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Bone inner structure suggests increasing aquatic adaptations in Desmostylia (Mammalia, Afrotheria)
The paleoecology of desmostylians has been discussed controversially with a general consensus that desmostylians were aquatic or semi-aquatic to some extent. Bone microanatomy can be used as a powerful tool to infer habitat preference of extinct animals. However, bone microanatomical studies of desm...
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Published in: | PloS one 2013-04, Vol.8 (4), p.e59146-e59146 |
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description | The paleoecology of desmostylians has been discussed controversially with a general consensus that desmostylians were aquatic or semi-aquatic to some extent. Bone microanatomy can be used as a powerful tool to infer habitat preference of extinct animals. However, bone microanatomical studies of desmostylians are extremely scarce.
We analyzed the histology and microanatomy of several desmostylians using thin-sections and CT scans of ribs, humeri, femora and vertebrae. Comparisons with extant mammals allowed us to better understand the mode of life and evolutionary history of these taxa. Desmostylian ribs and long bones generally lack a medullary cavity. This trait has been interpreted as an aquatic adaptation among amniotes. Behemotops and Paleoparadoxia show osteosclerosis (i.e. increase in bone compactness), and Ashoroa pachyosteosclerosis (i.e. combined increase in bone volume and compactness). Conversely, Desmostylus differs from these desmostylians in displaying an osteoporotic-like pattern.
In living taxa, bone mass increase provides hydrostatic buoyancy and body trim control suitable for poorly efficient swimmers, while wholly spongy bones are associated with hydrodynamic buoyancy control in active swimmers. Our study suggests that all desmostylians had achieved an essentially, if not exclusively, aquatic lifestyle. Behemotops, Paleoparadoxia and Ashoroa are interpreted as shallow water swimmers, either hovering slowly at a preferred depth, or walking on the bottom, and Desmostylus as a more active swimmer with a peculiar habitat and feeding strategy within Desmostylia. Therefore, desmostylians are, with cetaceans, the second mammal group showing a shift from bone mass increase to a spongy inner organization of bones in their evolutionary history. |
doi_str_mv | 10.1371/journal.pone.0059146 |
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We analyzed the histology and microanatomy of several desmostylians using thin-sections and CT scans of ribs, humeri, femora and vertebrae. Comparisons with extant mammals allowed us to better understand the mode of life and evolutionary history of these taxa. Desmostylian ribs and long bones generally lack a medullary cavity. This trait has been interpreted as an aquatic adaptation among amniotes. Behemotops and Paleoparadoxia show osteosclerosis (i.e. increase in bone compactness), and Ashoroa pachyosteosclerosis (i.e. combined increase in bone volume and compactness). Conversely, Desmostylus differs from these desmostylians in displaying an osteoporotic-like pattern.
In living taxa, bone mass increase provides hydrostatic buoyancy and body trim control suitable for poorly efficient swimmers, while wholly spongy bones are associated with hydrodynamic buoyancy control in active swimmers. Our study suggests that all desmostylians had achieved an essentially, if not exclusively, aquatic lifestyle. Behemotops, Paleoparadoxia and Ashoroa are interpreted as shallow water swimmers, either hovering slowly at a preferred depth, or walking on the bottom, and Desmostylus as a more active swimmer with a peculiar habitat and feeding strategy within Desmostylia. Therefore, desmostylians are, with cetaceans, the second mammal group showing a shift from bone mass increase to a spongy inner organization of bones in their evolutionary history.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0059146</identifier><identifier>PMID: 23565143</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Active control ; Adaptation ; Adaptation, Physiological ; Adaptations ; Afrotheria ; Amniota ; Analysis ; Animals ; Biocompatibility ; Biological evolution ; Biology ; Biomedical materials ; Bone and Bones - anatomy & histology ; Bone and Bones - cytology ; Bone density ; Bone mass ; Bones ; Buoyancy ; Cetacea ; Computed tomography ; Desmostylia ; Earth Sciences ; Endangered & extinct species ; Evolution ; Extinct animals ; Extinction ; Geology ; Habitat preferences ; Histology ; Hovering ; Hypotheses ; Mammalia ; Mammals ; Mammals - classification ; Mammals - physiology ; Marine ; Morphology ; Museums ; Osteoporosis ; Osteosclerosis ; Paleoecology ; Paleontology ; Phylogenetics ; Phylogeny ; Physiology ; Prehistoric mammals ; Principal Component Analysis ; Ribs (structural) ; Sciences of the Universe ; Shallow water ; Spine ; Studies ; Swimming ; Taxa ; Trichechus manatus latirostris ; Ursus maritimus ; Vertebra ; Vertebrae ; Veterinary Science ; Walking ; Water depth</subject><ispartof>PloS one, 2013-04, Vol.8 (4), p.e59146-e59146</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Hayashi et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2013 Hayashi et al 2013 Hayashi et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-a848t-41a3c400ddabcb89f8c7c8b1f0ef90f79c326d71d73be0b7188e20772e0bff233</citedby><cites>FETCH-LOGICAL-a848t-41a3c400ddabcb89f8c7c8b1f0ef90f79c326d71d73be0b7188e20772e0bff233</cites><orcidid>0000-0001-8789-5545</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1330900728/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1330900728?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23565143$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-02115144$$DView record in HAL$$Hfree_for_read</backlink></links><search><contributor>Viriot, Laurent</contributor><creatorcontrib>Hayashi, Shoji</creatorcontrib><creatorcontrib>Houssaye, Alexandra</creatorcontrib><creatorcontrib>Nakajima, Yasuhisa</creatorcontrib><creatorcontrib>Chiba, Kentaro</creatorcontrib><creatorcontrib>Ando, Tatsuro</creatorcontrib><creatorcontrib>Sawamura, Hiroshi</creatorcontrib><creatorcontrib>Inuzuka, Norihisa</creatorcontrib><creatorcontrib>Kaneko, Naotomo</creatorcontrib><creatorcontrib>Osaki, Tomohiro</creatorcontrib><title>Bone inner structure suggests increasing aquatic adaptations in Desmostylia (Mammalia, Afrotheria)</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>The paleoecology of desmostylians has been discussed controversially with a general consensus that desmostylians were aquatic or semi-aquatic to some extent. Bone microanatomy can be used as a powerful tool to infer habitat preference of extinct animals. However, bone microanatomical studies of desmostylians are extremely scarce.
We analyzed the histology and microanatomy of several desmostylians using thin-sections and CT scans of ribs, humeri, femora and vertebrae. Comparisons with extant mammals allowed us to better understand the mode of life and evolutionary history of these taxa. Desmostylian ribs and long bones generally lack a medullary cavity. This trait has been interpreted as an aquatic adaptation among amniotes. Behemotops and Paleoparadoxia show osteosclerosis (i.e. increase in bone compactness), and Ashoroa pachyosteosclerosis (i.e. combined increase in bone volume and compactness). Conversely, Desmostylus differs from these desmostylians in displaying an osteoporotic-like pattern.
In living taxa, bone mass increase provides hydrostatic buoyancy and body trim control suitable for poorly efficient swimmers, while wholly spongy bones are associated with hydrodynamic buoyancy control in active swimmers. Our study suggests that all desmostylians had achieved an essentially, if not exclusively, aquatic lifestyle. Behemotops, Paleoparadoxia and Ashoroa are interpreted as shallow water swimmers, either hovering slowly at a preferred depth, or walking on the bottom, and Desmostylus as a more active swimmer with a peculiar habitat and feeding strategy within Desmostylia. Therefore, desmostylians are, with cetaceans, the second mammal group showing a shift from bone mass increase to a spongy inner organization of bones in their evolutionary history.</description><subject>Active control</subject><subject>Adaptation</subject><subject>Adaptation, Physiological</subject><subject>Adaptations</subject><subject>Afrotheria</subject><subject>Amniota</subject><subject>Analysis</subject><subject>Animals</subject><subject>Biocompatibility</subject><subject>Biological evolution</subject><subject>Biology</subject><subject>Biomedical materials</subject><subject>Bone and Bones - anatomy & histology</subject><subject>Bone and Bones - cytology</subject><subject>Bone density</subject><subject>Bone mass</subject><subject>Bones</subject><subject>Buoyancy</subject><subject>Cetacea</subject><subject>Computed tomography</subject><subject>Desmostylia</subject><subject>Earth Sciences</subject><subject>Endangered & extinct species</subject><subject>Evolution</subject><subject>Extinct animals</subject><subject>Extinction</subject><subject>Geology</subject><subject>Habitat preferences</subject><subject>Histology</subject><subject>Hovering</subject><subject>Hypotheses</subject><subject>Mammalia</subject><subject>Mammals</subject><subject>Mammals - classification</subject><subject>Mammals - physiology</subject><subject>Marine</subject><subject>Morphology</subject><subject>Museums</subject><subject>Osteoporosis</subject><subject>Osteosclerosis</subject><subject>Paleoecology</subject><subject>Paleontology</subject><subject>Phylogenetics</subject><subject>Phylogeny</subject><subject>Physiology</subject><subject>Prehistoric mammals</subject><subject>Principal Component Analysis</subject><subject>Ribs (structural)</subject><subject>Sciences of the Universe</subject><subject>Shallow water</subject><subject>Spine</subject><subject>Studies</subject><subject>Swimming</subject><subject>Taxa</subject><subject>Trichechus manatus latirostris</subject><subject>Ursus maritimus</subject><subject>Vertebra</subject><subject>Vertebrae</subject><subject>Veterinary Science</subject><subject>Walking</subject><subject>Water depth</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNqNk-tr1EAQwIMotp7-B6IBQXrgnftKsvkinPXRg5OCr6_LZDPJpSTZ625S7H_vppeWSykogWR25jezmVcQvKRkSXlC31-Y3rZQL3emxSUhUUpF_Cg4pilni5gR_vhAPgqeOXfhIS7j-GlwxHgUR1Tw4yD76N3Dqm3Rhq6zve56i6HryxJd57xBWwRXtWUIlz10lQ4hh13nJdMO5vATusa47rquIDz5Bk0DXnoXrgprui3aCubPgycF1A5fjN9Z8OvL55-nZ4vN-df16WqzAClktxAUuBaE5DlkOpNpIXWiZUYLgkVKiiTVnMV5QvOEZ0iyhEqJjCQJ84eiYJzPgtf7uLvaODWWxynKOUkJSZj0xHpP5AYu1M5WDdhrZaBSNwpjSwXW51ijQk0locghkyg0jYFiEQuRRf7fWBShj_VhvK3PGsw1tp2FehJ0ammrrSrNleIxjQghPsB8H2B7z-1stVGDjjBKfZPEFfXsyXiZNZe974xqKqexrqFF0_scRSQj5l_Jv1HORBpT5mdjFry5hz5ctJEqwdelagvj09FDULUSiRQijsRQ_OUDlH9ybCrtZ6yovH7iMJ84eKbDP10JvXNq_eP7_7Pnv6fs2wN2i1B3W2fq_mZgp6DYg9oa5ywWd02gRA0bdlsNNWyYGjfMu7067Pud0-1K8b-59CBL</recordid><startdate>20130402</startdate><enddate>20130402</enddate><creator>Hayashi, Shoji</creator><creator>Houssaye, Alexandra</creator><creator>Nakajima, Yasuhisa</creator><creator>Chiba, Kentaro</creator><creator>Ando, Tatsuro</creator><creator>Sawamura, Hiroshi</creator><creator>Inuzuka, Norihisa</creator><creator>Kaneko, Naotomo</creator><creator>Osaki, Tomohiro</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>7ST</scope><scope>7TN</scope><scope>7U6</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-8789-5545</orcidid></search><sort><creationdate>20130402</creationdate><title>Bone inner structure suggests increasing aquatic adaptations in Desmostylia (Mammalia, Afrotheria)</title><author>Hayashi, Shoji ; Houssaye, Alexandra ; Nakajima, Yasuhisa ; Chiba, Kentaro ; Ando, Tatsuro ; Sawamura, Hiroshi ; Inuzuka, Norihisa ; Kaneko, Naotomo ; Osaki, Tomohiro</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a848t-41a3c400ddabcb89f8c7c8b1f0ef90f79c326d71d73be0b7188e20772e0bff233</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Active control</topic><topic>Adaptation</topic><topic>Adaptation, Physiological</topic><topic>Adaptations</topic><topic>Afrotheria</topic><topic>Amniota</topic><topic>Analysis</topic><topic>Animals</topic><topic>Biocompatibility</topic><topic>Biological evolution</topic><topic>Biology</topic><topic>Biomedical materials</topic><topic>Bone and Bones - 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Academic</collection><collection>Environment Abstracts</collection><collection>Oceanic Abstracts</collection><collection>Sustainability Science Abstracts</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Open Access: DOAJ - Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hayashi, Shoji</au><au>Houssaye, Alexandra</au><au>Nakajima, Yasuhisa</au><au>Chiba, Kentaro</au><au>Ando, Tatsuro</au><au>Sawamura, Hiroshi</au><au>Inuzuka, Norihisa</au><au>Kaneko, Naotomo</au><au>Osaki, Tomohiro</au><au>Viriot, Laurent</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Bone inner structure suggests increasing aquatic adaptations in Desmostylia (Mammalia, Afrotheria)</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-04-02</date><risdate>2013</risdate><volume>8</volume><issue>4</issue><spage>e59146</spage><epage>e59146</epage><pages>e59146-e59146</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>The paleoecology of desmostylians has been discussed controversially with a general consensus that desmostylians were aquatic or semi-aquatic to some extent. Bone microanatomy can be used as a powerful tool to infer habitat preference of extinct animals. However, bone microanatomical studies of desmostylians are extremely scarce.
We analyzed the histology and microanatomy of several desmostylians using thin-sections and CT scans of ribs, humeri, femora and vertebrae. Comparisons with extant mammals allowed us to better understand the mode of life and evolutionary history of these taxa. Desmostylian ribs and long bones generally lack a medullary cavity. This trait has been interpreted as an aquatic adaptation among amniotes. Behemotops and Paleoparadoxia show osteosclerosis (i.e. increase in bone compactness), and Ashoroa pachyosteosclerosis (i.e. combined increase in bone volume and compactness). Conversely, Desmostylus differs from these desmostylians in displaying an osteoporotic-like pattern.
In living taxa, bone mass increase provides hydrostatic buoyancy and body trim control suitable for poorly efficient swimmers, while wholly spongy bones are associated with hydrodynamic buoyancy control in active swimmers. Our study suggests that all desmostylians had achieved an essentially, if not exclusively, aquatic lifestyle. Behemotops, Paleoparadoxia and Ashoroa are interpreted as shallow water swimmers, either hovering slowly at a preferred depth, or walking on the bottom, and Desmostylus as a more active swimmer with a peculiar habitat and feeding strategy within Desmostylia. Therefore, desmostylians are, with cetaceans, the second mammal group showing a shift from bone mass increase to a spongy inner organization of bones in their evolutionary history.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23565143</pmid><doi>10.1371/journal.pone.0059146</doi><tpages>e59146</tpages><orcidid>https://orcid.org/0000-0001-8789-5545</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 1932-6203 |
ispartof | PloS one, 2013-04, Vol.8 (4), p.e59146-e59146 |
issn | 1932-6203 1932-6203 |
language | eng |
recordid | cdi_plos_journals_1330900728 |
source | Publicly Available Content Database (Proquest) (PQ_SDU_P3); NCBI_PubMed Central(免费) |
subjects | Active control Adaptation Adaptation, Physiological Adaptations Afrotheria Amniota Analysis Animals Biocompatibility Biological evolution Biology Biomedical materials Bone and Bones - anatomy & histology Bone and Bones - cytology Bone density Bone mass Bones Buoyancy Cetacea Computed tomography Desmostylia Earth Sciences Endangered & extinct species Evolution Extinct animals Extinction Geology Habitat preferences Histology Hovering Hypotheses Mammalia Mammals Mammals - classification Mammals - physiology Marine Morphology Museums Osteoporosis Osteosclerosis Paleoecology Paleontology Phylogenetics Phylogeny Physiology Prehistoric mammals Principal Component Analysis Ribs (structural) Sciences of the Universe Shallow water Spine Studies Swimming Taxa Trichechus manatus latirostris Ursus maritimus Vertebra Vertebrae Veterinary Science Walking Water depth |
title | Bone inner structure suggests increasing aquatic adaptations in Desmostylia (Mammalia, Afrotheria) |
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