The origin of an invasive air sac system in sauropodomorph dinosaurs.
South America
Triassic
bone histology
ornithodira
respiratory system
Journal
Anatomical record (Hoboken, N.J. : 2007)
ISSN: 1932-8494
Titre abrégé: Anat Rec (Hoboken)
Pays: United States
ID NLM: 101292775
Informations de publication
Date de publication:
Apr 2024
Apr 2024
Historique:
revised:
03
03
2023
received:
24
01
2023
accepted:
06
03
2023
medline:
18
3
2024
pubmed:
28
3
2023
entrez:
27
3
2023
Statut:
ppublish
Résumé
One of the most remarkable features in sauropod dinosaurs relates to their pneumatized skeletons permeated by a bird-like air sac system. Many studies described the late evolution and diversification of this trait in mid to late Mesozoic forms but few focused on the origin of the invasive respiratory diverticula in sauropodomorphs. Fortunately, it is possible to solve this thanks to the boom of new species described in the last decade as well as the broad accessibility of new technologies. Here we analyze the unaysaurid sauropodomorph Macrocollum itaquii from the Late Triassic (early Norian) of southern Brazil using micro-computed tomography. We describe the chronologically oldest and phylogenetically earliest unambiguous evidence of an invasive air sac system in a dinosaur. Surprisingly, this species presented a unique pattern of pneumatization in non-sauropod sauropodomorphs, with pneumatic foramina in posterior cervical and anterior dorsal vertebrae. This suggests that patterns of pneumatization were not cladistically consistent prior to the arrival of Jurassic eusauropods. Additionally, we describe the protocamerae tissue, a new type of pneumatic tissue with properties of both camellae and camerae. This reverts the previous hypothesis which stated that the skeletal pneumatization first evolved into camarae, and derived into delicate trabecular arrangements. This tissue is evidence of thin camellate-like tissue developing into larger chambers. Finally, Macrocollum is an example of the gradual evolution of skeletal tissues responding to the fastly specializing Respiratory System of saurischian dinosaurs.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1084-1092Subventions
Organisme : Fundação de Amparo à Pesquisa do Estado de São Paulo
ID : FAPESP 2019/16727-3
Organisme : Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul
ID : 21/2551-0000680-3
Organisme : Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul
ID : FAPERGS 1/2551-0002030-0
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
ID : 309414/2019-9
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
ID : 422568/2018-0
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
ID : 404095/2021-6
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
ID : 307333/2021-3
Informations de copyright
© 2023 The Authors. The Anatomical Record published by Wiley Periodicals LLC on behalf of American Association for Anatomy.
Références
Aureliano, T., Ghilardi, A. M., Müller, R. T., Kerber, L., Pretto, F. A., Fernandes, M. A., Ricardi-Branco, F., & Wedel, M. J. (2022). The absence of an invasive air sac system in the earliest dinosaurs suggests multiple origins of vertebral pneumaticity. Scientific Reports, 12, 20844.
Aureliano, T., Ghilardi, A. M., Silva-Junior, J. C. G., Martinelli, A. G., Ribeiro, L. C. B., Marinho, T., Fernandes, M. A., Ricardi-Branco, F., & Sander, P. M. (2020). Influence of taphonomy on histological evidence for vertebral pneumaticity in an upper cretaceous titanosaur from South America. Cretaceous Research, 108, 104337.
Bandeira, K. L. N., Simbras, F. M., Machado, E. B., et al. (2016). A new giant Titanosauria (Dinosauria: Sauropoda) from the late cretaceous Bauru group. Brazil. PLoS One, 11, e0163373.
Britt, B. B. (1994). Pneumatic postcranial bones in dinosaurs and other archosaurs.
Brochu, C. A. (1996). Closure of neurocentral sutures during crocodilian ontogeny: Implications for maturity assessment in fossil archosaurs. Journal of Vertebrate Paleontology, 16, 49-62.
Butler, R. J., Barrett, P. M., & Gower, D. J. (2012). Reassessment of the evidence for postcranial skeletal pneumaticity in Triassic archosaurs, and the early evolution of the avian respiratory system. PLoS One, 7, e34094.
Carballido, J. L., Pol, D., Otero, A., Cerda, I. A., Salgado, L., Garrido, A. C., Ramezani, J., Cúneo, N. R., & Krause, J. M. (2017). A new giant titanosaur sheds light on body mass evolution among sauropod dinosaurs. Proceedings of the Royal Society B, 284, 20171219.
Cerda, I. A., Paulina Carabajal, A., Salgado, L., Coria, R. A., Reguero, M. A., Tambussi, C. P., & Moly, J. J. (2012). The first record of a sauropod dinosaur from Antarctica. Naturwissenschaften, 99, 83-87.
Cerda, I. A., Salgado, L., & Powell, J. E. (2012). Extreme postcranial pneumaticity in sauropod dinosaurs from South America. Paläontologische Zeitschrift, 86, 441-449.
CloudCompare. (2018). Version 2.9. 1 [GPL software].
Curry Rogers, K., & Forster, C. A. (2001). The last of the dinosaur titans: A new sauropod from Madagascar. Nature, 412, 530-534.
Díez Díaz, V. (2022). Titanosaur boom. Nature Ecology & Evolution, 6, 251-252.
Fedorov, A., Beichel, R., Kalpathy-Cramer, J., Finet, J., Fillion-Robin, J. C., Pujol, S., Bauer, C., Jennings, D., Fennessy, F., Sonka, M., Buatti, J., Aylward, S., Miller, J. V., Pieper, S., & Kikinis, R. (2012). 3D slicer as an image computing platform for the quantitative imaging network. Magnetic Resonance Imaging, 30, 1323-1341.
Ghilardi, A. M., Aureliano, T., Duque, R. R. C., Fernandes, M. A., Barreto, A. M. F., & Chinsamy, A. (2016). A new titanosaur from the lower cretaceous of Brazil. Cretaceous Research, 67, 16-24.
González Riga, B. J., Lamanna, M. C., Ortiz David, L. D., Calvo, J. O., & Coria, J. P. (2016). A gigantic new dinosaur from Argentina and the evolution of the sauropod hind foot. Scientific Reports, 6, 19165.
Lacovara, K. J., Lamanna, M. C., Ibiricu, L. M., Poole, J. C., Schroeter, E. R., Ullmann, P. V., Voegele, K. K., Boles, Z. M., Carter, A. M., Fowler, E. K., Egerton, V. M., Moyer, A. E., Coughenour, C. L., Schein, J. P., Harris, J. D., Martínez, R. D., & Novas, F. E. (2014). A gigantic, exceptionally complete titanosaurian sauropod dinosaur from southern Patagonia Argentina. Scientific Reports, 4, 6196.
Langer, M. C., Ramezani, J., & Da Rosa, Á. A. S. (2018). U-Pb age constraints on dinosaur rise from South Brazil. Gondwana Research, 57, 133-140.
McLelland, J. (1989). Anatomy of the lungs and air sacs. Form and function in birds, 4, 221-279.
Mo, J., Ma, F., Yu, Y., & Xu, X. (2023). A new Titanosauriform sauropod with an unusual tail from the lower cretaceous of northeastern China. Cretaceous Research, 144, 105449.
Müller, R. T., da Rosa, Á. A. S., Roberto da Silva, L., Aires, A. S. S., Pacheco, C. P., Pavanatto, A. E. B., & Dias-da-Silva, S. (2015). Wachholz, a new exquisite dinosaur-bearing fossiliferous site from the upper Triassic of southern Brazil. Journal of South American Earth Sciences, 61, 120-128.
Müller, R. T., Garcia, M. S., Da-Rosa, Á. A. S., & Dias-da-Silva, S. (2018). Under pressure: Effect of sedimentary compression on the iliac morphology of early sauropodomorphs. Journal of South American Earth Sciences, 88, 345-351.
Müller, R. T., Langer, M. C., & Dias-da-Silva, S. (2018). An exceptionally preserved association of complete dinosaur skeletons reveals the oldest long-necked sauropodomorphs. Biology Letters, 14, 20180633. https://doi.org/10.1098/rsbl.2018.0633
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.
Otero, A., Carballido, J. L., Salgado, L., Canudo, J. I., & Garrido, A. C. (2021). Report of a giant titanosaur sauropod from the upper cretaceous of Neuquén Province Argentina. Cretaceous Research, 122, 104754.
Perry, S. F., Christian, A., Breuer, T., et al. (2009). Implications of an avian-style respiratory system for gigantism in sauropod dinosaurs. Journal of Experimental Zoology. Part A, Ecological Genetics and Physiology, 311, 600-610.
Rigby, S. L., Poropat, S. F., Mannion, P. D., Pentland, A. H., Sloan, T., Rumbold, S. J., Webster, C. B., & Elliott, D. A. (2021). A juvenile Diamantinasaurus matildae (Dinosauria: Titanosauria) from the upper cretaceous Winton formation of Queensland, Australia, with implications for sauropod ontogeny. Journal of Vertebrate Paleontology, 41(6), p.e2047991. https://doi.org/10.1080/02724634.2021.2047991
Sander, P. M., Christian, A., Clauss, M., Fechner, R., Gee, C. T., Griebeler, E. M., Gunga, H. C., Hummel, J., Mallison, H., Perry, S. F., Preuschoft, H., Rauhut, O. W. M., Remes, K., Tütken, T., Wings, O., & Witzel, U. (2011). Biology of the sauropod dinosaurs: The evolution of gigantism. Biological Reviews of the Cambridge Philosophical Society, 86, 117-155.
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671-675.
Schwarz, D., & Fritsch, G. (2006). Pneumatic structures in the cervical vertebrae of the late Jurassic Tendaguru sauropods brachiosaurus brancai and Dicraeosaurus. Eclogae Geologicae Helvetiae, 99, 65-78.
Wedel, M. J. (2003). Vertebral pneumaticity, air sacs, and the physiology of sauropod dinosaurs. Paleobiology, 29, 243-255.
Wedel, M. J. (2007). What pneumaticity tells us about “prosauropods”, and vice versa. Special Papers in Palaeontology, 77, 207-222.
Wedel, M. J. (2009). Evidence for bird-like air sacs in saurischian dinosaurs. Journal of Experimental Zoology. Part A, Ecological Genetics and Physiology, 311, 611-628.
Wedel, M. J., Cifelli, R. L., & Sanders, R. K. (2000). Osteology, paleobiology, and relationships of the sauropod dinosaur Sauroposeidon. Acta Palaeontologica Polonica, 45(4), 343.
Wiersma-Weyand, K., Canoville, A., Siber, H.-J., & Sander, P. M. (2021). Testing hypothesis of skeletal unity using bone histology: The case of the sauropod remains from the Howe-Stephens and Howe Scott quarries. Palaeontol Electronica. https://doi.org/10.26879/766
Wilson, J. A. (1999). A nomenclature for vertebral laminae in sauropods and other saurischian dinosaurs. Journal of Vertebrate Paleontology, 19, 639-653.
Wilson, J. A. (2012). New vertebral laminae and patterns of serial variation in vertebral laminae of sauropod dinosaurs.
Wilson, J. A., D'Emic, M. D., Ikejiri, T., et al. (2011). A nomenclature for vertebral fossae in sauropods and other saurischian dinosaurs. PLoS One, 6, e17114.
Woodward, H. N., & Lehman, T. M. (2009). Bone histology and microanatomy of Alamosaurus sanjuanensis (Sauropoda: Titanosauria) from the Maastrichtian of big bend National Park, Texas. Journal of Vertebrate Paleontology, 29, 807-821.
Yates, A. M., Wedel, M. J., & Bonnan, M. F. (2012). The early evolution of postcranial skeletal Pneumaticity in sauropodomorph dinosaurs. Acta Palaeontologica Polonica, 57, 85-100.
Zurriaguz, V., & Powell, J. E. (2015). New contributions to the presacral osteology of Saltasaurus loricatus (Sauropoda, Titanosauria) from the upper cretaceous of northern Argentina. Cretaceous Research, 54, 283-300.