos" last="Jaramillo">Carlos Jaramillo</name>
<affiliation>
<nlm:aff id="aff5">
<institution>Smithsonian Tropical Research Institute</institution>
, Balboa,
<country>Panama</country>
;</nlm:aff>
</affiliation>
</author>
</analytic>
<series>
<title level="j">Proceedings of the National Academy of Sciences of the United States of America</title>
<idno type="ISSN">0027-8424</idno>
<idno type="eISSN">1091-6490</idno>
<imprint>
<date when="2011">2011</date>
</imprint>
</series>
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<front>
<div type="abstract" xml:lang="en">
<p>The flowering plants that dominate modern vegetation possess leaf gas exchange potentials that far exceed those of all other living or extinct plants. The great divide in maximal ability to exchange CO
<sub>2</sub>
for water between leaves of nonangiosperms and angiosperms forms the mechanistic foundation for speculation about how angiosperms drove sweeping ecological and biogeochemical change during the Cretaceous. However, there is no empirical evidence that angiosperms evolved highly photosynthetically active leaves during the Cretaceous. Using vein density (
<italic>D</italic>
<sub>V</sub>
) measurements of fossil angiosperm leaves, we show that the leaf hydraulic capacities of angiosperms escalated several-fold during the Cretaceous. During the first 30 million years of angiosperm leaf evolution, angiosperm leaves exhibited uniformly low vein
<italic>D</italic>
<sub>V</sub>
that overlapped the
<italic>D</italic>
<sub>V</sub>
range of dominant Early Cretaceous ferns and gymnosperms. Fossil angiosperm vein densities reveal a subsequent biphasic increase in
<italic>D</italic>
<sub>V</sub>
. During the first mid-Cretaceous surge, angiosperm
<italic>D</italic>
<sub>V</sub>
first surpassed the upper bound of
<italic>D</italic>
<sub>V</sub>
limits for nonangiosperms. However, the upper limits of
<italic>D</italic>
<sub>V</sub>
typical of modern megathermal rainforest trees first appear during a second wave of increased
<italic>D</italic>
<sub>V</sub>
during the Cretaceous-Tertiary transition. Thus, our findings provide fossil evidence for the hypothesis that significant ecosystem change brought about by angiosperms lagged behind the Early Cretaceous taxonomic diversification of angiosperms.</p>
</div>
</front>
</TEI>
<pmc article-type="research-article">
<pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">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>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">21536892</article-id>
<article-id pub-id-type="pmc">3100944</article-id>
<article-id pub-id-type="publisher-id">201014456</article-id>
<article-id pub-id-type="doi">10.1073/pnas.1014456108</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Biological Sciences</subject>
<subj-group>
<subject>Evolution</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Feild</surname>
<given-names>Taylor S.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
<xref ref-type="corresp" rid="cor1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Brodribb</surname>
<given-names>Timothy J.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Iglesias</surname>
<given-names>Ari</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Chatelet</surname>
<given-names>David S.</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Baresch</surname>
<given-names>Andres</given-names>
</name>
<xref ref-type="aff" rid="aff5">
<sup>e</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Upchurch</surname>
<given-names>Garland R.</given-names>
<suffix>Jr.</suffix>
</name>
<xref ref-type="aff" rid="aff6">
<sup>f</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Gomez</surname>
<given-names>Bernard</given-names>
</name>
<xref ref-type="aff" rid="aff7">
<sup>g</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Mohr</surname>
<given-names>Barbara A. R.</given-names>
</name>
<xref ref-type="aff" rid="aff8">
<sup>h</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Coiffard</surname>
<given-names>Clement</given-names>
</name>
<xref ref-type="aff" rid="aff8">
<sup>h</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Kvacek</surname>
<given-names>Jiri</given-names>
</name>
<xref ref-type="aff" rid="aff9">
<sup>i</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Jaramillo</surname>
<given-names>Carlos</given-names>
</name>
<xref ref-type="aff" rid="aff5">
<sup>e</sup>
</xref>
</contrib>
<aff id="aff1">
<sup>a</sup>
Department of Ecology and Evolutionary Biology,
<institution>University of Tennessee</institution>
, Knoxville,
<country>TN 37996</country>
;</aff>
<aff id="aff2">
<sup>b</sup>
Department of Plant Science,
<institution>University of Tasmania</institution>
, Hobart, 7001 Tasmania,
<country>Australia</country>
;</aff>
<aff id="aff3">
<sup>c</sup>
Facultad de Ciencias Naturales y Museo,
<institution>Universidad Nacional de La Plata</institution>
, 1900 La Plata,
<country>Argentina</country>
;</aff>
<aff id="aff4">
<sup>d</sup>
Department of Ecology and Evolutionary Biology,
<institution>Brown University</institution>
, Providence, RI 02912;</aff>
<aff id="aff5">
<sup>e</sup>
<institution>Smithsonian Tropical Research Institute</institution>
, Balboa,
<country>Panama</country>
;</aff>
<aff id="aff6">
<sup>f</sup>
Department of Biology,
<institution>Texas State University</institution>
, San Marcos, TX 78666;</aff>
<aff id="aff7">
<sup>g</sup>
Université Lyon 1,
<institution>Centre National de la Recherche Scientifique-Unité Mixte de Recherche 5125</institution>
, Paléoenvironnements et Paléobiosphère, Villeurbanne,
<country>France</country>
;</aff>
<aff id="aff8">
<sup>h</sup>
Collections,
<institution>Museum of Natural History</institution>
, 10 115 Berlin,
<country>Germany</country>
; and</aff>
<aff id="aff9">
<sup>i</sup>
National Museum, Prague,
<country>Czech Republic</country>
</aff>
</contrib-group>
<author-notes>
<corresp id="cor1">
<sup>1</sup>
To whom correspondence should be addressed. E-mail:
<email>hedyosmum@gmail.com</email>
.</corresp>
<fn fn-type="edited-by">
<p>Edited by Peter Crane, Yale School of Forestry and Environmental Studies, New Haven, CT, and approved April 4, 2011 (received for review September 26, 2010)</p>
</fn>
<fn fn-type="con">
<p>Author contributions: T.S.F. designed research; T.S.F., A.I., D.S.C., A.B., G.R.U., B.G., B.A.R.M., C.C., J.K., and C.J. performed research; T.S.F., T.J.B., and A.I. analyzed data; and T.S.F., T.J.B., A.I., G.R.U., B.G., B.A.R.M., C.C., J.K., and C.J. wrote the paper.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub">
<day>17</day>
<month>5</month>
<year>2011</year>
</pub-date>
<pub-date pub-type="epub">
<day>2</day>
<month>5</month>
<year>2011</year>
</pub-date>
<volume>108</volume>
<issue>20</issue>
<fpage>8363</fpage>
<lpage>8366</lpage>
<self-uri xlink:title="pdf" xlink:type="simple" xlink:href="pnas.201014456.pdf"></self-uri>
<abstract>
<p>The flowering plants that dominate modern vegetation possess leaf gas exchange potentials that far exceed those of all other living or extinct plants. The great divide in maximal ability to exchange CO
<sub>2</sub>
for water between leaves of nonangiosperms and angiosperms forms the mechanistic foundation for speculation about how angiosperms drove sweeping ecological and biogeochemical change during the Cretaceous. However, there is no empirical evidence that angiosperms evolved highly photosynthetically active leaves during the Cretaceous. Using vein density (
<italic>D</italic>
<sub>V</sub>
) measurements of fossil angiosperm leaves, we show that the leaf hydraulic capacities of angiosperms escalated several-fold during the Cretaceous. During the first 30 million years of angiosperm leaf evolution, angiosperm leaves exhibited uniformly low vein
<italic>D</italic>
<sub>V</sub>
that overlapped the
<italic>D</italic>
<sub>V</sub>
range of dominant Early Cretaceous ferns and gymnosperms. Fossil angiosperm vein densities reveal a subsequent biphasic increase in
<italic>D</italic>
<sub>V</sub>
. During the first mid-Cretaceous surge, angiosperm
<italic>D</italic>
<sub>V</sub>
first surpassed the upper bound of
<italic>D</italic>
<sub>V</sub>
limits for nonangiosperms. However, the upper limits of
<italic>D</italic>
<sub>V</sub>
typical of modern megathermal rainforest trees first appear during a second wave of increased
<italic>D</italic>
<sub>V</sub>
during the Cretaceous-Tertiary transition. Thus, our findings provide fossil evidence for the hypothesis that significant ecosystem change brought about by angiosperms lagged behind the Early Cretaceous taxonomic diversification of angiosperms.</p>
</abstract>
<kwd-group>
<kwd>angiosperm evolution</kwd>
<kwd>plant evolution</kwd>
<kwd>transpiration</kwd>
<kwd>tropical rainforest</kwd>
<kwd>venation</kwd>
</kwd-group>
</article-meta>
</front>
</pmc>
</record>

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