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      Cranial biomechanics underpins high sauropod diversity in resource-poor environments

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          Abstract

          High megaherbivore species richness is documented in both fossil and contemporary ecosystems despite their high individual energy requirements. An extreme example of this is the Late Jurassic Morrison Formation, which was dominated by sauropod dinosaurs, the largest known terrestrial vertebrates. High sauropod diversity within the resource-limited Morrison is paradoxical, but might be explicable through sophisticated resource partitioning. This hypothesis was tested through finite-element analysis of the crania of the Morrison taxa Camarasaurus and Diplodocus. Results demonstrate divergent specialization, with Camarasaurus capable of exerting and accommodating greater bite forces than Diplodocus, permitting consumption of harder food items. Analysis of craniodental biomechanical characters taken from 35 sauropod taxa demonstrates a functional dichotomy in terms of bite force, cranial robustness and occlusal relationships yielding two polyphyletic functional ‘grades’. Morrison taxa are widely distributed within and between these two morphotypes, reflecting distinctive foraging specializations that formed a biomechanical basis for niche partitioning between them. This partitioning, coupled with benefits associated with large body size, would have enabled the high sauropod diversities present in the Morrison Formation. Further, this provides insight into the mechanisms responsible for supporting the high diversities of large megaherbivores observed in other Mesozoic and Cenozoic communities, particularly those occurring in resource-limited environments.

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          Structural Extremes in a Cretaceous Dinosaur

          Fossils of the Early Cretaceous dinosaur, Nigersaurus taqueti, document for the first time the cranial anatomy of a rebbachisaurid sauropod. Its extreme adaptations for herbivory at ground-level challenge current hypotheses regarding feeding function and feeding strategy among diplodocoids, the larger clade of sauropods that includes Nigersaurus. We used high resolution computed tomography, stereolithography, and standard molding and casting techniques to reassemble the extremely fragile skull. Computed tomography also allowed us to render the first endocast for a sauropod preserving portions of the olfactory bulbs, cerebrum and inner ear, the latter permitting us to establish habitual head posture. To elucidate evidence of tooth wear and tooth replacement rate, we used photographic-casting techniques and crown thin sections, respectively. To reconstruct its 9-meter postcranial skeleton, we combined and size-adjusted multiple partial skeletons. Finally, we used maximum parsimony algorithms on character data to obtain the best estimate of phylogenetic relationships among diplodocoid sauropods. Nigersaurus taqueti shows extreme adaptations for a dinosaurian herbivore including a skull of extremely light construction, tooth batteries located at the distal end of the jaws, tooth replacement as fast as one per month, an expanded muzzle that faces directly toward the ground, and hollow presacral vertebral centra with more air sac space than bone by volume. A cranial endocast provides the first reasonably complete view of a sauropod brain including its small olfactory bulbs and cerebrum. Skeletal and dental evidence suggests that Nigersaurus was a ground-level herbivore that gathered and sliced relatively soft vegetation, the culmination of a low-browsing feeding strategy first established among diplodocoids during the Jurassic.
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            Global environmental controls of diversity in large herbivores.

            Large mammalian herbivores occupy half of the earth's land surface and are important both ecologically and economically, but their diversity is threatened by human activities. We investigated how the diversity of large herbivores changes across gradients of global precipitation and soil fertility. Here we show that more plant-available moisture reduces the nutrient content of plants but increases productivity, whereas more plant-available nutrients increase both of these factors. Because larger herbivore species tolerate lower plant nutrient content but require greater plant abundance, the highest potential herbivore diversity should occur in locations with intermediate moisture and high nutrients. These areas are dry enough to yield high quality plants and support smaller herbivores, but productive enough to support larger herbivores. These predictions fit with observed patterns of body size and diversity for large mammalian herbivores in North America, Africa and Australia, and yield a global map of regions with potentially high herbivore diversity. Thus, gradients of precipitation, temperature and soil fertility might explain the global distribution of large herbivore diversity and help to identify crucial areas for conservation and restoration.
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              Requirements for comparing the performance of finite element models of biological structures.

              The widespread availability of three-dimensional imaging and computational power has fostered a rapid increase in the number of biologists using finite element analysis (FEA) to investigate the mechanical function of living and extinct organisms. The inevitable rise of studies that compare finite element models brings to the fore two critical questions about how such comparative analyses can and should be conducted: (1) what metrics are appropriate for assessing the performance of biological structures using finite element modeling? and, (2) how can performance be compared such that the effects of size and shape are disentangled? With respect to performance, we argue that energy efficiency is a reasonable optimality criterion for biological structures and we show that the total strain energy (a measure of work expended deforming a structure) is a robust metric for comparing the mechanical efficiency of structures modeled with finite elements. Results of finite element analyses can be interpreted with confidence when model input parameters (muscle forces, detailed material properties) and/or output parameters (reaction forces, strains) are well-documented by studies of living animals. However, many researchers wish to compare species for which these input and validation data are difficult or impossible to acquire. In these cases, researchers can still compare the performance of structures that differ in shape if variation in size is controlled. We offer a theoretical framework and empirical data demonstrating that scaling finite element models to equal force: surface area ratios removes the effects of model size and provides a comparison of stress-strength performance based solely on shape. Further, models scaled to have equal applied force:volume ratios provide the basis for strain energy comparison. Thus, although finite element analyses of biological structures should be validated experimentally whenever possible, this study demonstrates that the relative performance of un-validated models can be compared so long as they are scaled properly.
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                Author and article information

                Journal
                Proc Biol Sci
                Proc. Biol. Sci
                RSPB
                royprsb
                Proceedings of the Royal Society B: Biological Sciences
                The Royal Society
                0962-8452
                1471-2954
                22 November 2014
                22 November 2014
                : 281
                : 1795
                : 20142114
                Affiliations
                [1 ]School of Earth Sciences , University of Bristol, Life Sciences Building, 24 Tyndall Avenue, Bristol BS8 1TP, UK
                [2 ]Department of Earth Sciences, The Natural History Museum , Cromwell Road, London SW7 5DB, UK
                Author notes
                Article
                rspb20142114
                10.1098/rspb.2014.2114
                4213629
                25297869
                614e5675-fd3c-4466-8899-c55f4b22e4e9

                © 2014 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : 25 August 2014
                : 8 September 2014
                Categories
                1001
                144
                25
                60
                Research Articles
                Custom metadata
                November 22, 2014

                Life sciences
                niche partitioning,megaherbivores,sauropod,morrison formation,biomechanics,finite-element analysis

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