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Locomotion in non-avian dinosaurs: integrating data from hindlimb kinematics, in vivo strains, and bone morphology

Published online by Cambridge University Press:  08 February 2016

Matthew T. Carrano
Matthew T. Carrano*
Affiliation:
Department of Organismal Biology and Anatomy, University of Chicago, Chicago, Illinois 60637
*
Present address: Department of Anatomical Sciences, Health Sciences Center T-8, State University of New York at Stony Brook, Stony Brook, New York 11794. E-mail: [email protected]
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Abstract

Analyses of non-avian dinosaur locomotion have been hampered by the lack of an appropriate locomotor analog among extant taxa. Birds, though members of the clade Dinosauria, have undergone significant modifications in hindlimb osteology and musculature. These changes have resulted in a uniquely developed system of limb kinematics (involving a more horizontal femoral posture and knee-dominated limb motion), which precludes the direct use of extant birds as models for non-avian dinosaur locomotion. Analyses of locomotor data from extant birds and mammals suggest a causal link between general hindlimb kinematics, bone strains, and limb bone morphology among these taxa. A model is proposed that relates the amount of torsional loading in femora to bone orientation, such that torsion is maximal in horizontal femora and minimal in vertical femora. Since bone safety factors are lower for torsional shear strains than for longitudinal axial strains, an increase in torsion can potentially affect bone morphology dramatically over evolutionary time. Interpreting the nearly identical limb bone dimensions and limb element proportions of non-avian dinosaurs and mammals in the light of this relationship supports the prediction of similar vertical femoral postures and hip-driven limb kinematics in these two groups.

This information can be used to interpret patterns of locomotor evolution within Dinosauria. The evolution of quadrupedalism with large body size and the acquisition of cursorial or graviportal limb morphologies occurred repeatedly but did not affect the underlying uniformity of dinosaur locomotor morphology. Only derived coelurosaurian theropods (paravians) developed significant modifications of the basic dinosaurian patterns of limb use. Changes in theropod hindlimb kinematics and posture apparently began shortly prior to the origin of flight, but did not acquire a characteristically modern avian aspect until after the later acquisition of derived flight characteristics.

Type
Articles
Information
Paleobiology , Volume 24 , Issue 4 , Fall 1998 , pp. 450 - 469
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Alexander, R. M. 1981. Factors of safety in the structure of animals. Science Progress 67:119–140.Google ScholarPubMed
Alexander, R. M., Maloiy, G. M. O., Njau, R., and Jayes, A. S. 1979. Mechanics of running in the ostrich (Struthio camelus). Journal of Zoology 187:169–178.CrossRefGoogle Scholar
Biewener, A. A. 1983. Allometry of quadrupedal locomotion: the scaling of duty factor, bone curvature and limb orientation to body size. Journal of Experimental Biology 105:147–171.CrossRefGoogle ScholarPubMed
Biewener, A. A. 1989. Scaling body support in mammals: limb posture and muscle mechanics. Science 245:45–48.CrossRefGoogle ScholarPubMed
Biewener, A. A. 1990. Biomechanics of mammalian terrestrial locomotion. Science 250:1097–1103.CrossRefGoogle ScholarPubMed
Biewener, A. A. 1992. In vivo measurement of bone strain and tendon force. Pp. 123–147in Biewener, A. A., ed. Biomechanics: structures and systems. IRL at Oxford University Press, Oxford.CrossRefGoogle Scholar
Biewener, A. A. 1993. Safety factors in bone strength. Calcified Tissue International 53:S68–S74.CrossRefGoogle ScholarPubMed
Biewener, A. A., and Bertram, J. E. A. 1993a. Mechanical loading and bone growth in vivo. Pp. 1–36in Hall, B. K., ed. Bone, Vol. 7 (Bone Growth—B). CRC, Boca Raton, Fla.Google ScholarPubMed
Biewener, A. A. 1993b. Skeletal strain pattern in relation to exercise training during growth. Journal of Experimental Biology 185:51–69.CrossRefGoogle ScholarPubMed
Biewener, A. A., and Dial, K. P. 1995. In vivo strain in the humerus of pigeons (Columba livia) during flight. Journal of Morphology 225:61–75.CrossRefGoogle Scholar
Biewener, A. A., and Taylor, R. C. 1986. Bone strain: a determinant of gait and speed? Journal of Experimental Biology 123:383–400.CrossRefGoogle Scholar
Biewener, A. A., Thomason, J. J., and Lanyon, L. E. 1983. Mechanics of locomotion and jumping in the forelimb of the horse (Equus): in vivo stress developed in the radius and metacarpus. Journal of Zoology 214:547–565.CrossRefGoogle Scholar
Brinkman, D. 1980. The hind limb step cycle of Caiman sclerops and the mechanics of the crocodile tarsus and metatarsus. Canadian Journal of Zoology 58:2187–2200.CrossRefGoogle Scholar
Carrano, M. T. 1998a. The evolution of dinosaur locomotion: functional morphology, biomechanics, and modern analogs. . University of Chicago, Chicago.Google Scholar
Carrano, M. T. 1998b. What, if anything, is a cursor? Categories versus continua for determining locomotor performance in dinosaurs and mammals. Journal of Zoology (in press).CrossRefGoogle Scholar
Chiappe, L. M., Norell, M. A., and Clark, J. M. 1996. Phylogenetic position of Mononykus (Aves: Alvarezsauridae) from the Late Cretaceous of the Gobi Desert. Memoirs of the Queensland Museum 39:557–582.Google Scholar
Coombs, W. P. Jr. 1978. Theoretical aspects of cursorial adaptations in dinosaurs. Quarterly Review of Biology 53:393–418.CrossRefGoogle Scholar
Cowin, S. C. 1987. Bone remodeling of diaphyseal surfaces by torsional loads: theoretical predictions. Journal of Biomechanics 20:1111–1120.CrossRefGoogle ScholarPubMed
Crompton, A. W., Robinson, E., and Shapiro, M. D. 1996. Bone growth and remodeling in the avian hind limb. Journal of Vertebrate Paleontology 16:64A.Google Scholar
de Queiroz, K., and Gauthier, J. 1990. Phyogeny as a central principle in taxonomy: phylogenetic definitions of taxon names. Systematic Zoology 39:307–322.CrossRefGoogle Scholar
de Queiroz, K. 1992. Phylogenetic taxonomy. Annual Review of Ecology and Systematics 23:449–480.CrossRefGoogle Scholar
Foote, M. 1992. Rarefaction analysis of morphological and taxonomic diversity. Paleobiology 18:1–16.CrossRefGoogle Scholar
Forster, C. A., Sampson, S. D., Chiappe, L. M., and Krause, D. W. 1998. The theropod ancestry of birds: new evidence from the Late Cretaceous of Madagascar. Science 279:1915–1918.CrossRefGoogle ScholarPubMed
Galton, P. M. 1990. Basal Sauropodomorpha-Prosauropoda. Pp. 320–344in Weishampel, D. B., Dodson, P., and Osmólska, H., eds. The Dinosauria. University of California Press, Berkeley and Los Angeles.Google Scholar
Garland, T. Jr. 1983. The relation between maximal running speed and body mass in terrestrial mammals. Journal of Zoology 199:157–170.CrossRefGoogle Scholar
Garland, T. Jr., and Janis, C. M. 1993. Does metatarsal/femur ratio predict running speed in cursorial mammals? Journal of Zoology 229:133–151.CrossRefGoogle Scholar
Gatesy, S. M. 1990. Caudofemoral musculature and the evolution of theropod locomotion. Paleobiology 16:170–186.CrossRefGoogle Scholar
Gatesy, S. M. 1991a. Hind limb scaling in birds and other theropods: implications for terrestrial locomotion. Journal of Morphology 209:83–96.CrossRefGoogle ScholarPubMed
Gatesy, S. M. 1991b. Hind limb movements of the American alligator (Alligator mississippiensis) and postural grades. Journal of Zoology 224:577–588.CrossRefGoogle Scholar
Gatesy, S. M. 1995. Functional evolution of the hindlimb and tail from basal theropods to birds. Pp 219–234in Thomason, J. J. and Weishampel, D. B., eds. Functional morphology in vertebrate paleontology. Cambridge University Press, Cambridge.Google Scholar
Gatesy, S. M., and Biewener, A. A. 1991. Bipedal locomotion: effects of speed, size and limb posture in birds and humans. Journal of Zoology 224:127–147.CrossRefGoogle Scholar
Gatesy, S. M., and Dial, K. P. 1996a. Locomotor modules and the evolution of avian flight. Evolution 50:331–340.CrossRefGoogle ScholarPubMed
Gatesy, S. M. 1996b. From frond to fan: Archaeopteryx and the evolution of short-tailed birds. Evolution 50:2037–2048.Google ScholarPubMed
Gatesy, S. M., and Middleton, K. H. 1997. Bipedalism, flight, and the evolution of theropod locomotor diversity. Journal of Vertebrate Paleontology 17:308–329.CrossRefGoogle Scholar
Gauthier, J. 1986. Saurischian monophyly and the origin of birds. In Padian, K., ed. The origin of birds and the evolution of flight. Memoirs of the California Academy of Sciences, San Francisco 8:1–47.Google Scholar
Gauthier, J., and Padian, K. 1985. Phylogenetic, functional, and aerodynamic analyses of the origin of birds and their flight. Pp. 185–197in Hecht, M. K., Ostrom, J. H., Viohl, G., and Wellnhofer, P., eds. The beginnings of birds. Proceedings of the International Archaeopteryx Conference, Eichstätt.Google Scholar
Gregory, W. K. 1912. Notes on the principles of quadrupedal locomotion and on the mechanism of the limbs in hoofed animals. Annals of the New York Academy of Sciences 22:287–294.CrossRefGoogle Scholar
Heglund, N. C., and Taylor, C. R. 1988. Speed, stride frequency and energy cost per stride: how do they change with body size and gait? Journal of Experimental Biology 138:301–318.CrossRefGoogle ScholarPubMed
Heglund, N. C., Fedak, M. A., Taylor, C. R., and Cavangna, G. A. 1982. Energetics and mechanics of terrestrial locomotion. IV. Total mechanical energy changes as a function of speed and body size in birds and mammals. Journal of Experimental Biology 97:57–66.CrossRefGoogle ScholarPubMed
Heinrich, R. E., Ruff, C. B., and Weishampel, D. B. 1993. Femoral ontogeny and locomotor biomechanics of Dryosaurus lettowvorbecki (Dinosauria, Iguanodontia). Zoological Journal of the Linnean Society 108:179–196.CrossRefGoogle Scholar
Holtz, T. R. Jr. 1994a. The arctometatarsalian pes, an unusual structure of the metatarsus of Cretaceous Theropoda (Dinosauria: Saurischia). Journal of Vertebrate Paleontology 14:480–519.CrossRefGoogle Scholar
Holtz, T. R. Jr. 1994b. The phylogenetic position of the Tyrannosauridae: implications for theropod systematics. Journal of Paleontology 68:1100–1117.CrossRefGoogle Scholar
Janis, C. M., and Wilhelm, P. B. 1993. Were there mammalian pursuit predators in the Tertiary? Dances with wolf avatars. Journal of Mammalian Evolution 1:103–125.CrossRefGoogle Scholar
Jenkins, F. A. Jr. 1971. Limb posture and locomotion in the Virginia opossum (Didelphis marsupialis) and in other non-cursorial mammals. Journal of Zoology 165:303–315.CrossRefGoogle Scholar
Jenkins, F. A. Jr., and Camazine, S. M. 1977. Hip structure and locomotion in ambulatory and cursorial carnivores. Journal of Zoology 181:351–370.CrossRefGoogle Scholar
Ji, Q., Currie, P. J., Norell, M. A., and Ji, S. 1998. Two feathered dinosaurs from northeastern China. Nature 393:753–762.Google Scholar
Keller, T. S., and Spengler, D. M. 1989. Regulation of bone stress and strain in the immature rat femur. Journal of Biomechanics 22:1115–1127.CrossRefGoogle ScholarPubMed
Kram, R., and Taylor, C. R. 1990. Energetics of running: a new perspective. Nature 346:265–267.CrossRefGoogle ScholarPubMed
LaBarbera, M. 1989. Analyzing body size as a factor in ecology and evolution. Annual Review of Ecology and Systematics 20:97–117.CrossRefGoogle Scholar
Lanyon, L. E. 1981. Locomotor loading and functional adaptation in limb bones. Symposium of the Zoological Society of London 48:305–329.Google Scholar
Lanyon, L. E. 1987. Functional strain in bone tissue as an objective, and controlling stimulus for adaptive bone remodelling. Journal of Biomechanics 20:1083–1093.CrossRefGoogle ScholarPubMed
Lauder, G. V. 1990. Functional morphology and systematics: studying functional patterns in an historical context. Annual Review of Ecology and Systematics 21:317–340.CrossRefGoogle Scholar
Livezey, B. C. 1997. A phylogenetic analysis of basal Anseriformes, the fossil Presbyornis, and the interordinal relationships of waterfowl. Zoological Journal of the Linnean Society 121:361–428.Google Scholar
Maddison, W. P., Donoghue, M. J., and Maddison, D. R. 1984. Outgroup analysis and parsimony. Systematic Zoology 33:83–103.CrossRefGoogle Scholar
Maynard Smith, J., and Savage, R. J. G. 1955. Some locomotory adaptations in mammals. Journal of the Linnean Society of London 42:603–622.CrossRefGoogle Scholar
Novas, F. E., and Puerta, P. F. 1997. New evidence concerning avian origins from the Late Cretaceous of Patagonia. Nature 387:390–392.CrossRefGoogle Scholar
Ostrom, J. H. 1969. Osteology of Deinonychus antirrhopus, an unusual theropod from the Lower Cretaceous of Montana. Peabody Museum Bulletin 30:1–165.Google Scholar
Ostrom, J. H. 1976. Some hypothetical anatomical stages in the evolution of avian flight. Smithsonian Contributions to Paleobiology 27:1–21.Google Scholar
Padian, K., and Chaippe, L. M. 1998. The origin and early evolution of birds. Biological Reviews 73:1–42.CrossRefGoogle Scholar
Padian, K., and Olsen, P. E. 1989. Ratite footprints and the stance and gait of Mesozoic theropods. Pp. 231–341in Gillette, D. D. and Lockley, M. G., eds. Dinosaur tracks and traces. Cambridge University Press, Cambridge.Google Scholar
Perle, A. 1985. Comparative myology of the pelvic-femoral region in the bipedal dinosaurs. Paleontological Journal 1985:105–109.Google Scholar
Raup, D. M. 1975. Taxonomic diversity estimation using rarefaction. Paleobiology 1:333–342.CrossRefGoogle Scholar
Romer, A. S. 1923a. The pelvic musculature of saurischian dinosaurs. Bulletin of the American Museum of Natural History 48:605–617.Google Scholar
Romer, A. S. 1923b. Crocodilian pelvic muscles and their avian and reptilian homologues. Bulletin of the American Museum of Natural History 48:533–552.Google Scholar
Rubin, C. T., and Lanyon, L. E. 1982. Limb mechanics as a function of speed and gait: a study of functional strains in the radius and tibia of horse and dog. Journal of Experimental Biology 101:187–211.CrossRefGoogle Scholar
Russell, D. A. 1972. Ostrich dinosaurs from the Late Cretaceous of western Canada. Canadian Journal of Earth Sciences 9:375–402.CrossRefGoogle Scholar
Russell, D. A., and Dong, Z. 1993. A nearly complete skeleton of a new troodontid dinosaur from the Early Cretaceous of the Ordos Basin, Inner Mongolia, People's Republic of China. Canadian Journal of Earth Sciences 30:2163–2173.CrossRefGoogle Scholar
Sereno, P. C. 1997. The origin and evolution of dinosaurs. Annual Reviews of Earth and Planetary Sciences 25:435–489.CrossRefGoogle Scholar
Sereno, P. C., Wilson, J. A., Larsson, H. C. E., Dutheil, D. B., and Sues, H.-D. 1994. Early Cretaceous dinosaurs from the Sahara. Science 266:267–271.CrossRefGoogle ScholarPubMed
Sokal, R. R., and Rohlf, F. J. 1995. Biometry, 3d ed.W. H. Freeman, New York.Google Scholar
Steudel, K. 1990a. The work and energetic cost of locomotion. I. The effects of limb mass distribution in quadrupeds. Journal of Experimental Biology 154:273–285.CrossRefGoogle ScholarPubMed
Steudel, K. 1990b. The work and energetic cost of locomotion. II. Partitioning the cost of internal and external work within a species. Journal of Experimental Biology 154:287–303.CrossRefGoogle ScholarPubMed
Steudel, K., and Beattie, J. 1993. Scaling of cursoriality in mammals. Journal of Morphology 217:55–63.CrossRefGoogle ScholarPubMed
Tarsitano, S. 1983. Stance and gait in theropod dinosaurs. Acta Palaeontologica Polonica 28:251–264.Google Scholar
Taylor, C. R. 1985. Force development during sustained locomotion: a determinant of gait, speed and metabolic power. Journal of Experimental Biology 115:252–262.CrossRefGoogle ScholarPubMed
Taylor, C. R., Heglund, N. C., and Maloiy, G. M. O. 1982. Energetics and mechanics of terrestrial locomotion. I. Metabolic energy consumption as a function of speed and body size in birds and mammals. Journal of Experimental Biology 97:1–21.CrossRefGoogle ScholarPubMed
Weishampel, D. B., and Horner, J. R. 1990. Hadrosauridae. Pp. 534–561in Weishampel, D. B., Dodson, P., and Osmólska, H., eds. The Dinosauria. University of California Press, Berkeley and Los Angeles.Google Scholar
Weishampel, D. B., Dodson, P., and Osmólska, H. 1990. The Dinosauria. University of California Press, Berkeley and Los Angeles.Google Scholar
Wilkinson, L. 1989. SYSTAT: the system for statistics. Systat, Inc., Evanston, Ill.Google Scholar