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      Biology of the sauropod dinosaurs: the evolution of gigantism

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          Abstract

          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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          The evolution of body size: what keeps organisms small?

          It is widely agreed that fecundity selection and sexual selection are the major evolutionary forces that select for larger body size in most organisms. The general, equilibrium view is that selection for large body size is eventually counterbalanced by opposing selective forces. While the evidence for selection favoring larger body size is overwhelming, counterbalancing selection favoring small body size is often masked by the good condition of the larger organism and is therefore less obvious. The suggested costs of large size are: (1) viability costs in juveniles due to long development and/or fast growth; (2) viability costs in adults and juveniles due to predation, parasitism, or starvation because of reduced agility, increased detectability, higher energy requirements, heat stress, and/or intrinsic costs of reproduction; (3) decreased mating success of large males due to reduced agility and/or high energy requirements; and (4) decreased reproductive success of large females and males due to late reproduction. A review of the literature indicates a substantial lack of empirical evidence for these various mechanisms and highlights the need for experimental studies that specifically address the fitness costs of being large at the ecological, physiological, and genetic levels. Specifically, theoretical investigations and comprehensive case studies of particular model species are needed to elucidate whether sporadic selection in time and space is sufficient to counterbalance perpetual and strong selection for large body size.
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            GEOCARBSULF: A combined model for Phanerozoic atmospheric O2 and CO2

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              Sauropod dinosaur phylogeny: critique and cladistic analysis

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                Author and article information

                Journal
                Biol Rev Camb Philos Soc
                brv
                Biological Reviews of the Cambridge Philosophical Society
                Blackwell Publishing Ltd
                1464-7931
                1469-185X
                February 2011
                : 86
                : 1
                : 117-155
                Affiliations
                [1 ]simpleSteinmann Institute, Division of Palaeontology, University of Bonn Nussallee 8, 53115 Bonn, Germany
                [2 ]simpleInstitut für Biologie und Sachunterricht und ihre Didaktik, University of Flensburg Auf dem Campus 1, 24943 Flensburg, Germany
                [3 ]simpleClinic for Zoo Animals, Exotic Pets and Wildlife, University of Zurich Winterthurerstr. 260, 8057 Zurich, Switzerland
                [4 ]simpleBayerische Staatssammlung für Paläontologie und Geologie, University of Munich Richard-Wagner-Strasse 10, 80333 Munich, Germany
                [5 ]simpleInstitut für Zoologie, Abteilung Ökologie, University of Mainz Johann-Joachim-Becher Weg 13, 55128 Mainz, Germany
                [6 ]simpleZentrum für Weltraummedizin Berlin, Institut für Physiologie, Charite-University of Berlin Arnimallee 22, 14195 Berlin, Germany
                [7 ]simpleInstitut für Tierwissenschaften, University of Bonn Endenicher Allee 15, 53115 Bonn, Germany
                [8 ]simpleMuseum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitätsforschung an der Humboldt-Universität zu Berlin Invalidenstrasse 43, 10115 Berlin, Germany
                [9 ]simpleInstitut für Zoologie, Morphologie und Systematik, University of Bonn Poppelsdorfer Schloss, 53115 Bonn, Germany
                [10 ]simpleInstitut für Anatomie, Abteilung für Funktionelle Morphologie, University of Bochum Universitätsstrasse 150, 44801 Bochum, Germany
                [11 ]simpleSteinmann Institute, Division of Mineralogy, University of Bonn Poppelsdorfer Schloss, 53115 Bonn, Germany
                [12 ]simpleInstitut für Konstruktionstechnik, Fakultät für Maschinenbau, University of Bochum Universitätsstrasse 150, 44801 Bochum, Germany
                Author notes

                Re-use of this article is permitted in accordance with the Terms and Conditions set out at http://wileyonlinelibrary.com/onlineopen#OnlineOpen_Terms

                Article
                10.1111/j.1469-185X.2010.00137.x
                3045712
                21251189
                ab1f6344-df63-4f10-b5d5-0b99ecb941ca
                Biological Reviews © 2011 Cambridge Philosophical Society

                Re-use of this article is permitted in accordance with the Creative Commons Deed, Attribution 2.5, which does not permit commercial exploitation.

                History
                : 09 September 2009
                : 13 March 2010
                : 16 March 2010
                Categories
                Original Articles

                Ecology
                sauropoda,evolutionary innovation,phylogenetic heritage,long neck,dinosauria,gigantism,mesozoic
                Ecology
                sauropoda, evolutionary innovation, phylogenetic heritage, long neck, dinosauria, gigantism, mesozoic

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