Evolution of the dinosauriform respiratory apparatus: New evidence from the postcranial axial skeleton

Anatomical Record

Volumn 294, Issue 9, 2011, Pages 1532-1547

  Schachner, Emma R ^a,b   Farmer, C G ^b   McDonald, Andrew T ^a   Dodson, Peter ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF UTAH   (United States)

Author keywords

Archosauria; Dinosauriformes; Lung morphology; Postcranial skeleton; Respiration

Indexed keywords

AIR SAC; AIRFLOW; ARTICLE; BIRD; BRONCHUS; DINOSAUR; EVOLUTION; LUNG VENTILATION; MESOZOIC; NONHUMAN; PLEURA; PRIORITY JOURNAL; RESPIRATORY SYSTEM; RIB; SKELETON; THORAX WALL; VERTEBRATE;

ARCHOSAURIA; DINOSAURIFORMES; LUNG MORPHOLOGY; POSTCRANIAL SKELETON; RESPIRATION;

ANIMALS; BIOLOGICAL EVOLUTION; DINOSAURS; RESPIRATION; RESPIRATORY SYSTEM; RIBS; SPINE;

ANIMALIA; ARCHOSAURIA; AVES; CROCODYLIDAE (ALL CROCODILES); DINOSAURIA; SAURISCHIA; VERTEBRATA;

EID: 80051770953     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.21439     Document Type: Article

References (92)

1. Averianov AO, Voronkevich AV, Leshchinskiy SV, Fayngertz AV. 2006. A ceratopsian dinosaur Psittacosaurus sibiricus from the Early Cretaceous of West Siberia, Russia and its phylogenetic relationships. J Syst Palaeontol 4: 359-395.
2. Brochu CA. 2003. Osteology of Tyrannosaurus rex: insights from a nearly complete skeleton and high-resolution computed tomographic analysis of the skull. J Vertebr Paleontol Mem 7 22: 1-138.
3. Brown B. 1908. The Ankylosauridae, a new family of armored dinosaurs from the Upper Cretaceous. Bull Am Mus Nat Hist 24: 187-201.
4. Brown B, Schlaikjer EM. 1942. The skeleton of Leptoceratops with the description of a new species. Am Mus Novit 1169: 1-15.
5. Boggs DF, Jenkins FA, Dial KP. 1997. The effects of the wingbeat cycle on respiration in black-billed magpies (Pica pica). J Exp Biol 200: 1403-1412.
6. Butler RJ. 2005. The 'fabrosaurid' ornithischian dinosaurs of the Upper Elliot Formation (Lower Jurassic) of South Africa and Lesotho. Zool J Linn Soc Lond 145: 175-218.
7. Carpenter K. 2004. Redescription of Ankylosaurus magniventris Brown 1908 (Ankylosauridae) from the Upper Cretaceous of the Western Interior of North America. Can J Earth Sci 41: 961-986.
8. Carpenter K, Miles CA, Cloward K. 2001. New primitive stegosaur from the Morrison Formation, Wyoming. In: Carpenter K, editor. The armored dinosaurs. Bloomington, IN: Indiana University Press. p 55-75.
9. Carpenter K, Wilson Y. 2008. A new species of Camptosaurus (Ornithopoda: Dinosauria) from the Morrison Formation (Upper Jurassic) of Dinosaur National Monument, Utah, and a biomechanical analysis of its forelimb. Ann Carn Mus 76: 227-263.
10. Carrier DR. 1987. The evolution of locomotor stamina in tetrapods: circumventing a mechanical constraint. Paleobiology 13: 326-341.
11. Carrier DR, Farmer CG. 2000a. The integration of ventilation and locomotion in archosaurs. Am Zool 40: 87-100.
12. Carrier DR, Farmer CG. 2000b. The evolution of pelvic aspiration in archosaurs. Paleobiology 26: 271-293.
13. Claessens LPAM. 2004a. Archosaurian respiration and the pelvic girdle aspiration breathing of crocodyliforms. Proc R Soc Lond R B 271: 1461-1465.
14. Claessens LPAM. 2004b. Dinosaur gastralia: origin, morphology, and function. J Vertebr Paleontol 24: 89-106.
15. Claessens LPAM. 2009a. A cineradiographic study of lung ventilation in Alligator mississippiensis. J Exp Zool 311A: 563-585.
16. Claessens LPAM. 2009b. The skeletal kinematics of lung ventilation in three basal bird taxa (emu, tinamou, and guinea fowl). J Exp Zool 311A: 586-599.
17. Claessens LPAM, O'Connor PM, Unwin DM. 2009. Respiratory evolution facilitated the origin of pterosaur flight and aerial gigantism. PLoS One 4: 1-8.
18. Codd JR, Manning PL, Norell MA, Perry SF. 2008. Avian-like breathing mechanics in maniraptoran dinosaurs. Proc R Soc B 1233: 1-5.
19. Colbert EH. 1981. A primitive ornithischian dinosaur from the Kayenta Formation of Arizona. Mus Northern Ariz Press Bull Series 53: 1-61.
20. Cooper MR. 1981. The prosauropod dinosaur Massospondylus carinatus Owen from Zimbabwe: its biology, mode of life and phylogenetic significance. Occas Pap Natl Mus Rhod B Nat sci 6: 689-840.
21. Currie PJ, Zhao X-J. 1993. A new carnosaur (Dinosauria, Theropoda) from the Jurassic of Xinjiang, People's Republic of China. Can J Earth Sci 30: 2037-2081.
22. Duncker HR. 1971. The lung air sac system in birds. Adv Anat Embryol Cell Biol 45: 1-171.
23. Duncker HR. 1972. Structure of the avian lungs. Respir Physiol 14: 44-63.
24. Duncker HR. 1974. Structure of the avian respiratory tract. Respir Physiol 22: 1-19.
25. Dzik J. 2003. A beaked herbivorous archosaur with dinosaur affinities from the Early Late Triassic of Poland. J Vertebr Paleontol 23: 556-574.
26. Ezcurra MD. 2006. A review of the systematic position of the dinosauriform archosaur Eucoelophysis baldwini Sullivan and Lucas, 1999 from the Upper Triassic of New Mexico, USA. Geodiversitas 28: 649-684.
27. Farmer CG. 2006. On the origin of avian air sacs. Respir Physiol Neurobiol 154: 89-106.
28. Farmer CG. 2010. The provenance of alveolar and parabronchial lungs: insights from paleoecology and the discovery of cardiogenic, unidirectional airflow in the American alligator (Alligator mississippiensis). Physiol Biochem Zool 83: 1-15.
29. Farmer CG, Sanders K. 2010. Unidirectional airflow in the lungs of alligators. Science 327: 338-340.
30. Forster CA. 1990. The postcranial skeleton of the ornithopod dinosaur Tenontosaurus tilletti. J Vert Paleontol 10: 273-294.
31. Galton PM. 1974. The ornithischian dinosaur Hypsilophodon from the Wealden of the Isle of Wight. Bull Br Mus (Nat Hist) Geol 25: 1-152.
32. Galton PM. 1976. Prosauropod dinosaur (Reptilia: Saurischia) of North America. Postilla 169 25: 1-98.
33. Galton PM. 1990. A partial skeleton of the stegosaurian dinosaur Lexovisaurus from the uppermost Lower Callovian (Middle Jurassic) of Normandy, France. Geologica et Palaeontologica 24: 185-199.
34. Galton PM, Upchurch P. 2004. Prosauropoda. In: Weishampel D, Dodson P Osmólska H, editors. The Dinosauria, 2nd ed. Berkeley: University of California Press. p 232-258.
35. Gauthier JA. 1986. Saurischian monophyly and the origin of birds. In: Padian K, editor. The origin of birds and the evolution of flight. Memoirs of the California Academy of Sciences 8: 1-55.
36. Gier HT. 1952. The air sacs of the loon. The Auk 69: 40-49.
37. Gilmore CW. 1936. Osteology of Apatosaurus with special reference to specimens in the Carnegie museum. Mem Carnegie Mus 11: 175-299.
38. Hatcher JB. 1901. Diplodocus (Marsh): its osteology, taxonomy, and probable habits, with a restoration of the skeleton. Mem Carnegie Mus 1: 1-64.
39. Hatcher JB, Marsh OC, Lull RS. 1907. The Ceratopsia. U.S. Geol Surv Monogr 49: 1-300.
40. Hicks JW, Farmer CG. 1999. Gas exchange potential in reptilian lugs: implications for the dinosaur-avian connection. Respir Physiol 117: 73-83.
41. Holmes RB, Ryan MJ, Murray AM. 2005. Photographic atlas of the postcranial skeleton of the type specimen of Styracosaurus albertensis with additional isolated cranial elements from Alberta. Can Mus Nat Syllogeus 75: 1-75.
42. Hooley RW. 1925. On the skeleton of Iguanodon atherfieldensis from the Wealden. Q J Geol Soc London 81: 1-61f.
43. Huene FV. 1926. Vollständige osteology eines Plateosauriden aus dem schwäbischen Keuper. Geol Palaeontol Abhandl N F 15: 139-179.
44. Janensch W. 1950. Die Wirbelsäule von Brachiosaurus brancai. Palaeontographica 3(Suppl. 7): 27-93.
45. Kutty TS, Chatterjee S, Galton PM, Upchurch P. 2007. Basal sauropodomorphs (Dinosauria: Saurischia) from the lower Jurassic of India: their anatomy and relationships. J Paleontol 81: 1218-1240.
46. Lull RS, Wright NE. 1942. Hadrosaurian dinosaurs of North America. Geol Soc Am Spec Pap 40: 1-242.
47. Madsen JHM, Jr. 1976. Allosaurus fragilis: a revised osteology. Bull Utah Geol Survey 109: 1-163.
48. Maidment SCR, Wei G, Norman DB. 2006. Re-description of the postcranial skeleton of the Middle Jurassic stegosaur Huayangosaurus taibaii. J Vertebr Paleontol 26: 944-956.
49. Maina JN. 2002. Structure, function and evolution of gas exchangers: comparative perspectives. J Anat 201: 281-304.
50. Maina JN. 2005. The lung-air sac system of birds: development, structure, and function. Berlin: Springer-Verlag.
51. Maina JN. 2006. Spectacularly robust! Tensegrity principle explains the mechanical strength of the avian lung. Respir Physiol Neurobiol 155: 1-10.
52. Maina JN, Nathaniel C. 2001. A qualitative and quantitative study of the lung of an ostrich, Struthio camelus. J Exp Biol 204: 2313-2330.
53. Maina JN, West JB. 2005. Thin and Strong! The bioengineering dilemma in the structural and functional design of the blood-gas barrier. Physiol Rev 85: 811-844.
54. Maryanska T. 1977. Ankylosauridae (Dinosauria) from Mongolia. Palaeontol Polonica 37: 85-151.
55. Maryanska T, Osmólska H. 1974. Pachycephalosauria, a new suborder of ornithischian dinosaurs. Palaeontol Polonica 30: 45-102.
56. McDonald AT. 2011. The taxonomy of species assigned to Camptosaurus (Dinosauria: Ornithopoda). Zootaxa 2783: 52-68.
57. McIntosh JS, Miles CA, Cloward KC, Parker JR. 1996. A new nearly complete skeleton of Camarasaurus. Bull Gunma Mus Nat Hist 1: 1-87.
58. McLelland J. 1989. Anatomy of the lungs and air sacs. In: King AS, McLelland J, editors. Form and function in birds. London: Academic Press. Vol. 4: p 221-279.
59. Mook CC. 1921. Notes on the postcranial skeleton in the Crocodilia. Bull Am Mus Nat Hist 44: 67-100.
60. Nesbitt S. 2007. The anatomy of Effigia okeeffeae (Archosauria, Suchia), theropod-like convergence, and the distribution of related taxa. Bull Am Mus Nat Hist 302: 1-84.
61. Nesbitt SJ, Irmis RB, Parker WG, Smith ND, Turner AH, Rowe T. 2009. Hindlimb osteology and distribution of basal dinosauromorphs from the Late Triassic of North America. J Vertebr Paleontol 29: 498-516.
62. Norman DB. 1986. On the anatomy of Iguanodon atherfieldensis (Ornithischia: Ornithopoda). Bull Inst R Sci Nat Belg Sci Terre 56: 281-372.
63. Novas NE. 1993. New information on the systematics and postcranial skeleton of Herrerasaurus ischigualastensis (Theropoda: Herrerasauridae) from the Ischigualasto formation (Upper Triassic) of Argentina. J Vertebr Paleontol 13: 400-423.
64. O'Connor PM. 2004. Pulmonary pneumaticity in the postcranial skeleton of extant aves: a case study examining anseriformes. J Morphol 261: 141-161.
65. O'Connor PM. 2006. Postcranial pneumaticity: an evaluation of soft-tissue influences on the postcranial skeleton and the reconstruction of pulmonary anatomy in archosaurs. J Morphol 267: 1199-1226.
66. O'Connor PM. 2009. Evolution of archosaurian body plans: skeletal adaptations of an air-sac-based breathing apparatus in birds and other archosaurs. J Exp Zool 311: 629-646.
67. O'Connor PM, Claessens LPAM. 2005. Basic avian pulmonary design and flow-through ventilation in non-avian theropod dinosaurs. Nature 436: 253-256.
68. Ostrom JH, McIntosh JS. 1966. Marsh's dinosaurs: The collections from Como Bluff. New Haven: Yale University Press. 388 pp. Reprint, New Haven: Yale University Press, 1999.
69. Owerkowicz T, Farmer CG, Hicks JW, Brainerd EL. 1999. Contribution of gular pumping to lung ventilation in monitor lizards. Science 284: 1661-1663.
70. Padian K, Horner JR. 2004. Dinosaur physiology. In: Weishampel DB, Dodson P, and Osmólska H, editors. The dinosauria. 2nd ed. Berkeley: University of California Press. p 660-671.
71. Parks WA. 1935. New species of trachodont dinosaurs from the Cretaceous formations of Alberta with notes on other species. Univ Toronto Stud Geol Ser 37: 5-45.
72. Paul GS. 2002. Dinosaurs of the air: the evolution and loss of fl{ligature}ight in dinosaurs and birds. Baltimore: The Johns Hopkins University Press.
73. Perry SF. 1983. Reptilian lungs: functional anatomy and evolution. Adv Anat Embryol Cell Biol 79: 1-81.
74. Perry SF. 1989. Mainstreams in the evolution of vertebrate respiratory structures. In: King AS, McLelland J, editors. Form and function in birds. London: Academic Press. Vol. 4: p 1-67.
75. Perry SF. 1992. Gas exchange strategies in reptiles and the origin of the avian lung. In: Wood SC, Weber RE, Hargens AR, Millard RW, editors. Physiological adaptations in vertebrates: respiration, circulation, and metabolism. New York, NY: Marcel Dekker. p 149-167.
76. Perry SF. 1998. Lungs: comparative anatomy, functional morphology, and evolution. In: Gans C, Gaunt AS, editors. Biology of the reptilia: morphology G visceral organs. New York: Society for the Study of Amphibians and Reptiles. Vol. 19: p 1-92.
77. Perry SF, Christian A, Thomas B, Pajor N, Codd JR. 2009. Implications of an avian-style respiratory system for gigantism in sauropod dinosaurs. J Integr Biol 311A.
78. Perry SF, Reuter C. 1999. Hypothetical lung structure of Brachiosaurus (Dinosauria: Sauropoda) based on functional constraints. Mitt Mus Natkd Berl Geowiss Reihe 2: 75-79.
79. Perry SF, Sander M. 2004. Reconstructing the evolution of the respiratory apparatus in tetrapods. Respir Physiol Neurobiol 144: 125-139.
80. Pinna G. 1979. Osteologia dello scheletro di Kritosaurus notabilis (Lambe, 1914) del Museo Civico di Storia Naturale di Milano. Memorie della societa Italiana di scienze naturali Museo Civico di Storia Naturale di Milano 22: 33-55.
81. Schachner ER, Lyson TR, Dodson P. 2009. Evolution of the respiratory system in nonavaian theropods: evidence from rib and vertebral morphology. Anat Rec 292: 1501-1513.
82. Schif fff JA. 2004. Old Yale: what Yale brought to the fair. Yale Alumni Magazine 67: 72.
83. Sereno PC, Arcucci AB. 1994. Dinosaurian precursors from the Middle Triassic of Argentina: Marasuchus lilloensis, gen. nov. J Vertebr Paleontol 14: 53-73.
84. Sereno PC, Chao S. 1988. Psittacosaurus meileyingensis (Ornithischia: Ceratopsia), a new psittacosaur from the Lower Cretaceous of northeastern China. J Vert Paleontol 8: 353-365.
85. Sereno PC, Chenggang R. 1992. Early evolution of avian flight and perching: new evidence from the Lower Cretaceous of China. Science 255: 845-848.
86. Uriona TJ, Farmer CG. 2008. Recruitment of the diaphragmaticus, ischiopubis and other respiratory muscles to control pitch and roll in the American alligator (Alligator mississippiensis). J Exp Biol 211: 1141-1147.
87. Wedel MJ. 2003. Vertebral pneumaticity, air sacs, and the physiology of sauropod dinosaurs. Paleobiology 29: 243-255.
88. Wedel MJ. 2006. Origin of postcranial skeletal pneumaticity in dinosaurs. Integrative Zool 2: 80-85.
89. Wedel MJ. 2007. What pneumaticity tell us about 'prosauropods', and vice versa. Palaeontol 77: 207-222.
90. Wedel MJ. 2009. Evidence for bird-like air sacs in saurischian dinosaurs. J Exp Biol 311: 611-628.
91. Witmer LM. 1995. The extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. In: Thomason JJ, editor. Functional morphology in vertebrate paleontology. Cambridge, UK: Cambridge University Press. p 19-33.
92. Zimmer K. 1935. Beitrage zur Mechanik der Atmung bei den Viigeln im Stand und Flug. Auf Grund ana-tomisch-physiologischer und experimenteller Studien. Zoologicu 33 Heft 88: l-69.