Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Extreme postcranial pneumaticity in sauropod dinosaurs from South America

Abstract

Birds are unique among living tetrapods in possessing pneumaticity of the postcranial skeleton, with invasion of bone by the lung and air-sac system. Postcranial skeletal pneumaticity (PSP) has been reported in numerous extinct archosaurs including pterosaurs and non-avian dinosaurs. Here we report a case of extreme PSP in a group of small-bodied, armored sauropod dinosaurs from the Upper Cretaceous of South America. Based on osteological data, we report an extensive invasion of pneumatic diverticula along the vertebral column, reaching the distal portion of the tail. Also, we provide evidence of pneumaticity in both pectoral and pelvic girdles. Our study reveals that the extreme PSP in archosaurs is not restricted to pterosaurs and theropod dinosaurs.

Kurzfassung

Vögel sind einzigartig innerhalb der lebenden Tetrapoden, da sie eine Pneumatisierung des Postkranialskeletts aufweisen, welche die Invasion von Knochen durch die Lunge und Luftsack-Systeme einschließt. Diese postkraniale Skelettpneumatisierung (PSP) ist bereits in zahlreichen ausgestorbenen Archosauriern, einschließlich Pterosauriern und Dinosauriern, die nicht der Vogellinie angehören, beschrieben worden. Hier berichten wir über einen Fall von extremer PSP in einer Gruppe von kleinwüchsigen, gepanzerten sauropoden Dinosauriern aus der Oberkreide von Südamerika. Basierend auf osteologischen Daten lässt sich eine umfangreiche Invasion von pneumatischen Divertikeln entlang der Wirbelsäule nachweisen, welche sich bis in die distalen Bereiche des Schwanzes erstreckt. Darüber hinaus zeigen sich Hinweise auf Pneumatisierung in beiden Brust- und Beckengürteln. Unsere Studie zeigt, dass diese extreme Form von PSP in Archosauriern nicht auf Flugsaurier und theropode Dinosaurier beschränkt ist.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Benson, R.B.J., R.J. Butler, M.T. Carrano, and P.M. O’Connor. 2011. Air-filled postcranial bones in theropod dinosaurs: Physiological implications and the ‘reptile’–bird transition. Biological Reviews of the Cambridge Philosophical Society. doi:10.1111/j.1469-185X.2011.00190.x.

  2. Bonaparte, J.F. and Powell. J.E. 1980. A continental assemblage of tetrapods from the Upper Cretaceous beds of El Brete, northwestern Argentina (Sauropoda-Coelurosauria-Carnosauria-Aves). Mémories de la Socie¡été Géologique de France 139:19–28.

  3. Britt, B.B. 1993. Pneumatic postcranial bones in dinosaurs and other archosaurs. Dissertation, University of Calgary.

  4. Buttler, R.J., P.M. Barrettt, and D.J. Gower. 2009. Postcranial skeletal pneumaticity and air-sacs in the earliest pterosaurs. Biology Letters 5: 557–560. doi:10.1098/rsbl.2009.0139.

  5. Butler, R.J., P.M. Barrett, and D.J. Gower. 2012. Reassessment of the evidence for postcranial skeletal pneumaticity in Triassic archosaurs, and the early evolution of the avian respiratory system. PLoS One 7(3): e34094. doi:10.1371/journal.pone.0034094.

  6. Calvo, J.O., B.J. González Riga, and J.D. Porfiri. 2007a. A new titanosaur sauropod from the Late Cretaceous of Neuquén, Patagonia, Argentina. Arquivos do Museu Nacional 65: 485–504.

  7. Calvo, J.O., J.D. Porfiri, B.J. González Riga, and A.W.A. Kellner. 2007b. A new Cretaceous terrestrial ecosystem from Gondwana with the description of a new sauropod dinosaur. Anais da Academia Brasileira de Ciencias 79: 529–541.

  8. Carvalho, I.S., L. dos Santos Avilla, and L. Salgado. 2003. Amazonsaurus maranhensis gen. et sp. nov. (Sauropoda, Diplodocoidea) from the Lower Cretaceous (Aptian-Albian) of Brazil. Cretaceous Research 24: 697–713.

  9. Claessens, L.P.A., P.M. O’Connor, and D.M. Unwin. 2009. Respiratory evolution facilitated the origin of pterosaur flight and aerial gigantism. PLoS One 4: e4497. doi:10.1371/journal.pone.0004497.

  10. Duncker, H.-R. 1971. The lung air-sac system of birds. Advances in Anatomy, Embroylogical and Cell Biology 45: 1–171.

  11. Gonzáles Riga, B.J., E. Previtera, and C.A. Pirrone. 2009. Malarguesaurus florenciae gen. et sp. nov., a new titanosauriform (Dinosauria, Sauropoda) from the Upper Cretaceous of Mendoza, Argentina. Cretaceous Research 30: 135–148.

  12. Hocknull, S.A., M.A. White, T.R. Tischler, A.G. Cook, N.D. Calleja, T. Sloan, and E.A. Elliott. 2009. New Mid-Cretaceous (Late Albian) Dinosaurs from Winton, Queensland, Australia. PLos One 4(7): e6190. doi:10.1371/journal.pone.0006190.

  13. Janensch, W. 1947. Pneumatizitat bei Wirbeln von sauropoden und anderen saurischien. Palaeontographica 3: 1–25.

  14. McIntosh, J.S. 1990. Sauropoda. In The Dinosauria 1st edn, eds. D.B. Weishampel, P. Dodson & H. Osmólska, 345–401. Berkeley: University of California Press.

  15. O’Connor, P.M. 2006. Postcranial pneumaticity: An evaluation of soft-tissue influences on the postcranial skeleton and the reconstruction of pulmonary anatomy in archosaurs. Journal of Morphology 267: 1199–1226. doi:10.1002/jmor.10470.

  16. O’Connor, P.M., and L.P.A. Claessens. 2005. Basic avian pulmonary design and flow-through ventilation in nonavian theropod dinosaurs. Nature 436: 253–256. doi:10.1038/nature03716.

  17. Otero, A. 2010. The appendicular skeleton of Neuquensaurus, a Late Cretaceous saltasaurine sauropod from Patagonia, Argentina. Acta Palaeontologica Polonica 55: 399–426.

  18. Perry, S.F., T. Breuer, and N. Pajor. 2011. Structure and function of the sauropod respiratory system. In Biology of the sauropod dinosaurs: Understanding the life of giants, ed. N. Klein, K. Remes, C.T. Gee, and P.M. Sander, 83–93. Bloomington and Indianapolis: Indiana University Press.

  19. Powell, J.E. 2003. Revision of South American Titanosaurid dinosaurs: Palaeobiological, palaeobiogeographical and phylogenetic aspects. Records of the Queen Victoria Museum 111: 1–173.

  20. Salgado, L., S. Apesteguía, and S.E. Heredia. 2005. A new specimen of Neuquensaurus australis, a Late Cretaceous saltasaurine titanosaur from North Patagonia. Journal of Vertebrate Paleontology 25: 623–634.

  21. Salgado, L., and C. Azpilicueta. 2000. Un nuevo saltasaurino (Sauropoda, Titanosauridae) de la Provincia de Río Negro (Formación Allen, Cretácico Superior), Patagonia, Argentina. Ameghiniana 37: 259–264.

  22. Salgado, L., R.A. García, and J.D. Daza. 2006. Consideraciones sobre las láminas neurales de los dinosaurios saurópodos y su significado morfofuncional. Revista del Museo Argentino de Ciencias Naturales 8: 69–79.

  23. Salgado, L., and J.F. Bonaparte. 2007. Sauropodomorpha. In Patagonian Mesozoic reptiles, ed. Z. Gasparini, L. Salgado, and R.A. Coria, 188–228. Indiana: Indiana University Press.

  24. Salgado, L., R.A. Coria, and J.O. Calvo. 1997. Evolution of titanosaurid sauropods. I: Phylogenetic analysis based en the postcranial evidence. Ameghiniana 34: 3–32.

  25. Sander, P.M., A. Christian, M. Clauss, R. Fechner, C.T. Gee, E.M. Griebeler, H.C. Gunga, J. Hummel, H. Mallison, S.F. Perry, H. Preuschoft, O.W.M. Rauhut, K. Remes, T. Tütken, O. Wings, and U. Witzel. 2011. Biology of the sauropod dinosaurs: The evolution of gigantism. Biological Reviews of the Cambridge Philosophical Society 86: 117–155. doi:10.1111/j.1469-185X.2010.00137.x.

  26. Sanz, J.L., J.E. Powell, J. Le Loeuff, R. Martínez, and X. Pereda Suberbiola. 1999. Sauropod remains from the Upper Cretaceous of Laño (northcentral Spain). Titanosaur phylogenetic relationships. Estudios del Museo de Ciencias Naturales de Lava 14: 235–255.

  27. Sereno, P.C., R.N. Martínez, J.A. Wilson, D.J. Varrichio, O.A. Alcober, and H.C.E. Larsson. 2008. Evidence for avian intrathoracic air sacs in a new predatory dinosaur from Argentina. PLoS One 3: e3303. doi:10.1371/journal.pone.0003303.

  28. Schwarz, D., E.D. Frey, and C. Meyer. 2007. Pneumaticity and soft-tissue reconstructions in the neck of diplodocid and dicraeosaurid sauropods. Acta Palaeontologica Polonica 52: 167–1188.

  29. Wedel, M.J. 2007. What pneumaticity tells us about ‘prosauropods’, and vice versa. Special Papers in Palaeontology 77: 207–222.

  30. Wedel, M.J. 2009. Evidence for bird-like air-sacs in saurischian dinosaurs. Journal of Experimental Zoology A 311: 611–628. doi:10.1002/jez.513.

  31. Wedel, M.J. 2003. Vertebral pneumaticity, air sacs, and the physiology of sauropod dinosaurs. Paleobiology 29: 243–255. doi:10.1666/0094-8373(2003)029<0243:VPASAT>2.0.CO;2.

  32. Wedel, M.J., R.L. Cifelli, and R.K. Sanders. 2000. Osteology, paleobiology, and relationships of the sauropod dinosaur Sauroposeidon. Acta Palaeontologica Polonica 45: 343–388.

  33. Wilson, J.A. 2000. A nomenclature for vertebral laminae in sauropods and other saurischian dinosaurs. Journal of Vertebrate Paleontology 19: 639–656.

  34. Wilson, J.A. 2005. Overview of sauropod phylogeny and evolution. In The sauropods: Evolution and paleobiology, ed. K. Curry Rogers, and J.A. Wilson, 15–49. Berkeley: University of California Press.

  35. Wilson, J.A., and P. Upchurch. 2003. A revision of Titanosaurus Lydekker (Dinosauria–Sauropoda), the first dinosaur genus with a “Gondwanan” distribution. Journal of Systematic Palaeontology 1: 125–160.

  36. Wilson, J.A., and P. Upchurch. 2009. Redescription and reassessment of the phylogenetic affinities of Euhelopus zdanskyi (Dinosauria: Sauropoda) from the Early Cretaceous of China. Journal of Systematic Palaeontology 7: 199–239.

  37. Wilson, J.A., M.D. D’Emic, T. Ikejiri, E.M. Moacdieh, and J.A. Whitlock. 2011. A nomenclature for vertebral fossae in sauropods and other saurischian dinosaurs. PLoS One 6(2): e17114. doi:10.1371/journal.pone.0017114.

  38. Wiman, C. 1929. Die Kreide-Dinosaurier aus Shantung. Palaeontologia Sinica (series C) 6: 1–67.

  39. Woodward, H.N., and T. Lehman. 2009. Bone histology and microanatomy of Alamosaurus sanjuanensis (Sauropoda, Titanosauria) from the Maastrichtian of the Big Bend National Park, Texas. Journal of Vertebrate Paleontology 29: 807–821.

  40. Yates, A.M., M.J. Wedel, and M.F. Bonnan. 2012. The early evolution of postcranial skeletal pneumaticity in sauropodomorph dinosaurs. Acta Palaeontologica Polonica 57: 85–100.

  41. Xu, X., X. Zhang, Q. Tan, J. Wang, X. Zhao, and L. Tan. 2006. A new titanosaurian sauropod from Late Cretaceous of Nei Mongol. Acta Geologica Sinica 80: 20–26.

Download references

Acknowledgments

We thank Marcelo Reguero, Lucas Pomi, Carlos Muñoz, Norma Brugni and all the staff of Comision Amigos del Museo of Cinco Saltos for access to the specimens under their care, Maia Quintili, Silvia Fasano, Juan José Perazzolo and the authorities of the Policlinico Neuquén for CT scans, Brooks Britt for access to his unpublished PhD thesis, Rodrigo Pellegrini for reading the text and useful comments, Torsten Scheyer for translating the abstract into German and Jorge González for the skeletal reconstruction of Saltasaurus in Fig. 2. The quality of is work has been substantially improved by the useful comments and critical reviews of Roger Benson, Paul Upchurch and Richard Butler. This work was supported by Conicet (PIP 6455 to L.S) and Agencia de Promoción Científica y Técnica (PICT 357 to L.S.).

Author information

Correspondence to Ignacio A. Cerda.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Cerda, I.A., Salgado, L. & Powell, J.E. Extreme postcranial pneumaticity in sauropod dinosaurs from South America. Paläontol Z 86, 441–449 (2012). https://doi.org/10.1007/s12542-012-0140-6

Download citation

Keywords

  • Sauropoda
  • Titanosauria
  • Upper Cretaceous
  • Air-sac system
  • Appendicular pneumaticity

Schlüsselwörter

  • Sauropoda
  • Titanosauria
  • Oberkreide
  • Luftsacksysteme
  • Appendikularpneumatisierung