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      Divergent locomotor evolution in “giant” kangaroos: Evidence from foot bone bending resistances and microanatomy

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          Abstract

          The extinct sthenurine (giant, short‐faced) kangaroos have been proposed to have a different type of locomotor behavior to extant (macropodine) kangaroos, based both on physical limitations (the size of many exceeds the proposed limit for hopping) and anatomical features (features of the hind limb anatomy suggestive of weight‐bearing on one leg at a time). Here, we use micro computerised tomography (micro‐CT) scans of the pedal bones of six kangaroos, three sthenurine, and three macropodine, ranging from ~50 to 150 kg, to investigate possible differences in bone resistances to bending and cortical bone distribution that might relate to differences in locomotion. Using second moment of area analysis, we show differences in resistance to bending between the two subfamilies. Distribution of cortical bone shows that sthenurines had less resistant calcaneal tubers, implying a different foot posture during locomotion, and the long foot bones were more resistant to the medial bending stresses. These differences were the most pronounced between Pleistocene monodactyl sthenurines ( Sthenurus stirlingi and Procoptodon browneorum) and the two species of Macropus (the extant M. giganteus and the extinct M. cf. M. titan) and support the hypothesis that these derived sthenurines employed bipedal striding. The Miocene sthenurine Hadronomas retains some more macropodine‐like features of bone resistance to bending, perhaps reflecting its retention of the fifth pedal digit. The Pleistocene macropodine Protemnodon has a number of unique features, possibly indicative of a type of locomotion unlike the other kangaroos.

          Abstract

          Internal bone anatomy and resistance to bending along the bone support the hypothesis of different gaits in the extinct kangaroos.

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          Most cited references66

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          BoneJ: Free and extensible bone image analysis in ImageJ.

          Bone geometry is commonly measured on computed tomographic (CT) and X-ray microtomographic (μCT) images. We obtained hundreds of CT, μCT and synchrotron μCT images of bones from diverse species that needed to be analysed remote from scanning hardware, but found that available software solutions were expensive, inflexible or methodologically opaque. We implemented standard bone measurements in a novel ImageJ plugin, BoneJ, with which we analysed trabecular bone, whole bones and osteocyte lacunae. BoneJ is open source and free for anyone to download, use, modify and distribute. Copyright © 2010 Elsevier Inc. All rights reserved.
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            Biomechanical consequences of scaling.

            To function over a lifetime of use, materials and structures must be designed to have sufficient factors of safety to avoid failure. Vertebrates are generally built from materials having similar properties. Safety factors are most commonly calculated based on the ratio of a structure's failure stress to its peak operating stress. However, yield stress is a more likely limit, and work of fracture relative to energy absorption is likely the most relevant measure of a structure's safety factor, particularly under impact loading conditions characteristic of locomotion. Yet, it is also the most difficult to obtain. For repeated loading, fatigue damage and eventual failure may be critical to the design of biological structures and will result in lower safety factors. Although area:volume scaling predicts that stresses will increase with size, interspecific comparisons of mammals and birds show that skeletal allometry is modest, with most groups scaling (l proportional, variant d0.89) closer to geometric similarity (isometry: l proportional, variant d1.0) than to elastic similarity (l proportional, variant d0.67) or stress similarity (l proportional, variant d0.5). To maintain similar peak bone and muscle stresses, terrestrial mammals change posture when running, with larger mammals becoming more erect. More erect limbs increases their limb muscle mechanical advantage (EMA) or ratio of ground impulse to muscle impulse (r/R= integral G/integral Fm). The increase in limb EMA with body weight (proportional, variant W0.25) allows larger mammals to match changes in bone and muscle area (proportional, variant W0.72-0.80) to changes in muscle force generating requirements (proportional, variantW0.75), keeping bone and muscle stresses fairly constant across a size range 0.04-300 kg. Above this size, extremely large mammals exhibit more pronounced skeletal allometry and reduced locomotor ability. Patterns of ontogenetic scaling during skeletal growth need not follow broader interspecific scaling patterns. Instead, negative allometric growth (becoming more slender) is often observed and may relate to maturation of the skeleton's properties or the need for younger animals to move at faster speeds compared with adults. In contrast to bone and muscle stress patterns, selection for uniform safety factors in tendons does not appear to occur. In addition to providing elastic energy savings, tendons transmit force for control of motion of more distal limb segments. Their role in elastic savings requires that some tendons operate at high stresses (and strains), which compromises their safety factor. Other 'low stress' tendons have larger safety factors, indicating that their primary design is for stiffness to reduce the amount of stretch that their muscles must overcome when contracting to control movement.
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              Long-bone circumference and weight in mammals, birds and dinosaurs

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                Author and article information

                Contributors
                a.wagstaffe-2020@hull.ac.uk
                Journal
                J Morphol
                J Morphol
                10.1002/(ISSN)1097-4687
                JMOR
                Journal of Morphology
                John Wiley & Sons, Inc. (Hoboken, USA )
                0362-2525
                1097-4687
                18 January 2022
                March 2022
                : 283
                : 3 ( doiID: 10.1002/jmor.v283.3 )
                : 313-332
                Affiliations
                [ 1 ] Department of Earth Sciences University of Bristol Bristol UK
                [ 2 ] Energy and Environment Institute University of Hull Hull UK
                [ 3 ] Center for Anatomical and Human Studies, Hull York Medical School University of York York UK
                [ 4 ] Department of Ecology and Evolutionary Biology Brown University Providence Rhode Island USA
                Author notes
                [*] [* ] Correspondence

                Amber Y. Wagstaffe, Energy and Environment Institute, University of Hull, Hull, HU6 7RX, UK.

                Email: a.wagstaffe-2020@ 123456hull.ac.uk

                Author information
                https://orcid.org/0000-0002-8248-3370
                Article
                JMOR21445
                10.1002/jmor.21445
                9303454
                34997777
                64d15717-e83d-4c65-9f5e-85a31081d762
                © 2022 The Authors. Journal of Morphology published by Wiley Periodicals LLC.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.

                History
                : 06 December 2021
                : 23 July 2021
                : 03 January 2022
                Page count
                Figures: 9, Tables: 2, Pages: 20, Words: 16708
                Funding
                Funded by: Bushnell Foundation
                Funded by: University of Bristol MSc Program in Palaeobiology
                Categories
                Research Article
                Research Articles
                Custom metadata
                2.0
                March 2022
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.1.7 mode:remove_FC converted:21.07.2022

                bone resistance to bending,locomotion,macropodinae,pedal anatomy,sthenurinae

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