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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
Main Authors: Hayashi, Shoji, Houssaye, Alexandra, Nakajima, Yasuhisa, Chiba, Kentaro, Ando, Tatsuro, Sawamura, Hiroshi, Inuzuka, Norihisa, Kaneko, Naotomo, Osaki, Tomohiro
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creator Hayashi, Shoji
Houssaye, Alexandra
Nakajima, Yasuhisa
Chiba, Kentaro
Ando, Tatsuro
Sawamura, Hiroshi
Inuzuka, Norihisa
Kaneko, Naotomo
Osaki, Tomohiro
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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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 &amp; Fisheries Abstracts (ASFA) 1: Biological Sciences &amp; Living Resources</collection><collection>Aquatic Science &amp; 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>
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identifier ISSN: 1932-6203
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issn 1932-6203
1932-6203
language eng
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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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