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      A New Look at Ichthyosaur Long Bone Microanatomy and Histology: Implications for Their Adaptation to an Aquatic Life

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          Abstract

          Background

          Ichthyosaurs are Mesozoic reptiles considered as active swimmers highly adapted to a fully open-marine life. They display a wide range of morphologies illustrating diverse ecological grades. Data concerning their bone microanatomical and histological features are rather limited and suggest that ichthyosaurs display a spongious, “osteoporotic-like” bone inner structure, like extant cetaceans. However, some taxa exhibit peculiar features, suggesting that the analysis of the microanatomical and histological characteristics of various ichthyosaur long bones should match the anatomical diversity and provide information about their diverse locomotor abilities and physiology.

          Methodology/Principal Findings

          The material analyzed for this study essentially consists of mid-diaphyseal transverse sections from stylopod bones of various ichthyosaurs and of a few microtomographic (both conventional and synchrotron) data. The present contribution discusses the histological and microanatomical variation observed within ichthyosaurs and the peculiarities of some taxa ( Mixosaurus, Pessopteryx). Four microanatomical types are described. If Mixosaurus sections differ from those of the other taxa analyzed, the other microanatomical types, characterized by the relative proportion of compact and loose spongiosa of periosteal and endochondral origin respectively, seem to rather especially illustrate variation along the diaphysis in taxa with similar microanatomical features. Our analysis also reveals that primary bone in all the ichthyosaur taxa sampled (to the possible exception of Mixosaurus) is spongy in origin, that cyclical growth is a common pattern among ichthyosaurs, and confirms the previous assumptions of high growth rates in ichthyosaurs.

          Conclusions/Significance

          The occurrence of two types of remodelling patterns along the diaphysis, characterized by bone mass decrease and increase respectively is described for the first time. It raises questions about the definition of the osseous microanatomical specializations bone mass increase and osteoporosis, notably based on the processes involved, and reveals the difficulty in determining the true occurrence of these osseous specializations in ichthyosaurs.

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          Most cited references12

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          Three rules for bone adaptation to mechanical stimuli.

          The primary mechanical function of bones is to provide rigid levers for muscles to pull against, and to remain as light as possible to allow efficient locomotion. To accomplish this bones must adapt their shape and architecture to make efficient use of material. Bone adaptation during skeletal growth and development continuously adjusts skeletal mass and architecture to changing mechanical environments. There are three fundamental rules that govern bone adaptation: (1) It is driven by dynamic, rather than static, loading. (2) Only a short duration of mechanical loading is necessary to initiate an adaptive response. (3) Bone cells accommodate to a customary mechanical loading environment, making them less responsive to routine loading signals. From these rules, several mathematical equations can be derived that provide simple parametric models for bone adaptation.
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            Three-dimensional synchrotron virtual paleohistology: a new insight into the world of fossil bone microstructures.

            The recent developments of phase-contrast synchrotron imaging techniques have been of great interest for paleontologists, providing three-dimensional (3D) tomographic images of anatomical structures, thereby leading to new paleobiological insights and the discovery of new species. However, until now, it has not been used on features smaller than 5-7 μm voxel size in fossil bones. Because much information is contained within the 3D histological architecture of bone, including an ontogenetic record, crucial for understanding the paleobiology of fossil species, the application of phase-contrast synchrotron tomography to bone at higher resolutions is potentially of great interest. Here we use this technique to provide new 3D insights into the submicron-scale histology of fossil and recent bones, based on the development of new pink-beam configurations, data acquisition strategies, and improved processing tools. Not only do the scans reveal by nondestructive means all of the major features of the histology at a resolution comparable to that of optical microscopy, they provide 3D information that cannot be obtained by any other method.
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              New Ophthalmosaurid Ichthyosaurs from the European Lower Cretaceous Demonstrate Extensive Ichthyosaur Survival across the Jurassic–Cretaceous Boundary

              Background Ichthyosauria is a diverse clade of marine amniotes that spanned most of the Mesozoic. Until recently, most authors interpreted the fossil record as showing that three major extinction events affected this group during its history: one during the latest Triassic, one at the Jurassic–Cretaceous boundary (JCB), and one (resulting in total extinction) at the Cenomanian-Turonian boundary. The JCB was believed to eradicate most of the peculiar morphotypes found in the Late Jurassic, in favor of apparently less specialized forms in the Cretaceous. However, the record of ichthyosaurs from the Berriasian–Barremian interval is extremely limited, and the effects of the end-Jurassic extinction event on ichthyosaurs remains poorly understood. Methodology/Principal Findings Based on new material from the Hauterivian of England and Germany and on abundant material from the Cambridge Greensand Formation, we name a new ophthalmosaurid, Acamptonectes densus gen. et sp. nov. This taxon shares numerous features with Ophthalmosaurus, a genus now restricted to the Callovian–Berriasian interval. Our phylogenetic analysis indicates that Ophthalmosauridae diverged early in its history into two markedly distinct clades, Ophthalmosaurinae and Platypterygiinae, both of which cross the JCB and persist to the late Albian at least. To evaluate the effect of the JCB extinction event on ichthyosaurs, we calculated cladogenesis, extinction, and survival rates for each stage of the Oxfordian–Barremian interval, under different scenarios. The extinction rate during the JCB never surpasses the background extinction rate for the Oxfordian–Barremian interval and the JCB records one of the highest survival rates of the interval. Conclusions/Significance There is currently no evidence that ichthyosaurs were affected by the JCB extinction event, in contrast to many other marine groups. Ophthalmosaurid ichthyosaurs remained diverse from their rapid radiation in the Middle Jurassic to their total extinction at the beginning of the Late Cretaceous.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                21 April 2014
                : 9
                : 4
                : e95637
                Affiliations
                [1 ]Steinmann-Institut für Geologie, Mineralogie und Paläontologie, Universität Bonn, Bonn, Germany
                [2 ]Paläontologisches Institut und Museum der Universität Zürich, Zürich, Switzerland
                [3 ]Geology department, University of Liège, Liège, Belgium
                Raymond M. Alf Museum of Paleontology, United States of America
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: AH PMS. Performed the experiments: AH. Analyzed the data: AH PMS. Contributed reagents/materials/analysis tools: AH CK PMS TMS VF. Wrote the paper: AH. Critical revision of the manuscript: AH CK PMS TMS VF.

                Article
                PONE-D-14-03493
                10.1371/journal.pone.0095637
                3994080
                24752508
                e76b50e6-711b-45e6-b00e-9c97824c5eec
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 23 January 2014
                : 27 March 2014
                Page count
                Pages: 10
                Funding
                AH acknowledges financial support from the Alexander von Humboldt Foundation, TMS from the Swiss National Science Foundation (grant no. 31003A 146440), and CK from the DAAD (D/09/46969). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Anatomy
                Histology
                Ecology
                Paleoecology
                Evolutionary Biology
                Organismal Evolution
                Marine Biology
                Paleontology
                Paleobiology
                Paleozoology
                Vertebrate Paleontology
                Zoology
                Ecology and Environmental Sciences

                Uncategorized
                Uncategorized

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