Hostname: page-component-77c89778f8-m8s7h Total loading time: 0 Render date: 2024-07-17T11:09:13.300Z Has data issue: false hasContentIssue false
  • English
  • Français

Craniocervical feeding dynamics of Tyrannosaurus rex

Published online by Cambridge University Press:  08 April 2016

Eric Snively  and
Anthony P. Russell
Eric Snively
Affiliation:
Department of Biological Sciences, University of Calgary, 2500 University Drive NW, Calgary, Alberta T2N 1N4, Canada. E-mail: esnively@ucalgary.ca
Anthony P. Russell
Affiliation:
Department of Biological Sciences, University of Calgary, 2500 University Drive NW, Calgary, Alberta T2N 1N4, Canada. E-mail: arussell@ucalgary.ca
Get access Rights & Permissions [Opens in a new window]

Abstract

Tyrannosaurus rex and other tyrannosaurid theropods exerted high bite forces, and large muscle attachments suggest that the tyrannosaurid neck was a concomitantly powerful component of the feeding apparatus. We examine accelerative and work-generating capacity (WGC) of neck muscles in adult Tyrannosaurus rex, using a 3-D vector-based method that incorporates aspects of muscle force generation, reconstruction of muscle morphology and moment arms, and rotational inertias of the head and neck. Under conservative assumptions, radial accelerations of the head by large superficial muscles (M. transversospinalis capitis, M. complexus, and M. longissimus capitis superficialis) enabled rapid gaze shifts and imparted high tangential velocities to food sufficient for inertial feeding. High WGC by these and deeper muscles under eccentric contraction indicate high efficacy for tearing flesh, especially with the head and neck in an extended posture. Sensitivity analyses suggest that assigned density of the antorbital region has substantial effects on calculated rotational inertia, and hence on the accuracy of results. However, even with high latitude for estimation errors, the results indicate that adult T. rex could strike rapidly at prey and engage in complexly modulated inertial feeding, as seen in extant archosaurs.

Type
Articles
Information
Paleobiology , Volume 33 , Issue 4 , Fall 2007 , pp. 610 - 638
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

Akima, H., Kuno, S., Takahashi, H., Fukunaga, T., and Katsuta, S. 2000. The use of magnetic resonance images to investigate the influence of recruitment on the relationship between torque and cross-sectional area in human muscle. European Journal of Applied Physiology 83: 475–480.Google Scholar
Bakker, R. T. 1998 (2000). Brontosaur killers: Late Jurassic allosaurids as sabre-tooth cat.analogues. Gaia 15: 145–158.Google Scholar
Bakker, R. T., Williams, M., and Currie, P. J. 1988. Nanotyrannus, a new genus of pygmy tyrannosaur, from the latest Cretaceous of Montana. Hunteria 1(5).Google Scholar
Bamman, M. W., Newcomer, B. R., Larson-Meyer, D., Weisner, R. L., and Hunter, G. R. 2000. Evaluation of the strength-size relation in vivo using various muscle size indices. Medicine and Science in Sports and Exercise 32: 1307–1313.Google Scholar
Brechue, W. F., and Abe, T. 2002. The role of FFM accumulation and skeletal muscle architecture in powerlifting performance. European Journal of Applied Physiology 86: 327–336.Google Scholar
Brochu, C. A. 2003. Osteology of Tyrannosaurus rex: insights from a nearly complete skeleton and high-resolution computed tomographic analysis of the cranium. Journal of Vertebrate Paleontology 24(Suppl. to No. 4): 1–138.CrossRefGoogle Scholar
Bryant, H. N., and Russell, A. P. 1992. The role of phylogenetic analysis in the inference of unpreserved attributes of extinct taxa. Philosophical Transactions of the Royal Society of London B 337: 405–418.Google Scholar
Carpenter, K., and Smith, M. B. 2001. Forelimb osteology and biomechanics of Tyrannosaurus : Pp. 90–116 in Tanke, D. H. and Carpenter, K., eds. Mesozoic vertebrate life. Indiana University Press, Bloomington.Google Scholar
Carrier, D. R., Walter, R. M., and Lee, D. V. 2001. Influence of rotational inertia on turning performance of theropod dinosaurs: clues from humans with increased rotational inertia. Journal of Experimental Biology 204: 391–3926.Google Scholar
Charig, A. J., and Milner, A. C. 1997. Baryonyx walkeri, a fish-eating dinosaur from the Wealden of Surrey. Bulletin of the British Museum of Natural History (Geology) 53: 11–70.Google Scholar
Cheng, E. J., and Scott, S. H. 2000. Morphometry of Macaca mulatta forelimb. I. Shoulder and elbow muscles and segment inertial parameters. Journal of Morphology 245: 206–224.3.0.CO;2-U>CrossRefGoogle ScholarPubMed
Cleuren, J., and De Vree, F. 2000. Feeding in crocodilians. Pp. 337–358 in Schwenk, K., ed. Feeding: form, function, and evolution in tetrapod vertebates. Academic Press, San Diego.Google Scholar
Cong, L.-Y., Hou, L.-H., Wu, X.-C., and Hou, J.-F. 1998. The gross anatomy of Alligator sinensis Fauvel. Science Press, Beijing.Google Scholar
Coombs, W. P. Jr. 1978. Theoretical aspects of cursorial adaptations in dinosaurs. Quarterly Review of Biology 53: 393–418.CrossRefGoogle Scholar
Delp, S. L., and Loan, J. P. 1995. A graphics-based software system to develop and analyze models of musculoskeletal structure. Computers in Biology and Medicine 25: 21–34.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
Frey, E. 1988. Anatomie des Korperstammes von Alligator mississippiensis Daudin. Stuttgarter Beitrage zur Naturkunde A 424: 1–106.Google Scholar
Fukunaga, T., Miyatani, M., Kouzaki, M., Kawakami, Y., and Kanehisa, H. 2001. Muscle volume is a major determinant of joint torque in humans. Acta Physiologica Scandinavica 172: 249–255.CrossRefGoogle Scholar
Gans, C. 1979. Momentarily excessive construction as the basis for protoadaptation. Evolution 331: 227–233.Google Scholar
Gillooly, J. S., Allen, A. P., and Charnov, E. L. 2006. Dinosaur fossils predict body temperatures. PLoS Biology 4: 1467–1469.Google Scholar
Gordon, J. E. 1978. Structures: or, why things don't fall down. Plenum, New York.Google Scholar
Guyton, A. C., and Hall, J. E. 1996. Textbook of medical physiology, 9th ed. Saunders, Philadelphia.Google Scholar
Halliday, D., Resnick, R., and Walker, J. 1994. Fundamentals of physics, 4th ed. Wiley, New York.Google Scholar
Henderson, D. M. 1999. A mathematical and computational analysis of the biomechanics of walking theropod dinosaurs. , University of Bristol, Bristol, U.K. Google Scholar
Henderson, D. M. 2002. The eyes have it: the sizes, shapes, and orientations of theropod orbits as indicators of cranium strength and bite force. Journal of Vertebrate Paleontology 22: 766–778.Google Scholar
Henderson, D. M., and Snively, E. 2003. Tyrannosaurus en pointe: allometry minimized rotational inertia of large carnivorous dinosaurs. Proceedings of the Royal Society of London B 271(Suppl. 3): S57–S60.Google Scholar
Hengst, R. A. 2004. Gravity and the T. rex backbone. Journal of Vertebrate Paleontology 24(Suppl. to No. 3): 69A–70A.Google Scholar
Hildebrand, M., and Goslow, G. 2001. Analysis of vertebrate structure, 5th ed. Wiley, New York.Google Scholar
Holtz, T. R. Jr. 1994. The phylogenetic position of the Tyrannosauridae: implications for theropod systematics. Journal of Paleontology 68: 1100–1117.Google Scholar
Holtz, T. R. Jr. 1995. The arctometatarsalian pes, an unusual structure of Cretaceous Theropoda (Dinosauria: Saurischia). Journal of Vertebrate Paleontology 14: 480–519.Google Scholar
Holtz, T. R. Jr. 2002. Theropod predation: evidence and ecomorphology. In Kelly, P. H., Koweleski, M., and Hansen, T. A., eds. Predator-prey interactions in the fossil record. Topics in Geobiology 17: 325–340. Kluwer Academic/Plenum, New York.Google Scholar
Holtz, T. R. Jr. 2004. Tyrannosauroidea. Pp. 111–136 in Weishampel, D. B., Dodson, P., and Osmólska, H., eds. The Dinosauria, 2d ed. University of California Press, Berkeley.CrossRefGoogle Scholar
Horstmann, T., Mayer, F., Maschmann, J., Niess, A., Roecker, K., and Dickhuth, H.-H. 2001. Metabolic reaction after concentric and eccentric endurance-exercise of the knee and ankle. Medicine and Science in Sports and Exercise 33: 791–795.Google Scholar
Hutchinson, J. R. 2004a. Biomechanical modeling and sensitivity analysis of bipedal running ability. I. Extant taxa. Journal of Morphology 262: 421–440.Google Scholar
Hutchinson, J. R. 2004b. Biomechanical modeling and sensitivity analysis of bipedal running ability. II. Extinct taxa. Journal of Morphology 262: 441–461.Google Scholar
Hutchinson, J. R., and Garcia, M. 2002. Tyrannosaurus was not a fast runner. Nature 415: 1018–1021.Google Scholar
Johnston, I. A. 1985. Sustained force development: specializations and variation among the vertebrates. Journal of Experimental Biology 115: 219–251.CrossRefGoogle ScholarPubMed
Juul-Kristensen, B., Bojsen-Møller, F., Finsen, L., Eriksson, J., Johansson, G., Ståhlberg, F., and Ekdahl, C. 2000. Muscle sizes and moment arms determined by magnetic resonance imaging. Cells, Tissues, Organs 167: 214–222.Google Scholar
Kawakami, Y., Abe, T., Kun, S. Y., and Fukunaga, T. 1995. Training-induced changes in muscle architecture and specific tension. European Journal of Applied Physiology 72: 37–43.Google Scholar
Keshner, E. A., Statler, K. D., and Delp, S. L. 1997. Kinematics of the freely moving head and neck of the cat. Experimental Brain Research 115: 257–266.Google Scholar
Lindstedt, S. L., LaStayo, P. C., and Reich, T. E. 2001. When active muscles lengthen: properties and consequences of eccentric contractions. News in Physiological Sciences 16: 256–261.Google ScholarPubMed
Meers, M. B. 2003. Maximum bite force and prey size of Tyrannosaurus rex and their relationship to the inference of feeding behavior. Historical Biology 16: 1–12.CrossRefGoogle Scholar
Molnar, R. E. 1973. The cranial morphology of Tyrannosaurus rex (Reptilia: Saurischia). . University of California, Los Angeles.Google Scholar
Molnar, R. E. 1998 (2000). Mechanical factors in the design of the cranium of Tyrannosaurus rex (Osborn 1905). Gaia 15: 193–218.Google Scholar
Motani, R. 2001. Estimating body mass from silhouettes: testing the assumption of elliptical body cross-sections. Paleobiology 27: 735–750.Google Scholar
Ng, B. H., Chou, S. M., Lim, B. H., and Chuong, A. 2004. Strain rate effect on the failure rate of tendons. Proceedings of the Institution of Mechanical Engineers, Part H, Journal of Engineering in Medicine 218: 203–206.CrossRefGoogle ScholarPubMed
Paul, G. S. 1988. Predatory dinosaurs of the world: a complete illustrated guide. Simon and Schuster, New York.Google Scholar
Pearsall, A. W., Hollis, J. M., Russell, G. V., and Scheer, Z. 2003. A biomechanical comparison of three lower extremity tendons for ligamentous reconstruction about the knee. Arthroscopy 19: 1091–1096.Google Scholar
Provenzano, P. P., Heisey, D., Hayashi, K., Lakes, R., and Vanderby, R. Jr. 2002. Subfailure damage in ligament: a structural and cellular evaluation. Journal of Applied Physiology 92: 362–371.Google Scholar
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. 2005. 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., May Smith, P., Thomason, J. J., and Upchurch, P. 2001. Cranial design and function in a large theropod dinosaur. Nature 409: 1033–1037.Google Scholar
Richmond, F. J. R. 1998. Elements of style in neuromuscular architecture. American Zoologist 38: 729–742.Google Scholar
Rosse, C., and Gaddum-Rosse, P. 1997. Hollinshead's textbook of anatomy, 5th ed. Lippincott-Raven, Philadelphia.Google Scholar
Schechtman, H., and Bader, D. L. 2002. Fatigue damage of human tendons. Journal of Biomechanics 35: 347–353.Google Scholar
Seidel, R. 1978. The somatic musculature of the cervical and occipital regions of Alligator mississippiensis. . City University of New York, New York.Google Scholar
Selbie, W. S., Thomson, D. B., and Richmond, F. J. R. 1993. Sagittal-plane mobility of the cat cervical spine. Journal of Biomechanics 26: 917–927.CrossRefGoogle ScholarPubMed
Senter, P., and Robins, J. H. 2005. Range of motion in the forelimb of the theropod dinosaur Acrocanthosaurus atokensis, and implications for predatory behavior. Journal of Zoology 266: 307–318.Google Scholar
Snively, E. 2006. Neck musculoskeletal function in the Tyrannosauridae (Theropoda, Coelurosauria): implications for feeding dynamics. , University of Calgary, Calgary, Alberta.Google Scholar
Snively, E., and Russell, A. P. 2002. The tyrannosaurid metatarsus: bone strain and inferred ligament function. Senckenbergiana Lethaea 82: 35–42.Google Scholar
Snively, E., and Russell, A. P. 2003. A kinematic model of tyrannosaurid (Dinosauria, Theropoda) arctometatarsus function. Journal of Morphology 255: 215–227.Google Scholar
Snively, E., Russell, A. P., and Powell, G. L. 2004. Evolutionary morphology of the coelurosaurian arctometatarsus: descriptive, morphometric, and phylogenetic approaches. Zoological Journal of the Linnean Society 142: 525–553.Google Scholar
Snively, E., Henderson, D. M., and Phillips, D. S. 2006. Fused and vaulted nasals of tyrannosaurid dinosaurs: implications for cranial strength and feeding mechanics. Acta Palaeontologica Polonica 51: 435–454.Google Scholar
Stevens, K. A., and Parrish, M. J. 1999. Neck posture in two Jurassic sauropod dinosaurs. Science 284: 798–800.Google Scholar
Syme, D. A. 2006. Functional properties of skeletal muscle. Fish Biomechanics 23: 179–240.Google Scholar
Therrien, F., Henderson, D. M., and Ruff, C. B. 2005. Bite me: biomechanical models of theropod mandibles and implications for feeding behavior. Pp. 179–237 in Carpenter, K., ed. The carnivorous dinosaurs. Indiana University Press, Bloomington.Google Scholar
Thorpe, S. K. S., Crompton, R. H., Günther, M. M., Ker, R. F., and Alexander, R. M. 1999. Dimensions and moment arms of the hind- and forelimb muscles of common chimpanzees. American Journal of Physical Anthropology 110: 179–199.Google Scholar
Tsuihiji, T. 2005. Homologies of the transversospinalis muscles in the anterior presacral region of Sauria (crown Diapsida). Journal of Morphology 263: 151–178.Google Scholar
Vasavada, A. N., Li, S., and Delp, S. L. 1998. Influence of muscle morphometry and moment arms on the moment-generating capacity of human neck muscles. Spine 23: 412–422.Google Scholar
Wedel, M. J. 2004. Skeletal pneumaticity in saurischian dinosaurs and its implications for mass estimates. Journal of Vertebrate Paleontology 24(Suppl. to No. 3): 127A.Google Scholar
Wegweiser, M. B., Breithaupt, B., and Chapman, R. 2004. Attack behavior of tyrannosaurid dinosaur(s): Cretaceous crime scenes, really old evidence, and “smoking guns.” Journal of Vertebrate Paleontology 24(Suppl. to No. 3): 127A.Google Scholar
Witmer, L. M. 1995. The extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. Pp. 19–33 in Thomason, J. J., ed. Functional morphology in vertebrate paleontology. Cambridge University Press, Cambridge.Google Scholar
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. Society of Vertebrate Paleontology Memoir 3. Journal of Vertebrate Paleontology 17 (Suppl. to No. 1).Google Scholar
Wroe, S., McHenry, C., and Thomason, J. 2005. Bite club: comparative bite force in big biting mammals and the prediction of predatory behavior in fossil taxa. Proceedings of the Royal Society of London B 272: 619–625.Google Scholar
Yamaguchi, G. T. 2001. Dynamic modeling of the musculoskeletal system: a vectorized approach for biomechanical analysis in three dimensions. Kluwer Academic, Boston.Google Scholar
Supplementary material: File

Snively and Russell supplementary material

Supplementary Tables S1-S12

Download Snively and Russell supplementary material(File)
File 628.7 KB