Lung structure and ventilation in theropod dinosaurs and early birds

Science

Volumn 278, Issue 5341, 1997, Pages 1267-1270

  Ruben, John A ^a   Jones, Terry D ^a   Geist, Nicholas R ^a   Hillenius, W Jaap ^b  

^a OREGON STATE UNIVERSITY   (United States)

^b Department of Teacher Education and Department of Sociology and Anthropology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIRD; DINOSAUR; LUNG; THEROPOD;

ARTICLE; DIAPHRAGM MUSCLE; FOSSIL; LUNG GAS EXCHANGE; LUNG VENTILATION; MUSCLE CONTRACTILITY; NONHUMAN; PHYSICAL ANTHROPOLOGY; PRIORITY JOURNAL; RESPIRATORY AIRFLOW;

EID: 0030666688     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.278.5341.1267     Document Type: Article

References (32)

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8. 2 exchange are limited primarily by hydrostatic pressure constraints on pulmonary blood flow (19). Thus, in order for a modern reptile (the active lizard Varanus, for example) with a bellowslike septate lung to attain endothermlike rates of maximal oxygen consumption {about 10 times those of active ectotherms [A. F. Bennett and J. A. Ruben, Science 206, 649 (1979)]}, maximal pulmonary blood flow have to be accelerated by about 10 times, or about 5 times if blood oxygen carrying capacity were to approximate that in many mammals {20 volume % rather than the actual 10 volume % in modern lizards [A. F. Bennett, J. Comp. Biochem. Physiol. 46, 673 (1973)]}. In either case, because pulmonary hydrostatic pressure is largely a product of blood flow rate, pulmonary capillary pressures would be far in excess of dangerous levels [≈ 45 millimeters of mercury (mmHg)], approaching at least 100 mmHg if not far higher {based on the observed similarity of resting mean pulmonary arterial pressure in mammals and normal Varanus (about 20 mm Hg at a body temperature Of 35°C) [A. Ischimatsu, J. W. Hicks, N. Heisler, Respir. Physiol. 71, 83 (1988)] and the assumption that (i) pulmonary capillary recruitment is maximal in exercising tetrapods and (ii) that mean arterial pressure during intense exercise in normal Varanus is actually broadly equivalent to that in mammals (about 35 mm Hg) (19)}. Hypothetically, these pressure constraints on the bellowslike septate lung might be overcome either by increasing the magnitude of lung vascularization (thus decreasing pulmonary capillary resistance to blood flow) or by increasing total lung volume by a factor of at least 5. However, a substantial increase in lung vascularization would necessarily restrict the volume of nonvascularized portions of the lung, thereby reducing capacity for lung ventilation. Alternately, an increase by a factor of 5 in total lung volume would leave little, if any, space in the visceral cavity for organs other than the lung.
9. P. Scheid and J. Piiper, in Form and Function in Birds, A. S. King and J. McLelland, Eds. (Academic Press, New York, 1989), vol. 4, pp. 369-391.
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12. K. Schmidt-Neilsen, Sci. Am. 225, 72 (December 1971); M. R. Fedde, in Bird Respiration, T. J. Seller, Ed. (CRC Press, Boca Raton, FL, 1987), vol. 1, pp. 3-37; J. H. Brackenbury, ibid., pp. 39-69.
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18. Rather than representing primitive archosaurian structures, it is probable that the hepatic-piston diaphragm systems in crocodilians and theropods are convergently derived. Pelvic anatomy in early "protodinosaurs" such as Lagosuchus, as well as in all ornithischian dinosaurs, shows no evidence of the pubis having served as a site of origin for similar diaphragmatic musculature (pubic bones are comparatively less well developed, and in ornithischian dinosaurs a pubic symphysis is absent). See R. Carroll, Vertebrate Paleontology and Evolution (Freeman, New York, 1988).
19. G. Heilmann, Origin of Birds (Appleton, New York, 1927).
20. J. J. Baumel, personal communication; _, J. A. Wilson, D. R. Bergren, J. Exp. Biol. 151, 263 (1990).
21. J. J. Baumel, personal communication; _, J. A. Wilson, D. R. Bergren, J. Exp. Biol. 151, 263 (1990).
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23. A few theropod dinosaurs [for example, Segnosaurus and Adasaurus (9)] possess a moderately opisthopubic pelvis, but the distal pubis remains ventrally situated and the degree of dorsal rotation of the pubis does not approximate that in Archaeopteryx and the enantiornithine birds.
24. The position of the pubis in Archaeopteryx has occasionally been interpreted as having been vertical rather than severely opisthopubic [for example, J. H. Ostrom, Biol. J. Linn. Soc. London 8, 91 (1976)]. However, the overall similarity of the pelvis of Archaeopteryx to those of the enantiornithine birds, especially the presence of the hypopubic cup, as well as the morphology of the London and Berlin Archaeopteryx specimens, offer support for our interpretation of the pelvic structure of these early birds [L. D. Martin, in Origin of the Higher Groups of Tetrapods, H. P. Schultze and L. Trueb, Eds. (Cornell Univ. Press, Ithaca, NY, 1991), pp. 485-540.
25. The position of the pubis in Archaeopteryx has occasionally been interpreted as having been vertical rather than severely opisthopubic [for example, J. H. Ostrom, Biol. J. Linn. Soc. London 8, 91 (1976)]. However, the overall similarity of the pelvis of Archaeopteryx to those of the enantiornithine birds, especially the presence of the hypopubic cup, as well as the morphology of the London and Berlin Archaeopteryx specimens, offer support for our interpretation of the pelvic structure of these early birds [L. D. Martin, in Origin of the Higher Groups of Tetrapods, H. P. Schultze and L. Trueb, Eds. (Cornell Univ. Press, Ithaca, NY, 1991), pp. 485-540.
26. D.S. Peters and E. Görgner, in Proceedings of the II International Symposium of Avian Paleontology, K. Campbell, Ed. (Los Angeles Museum of Natural History Press, Los Angeles, CA, 1992), pp. 29-37.
27. However, against Peters and Görgner, see A. Feduccia, Science 259, 790 (1993).
28. J. B. West and O. Mathieu-Costello, Eur. J. Appl. Physicl. 70, 99 (1995).
29. F. E. Novas, J. Vertebr. Paleontol. 13, 400 (1993).
30. A. S. Romer, Bull. Am. Mus. Nat. Hist. 48, 605 (1923).
31. Figure 6B was modified from (13) and A. Feduccia, The Origin and Evolution of Birds (Yale Univ. Press, New Haven, CT, 1996).
32. We thank J. Baumel, A. Bennett, P. Dodson, J. Farlow, A. Feduccia, J. Hicks, L. Martin, S. Perry, L. Witmer, and G. Zug for invaluable discussions and constructive criticisms. We offer special thanks to D. Bubier and D. Wolberg (Philadelphia Academy of Sciences) for Sinosauropteryx photos. R. Elsie provided alligator specimens. Figures 3, 4, and 6 were drawn by R. Jones. This work was supported by NSF grant IBN-9420290 to W.J.H. and J.A.R.