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      Phylogeny, Histology and Inferred Body Size Evolution in a New Rhabdodontid Dinosaur from the Late Cretaceous of Hungary

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          Abstract

          Background

          Rhabdodontid ornithopod dinosaurs are characteristic elements of Late Cretaceous European vertebrate faunas and were previously collected from lower Campanian to Maastrichtian continental deposits. Phylogenetic analyses have placed rhabdodontids among basal ornithopods as the sister taxon to the clade consisting of Tenontosaurus, Dryosaurus, Camptosaurus, and Iguanodon. Recent studies considered Zalmoxes, the best known representative of the clade, to be significantly smaller than closely related ornithopods such as Tenontosaurus, Camptosaurus, or Rhabdodon, and concluded that it was probably an island dwarf that inhabited the Maastrichtian Haţeg Island.

          Methodology/Principal Findings

          Rhabdodontid remains from the Santonian of western Hungary provide evidence for a new, small-bodied form, which we assign to Mochlodon vorosi n. sp. The new species is most similar to the early Campanian M. suessi from Austria, and the close affinities of the two species is further supported by the results of a global phylogenetic analysis of ornithischian dinosaurs. Bone histological studies of representatives of all rhabdodontids indicate a similar adult body length of 1.6–1.8 m in the Hungarian and Austrian species, 2.4–2.5 m in the subadults of both Zalmoxes robustus and Z. shqiperorum and a much larger, 5–6 m adult body length in Rhabdodon. Phylogenetic mapping of femoral lengths onto the results of the phylogenetic analysis suggests a femoral length of around 340 mm as the ancestral state for Rhabdodontidae, close to the adult femoral lengths known for Zalmoxes (320–333 mm).

          Conclusions/Significance

          Our analysis of body size evolution does not support the hypothesis of autapomorhic nanism for Zalmoxes. However, Rhabdodon is reconstructed as having undergone autapomorphic giantism and the reconstructed small femoral length (245 mm) of Mochlodon is consistent with a reduction in size relative to the ancestral rhabdodontid condition. Our results imply a pre-Santonian divergence between western and eastern rhabdodontid lineages within the western Tethyan archipelago.

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          Biology of the sauropod dinosaurs: the evolution of gigantism

          The herbivorous sauropod dinosaurs of the Jurassic and Cretaceous periods were the largest terrestrial animals ever, surpassing the largest herbivorous mammals by an order of magnitude in body mass. Several evolutionary lineages among Sauropoda produced giants with body masses in excess of 50 metric tonnes by conservative estimates. With body mass increase driven by the selective advantages of large body size, animal lineages will increase in body size until they reach the limit determined by the interplay of bauplan, biology, and resource availability. There is no evidence, however, that resource availability and global physicochemical parameters were different enough in the Mesozoic to have led to sauropod gigantism. We review the biology of sauropod dinosaurs in detail and posit that sauropod gigantism was made possible by a specific combination of plesiomorphic characters (phylogenetic heritage) and evolutionary innovations at different levels which triggered a remarkable evolutionary cascade. Of these key innovations, the most important probably was the very long neck, the most conspicuous feature of the sauropod bauplan. Compared to other herbivores, the long neck allowed more efficient food uptake than in other large herbivores by covering a much larger feeding envelope and making food accessible that was out of the reach of other herbivores. Sauropods thus must have been able to take up more energy from their environment than other herbivores. The long neck, in turn, could only evolve because of the small head and the extensive pneumatization of the sauropod axial skeleton, lightening the neck. The small head was possible because food was ingested without mastication. Both mastication and a gastric mill would have limited food uptake rate. Scaling relationships between gastrointestinal tract size and basal metabolic rate (BMR) suggest that sauropods compensated for the lack of particle reduction with long retention times, even at high uptake rates. The extensive pneumatization of the axial skeleton resulted from the evolution of an avian-style respiratory system, presumably at the base of Saurischia. An avian-style respiratory system would also have lowered the cost of breathing, reduced specific gravity, and may have been important in removing excess body heat. Another crucial innovation inherited from basal dinosaurs was a high BMR. This is required for fueling the high growth rate necessary for a multi-tonne animal to survive to reproductive maturity. The retention of the plesiomorphic oviparous mode of reproduction appears to have been critical as well, allowing much faster population recovery than in megaherbivore mammals. Sauropods produced numerous but small offspring each season while land mammals show a negative correlation of reproductive output to body size. This permitted lower population densities in sauropods than in megaherbivore mammals but larger individuals. Our work on sauropod dinosaurs thus informs us about evolutionary limits to body size in other groups of herbivorous terrestrial tetrapods. Ectothermic reptiles are strongly limited by their low BMR, remaining small. Mammals are limited by their extensive mastication and their vivipary, while ornithsichian dinosaurs were only limited by their extensive mastication, having greater average body sizes than mammals.
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            Archosaur adductor chamber evolution: integration of musculoskeletal and topological criteria in jaw muscle homology.

            The homologies of jaw muscles among archosaurs and other sauropsids have been unclear, confounding interpretation of adductor chamber morphology and evolution. Relevant topological patterns of muscles, nerves, and blood vessels were compared across a large sample of extant archosaurs (birds and crocodylians) and outgroups (e.g., lepidosaurs and turtles) to test the utility of positional criteria, such as the relative position of the trigeminal divisions, as predictors of jaw muscle homology. Anatomical structures were visualized using dissection, sectioning, computed tomography (CT), and vascular injection. Data gathered provide a new and robust view of jaw muscle homology and introduce the first synthesized nomenclature of sauropsid musculature using multiple lines of evidence. Despite the great divergences in cephalic morphology among birds, crocodylians, and outgroups, several key sensory nerves (e.g., n. anguli oris, n. supraorbitalis, n. caudalis) and arteries proved useful for muscle identification, and vice versa. Extant crocodylians exhibit an apomorphic neuromuscular pattern counter to the trigeminal topological paradigm: the maxillary nerve runs medial, rather than lateral to M. pseudotemporalis superficialis. Alternative hypotheses of homology necessitate less parsimonious interpretations of changes in topology. Sensory branches to the rictus, external acoustic meatus, supraorbital region, and other cephalic regions suggest conservative dermatomes among reptiles. Different avian clades exhibit shifts in some muscle positions, but maintain the plesiomorphic, diapsid soft-tissue topological pattern. Positional data suggest M. intramandibularis is merely the distal portion of M. pseudotemporalis separated by an intramuscular fibrocartilaginous sesamoid. These adductor chamber patterns indicate multiple topological criteria are necessary for interpretations of soft-tissue homology and warrant further investigation into character congruence and developmental connectivity. Copyright (c) 2007 Wiley-Liss, Inc.
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              Developmental plasticity in the life history of a prosauropod dinosaur.

              Long-bone histology indicates that the most common early dinosaur, the prosauropod Plateosaurus engelhardti from the Upper Triassic of Central Europe, had variable life histories. Although Plateosaurus grew at the fast rates typical for dinosaurs, as indicated by fibrolamellar bone, qualitative (growth stop) and quantitative (growth-mark counts) features of its histology are poorly correlated with body size. Individual life histories of P. engelhardti were influenced by environmental factors, as in modern ectothermic reptiles, but not in mammals, birds, or other dinosaurs.
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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, USA )
                1932-6203
                2012
                21 September 2012
                : 7
                : 9
                : e44318
                Affiliations
                [1 ]Hungarian Academy of Sciences–Eötvös Loránd University, Lendület Dinosaur Research Group, Budapest, Hungary
                [2 ]GeoBio-Center, Ludwig-Maximilians-Universität München, Munich, Germany
                [3 ]Center for Functional Anatomy and Evolution, Johns Hopkins University, Baltimore, Maryland, United States of America
                Monash University, Australia
                Author notes

                Competing Interests: The funding received from the Hungarian Oil and Gas Company (MOL) does not alter the authors' adherence to all the PLOS ONE policies on sharing data and materials.

                Conceived and designed the experiments: AŐ EP RB. Performed the experiments: AŐ EP. Analyzed the data: AŐ EP RB. Contributed reagents/materials/analysis tools: AŐ EP RB. Wrote the paper: AŐ EP RB DW.

                Article
                PONE-D-12-14120
                10.1371/journal.pone.0044318
                3448614
                23028518
                c24b0af5-ca60-4e09-84e7-5d730aee104d
                Copyright @ 2012

                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
                : 16 May 2012
                : 1 August 2012
                Page count
                Pages: 25
                Funding
                Field and laboratory work was supported by the MTA–ELTE Lendület Dinosaur Research Group (Grant no. 95102), Hungarian Scientific Research Fund (OTKA T–38045, PD 73021, NF 84193), National Geographic Society (Grant No. 7228–02, 7508–03), Bolyai Fellowship (Ő.A.), Hungarian Natural History Museum, Eötvös Loránd University, Jurassic Foundation, Hantken Foundation, and the Hungarian Oil and Gas Company (MOL). RJB was supported during the completion of this research by an Alexander von Humboldt Postdoctoral Research Fellowship and the German Research Foundation Emmy Noether Programme (BU 2587/3-1). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Anatomy and Physiology
                Developmental Biology
                Morphogenesis
                Growth Control
                Evolutionary Biology
                Histology
                Earth Sciences
                Paleontology
                Biogeography
                Biostratigraphy
                Paleobiology
                Vertebrate Paleontology

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                Uncategorized

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