Cranial performance in the Komodo dragon (Varanus komodoensis) as revealed by high‐resolution 3‐D finite element analysis

The Komodo dragon (Varanus komodoensis) displays a unique hold and pull‐feeding technique. Its delicate ‘space‐frame’ skull morphology differs greatly from that apparent in most living large prey specialists and is suggestive of a high degree of optimization, wherein use of materials is minimized. Here, using high‐resolution finite element modelling based on dissection and in vivo bite and pull data, we present results detailing the mechanical performance of the giant lizard's skull. Unlike most modern predators, V. komodoensis applies minimal input from the jaw muscles when butchering prey. Instead it uses series of actions controlled by postcranial muscles. A particularly interesting feature of the performance of the skull is that it reveals considerably lower overall stress when these additional extrinsic forces are added to those of the jaw adductors. This remarkable reduction in stress in response to additional force is facilitated by both internal and external bone anatomy. Functional correlations obtained from these analyses also provide a solid basis for the interpretation of feeding ecology in extinct species, including dinosaurs and sabre‐tooth cats, with which V. komodoensis shares various cranial and dental characteristics.

[1]  E. Pedroni,et al.  The calibration of CT Hounsfield units for radiotherapy treatment planning. , 1996, Physics in medicine and biology.

[2]  H. Cardoso Brief communication: the collection of identified human skeletons housed at the Bocage Museum (National Museum of Natural History), Lisbon, Portugal. , 2006, American journal of physical anthropology.

[3]  P. Withers,et al.  Diet and foraging behaviour of the semi-aquatic Varanus mertensi (Reptilia : Varanidae) , 2005 .

[4]  Claudio Ciofi,et al.  Parthenogenesis in Komodo dragons , 2006, Nature.

[5]  Lance D. McBrayer,et al.  Bite Force, Behavior, and Electromyography in the Teiid Lizard, Tupinambis teguixin , 2002, Copeia.

[6]  Emily J Rayfield,et al.  Cranial mechanics and feeding in Tyrannosaurus rex , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[7]  E. Rayfield,et al.  Ecological and evolutionary implications of dinosaur feeding behaviour. , 2006, Trends in ecology & evolution.

[8]  Peter Aerts,et al.  Static biting in lizards: functional morphology of the temporal ligaments , 1998 .

[9]  David S Strait,et al.  Modeling elastic properties in finite-element analysis: how much precision is needed to produce an accurate model? , 2005, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[10]  R. B. Ashman,et al.  Relations of mechanical properties to density and CT numbers in human bone. , 1995, Medical engineering & physics.

[11]  S. Reilly,et al.  Prey processing in amniotes: biomechanical and behavioral patterns of food reduction. , 2001, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[12]  Kathleen K. Smith An electromyographic study of the function of the jaw adducting muscles in Varanus exanthematicus (varanidae) , 1982, Journal of morphology.

[13]  S. Herring,et al.  Biomechanics of the rostrum and the role of facial sutures , 2003, Journal of morphology.

[14]  S. Wroe,et al.  Bite forces and evolutionary adaptations to feeding ecology in carnivores. , 2007, Ecology.

[15]  Philip Clausen,et al.  High‐Resolution Three‐Dimensional Computer Simulation of Hominid Cranial Mechanics , 2007, Anatomical record.

[16]  Ulrich Witzel,et al.  Functional shape of the skull in vertebrates: which forces determine skull morphology in lower primates and ancestral synapsids? , 2005, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[17]  S. Herring,et al.  Craniofacial sutures: Morphology, growth, and in vivo masticatory strains , 1999, Journal of morphology.

[18]  R. Alexander,et al.  Estimates of forces exerted by the jaw muscles of some reptiles , 1987 .

[19]  Stephen Wroe,et al.  Supermodeled sabercat, predatory behavior in Smilodon fatalis revealed by high-resolution 3D computer simulation , 2007, Proceedings of the National Academy of Sciences.

[20]  L. McBrayer,et al.  Prey transport kinematics in Tupinambis teguixin and Varanus exanthematicus: conservation of feeding behavior in 'chemosensory-tongued' lizards. , 2000, The Journal of experimental biology.

[21]  S W Herring,et al.  Strain in the braincase and its sutures during function. , 2000, American journal of physical anthropology.

[22]  Emily J. Rayfield,et al.  Cranial design and function in a large theropod dinosaur , 2001, Nature.

[23]  D. Henderson,et al.  Fused and vaulted nasals of tyrannosaurid dinosaurs: Implications for cranial strength and feeding mechanics , 2006 .

[24]  W L Hylander,et al.  Elastic properties and masticatory bone stress in the macaque mandible. , 2000, American journal of physical anthropology.

[25]  W. Hylander Mandibular function in Galago crassicaudatus and Macaca fascicularis: An in vivo approach to Stress Analysis of the mandible , 1979, Journal of morphology.

[26]  P. Aerts,et al.  BITE ANF JOINT FORCE ANALYISS IN CAIMNAN CROCODILUS , 1995 .

[27]  Emily J. Rayfield,et al.  Aspects of comparative cranial mechanics in the theropod dinosaurs Coelophysis, Allosaurus and Tyrannosaurus , 2005 .

[28]  William A. Akersten Canine function in Smilodon (Mammalia; Felidae; Machairodontinae) , 1985, Contributions to Science.

[29]  R. Mertens Die Familie der Warane (Varanidae) , 1942 .

[30]  W. Auffenberg The Behavioral Ecology of the Komodo Monitor , 1981 .

[31]  S. Wroe,et al.  Bite club: comparative bite force in big biting mammals and the prediction of predatory behaviour in fossil taxa , 2005, Proceedings of the Royal Society B: Biological Sciences.

[32]  A. Russell,et al.  Functional variation of neck muscles and their relation to feeding style in Tyrannosauridae and other large theropod dinosaurs , 2007, Anatomical record.

[33]  R B Ashman,et al.  Elastic properties of human supraorbital and mandibular bone. , 1993, American journal of physical anthropology.

[34]  J. Thomason,et al.  Analysis of strain and stress in the equine hoof capsule using finite element methods: comparison with principal strains recorded in vivo. , 2010, Equine veterinary journal.

[35]  A. Herrel,et al.  Modulatory complexity of the feeding repertoire in scincid lizards , 1999, Journal of Comparative Physiology A.

[36]  Anthony Herrel,et al.  Sexual dimorphism of head size in Gallotia galloti: testing the niche divergence hypothesis by functional analyses , 1999 .

[37]  E. Rayfield Finite Element Analysis and Understanding the Biomechanics and Evolution of Living and Fossil Organisms , 2007 .

[38]  T. Frazzetta A functional consideration of cranial kinesis in lizards , 1962, Journal of morphology.

[39]  Philip Clausen,et al.  Computer simulation of feeding behaviour in the thylacine and dingo as a novel test for convergence and niche overlap , 2007, Proceedings of the Royal Society B: Biological Sciences.

[40]  J. Thomason,et al.  Functional Morphology in Vertebrate Paleontology , 1998 .

[41]  C. McHenry,et al.  Bite force to skull stress correlation - modelling the skull of Alligator mississippiensis , 2001 .

[42]  A. Busbey Form and function of the feeding apparatus of Alligator mississippiensis , 1989, Journal of morphology.

[43]  Rebecca Snyder,et al.  Morphological changes in pedal phalanges through ornithopod dinosaur evolution: A biomechanical approach , 2007, Journal of morphology.

[44]  Ian R Grosse,et al.  Finite-element analysis of biting behavior and bone stress in the facial skeletons of bats. , 2005, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[45]  Callum F Ross,et al.  Comparison of beam theory and finite-element analysis with in vivo bone strain data from the alligator cranium. , 2005, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[46]  C. McHenry,et al.  Biomechanics of the rostrum in crocodilians: a comparative analysis using finite-element modeling. , 2006, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.