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Research Article

Osteohistology of Uberabatitan ribeiroi (Dinosauria, Sauropoda) provides insight into the life history of titanosaurs

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Received 25 Jun 2023, Accepted 25 Aug 2023, Published online: 07 Sep 2023

References

  • Apaldetti C, Martínez RN, Cerda IA, Pol D, Alcober O. 2018. An early trend towards gigantism in Triassic sauropodomorph dinosaurs. Nat Ecol Evol. 2:1227–1232.
  • Aureliano T, Ghilardi AM, Silva Junior JCG, Martinelli AG, Ribeiro LCB, Marinho T, Fernandes MA, Ricardi Blanco F, Sander PM. 2019. Influence of taphonomy on histological evidence for vertebral pneumaticity in an upper Cretaceous titanosaur from South America. Cretaceous Res. 108:104337. doi:10.1016/j.cretres.2019.104337.
  • Báez AM, Gómez RO, Ribeiro LC, Martinelli AG, Teixeira VP, Ferraz ML. 2012. The diverse cretaceous neobatrachian fauna of South America: Uberabatrachus carvalhoi, a new frog from the Maastrichtian Marília Formation, Minas Gerais, Brazil. Gondwana Research. 22(3–4):1141–1150. doi: 10.1016/j.gr.2012.02.021.
  • Botha J, Choiniere JN, Benson RB. 2022. Rapid growth preceded gigantism in sauropodomorph evolution. Curr Biol. 32(20):4501–4507. doi: 10.1016/j.cub.2022.08.031.
  • Brum AS, Bandeira KLN, Holgado K, Souza BG, Pêgas LV, Sayão RM, Campos JA, Alexander A. 2021. Palaeohistology and palaeopatology of an aeolosaurini (Sauropoda: Titanosauria) from morro do cambambe (Upper Cretaceous, Brazil). Spanish J Palaeontol. 36(1):1–36. doi: 10.7203/sjp.36.1.20305.
  • Brum AS, Bandeira KLN, Sayão JM, Campos DA, Kellner AWA. 2022. Microstructure of axial bones of lithostrotian titanosaurs (Neosauropoda: Sauropodomorpha) shows extended fast-growing phase. Cretaceous Res. 136:105220. doi:10.1016/j.cretres.2022.105220.
  • Campos DA, Kellner AWA. 1999. On some sauropod (Titanosauridae) pelves from the continental Cretaceous of Brazil. National Science Museum Monographs. 15:143–166.
  • Candeiro CR, Martinelli AG, Avilla L, Rich T. 2006. Tetrapods from the upper cretaceous (Turonian–Maastrichtian) Bauru group of Brazil: a reappraisal. Cretaceous Res. 27(6):923–946. doi: 10.1016/j.cretres.2006.05.002.
  • Carballido JL, Pol D, Otero A, Cerda IA, Salgado L, Garrido AC, Ramezani J, Cúneo NR, Krause JM. 2017. A new giant titanosaur sheds light on body mass evolution among sauropod dinosaurs. Proc R Soc B. 284(1860):20171219. doi: 10.1098/rspb.2017.1219.
  • Castanet J. 2006. Time recording in bone microstructures of endothermic animals; functional relationships. C R Palevol. 5(3–4):629–636. doi: 10.1016/j.crpv.2005.10.006.
  • Castanet J, Baez M. 1991. Adaptation and evolution in Gallotia lizards from the Canary Islands: age, growth, maturity and longevity. Amphib Reptilia. 12(1):81–102. doi: 10.1163/156853891X00356.
  • Castanet J, Francillon-Vieillot H, Meunier FJ, de Ricqlès A. 1993. Bone and individual aging. In: Hall B, editor. Bone: bone growth. (Vol. 7). Boca Raton: CRC Press; pp. 245–283.
  • Cerda IA. 2009. Consideraciones sobre la histogénesis de las costillas cervicales en los dinosaurios saurópodos. Ameghiniana. 46:193–198.
  • Cerda IA. 2022. South American sauropodomorphs: what their bone histology has revealed to us. In: Otero A, Carballido J Pol D, editors. South American sauropodomorph dinosaurs record, diversity and evolution. Springer International Publishing; pp. 473–501. doi:10.1007/978-3-030-95959-3_13.
  • Cerda IA, Carballido JL, González R, Salgado L, Zurriaguz VL. 2021. Osteology, paleohistology and phylogenetic relationships of Pellegrinisaurus powelli (Dinosauria: Sauropoda) from the upper cretaceous of Argentinean patagonia. Cretaceous Res. 104957:104957. doi:10.1016/j.cretres.2021.104957.
  • Cerda IA, Casal GA, Martinez RD, Ibiricu LM. 2015. Histological evidence for a supraspinous ligament in sauropod dinosaurs. R Soc Open Sci. 2(10):150369. doi: 10.1098/rsos.150369.
  • Cerda IA, Chinsamy Turan A, Pol D, Apaldetti C, Otero A, Powell JE, Martínez RN, Claessens L. 2017. Novel insight into the origin of the growth dynamics of sauropod dinosaurs. PLoS One. 12(6):e0179707. doi: 10.1371/journal.pone.0179707.
  • Cerda IA, García RA, Powell JE, Lopez O. 2015. Morphology, microanatomy, and histology of titanosaur (Dinosauria, Sauropoda) osteoderms from the upper cretaceous of patagonia. J Vertebr Paleontol. 35(1):e905791. doi: 10.1080/02724634.2014.905791.
  • Cerda IA, Pereyra ME, Garrone M, Ponce D, Navarro TG, González R, Militello M, Luna CA, Jannello JM. 2020. A basic guide for sampling and preparation of extant and fossil bones for histological studies. Publicación Electrónica Asociación Paleontológica Argentina. 20:15–28. doi:10.5710/PEAPA.07.04.2020.314.
  • Chinsamy Turan A. 2005. The microstructure of dinosaur bones: deciphering biology through fine scale techniques. Baltimore: The Johns Hopkins University Press; pp. 631–632.
  • Chinsamy Turan A, Raath MA. 1992. Preparation of fossil bone for histological examination. Palaeontologia Africana. 29:39–44.
  • Company J. 2011. Bone histology of the titanosaur Lirainosaurus astibiae (Dinosauria: Sauropoda) from the latest Cretaceous of Spain. Naturwissenschaften. 98(1):67–78. doi: 10.1007/s00114-010-0742-3.
  • Curry Rogers KA, Erickson GM. 2005. Sauropod histology: microscopic views on the lives of giants. In: Curry Rogers K Erickson G, editors The sauropods: evolution and paleobiology; pp. 303–326. doi:10.1525/california/9780520246232.003.0012.
  • Curry Rogers K, Kulik Z. 2018. Osteohistology of Rapetosaurus krausei (Sauropoda: Titanosauria) from the upper cretaceous of madagascar. J Vertebr Paleontol. 38(4):((1)–((24). doi: 10.1080/02724634.2018.1493689.
  • D’Emic MD. 2012. The early evolution of titanosauriform sauropod dinosaurs. Zool J Linn Soc. 166(3):624–671. doi: 10.1111/j.1096-3642.2012.00853.x.
  • Díez Díaz V, Garcia G, Pereda-Suberbiola X, Jentgen-Ceschino B, Stein K, Godefroit P, Valentin X. 2018. The titanosaurian dinosaur Atsinganosaurus velauciensis (Sauropoda) from the upper cretaceous of southern France: new material, phylogenetic affinities, and palaeobiogeographical implications. Cretaceous Res. 91:429–456. doi:10.1016/j.cretres.2018.06.015.
  • Erickson GM. 2014. On dinosaur growth. Annu Rev Earth Planet Sci. 42(1):675–697. doi: 10.1146/annurev-earth-060313-054858.
  • Erickson GM, Curry Rogers K, Varrichio DJ, Norell MA, Xu X. 2007. Growth patterns in brooding dinosaurs reveals the timing of sexual maturity in non-avian dinosaurs and genesis of the avian condition. Biol Lett. 3(5):558–561. doi: 10.1098/rsbl.2007.0254.
  • Fernandes LA, Coimbra AM. 2000. Revisão estratigráfica da parte oriental da bacia bauru (neocretaceo). RBG. 30(4):717–728. doi: 10.25249/0375-7536.2000304717728.
  • França MAGD, Langer MC. 2005. A new freshwater turtle (Reptilia, Pleurodira, Podocnemidae) from the upper Cretaceous (Maastrichtian) of Minas Gerais, Brazil. Geodiversitas. 27(3):391.
  • Francillon-Vieillot H, de Buffrénil V, Castanet J, Géraudie J, Meunier FJ, Sire J, de Ricqlès A. 1990. Microstructure and mineralization of vertebrate skeletal tissues. Skeletal Biominer. 1:471–530.
  • Gallina PA. 2012. Histología Ósea del Titanosaurio Bonitasaura salgadoi (Dinosauria: Sauropoda) del Cretácico Superior de Patagonia. Ameghiniana. 49(3):289–302. doi: 10.5710/AMGH.v49i3(519).
  • García RA, Salgado L, Fernández MS, Cerda IA, Carabajal AP, Otero A, Coria RA, Fiorelli LE. 2015. Paleobiology of titanosaurs: reproduction, development, histology, pneumaticity, locomotion and neuroanatomy from the South American fossil record. Ameghiniana. 52(1):29–68. doi: 10.5710/AMGH.16.07.2014.829.
  • González R, Cerda IA, Filippi LS, Salgado L. 2020. Early growth dynamics of titanosaur sauropods inferred from bone histology. Palaeogeogr Palaeoclimatol Palaeoecol. 537:109404. doi:10.1016/j.palaeo.2019.109404.
  • Gorscak E, O´connor PM. 2016. Time-calibrated models support congruency between Cretaceous continental rifting and titanosaurian evolutionary history. Biol Lett. 12:20151047. doi:10.1098/rsbl.2015.1047. 4
  • Hechenleitner EM, Leuzinger L, Martinelli AG, Rocher S, Fiorelli LE, Taborda JR, Salgado L. 2020. Two Late Cretaceous sauropods reveal titanosaurian dispersal across South America. Commun Biol. 3(1):622. doi: 10.1038/s42003-020-01338-w.
  • Ibiricu LM, Lamanna MC, Martínez RDF, Casal GA, Cerda IA, Martínez G, Salgado L. 2017. A novel form of postcranial skeletal pneumaticity in a sauropod dinosaur: implications for the paleobiology of rebbachisauridae. Acta Palaeontol Pol. 62:1–16. doi:10.4202/app.00316.2016.
  • Ikejiri T. 2012. Histology-based morphology of the neurocentral synchondrosis in Alligator mississippiensis (Archosauria, Crocodylia). Anat Rec. 295(1):18–31. doi: 10.1002/ar.21495.
  • Iori FV, Araújo-Júnior HI, Tavares SAS, Marinho TS, Martinelli AG. 2021. New theropod dinosaur from the Late Cretaceous of Brazil improves abelisaurid diversity. J S Am Earth Sci. 112:103551. doi:10.1016/j.jsames.2021.103551.
  • Kellner AWA, Campos DDA, Trotta MNF. 2005. Description of a titanosaurid caudal series from the Bauru group, Late Cretaceous of Brazil. Arquivos do Museu Nacional. 63(3):529–564.
  • Khonsue W, Chaiananporn T, Pomchote P. 2010. Skeletochronological assessment of age in the Himalayan crocodile newt, Tylototriton verrucosus (Anderson, 1871) from Thailand. Trop Nat Hist. 10:181–188.
  • Klein N, Christian A, Sander PM. 2012a. Histology shows that elongated neck ribs in sauropod dinosaurs are ossified tendons. Biol Lett. 8(6):1032–1035. doi: 10.1098/rsbl.2012.0778.
  • Klein N, Sander M. 2008. Ontogenetic stages in the long bone histology of sauropod dinosaurs. Paleobiology. 34(2):247–263. doi: 10.1666/0094-8373(2008)034[0247:OSITLB]2.0.CO;2.
  • Klein N, Sander PM. 2007. Bone histology and growth of the prosauropod dinosaur Plateosaurus engelhardti von Meyer, 1837 from the norian bonebeds of trossingen (Germany) and Frick (Switzerland). Spec Papers In Palaeontology. 77:169–206.
  • Klein N, Sander PM, Stein K, Le Loeuff J, Carballido JL, Buffetaut E. 2012b. Modified laminar bone in Ampelosaurus atacis and other titanosaurs (Sauropoda): implications for life history and physiology. PLoS One. 7(5):e36907. doi: 10.1371/journal.pone.0036907.
  • Klein N, Sander PM, Suteethorn V. 2009. Bone histology and its implications for the life history and growth of the early Cretaceous titanosaur Phuwiangosaurus sirindhornae. Geol Soc London, Spec Publ. 315(1):217–228. doi: 10.1144/SP315.15.
  • Lee AH, Werning S. 2008. Sexual maturity in growing dinosaurs does not fit reptilian growth models. Proc Nat Acad Sci. 105(2):582–587. doi: 10.1073/pnas.0708903105.
  • Martinelli AG, Marinho TS, Filippi LS, Ribeiro LCB, Ferraz MLF, Cavellani CL, Teixeira VPA. 2015. Cranial bones and atlas of titanosaurs (Dinosauria, Sauropoda) from Late Cretaceous (Bauru group) of Uberaba, Minas Gerais state, Brazil. J S Am Earth Sci. 61(2015):164–170. doi: 10.1016/j.jsames.2015.02.009.
  • Martinelli AG, Riff D, Lopes RP. 2011. Discussion about the occurrence of the genus Aeolosaurus Powell 1987 (Dinosauria, Titanosauria) in the upper Cretaceous of Brazil. Gaea: Journal Of Geoscience. 7(1):34. doi: 10.4013/gaea.2011.71.03.
  • Martinelli AG, Teixeira VP. 2015. The Late Cretaceous vertebrate record from the Bauru group in the Triângulo Mineiro, southeastern Brazil. Boletín Geológico y Minero. 126(1):129–158.
  • Martinelli AG, Teixeira VP, Marinho TS, Fonseca PH, Cavellani CL, Araujo AJ, Ribeiro LC, Ferraz ML. 2015. Fused mid‐caudal vertebrae in the titanosaur Uberabatitan ribeiroi from the Late Cretaceous of Brazil and other bone lesions. Lethaia. 48(4):456–462. doi: 10.1111/let.12117.
  • Martínez RDF, Lamanna MC, Novas FE, Ridgely RC, Casal GA, Martínez JE, Vita JR, Witmer LM, Joger U. 2016. A basal lithostrotian titanosaur (Dinosauria: Sauropoda) with a complete skull: implications for the evolution and paleobiology of Titanosauria. PLoS One. 11(4):e0151661. doi: 10.1371/journal.pone.0151661.
  • Menegazzo MC, Catuneanu O, Chang HK. 2016. The South American retroarc foreland system: the development of the bauru basin in the back-bulge province. Mar Petrol Geol. 73:131–156. doi:10.1016/j.marpetgeo.2016.02.027.
  • Mitchell J, Sander PM, Stein K. 2017. Can secondary osteons be used as ontogenetic indicators in sauropods? Extending the histological ontogenetic stages into senescence. Paleobiology. 43(2):321–342. doi: 10.1017/pab.2016.47.
  • Navarro BA, Ghilardi AM, Aureliano T, Díez Díaz V, Bandeira KL, Cattaruzzi AGS, Ori FV, Martine AM, Carvalho AB, Anelli LE, et al. 2022. A new nanoid titanosaur (Dinosauria: Sauropoda) from the upper Cretaceous of Brazil. Ameghiniana. 59(5):317–354. doi: 10.5710/AMGH.25.08.2022.3477.
  • Novas FE, de Souza Carvalho I, Ribeiro LCB, Méndez AH. 2008. First abelisaurid bone remains from the Maastrichtian Marília Formation, Bauru basin, Brazil. Cretaceous Res. 29(4):625–635. doi: 10.1016/j.cretres.2008.01.010.
  • Otero A, Carballido JL, Pol D, Otero A, Carballido JL, Pol D. 2022. South American sauropodomorph dinosaurs: record, diversity and evolution. Cham: Springer International Publishing. 590. doi: 10.1007/978-3-030-95959-3.
  • Powell JE. 2003. Revision of South American Titanosaurid dinosaurs: paleobiological, paleobiogepgraphical and phylogenetic aspects. Records Of The Queen Victoria Museum. 111:1–173.
  • Ricqlès de A. 2006. Paléohistologie et paléobiochimie des vertébrés dans les Annales de Paléontologie. Ann Paleontol. 92(2):187–196. doi: 10.1016/j.annpal.2006.03.009.
  • Ricqlès de A, Meunier FJ, Castanet J, Francillon-Vieillot H. 1991. Comparative microstructure of bone. In: Hall BBK, editor Bone, volume 3: bone matrix and bone specific products. Boca Raton, Florida: CRC Press; pp. 1–78.
  • Salgado L, Carvalho I. 2008. Uberabatitan ribeiroi, a new titanosaur from the Marília Formation (Bauru group, upper Cretaceous. Minas Gerais, Brazil, Palaeontology. 51(4):881–901. doi: 10.1111/j.1475-4983.2008.00781.x.
  • Sander PM. 2000. Long bone histology of the Tendaguru sauropods: implications for growth and biology. Paleobiology. 26(3):466–488. doi: 10.1666/0094-8373(2000)026<0466:LHOTTS>2.0.CO;2.
  • Sander PM, Klein N. 2005. Developmental plasticity in the life history of a prosauropod dinosaur. Sci. 310(5755):1800–1802. doi: 10.1126/science.1120125.
  • Sander PM, Klein N, Buffetaut E, Cuny G, Suteethorn V, Le Loeuff J. 2004. Adaptive radiation in sauropod dinosaurs: bone histology indicates rapid evolution of giant body size through acceleration. Organisms Diversity & Evolution. 4(3):165–173. doi: 10.1016/j.ode.2003.12.002.
  • Sander PM, Klein N, Stein K, Wings O. 2011. Sauropod bone histology and implications for sauropod biology. In: Klein N, Remes K, Gee CT Sander PM, editors Biology of the sauropod dinosaurs: understanding the life of giants. Bloomington: Indiana University Press; pp. 276–302.
  • Sander PM, Mateus O, Laven T, Knötschke N. 2006. Bone histology indicates insular dwarfism in a new Late Jurassic sauropod dinosaur. Nature. 441(7094):739–741. doi: 10.1038/nature04633.
  • Santucci RM 2002. Revisão dos Titanosauridae (Saurischia, Sauropoda) do Cretáceo Superior Continental da Bacia Bauru. Rio Claro. 179 p. MSc. Thesis, Instituto de Geociéncias e Ciencias Exatas, Universidade Estadual Paulista.
  • Santucci RM, Bertini RJ. 2006. A large sauropod titanosaur from Peirópolis, Bauru group, Brazil. Neues Jahrbuch für Geologie und Pa läontologie-Monatshefte. 2006(6):344–360. doi: 10.1127/njgpm/2006/2006/344.
  • Silva Junior JCG, Marinho TS, Martinelli AG, Langer MC. 2019. Osteology and systematics of Uberabatitan ribeiroi (Dinosauria; Sauropoda): a Late Cretaceous titanosaur from Minas Gerais, Brazil. Zootaxa. 4577(3):401–438. doi: 10.11646/zootaxa.4577.3.1.
  • Silva Junior JCG, Martinelli AG, Marinho T, da Silva JI, Langer M. 2022. New specimens of Baurutitan britoi and a taxonomic reassessment of the titanosaur dinosaur fauna (Sauropoda) from the Serra da Galga Formation (Late Cretaceous) of Brazil. PeerJ. 10:e14333. doi:10.7717/peerj.14333.
  • Silva Junior JCG, Martinelli AG, Ribeiro LC, Marinho TS. 2017. Description of a juvenile titanosaurian dinosaur from the upper Cretaceous of Brazil. Cretaceous Res. 76:19–27. doi:10.1016/j.cretres.2017.03.029.
  • Soares MVT, Basilici G, Marinho TS, Martinelli AG, Marconato A, Mountney NP, Ribeiro LCB, Mesquita ÁF, Vasques JT, Junior FRA. 2020. Sedimentology of a distributive fluvial system: the serra da galga formation, a new lithostratigraphic unit (upper Cretaceous, Bauru Basin, Brazil). Geol J. 56(2):951–975. doi: 10.1002/gj.3987.
  • Stein K, Csiki Z, Curry Rogers KA, Weishampel DB, Redelstorff R, Carballido JL, Sander PM. 2010. Small body size and extreme cortical bone remodeling indicate phyletic dwarfism in Magyarosaurus dacus (Sauropoda: Titanosauria). Proc Natl Acad Sci USA. 107(20):9258–9263. doi: 10.1073/pnas.1000781107.
  • Upchurch P, Barrett PM, Dodson P. 2004. The Dinosauria. In: Weishampel D, Dodson P Osmo´lska H, editors. The dinosauria. Berkeley, CA: University of California Press; pp. 259–322. doi: 10.1525/california/9780520242098.003.0015.
  • Waskow K, Sander PM. 2014. Growth record and histological variation in the dorsal ribs of Camarasaurus sp. (Sauropoda) J Vertebr Paleontol. 34(4):852–869. doi: 10.1080/02724634.2014.840645.
  • Windholz GJ, Cerda IA. 2021. Paleohistology of two dicraeosaurid dinosaurs (Sauropoda; Diplodocoidea) from La Amarga Formation (Barremian–Aptian, Lower Cretaceous), Neuquén Basin, Argentina: paleobiological implications. Cretaceous Res. 128:104965. doi:10.1016/j.cretres.2021.104965.
  • Woodruff DC, Fowler DW, Horner JR. 2017. A new multi-faceted framework for deciphering diplodocid ontogeny. Palaeontol Electron. 1–53. doi: 10.26879/674.
  • Woodward HN, Lehman TM. 2009. Bone histology and microanatomy of Alamosaurus sanjuanensis (Sauropoda: Titanosauria) from the maastrichtian of big bend national park, texas. J Vertebr Paleontol. 29(3):807–821. doi: 10.1671/039.029.0310.

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