Abstract
Birds are unique among living vertebrates in possessing pneumaticity of the postcranial skeleton, with invasion of bone by the pulmonary air-sac system1,2,3,4. The avian respiratory system includes high-compliance air sacs that ventilate a dorsally fixed, non-expanding parabronchial lung2,3,5,6. Caudally positioned abdominal and thoracic air sacs are critical components of the avian aspiration pump, facilitating flow-through ventilation of the lung and near-constant airflow during both inspiration and expiration, highlighting a design optimized for efficient gas exchange2,5,6,7,8. Postcranial skeletal pneumaticity has also been reported in numerous extinct archosaurs including non-avian theropod dinosaurs and Archaeopteryx9,10,11,12. However, the relationship between osseous pneumaticity and the evolution of the avian respiratory apparatus has long remained ambiguous. Here we report, on the basis of a comparative analysis of region-specific pneumaticity with extant birds, evidence for cervical and abdominal air-sac systems in non-avian theropods, along with thoracic skeletal prerequisites of an avian-style aspiration pump. The early acquisition of this system among theropods is demonstrated by examination of an exceptional new specimen of Majungatholus atopus, documenting these features in a taxon only distantly related to birds. Taken together, these specializations imply the existence of the basic avian pulmonary Bauplan in basal neotheropods, indicating that flow-through ventilation of the lung is not restricted to birds but is probably a general theropod characteristic.
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References
Hunter, J. An account of certain receptacles of air, in birds, which communicate with the lungs, and are lodged both among the fleshy parts and in the hollow bones of those animals. Phil. Trans. R. Soc. Lond. 64, 205–213 (1774)
Duncker, H.-R. The lung air sac system of birds. Adv. Anat. Embryol. Cell Biol. 45, 1–171 (1971)
Perry, S. F. Reptilian lungs: functional anatomy and evolution. Adv. Anat. Embryol. Cell Biol. 79, 1–81 (1983)
O'Connor, P. M. Pulmonary pneumaticity in the postcranial skeleton of extant Aves: a case study examining Anseriformes. J. Morphol. 261, 141–161 (2004)
Maina, J. N. Comparative respiratory morphology: themes and principles in the design and construction of the gas exchangers. Anat. Rec. 261, 25–44 (2000)
Duncker, H.-R. in Complex Organismal Functions: Integration and Evolution in Vertebrates (eds Wake, D. B. & Roth, G.) 147–169 (Wiley, Hoboken, New Jersey, 1989)
Brackenbury, J. H. Airflow dynamics in the avian lung as determined by direct and indirect methods. Respir. Physiol. 13, 319–329 (1971)
Kuethe, D. O. Fluid mechanical valving of air flow in bird lungs. J. Exp. Biol. 136, 1–12 (1988)
Britt, B. B. Pneumatic Postcranial Bones in Dinosaurs and Other Archosaurs. Dissertation, Univ. Calgary (1993)
Britt, B. B., Makovicky, P. J., Gauthier, J. & Bonde, N. Postcranial pneumatization in Archaeopteryx. Nature 395, 374–376 (1998)
Forster, C. A., Sampson, S. D., Chiappe, L. M. & Krause, D. W. The theropod ancestry of birds: new evidence from the Late Cretaceous of Madagascar. Science 279, 1915–1919 (1998)
O'Connor, P. M. Pulmonary Pneumaticity in Extant Birds and Extinct Archosaurs. Dissertation, Stony Brook Univ. (2003)
Sereno, P. C. The evolution of dinosaurs. Science 284, 2137–2147 (1999)
Ruben, J. A., Jones, T. D., Geist, N. R. & Hillenius, W. J. Lung structure and ventilation in theropod dinosaurs and early birds. Science 278, 1267–1270 (1997)
Ruben, J. A., Dal Sasso, C., Geist, N. R., Jones, T. D. & Signore, M. Pulmonary function and metabolic physiology of theropod dinosaurs. Science 283, 514–516 (1998)
Ruben, J. A., Jones, T. D. & Geist, N. R. Respiration and reproductive paleophysiology of dinosaurs and early birds. Physiol. Biochem. Zool. 72, 141–164 (2003)
Chinsamy, A. & Hillenius, W. J. in The Dinosauria (eds Weishampel, D. B., Dodson, P. & Osmólska, H.) 643–659 (Univ. California Press, Berkeley, 2004)
Perry, S. F. in New Perspectives on the Origin and Early Evolution of Birds (eds Gauthier, J. & Gall, L. F.) 429–441 (Spec. Pub. Peabody Mus. Nat. Hist., New Haven, 2001)
Paul, G. S. in Perspectives on the Origin and Early Evolution of Birds (eds Gauthier, J. & Gall, L. F.) 464–482 (Spec. Pub. Peabody Mus. Nat. Hist., New Haven, 2001)
Cover, M. S. Gross and microscopic anatomy of the respiratory system of the turkey: III. The air sacs. Am. J. Vet. Res. 14, 239–245 (1953)
Sampson, S. D. et al. Predatory dinosaur remains from Madagascar: Implications for the Cretaceous biogeography of Gondwana. Science 280, 1048–1051 (1998)
Zimmer, K. Beiträge zur Mechanik der Atmung bei den Vögeln in Stand und Flug. Zoologica 33, 1–69 (1935)
Jenkins, F. A. Jr, Dial, K. P. & Goslow, G. E. Jr A cineradiographic analysis of bird flight: the wishbone in starlings is a spring. Science 241, 1495–1498 (1988)
Claessens, L. P. A. M. Dinosaur gastralia; origin, morphology, and function. J. Vertebr. Paleontol. 24, 89–106 (2004)
Wedel, M. Vertebral pneumaticity, air sacs, and the physiology of sauropod dinosaurs. Paleobiology 29, 243–255 (2003)
Xu, X. et al. Basal tyrannosauroids from China and evidence of protofeathers in tyrannosauroids. Nature 431, 680–684 (2004)
Padian, K., de Ricqles, A. J. & Horner, J. R. Dinosaurian growth rates and bird origins. Nature 412, 405–408 (2001)
Ericson, G. M., Curry Rogers, K. & Yerby, S. A. Dinosaurian growth patterns and rapid avian growth rates. Nature 412, 429–433 (2001)
Norell, M. A., Clark, J. M., Chiappe, L. M. & Dashzeveg, D. A nesting dinosaur. Nature 378, 774–776 (1995)
Xu, X. & Norell, M. A. A new troodontid dinosaur from China with avian-like sleeping posture. Nature 431, 838–841 (2004)
Acknowledgements
We thank M. T. Carrano, F. A. Jenkins, D. W. Krause, K. Padian, N. J. Stevens and C. S. Sullivan for comments on the manuscript; L. M. Witmer, H.-R. Duncker, A. A. Biewener, B. B. Britt, A. W. Crompton, C. A. Forster, S. F. Perry, S. D. Sampson and M. J. Wedel for discussions; the Université d'Antananarivo for permission to study UA 8678; H.-R. Duncker for access to avian preparations; R. Main and M. Daley for providing birds for cineradiographic studies; A. Milner, D. Unwin, J. Flynn, W. Simpson, P. Sereno, B. Livezey, X. Luo, M. Norell and K. Padian for providing access to specimens in their care; and R. Ridgely for assistance with Figs 1b and 4. Funding was provided by the NSF Graduate Research Fellowship Program, the Society for Integrative and Comparative Biology, an Estes Award from the Society of Vertebrate Paleontology, and the Jurassic Foundation to P.M.O; an NSF Doctoral Dissertation Improvement Grant and Harvard University to L.C.; and the S. & D. Welles Research Fund to P.M.O. and L.C.
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Supplementary Notes
This files contains Supplementary Materials, Supplementary Methods, Supplementary Data and Supplementary Table S1 and S2. The legend for Supplementary Video S1 is also included. (DOC 320 kb)
Supplementary Video S1
Cineradiographic (X-ray film) clip of a 0.48 kg Tinamou (Nothoprocta perdicaria), demonstrating the greater excursion of the caudal margin of the sternum and posterior ventral body wall upon inspiration. Experimental subject shot in lateral projection at 70 kV and 220mA, X-ray positive (head is to the left side of image). (MOV 2691 kb)
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O'Connor, P., Claessens, L. Basic avian pulmonary design and flow-through ventilation in non-avian theropod dinosaurs. Nature 436, 253–256 (2005). https://doi.org/10.1038/nature03716
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DOI: https://doi.org/10.1038/nature03716
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