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First Reported Cases of Biomechanically Adaptive Bone Modeling in Non-Avian Dinosaurs

Identifieur interne : 000022 ( Pmc/Curation ); précédent : 000021; suivant : 000023

First Reported Cases of Biomechanically Adaptive Bone Modeling in Non-Avian Dinosaurs

Auteurs : Jorge Cubo [France] ; Holly Woodward [États-Unis] ; Ewan Wolff [États-Unis] ; John R. Horner [États-Unis]

Source :

RBID : PMC:4495995

Abstract

Predator confrontation or predator evasion frequently produces bone fractures in potential prey in the wild. Although there are reports of healed bone injuries and pathologies in non-avian dinosaurs, no previously published instances of biomechanically adaptive bone modeling exist. Two tibiae from an ontogenetic sample of fifty specimens of the herbivorous dinosaur Maiasaura peeblesorum (Ornithopoda: Hadrosaurinae) exhibit exostoses. We show that these outgrowths are cases of biomechanically adaptive periosteal bone modeling resulting from overstrain on the tibia after a fibula fracture. Histological and biomechanical results are congruent with predictions derived from this hypothesis. Histologically, the outgrowths are constituted by radial fibrolamellar periosteal bone tissue formed at very high growth rates, as expected in a process of rapid strain equilibration response. These outgrowths show greater compactness at the periphery, where tensile and compressive biomechanical constraints are higher. Moreover, these outgrowths increase the maximum bending strength in the direction of the stresses derived from locomotion. They are located on the antero-lateral side of the tibia, as expected in a presumably bipedal one year old individual, and in the posterior position of the tibia, as expected in a presumably quadrupedal individual at least four years of age. These results reinforce myological evidence suggesting that Maiasaura underwent an ontogenetic shift from the primitive ornithischian bipedal condition when young to a derived quadrupedal posture when older.


Url:
DOI: 10.1371/journal.pone.0131131
PubMed: 26153689
PubMed Central: 4495995

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PMC:4495995

Le document en format XML

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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 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">26153689</article-id>
<article-id pub-id-type="pmc">4495995</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0131131</article-id>
<article-id pub-id-type="publisher-id">PONE-D-15-12202</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>First Reported Cases of Biomechanically Adaptive Bone Modeling in Non-Avian Dinosaurs</article-title>
<alt-title alt-title-type="running-head">Biomechanically Adaptive Bone Modeling in
<italic>Maiasaura</italic>
</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Cubo</surname>
<given-names>Jorge</given-names>
</name>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff002">
<sup>2</sup>
</xref>
<xref rid="cor001" ref-type="corresp">*</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Woodward</surname>
<given-names>Holly</given-names>
</name>
<xref ref-type="aff" rid="aff003">
<sup>3</sup>
</xref>
<xref ref-type="aff" rid="aff004">
<sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Wolff</surname>
<given-names>Ewan</given-names>
</name>
<xref ref-type="aff" rid="aff005">
<sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Horner</surname>
<given-names>John R.</given-names>
</name>
<xref ref-type="aff" rid="aff003">
<sup>3</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff001">
<label>1</label>
<addr-line>Sorbonne Universités, UPMC Univ Paris 06, UMR 7193, Institut des Sciences de la Terre Paris (iSTeP), 4 Place Jussieu, BC19, F-75005, Paris, France</addr-line>
</aff>
<aff id="aff002">
<label>2</label>
<addr-line>CNRS, UMR 7193, Institut des Sciences de la Terre Paris (iSTeP), F-75005, Paris, France</addr-line>
</aff>
<aff id="aff003">
<label>3</label>
<addr-line>Montana State University, Museum of the Rockies, 600 West Kagy Boulevard, Bozeman, Montana, 59717, United States of America</addr-line>
</aff>
<aff id="aff004">
<label>4</label>
<addr-line>Department of Anatomy and Cell Biology, Oklahoma State University Center for Health Sciences, 1111 W. 17th St., Tulsa, OK, 74107, United States of America</addr-line>
</aff>
<aff id="aff005">
<label>5</label>
<addr-line>Small Animal Internal Medicine, Purdue University College of Veterinary Medicine, 625 Harrison Street, West Lafayette, IN, 47907, United States of America</addr-line>
</aff>
<contrib-group>
<contrib contrib-type="editor">
<name>
<surname>Farke</surname>
<given-names>Andrew A.</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1">
<addr-line>Raymond M. Alf Museum of Paleontology, UNITED STATES</addr-line>
</aff>
<author-notes>
<fn fn-type="conflict" id="coi001">
<p>
<bold>Competing Interests: </bold>
The authors have declared that no competing interests exist.</p>
</fn>
<fn fn-type="con" id="contrib001">
<p>Conceived and designed the experiments: JC HW EW JRH. Performed the experiments: JC HW EW JRH. Analyzed the data: JC HW EW JRH. Contributed reagents/materials/analysis tools: JC HW EW JRH. Wrote the paper: JC HW EW JRH. Proposed the adaptive bone modeling hypothesis: JC.</p>
</fn>
<corresp id="cor001">* E-mail:
<email>jorge.cubo_garcia@upmc.fr</email>
</corresp>
</author-notes>
<pub-date pub-type="epub">
<day>8</day>
<month>7</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="collection">
<year>2015</year>
</pub-date>
<volume>10</volume>
<issue>7</issue>
<elocation-id>e0131131</elocation-id>
<history>
<date date-type="received">
<day>23</day>
<month>3</month>
<year>2015</year>
</date>
<date date-type="accepted">
<day>27</day>
<month>5</month>
<year>2015</year>
</date>
</history>
<permissions>
<copyright-year>2015</copyright-year>
<copyright-holder>Cubo 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:type="simple" xlink:href="pone.0131131.pdf"></self-uri>
<abstract>
<p>Predator confrontation or predator evasion frequently produces bone fractures in potential prey in the wild. Although there are reports of healed bone injuries and pathologies in non-avian dinosaurs, no previously published instances of biomechanically adaptive bone modeling exist. Two tibiae from an ontogenetic sample of fifty specimens of the herbivorous dinosaur
<italic>Maiasaura peeblesorum</italic>
(Ornithopoda: Hadrosaurinae) exhibit exostoses. We show that these outgrowths are cases of biomechanically adaptive periosteal bone modeling resulting from overstrain on the tibia after a fibula fracture. Histological and biomechanical results are congruent with predictions derived from this hypothesis. Histologically, the outgrowths are constituted by radial fibrolamellar periosteal bone tissue formed at very high growth rates, as expected in a process of rapid strain equilibration response. These outgrowths show greater compactness at the periphery, where tensile and compressive biomechanical constraints are higher. Moreover, these outgrowths increase the maximum bending strength in the direction of the stresses derived from locomotion. They are located on the antero-lateral side of the tibia, as expected in a presumably bipedal one year old individual, and in the posterior position of the tibia, as expected in a presumably quadrupedal individual at least four years of age. These results reinforce myological evidence suggesting that
<italic>Maiasaura</italic>
underwent an ontogenetic shift from the primitive ornithischian bipedal condition when young to a derived quadrupedal posture when older.</p>
</abstract>
<funding-group>
<funding-statement>Funding and support for HW was provided by Gerry Ohrstrom, the Museum of the Rockies, the Jurassic Foundation, the Geological Society of America, and NSF grant #EAR 8705986. Funding and support for JC was provided by the CNRS (France), the UPMC-Sorbonne Universités (France) and by the grants CGL-2011-23919 and CGL-2012-34459 of the Spanish Ministry of Economy and Competitiveness. 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="0"></table-count>
<page-count count="11"></page-count>
</counts>
<custom-meta-group>
<custom-meta id="data-availability">
<meta-name>Data Availability</meta-name>
<meta-value>All data underlying the findings in our study are freely available in the manuscript and in a public repository (high resolution images of tibiae examined in this report can be downloaded from Morphobank
<ext-link ext-link-type="uri" xlink:href="http://www.morphobank.org">www.morphobank.org</ext-link>
; project P2136).</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
<notes>
<title>Data Availability</title>
<p>All data underlying the findings in our study are freely available in the manuscript and in a public repository (high resolution images of tibiae examined in this report can be downloaded from Morphobank
<ext-link ext-link-type="uri" xlink:href="http://www.morphobank.org">www.morphobank.org</ext-link>
; project P2136).</p>
</notes>
</front>
</pmc>
</record>

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