Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-19T06:01:44.777Z Has data issue: false hasContentIssue false
  • English
  • Français

A computational analysis of locomotor anatomy and body mass evolution in Allosauroidea (Dinosauria: Theropoda)

Published online by Cambridge University Press:  08 February 2016

Karl T. Bates ,
Roger B. J. Benson  and
Peter L. Falkingham
Karl T. Bates
Affiliation:
Department of Musculoskeletal Biology, Institute of Aging and Chronic Disease, University of Liverpool, Sherrington Buildings, Ashton Street, Liverpool, L69 3GE, United Kingdom. E-mail: [email protected]
Roger B. J. Benson
Affiliation:
Department of Earth Sciences, University of Cambridge, Downing Street, Cambridge, CB2 3EQ, United Kingdom. E-mail: [email protected]
Peter L. Falkingham
Affiliation:
School of Earth, Atmospheric and Environmental Science, University of Manchester, Williamson Building, Oxford Road, Manchester, M13 9PL, United Kingdom. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

We investigate whether musculoskeletal anatomy and three-dimensional (3-D) body proportions were modified during the evolution of large (>6000 kg) body size in Allosauroidea (Dinosauria: Theropoda). Three adaptations for maintaining locomotor performance at large body size, related to muscle leverage, mass, and body proportions, are tested and all are unsupported in this analysis. Predictions from 3-D musculoskeletal models of medium-sized (Allosaurus) and large-bodied (Acrocanthosaurus) allosauroids suggest that muscle leverage scaled close to isometry, well below the positive allometry required to compensate for declining muscle cross-sectional area with increasing body size. Regression analyses on a larger allosauroid data set finds slight positive allometry in the moment arms of major hip extensors, but isometry is included within confidence limits. Contrary to other recent studies of large-bodied theropod clades, we found no compelling evidence for significant positive allometry in muscle mass between exemplar medium- and large-bodied allosauroids. Indeed, despite the uncertainty in quantitative soft tissue reconstruction, we find strong evidence for negative allometry in the caudofemoralis longus muscle, the single largest hip extensor in non-avian theropods. Finally, we found significant inter-study variability in center-of-mass predictions for allosauroids, but overall observe that consistently proportioned soft tissue reconstructions produced similar predictions across the group, providing no support for a caudal shift in the center of mass in larger taxa that might otherwise reduce demands on hip extensor muscles during stance. Our data set provides further quantitative support to studies that argue for a significant decline in locomotor performance with increasing body size in non-avian theropods. However, although key pelvic limb synapomorphies of derived allosauroids (e.g., dorsomedially inclined femoral head) evolved at intermediate body sizes, they may nonetheless have improved mass support.

Type
Articles
Information
Paleobiology , Volume 38 , Issue 3 , Summer 2012 , pp. 486 - 507
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

Abourachid, A., and Renous, S. 2000. Bipedal locomotion in ratites (Paleognatiform) [sic]: examples of cursorial birds. Ibis 142:538–549.CrossRefGoogle Scholar
Alexander, R. M. 1977. Mechanics and scaling of terrestrial locomotion. Pp. 93–110inPedley, T. J., ed. Scale effects in animal locomotion. Academic Press, New York.Google Scholar
Alexander, R. M., and Jayes, A. S. 1983. A dynamic similarity hypothesis for the gaits of quadrupedal mammals. Journal of Zoology 201:135–152.CrossRefGoogle Scholar
Alexander, R. M., Jayes, A. S., Maloiy, G. M. O., and Wathuta, E. M. 1981. Allometry of the leg muscles of mammals. Journal of Zoology 194:539–552.CrossRefGoogle Scholar
Allen, V., Paxton, H., and Hutchinson, J. R. 2009. Variation in center of mass estimates for extant sauropsids and its importance for reconstructing inertial properties of extinct archosaurs. Anatomical Record 292:1442–1461.CrossRefGoogle ScholarPubMed
An, K. N., Takahashi, K., Harrigan, T. P., and Chao, E. Y. 1984. Determination of muscle orientations and moment arms. Journal of Biomechanical Engineering 106:280–283.CrossRefGoogle ScholarPubMed
Azuma, Y., and Currie, P. J. 2000. A new carnosaur (Dinosauria: Theropoda) from the Lower Cretaceous of Japan. Canadian Journal of Earth Sciences 37:1735–1753.CrossRefGoogle Scholar
Bakker, R. T. 1986. Dinosaur heresies. William Morrow, New York.Google Scholar
Bates, K. T., Manning, P. L., Hodgetts, D., and Sellers, W. I. 2009a. Estimating mass properties of dinosaurs using laser imaging and computer modelling. PLoS ONE 4 (2):e4532doi:10.1371.CrossRefGoogle ScholarPubMed
Bates, K. T., Falkingham, P. L., Breithaupt, B. H., Hodgetts, D., Sellers, W. I., and Manning, P. L. 2009b. How big was ‘Big Al’? Quantifying the effect of soft tissue and osteological unknowns on mass predictions for Allosaurus (Dinosauria: Theropoda). Palaeontological Electronica 12 (3):14A. http://palaeo-electronica.org/2009_3/186/index.html.Google Scholar
Bates, K. T., Manning, P. L., Margetts, L., and Sellers, W. I. 2010. Sensitivity analysis in evolutionary robotic simulations of bipedal dinosaur running. Journal of Vertebrate Paleontology 30:458–466.CrossRefGoogle Scholar
Benson, R. G. J., Carrano, M. T., and Brusatte, S. L. 2010. A new clade of archaic large-bodied predatory dinosaurs (Theropoda: Allosauroidea) that survived to the latest Mesozoic. Naturwissenschaften 97:71–78.CrossRefGoogle Scholar
Biewener, A. A. 1989. Scaling body support in mammals: limb design and muscle mechanics. Science 245:45–48.CrossRefGoogle Scholar
Biewener, A. A. 1990. Biomechanics of mammalian terrestrial locomotion. Science 250:1097–1103.CrossRefGoogle ScholarPubMed
Bonnan, M. F. 2004. Morphometric analysis of humerus and femur shape in Morrison sauropods: implications for functional morphology and paleobiology. Paleobiology 30:444–470.2.0.CO;2>CrossRefGoogle Scholar
Bonnan, M. F., Sandrik, J. L., Nishiwaki, T., Wilhite, D. R., Elsey, R. M., and Vittore, C. 2010. Calcified cartilage shape in archosaur long bones reflects overlying joint shape in stress-bearing elements: Implications for nonavian dinosaur locomotion. Anatomical Record 293:2044–2055.CrossRefGoogle ScholarPubMed
Brusatte, S. L., and Sereno, P. C. 2008. Phylogeny of Allosauroidea (Dinosauria: Theropoda): comparative analysis and resolution. Journal of Systematic Palaeontology 6:155–182.CrossRefGoogle Scholar
Brusatte, S. L., Benson, R. B. J., and Hutt, S. 2008. The osteology of Neovenator salerii (Dinosauria: Theropoda) from the Wealden Group (Barremian) of the Isle of Wight. Monograph of the Palaeontological Society 162 (631):1–166.Google Scholar
Carrano, M. T. 1998. Locomotion in non-avian dinosaurs: integrating data from hind limb kinematics, in vivo strains, and bone morphology. Paleobiology 24:450–469.CrossRefGoogle Scholar
Carrano, M. T. 2001. Implications of limb bone scaling, curvature and eccentricity in mammals and non-avian dinosaurs. Journal of Zoology, London 254:41–55.CrossRefGoogle Scholar
Carrano, M. T., and Hutchinson, J. R. 2002. Pelvic and hind limb musculature of Tyrannosaurus rex (Dinosauria: Theropoda). Journal of Morphology 253:207–228.CrossRefGoogle ScholarPubMed
Christiansen, P. 2002. Locomotion in terrestrial mammals: the influence of body mass, limb length and bone proportions on speed. Zoological Journal of the Linnean Society 136:685–714.CrossRefGoogle Scholar
Christiansen, P., and Bonde, N. 2002. Limb proportions and avian terrestrial locomotion. Journal für Ornithologie 143:356–371.CrossRefGoogle Scholar
Coria, R. A., and Salgado, L. 1995. A new giant carnivorous dinosaur from the Cretaceous of Patagonia. Nature 377:224–226.CrossRefGoogle Scholar
Currie, P. J., and Zhao, X. J. 1993. A new carnosaur (Dinosauria: Theropoda) form the Jurassic of Xinjiang, People's Republic of China. Canadian Journal of Earth Sciences 30:2037–2081.CrossRefGoogle Scholar
Gatesy, S. M. 1990. Caudofemoralis musculature and the evolution of theropod locomotion. Paleobiology 16:170–186.CrossRefGoogle Scholar
Gatesy, S. M. 1995. Functional evolution of the hind limb and tail from basal theropods to birds. Pp. 219–234inThomason, J. J., ed. Functional morphology in vertebrate palaeontology. Cambridge University Press, Cambridge.Google Scholar
Gatesy, S. M., Baeker, M., and Hutchinson, J. R. 2009. Constraint-based exclusion of limb poses for reconstructing theropod dinosaur locomotion. Journal of Vertebrate Paleontology 29:535–544.CrossRefGoogle Scholar
Günther, M., and Blickhan, R. 2002. Joint stiffness of the ankle and the knee in running. Journal of Biomechanics 35:1459–1474.CrossRefGoogle ScholarPubMed
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/issue1_01.htm.Google Scholar
Henderson, D., and Snively, E. 2003. Tyrannosaurus en pointe: allometry minimized rotational inertia of large carnivorous dinosaurs. Proceedings of the Royal Society of London B 271 (Biology Letters Suppl. 3):S57–S60.Google Scholar
Hocknull, S. A., White, M. A., Tischler, T. R., Cook, A. G., Calleja, N. D., Sloan, T., and Elliott, D. A. 2009. New mid-Cretaceous (latest Albian) dinosaurs from Winton, Queensland, Australia. PLoS ONE 4 (7):1–51.CrossRefGoogle ScholarPubMed
Hutchinson, J. R. 2001a. The evolution of pelvic osteology and soft tissues on the line to extant birds (Neornithes). Zoological Journal of the Linnean Society 131:123–168.CrossRefGoogle Scholar
Hutchinson, J. R. 2001b. The evolution of femoral osteology and soft tissues on the line to extant birds (Neornithes). Zoological Journal of the Linnean Society 131:169–197.CrossRefGoogle Scholar
Hutchinson, J. R. 2004a. Biomechanical modeling and sensitivity analysis of bipedal running. I. Extant taxa. Journal of Morphology 262:421–440.CrossRefGoogle ScholarPubMed
Hutchinson, J. R. 2004b. Biomechanical modeling and sensitivity analysis of bipedal running ability. II. Extinct taxa. Journal of Morphology 262:441–461.CrossRefGoogle ScholarPubMed
Hutchinson, J. R., and Allen, V. 2008. The evolutionary continuum of limb function from early theropods to birds. Naturwissenschaften 96:423–448.CrossRefGoogle ScholarPubMed
Hutchinson, J. R., and Gatesy, S. M. 2000. Adductors, abductors, and the evolution of archosaur locomotion. Paleobiology 26:734–751.2.0.CO;2>CrossRefGoogle Scholar
Hutchinson, J. R., Anderson, F. C., Blemker, S. S., and Delp, S. L. 2005. Analysis of hind limb muscle moment arms in Tyrannosaurus rex using a three-dimensional musculoskeletal computer model: implications for stance, gait, and speed. Paleobiology 31:676–701.CrossRefGoogle Scholar
Hutchinson, J. R., Ng-Thow-Hing, V., and Anderson, F. C. 2007. A 3D interactive method for estimating body segmental parameters in animals: application to the turning and running performance of Tyrannosaurus rex. Journal of Theoretical Biology 246:660–680.CrossRefGoogle Scholar
Hutchinson, J. R., Miller, C. E., Fritsch, G., and Hildebrandt, T. 2008. The anatomical foundation for multidisciplinary studies of animal limb function: examples from dinosaur and elephant limb imaging studies. Pp. 23–38inFrey, R. and Endo, H., eds. Anatomical imaging techniques: towards a new morphology. Springer, Berlin.CrossRefGoogle Scholar
Hutchinson, J. R., Bates, K. T., and Allen, V. A. 2011a. Tyrannosaurus rex redux: Tyrannosaurus tail portrayals. Anatomical Record 294:756–758.CrossRefGoogle ScholarPubMed
Hutchinson, J. R., Bates, K. T., Molnar, J., Allen, V., and Makovicky, P. J. 2011b. A computational and comparative analysis of limb and body proportions in Tyrannosaurus rex with implications for locomotion, physiology and growth. PLoS ONE 6 (10):e26037. doi:10.1371/journal.pone.0026037.CrossRefGoogle Scholar
Main, R. P., and Biewener, A. A. 2007. Skeletal strain patterns and growth in the emu hindlimb during ontogeny. Journal of Experimental Biology 210:2676–2690.CrossRefGoogle Scholar
Marx, J. O., Olsson, C. M., and Larsson, L. 2006. Scaling of skeletal muscle shortening velocity in mammals representing a 100,000-fold difference in body size. European Journal of Physiology 452:222–230.CrossRefGoogle ScholarPubMed
McMahon, T. A. 1975. Allometry and biomechanics: limb bones in adult ungulates. American Naturalist 109:547–563.CrossRefGoogle Scholar
Medler, S. 2002. Comparative trends in shortening velocity and force production in skeletal muscle. American Journal of Regulatory and Integrative Comparative Physiology 283:R368–R378.CrossRefGoogle Scholar
Osmolska, H. 1990. Theropoda. Pp. 148–319inWeishampel, D. B., Dodson, P., and Osmólska, H., eds. The Dinosauria. University of California Press, Berkeley.Google Scholar
Paul, G. S. 1988. Predatory dinosaurs of the world. Simon and Schuster, New York.Google Scholar
Paul, G. S. 2008. The extreme lifestyles and habits of the gigantic tyrannosaurid superpredators of the Late Cretaceous of North America and Asia. Pp. 307–354inLarson, P. and Carpenter, K., eds. Tyrannosaurus rex: the tyrant king. Indiana University Press, Bloomington.Google Scholar
Persons, W. S., and Currie, P. J. 2011. The tail of Tyrannosaurus: reassessing the size and locomotive importance of the M. caudofemoralis in non-avian theropods. Anatomical Record 294:119–131.CrossRefGoogle Scholar
Roberts, T. J. 2001. Muscle force and stress during running in dogs and wild turkeys. Bulletin of the Museum of Comparative Zoology 156:283–295.Google Scholar
Roberts, T. J., Chen, M. S., and Taylor, C. R. 1998. Energetics of bipedal running. II. Limb design and running mechanics. Journal of Experimental Biology 201:2753–2762.CrossRefGoogle ScholarPubMed
Rubenson, J., Heliams, D. B., Lloyd, D. G., and Fournier, P. A. 2003. Gait selection in the ostrich: mechanical and metabolic characteristics of walking and running with and without an aerial phase. Proceedings of the Royal Society of London B 271:1091–1099.CrossRefGoogle Scholar
Sellers, W. I., and Manning, P. L. 2007. Estimating dinosaur maximum running speeds using evolutionary robotics. Proceedings of the Royal Society of London B 274:2711–2716.Google ScholarPubMed
Sereno, P. C. 1999. The evolution of the dinosaurs. Science 284:2137–2147.CrossRefGoogle ScholarPubMed
Therrien, F., and Henderson, D. M. 2007. My theropod is bigger than yours…or not: estimating body size from skull length in theropods. Journal of Vertebrate Paleontology 27:108–115.CrossRefGoogle Scholar