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      Merging cranial histology and 3D-computational biomechanics: a review of the feeding ecology of a Late Triassic temnospondyl amphibian

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          Abstract

          Finite Element Analysis (FEA) is a useful method for understanding form and function. However, modelling of fossil taxa invariably involves assumptions as a result of preservation-induced loss of information in the fossil record. To test the validity of predictions from FEA, given such assumptions, these results could be compared to independent lines of evidence for cranial mechanics. In the present study a new concept of using bone microstructure to predict stress distribution in the skull during feeding is put forward and a correlation between bone microstructure and results of computational biomechanics (FEA) is carried out. The bony framework is a product of biological optimisation; bone structure is created to meet local mechanical conditions. To test how well results from FEA correlate to cranial mechanics predicted from bone structure, the well-known temnospondyl Metoposaurus krasiejowensis was used as a model. A crucial issue to Temnospondyli is their feeding mode: did they suction feed or employ direct biting, or both? Metoposaurids have previously been characterised either as active hunters or passive bottom dwellers. In order to test the correlation between results from FEA and bone microstructure, two skulls of Metoposaurus were used , one modelled under FE analyses, while for the second one 17 dermal bone microstructure were analysed. Thus, for the first time, results predicting cranial mechanical behaviour using both methods are merged to understand the feeding strategy of Metoposaurus. Metoposaurus appears to have been an aquatic animal that exhibited a generalist feeding behaviour. This taxon may have used two foraging techniques in hunting; mainly bilateral biting and, to a lesser extent, lateral strikes. However, bone microstructure suggests that lateral biting was more frequent than suggested by Finite Element Analysis (FEA). One of the potential factors that determined its mode of life may have been water levels. During optimum water conditions, metoposaurids may have been more active ambush predators that were capable of lateral strikes of the head. The dry season required a less active mode of life when bilateral biting is particularly efficient. This, combined with their characteristically anteriorly positioned orbits, was optimal for ambush strategy. This ability to use alternative modes of food acquisition, independent of environmental conditions, might hold the key in explaining the very common occurrence of metoposaurids during the Late Triassic.

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          The many adaptations of bone.

          J.D Currey (2003)
          Studies concerned with the "adaptations" in bones usually deal with modelling taking place during the individual's lifetime. However, many adaptations are produced over evolutionary time. This survey samples some adaptations of bone that may occur over both length scales, and tries to show whether short- or long-term adaptation is important. (a) Woven and lamellar bone. Woven bone is less mechanically competent than lamellar bone but is frequently found in bones that grow quickly. (b) Stress concentrations in bone. Bone is full of cavities that potentially may act as stress concentrators. Usually these cavities are oriented to minimise their stress-concentrating effect. Furthermore, the "flow" of lamellae round the cavities will still further reduce their stress-concentrating effect, but the elastic anisotropy of bone will, contrarily, tend to enhance it in normal loading situations. (c) Stiffness versus toughness. The mineral content of bone is the main determinant of differences in mechanical properties. Different bones have different mineral contents that optimise the mix of stiffness and toughness needed. (d) Synergy of whole bone architecture and material properties. As bone material properties change during growth the architecture of the whole bone is modified concurrently, to produce an optimum mechanical behaviour of the whole bone. (e) Secondary remodelling. The formation of secondary osteones in general weakens bone. Various suggestions that have been put forward to account for secondary remodelling: enabling mineral homeostasis; removing dead bone; changing the grain of the bone; taking out microcracks. (f) The hollowness of bones. It is shown how the degree of hollowness is adapted to the life of the animal.
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            Assessing a relationship between bone microstructure and growth rate: a fluorescent labelling study in the king penguin chick (Aptenodytes patagonicus).

            Microstructure-function relationships remain poorly understood in primary bone tissues. The relationship between bone growth rate and bone tissue type, although documented in some species by previous works, remains somewhat unclear and controversial. We assessed this relationship in a species with extreme adaptations, the king penguin (Aptenodytes patagonicus). These birds have a peculiar growth, interrupted 3 months after hatching by the austral winter. Before this interruption, chicks undergo extremely rapid statural and ponderal growth. We recorded experimentally (by means of fluorescent labelling) the growth rate of bone tissue in four long bones (humerus, radius, femur and tibiotarsus) of four king penguin chicks during their fastest phase of growth (3-5 weeks after hatching) and identified the associated bone tissue types ('laminar', 'longitudinal', 'reticular' or 'radial' fibro-lamellar bone tissue). We found the highest bone tissue growth rate known to date, up to 171 microm day(-1) (mean 55 microm day(-1)). There was a highly significant relationship between bone tissue type and growth rate (P<10(-6)). Highest rates were obtained with the radial microarchitecture of fibro-lamellar bone, where cavities in the woven network are aligned radially. This result supports the heuristic value of a relationship between growth rate and bone primary microstructure. However, we also found that growth rates of bone tissue types vary according to the long bone considered (P<10(-5)) (e.g. growth rates were 38% lower in the radius than in the other long bones), a result that puts some restriction on the applicability of absolute growth rate values (e.g. to fossil species). The biomechanical disadvantages of accelerated bone growth are discussed in relation to the locomotor behaviour of the chicks during their first month of life.
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              Bone profiler: a tool to quantify, model, and statistically compare bone-section compactness profiles

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                Author and article information

                Contributors
                Journal
                PeerJ
                PeerJ
                peerj
                peerj
                PeerJ
                PeerJ Inc. (San Francisco, USA )
                2167-8359
                26 February 2018
                2018
                : 6
                : e4426
                Affiliations
                [1 ]Steinmann Institute, University of Bonn , Bonn, Germany
                [2 ]Department of Biosystematics, University of Opole , Opole, Poland
                [3 ]European Centre of Palaeontology, University of Opole , Opole, Poland
                [4 ]Centre of Natural History, University of Hamburg , Hamburg, Germany
                [5 ]Virtual Paleontology Department, Institut Català de Paleontologia M. Crusafont , Cerdanyola del Vallès, Spain
                [6 ]Centre de Recherches en Paléobiodiversité et Paléoenvironnements, Muséum national d’Histoire Naturelle , Paris, France
                Article
                4426
                10.7717/peerj.4426
                5831156
                29503770
                3b58596d-bd3f-436c-aca7-52b81bc06274
                ©2018 Konietzko-Meier et al.

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.

                History
                : 5 September 2017
                : 8 February 2018
                Funding
                Funded by: Deutsche Forschungsgemeinschaft (DFG, German Research Foundation)
                Award ID: KA 1525/9-2
                Funded by: Beatriu de Pinos
                Award ID: 2014-BP-A 00048
                Funded by: Spanish Ministerio de Economía, Industria y Competitividad and the European Regional Development Fund of the European Union (MINECO/FEDER EU)
                Award ID: project CGL2014-54373-P
                Funded by: CERCA programme (Generalitat de Catalunya)
                Jordi Marcé-Nogué was supported by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation, KA 1525/9-2). Josep Fortuny was supported by (1) a postdoc grant, “Beatriu de Pinos” 2014-BP-A 00048, from the Generalitat de Catalunya; (2) Spanish Ministerio de Economía, Industria y Competitividad and the European Regional Development Fund of the European Union (MINECO/FEDER EU, project CGL2014-54373-P); (3) the CERCA programme (Generalitat de Catalunya). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Bioengineering
                Paleontology
                Histology

                bone histology,dermal bone,fea,temnospondyli,feeding strategy,metoposaurus,skull

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