Comparative analysis of the vertebral pneumatization in pterosaurs (Reptilia: Pterosauria) and extant birds (Avialae: Neornithes)

Autoři: Richard Buchmann aff001;  Leonardo dos Santos Avilla aff002;  Taissa Rodrigues aff001
Působiště autorů: Laboratório de Paleontologia, Departamento de Ciências Biológicas, Centro de Ciências Humanas e Naturais, Universidade Federal do Espírito Santo, Vitória, ES, Brazil aff001;  Laboratório de Mastozoologia, Departamento de Zoologia, Universidade Federal do Estado do Rio de Janeiro, Rio de Janeiro, RJ, Brazil aff002;  Programa de Pós-graduação em Ciências Biológicas (Biodiversidade Neotropical), Universidade Federal do Estado do Rio de Janeiro, Rio de Janeiro, RJ, Brazil aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article


Birds and pterosaurs have pneumatic bones, a feature likely related to their flight capabilities but whose evolution and origin is still poorly understood. Pneumatic foramina are present on the external surface of the bone and are reliable indicators of post-cranial skeletal pneumatization present in Pterosauria, Eusauropoda, and Neotheropoda. Here, we carried out a qualitative analysis of the position, size and number of pneumatic foramina of the cervical and thoracic/dorsal vertebrae of pterosaurs and birds, as they have the potential to challenge hypotheses about the emergence and evolution of the respiratory trait in these groups. We also discussed differences between pneumatic and vascular foramina for identification purposes. Besides phylogenetic representativeness, the pterosaur taxonomic sampling considered the preservation of specimens and, for birds, their life habit, as this relates to the level of pneumatization. Pneumatic foramina on the lateral faces of the centrum of the mid-cervical vertebrae of pterosaurs and birds differ in position and size, and those adjacent to the neural canal additionally differ in number. The avian posterior cervical vertebrae show a higher number of pneumatic foramina in comparison to their mid-cervicals, while the opposite is true for pterosaurs, suggesting differences in the cervical air sac of these clades. Pneumatic foramina were found at the base of the transverse processes of the notarial vertebrae of birds, while they were absent from some of the pterosaurs analyzed here, revealing the presence of a pneumatic hiatus in the vertebral column that might be explained due to the distance of this structure to the cervical air sac. These findings indicate that, although the overall skeletal pneumatization of pterosaurs and birds present deep homologies, some pneumatic features occurred convergently because variation in the number of pneumatic foramina along the vertebral column is related to the position of the air sacs in pterosaurs and birds and/or the habit of each species. There is an evident reduction of the pneumatic foramina in birds that have aquatic foraging and an increase in the ones which perform static soaring. Although we did not find any external anatomical difference between pneumatic and vascular foramina, we observed that vascular foramina occur at specific sites and thus identification on the basis of location is reliable.

Klíčová slova:

Animal flight – Bird flight – Birds – Cervical vertebrae – Habits – Spine – Vertebrae – Pterosauria


1. Crisp E. On the presence or absence of air in the bones of birds. Proceedings of the Zoological Society of London. 1857: 215–220.

2. Müller B. The air-sacs of the pigeon. Smith Misc College. 1908;50: 365–414.

3. O’Connor PM. Pulmonary pneumaticity in the postcranial skeleton of extant Aves: a case study examining Anseriformes. J Morphol. 2004;261: 141–161. doi: 10.1002/jmor.10190 15216520

4. O’Connor PM. Postcranial pneumaticity: an evaluation of soft-tissue influences on the postcranial skeleton and the reconstruction of pulmonary anatomy in archosaurs. J Morphol. 2006;267: 1199–1226. doi: 10.1002/jmor.10470 16850471

5. O’Connor PM, Claessens LPAM. Basic avian pulmonary design and flowthrough ventilation in nonavian theropod dinosaurs. Nature. 2005;436: 253–256. doi: 10.1038/nature03716 16015329

6. Gower DJ. Possible postcranial pneumaticity in the last common ancestor of birds and crocodilians: evidence from Erythrosuchus and other Mesozoic archosaurs. Naturwissenschaften. 2001;88: 119–122. doi: 10.1007/s001140100206 11402840

7. Claessens LPAM, O’Connor PM, Unwin DM. Respiratory evolution facilitated the origin of pterosaur flight and aerial gigantism. PLoS One 2009;4: e4497. doi: 10.1371/journal.pone.0004497 19223979

8. Butler RJ, Barrett PM, Gower DJ. Reassessment of the evidence for postcranial skeletal pneumaticity in Triassic archosaurs, and the early evolution of the avian respiratory system. PLoS One. 2012;7: e34094. doi: 10.1371/journal.pone.0034094 22470520

9. Kellner AWA, Tomida Y. Description of a new species of Anhangueridae (Pterodactyloidea) with comments on the pterosaur fauna from the Santana Formation (Aptian-Albian), Northeastern Brazil. National Science Museum, Monographs, Tokyo. 2000;17:1–135. doi: 10.1159/000061634

10. Sayão JM, Kellner AWA. Novo esqueleto parcial de pterossauro (Pterodactyloidea, Tapejaridae) from the Crato (Aptiano), Formação Santana, Bacia do Araripe, Nordeste do Brasil. Estudos Geológicos. 2006;16: 16–40.

11. Kellner AWA, Campos DA, Sayão JM, Saraiva AAF, Rodrigues T, Oliveira G, et al. The largest flying reptile from Gondwana: a new specimen of Tropeognathus cf. T. mesembrinus Wellnhofer, 1987 (Pterodactyloidea, Anhangueridae) and other large pterosaurs from the Romualdo Formation, Lower Cretaceous, Brazil. An Acad Bras Cienc. 2013;85: 113–135. doi: 10.1590/S0001-37652013000100009 23538956

12. Vila Nova BC, Sayão JM, Langer MC, Kellner AWA. Comments on the cervical vertebrae of the Tapejaridae (Pterosauria, Pterodactyloidea) with description of new specimens. Hist Biol. 2015;27: 770–780. doi: 10.1080/08912963.2015.1007049

13. Buchmann R, Rodrigues T, Polegario S, Kellner AWA. New information on the postcranial skeleton of the Thalassodrominae (Pterosauria, Pterodactyloidea, Tapejaridae). Hist Biol. 2018;30: 1139–1149. doi: 10.1080/08912963.2017.1343314

14. Yuri T, Kimball RT, Harshman J, Bowie RCK, Braun MJ, Chojnowski JL, et al. Parsimony and model-based analyses of indels in avian nuclear genes reveal congruent and incongruent phylogenetic signals. Biol. 2013;2: 419–444. doi: 10.3390/biology2010419 24832669

15. Kerlinger P. Water-crossign behavior of raptors during migration. Wilson Bull. 1985;97: 109–113.

16. Prince PA, Wood AG, Barton T, Croxall JP. Satellite tracking of wandering albatrosses (Diomedea exulans) in South Atlantic. Antarct Sci. 1992;4: 31–36. doi: 10.1017/S0954102092000075

17. Sick H, Pacheco JF. Ornitologia Brasileira. 1st ed. Rio de Janeiro: Editora Nova Fronteira; 1997.

18. Anchundia DJ, Anderson JF, Anderson DJ. Overland flight by seabirds at Isla Isabela, Galápagos. Mar Ornithol. 2017;45: 139–141.

19. Bennett SC. The osteology and functional morphology of the Late Cretaceous pterosaur Pteranodon. Paleontographica Abt. A. 2001;260: 1–153.

20. Baumel JJ, Witmer LM. Osteologia. In: Baumel JJ, King AS, Breazile JE, Howard EE, Vanden Berge JC, editors. Handbook of avian anatomy: Nomina anatomica avium. 2nd ed. Cambridge: Nuttal Ornithological Club; 1993. pp. 45–132.

21. Zusi RL. Structural adaptations of the head and neck in the Black Skimmer, Rhynchops nigra Linnaeus. Publications of the Nuttal Ornithological Club 1962;3: 1–153.

22. Wilson JA, D’Emic MD, Ikejiri T, Moacdieh EM, Whitlock JA. A nomenclature for vertebral fossae in sauropods and other saurischian dinosaurs. PLOS ONE. 2011;6(2): e17114. doi: 10.1371/journal.pone.0017114 21386963

23. Kellner AWA. Pterosaur phylogeny and comments on the evolutionary history of the group. Geol Soc Spec Publ. 2003;217: 105–137. doi: 10.1144/GSL.SP.2003.217.01.10

24. Benson RB, Butler RJ, Carrano MT, O’Connor. Air-filled postcranial bones in theropod dinosaurs: physiological implications and the ‘reptile’–bird transition. Biol Rev. 2012;87(1): 168–193. doi: 10.1111/j.1469-185X.2011.00190.x 21733078

25. Butler RJ, Barrett PM, Gower DJ. Postcranial skeletal pneumaticity and air-sacs in the earliest pterosaurs. Biol Lett. 2009;5: 557–560. doi: 10.1098/rsbl.2009.0139 19411265

26. Buchmann R, Rodrigues T. The evolution of pneumatic foramina in pterosaur vertebrae. An Acad Bras Cienc. 2019;91: e20180782.

27. De Buisonjé PH. Santanadactylus brasilensis nov. gen., nov. sp., a long-necked, large pterosaurier from the Aptian of Brasil. Proc K Ned Akad Wet B. 1980;83: 145–172.

28. Wellnhofer P. Weitere Pterosaurierfunde aus der Santana-Formation (Apt) der Chapada do Araripe, Brasilien. Palaeontographica Abt. A. 1991;215: 43–101.

29. Veldmeijer AJ, Meijer HJM, Signore M. Description of pterosaurian (Pterodactyloidea: Anhangueridae, Brasileodactylus) remains from the Lower Cretaceous of Brazil. Deinsea. 2009;13: 9–40.

30. O’Connor PM. The postcranial axial skeleton of Majungasaurus crenatissimus (Theropoda: Abelisauridae) from the Late Cretaceous of Madagascar. Society of Vertebrate Paleontology Memoir. 2007;8: 127–162.

31. Rauhut OWM. The interrelationships and evolution of basal theropod dinosaurs. Spec Pap Palaeontol. 2003;69: 1–213.

32. Kellner AWA. Comments on Triassic pterosaurs with discussion about ontogeny and description of new taxa. An Acad Bras Cienc. 2015;87: 669–689. doi: 10.1590/0001-3765201520150307 26131631

33. Andres B, Clark J, Xu X. A new rhamphorhynchid pterosaur from the Upper Jurassic of Xinjiang, China, and the phylogenetic relationships of basal pterosaurs. J Vertebr Paleontol. 2010;30: 163–187. doi: 10.1080/02724630903409220

34. Curry Rogers K, Forster CA. The last of the dinosaur titans: a new sauropod from Madagascar. Nature. 2001;412: 530–534. doi: 10.1038/35087566 11484051

35. Averianov AO. The osteology of Azhdarcho lancicollis Nessov, 1984 (Pterosauria, Azhdarchidae) from the Late Cretaceous of Uzbekistan. Proc Zool Inst RAS. 2010;314: 264–317.

36. Rodrigues T, Kellner AWA, Mader BJ, Russell DA. New pterosaur specimens from the Kem Kem Beds (Upper Cretaceous, Cenomanian) of Morocco. Riv Ital Paleontol S. 2011;117: 149–160.

37. Bonde N, Christiansen P. The detailed anatomy of Rhamphorhynchus: axial pneumaticity and its implications. Geol Soc Spec Publ. 2003;217: 217–232. doi: 10.1144/GSL.SP.2003.217.01.13

38. Andres B, Ji Q. A new pterosaur from the Liaoning Province of China, the phylogeny of the Pterodactyloidea, and convergence in their cervical vertebrae. Palaeontology. 2008;51: 453–469. doi: 10.1111/j.1475-4983.2008.00761.x

39. Wedel MJ. What pneumaticity tells us about ‘prosauropods’, and vice versa. Spec Pap Palaeontol. 2007;77: 207–222.

40. Wellnhofer P, Buffetaut E, Gigase P. A pterosaurian notarium from the Lower Cretaceous of Brazil. Palaontol Z. 1983;57: 147–157.

41. Pinheiro FL, Rodrigues T. Anhanguera taxonomy revisited: is our understanding of Santana Group pterosaur diversity biased by poor biological and stratigraphic control?. PeerJ. 2017; 5: e3285. doi: 10.7717/peerj.3285 28484676

42. Hogg DA. The distribution of pneumatisation in the skeleton of the adult domestic fowl. J Anat. 1984a; 138:617–629.

43. Wedel MJ. Evidence for bird-like air sacs in saurischian dinosaurs. J Exp Zool. 2009;311A. doi: 10.1002/jez.513 19204909

44. Wedel MJ, Taylor MP. Caudal pneumaticity and pneumatic hiatuses in the sauropod dinosaus Giraffatitan and Apatosaurus. PLOS ONE. 2013;8 (10): e78213. doi: 10.1371/journal.pone.0078213 24205162

45. Hogg DA. Fusions occurring in the postcranial skeleton of the domestic fowl. J Anat. 1982;135: 501–512. 7153169

46. Hogg DA. The development of pneumatisation in the postcranial skeleton of the domestic fowl. J Anat. 1984b; 139:105–113.

47. Eck K, Elgin RA, Frey E. On the osteology of Tapejara wellnhoferi Kellner 1989 and the first occurrence of a multiple specimen assemblage from the Santana Formation, Araripe Basin, NE-Brazil. Swiss J Palaeontol. 2011;130: 277–296. doi: 10.1007/s13358-011-0024-5

48. Elgin RA, Hone DWE. Pneumatization of an immature azhdarchoid pterosaur. Cretac Res. 2013;45: 16–24. doi: 10.1016/j.cretres.2013.06.006

49. O’Connor PM. Evolution of archosaurian body plans: skeletal adaptations of an air-sac-based breathing apparatus in birds and other archosaurs. J Exp Zool. 2009; 311A: 504–521.

50. Baumel JJ. Systema cardiovasculare. In: Baumel JJ, King AS, Breazile JE, Howard EE, Vanden Berge JC, editors. Handbook of avian anatomy: Nomina anatomica avium. 2nd ed. Cambridge: Nuttal Ornithological Club; 1993. pp. 45–132.

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