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Basic avian pulmonary design and flow-through ventilation in non-avian theropod dinosaurs

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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Figure 1: Pulmonary air-sac system in a bird.
Figure 2: Proposed relationships of theropod taxa used in study (modified from references 11 and 13).
Figure 3: Vertebral pneumaticity in avian and non-avian theropods.
Figure 4: Reconstruction of pulmonary air-sac system in Majungatholus atopus (based on UA 8678/FMNH PR 2278/2100 (ref.21)).

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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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Correspondence to Patrick M. O'Connor.

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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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