Hostname: page-component-848d4c4894-p2v8j Total loading time: 0.001 Render date: 2024-05-20T17:15:15.391Z Has data issue: false hasContentIssue false
  • English
  • Français

The evolution of locomotor stamina in tetrapods: circumventing a mechanical constraint

Published online by Cambridge University Press:  08 April 2016

David R. Carrier
David R. Carrier*
Affiliation:
Department of Biology, The University of Michigan, Ann Arbor, Michigan 48109
Get access Rights & Permissions [Opens in a new window]

Abstract

Endothermic tetrapods differ dramatically from ectothermic tetrapods in having a great capacity to sustain vigorous locomotion. I suggest that this difference reflects alternative adaptive responses to a mechanical constraint that was an inherent consequence of the vertebrate transition from aquatic to terrestrial modes of locomotion and respiration. The earliest tetrapods may not have been able to walk and breathe at the same time. Their sprawling gait and lateral vertebral bending would have required unilateral contractions of the thoracic musculature that may have interfered with the bilateral movements necessary for breathing. Modern lizards, whose locomotor and respiratory anatomy resembles that of the early tetrapods, provide support for this hypothesis because their breathing is greatly reduced during locomotor activity. Tetrapod lineages that gave rise to modern ectotherms apparently retained the constraint, becoming either highly specialized for burst activity based on anaerobic metabolism or specialized in passive mechanisms of defense against predators. The lineages from which birds and mammals are derived have undergone morphological changes that enable simultaneous running and breathing. In modern tetrapods upright posture is correlated with endothermic metabolism. This correlation may have arisen to circumvent ancestral constraints on locomotor stamina.

Type
Articles
Information
Paleobiology , Volume 13 , Issue 3 , Summer 1987 , pp. 326 - 341
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

Alexander, R. McN. 1985. The ideal and the feasible: physical constraints on evolution. Biol. J. Linn. Soc. 26:345–358.Google Scholar
Andrews, S. M. and Stanley, T. S. 1970. The postcranial skeleton of Eusthenopteron foordi Whiteaves. Roy. Soc. Edinburgh, Trans. 68:207–329.Google Scholar
Avery, R. A., Mueller, C. F., Smith, J. A., and Bond, D. J. 1987. The movement patterns of lacertid lizards: speed, gait and pauses in Lacerta vivipara. J. Zool., Lond. 211:47–63.Google Scholar
Bakker, R. T. 1971. Dinosaur physiology and the origin of mammals. Evolution. 25:636–658.Google Scholar
Bakker, R. T. 1972. Locomotor energetics of lizards and mammals compared. The Physiologist. 15:76.Google Scholar
Bakker, R. T. 1975. Experimental and fossil evidence for the evolution of tetrapod bioenergetics. Pp. 365–399. In: Gates, D. M. and Schment, R. B., eds. Perspectives of Biophysical Ecology. Springer-Verlag; New York.CrossRefGoogle Scholar
Bakker, R. T. 1980. Dinosaur heresy—dinosaur renaissance. Pp. 351–505. In: Thomas, R. D. K. and Olson, E. C., eds. A Cold Look at the Warm Blooded Dinosaurs. Westview Press, Inc.; Boulder, Colorado.Google Scholar
Beamish, F. W. H. 1978. Swimming capacity. Pp. 101–187. In: Hoar, W. S. and Randall, D. J., eds. Fish Physiology, vol. VII. Academic Press, Inc.; London.Google Scholar
Belkin, D. A. 1961. The running speeds of the lizards Dipsosaurus dorsalis and Callisaurus draconoides. Copeia. 1961:223–224.Google Scholar
Bennett, A. F. 1978. Activity metabolism of the lower vertebrates. Ann. R. Physiol. 400:447–469.Google Scholar
Bennett, A. F. 1980. The metabolic foundations of vertebrate behavior. BioScience. 30:452–456.CrossRefGoogle Scholar
Bennett, A. F. 1982. The energetics of reptilian activity. Pp. 155–199. In: Gans, C. and Pough, F. H., eds. Biology of the Reptilia, vol. 13. Academic Press; London.Google Scholar
Bennett, A. F. 1985. Energetics and locomotion. Pp. 173–184. In: Hildebrand, M., Bramble, D. M., Liem, K. F., and Wake, D. B., eds. Functional Vertebrate Morphology. Harvard University Press; Cambridge, Massachusetts.Google Scholar
Bennett, A. F. and Dalzell, B. 1973. Dinosaur physiology: a critique. Evolution. 27:170–174.CrossRefGoogle Scholar
Bennett, A. F. and Ruben, J. A. 1979. Endothermy and activity in vertebrates. Science. 206:649–654.Google Scholar
Bennett, A. F. and Ruben, J. A. 1986. The metabolic and thermoregulatory status of therapsids. Pp. 207–218. In: Hottonx, N. III, Maclean, P. D., Roth, J. J., and Roth, E. C., eds. The Ecology and Biology of Mammal-like Reptiles. Smithsonian Institution Press; Washington, D.C.Google Scholar
Benton, M. J. 1983. The Triassic reptile Hyperodapedon from Elgin: functional morphology and relationships. Phil. Trans. R. Soc. Lond. B. 302:605–717.Google Scholar
Berger, M., Roy, O. Z., and Hart, J. S. 1970. The co-ordination between respiration and wing beats in birds. Z. Vergl. Physiol. 66:190–200.Google Scholar
Bramble, D. M. 1983. Respiratory patterns and control during unrestrained human running. Pp. 213–220. In: Whipp, B. J. and Wiberg, D. M., eds. Modelling and Control of Breathing. Elsevier; New York.Google Scholar
Bramble, D. M. 1986. Biochemical and neuromotor factors in mammalian locomotor—respiratory coupling. Pp. 130–149. In: Othmer, H. G., ed. Nonlinear Oscillations in Biology and Chemistry. Springer-Verlag; Berlin.Google Scholar
Bramble, D. M. 1987. Axial-appendicular dynamics in the integration of breathing and gait in mammals. Amer. Zool. In Press.Google Scholar
Bramble, D. M. and Carrier, D. R. 1983. Running and breathing in mammals. Science. 219:251–256.Google Scholar
Brink, A. S. 1956. Speculations on some advanced mammalian characteristics in the higher mammal-like reptiles. Palaeont. Afr. 3:3–39.Google Scholar
Butler, P. J. 1982. Respiration during flight and diving in birds. Pp. 103–114. In: Addink, A. D. F. and Spronk, N., eds. Exogenous and Endogenous Influences in Metabolic and Neural Control. Pergamon Press; Oxford.Google Scholar
Carpenter, R. E. 1986. Flight physiology of intermediate-sized fruit bats (Pteropodidae). J. Exp. Biol. 120:79–103.Google Scholar
Carrier, D. R. 1984. The energetic paradox of human running and hominid evolution. Curr. Anthr. 25:483–495.Google Scholar
Carrier, D. R. 1987. Lung ventilation during walking and running in four species of lizards. Exp. Biol. 47:33–42.Google Scholar
Charig, A. 1972. The evolution of the archosaur pelvis and hindlimb: an explanation in functional terms. Pp. 121–155. In: Joysey, K. A. and Kemp, T. M., eds. Studies in Vertebrate Evolution. Oliver and Boyd; Edinburgh.Google Scholar
Clemens, H. B. 1961. The migration, age and growth of Pacific albacore (Thunnus germa), 1951–1958. Fish. Bull. Calif. 115:1–128.Google Scholar
Colbert, E. H. and Mook, C. C. 1951. The ancestral crocodilian Protosuchus. Bull. Amer. Mus. Nat. Hist. 97:147–182.Google Scholar
Cott, H. B. 1961. Scientific results of an inquiry into the ecology and economic status of the Nile crocodile, Crocodylus niloticus, in Uganda and Northern Rhodesia. Trans. Zool. Soc. Lond. 29:211–311.Google Scholar
Crompton, A. W. and Jenkins, F. A. 1979. Origin of mammals. Pp. 59–73. In: Lillegraven, J. A., Kielan-Jaworowska, Z., and Clemens, W. A., eds. Mesozoic Mammals. University of California Press; Berkeley.Google Scholar
Crush, P. J. 1984. A late upper Triassic sphenosuchid crocodilian from Wales. Palaeontology. 27:131–157.Google Scholar
Dorf, E. 1970. Paleobotanical evidence of Mesozoic and Cenozoic climatic changes. Proc. N. Amer. Paleontol. Conv. 1969 D:323–346.Google Scholar
Eaton, G. F. 1910. Osteology of Pteranodon. 101 pp. Memoirs of the Connecticut Academy of Arts and Sciences. Yale University; New Haven, Connecticut.Google Scholar
Fedde, M. R., Burger, R. E., and Kitchell, R. L. 1964. Anatomic and electromyographic studies of the costopulmonary muscles in the cock. Poultry Sci. 43:1177–1184.Google Scholar
Gambaryan, P. P. 1974. How Mammals Run. 367 pp. John Wiley and Sons; New York.Google Scholar
Gans, C. 1970a. Respiration in early tetrapods—the frog is a red herring. Evolution. 24:723–734.Google Scholar
Gans, C. 1970b. Strategy and sequence in the evolution of the external gas exchangers of ectothermal vertebrates. Forma et Functio. 3:61–104.Google Scholar
Gans, C. and Clark, B. 1976. Studies on ventilation in Caiman crocodilus (Crocodilia: Reptilia). Respir. Physiol. 26:285–301.Google Scholar
Garland, T. 1982. Scaling maximal running speed and maximal aerobic speed to body mass in mammals and lizards. The Physiologist. 25:338.Google Scholar
Gasc, J.-P. 1981. Axial Musculature. Pp. 355–435. In: Gans, C. and Parsons, T. S., eds. Biology of the Reptilia, vol. II. Academic Press; London.Google Scholar
Gauthier, J. A. 1984. A cladistic analysis of the higher systematic categories of the Diapsida. Ph.D. dissertation, Department of Paleontology, University of California; Berkeley.Google Scholar
Gauthier, J. A. 1986. Saurischian monophyly and the origin of birds. Pp. 1–47. In: Padian, K., ed. The Origin of Birds and the Evolution of Flight. California Academy of Sciences; San Francisco.Google Scholar
Gleeson, T. T., Mitchell, G. S., and Bennett, A. F. 1980. Cardiovascular response to graded activity in the lizards Varanus and Iguana. Am. J. Physiol. 239:R174–179.Google Scholar
Gray, J. 1968. Animal Locomotion. 479 pp. Norton; New York.Google Scholar
Heath, J. E. 1968. The origin of thermoregulation. Pp. 259–278. In: Drake, E., ed. Evolution and Environment. Yale University Press; New Haven, Conn.Google Scholar
Heinrich, B. 1977. Why have some animals evolved to regulate a high body temperature? Am. Nat. 111:623–640.CrossRefGoogle Scholar
Heisler, N., Neumann, P., and Maloiy, G. M. O. 1983. The mechanism of intracardiac shunting in the lizard Varanus exanthematicus. J. Exp. Biol. 105:15–31.CrossRefGoogle ScholarPubMed
Herald, E. S. and Ripley, W. E. 1951. The relative abundance of sharks and bat sting rays in San Francisco Bay. Calif. Fish Game. 37:315–329.Google Scholar
Hildebrand, M. 1974. Analysis of Vertebrate Structure. 710 pp. John Wiley and Sons; New York.Google Scholar
Hildebrand, M. and Hurley, J. P. 1985. Energy of the oscillating legs of a fast-moving cheetah, pronghorn, jackrabbit, and elephant. J. Morph. 184:23–31.Google Scholar
Hoffstetter, R. and Gasc, J.-P. 1969. Vertebrae and ribs of modern reptiles. Pp. 201–302. In: Gans, C, Bellairs, A. A., and Parsons, T. S., eds. Biology of the Reptilia, vol. I. Academic Press; London.Google Scholar
Hornicke, H., Meixner, R. M., and Pollmann, U. 1983. Respiration in exercising horses. Pp. 7–16. In: Snow, D. H., Persson, S. G. B., and Rose, R. J., eds. Equine Exercise Physiology. Burlington Press; Cambridge, England.Google Scholar
Huxley, T. H. 1882. On the respiratory organs of Apteryx. Proc. Zool. Soc. Lond. 1882:560–569.Google Scholar
Inger, R. F. 1957. Ecological aspects of the origins of the tetrapods. Evolution. 11:373–376.CrossRefGoogle Scholar
Jenkins, F. A. 1970a. Cynodont postcranial anatomy and the “prototherian” level of mammalian organizaiton. Evolution. 24:230–252.Google Scholar
Jenkins, F. A. 1970b. Limb movements in a monotreme (Tachyglossus aculeatus): a cineradiographic analysis. Science. 198:1473–1475.Google Scholar
Jenkins, F. A. 1971. The postcranial skeleton of African cynodonts. Bull. Peabody Mus. Nat. Hist. 36:1–216.Google Scholar
Jenkins, F. A. and Parrington, F. R. 1976. The postcranial skeletons of the Triassic mammals Eozostrodon, Megazostrodon and Erythrotherium. Phil. Trans. R. Soc. B. 273:387–431.Google Scholar
Jenkins, F. A. and Weijs, W. A. 1979. The functional anatomy of the shoulder in the Virginia opossum (Didelphis virginiana). J. Zool., Lond. 188:379–410.Google Scholar
Jones, D. R. and Randall, D. J. 1978. The respiratory and circulatory systems during exercise. Pp. 425–501. In: Hoar, W. S. and Randall, D. J., eds. Fish Physiology, vol VII. Academic Press, Inc; London.Google Scholar
Kemp, T. S. 1982. Mammal-like Reptiles and the Origin of Mammals. 363 pp. Academic Press; London.Google Scholar
Kimura, T., Okada, M., and Ishida, H. 1979. Kinesiological characteristics of primate walking: its significance in human walking. Pp. 297–312. In: Morbeck, M. E., Preuschoft, H., and Gomberg, N., eds. Environment, Behavior and Morphology: Dynamic Interactions in Primates. Gustav Fisher; New York.Google Scholar
Maynard Smith, J., Burian, R., Kauffman, S., Alberch, P., Cambell, J., Goodman, B., Lande, R., Raup, D., and Wolpert, L. 1985. Developmental constraints and evolution. Quart. Rev. Biol. 60:265–287.CrossRefGoogle Scholar
Maynard Smith, J. and Savage, R. J. G. 1956. Some locomotory adaptations in mammals. Zool. J. Linn. Soc. 42:603–622.CrossRefGoogle Scholar
Mitchell, G. S., Gleeson, T. T., and Bennett, A. F. 1981. Pulmonary oxygen transport during activity in lizards. Respir. Physiol. 43:365–375.Google Scholar
Mognoni, P., Saibene, F., and Sant' Ambrogio, G. 1969. Contribution of the diaphragm and the other inspiratory muscles to different levels of tidal volume and static inspiratory effort in the rabbit. J. Physiol. 202:517–534.Google Scholar
Muybridge, E. 1887. Animal Locomotion. An electro-photographic investigation of consecutive phases of animal movements. 264 pp. Lippincott; Philadelphia.Google Scholar
Nishi, S. 1938. Muskel des Rumpfes. Pp. 351–442. In: Bolk, L., Goppert, E., Kallius, E., and Lubosch, W., eds. Handbuch der vergleichenden Anatomie der Wirbeltiere. Schwarzenberg; Berlin and Wien.Google Scholar
Olson, E. C. 1936. The dorsal axial musculature of certain primitive Permian tetrapods. J. Morph. 59:265–311.Google Scholar
Ostrom, J. H. 1970. Terrestrial vertebrates as indicators of Mesozoic climates. Pp. 347–376. In: Yochelson, E. L., ed. Proceedings of the North American Paleontological Convention 1969. Allen Press, Inc.; Lawrence, Kansas.Google Scholar
Padian, K. 1983. A functional analysis of flying and walking in pterosaurs. Paleobiology. 9:218–239.Google Scholar
Panchen, A. L. 1977. The origin and early evolution of tetrapod vertebrae. Pp. 289–318. In: Andrews, S. M., Miles, R. S., and Walker, A. D., eds. Problems in Vertebrate Evolution. Academic Press; London.Google Scholar
Parrish, J. M. 1986. Locomotor adaptations in the hindlimb and pelvis of the Thecodontia. Hunteria. 2:3–35.Google Scholar
Pough, F. H. 1979. Origin and early radiation of reptiles. Pp. 377–400. In: McFarland, W. N., Pough, F. H., Cade, T. J., and Heiser, J. B., eds. Vertebrate Life. Macmillan; New York.Google Scholar
Pridmore, P. A. 1985. Terrestrial locomotion in monotremes (Mammalia: Monotremata). J. Zool., Lond. 205:53–73.Google Scholar
Regal, P. J. and Gans, C. 1980. The revolution in thermal physiology, implications for dinosaurs. Pp. 167–188. In: Thomas, R. D. K. and Olson, E. C., eds. A Cold Look at the Warm Blooded Dinosaurs. AAAS Selected Symposia Series. Westview Press; Boulder, Colo.Google Scholar
Rewcastle, S. C. 1981. Stance and gait in tetrapods: an evolutionary scenario. Symp. Zool. Soc. Lond. 48:239–267.Google Scholar
Ricqlès, A. 1978. Recherches paléohistologiques sur les os longs des tetrapodes. VII. Annales de Paléontologie. 64:85–111.Google Scholar
Rockwell, H., Evans, F. G., and Pheasant, H. C. 1938. The comparative morphology of the vertebrate spinal column. Its form as related to function. J. Morph. 63:87–117.Google Scholar
Romer, A. S. 1933. Vertebrate Paleontology. 468 pp. University of Chicago Press; Chicago.Google Scholar
Romer, A. S. 1956. Osteology of the Reptiles. 722 pp. University of Chicago Press; Chicago.Google Scholar
Romer, A. S. 1972. Skin breathing—primary or secondary? Respir. Physiol. 14:183–192.Google ScholarPubMed
Romer, A. S. and Price, L. W. 1940. Review of the Pelycosauria. Geol. Soc. Am. Spec. Pap. 28:1–538.Google Scholar
Ruben, J. A. and Battalia, D. E. 1979. Aerobic and anaerobic metabolism during activity in small rodents. J. Exp. Zool. 208:73–76.Google Scholar
Schmidt-Nielsen, K. 1979. Animal Physiology: Adaptation and Environment. 560 pp. Cambridge University Press; Cambridge.Google Scholar
Schuh, F. 1951. Das Warmbluterproblem in der Paläontologie. Paläont. Z. 24:194–200.Google Scholar
Slijper, E. J. 1946. Comparative biologic-anatomical investigations on the vertebral column and spinal musculature of mammals. Verh. K. Ned. Akad. Wet. 42:1–128.Google Scholar
Snyder, R. C. 1949. Bipedal locomotion of the lizard Basiliscus basiliscus. Copeia. 1949:129–137.Google Scholar
Snyder, R. C. 1962. Adaptations for bipedal locomotion of lizards. Am. Zool. 2:191–203.Google Scholar
Storer, R. W. 1982. Fused thoracic vertebrae in birds: their occurrence and possible significance. J. Yamashina Inst. Ornith. 14:86–95.Google Scholar
Suther, R. A., Thomas, S. P., and Suther, B. J. 1972. Respiration, wing-beat and ultrasonic pulse emission in an echolocating bat. J. Exp. Biol. 56:37–48.Google Scholar
Taigen, T. L. 1983. Activity metabolism of anuran amphibians: implications for the origin of endothermy. Amer. Nat. 121:94–109.Google Scholar
Taylor, C. R. 1973. Energy cost of animal locomotion. Pp. 23–42. In: Bolis, L., Schmidt-Nielsen, K., and Maddrell, S. H. P., eds. Comparative Physiology: Locomotion, Respiration, Transport and Blood. American Elsevier Publ. Co.; New York.Google Scholar
Taylor, C. R., Schmidt-Nielsen, K., and Raab, J. L. 1970. Scaling of energetic cost of running to body size in mammals. Am. J. Physiol. 219:1104–1107.Google Scholar
Tenney, S. M. and Tenney, J. B. 1970. Quantitative morphology of cold-blooded lungs: Amphibia and Reptilia. Respir. Physiol. 9:197–215.CrossRefGoogle ScholarPubMed
Thomas, S. P. 1981. Ventilation and oxygen extraction in the bat Pteropus gouldii during rest and steady flight. J. Exp. Biol. 94:231–250.Google Scholar
Tucker, V. A. 1975. The energetic cost of moving about. Am. Sci. 63:413–419.Google Scholar
Vallois, H. V. 1922. Les transformations de la musculature de lepisome chez les vertébrés. Archs. Morph. Gén. Exp. 13:1–538.Google Scholar
Walker, A. D. 1970. A revision of the Jurassic reptile Hallopus victor (Marsh), with remarks on the classification of crocodiles. Phil. Trans. Roy. Soc. Lond. 257:323–371.Google Scholar
Webb, G. J. W. and Gans, C. 1982. Galloping in Crocodylus johnstoni—a reflection of terrestrial activity. Rec. Aust. Mus. 34:607–618.Google Scholar
Webb, P. W. 1975. Synchrony of locomotion and ventilation in Cymatogaster aggregata. Can. J. Zool. 53:904–907.Google Scholar
Weis-Fogh, T. 1967. Respiration and tracheal ventilation in locusts and other flying insects. J. Exp. Biol. 47:561–587.Google Scholar
White, F. N. 1976. Circulation. Pp. 275–334. In: Gans, C. and Dawson, W. R., eds. Biology of the Reptilia, Vol. 5. Academic Press; London.Google Scholar
Wood, S. C. and Lenfant, C. J. M. 1976. Respiration: mechanics control and gas exchange. Pp. 225–274. In: Gans, C. and Dawson, W. R., eds. Biology of the Reptilia, Vol. 5. Academic Press; London.Google Scholar
Zug, G. R. 1974. Crocodilian galloping. An unique gait for reptiles. Copeia. 1974:550–551.Google Scholar