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      The Costs of Carnivory

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      PLoS Biology
      Public Library of Science

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          Abstract

          Mammalian carnivores fall into two broad dietary groups: smaller carnivores (<20 kg) that feed on very small prey (invertebrates and small vertebrates) and larger carnivores (>20 kg) that specialize in feeding on large vertebrates. We develop a model that predicts the mass-related energy budgets and limits of carnivore size within these groups. We show that the transition from small to large prey can be predicted by the maximization of net energy gain; larger carnivores achieve a higher net gain rate by concentrating on large prey. However, because it requires more energy to pursue and subdue large prey, this leads to a 2-fold step increase in energy expenditure, as well as increased intake. Across all species, energy expenditure and intake both follow a three-fourths scaling with body mass. However, when each dietary group is considered individually they both display a shallower scaling. This suggests that carnivores at the upper limits of each group are constrained by intake and adopt energy conserving strategies to counter this. Given predictions of expenditure and estimates of intake, we predict a maximum carnivore mass of approximately a ton, consistent with the largest extinct species. Our approach provides a framework for understanding carnivore energetics, size, and extinction dynamics.

          Author Summary

          Carnivores fall into two dietary groups based on the energetic requirements of their feeding strategies: small-bodied species, which feed mostly on prey smaller than themselves, and large-bodied species, which prefer prey around their own size. While carnivores around the size of a lynx or larger can obtain higher net energy intake by switching to relatively large prey, the difficulty of catching and subduing these animals means that a large-prey specialist would expend twice as much energy as a small-prey specialist of equivalent body size. Analyzing the balance between energy intake and expenditure across a range of species, we predict that mammalian carnivores should have a maximum body mass of one ton. Thus, mammalian carnivores are relatively small compared with the largest extinct terrestrial herbivorous mammals, such as the Indricothere, which weighed around 15 tons. The largest existing carnivore, the polar bear, is only around half a ton, while the largest known extinct carnivores, such as the short-faced bear, weighed around one ton. This study suggests that those extremely large carnivores would have been heavily reliant on abundant large prey, helping to explain why the largest modern mammalian carnivores are rare and vulnerable to extinction.

          Abstract

          A simple theoretical model provides a framework to understand carnivore energy budgets and reveals insights into the evolution of body size in mammalian carnivores.

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          Most cited references59

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          Multiple causes of high extinction risk in large mammal species.

          Many large animal species have a high risk of extinction. This is usually thought to result simply from the way that species traits associated with vulnerability, such as low reproductive rates, scale with body size. In a broad-scale analysis of extinction risk in mammals, we find two additional patterns in the size selectivity of extinction risk. First, impacts of both intrinsic and environmental factors increase sharply above a threshold body mass around 3 kilograms. Second, whereas extinction risk in smaller species is driven by environmental factors, in larger species it is driven by a combination of environmental factors and intrinsic traits. Thus, the disadvantages of large size are greater than generally recognized, and future loss of large mammal biodiversity could be far more rapid than expected.
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            Bioenergetics and the Determination of Home Range Size

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              The scaling of animal space use.

              Space used by animals increases with increasing body size. Energy requirements alone can explain how population density decreases, but not the steep rate at which home range area increases. We present a general mechanistic model that predicts the frequency of interaction, spatial overlap, and loss of resources to neighbors. Extensive empirical evidence supports the model, demonstrating that spatial constraints on defense cause exclusivity of home range use to decrease with increasing body size. In large mammals, over 90% of available resources may be lost to neighbors. Our model offers a general framework to understand animal space use and sociality.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Biol
                pbio
                PLoS Biology
                Public Library of Science (San Francisco, USA )
                1544-9173
                1545-7885
                February 2007
                16 January 2007
                : 5
                : 2
                : e22
                Affiliations
                [1]Institute of Zoology, Zoological Society of London, London, United Kingdom
                Princeton University, United States of America
                Author notes
                * To whom correspondence should be addressed. E-mail: chris.carbone@ 123456ioz.ac.uk
                Article
                06-PLBI-RA-0856R2 plbi-05-02-05
                10.1371/journal.pbio.0050022
                1769424
                17227145
                a4dd8139-6919-4686-8cc0-0f7c5a0612e1
                Copyright: © 2007 Carbone et al. 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
                : 19 May 2006
                : 15 November 2006
                Page count
                Pages: 6
                Categories
                Research Article
                Ecology
                Ecology
                Evolutionary Biology
                Evolutionary Biology
                Mammals
                Custom metadata
                Carbone C, Teacher A, Rowcliffe JM (2007) The costs of carnivory. PLoS Biol 5(2): e22. doi: 10.1371/journal.pbio.0050022

                Life sciences
                Life sciences

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