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      Enamel Ultrastructure in Fossil Cetaceans (Cetacea: Archaeoceti and Odontoceti)

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          Abstract

          The transition from terrestrial ancestry to a fully pelagic life profoundly altered the body systems of cetaceans, with extreme morphological changes in the skull and feeding apparatus. The Oligocene Epoch was a crucial time in the evolution of cetaceans when the ancestors of modern whales and dolphins (Neoceti) underwent major diversification, but details of dental structure and evolution are poorly known for the archaeocete-neocete transition. We report the morphology of teeth and ultrastructure of enamel in archaeocetes, and fossil platanistoids and delphinoids, ranging from late Oligocene (Waitaki Valley, New Zealand) to Pliocene (Caldera, Chile). Teeth were embedded in epoxy resin, sectioned in cross and longitudinal planes, polished, etched, and coated with gold palladium for scanning electron microscopy (SEM) observation. SEM images showed that in archaeocetes, squalodontids and Prosqualodon (taxa with heterodont and nonpolydont/limited polydont teeth), the inner enamel was organized in Hunter-Schreger bands (HSB) with an outer layer of radial enamel. This is a common pattern in most large-bodied mammals and it is regarded as a biomechanical adaptation related to food processing and crack resistance. Fossil Otekaikea sp. and delphinoids, which were polydont and homodont, showed a simpler structure, with inner radial and outer prismless enamel. Radial enamel is regarded as more wear-resistant and has been retained in several mammalian taxa in which opposing tooth surfaces slide over each other. These observations suggest that the transition from a heterodont and nonpolydont/limited polydont dentition in archaeocetes and early odontocetes, to homodont and polydont teeth in crownward odontocetes, was also linked to a marked simplification in the enamel Schmelzmuster. These patterns probably reflect functional shifts in food processing from shear-and-mastication in archaeocetes and early odontocetes, to pierce-and-grasp occlusion in crownward odontocetes, with the implication of less demanding feeding biomechanics as seen in most extant odontocetes.

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          Origin of whales from early artiodactyls: hands and feet of Eocene Protocetidae from Pakistan.

          Partial skeletons of two new fossil whales, Artiocetus clavis and Rodhocetus balochistanensis, are among the oldest known protocetid archaeocetes. These came from early Lutetian age (47 million years ago) strata in eastern Balochistan Province, Pakistan. Both have an astragalus and cuboid in the ankle with characteristics diagnostic of artiodactyls; R. balochistanensis has virtually complete fore- and hind limbs. The new skeletons are important in augmenting the diversity of early Protocetidae, clarifying that Cetacea evolved from early Artiodactyla rather than Mesonychia and showing how early protocetids swam.
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            Dental enamel as a dietary indicator in mammals.

            The considerable variation in shape, size, structure and properties of the enamel cap covering mammalian teeth is a topic of great evolutionary interest. No existing theories explain how such variations might be fit for the purpose of breaking food particles down. Borrowing from engineering materials science, we use principles of fracture and deformation of solids to provide a quantitative account of how mammalian enamel may be adapted to diet. Particular attention is paid to mammals that feed on 'hard objects' such as seeds and dry fruits, the outer casings of which appear to have evolved structures with properties similar to those of enamel. These foods are important in the diets of some primates, and have been heavily implicated as a key factor in the evolutionary history of the hominin clade. As a tissue with intrinsic weakness yet exceptional durability, enamel could be especially useful as a dietary indicator for extinct taxa.
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              Analysis of fracture and deformation modes in teeth subjected to occlusal loading.

              An analysis of fracture and deformation modes in tooth enamel subjected to occlusal loading is presented. Several competing modes are identified: deformation by yield beneath the indenter; median cracking from the ensuing plastic zone and analogous radial cracking from the dentin-enamel junction along the load axis; and margin cracking from the cervical enamel-cement junction. The analysis, based on a simple model of tooth geometry, presents relations for the critical loads to initiate these damage modes within the enamel, and to drive ensuing cracks longitudinally around the tooth walls to failure. The relations are explicit in their dependence on characteristic tooth dimensions - enamel thickness and cuspal radius - and on material properties - modulus, hardness, toughness and strength. Provision is made to incorporate properties of the occlusal contact, whether from opposing dentition or intervening food particles. All these features are demonstrated on critical-load master diagrams. A characteristic feature of the damage evolution is the gradual evolution of each mode with increasing load, so that failure is generally a prolonged rather than abrupt event. This accounts for the remarkable damage tolerance of natural teeth. The equations may enable basic predictions of tooth responses for humans and animals under a variety of specified dietary and functional conditions.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                2015
                28 January 2015
                : 10
                : 1
                : e0116557
                Affiliations
                [1 ]Department of Geology, University of Otago, Dunedin, New Zealand
                [2 ]Sir John Walsh Research Institute, Faculty of Dentistry, University of Otago, Dunedin, New Zealand
                NYIT College of Osteopathic Medicine, UNITED STATES
                Author notes

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

                Conceived and designed the experiments: CL JAK REF. Performed the experiments: CL. Analyzed the data: CL JAK REF. Contributed reagents/materials/analysis tools: CL JAK REF. Wrote the paper: CL JAK REF.

                Article
                PONE-D-14-32897
                10.1371/journal.pone.0116557
                4309603
                25629995
                a090150a-0460-426b-a399-a1cf5de5db00
                Copyright @ 2015

                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 July 2014
                : 9 December 2014
                Page count
                Figures: 5, Tables: 2, Pages: 14
                Funding
                CL received an University of Otago PhD scholarship and Sir John Walsh Research Institute Postdoctoral Fellowship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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