Hostname: page-component-745bb68f8f-mzp66 Total loading time: 0 Render date: 2025-01-12T12:56:59.828Z Has data issue: false hasContentIssue false
  • English
  • Français

The origin of the avian flight stroke: a kinematic and kinetic perspective

Published online by Cambridge University Press:  08 April 2016

Stephen M. Gatesy  and
David B. Baier
Stephen M. Gatesy
Affiliation:
Department of Ecology and Evolutionary Biology, Brown University, Providence, Rhode Island 02912. E-mail: [email protected]
David B. Baier
Affiliation:
Department of Ecology and Evolutionary Biology, Brown University, Providence, Rhode Island 02912. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Flying birds flap their wings to generate aerodynamic forces large enough to overcome weight and drag. During this behavior, the forelimbs are displaced and deformed in a complex, coordinated sequence of movements collectively known as the “flight stroke.” Despite an influx of relevant fossil material and new functional insights from extant birds, the historical origin of the avian flight stroke remains poorly resolved. Potential behavioral precursors have been identified primarily on the basis of kinematic resemblance—similarity of movement irrespective of underlying mechanisms. We discuss fundamental issues of motion analysis that are frequently overlooked by paleontologists, and conclude that a purely kinematic approach is insufficient. Consideration of kinetics, the forces responsible for motion, offers a more complete picture of flight stroke evolution. We introduce six kinetic components that interact to determine a limb's trajectory. Phylogenetic mapping reveals that forelimb loading patterns have undergone at least two major transitions on the line from basal archosaur to modern bird. Using this kinematic and kinetic perspective, we offer four specific criteria to help constrain and evaluate competing scenarios for the origin of the avian flight stroke.

Type
Articles
Information
Paleobiology , Volume 31 , Issue 3 , Summer 2005 , pp. 382 - 399
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

Altenbach, J. S., and Hermanson, J. W. 1987. Bat flight muscle function and the scapulo-humeral lock. Pp. 100–118in Fenton, M. B., Racey, P., and Rayner, J. M. V., eds. Recent advances in the study of bats. Cambridge University Press, New York.Google Scholar
Bernstein, N. A. 1967. The coordination and regulation of movements. Pergamon Press, London.Google Scholar
Biewener, A. A., and Full, R. J. 1992. Force platform and kinematic analysis. Pp. 45–73in Biewener, A. A., ed. Biomechanics—structures and systems: a practical approach. Oxford University Press, Oxford.Google Scholar
Biewener, A. A., Corning, W. R., and Tobalske, B. W. 1998. In vivo pectoralis muscle force-length behavior during level flight in pigeons (Columba livia). Journal of Experimental Biology 201:3293–3307.Google Scholar
Bock, W. J. 1986. The arboreal origin of avian flight. Memoirs of the California Academy of Sciences 8:57–72.Google Scholar
Brown, R. H. J. 1948. The flapping cycle of the pigeon. Journal of Experimental Biology 25:322–333.CrossRefGoogle ScholarPubMed
Bundle, M. W., and Dial, K. P. 2003. Mechanics of wing-assisted incline running (WAIR). Journal of Experimental Biology 206:4553–4564.Google Scholar
Burgers, P., and Chiappe, L. M. 1999. The wing of Archaeopteryx as a primary thrust generator. Nature 399:60–62.Google Scholar
Carpenter, K. 2002. Forelimb biomechanics of nonavian theropod dinosaurs in predation. Senckenbergiana lethaea 82:59–76.Google Scholar
Chatterjee, S. 1997. The rise of birds: 225 million years of evolution. Johns Hopkins University Press, Baltimore.Google Scholar
Chatterjee, S. 1999. Protoavis and the early evolution of birds. Palaeontographica 254:1–100.Google Scholar
Chen, P.-J., Dong, Z.-M, and Zhen, S.-N. 1998. An exceptionally well-preserved theropod dinosaur from the Yixian Formation of China. Nature 391:147–152.Google Scholar
Chiappe, L. M. 1995. The first 85 million years of avian evolution. Nature 378:349–355.CrossRefGoogle Scholar
Chiappe, L. M., and Dyke, G. J. 2002. The Mesozoic radiation of birds. Annual Review of Ecology and Systematics 33:91–124.Google Scholar
Chiappe, L. M., and Witmer, L. M. 2002. Mesozoic birds: above the heads of dinosaurs. University of California Press, Berkeley.Google Scholar
Clark, J. M., Norell, M. A., and Makovicky, P. J. 2002. Cladistic approaches to the relationships of birds to other theropod dinosaurs. Pp. 31–61in Chiappe, and Witmer, 2002.Google Scholar
Daniel, T. L., and Tu, M. S. 1999. Animal movement, mechanical tuning and coupled systems. Journal of Experimental Biology 202:3415–3421.Google Scholar
Dial, K. P. 2003. Wing-assisted incline running and the evolution of flight. Science 299:402–404.Google Scholar
Dial, K. P., Goslow, G. E. Jr., and Jenkins, F. A. Jr. 1991. The functional anatomy of the shoulder in the European starling (Sturnus vulgaris). Journal of Morphology 207:327–344.Google Scholar
Dubbeldam, J. L. 2001. Evolution of playlike behaviour and the uncoupling of neural locomotor mechanisms. Netherlands Journal of Zoology 51:335–345.Google Scholar
Dunn, F., and Parberry, I. 2002. 3D math primer for graphics and game development. Wordware, Plano, Texas.Google Scholar
Ebel, K. 1996. On the origin of flight in Archaeopteryx and in pterosaurs. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen 202:269–285.Google Scholar
Faulkes, Z., and Paul, D. H. 1997. Coordination between the legs and tail during digging and swimming in sand crabs. Journal of Comparative Physiology A 180:161–169.Google Scholar
Garner, J. P., Taylor, G. K., and Thomas, A. L. R. 1999. On the origin of birds: the sequence of character acquisition in the evolution of avian flight. Proceedings of the Royal Society of London B 266:1259–1266.Google Scholar
Gatesy, S. M. 1990. Caudofemoral musculature and the evolution of theropod locomotion. Paleobiology 16:170–186.CrossRefGoogle Scholar
Gatesy, S. M. 1999. Guineafowl hind limb function II: electromyographic analysis and motor pattern evolution. Journal of Morphology 240:115–125.Google Scholar
Gatesy, S. M. 2002. Locomotor evolution on the line to modern birds. Pp. 432–447in Chiappe, and Witmer, 2002.Google Scholar
Gatesy, S. M., and Dial, K. P. 1996. Locomotor modules and the evolution of avian flight. Evolution 50:331–340.Google Scholar
Gauthier, J. 1984. A cladistic analysis of the higher systematic categories of the Diapsida. Ph.D. dissertation. University of California, Berkeley.Google Scholar
Gauthier, J. 1986. Saurischian monophyly and the origin of birds. Memoirs of the California Academy of Sciences 8:1–55.Google Scholar
Gauthier, J., and Gall, J. F., eds. 2001. New perspectives on the origin and early evolution of birds. Peabody Museum of Natural History, Yale University, New Haven, Conn.Google Scholar
Gauthier, J. A., 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 1984. Freunde des Jura-Museums, Eichstätt, Germany.Google Scholar
Gishlick, A. D. 2001a. The function of the manus and forelimb of Deinonychus antirrhopus and its importance for the origin of avian flight. Pp. 301–318in Gauthier, and Gall, 2001.Google Scholar
Gishlick, A. D. 2001b. Predatory behavior in maniraptoran theropods. Pp. 414–417in Briggs, D. E. G. and Crowther, P. R., eds. Paleobiology II. Blackwell Science, Malden, Mass.Google Scholar
Goslow, G. E. Jr., Dial, K. P., and Jenkins, F. A. Jr. 1989. The avian shoulder: an experimental approach. American Zoologist 29:287–301.CrossRefGoogle Scholar
Gould, S. J., and Vrba, E. S. 1982. Exaptation—a missing term in the science of form. Paleobiology 8:4–15.Google Scholar
Hecht, M. K., Ostrom, J. H., Viohl, G., and Wellnhofer, P., eds. 1985. The beginnings of birds: proceedings of the international Archaeopteryx conference, Eichstätt 1984. Freunde des Jura-Museums, Eichstätt, Germany.Google Scholar
Hedrick, T. L., Tobalske, B. W., and Biewener, A. A. 2002. Estimates of circulation and gait change based on a three-dimensional kinematic analysis of flight in cockatiels (Nymphicus hollandicus) and ringed turtle-doves (Streptopelia risoria). Journal of Experimental Biology 205:1389–1409.CrossRefGoogle ScholarPubMed
Hedrick, T. L., Usherwood, J. R., and Biewener, A. A. 2004. Wing inertia and whole-body acceleration: an analysis of instantaneous aerodynamic force production in cockatiels (Nymphicus hollandicus) flying across a range of speeds. Journal of Experimental Biology 207:1689–1702.Google Scholar
Hermanson, J. W., and Altenbach, J. S. 1983. The functional anatomy of the shoulder of the Pallid bat, Antrozous pallidus. Journal of Mammalogy 64:62–75.Google Scholar
Holtz, T. R. Jr. 1994. The phylogenetic position of the Tyrannosauridae: implications for theropod systematics. Journal of Paleontology 68:1100–1117.CrossRefGoogle Scholar
Hutchinson, J. R., and Garcia, M. 2002. Tyrannosaurus was not a fast runner. Nature 15:1018–1021.CrossRefGoogle Scholar
Jenkins, F. A. Jr. 1993. The evolution of the avian shoulder joint. American Journal of Science 293:253–267.Google Scholar
Jenkins, F. A. Jr., and Goslow, G. E. Jr. 1983. The functional anatomy of the shoulder of the Savannah Monitor lizard (Varanus exanthematicus). Journal of Morphology 175:195–216.CrossRefGoogle ScholarPubMed
Jenkins, F. A. Jr., Dial, K. P., and Goslow, G. E. Jr. 1988. A cineradiographic analysis of bird flight: the wishbone in starlings is a spring. Science 241:1495–1498.CrossRefGoogle ScholarPubMed
Ji, Q., and Ji, S. A. 1997. Protarchaeopterygid bird (Protarchaeopteryx gen. nov.)—fossil remains of archaeopterygids from China. Chinese Geology 238:38–41.Google Scholar
Ji, Q., Currie, P. J., Norell, M. A., and Ji, S. A. 1998. Two feathered dinosaurs from northeastern China. Nature 393:753–761.Google Scholar
Johnston, R. M., and Bekoff, A. 1992. Constrained and flexible features of rhythmical hindlimb movements in chicks: kinematic profiles of walking, swimming and airstepping. Journal of Experimental Biology 171:43–66.Google Scholar
Katz, P. S., and Harris-Warrick, R. M. 1999. The evolution of neuronal circuits underlying species-specific behavior. Current Opinions in Neurobiology 9:628–633.CrossRefGoogle ScholarPubMed
Lieber, R. L. 1992. Skeletal muscle structure and function. Williams and Wilkins, Baltimore.Google Scholar
Marey, J. E. 1888. The mechanism of flight of birds. Nature 37:369–374.Google Scholar
Marey, J. E. 1894. Le mouvement. Masson, Paris.Google Scholar
Nopcsa, F. 1907. Ideas on the origin of flight. Proceedings of the Zoological Society of London 1907:223–236.Google Scholar
Nopcsa, F. 1923. On the origin of flight in birds. Proceedings of the Zoological Society of London 1923:463–477.CrossRefGoogle Scholar
Norell, M., Clark, J. M., and Makovicky, P. J. 2001. Phylogenetic relationships among coelurosaurian theropods. Pp. 49–67in Gauthier, and Gall, 2001.Google Scholar
Norell, M., Ji, Q., Gau, K., Yuan, C., Zhao, Y., and Wang, L. 2002. ‘Modern’ feathers on a non-avian dinosaur. Nature 416:36–37.Google Scholar
Ostrom, J. H. 1969. Osteology of Deinonychus antirrhopus, an unusual theropod from the Lower Cretaceous of Montana. Bulletin of the Yale Peabody Museum of Natural History 30:1–165.Google Scholar
Ostrom, J. H. 1973. The ancestry of birds. Nature 242:136.Google Scholar
Ostrom, J. H. 1974. Archaeopteryx and the origin of flight. Quarterly Review of Biology 49:27–47.Google Scholar
Ostrom, J. H. 1976. Archaeopteryx and the origin of birds. Biological Journal of the Linnean Society 8:91–182.Google Scholar
Ostrom, J. H. 1979. Bird flight: how did it begin? American Scientist 67:46–56.Google Scholar
Özkaya, N., and Nordin, M. 1999. Fundamentals of biomechanics: equilibrium, motion, and deformation. Springer, New York.Google Scholar
Padian, K. 1982. Macroevolution and the origin of major adaptations: vertebrate flight as a paradigm for the analysis of patterns. Proceedings of the Third North American Paleontological Convention 2:387–392.Google Scholar
Padian, K. 1985. The origins and aerodynamics of flight in extinct vertebrates. Paleontology 28:413–433.Google Scholar
Padian, K. 1987. A comparative phylogenetic and functional approach to the origin of vertebrate flight. Pp. 3–23in Fenton, M. B., Racey, P., and Rayner, J. M. V., eds. Recent advances in the study of bats. Cambridge University Press, Cambridge.Google Scholar
Padian, K. 2001. Stages in the origin of bird flight: beyond the arboreal-cursorial dichotomy. Pp. 255–272in Gauthier, and Gall, 2001.Google Scholar
Padian, K., and Chiappe, L. M. 1998. The origin and early evolution of birds. Biological Reviews 73:1–42.Google Scholar
Pennycuick, C. J. 1968. Power requirements for horizontal flight in the pigeon Columba livia. Journal of Experimental Biology 49:527–555.Google Scholar
Poppen, N. K., and Walker, P. S. 1978. Forces at the glenohumeral joint in abduction. Clinical Orthopaedics 135:165–170.Google Scholar
Roberts, T. J., Marsh, R. L., Weyand, P. G., and Taylor, C. R. 1997. Muscular force in running turkeys: the economy of minimizing work. Science 275:1113–1115.Google Scholar
Romer, A. S. 1956. Osteology of the reptiles. University of Chicago Press, Chicago.Google Scholar
Sereno, P. C. 1997. The origin and evolution of dinosaurs. Annual Review of Earth and Planetary Sciences 25:435–489.Google Scholar
Sereno, P. C. 1999. The evolution of dinosaurs. Science 284:2137–2147.CrossRefGoogle ScholarPubMed
Smith, J. L., and Zernicke, R. F. 1987. Predictions for neural control based on limb dynamics. Trends in Neurosciences 10:123–128.Google Scholar
Soechting, J. F., and Flanders, M. 1992. Moving in three-dimensional space: frames of reference, vectors, and coordinate systems. Annual Review of Neuroscience 15:167–191.Google Scholar
Sy, M. 1936. Funktionell-anatomische untersuchungen am vogelflugel. Journal für Ornithologie 84:199–296.Google Scholar
Tobalske, B. W., and Dial, K. P. 1996. Flight kinematics of black-billed magpies and pigeons over a wide range of speeds. Journal of Experimental Biology 199:263–280.Google Scholar
Wainwright, P. C., and Turingan, R. G. 1997. Evolution of pufferfish inflation behavior. Evolution 51:506–518.Google Scholar
Warrick, D. R., and Dial, K. P. 1998. Kinematic, aerodynamic and anatomical mechanisms in the slow, maneuvering flight of pigeons. Journal of Experimental Biology 201:655–672.Google Scholar
Williston, S. W. 1879. Are birds derived form dinosaurs? Kansas City Review of Science 3:457–460.Google Scholar
Xu, X., Tang, Z.-L., and Wang, X.-L. 1999a. A therozinosauroid dinosaur with integumentary structures from China. Nature 399:350–354.Google Scholar
Xu, X., Wang, X.-L., and Wu, X.-C. 1999b. A dromaeosaurid dinosaur with a filamentous integument from the Yixian Formation of China. Nature 401:262–266.Google Scholar
Xu, X., Zhou, Z., Wang, X., Kuang, X., Zhang, F., and Xiangke, D. 2003. Four-winged dinosaurs from China. Nature 421:335–340.Google Scholar