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The evolution of pelvic aspiration in archosaurs

Published online by Cambridge University Press:  08 February 2016

David R. Carrier  and
Colleen G. Farmer
David R. Carrier
Affiliation:
Department of Biology, University of Utah, Salt Lake City, Utah 84112. E-mail: carrier@biology.utah.edu
Colleen G. Farmer
Affiliation:
Department of Ecology and Evolutionary Biology, University of California, Irvine, California 92697. E-mail: cfarmer@uci.edu
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Abstract

Movements of the pelvic girdle have recently been found to contribute to inspiratory airflow in both crocodilians and birds. Although the mechanisms are quite different in birds and crocodilians, participation of the pelvic girdle in the production of inspiration is rare among vertebrates. This raises the possibility that the pelvic musculoskeletal system may have played a role in the ventilation of basal archosaurs. Judging from the mechanism of pelvic aspiration in crocodilians and the structure of gastralia in basal archosaurs, we suggest that an ischiotruncus muscle pulled the medial aspect of the gastralia caudally, and thereby helped to produce inspiration by increasing the volume of the abdominal cavity. From this basal mechanism, several archosaur lineages appear to have evolved specialized gastralia, pelvic kinesis, and/or pelvic mobility. Kinetic pubes appear to have evolved independently in at least two clades of Crocodylomorpha. This convergence suggests that a diaphragmatic muscle may be basal for Crocodylomorpha. The pelvis of pterosaurs was long, open ventrally, and had prepubic elements that resembled the pubic bones of Recent crocodilians. These characters suggest convergence on the pelvic aspiratory systems of both birds and crocodilians. The derived configuration of the pubis, ischium and gastralia of non-avian theropods appears to have enhanced the basal gastral breathing mechanism. Changes in structure of the pelvic musculoskeletal system that were present in both dromaeosaurs and basal birds may have set the stage for a gradual reduction in the importance of gastral breathing and for the evolution of the pelvic aspiration system of Recent birds. Lastly, the structure of the pelvis of some ornithischians appears to have been permissive of pubic and ischial kinesis. Large platelike prepubic processes evolved three times in Ornithischia. These plates are suggested to have been instrumental in an active expansion of the lateral abdominal wall to produce inspiratory flow. Thus, many of the unique features found in the pelvic girdles of various archosaur groups may be related to the function of lung ventilation rather than to locomotion.

Type
Articles
Information
Paleobiology , Volume 26 , Issue 2 , Spring 2000 , pp. 271 - 293
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Baumel, J. J. 1988. Functional morphology of the tail apparatus of the pigeon (Columba livia). Advances in Anatomy, Embryology and Cell Biology 110:1–115.CrossRefGoogle Scholar
Baumel, J. J., Wilson, J. A., and Bergren, D. R. 1990. The ventilatory movements of the avian pelvis and tail: function of the muscles of the tail region of the pigeon (Columba livia). The Journal of Experimental Biology 151:263–277.CrossRefGoogle ScholarPubMed
Benton, M. J., and Clark, J. 1988. Archosaur phylogeny and the relationships of the Crocodylia. Pp. 289–332in Benton, M. J., ed. The phylogeny and classification of the tetrapods, Vol. I. Clarendon, Oxford.Google Scholar
Boelaert, R. 1942. Sur la physiologie de la respiration de l'Alligator mississippiensis. Archives Internationales de Physiologie 52:57–72.CrossRefGoogle Scholar
Boggs, D. F. 1997. Coordinated control of respiratory pattern during locomotion in birds. American Zoologist 37:41–53.CrossRefGoogle Scholar
Boggs, D. F., Jenkins, F. A., and Dial, K. P. 1997. The effects of the wingbeat cycle on respiration in black-billed magpies (Picapica). The Journal of Experimental Biology 200:1403–1412.CrossRefGoogle Scholar
Brainerd, E. L., Ditelberg, J. S., and Bramble, D. M. 1993. Lung ventilation in salamanders and the evolution of vertebrate air-breathing mechanisms. Biological Journal of the Linnean Society 49:163–183.CrossRefGoogle Scholar
Bramble, D. M., and Carrier, D. R. 1983. Running and breathing in mammals. Science 219:251–256.CrossRefGoogle ScholarPubMed
Britt, B. B., Makovicky, P., Gauthier, J., and Bonde, N. 1998. Postcranial pneumatization in Archaeopteryx. Nature 395:374–376.CrossRefGoogle Scholar
Brown, B. 1916. Corythosaurus casuarius: skeleton, musculature and epidermis. Bulletin of the American Museum of Natural History 35:709–716.Google Scholar
Carrier, D. R. 1987. The evolution of locomotor stamina in tetrapods: circumventing a mechanical constraint. Paleobiology 13:326–341.CrossRefGoogle Scholar
Carrier, D. R. 1989. Ventilatory action of the hypaxial muscles of Iguana iguana: a function of slow muscle. Journal of Experimental Biology 143:435–457.CrossRefGoogle ScholarPubMed
Charig, A. F. 1972. The evolution of the archosaur pelvis and hind-limb: an explanation in functional terms. Pp. 121–155in Joysey, K. A. and Kemp, T. S., eds. Studies in vertebrate evolution. Winchester, New York.Google Scholar
Chatterjee, S. 1985. Postosuchus, a new thecodontian reptile from the Triassic of Texas and the origin of tyrannosaurs. Philosophical Transactions of the Royal Society of London B 309:395–460.Google Scholar
Claessens, L. 1996. Dinosaur gastralia and their function in respiration. Journal of Vertebrate Paleontology 16:28A.Google Scholar
Claessens, L. 1997. Gastralia. Pp. 269–270in Currie, P. J. and Padian, K., eds. Encyclopedia of dinosaurs. Academic Press, San Diego.Google Scholar
Colbert, E. H., and Mook, C. C. 1951. The ancestral crocodilian Protosuchus. Bulletin of the American Museum of Natural History 97:146–182.Google Scholar
Crush, P. J. 1984. A late Upper Triassic Sphenosuchid crocodilian from Wales. Palaeontology 27:131–157.Google Scholar
De Troyer, A., and Loring, S. H. 1986. Action of the respiratory muscles. Pp. 443–561in Macklem, P. T. and Mead, J., eds. Handbook of physiology: the respiratory system. American Physiological Society, Bethesda, Md.Google Scholar
Dodson, P. 1996. The horned dinosaurs. Princeton University Press, Princeton, N.J.Google Scholar
Dodson, P., and Currie, P. J. 1990. Neoceratopsia. Pp. 593–618in Weishampel, et al. 1990.Google Scholar
Eaton, C. F. 1910. Osteology of Pteranodon. Memoirs of the Connecticut Academy of Arts and Sciences 2:1–38.Google Scholar
Ewer, R. F. 1965. The anatomy of the thecodont reptile Euparkeria capensis Broom. Philosophical Transactions of the Royal Society of London B 248:379–435.Google Scholar
Farmer, C. G., and Carrier, D. R. 2000a. Pelvic aspiration in the American alligator (Alligator mississippiensis). Journal of Experimental Biology (in press).CrossRefGoogle Scholar
Farmer, C. G. 2000b. Ventilation and gas exchange in the American alligator (Alligator mississippiensis) during treadmill-exercise. Journal of Experimental Biology (in press).Google Scholar
Fastovsky, D. E., and Weishampel, D. B. 1996. The evolution and extinction of the dinosaurs. Cambridge University Press, Cambridge.Google Scholar
Fedde, M. R. 1976. Respiration. Pp. 122–145in Sturkie, P. D., ed. Avian physiology. Springer, New York.CrossRefGoogle Scholar
Fedde, M. R., DeWet, P. D., and Kitchell, R. L. 1969. Motor unit recruitment pattern and tonic activity in respiratory muscles of Gallus domesticus. Journal of Neurophysiology 32:995–1004.CrossRefGoogle ScholarPubMed
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 279:1915–1919.CrossRefGoogle ScholarPubMed
Galton, P. M. 1990. Stegosauria. Pp. 435–455in Weishampel, et al. 1990.Google Scholar
Gans, C., and Clark, B. 1976. Studies on ventilation of Caiman crocodilus (Crocodilia: Reptilia). Respiration Physiology 26:285–301.CrossRefGoogle ScholarPubMed
Gans, C., and Hughes, G. M. 1967. The mechanism of lung ventilation in the tortoise Testudo graeca Linne. Journal of Experimental Biology 47:1–20.CrossRefGoogle ScholarPubMed
Gatesy, S. M., and Dial, K. P. 1993. Tail muscle activity patterns in walking and flying pigeons (Columba livia). Journal of Experimental Biology 176:55–76.CrossRefGoogle Scholar
Gaunt, A. S., and Gans, C. 1969. Mechanics of respiration in the Snapping Turtle, Chelydra serpentina (Linne). Journal of Morphology 128:195–228.CrossRefGoogle Scholar
Gauthier, J. A., Kluge, A. G., and Rowe, T. 1988. The early evolution of Amniota. Pp. 103–155in Benton, M. J., ed. The phylogeny and classification of the tetrapods, Vol. 1. Clarendon, Oxford.Google Scholar
Gilmore, C. W. 1914. Osteology of the armored dinosaurs in the United States National Museum, with special reference to the genus Stegosaurus. Bulletin of the United States National Museum 89:1–136.Google Scholar
Hedges, S. B., and Poling, L. L. 1999. A molecular phylogeny of reptiles. Science 283:998–1000.CrossRefGoogle ScholarPubMed
Hou, L., Martin, L. D., Zhou, Z., and Feduccia, A. 1996. Early adaptive radiation of birds: evidence from fossils from northeastern China. Science 274:1164–1167.CrossRefGoogle ScholarPubMed
Jensen, J. A., and Padian, K. 1989. Small pterosaurs and dinosaurs from the Uncompahgre fauna (Brushy Basin Member, Morrison Formation:? Tithonian), Late Jurassic, Western Colorado. Journal of Paleontology 63:364–373.CrossRefGoogle Scholar
Ji, Q., Chiappe, L. M., and Ji, S. 1999. A new late Mesozoic confuciusornithid bird from China. Journal of Vertebrate Paleontology 19:1–7.Google Scholar
Kadano, H., Okada, T., and Ono, K. 1963. Electromyographic studies on the respiratory muscles of the chicken. Poultry Science 42:121–128.CrossRefGoogle Scholar
Lambe, L. M. 1917. The Cretaceous carnivorous dinosaur Gorgosaurus. Geological Survey of Canada Memoir 100:1–84.Google Scholar
Liem, K. F. 1985. Ventilation. Pp. 185–209in Hildebrand, M., Bramble, D. M., Liem, K. F., and Wake, D. B., eds. Functional vertebrate morphology. Harvard University Press Cambridge.CrossRefGoogle Scholar
Marsh, O. C. 1891. The gigantic Ceratopsidae, or horned dinosaurs, of North America. American Journal of Sciences 41:167–178.CrossRefGoogle Scholar
Nash, D. 1968. A crocodile from the Upper Triassic of Lesotho. Journal of Zoology 156:163–179.CrossRefGoogle Scholar
Nishi, S. 1938. Muskeln des Rumpfes. Pp. 351–442in Bolk, L., Goppert, E., Kallius, E., and Lubosch, W., eds. Handbuch der vergleichenden Anatomie der Wirbeltiere. Urban und Schwarzenberg, Berlin.Google Scholar
Norell, M. A., and Makovicky, P. J. 1997. Important features of the dromaeosaur skeleton: information from a new specimen. American Museum Novitates 3215:1–28.Google Scholar
Norman, D. B., and Weishample, D. B. 1990. Iguanodontidae and related orhithopods. Pp. 510–533in Weishampel, et al. 1990.Google Scholar
Ostrom, J. H. 1969. Osteology of Deinonychus antirrhopus, an unusual theropod from the Lower Cretaceous of Montana. Pea-body Museum of Natural History Bulletin 30:1–165.Google Scholar
Ostrom, J. H. 1976. Archaeopteryx and the origin of birds. Biological Journal of the Linnean Society 8:91–182.CrossRefGoogle Scholar
Ostrom, J. H., and McIntosh, J. S. 1966. Marsh's dinosaurs. Yale University Press, New Haven, Conn.Google Scholar
Owerkowicz, T., Farmer, C. G., Hicks, J. W., and Brainerd, E. L. 1999. Contribution of gular pumping to lung ventilation in monitor lizards. Science 284:1661–1663.CrossRefGoogle ScholarPubMed
Padian, K. 1983. A functional analysis of flying and walking in pterosaurs. Paleobiology 9:218–239.CrossRefGoogle Scholar
Padian, K., and Chiappe, L. M. 1998. The origin and early evolution of birds. Biological Review 73:1–42.CrossRefGoogle Scholar
Parrish, M. J. 1987. The origin of crocodilian locomotion. Paleobiology 13:396–414.CrossRefGoogle Scholar
Parrish, M. J. 1991. A new specimen of an early crocodylomorph (cf. Sphenosuchus sp.) from the Upper Triassic Chinle Formation of Petrified Forest National Park, Arizona. Journal of Vertebrate Paleontology 11:198–212.CrossRefGoogle Scholar
Perry, S. F. 1983. Reptilian lungs, functional anatomy and evolution. Advances in Anatomy, Embryology, and Cell Biology 79:1–81.CrossRefGoogle ScholarPubMed
Romer, A. S. 1923a. The ilium in dinosaurs and birds. Bulletin of the American Museum of Natural History 48:141–145.Google Scholar
Romer, A. S. 1923b. The pelvic musculature of saurischian dinosaurs. Bulletin of the American Museum of Natural History 48:605–617.Google Scholar
Romer, A. S. 1923c. Crocodilian pelvic muscles and their avian and reptilian homologues. Bulletin of the American Museum of Natural History 48:533–552.Google Scholar
Romer, A. S. 1927. The pelvic musculature of ornithischian dinosaurs. Acta Zoologica 8:225–275.CrossRefGoogle Scholar
Romer, A. S. 1956. The osteology of the Reptilia. University of Chicago Press, Chicago.Google Scholar
Ruben, J. A., Del Sasso, C., Geist, N. R., Hillenius, W. J., Jones, T. D., and Signore, M. 1999. Pulmonary function and metabolic physiology of theropod dinosaurs. Science 283:514–516.CrossRefGoogle ScholarPubMed
Santa Luca, A. P. 1984. Postcranial remains of Fabrosauridae (Reptilia: Ornithischia) from Stormberg of Southern Africa. Palaeontologia Africana 25:151–180.Google Scholar
Sereno, P. C. 1986. Phylogeny of the bird-hipped dinosaurs (Order Ornithischia). National Geographic Research 2:234–256.Google Scholar
Sereno, P. C. 1990. Psittacosauridae. Pp. 579–592in Weishampel, et al. 1990.Google Scholar
Sereno, P. C. 1991. Basal archosaurs: phylogenetic relationships and functional implications. Society of Vertebrate Paleontology Memoir 2. Journal of Vertebrate Paleontology 11:1–53.CrossRefGoogle Scholar
Sereno, P. C., and Chenggang, R. 1992. Early evolution of avian flight and perching: new evidence from the Lower Cretaceous of China. Science 255:845–848.CrossRefGoogle ScholarPubMed
Sereno, P. C., and Wild, R. 1992. Procompsognathus: theropod, “thecodont” or both? Journal of Vertebrate Paleontology 12:435–458.CrossRefGoogle Scholar
Taquet, P. 1976. Géologie et paléontologie du gisement de Gadoufaoua (Aptien du Niger). Cahiers de Paléontologie, C.N.R.S., Paris.Google Scholar
Thulborn, R. A. 1972. The post-cranial skeleton of the Triassic ornithischian dinosaur Fabrosaurus australis. Palaeontology 15:29–60.Google Scholar
Walker, A. D. 1970. A revision of the Jurassic reptile Hallopus victor (Marsh), with remarks on the classification of crocodiles. Philosophical Transactions of the Royal Society of London B 257:323–371.Google Scholar
Walker, A. D. 1977. Evolution of the pelvis in birds and dinosaurs. Pp. 319–357in Andrews, S. M., Miles, R. S. and Walker, A. D., eds. Problems in vertebrate evolution. Academic Press, New York.Google Scholar
Weishampel, D. B., and Horner, J. R. 1990. Hadrosauridae. Pp. 534–561in Weishampel, et al. 1990.Google Scholar
Weishampel, D. B., and Witmer, L. M. 1990a. Lesothosaurus, Pisanosaurus, and Technosaurus. Pp. 416–425in Weishampel, et al. 1990.Google Scholar
Weishampel, D. B. 1990b. Heterodontosauridae. Pp. 486–497in Weishampel, et al. 1990.Google Scholar
Weishampel, D. B., Dodson, P., and Osmolska, H., eds. 1990. The Dinosauria. University of California Press, Berkeley.Google Scholar
Wellnhofer, P. 1978. Handbuch der Paläoherpetologie, Teil 19. Gustav Fischer, Stuttgart.Google Scholar
Wellnhofer, P. 1991. The illustrated encyclopedia of pterosaurs. Crescent Books, New York.Google Scholar
Wellnhofer, P. 1992. A new specimen of Archaeopteryx from the Solnhofen Limestone. Pp. 3–23in Campbell, K. E. ed. Papers in avian paleontology. Natural History Museum of Los Angeles, Los Angeles.Google Scholar
Wu, X. C., Brinkman, D. B., and Lu, J. C. 1994. A new species of Shantungosuchus from the Lower Cretaceous of Inner Mongolia (China), with comments on S. chuhsienensis Young, 1961 and phylogenetic position of the genus. Journal of Vertebrate Paleontology 14:210–229.CrossRefGoogle Scholar
Young, I. S., Alexander, R. McN., Woakes, A. J., Butler, P. J., and Anderson, L. 1992. The synchronization of ventilation and locomotion in horses (Equus). Journal of Experimental Biology 166:19–31.CrossRefGoogle ScholarPubMed
Zimmer, K. 1935. Beitrage zur Mechanik der Atmung bei den Vogeln in Stand und Flug. Zoologica 33:1–69.Google Scholar