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      Mechanical Analysis of Feeding Behavior in the Extinct “Terror Bird” Andalgalornis steulleti (Gruiformes: Phorusrhacidae)

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          Abstract

          The South American phorusrhacid bird radiation comprised at least 18 species of small to gigantic terrestrial predators for which there are no close modern analogs. Here we perform functional analyses of the skull of the medium-sized (∼40 kg) patagornithine phorusrhacid Andalgalornis steulleti (upper Miocene–lower Pliocene, Andalgalá Formation, Catamarca, Argentina) to assess its mechanical performance in a comparative context. Based on computed tomographic (CT) scanning and morphological analysis, the skull of Andalgalornis steulleti is interpreted as showing features reflecting loss of intracranial immobility. Discrete anatomical attributes permitting such cranial kinesis are widespread phorusrhacids outgroups, but this is the first clear evidence of loss of cranial kinesis in a gruiform bird and may be among the best documented cases among all birds. This apomorphic loss is interpreted as an adaptation for enhanced craniofacial rigidity, particularly with regard to sagittal loading. We apply a Finite Element approach to a three-dimensional (3D) model of the skull. Based on regression analysis we estimate the bite force of Andalgalornis at the bill tip to be 133 N. Relative to results obtained from Finite Element Analysis of one of its closest living relatives (seriema) and a large predatory bird (eagle), the phorusrhacid's skull shows relatively high stress under lateral loadings, but low stress where force is applied dorsoventrally (sagittally) and in “pullback” simulations. Given the relative weakness of the skull mediolaterally, it seems unlikely that Andalgalornis engaged in potentially risky behaviors that involved subduing large, struggling prey with its beak. We suggest that it either consumed smaller prey that could be killed and consumed more safely (e.g., swallowed whole) or that it used multiple well-targeted sagittal strikes with the beak in a repetitive attack-and-retreat strategy.

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          Most cited references16

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          Bite club: comparative bite force in big biting mammals and the prediction of predatory behaviour in fossil taxa.

          We provide the first predictions of bite force (BS) in a wide sample of living and fossil mammalian predators. To compare between taxa, we calculated an estimated bite force quotient (BFQ) as the residual of BS regressed on body mass. Estimated BS adjusted for body mass was higher for marsupials than placentals and the Tasmanian devil (Sarcophilus harrisii) had the highest relative BS among extant taxa. The highest overall BS was in two extinct marsupial lions. BFQ in hyaenas were similar to those of related, non-osteophagous taxa challenging the common assumption that osteophagy necessitates extreme jaw muscle forces. High BFQ in living carnivores was associated with greater maximal prey size and hypercarnivory. For fossil taxa anatomically similar to living relatives, BFQ can be directly compared, and high values in the dire wolf (Canis dirus) and thylacine (Thylacinus cynocephalus) suggest that they took relatively large prey. Direct inference may not be appropriate where morphologies depart widely from biomechanical models evident in living predators and must be considered together with evidence from other morphological indicators. Relatively low BFQ values in two extinct carnivores with morphologies not represented among extant species, the sabrecat, Smilodon fatalis, and marsupial sabretooth, Thylacosmilus atrox, support arguments that their killing techniques also differed from extant species and are consistent with 'canine-shear bite' and 'stabbing' models, respectively. Extremely high BFQ in the marsupial lion, Thylacoleo carnifex, indicates that it filled a large-prey hunting niche.
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            Bite forces and evolutionary adaptations to feeding ecology in carnivores.

            The Carnivora spans the largest ecological and body size diversity of any mammalian order, making it an ideal basis for studies of evolutionary ecology and functional morphology. For animals with different feeding ecologies, it may be expected that bite force represents an important evolutionary adaptation, but studies have been constrained by a lack of bite force data. In this study we present predictions of bite forces for 151 species of extant carnivores, comprising representatives from all eight families and the entire size and ecological spectrum within the order. We show that, when normalized for body size, bite forces differ significantly between the various feeding categories. At opposing extremes and independent of genealogy, consumers of tough fibrous plant material and carnivores preying on large prey both have high bite forces for their size, while bite force adjusted for body mass is low among specialized insectivores. Omnivores and carnivores preying on small prey have more moderate bite forces for their size. These findings indicate that differences in bite force represent important adaptations to and indicators of differing feeding ecologies throughout carnivoran evolution. Our results suggest that the incorporation of bite force data may assist in the construction of more robust evolutionary and palaeontological analyses of feeding ecology.
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              Supermodeled sabercat, predatory behavior in Smilodon fatalis revealed by high-resolution 3D computer simulation.

              The American sabercat Smilodon fatalis is among the most charismatic of fossil carnivores. Despite broad agreement that its extraordinary anatomy reflects unique hunting techniques, after >150 years of study, many questions remain concerning its predatory behavior. Were the "sabers" used to take down large prey? Were prey killed with an eviscerating bite to the abdomen? Was its bite powerful or weak compared with that of modern big cats? Here we quantitatively assess the sabercat's biomechanical performance using the most detailed computer reconstructions yet developed for the vertebrate skull. Our results demonstrate that bite force driven by jaw muscles was relatively weak in S. fatalis, one-third that of a lion (Panthera leo) of comparable size, and its skull was poorly optimized to resist the extrinsic loadings generated by struggling prey. Its skull is better optimized for bites on restrained prey where the bite is augmented by force from the cervical musculature. We conclude that prey were brought to ground and restrained before a killing bite, driven in large part by powerful cervical musculature. Because large prey is easier to restrain if its head is secured, the killing bite was most likely directed to the neck. We suggest that the more powerful jaw muscles of P. leo may be required for extended, asphyxiating bites and that the relatively low bite forces in S. fatalis might reflect its ability to kill large prey more quickly, avoiding the need for prolonged bites.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2010
                18 August 2010
                : 5
                : 8
                : e11856
                Affiliations
                [1 ]CONICET - División Paleontología Vertebrados, Facultad de Ciencias Naturales y Museo, Museo de La Plata, Universidad Nacional de La Plata, La Plata, Argentina
                [2 ]Laboratorio de Paleontología, Instituto de Geociencias, Universidad Austral de Chile, Valdivia, Chile
                [3 ]Evolution and Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, Australia
                [4 ]Department of Biomedical Sciences, College of Osteopathic Medicine, Ohio University, Athens, Ohio, United States of America
                Zoological Society of London, United Kingdom
                Author notes

                Conceived and designed the experiments: FJD CPT KM SW. Performed the experiments: FJD CPT. Analyzed the data: FJD KM SW. Contributed reagents/materials/analysis tools: LMW SW. Wrote the paper: FJD CPT KM LMW SW.

                Article
                09-PONE-RA-10901R1
                10.1371/journal.pone.0011856
                2923598
                20805872
                5e7295aa-8938-40a9-9d7b-f247a9f5e3d1
                Degrange 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
                : 8 June 2009
                : 28 June 2010
                Page count
                Pages: 7
                Categories
                Research Article
                Evolutionary Biology/Bioinformatics
                Evolutionary Biology/Paleontology
                Mathematics/Finite Element Analysis

                Uncategorized
                Uncategorized

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