Hostname: page-component-76fb5796d-r6qrq Total loading time: 0 Render date: 2024-04-25T19:37:38.269Z Has data issue: false hasContentIssue false

Vertebral pneumaticity, air sacs, and the physiology of sauropod dinosaurs

Published online by Cambridge University Press:  08 April 2016

Mathew J. Wedel*
Affiliation:
Oklahoma Museum of Natural History and Department of Zoology, University of Oklahoma, Norman, Oklahoma 73072

Abstract

The vertebrae of sauropod dinosaurs are characterized by complex architecture involving laminae, fossae, and internal chambers of various shapes and sizes. These structures are interpreted as osteological correlates of a system of air sacs and pneumatic diverticula similar to that of birds. In extant birds, diverticula of the cervical air sacs pneumatize the cervical and anterior thoracic vertebrae. Diverticula of the abdominal air sacs pneumatize the posterior thoracic vertebrae and synsacrum later in ontogeny. This ontogenetic sequence in birds parallels the evolution of vertebral pneumaticity in sauropods. In basal sauropods, only the presacral vertebrae were pneumatized, presumably by diverticula of cervical air sacs similar to those of birds. The sacrum was also pneumatized in most neosauropods, and pneumatization of the proximal caudal vertebrae was achieved independently in Diplodocidae and Titanosauria. Pneumatization of the sacral and caudal vertebrae in neosauropods may indicate the presence of abdominal air sacs. Air sacs and skeletal pneumaticity probably facilitated the evolution of extremely long necks in some sauropod lineages by overcoming respiratory dead space and reducing mass. In addition, pulmonary air sacs may have conveyed to sauropods some of the respiratory and thermoregulatory advantages enjoyed by birds, a possibility that is consistent with the observed rapid growth rates of sauropods.

Type
Articles
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.)

Footnotes

*

Present address: University of California Museum of Paleontology and Department of Integrative Biology, 1101 Valley Life Sciences Building, Berkeley, California 94720-4780. E-mail: sauropod@socrates.berkeley.edu

References

Literature Cited

Bakker, R. T. 1972. Anatomical and ecological evidence of endothermy in dinosaurs. Nature 229:172174.10.1038/229172a0Google Scholar
Bernstein, M. H. 1976. Ventilation and respiratory evaporation in the flying crow, Corvus ossifragus. Respiration Physiology 26:371382.10.1016/0034-5687(76)90007-4Google Scholar
Bezuidenhout, A. J., Groenewald, H. B., and Soley, J. T. 1999. An anatomical study of the respiratory air sacs in ostriches. Onderstepoort Journal of Veterinary Research 66:317325.Google Scholar
Bossert, D. C., Chabreck, R. H., and Wright, V. L. 2000. Growth of farm-released and wild alligators in a Louisiana freshwater marsh. Pp. 419425in Grigg, G. C., Seebacher, F., and Franklin, C. E., eds. Crocodilian biology and evolution. Surrey Beatty, Chipping Norton, Australia.Google Scholar
Bouverot, P., and Dejours, P. 1971. Pathway of respired gas in the air sacs-lung apparatus of fowl and ducks. Respiration Physiology 13:330342.10.1016/0034-5687(71)90037-5Google Scholar
Brackenbury, J. H. 1971. Airflow dynamics in the avian lung as determined by direct and indirect methods. Respiration Physiology 13:319329.Google Scholar
Bremer, J. L. 1940. The pneumatization of the humerus in the common fowl and the associated activity of theelin. Anatomical Record 77:197211.10.1002/ar.1090770209Google Scholar
Britt, B. B. 1997. Postcranial pneumaticity. Pp. 590593in Currie, P. J. and Padian, K., eds. The encyclopedia of dinosaurs. Academic Press, San Diego.Google Scholar
Britt, B. B., Makovicky, P. J., Gauthier, J., and Bonde, N. 1998. Postcranial pneumatization in Archaeopteryx. Nature 395:374376.10.1038/26469Google Scholar
Christiansen, P., and Bonde, N. 2000. Axial and appendicular pneumaticity in Archaeopteryx. Proceedings of the Royal Society of London B 267:25012505.Google Scholar
Claessens, L. P. A. M., Perry, S. F., and Currie, P. J. 1998. Using comparative anatomy to reconstruct theropod respiration. Journal of Vertebrate Paleontology 18(Suppl. to No. 3):34A.Google Scholar
Cope, E. D. 1877. On a gigantic saurian from the Dakota Epoch of Colorado. Palaeontological Bulletin 25:510.Google Scholar
Cover, M. S. 1953. Gross and microscopic anatomy of the respiratory system of the turkey. III. The air sacs. American Journal of Veterinary Research 14:239245.Google Scholar
Curry, K. A. 1999. Ontogenetic histology of Apatosaurus (Dinosauria: Sauropoda): new insights on growth rates and longevity. Journal of Vertebrate Paleontology 19:654665.Google Scholar
Daniels, C. B., and Pratt, J. 1992. Breathing in long-necked dinosaurs: did the sauropods have bird lungs? Comparative Biochemistry and Physiology 101A:4346.10.1016/0300-9629(92)90625-ZGoogle Scholar
Dawson, W. R., and Whittow, G. C. 2000. Regulation of body temperature. Pp. 343390in Whittow, C. G., ed. Sturkie's avian physiology, 5th ed. Academic Press, New York.10.1016/B978-012747605-6/50015-8Google Scholar
Dodson, P. 1990. Sauropod paleoecology. Pp. 402407in Weishampel, D. B., Dodson, P., and Osmolska, H., eds. The Dinosauria. University of California Press, Berkeley.Google Scholar
Duncker, H.-R. 1971. The lung air sac system of birds. Advances in Anatomy, Embryology, and Cell Biology 45:1171.Google Scholar
Duncker, H.-R. 1972. Structure of avian lungs. Respiration Physiology 14:4463.10.1016/0034-5687(72)90016-3Google Scholar
Duncker, H.-R. 1974. Structure of the avian respiratory tract. Respiration Physiology 22:119.10.1016/0034-5687(74)90044-9Google Scholar
Erickson, G. M., Curry Rogers, K., and Yerby, S. A. 2001. Dinosaurian growth patterns and rapid avian growth rates. Nature 412:429433.10.1038/35086558Google Scholar
Fowler, M. E. 1991. Comparative clinical anatomy of ratites. Journal of Zoo and Wildlife Medicine 22:204227.Google Scholar
Gale, H. H. 1997. Breathing through a long neck: sauropod lung ventilation. Journal of Vertebrate Paleontology 17(Suppl. to No. 3):48A.Google Scholar
Gale, H. H. 1998. Lung ventilation costs of short-necked dinosaurs. Journal of Vertebrate Paleontology 18(Suppl. to No. 3):44A.Google Scholar
Gauthier, J. A. 1986. Saurischian monophyly and the origin of birds. California Academy of Sciences Memoir 8:155.Google Scholar
Gier, H. T. 1952. The air sacs of the loon. Auk 69:4049.10.2307/4081291Google Scholar
Gilmore, C. W. 1925. A nearly complete articulated skeleton of Camarasaurus, a saurischian dinosaur from the Dinosaur National Monument, Utah. Memoirs of the Carnegie Museum 10:347384.Google Scholar
Gower, D. J. 2001. Possible postcranial pneumaticity in the last common ancestor of birds and crocodilians: evidence from Erythrosuchus and other Mesozoic archosaurs. Naturwissenschaften 88:119122.10.1007/s001140100206Google Scholar
Hatcher, J. B. 1901. Diplodocus (Marsh): its osteology, taxonomy, and probable habits, with a restoration of the skeleton. Memoirs of the Carnegie Museum 1:163.Google Scholar
Henderson, D. M. 1999. Estimating the masses and centers of mass of extinct animals by 3-D mathematical slicing. Paleobiology 25:88106.Google Scholar
Hengst, R., and Rigby, J. K. Jr. 1994. Apatosaurus as a means of understanding dinosaur respiration. In Rosenberg, G. D. and Wolberg, D. L., eds. DinoFest. Paleontological Society Special Publication 7:199211. University of Tennessee Press, Knoxville.Google Scholar
Hogg, D. A. 1984a. The distribution of pneumatisation in the skeleton of the adult domestic fowl. Journal of Anatomy 138:617629.Google Scholar
Hogg, D. A. 1984b. The development of pneumatisation in the postcranial skeleton of the domestic fowl. Journal of Anatomy 139:105113.Google Scholar
Hutchinson, J. 2001. The evolution of pelvic osteology and soft tissues on the line to extant birds (Neornithes). Zoological Journal of the Linnean Society 131:123168.Google Scholar
Jain, S. L., Kutty, T. S., Roy-Chowdhury, T. K., and Chatterjee, S. 1979. Some characteristics of Barapasaurus tagorei, a sauropod dinosaur from the Lower Jurassic of Deccan, India. Proceedings of the IV International Gondwana Symposium, Calcutta 1:204216.Google Scholar
Janensch, W. 1947. Pneumatizitat bei Wirbeln von Sauropoden und anderen Saurischien. Palaeontographica 3(Suppl. 7):125.Google Scholar
King, A. S. 1966. Structural and functional aspects of the avian lungs and air sacs. International Review of General and Experimental Zoology 2:171267.Google Scholar
King, A. S. 1975. Aves respiratory system. Pp. 18831918in Getty, R., ed. Sisson and Grossman's the anatomy of the domestic animals, 5th ed., Vol. 2.Google Scholar
Saunders, W. B., Philadelphia. King, A. S., and Kelly, D. F. 1956. The aerated bones of Gallus domesticus: the fifth thoracic vertebra and sternal ribs. British Veterinary Journal 112:279283.Google Scholar
Kuethe, D. O. 1988. Fluid mechanical valving of air flow in bird lungs. Journal of Experimental Biology 136:112.Google Scholar
Marsh, O. C. 1877. Notice of new dinosaurian reptiles from the Jurassic Formation. American Journal of Science 14:514516.Google Scholar
Müller, B. 1907. The air-sacs of the pigeon. Smithsonian Miscellaneous Collections 50:365420.Google Scholar
Norman, D. 1985. The illustrated encyclopedia of dinosaurs. Crescent Books, New York.Google Scholar
Osborn, H. F. 1899. A skeleton of Diplodocus. Memoirs of the American Museum of Natural History 1:191214.Google Scholar
Padian, K. 2001. The false issues of bird origins: an historiographic perspective. Pp. 485499in Gauthier, J. and Gall, L. F., eds. New perspectives on the origin and early evolution of birds. Yale Peabody Museum, New Haven, Conn.Google Scholar
Padian, K., de Ricqlès, A. J., and Horner, J. R. 2001. Dinosaurian growth rates and bird origins. Nature 412:405408.10.1038/35086500Google Scholar
Paladino, F. V., Spotila, J. R., and Dodson, P. 1997. A blueprint for giants: modeling the physiology of large dinosaurs. Pp. 491504in Farlow, J. O. and Brett-Surman, M. K., eds. The complete dinosaur. Indiana University Press, Bloomington.Google Scholar
Paul, G. S. 1997. Dinosaur models: the good, the bad, and using them to estimate the mass of dinosaurs. Pp. 129154in Wolberg, D. L., Stump, E., and Rosenberg, G. D., eds. DinoFest International: Proceedings of a Symposium Sponsored by Arizona State University. Academy of Natural Sciences, Philadelphia.Google Scholar
Perry, S. F. 2001. Functional morphology of the reptilian and avian respiratory systems and its implications for theropod dinosaurs. Pp. 429441in Gauthier, J. and Gall, L. F., eds. New perspectives on the origin and early evolution of birds. Yale Peabody Museum, New Haven, Conn.Google Scholar
Perry, S. F., and Reuter, C. 1999. Hypothetical lung structure of Brachiosaurus (Dinosauria: Sauropoda) based on functional constraints. Geowissenschaftliche Reihe 2:7579.Google Scholar
Powell, F. L. 2000. Respiration. Pp. 233264in Whittow, C. G., ed. Sturkie's avian physiology, 5th ed. Academic Press, New York.10.1016/B978-012747605-6/50011-0Google Scholar
Powell, J. E. 1987. Morfología del esqueleto axial de los dinosaurios titanosauridos (Saurischia, Sauropoda) del Estado de Minas Gerais, Brasil. Anais do X Congreso Brasiliero de Paleontologia 155171.Google Scholar
Reid, R. E. H. 1997. Dinosaurian physiology: the case for “intermediate” dinosaurs. Pp. 449473in Farlow, J. O. and Brett-Surman, M. K., eds. The complete dinosaur. Indiana University Press, Bloomington.Google Scholar
Rimblot-Baly, F., de Ricqlès, A., and Zylberberg, L. 1995. Analyse paléohistologique d'une série de croissance partielle chez Lapparentosaurus madagascarensis (Jurassique Moyen): essai sur la dynamique de croissance d'un dinosaure sauropode. Annales de Paléontologie 81:4986.Google Scholar
Romer, A. S. 1966. Vertebrate paleontology, 3d ed. University of Chicago Press, Chicago.Google Scholar
Ruben, J. A., Dal Sasso, C., Geist, N. R., Hillenius, W. J., Jones, T. D., and Signore, M. 1999. Pulmonary function and metabolic physiology of theropod dinosaurs. Science 283:514516.Google Scholar
Sander, P. M. 2000. Longbone histology of the Tendaguru sauropods: implications for growth and biology. Paleobiology 26:466488.Google Scholar
Sanz, J. L., Powell, J. E., LeLoeuff, J., Martinez, R., and Pereda Superbiola, X. 1999. Sauropod remains from the Upper Cretaceous of Laño (north-central Spain). Titanosaur phylogenetic relationships. Estudios del Museo de Ciencias Naturales de Alava 14(Numero Especial l):235255.Google Scholar
Scheid, P., Slama, H., and Piiper, J. 1972. Mechanisms of unidirectional flow in parabronchi of avian lungs. Respiration Physiology 14:8395.10.1016/0034-5687(72)90019-9Google Scholar
Schmidt-Nielsen, K., Kanwisher, J., Lasiewski, R. C., Cohn, J. E., and Bretz, W. L. 1969. Temperature regulation and respiration in the ostrich. Condor 71:341352.Google Scholar
Seeley, H. G. 1870. On Ornithopsis, a gigantic animal of the pterodactyle kind from the Wealden. Annals of the Magazine of Natural History, series 4, 5:279283.Google Scholar
Sereno, P. C. 1991. Basal archosaurs: phylogenetic relationships and functional implications. Society of Vertebrate Paleontology Memoir 2.Google Scholar
Sereno, P. C. 1999. The evolution of dinosaurs. Science 284:21372147.Google Scholar
Sereno, P. C., Beck, A. L., Dutheil, D. B., Larsson, H. C. E., Lyon, G. H., Moussa, B., Sadleir, R. W., Sidor, C. A., Varricchio, D. J., Wilson, G. P., and Wilson, J. A. 1999. Cretaceous sauropods and the uneven rate of skeletal evolution among dinosaurs. Science 286:13421347.Google Scholar
Spotila, J. R., O'Connor, M. P., Dodson, P., and Paladino, F. V. 1991. Hot and cold running dinosaurs: body size, metabolism and migration. Modern Geology 16:203227.Google Scholar
Upchurch, P. 1998. The phylogenetic relationships of sauropod dinosaurs. Zoological Journal of the Linnean Society 124:43103.Google Scholar
Wedel, M. J. In press. The evolution of vertebral pneumaticity in sauropod dinosaurs. Journal of Vertebrate Paleontology.Google Scholar
Wedel, M. J., Cifelli, R. L., and Sanders, R. K. 2000. Osteology, paleobiology, and relationships of the sauropod dinosaur Sauroposeidon. Acta Palaeontologica Polonica 45:343388.Google Scholar
Wetherbee, D. K. 1951. Air-sacs in the English sparrow. Auk 68:242244.Google Scholar
Wilson, J. A. 1999. A nomenclature for vertebral laminae in sauropods and other saurischian dinosaurs. Journal of Vertebrate Paleontology 19:639653.Google Scholar
Wilson, J. A., and Sereno, P. C. 1998. Early evolution and higher-level phylogeny of sauropod dinosaurs. Society of Vertebrate Paleontology Memoir 5.Google Scholar
Witmer, L. M. 1987. The nature of the antorbital fossa of archosaurs: shifting the null hypothesis. Pp. 230235in Currie, P. J. and Koster, E. H., eds. Fourth symposium on Mesozoic terrestrial ecosystems, short papers. Occasional Paper No. 3, Royal Tyrrell Museum of Paleontology, Drumheller, Canada.Google Scholar
Witmer, L. M. 1997. The evolution of the antorbital cavity of archosaurs: a study in soft-tissue reconstruction in the fossil record with an analysis of the function of pneumaticity. Society of Vertebrate Paleontology Memoir 3.Google Scholar
Yates, A. M. 2001. A new look at Thecodontosaurus and the origin of sauropod dinosaurs. Journal of Vertebrate Paleontology 21(Suppl. to No. 3):116A.Google Scholar