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      First Reported Cases of Biomechanically Adaptive Bone Modeling in Non-Avian Dinosaurs

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          Abstract

          Predator confrontation or predator evasion frequently produces bone fractures in potential prey in the wild. Although there are reports of healed bone injuries and pathologies in non-avian dinosaurs, no previously published instances of biomechanically adaptive bone modeling exist. Two tibiae from an ontogenetic sample of fifty specimens of the herbivorous dinosaur Maiasaura peeblesorum (Ornithopoda: Hadrosaurinae) exhibit exostoses. We show that these outgrowths are cases of biomechanically adaptive periosteal bone modeling resulting from overstrain on the tibia after a fibula fracture. Histological and biomechanical results are congruent with predictions derived from this hypothesis. Histologically, the outgrowths are constituted by radial fibrolamellar periosteal bone tissue formed at very high growth rates, as expected in a process of rapid strain equilibration response. These outgrowths show greater compactness at the periphery, where tensile and compressive biomechanical constraints are higher. Moreover, these outgrowths increase the maximum bending strength in the direction of the stresses derived from locomotion. They are located on the antero-lateral side of the tibia, as expected in a presumably bipedal one year old individual, and in the posterior position of the tibia, as expected in a presumably quadrupedal individual at least four years of age. These results reinforce myological evidence suggesting that Maiasaura underwent an ontogenetic shift from the primitive ornithischian bipedal condition when young to a derived quadrupedal posture when older.

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          Most cited references22

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          Bone typology and growth rate: testing and quantifying 'Amprino's rule' in the mallard (Anas platyrhynchos).

          Periosteal bone histology expresses its rate of deposition. This fundamental relationship between bone structure and growth dynamics, first assumed by Amprino many decades ago, was quantified in preliminary studies, but never statistically tested. Moreover, the precise typological characters of bone tissue linked to growth rate remained poorly known. Here, we present the first statistical analysis of 'Amprino's rule', measured on comprehensive growth series of the mallard, Anas platyrhynchos. Growth rates were assessed by fluorescent labelling. Bone typology was described according to Ricqlès' typological classification. Results show that the presence and proportion of primary osteons, two consequences of bone initial porosity at the time of its deposit, are strongly related to bone growth rate. However, no significant relationship between primary osteons orientation and bone growth rate could be detected, at least for osteonal orientations (longitudinal, laminar and reticular) and growth rates values observed in mallard long bones. These results suggest that Amprino's rule holds for some major typological characters of primary compact bone tissues (i.e. primary osteons presence and proportion). However, it is irrelevant to some other characters (i.e. osteonal orientation), the meaning of which remains to be discovered.
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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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              Sizing the Jurassic theropod dinosaur Allosaurus: assessing growth strategy and evolution of ontogenetic scaling of limbs.

              Allosaurus is one of the most common Mesozoic theropod dinosaurs. We present a histological analysis to assess its growth strategy and ontogenetic limb bone scaling. Based on an ontogenetic series of humeral, ulnar, femoral, and tibial sections of fibrolamellar bone, we estimate the ages of the largest individuals in the sample to be between 13-19 years. Growth curve reconstruction suggests that maximum growth occurred at 15 years, when body mass increased 148 kg/year. Based on larger bones of Allosaurus, we estimate an upper age limit of between 22-28 years of age, which is similar to preliminary data for other large theropods. Both Model I and Model II regression analyses suggest that relative to the length of the femur, the lengths of the humerus, ulna, and tibia increase in length more slowly than isometry predicts. That pattern of limb scaling in Allosaurus is similar to those in other large theropods such as the tyrannosaurids. Phylogenetic optimization suggests that large theropods independently evolved reduced humeral, ulnar, and tibial lengths by a phyletic reduction in longitudinal growth relative to the femur.
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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, CA USA )
                1932-6203
                8 July 2015
                2015
                : 10
                : 7
                : e0131131
                Affiliations
                [1 ]Sorbonne Universités, UPMC Univ Paris 06, UMR 7193, Institut des Sciences de la Terre Paris (iSTeP), 4 Place Jussieu, BC19, F-75005, Paris, France
                [2 ]CNRS, UMR 7193, Institut des Sciences de la Terre Paris (iSTeP), F-75005, Paris, France
                [3 ]Montana State University, Museum of the Rockies, 600 West Kagy Boulevard, Bozeman, Montana, 59717, United States of America
                [4 ]Department of Anatomy and Cell Biology, Oklahoma State University Center for Health Sciences, 1111 W. 17th St., Tulsa, OK, 74107, United States of America
                [5 ]Small Animal Internal Medicine, Purdue University College of Veterinary Medicine, 625 Harrison Street, West Lafayette, IN, 47907, United States of America
                Raymond M. Alf Museum of Paleontology, UNITED STATES
                Author notes

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

                Conceived and designed the experiments: JC HW EW JRH. Performed the experiments: JC HW EW JRH. Analyzed the data: JC HW EW JRH. Contributed reagents/materials/analysis tools: JC HW EW JRH. Wrote the paper: JC HW EW JRH. Proposed the adaptive bone modeling hypothesis: JC.

                Article
                PONE-D-15-12202
                10.1371/journal.pone.0131131
                4495995
                26153689
                8bd7faa5-789d-4214-a012-7272d26e3bb2
                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 March 2015
                : 27 May 2015
                Page count
                Figures: 4, Tables: 0, Pages: 11
                Funding
                Funding and support for HW was provided by Gerry Ohrstrom, the Museum of the Rockies, the Jurassic Foundation, the Geological Society of America, and NSF grant #EAR 8705986. Funding and support for JC was provided by the CNRS (France), the UPMC-Sorbonne Universités (France) and by the grants CGL-2011-23919 and CGL-2012-34459 of the Spanish Ministry of Economy and Competitiveness. 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 data underlying the findings in our study are freely available in the manuscript and in a public repository (high resolution images of tibiae examined in this report can be downloaded from Morphobank www.morphobank.org; project P2136).

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