Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-26T18:02:52.179Z Has data issue: false hasContentIssue false
  • English
  • Français

Establishing a framework for archosaur cranial mechanics

Published online by Cambridge University Press:  08 April 2016

Emily J. Rayfield  and
Angela C. Milner
Emily J. Rayfield
Affiliation:
Department of Earth Sciences, University of Bristol, Wills Memorial Building, Queens Road, Bristol BS8 1RJ, United Kingdom. E-mail: [email protected]
Angela C. Milner
Affiliation:
Department of Palaeontology, Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The aim of this analysis was to establish the basic mechanical principles of simple archosaur cranial form. In particular we estimated the influence of two key archosaur innovations, the secondary palate and the antorbital fenestra, on the optimal resistance of biting-induced loads. Although such simplified models cannot substitute for more complex cranial geometries, they can act as a clearly derived benchmark that can serve as a reference point for future studies incorporating more complex geometry. We created finite element (FE) models comprising either a tall, domed (oreinirostral) snout or a broad, flat (platyrostral) archosaur snout. Peak von Mises stress was recorded in models with and without a secondary palate and/or antorbital fenestra after the application of bite loads to the tooth row. We examined bilateral bending and unilateral torsion-inducing bites for a series of bite positions along the jaw, and conducted a sensitivity analysis of material properties. Pairwise comparison between different FE morphotypes revealed that oreinirostral models are stronger than their platyrostral counterparts. Oreinirostral models are also stronger in bending than in torsion, whereas platyrostral models are equally susceptible to either load type. As expected, we found that models with a fenestra always have greatest peak stresses and by inference are “weaker,” significantly so in oreinirostral forms and anterior biting platyrostral forms. Surprisingly, although adding a palate always lowers peak stress, this is rarely by large magnitudes and is not significant in bilateral bending bites. The palate is more important in unilateral torsion-inducing biting. Two basic principles of archosaur cranial construction can be derived from these simple models: (1) forms with a fenestra are suboptimally constructed with respect to biting, and (2) the presence or absence of a palate is significant to cranial integrity in unilaterally biting animals. Extrapolating these results to archosaur cranial evolution, it appears that if mechanical optimization were the only criterion on which skull form is based, then most archosaurs could in theory strengthen their skulls to increase resistance to biting forces. These strengthened morphotypes are generally not observed in the fossil record, however, and therefore archosaurs appear subject to various non-mechanical morphological constraints. Carnivorous theropod dinosaurs, for example, may retain large suboptimal fenestra despite generating large bite forces, owing to an interplay between craniofacial ossification and pneumatization. Furthermore, living crocodylians appear to strengthen their skull with a palate and filled fenestral opening in the most efficient way possible, despite being constrained perhaps by hydrodynamic factors to the weaker platyrostral morphotype. The future challenge is to ascertain whether these simple predictions are maintained when the biomechanics of complex cranial geometries are explored in more detail.

Type
Articles
Information
Paleobiology , Volume 34 , Issue 4 , Fall 2008 , pp. 494 - 515
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Benton, M. J. 1999. Scleromochlus taylori and the origin of dinosaurs and pterosaurs. Philosophical Transactions of the Royal Society of London B 354:1423–1446.Google Scholar
Brochu, C. A. 2001a. Crocodylian snouts in space and time: phylogenetic approaches toward adaptive radiation. American Zoologist 41:564–585.Google Scholar
Brochu, C. A. 2001b. Progress and future directions in archosaur phylogenetics. Journal of Paleontology 75:1185–1201.Google Scholar
Broom, R. 1913. On the South African pseudosuchian Euparkeria and allied genera. Proceedings of the Zoological Society of London 1913:619–633.Google Scholar
Busbey, A. B. 1995. The structural consequences of skull flattening in crocodilians. Pp. 173–192 in Thomason, J. J., ed. Functional morphology in vertebrate paleontology. Cambridge University Press, Cambridge.Google Scholar
Case, E. C. 1924. A possible explanation of fenestration in the primitive reptilian skull, with notes on the temporal region of the genus Dimetrodon . Contributions from the Museum of Geology, University of Michigan 2:1–12.Google Scholar
Charig, A. J., and Milner, A. C. 1997. Baryonyx walkeri, a fish eating dinosaur from the Wealden of Surrey. Bulletin of the Natural History Museum, London (Geology) 53:11–70.Google Scholar
Clark, J. M. 1994. Patterns of evolution in Mesozoic Crocodyliformes. Pp. 84–96 in Fraser, N. C. and Sues, H. D., eds. In the shadow of the dinosaurs. Cambridge University Press, Cambridge.Google Scholar
Clark, J. M., and Norell, M. A. 1992. The Early Cretaceous crocodylomorph Hylaeochampsa vectiana from the Wealden of the Isle of Wight. American Museum Novitates 3032:1–19.Google Scholar
Currey, J. D. 1987. The evolution of the mechanical properties of amniote bone. Journal of Biomechanics 20:1035–44.Google Scholar
Currey, J. D. 2002. Bones: structure and mechanics. Princeton University Press, Princeton, N.J. Google Scholar
Currey, J. D., and Alexander, R. McN. 1985. The thickness of the walls of tubular bones. Journal of Zoology 206:453–468.CrossRefGoogle Scholar
Daniel, W., and McHenry, C. 2001. Bite force to skull stress correlation—modelling the skull of Alligator mississippiensis in Grigg, G. C., Seebacher, F., and Franklin, C. E., eds. Crocodilian biology and evolution. Surrey Beatty, Chipping Norton, Australia.Google Scholar
Dumont, E. R., Piccirillo, J., and Grosse, I. R. 2005. Finite-Element Analysis of biting behavior and bone stress in the facial skeletons of bats. The Anatomical Record 283A:319–330.Google Scholar
Erickson, G. M., Catanese, J., and Keaveny, T. M. 2002. Evolution of the biomechanical material properties of the femur. The Anatomical Record 268:115–124.Google Scholar
Erickson, G. M., Van Kirk, S. D., Su, J., Levenston, M. E., Caler, W. E., and Carter, D. R. 1996. Bite-force estimation for Tyrannosaurus rex from tooth-marked bones. Nature 382:706–708.Google Scholar
Frazzetta, T. H. 1968. Adaptive problems and possibilities in the temporal fenestration of a tetrapod skull. Journal of Morphology 125:145–158.Google Scholar
Gauthier, J. A. 1986. Saurischian monophyly and the origin of birds. In Padian, K., ed. The origin of birds and the evolution of flight. Memoirs of the Californian Academy of Sciences 8:1–55.Google Scholar
Gregory, W. K., and Adams, L. A. 1915. The temporal fossae of vertebrates in relation to the jaw muscles. Science 41:763–765.Google Scholar
Hammer, Ø., Harper, D. A. T., and Ryan, P. D. 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4. http://palaeo-electronica.org/2001_1/past/issuel_01.htm Google Scholar
Herrel, A., Aerts, P., and De Vree, F. 1998. Static biting in lizards: functional morphology of the temporal ligaments. Journal of Zoology 244:135–143.Google Scholar
Herring, S. W., and Teng, S. 2000. Strain in the braincase and its sutures during function. American Journal of Physical Anthropology 112:575–593.Google Scholar
Huxley, T. H. 1875. On Stagonolepis robertsoni, and on the evolution of the Crocodilia. Quarterly Journal of the Geological Society 31:423–438.Google Scholar
Jaslow, C. R., and Biewener, A. A. 1995. Strain patterns in the horncores, cranial bones and sutures of goats (Copra hircus) during impact loading. Journal of Zoology 235:193–210.Google Scholar
Kobayashi, Y., Lü, J.-C., Dong, Z.-M., Barsbold, R., Azuma, Y., and Tomida, Y. 1999. Herbivorous diet in an ornithomimid dinosaur. Nature 402:480–481.Google Scholar
Kupczik, K., Dobson, C. A., Fagan, M. J., Crompton, R. H., Oxnard, C. E., and O'Higgins, P. 2007. Assessing mechanical function of the zygomatic region in macaques: validation and sensitivity testing of finite element models. Journal of Anatomy 210:41–53.Google Scholar
Langston, W. J. 1973. The crocodilian skull in historical perspective. Pp. 263–284 in Gans, C. and Parsons, T. S., eds. Biology of the Reptilia. Academic Press, New York.Google Scholar
Lauder, G. V. 1995. On the inference of function from structure. Pp. 1–18 in Thomason, J. J., ed. Functional morphology in vertebrate paleontology. Cambridge University Press, Cambridge.Google Scholar
McHenry, C. R., Clausen, P. D., Daniel, W. J. T., Meers, M. B., and Pendharkar, A. 2006. Biomechanics of the rostrum in crocodilians: a comparative analysis using finite element analysis. The Anatomical Record 288A:827–849.Google Scholar
Metzger, K. A., Daniel, W. J. T., and Ross, C. F. 2005. Comparison of beam theory and finite-element analysis with in vivo bone strain data from the Alligator cranium. The Anatomical Record 283A:331–348.Google Scholar
Molnar, R. E. 1973. The Cranial Morphology and Mechanics of Tyrannosaurus rex (Reptilia: Saurischia). Ph.D. dissertation. University of California, Los Angeles.Google Scholar
Page, R. D. M. 2001. NEXUS Data Editor. http://taxonomy.zoology.gla.ac.uk/rod/rod.html Google Scholar
Pol, D., and Apesteguia, S. 2005. New Araripesuchus remains from the early Late Cretaceous (Cenomanian-Turonian) of Patagonia. American Museum Novitates 3490:1–38.CrossRefGoogle Scholar
Rafferty, K. L., Herring, S. W., and Marshall, C. D. 2003. Biomechanics of the rostrum and the role of facial sutures. Journal of Morphology 257:33–44.CrossRefGoogle ScholarPubMed
Rayfield, E. J. 2004. Cranial mechanics and feeding in Tyrannosaurus rex . Proceedings of the Royal Society of London B 271:1451–1459.Google Scholar
Rayfield, E. J. 2005a. Using finite-element analysis to investigate suture morphology: a case study using large carnivorous dinosaurs. The Anatomical Record 283A:349–365.CrossRefGoogle Scholar
Rayfield, E. J. 2005b. Aspects of comparative cranial mechanics in the theropod dinosaurs Coelophysis, Allosaurus and Tyrannosaurus . Zoological Journal of the Linnean Society 144:309–316.Google Scholar
Rayfield, E. J., Norman, D. B., Horner, C. C., Horner, J. R., Smith, P. May, Thomason, J. J., and Upchurch, P. 2001. Cranial design and function in a large theropod dinosaur. Nature 409:1033–1037.Google Scholar
Rayfield, E. J., Milner, A. C., Xuan, V. Bui, and Young, P. G. 2007. Functional morphology of spinosaur ‘crocodile-mimic’ dinosaurs. Journal of Vertebrate Paleontology 27:892–901.Google Scholar
Reig, O. A. 1970. The Proterosuchia and the early evolution of the archosaurs: an essay about the origin of a major taxon. Bulletin of the Museum of Comparative Zoology, Harvard University 139:229–292.Google Scholar
Ross, C. F. 2001. In vivo function of the craniofacial haft: the interorbital “pillar.” American Journal of Physical Anthropology 116:108–139.Google Scholar
Ross, C. A., and Metzger, K. A. 2004. Bone strain gradients and optimization in vertebrate skulls. Annals of Anatomy 186:387–396.Google Scholar
Schmidt-Nielson, K. 1984. Scaling: why is animal size so important? Cambridge University Press, Cambridge.Google Scholar
Sereno, P. C., Sidor, C. A., Larsson, H. C., and Gado, B. 2003. A new notosuchian from the early Cretaceous of Niger. Journal of Vertebrate Paleontology 23:477–482.Google Scholar
Smith, K. K. 1993. The form of the feeding apparatus in terrestrial vertebrates: studies of adaptation and constraint. Pp. 150–196 in Hanken, J. and Hall, B. K., eds. The skull, Vol. 3. University of Chicago Press, Chicago.Google Scholar
Steel, R. 1989. Crocodiles. Christopher Helm, Kent.Google Scholar
Strait, D. S., Wang, Q., Dechow, P. C., Ross, C. F., Richmond, B. G., Spencer, M. A., and Patel, B. A. 2005. Modeling elastic properties in finite element analysis: how much precision is needed to produce an accurate model? The Anatomical Record 283A:275–287.Google Scholar
Thomason, J. J., Grovum, L. E., Deswysen, A. G., and Bignell, W. W. 2001. In vivo surface strain and stereology of the frontal and maxillary bones of sheep: implications for the structural design of the mammalian skull. The Anatomical Record 264:325–338.Google Scholar
Thomason, J. J., and Russell, A. P. 1986. Mechanical factors in the evolution of the mammalian secondary palate—a theoretical analysis. Journal of Morphology 189:199–213.Google Scholar
Tykoski, R. S., Rowe, T., Ketcham, R. A., and Colbert, M. W. 2002. Calsoyasuchus valliceps, a new crocodyliform from the Early Jurassic Kayenta Formation of Arizona. Journal of Vertebrate Paleontology 22:593–611.Google Scholar
Walker, A. D. 1961. Triassic reptiles from the Elgin area: Stagonolepis, Dasygnathus and their allies. Philosophical Transactions of the Royal Society of London B 244:103–204.Google Scholar
Wang, Q., and Dechow, P. C. 2006. Elastic properties of external cortical bone in the craniofacial skeleton of the rhesus monkey. American Journal of Physical Anthropology 131:402–415.Google Scholar
Wang, Q., Dechow, P. C., Wright, B. W., Ross, C. F., Strait, D. S., Richmond, B. G., and Spencer, M. A., in press. Surface strain on bone and sutures in a monkey facial skeleton: an in vitro method and its relevance to Finite Element Analysis. In Vinyard, C. J., Ravosa, M., and Wall, C. E., eds. Primate craniofacial function and biology. Springer, New York.Google Scholar
Wang, Q., Strait, D. S., and Dechow, P. C. 2006. A comparison of cortical elastic properties in the craniofacial skeletons of three primate species and its relevance to human evolution. Journal of Human Evolution 51:375–382.CrossRefGoogle ScholarPubMed
Witmer, L. M. 1997. The evolution of the antorbital cavity of archosaurs: A study in soft-tissue reconstruction in the fossil record with an analysis of the function of pneumaticity. Journal of Vertebrate Paleontology 17:1–73.Google Scholar
Witzel, U., and Preuschoft, H. 2005. Finite-element model construction for the virtual synthesis of the skulls in vertebrates: case study of Diplodocus . The Anatomical Record 283A:391–401.Google Scholar
Supplementary material: File

Rayfield and Milner supplementary material

Appendices

Download Rayfield and Milner supplementary material(File)
File 56.8 KB