A unique coral biomineralization pattern has resisted 40 million years of major ocean chemistry change
Identifieur interne : 000B55 ( Pmc/Checkpoint ); précédent : 000B54; suivant : 000B56A unique coral biomineralization pattern has resisted 40 million years of major ocean chemistry change
Auteurs : Jarosław Stolarski [Pologne] ; Francesca R. Bosellini [Italie] ; Carden C. Wallace [Australie] ; Anne M. Gothmann [États-Unis] ; Maciej Mazur [Pologne] ; Isabelle Domart-Coulon [France] ; Eldad Gutner-Hoch [Israël] ; Rolf D. Neuser [Allemagne] ; Oren Levy [Israël] ; Aldo Shemesh [Israël] ; Anders Meibom [Suisse]Source :
- Scientific Reports [ 2045-2322 ] ; 2016.
Abstract
Today coral reefs are threatened by changes to seawater conditions associated with rapid anthropogenic global climate change. Yet, since the Cenozoic, these organisms have experienced major fluctuations in atmospheric CO2 levels (from greenhouse conditions of high pCO2 in the Eocene to low pCO2 ice-house conditions in the Oligocene-Miocene) and a dramatically changing ocean Mg/Ca ratio. Here we show that the most diverse, widespread, and abundant reef-building coral genus
Url:
DOI: 10.1038/srep27579
PubMed: 27302371
PubMed Central: 4908604
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, 52900 Ramat-Gan,<country>Israel</country>
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<author><name sortKey="Neuser, Rolf D" sort="Neuser, Rolf D" uniqKey="Neuser R" first="Rolf D." last="Neuser">Rolf D. Neuser</name>
<affiliation wicri:level="1"><nlm:aff id="a8"><institution>Institut für Geologie, Mineralogie und Geophysik, Ruhr-Universität Bochum</institution>
, D-44780 Bochum,<country>Germany</country>
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<country xml:lang="fr">Allemagne</country>
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<author><name sortKey="Shemesh, Aldo" sort="Shemesh, Aldo" uniqKey="Shemesh A" first="Aldo" last="Shemesh">Aldo Shemesh</name>
<affiliation wicri:level="1"><nlm:aff id="a9"><institution>Department of Earth and Planetary Sciences, The Weizmann Institute of Science</institution>
, P.O. Box 26, 76100 Rehovot,<country>Israel</country>
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<country xml:lang="fr">Israël</country>
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<author><name sortKey="Meibom, Anders" sort="Meibom, Anders" uniqKey="Meibom A" first="Anders" last="Meibom">Anders Meibom</name>
<affiliation wicri:level="1"><nlm:aff id="a10"><institution>Laboratory for Biological Geochemistry, School of Architecture, Civil and Environmental Engineering (ENAC), Ecole Polytechnique Fédérale de Lausanne (EPFL)</institution>
, CH-1015 Lausanne,<country>Switzerland</country>
</nlm:aff>
<country xml:lang="fr">Suisse</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<affiliation wicri:level="1"><nlm:aff id="a11"><institution>Center for Advanced Surface Analysis, Institute of Earth Sciences, Université de Lausanne</institution>
, CH-1015 Lausanne,<country>Switzerland</country>
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<country xml:lang="fr">Suisse</country>
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<series><title level="j">Scientific Reports</title>
<idno type="eISSN">2045-2322</idno>
<imprint><date when="2016">2016</date>
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<front><div type="abstract" xml:lang="en"><p>Today coral reefs are threatened by changes to seawater conditions associated with rapid anthropogenic global climate change. Yet, since the Cenozoic, these organisms have experienced major fluctuations in atmospheric CO<sub>2</sub>
levels (from greenhouse conditions of high pCO<sub>2</sub>
in the Eocene to low pCO<sub>2</sub>
ice-house conditions in the Oligocene-Miocene) and a dramatically changing ocean Mg/Ca ratio. Here we show that the most diverse, widespread, and abundant reef-building coral genus <italic>Acropora</italic>
(20 morphological groups and 150 living species) has not only survived these environmental changes, but has maintained its distinct skeletal biomineralization pattern for at least 40 My: Well-preserved fossil <italic>Acropora</italic>
skeletons from the Eocene, Oligocene, and Miocene show ultra-structures indistinguishable from those of extant representatives of the genus and their aragonitic skeleton Mg/Ca ratios trace the inferred ocean Mg/Ca ratio precisely since the Eocene. Therefore, among marine biogenic carbonate fossils, well-preserved acroporid skeletons represent material with very high potential for reconstruction of ancient ocean chemistry.</p>
</div>
</front>
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<biblStruct><analytic><author><name sortKey="Richter, D K" uniqKey="Richter D">D. K. Richter</name>
</author>
<author><name sortKey="Immenhauser, A" uniqKey="Immenhauser A">A. Immenhauser</name>
</author>
<author><name sortKey="Neuser, R D" uniqKey="Neuser R">R. D. Neuser</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Brahmi, C" uniqKey="Brahmi C">C. Brahmi</name>
</author>
<author><name sortKey="Kopp, C" uniqKey="Kopp C">C. Kopp</name>
</author>
<author><name sortKey="Domart Coulon, I" uniqKey="Domart Coulon I">I. Domart-Coulon</name>
</author>
<author><name sortKey="Stolarski, J" uniqKey="Stolarski J">J. Stolarski</name>
</author>
<author><name sortKey="Meibom, A" uniqKey="Meibom A">A. Meibom</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Houlbreque, F" uniqKey="Houlbreque F">F. Houlbreque</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Domart Coulon, I" uniqKey="Domart Coulon I">I. Domart-Coulon</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Meibom, A" uniqKey="Meibom A">A. Meibom</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Meibom, A" uniqKey="Meibom A">A. Meibom</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Bice, K L" uniqKey="Bice K">K. L. Bice</name>
</author>
<author><name sortKey="Layne, G D" uniqKey="Layne G">G. D. Layne</name>
</author>
<author><name sortKey="Dahl, K" uniqKey="Dahl K">K. Dahl</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Balthasar, U" uniqKey="Balthasar U">U. Balthasar</name>
</author>
<author><name sortKey="Cusack, M" uniqKey="Cusack M">M. Cusack</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Beerling, D J" uniqKey="Beerling D">D. J. Beerling</name>
</author>
<author><name sortKey="Royer, D L" uniqKey="Royer D">D. L. Royer</name>
</author>
</analytic>
</biblStruct>
</listBibl>
</div1>
</back>
</TEI>
<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Sci Rep</journal-id>
<journal-id journal-id-type="iso-abbrev">Sci Rep</journal-id>
<journal-title-group><journal-title>Scientific Reports</journal-title>
</journal-title-group>
<issn pub-type="epub">2045-2322</issn>
<publisher><publisher-name>Nature Publishing Group</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">27302371</article-id>
<article-id pub-id-type="pmc">4908604</article-id>
<article-id pub-id-type="pii">srep27579</article-id>
<article-id pub-id-type="doi">10.1038/srep27579</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>A unique coral biomineralization pattern has resisted 40 million years of major ocean chemistry change</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Stolarski</surname>
<given-names>Jarosław</given-names>
</name>
<xref ref-type="corresp" rid="c1">a</xref>
<xref ref-type="aff" rid="a1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bosellini</surname>
<given-names>Francesca R.</given-names>
</name>
<xref ref-type="aff" rid="a2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wallace</surname>
<given-names>Carden C.</given-names>
</name>
<xref ref-type="aff" rid="a3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Gothmann</surname>
<given-names>Anne M.</given-names>
</name>
<xref ref-type="aff" rid="a4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Mazur</surname>
<given-names>Maciej</given-names>
</name>
<xref ref-type="aff" rid="a5">5</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Domart-Coulon</surname>
<given-names>Isabelle</given-names>
</name>
<xref ref-type="aff" rid="a6">6</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Gutner-Hoch</surname>
<given-names>Eldad</given-names>
</name>
<xref ref-type="aff" rid="a7">7</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Neuser</surname>
<given-names>Rolf D.</given-names>
</name>
<xref ref-type="aff" rid="a8">8</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Levy</surname>
<given-names>Oren</given-names>
</name>
<xref ref-type="aff" rid="a7">7</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Shemesh</surname>
<given-names>Aldo</given-names>
</name>
<xref ref-type="aff" rid="a9">9</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Meibom</surname>
<given-names>Anders</given-names>
</name>
<xref ref-type="aff" rid="a10">10</xref>
<xref ref-type="aff" rid="a11">11</xref>
</contrib>
<aff id="a1"><label>1</label>
<institution>Institute of Paleobiology, Polish Academy of Sciences</institution>
, Twarda 51/55, PL-00-818 Warsaw,<country>Poland</country>
</aff>
<aff id="a2"><label>2</label>
<institution>Dipartimento di Scienze Chimiche e Geologiche, Università di Modena e Reggio Emilia</institution>
, Via Campi 103, 41125 Modena,<country>Italy</country>
</aff>
<aff id="a3"><label>3</label>
<institution>Biodiversity & Geosciences Program, Queensland Museum</institution>
, South Brisbane, Qld 4101,<country>Australia</country>
</aff>
<aff id="a4"><label>4</label>
<institution>University of Washington, School of Oceanography</institution>
, Box 357940, WA 98195-7940, Seattle,<country>USA</country>
</aff>
<aff id="a5"><label>5</label>
<institution>Department of Chemistry, University of Warsaw</institution>
, Pasteura 1, 02-093 Warsaw,<country>Poland</country>
</aff>
<aff id="a6"><label>6</label>
<institution>MCAM UMR7245 Muséum National d’Histoire Naturelle - CNRS, Sorbonne-Universités</institution>
, Paris,<country>France</country>
</aff>
<aff id="a7"><label>7</label>
<institution>The Mina & Everard Goodman Faculty of Life Science, Bar-Ilan University</institution>
, 52900 Ramat-Gan,<country>Israel</country>
</aff>
<aff id="a8"><label>8</label>
<institution>Institut für Geologie, Mineralogie und Geophysik, Ruhr-Universität Bochum</institution>
, D-44780 Bochum,<country>Germany</country>
</aff>
<aff id="a9"><label>9</label>
<institution>Department of Earth and Planetary Sciences, The Weizmann Institute of Science</institution>
, P.O. Box 26, 76100 Rehovot,<country>Israel</country>
</aff>
<aff id="a10"><label>10</label>
<institution>Laboratory for Biological Geochemistry, School of Architecture, Civil and Environmental Engineering (ENAC), Ecole Polytechnique Fédérale de Lausanne (EPFL)</institution>
, CH-1015 Lausanne,<country>Switzerland</country>
</aff>
<aff id="a11"><label>11</label>
<institution>Center for Advanced Surface Analysis, Institute of Earth Sciences, Université de Lausanne</institution>
, CH-1015 Lausanne,<country>Switzerland</country>
</aff>
</contrib-group>
<author-notes><corresp id="c1"><label>a</label>
<email>stolacy@twarda.pan.pl</email>
</corresp>
</author-notes>
<pub-date pub-type="epub"><day>15</day>
<month>06</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection"><year>2016</year>
</pub-date>
<volume>6</volume>
<elocation-id>27579</elocation-id>
<history><date date-type="received"><day>14</day>
<month>12</month>
<year>2015</year>
</date>
<date date-type="accepted"><day>17</day>
<month>05</month>
<year>2016</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2016, Macmillan Publishers Limited</copyright-statement>
<copyright-year>2016</copyright-year>
<copyright-holder>Macmillan Publishers Limited</copyright-holder>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/4.0/"><pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>
</license-p>
</license>
</permissions>
<abstract><p>Today coral reefs are threatened by changes to seawater conditions associated with rapid anthropogenic global climate change. Yet, since the Cenozoic, these organisms have experienced major fluctuations in atmospheric CO<sub>2</sub>
levels (from greenhouse conditions of high pCO<sub>2</sub>
in the Eocene to low pCO<sub>2</sub>
ice-house conditions in the Oligocene-Miocene) and a dramatically changing ocean Mg/Ca ratio. Here we show that the most diverse, widespread, and abundant reef-building coral genus <italic>Acropora</italic>
(20 morphological groups and 150 living species) has not only survived these environmental changes, but has maintained its distinct skeletal biomineralization pattern for at least 40 My: Well-preserved fossil <italic>Acropora</italic>
skeletons from the Eocene, Oligocene, and Miocene show ultra-structures indistinguishable from those of extant representatives of the genus and their aragonitic skeleton Mg/Ca ratios trace the inferred ocean Mg/Ca ratio precisely since the Eocene. Therefore, among marine biogenic carbonate fossils, well-preserved acroporid skeletons represent material with very high potential for reconstruction of ancient ocean chemistry.</p>
</abstract>
</article-meta>
</front>
<floats-group><fig id="f1"><label>Figure 1</label>
<caption><title>Skeleton texture and structure in Recent <italic>Acropora</italic>
.</title>
<p>(<bold>a</bold>
) lateral view of a branch of <italic>A</italic>
. <italic>eurystoma</italic>
(ZPAL H.25/118(966)) with large axial corallite (opening at tip) and smaller lateral corallites (arrow indicates region enlarged in Fig. 1b and sectioned in <xref ref-type="fig" rid="f2">Fig. 2a</xref>
), (<bold>b</bold>
) the most striking feature of the skeleton surface of <italic>Acropora</italic>
(here <italic>A</italic>
. <italic>eurystoma</italic>
) is its texture in the form of regular shingles which are aligned along the extensional direction of the structures they build (black arrow). Shingles cover the entire skeleton surface except of regions of the fast growth which tend to be more smooth. The shingles show incremental growth every ca. 3–4 μm (yellow arrows in enlargement), (<bold>c</bold>
) incremental growth lines of shingles in thin-sectioned skeleton of <italic>Acropora muricata</italic>
(ZPAL H.25/90(535B), (<bold>d</bold>
,<bold>e</bold>
) distal portions of coenosteal spinulae and short septal spines (<bold>d</bold>
, <italic>A. cervicornis</italic>
, ZPAL H.25/12(545); (<bold>e</bold>
) <italic>A. eurystoma</italic>
ZPAL H.25/118(966)) are relatively smooth (red arrows) in contrast to the rest of the skeleton, which exhibits the shingle structure. (<bold>f</bold>
,<bold>g</bold>
) extremely slender (orange arrows in <bold>g</bold>
) bundles of fibers form the edge of the growing front of shingles in <italic>A. muricata</italic>
, ZPAL H.25/90(535B). Fibers are aligned parallel to the surface of the skeleton.</p>
</caption>
<graphic xlink:href="srep27579-f1"></graphic>
</fig>
<fig id="f2"><label>Figure 2</label>
<caption><title>Microstructure and differentiation of shingles near the tip of coenosteal spinulae visualized by <sup>86</sup>
Sr labeling in Recent <italic>Acropora</italic>
(<italic>A. eurystoma</italic>
, ZPAL H.25/118(966)).</title>
<p>(<bold>a</bold>
) longitudinal section along the fast growing skeletal regions includes spinulae (yellow arrows), RAD (red arrows) and shingles (blue arrows). Ultra-thin transverse section (<bold>b</bold>
), polarized light)) and polished, slightly etched section (<bold>c</bold>
) reveal longitudinal sections of shingles bundles of fibers several hundreds of micrometers long (dashed arrow in (<bold>b</bold>
)), suggesting continuous growth of individual shingles, (<bold>d</bold>
) NanoSIMS <sup>86</sup>
Sr/<sup>44</sup>
Ca isotope mosaic map, (<bold>e</bold>
) SEM image of polished and etched sample, (<bold>f</bold>
) NanoSIMS and SEM images overlaid. <sup>86</sup>
Sr-labeling pulses (12 hours, separated by 36 hours, orange-yellow color) are continuous in the distal part of the spinula and discontinuous below, where shingles are forming. Blue regions represent skeleton with normal <sup>86</sup>
Sr/<sup>44</sup>
Ca ratio. Red lines with circles in d an e indicate RAD labeled with <sup>86</sup>
Sr. Dashed white line in e and f outlines the RAD region.</p>
</caption>
<graphic xlink:href="srep27579-f2"></graphic>
</fig>
<fig id="f3"><label>Figure 3</label>
<caption><title>Phylogenetic relationships of Recent acroporid taxa and their skeleton surface textures.</title>
<p>(<bold>a</bold>
) phylogenetic tree inferred by Bayesian analysis of combined mitochondrial cox1 and cob DNA sequences<xref ref-type="bibr" rid="b3">3</xref>
. All acroporids show shingled thickening deposits (<bold>b</bold>
,<bold>c</bold>
,<bold>e</bold>
–<bold>i</bold>
) but their arrangement and sizes differ among taxa (usually a species-level character), (<bold>d</bold>
) there are 3 major size-classes of shingles within the genus <italic>Acropora</italic>
, defined as the distance between the growing fronts of overlapping shingles (yellow arrows in <bold>b</bold>
,<bold>c</bold>
,<bold>e</bold>
–<bold>i</bold>
): (<bold>b</bold>
), <italic>Acropora echinata</italic>
(ZPAL H.25/83(534B)) illustrates small shingles, (<bold>c</bold>
) <italic>Acropora elegans</italic>
(ZPAL H.25/84(538A) illustrates large shingles. Shingles in other acroporids are illustrated with <italic>Alveopora allingi</italic>
(<bold>e</bold>
), ZPAL H.25/72(550A), <italic>Isopora crateriformis</italic>
(<bold>f</bold>
), ZPAL H.25/79(548), <italic>Anacropora forbesi</italic>
(<bold>g</bold>
), ZPAL H.25/87(800), <italic>Montipora verrucosa</italic>
(<bold>h</bold>
), ZPAL H.25/116(804), and <italic>Astreopora myriophtalma</italic>
(<bold>i</bold>
), ZPAL H.25/103(799). SEM images. Other examples are provided in <xref ref-type="supplementary-material" rid="S1">SI-Figs 2–5</xref>
.</p>
</caption>
<graphic xlink:href="srep27579-f3"></graphic>
</fig>
<fig id="f4"><label>Figure 4</label>
<caption><title>Example of good preservation of skeletal features (mineralogy, surface texture and microstructure) in fossil <italic>Acropora</italic>
.</title>
<p><italic>Acropora</italic>
sp. ZPAL H.27/20(C21), Oligocene (Chattian), Saint-Paul-lès-Dax, France. (<bold>a</bold>
) transverse section of corallum branch with white rectangle (enlargement in (<bold>d</bold>
)) indicating region analyzed with micro-Raman (<bold>g</bold>
,<bold>h</bold>
); shingled thickening deposits marked with yellow and region of rapid accretion deposits with red arrows. Surface of the branch with lateral corallites and coenosteum (<bold>b</bold>
). Enlargment of the calice surface (<bold>c</bold>
) with desmocyte attachment scars (orange arrows). Shingled thickening deposits, (yellow arrows in (<bold>e</bold>
,<bold>f</bold>
)) are still discernible, although this feature usually is the first that is eroded. Micro-Raman maps (<bold>g</bold>
,<bold>h</bold>
) of region indicated in d: aragonite lattice mode at 203 cm<sup>−1</sup>
(<bold>g</bold>
), and carbonate vibrational mode at 1085 cm<sup>−1</sup>
(<bold>h</bold>
) to show that skeleton is entirely aragonite. RAD are composed of more compact skeletal tissue in comparison to TD deposits and consequently epoxy impregnated only TD deposits (black areas), (<bold>i</bold>
) contact zone (polished and etched surface) between RAD and TD (shingles) deposits. Note regular increment lines in RAD and elongated bundles of fibers composing TD.</p>
</caption>
<graphic xlink:href="srep27579-f4"></graphic>
</fig>
<fig id="f5"><label>Figure 5</label>
<caption><title>Evolutionary continuity of shingle-like biomineralization pattern in <italic>Acropora</italic>
lineage.</title>
<p>(<bold>a</bold>
–<bold>d</bold>
) Direct comparison of microstructural features of modern (<bold>a</bold>
) and fossil (<bold>b</bold>
–<bold>d</bold>
) aragonite skeletons of <italic>Acropora</italic>
showing evidence of continuous growth of shingles. Shown are ultra-thin transverse sections (polarized transmitted light, crossed Nicols) of: (<bold>a</bold>
) extant <italic>A</italic>
. <italic>muricata</italic>
(ZPAL H.25/90(535B)), (<bold>b</bold>
) Miocene (Burdigalian) <italic>Acropora exerata</italic>
(ZPAL H.27/28(C56)), (<bold>c</bold>
) Miocene (Aquitanian) <italic>Acropora</italic>
sp. (ZPAL H.27/23(C54)); (<bold>d</bold>
) Middle Eocene <italic>Acropora alvarezi</italic>
(ZPAL H.27/18(C100)), (<bold>e</bold>
) regular incremental growth lines (yellow arrows) in shingled thickening deposits in Miocene (Aquitanian) <italic>Acropora</italic>
sp. (ZPAL H.27/23(C54).</p>
</caption>
<graphic xlink:href="srep27579-f5"></graphic>
</fig>
<fig id="f6"><label>Figure 6</label>
<caption><title>Evolutionary continuity of shingle-like biomineralization pattern in <italic>Acropora</italic>
lineage across geochemical gradients.</title>
<p>Seawater Mg/Ca composition during last 100 Ma inferred from diverse well preserved fossil corals (grey circles) following Gothman <italic>et al</italic>
.<xref ref-type="bibr" rid="b29">29</xref>
. Red circles represent Mg/Ca of seawater inferred from extant (ZPAL H.25/12(545), ZPAL H.25/86(802), ZPAL H.25/80(543A)) and best preserved aragonite fossil <italic>Acropora</italic>
samples (C-SCL-56, ZPAL H.27/23(C54), ZPAL H.27/20(C21), ZPAL H.27/18(C100)). Red, dashed line is the seawater Mg/Ca reconstruction based on halite fluid inclusions (blue dots)<xref ref-type="bibr" rid="b32">32</xref>
. Conventionally Mg/Ca of 2 was considered a boundary between aragonite and calcite precipitation (aragonite/calcite seas) but recent experiments<xref ref-type="bibr" rid="b40">40</xref>
show that there is a gradual and temperature-dependent shift in calcium carbonate polymorph proportions. Green curve indicates estimates of atmospheric CO<sub>2</sub>
reconstructed from terrestrial and marine proxies<xref ref-type="bibr" rid="b41">41</xref>
. Horizontal dashed green line indicates the present-day atmospheric CO<sub>2</sub>
concentration (ca. 400 ppm).</p>
</caption>
<graphic xlink:href="srep27579-f6"></graphic>
</fig>
</floats-group>
</pmc>
<affiliations><list><country><li>Allemagne</li>
<li>Australie</li>
<li>France</li>
<li>Israël</li>
<li>Italie</li>
<li>Pologne</li>
<li>Suisse</li>
<li>États-Unis</li>
</country>
</list>
<tree><country name="Pologne"><noRegion><name sortKey="Stolarski, Jaroslaw" sort="Stolarski, Jaroslaw" uniqKey="Stolarski J" first="Jarosław" last="Stolarski">Jarosław Stolarski</name>
</noRegion>
<name sortKey="Mazur, Maciej" sort="Mazur, Maciej" uniqKey="Mazur M" first="Maciej" last="Mazur">Maciej Mazur</name>
</country>
<country name="Italie"><noRegion><name sortKey="Bosellini, Francesca R" sort="Bosellini, Francesca R" uniqKey="Bosellini F" first="Francesca R." last="Bosellini">Francesca R. Bosellini</name>
</noRegion>
</country>
<country name="Australie"><noRegion><name sortKey="Wallace, Carden C" sort="Wallace, Carden C" uniqKey="Wallace C" first="Carden C." last="Wallace">Carden C. Wallace</name>
</noRegion>
</country>
<country name="États-Unis"><noRegion><name sortKey="Gothmann, Anne M" sort="Gothmann, Anne M" uniqKey="Gothmann A" first="Anne M." last="Gothmann">Anne M. Gothmann</name>
</noRegion>
</country>
<country name="France"><noRegion><name sortKey="Domart Coulon, Isabelle" sort="Domart Coulon, Isabelle" uniqKey="Domart Coulon I" first="Isabelle" last="Domart-Coulon">Isabelle Domart-Coulon</name>
</noRegion>
</country>
<country name="Israël"><noRegion><name sortKey="Gutner Hoch, Eldad" sort="Gutner Hoch, Eldad" uniqKey="Gutner Hoch E" first="Eldad" last="Gutner-Hoch">Eldad Gutner-Hoch</name>
</noRegion>
<name sortKey="Levy, Oren" sort="Levy, Oren" uniqKey="Levy O" first="Oren" last="Levy">Oren Levy</name>
<name sortKey="Shemesh, Aldo" sort="Shemesh, Aldo" uniqKey="Shemesh A" first="Aldo" last="Shemesh">Aldo Shemesh</name>
</country>
<country name="Allemagne"><noRegion><name sortKey="Neuser, Rolf D" sort="Neuser, Rolf D" uniqKey="Neuser R" first="Rolf D." last="Neuser">Rolf D. Neuser</name>
</noRegion>
</country>
<country name="Suisse"><noRegion><name sortKey="Meibom, Anders" sort="Meibom, Anders" uniqKey="Meibom A" first="Anders" last="Meibom">Anders Meibom</name>
</noRegion>
<name sortKey="Meibom, Anders" sort="Meibom, Anders" uniqKey="Meibom A" first="Anders" last="Meibom">Anders Meibom</name>
</country>
</tree>
</affiliations>
</record>
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