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

CONICET-División Paleontología Vertebrados, Facultad de Ciencias Naturales y Museo, Museo de La Plata, Universidad Nacional de La Plata, La Plata, Argentina.
PLoS ONE (Impact Factor: 3.23). 08/2010; 5(8):e11856. DOI: 10.1371/journal.pone.0011856
Source: PubMed


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 (approximately 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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    • "There was also overwhelming evidence that the mineral mass and microstructure and nanostructure of bone are susceptible to stimulation by mechanical loads, ensuring that its mechanical behavior and strength are adapted to environmental changes20212223242526272829.A Ba Ca Figure 1: (a) The three parts on the skull of birds and micro-CT scan images of cranial bone of (b) Great Spotted Woodpecker; (c) Grey Headed Woodpecker; (d) Eurasian hoopoe; (e) Mongolian skylark; (f) Great Tit: (A) forehead; (B) temporomandibular; (C) occiput. For example, the shape of the bill was adapted to the forces on it during drilling[30], and in vivo bite force was reflected in skull morphology and geometry and in the capacity for contraction of the jaw muscles[31,32]. The hyoid bone of woodpecker has unique strength and flexibility owing to its unique micro/nanohierarchical composite structures. It consists of a flexible cartilage and bone skeleton covered with a thin tissue layer having high strength of 136 MPa and elasticity of 3.74 GPa. "
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    ABSTRACT: Natural biological materials such as bone, teeth and nacre are nano-composites of protein and mineral frequently exhibit highly superior strength for self-assembly and nanofabrication. Mineral mass and microstructure/nanostructure of bone are susceptible to stimulation by mechanical loads, ensuring that its mechanical behavior and strength are adapted to environmental changes. Woodpeckers repeatedly drum tree trunks at a speed of 6-7 m s−1 and acceleration of ~1000 g with no head injuries. The uneven distribution of spongy bone has been founded on woodpecker's skull in our previous study. More knowledge of the distribution of the shock-absorbing spongy bone could be incorporated into the design of new safety helmets, sports products, and other devices that need to be able to resist the impact. In this study, the effect of microstructure of spongy bone in different parts on woodpecker’s skull compared with other birds was observed and analyzed. It was found that the unique coordinate ability of micro-parameters in different parts of woodpecker’s skull could be one of the most important roles of its resistance to impact injury. Better understanding of the materials would provide new inspirations of shock-absorbing composite materials in engineering.
    Full-text · Article · Nov 2013 · Journal of Nanomaterials
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    • "Andalgalornis steulleti (Kraglievich 1931), from the upper Miocene–lower Pliocene (≈6 million years ago) of Argentina, was a medium-sized patagornithine phorusrhacid of about 40 kg body mass, 1.4 m height, and 370 mm total skull length [11], [12]. Together with the long legs, the atypical large skull with high and narrow beak is a characteristic feature of all phorusrhacids [13]. "
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    ABSTRACT: Andalgalornis steulleti from the upper Miocene-lower Pliocene (≈6 million years ago) of Argentina is a medium-sized patagornithine phorusrhacid. It was a member of the predominantly South American radiation of 'terror birds' (Phorusrhacidae) that were apex predators throughout much of the Cenozoic. A previous biomechanical study suggests that the skull would be prepared to make sudden movements in the sagittal plane to subdue prey. We analyze the flexion patterns of the neck of Andalgalornis based on the neck vertebrae morphology and biometrics. The transitional cervical vertebrae 5th and 9th clearly separate regions 1-2 and 2-3 respectively. Bifurcate neural spines are developed in the cervical vertebrae 7th to 12th suggesting the presence of a very intricate ligamentary system and of a very well developed epaxial musculature. The presence of the lig. elasticum interespinale is inferred. High neural spines of R3 suggest that this region concentrates the major stresses during downstrokes. The musculoskeletal system of Andalgalornis seems to be prepared (1) to support a particularly big head during normal stance, and (2) to help the neck (and the head) rising after the maximum ventroflexion during a strike. The study herein is the first interpretation of the potential performance of the neck of Andalgalornis in its entirety and we considered this an important starting point to understand and reconstruct the flexion pattern of other phorusrhacids from which the neck is unknown.
    Full-text · Article · May 2012 · PLoS ONE
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    • "Psilopterus lemoinei (and all the phorusrhacids), as we stated previously , lack both hinges. This suggests that cranial kinesis was lost secondarily in the history of the Phorushracidae (Degrange et al., 2010). "
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    ABSTRACT: Psilopterus lemoinei, the largest species in this genus, was a small terror bird weighing 8–9 kg, and was a ground bird with functionally tridactyl feet. New remains of this phorusrhacid, including an exceptionally preserved anterior part of a skull recovered from the Patagonian Killik Aike Norte locality (Santa Cruz Formation, late early Miocene), is now available for study. The main purpose of this paper is to provide a detailed morphological description of Psilopterus lemoinei. The new fossils show for the first time that the internal structure of the beak is hollow and reinforced with thin-walled trabeculae. The absence of zona flexoria palatina and zona flexoria arcus jugalis are key features related to the evolution of cranial akinesis. Homologies of the narial and fenestra antorbitalis boundaries have been clarified. Our re-examination allows the establishment of primary osteological homologies useful in comparative anatomy, functional morphology, and phylogenetic studies.
    Full-text · Article · Sep 2011 · Journal of Vertebrate Paleontology
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