- Email: [email protected]
Description of a juvenile titanosaurian dinosaur from the Upper Cretaceous of Brazil
Accepted Manuscript Description of a juvenile titanosaurian dinosaur from the Upper Cretaceous of Brazil Julian C.G. Silva Junior, Agustín G. Martinelli, Luiz C.B. Ribeiro, Thiago S. Marinho PII:
S0195-6671(16)30391-3
DOI:
10.1016/j.cretres.2017.03.029
Reference:
YCRES 3575
To appear in:
Cretaceous Research
Received Date: 15 December 2016 Revised Date:
27 March 2017
Accepted Date: 30 March 2017
Please cite this article as: Silva Junior, J.C.G., Martinelli, A.G., Ribeiro, L.C.B., Marinho, T.S., Description of a juvenile titanosaurian dinosaur from the Upper Cretaceous of Brazil, Cretaceous Research (2017), doi: 10.1016/j.cretres.2017.03.029. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT 1
Description of a juvenile titanosaurian dinosaur from the Upper
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Cretaceous of Brazil
3 Julian C. G. Silva Junior1,4*, Agustín G. Martinelli4,3, Luiz C. B. Ribeiro4, Thiago S. Marinho2,4
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Preto, Universidade de São Paulo, Av. Bandeirantes, 3900, 14040-901, Ribeirão Preto, São Paulo, Brazil
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Departamento de Ciências Biológicas, Avenida Doutor Randolfo Borges Júnior, 38064-200, Uberaba,
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Laboratório de Paleontologia de Ribeirão Preto, Faculdade de Filosofia, Ciências e Letras de Ribeirão
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Instituto de Ciências Exatas, Naturais e Educação, Universidade Federal do Triângulo Mineiro,
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Minas Gerais, Brazil.
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Grande do Sul, Ave. Bento Gonçalves 9500, Agronomia, 91540–000, Porto Alegre, Rio Grande do Sul,
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Brazil.
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Peirópolis, Estanislau Collenghi 194, 38039-755, Peirópolis, Uberaba, Minas Gerais, Brazil.
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Departamento de Paleontologia e Estratigrafia, Instituto de Geociências, Universidade Federal do Rio
Centro de Pesquisas Paleontológicas “Llwelyn Ivor Price”, Universidade Federal do Triângulo Mineiro,
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* Corresponding author: [email protected]
Abstract: We describe a juvenile specimen of a titanosaurian sauropod dinosaur
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consisting of two dorsal and three caudal vertebral centra, an ilium fragment, and an ischium
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unearthed in 1991 from Site Km 153.5 of highway BR-050 in the Serra da Galga region,
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municipality of Uberaba, state of Minas Gerais, Brazil. The outcrop at the site is assigned to the
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Serra da Galga Member of the Marília Formation (Bauru Basin: Bauru Group; Upper
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Cretaceous: Maastrichtian). Although the material is very incomplete, features such as strongly
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procoelous caudal centra suggest an affinity with the titanosaurian clade Lithostrotia. The
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extensive vertebral pneumaticity with deep pleurocoels and well-developed camerae supports
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the hypothesis that, in titanosaurs, the air sac system was already present and fully developed
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even at early ontogenetic stages.
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Keywords: Sauropoda, Titanosauria, juvenile, Marília Formation, Upper Cretaceous, ontogeny, pneumaticity
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1. Introduction
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Titanosaurs represent the last great radiation of sauropod dinosaurs, with a
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globally distributed body-fossil record dating back to at least the late Early Cretaceous
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(D’emic, 2012). They are easily differentiated from other sauropods by a characteristic
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suite of features such as anterior and middle caudal vertebrae with a ventral longitudinal
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hollow (convergent in diplodocids), a platelike ischium with no emargination distal to
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pubic peduncle, six or seven sacral vertebraeand reduction of the articular surfaces for
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the manual phalanges on the metacarpals (e.g., Salgado et al., 1997; Wilson and Sereno,
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1998; Wilson, 2002; Wilson, 2006a). In the Cretaceous fossil record of Brazil
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titanosaurs represent the dinosaur clade with the highest taxonomic abundance (Kellner,
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1999; Novas, 2009; Bittencout and Langer, 2011), with ten species formally described
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to date. Of these, Baurutitan britoi Kellner, Campos, and Trotta 2005, Trigonosaurus
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pricei Campos, Kellner, Bertini and Santucci 2005, and Uberabatitan ribeiroi Salgado
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and Carvalho 2008 have been found in the region of Uberaba, in the state of Minas
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Gerais, in Upper Cretaceous rocks belonging to the Bauru Group of the Bauru Basin.
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Fossils of juvenile sauropod individuals are rare, possibly because their small
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size made them more susceptible to taphonomic processes such as weathering,
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scavenging, and transport (Behrensmeyer et al., 1979; Carpenter and McIntosh, 1994).
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Although most juvenile sauropod specimens consist of fragmentary material (Peterson
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and Gilmore, 1902; Britt and Naylor, 1994; Martin, 1994; Foster, 2005; Candeiro et al.,
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2011), there are some notable
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titanosauriform described by Schwarz et al. (2007) and Carballido et al. (2012), a
exceptions, such as the enigmatic probable
ACCEPTED MANUSCRIPT juvenile of the titanosaur Alamosaurus sanjuanensis Gilmore, 1922 (Lehman and
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Coulson, 2002), some juvenile remains of Europasaurus holgeri Sander, Mateus and
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Knötschke, 2006 (Carballido and Sander, 2014), a juvenile Rapetosaurus krausei Curry
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Rogers and Forster, 2001 (Curry Rogers, 2009), the recent records of a juvenile
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specimen of Barosaurus March, 1890 (Melstrom et al., 2016), and a putative record
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from the Lower Cretaceous of Brazil (Ghilardi et al., 2016).
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Here we describe a juvenile specimen of a titanosaurian sauropod dinosaur from
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the Marilia Formation, Bauru Basin, Brazil. This is the first juvenile specimen
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recovered from this formation and the most complete occurrence of a juvenile sauropod
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from Brazil.
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2. Geological Context
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The material here was recovered from an exposure of the Serra da Galga
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Member of the Marília Formation (Upper Cretaceous: Maastrichtian) of the Bauru
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Group in the Bauru Basin (Fernandes and Coimbra, 1998, 2008; Dias-Brito et al., 2001;
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Paula e Silva, 2003). The Bauru Basin covers most of the western plateau of the state of
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São Paulo and also extends to the Triângulo Mineiro (i.e., the westernmost portion of
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Minas Gerais state), southern Goiás state, and southeastern Mato Grosso and northern
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Mato Grosso do Sul states (Ribeiro and Carvalho, 2009) (Fig. 1).
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The subsurface of the Bauru Basin is composed of basalts of the Serra Geral
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Formation that are overlain by 300 m of sedimentary rocks that pertain to two
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chronologically correlated units, the Caiuá Group and the Bauru Group (Fernandes and
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Coimbra, 1998, 2008). The Caiuá Group includes the Rio Paraná, Goio Erê, and Santo
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Anastácio formations, which are composed of thin to very thin aeolian sandstones, that
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Basin during the Early Cretaceous (Fernandes and Coimbra, 2008). The Bauru Group is
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composed of the Vale do Rio do Peixe, Araçatuba, Presidente Prudente, São José do Rio
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Preto, Uberaba and Marília formations (sensu Fernandes, 2004). However, some
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authors disagree with this stratigraphic proposal. For example, Batezelli (2015) divided
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the Bauru Group into the Araçatuba, Uberaba, Adamantina, and Marília formations
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(Soares et al., 1980), with the latter including the Vale do Rio do Peixe, São José do Rio
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Preto and Presidente Prudente formations of Fernandes (2004).
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The Marília Formation consists of fining-upward cycles, including matrix-
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supported conglomerates with intra- and extraformational clasts, fine to very coarse
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sandstones, and rare mudstones (Menegazzo et al., 2016). The formation is divided into
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three members: the Serra da Galga, Ponte Alta, and Echaporã members, with the former
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cropping out exclusively in the Uberaba region. The Serra da Galga Member stands out
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as one of the most important paleontological units in the entire Bauru Group, having
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produced approximately 15 formally described fossil vertebrate taxa that collectively
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include fishes, frogs, lizards, turtles, crocodyliforms, and dinosaurs (sauropods and
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theropods, the latter including birds) (see Martinelli and Teixeira, 2015, and references
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therein). The Serra da Galga Member has also yielded remains of invertebrates (e.g.,
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ostracods, gastropods, bivalves) and charophytes.
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Figure 1 here. 1.5 column
Fig. 1. Geological map of the Bauru Basin in Brazil. Modified from Fernandes and Coimbra (1996).
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3. Materials and Methods
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The specimens were recovered in 1991 from a site about 500 m from the
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outcrops where the type materials of Uberabatitan were found. The remains are housed
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at the Centro de Pesquisas Paleontológicas “Llwelyn Ivor Price” (CPPLIP) of the
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Universidade Federal do Triângulo Mineiro (UFTM). Throughout the description of the vertebrae we employ the terminology
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proposed by Wedel (2003) for the classification of pneumatic features, and the
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terminology proposed by Wilson (2006b) for the anatomical structures. Anterior and
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posterior are used in place of cranial and caudal, respectively.
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Institutional abbreviations. CPPLIP: Centro de Pesquisas Paleontológicas Llwellyn
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Ivor Price.
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4. Systematic paleontology
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SAUROPODA Marsh 1878
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MACRONARIA Wilson and Sereno 1998
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TITANOSAURIFORMES Salgado, Coria and Calvo 1997
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TITANOSAURIA Bonaparte and Coria 1993
Gen. et sp. Indet
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Figures: 5 figures
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Referred material: The material consists of two dorsal centra (CPPLIP 0032 and
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CPPLIP 0115), three caudal centra (CPPLIP 0031, CPPLIP 0086, and CPPLIP 0114), a
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partial right ilium (CPPLIP 0029), and a partial right ischium (CPPLIP 0034).
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Locality and horizon: Serra da Galga Member of the Marília Formation (Maastrichtian),
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in the Serra da Galga region at kilometer 153.5 of the highway BR-050, in the
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municipality of Uberaba, Minas Gerais state, Brazil.
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4.1 Taphonomic observations
The outcrop where the specimen was found no longer exist, it was destroyed
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during a highway expansion, so only limited information regarding the stratigraphic
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environment could be recovered. However, it was found close to the outcrop where
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Uberabatitan was discovered within a braided fluvial system on a conglomeratic level,
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and the corresponding stratigraphy can be seen in Salgado and Carvalho, 2008.
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Fossils discovered in the Serra da Galga Member of the Marília Formation
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mostly consist of disarticulated fragments, possibly related to strong seasonal
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fluctuations in sedimentary cycles (Garcia et al., 1999). The high degree of abrasion,
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including fractured and rounded surfaces, indicates that these taphonomic features were
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generated during transport in high-energy environments (Behrensmeyer, 1975;
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Behrensmeyer et al., 1979). This conclusion is supported by the transportability scheme
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introduced by Voorhies (1969), who demonstrated that elements of the axial column
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and pelvic girdle (his groups 1 and 2) display the highest potential for transport in
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fluvial systems – a situation that potentially accounts for the taphonomic signature of,
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e.g., the juvenile titanosaur taphocenosis.
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ACCEPTED MANUSCRIPT Due to their close association in the field, corresponding size, and similar
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preservation, the elements are considered to belong to a single titanosaurian individual.
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The specimens are fragmentary, indicating possible prediagenetic transport, a
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hypothesis that is reinforced by the fact that the neural arches were not found
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associated. These are delicate structures that could have been easily destroyed or
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disarticulated in immature animals (Martin, 1994).
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4.2 Descriptions and Comparisons
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Dorsal vertebrae: CPPLIP 0032 (Fig. 2A–E) is a well-preserved opisthocoelous
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dorsal centrum, lacking only a small portion of its right anterior face. The lateral faces
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are short with deep pleurocoels on both sides. The floor of the neural canal is deep and
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strongly concave, a feature commonly observed in juvenile sauropods, in which the
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neural canal is more conspicuously developed than in adults (Britt and Naylor, 1994). A
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small orifice, located roughly at the anterior portion of the neural canal, was made
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artificially during the preparation of the material. The contact surfaces with the neural
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arch show a pattern of ridges and grooves, indicating that the neurocentral suture was
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unfused, a typical feature of juveniles (Martin, 1994).
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Dorsal centrum CPPLIP 0115 (Fig. 2F–J), the centrum is poorly preserved and
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heavily eroded on its left lateral face, but the right pleurocoel is preserved, measuring 28
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mm anteroposteriorly and 15 mm dorsoventrally. The right contact surface for the
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neural arch is poorly preserved, as is the neural canal.
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In both CPPLIP 0032 and CPPLIP 0115, the centrum is much less ventrally
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concave than in dorsal centra of the Patagonian saltasaurine titanosaur Neuquensaurus
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australis Lydekker, 1893 (Salgado et al., 2005). However, the new juvenile centra are
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similar to the middle dorsal centra of Overosaurus paradasorum Coria, Filippi,
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Chiappe, García, and Arcucci, 2013. In lateral view, the ventral limits of the anterior
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condyles are slightly more pronounced than those of the posterior cotyles, but without
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the ventral crest present in Overosaurus (Coria et al., 2013). The pleurocoels are located on the anterior-most portion of the centrum as in
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Bonatitan reigi Martinelli and Forasiepi, 2004. CPPLIP 0032 is also similar to dorsal
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centra of Trigonosaurus in that both pleurocoels occupy the dorsal-most portion of the
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centrum.
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CPPLIP 0032 and CPPLIP 0115 differ from the dorsal centra of a juvenile
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specimen of the diplodocid Brontosaurus parvus (Tschopp et al., 2015) with respect to
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the ventral extension of the condyles and cotyles, which do not surpass the ventral
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margins of the main body of the centra in the latter. Furthermore, the pleurocoels of
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Brontosaurus are located on the posterior portion of the centrum, connected to the
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cotyle.
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Figure 2 here. 2-column
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Fig. 2. Juvenile Titanosauria indet. from the Serra da Galga Member of the Marília Formation. Dorsal centrum CPPLIP 0032 in anterior (A), posterior (B), left lateral (C), right lateral (D), and dorsal (E) views. Dorsal centrum CPPLIP 0115 in anterior (F), posterior (G), left lateral (H), right lateral (I), and dorsal (J) views.
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Caudal vertebrae: CPPLIP 0031 (Fig. 3A–D) is a well-preserved procoelous
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caudal vertebral centrum. Based on these measurements, and comparisons with the
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other two preserved caudal centra, this centrum clearly pertained to an anterior caudal
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vertebra. The lateral faces are short, with the posterior condyle occupying one-third of
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the anteroposterior length of the centrum. The contact surfaces for the neural arch are
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well defined and short, reinforcing the identification of the vertebra as an anterior
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caudal.
ACCEPTED MANUSCRIPT CPPLIP 0114 (Fig. 3E–F) is a very poorly preserved caudal centrum. The
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posterior condyle is broken and the lateral faces are short. The contact surface of the
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neural arch is not preserved and its right portion is fragmented. The neural canal is very
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large, which may indicate that the centrum belonged to another anterior caudal vertebra,
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but one that was positioned more posteriorly than CPPLIP 0031.
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CPPLIP 0086 (Fig. 3G–H) is another fragmentary caudal centrum that is similar
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in size to CPPLIP 0114. The contact surfaces for the neural arch are poorly preserved,
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as are both lateral sides of the centrum. The neural canal is large and well preserved. Its
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diameter and proportions indicate that the centrum was also positioned near CPPLIP
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0031, and therefore probably represents part of another anterior caudal.
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The absence of the neural arches precludes the identification of the position of
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both CPPLIP 0086 and CPPLIP 0114. However, assuming that they belong to the same
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individual as CPPLIP 0031, it is probable that they derive from the middle section of
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the caudal series insofar as they are not much smaller than the latter centrum. Relative
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to the anterior centrum, which shows a strongly procoelous condition and a robust
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condyle, the condyles and the cotyles of both mid caudal are only slightly developed.
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TABLE 1. Vertebral measurements (mm). The values followed by a * represents complete structures.
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Identification
Element Maximum Maximum Maximum
Condyle
Condyle Cotyle Cotyle
Lenght
width
Height
Height
Width
Height Width
CPPLIP 0032
Dorsal
62
60
48
37
52
46*
55*
CPPLIP 0115
Dorsal
62
60
66
43
51
32
63
CPPLIP 0031
Caudal
70*
59*
50*
46*
75*
49*
90*
CPPLIP 0086
Caudal
47
43
30
34
54
35
55
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Caudal
47
40
24
32
55
32
59
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The caudal centra clearly differ from those of Baurutitan due primarily to the
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absence of a pronounced rim framing the posterior condyle, the lack of a deep
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depression in its central portion, and the absence of a ‘heart-shaped’ anterior cotyle.
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This latter feature also differentiates the centra from those of Bonitasaura salgadoi
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Apesteguía, 2004. The new caudals also differ from those of Trigonosaurus in having
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lateral and ventral margins that are less concave and bounded by the condyle. Despite
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the fact that the transverse processes are not fully preserved in CPPLIP 0031, they are
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similar to those of Neuquensaurus in being positioned anteriorly on the centrum.
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Fig. 3. Juvenile Titanosauria indet. from the Serra da Galga Member of the Marília Formation. Caudal centrum CPPLIP 0031 in right lateral (A), left lateral (B), dorsal (C), and ventral (D) views. Caudal centrum CPPLIP 0114 in ventral (E) and dorsal (F) views. Caudal centrum CPPLIP 0086 in ventral (G) and dorsal (H) views.
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Figure 3 here. 2-column
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Ilium: CPPLIP 0034 (Fig. 4A–B) is a fragment of a right ilium. It measures 134
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mm in maximum length and 84 mm in preserved height. The proximal portion of the
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pubic peduncle is preserved; it is robust and anteroposteriorly flattened. A small portion
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of the preacetabular process is also present as a thin lamina.
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Ischium: CPPLIP 0029 (Fig. 4C–D) is an almost complete right ischium that
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measures 208 mm in greatest length and 120 mm in preserved height. It has a semilunar
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shape in medial and lateral views. The iliac peduncle is short and its anterior face is
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concave where it forms part of the acetabulum. The pubic peduncle is not preserved.
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TABLE 2. Pelvic girdle measurements (mm)
Element
Preserved Length
CPPLIP 0034
Ilium
134
CPPLIP 0029
Ischium
208
Preserved Height 84
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Identification
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The ilium is too fragmented for comparisons, However the ischium, although
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heavily abraded, is a narrow, lamina-like structure, similar in appearance to those of
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Neuquensaurus and Saltasaurus loricatus Bonaparte and Powell, 1980. The iliac
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peduncle appears to have been relatively gracile and less robust than in Rapetsaurus or
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Nequensaurus.
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Fig. 4. Juvenile Titanosauria indet. from the Serra da Galga Member of the Marília Formation. Right lium CPPLIP 0034 in lateral (A) and medial (B) views. Right ischium CPPLIP 0029 in medial (C) and lateral (D) views.
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Figure 4 here. 2-column
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4.3 Pneumaticity
Postcranial pneumaticity in sauropod dinosaurs has been the subject of much
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investigation in recent years (Cerda et al., 2012; Wedel and Taylor, 2013).
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Pneumatization of the axial skeleton would have dramatically reduced its total mass and
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undoubtedly helped sauropods reach their massive body sizes (Wedel, 2009). Vertebral
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laminae (the series of thin, bony struts connecting the major vertebral landmarks) are
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thus best conceived of as a correlate of axial pneumaticity in saurischians, bounding
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negative space filled by pneumatic diverticula (Wilson, 1999). Wedel (2003a) introduced a classificatory scheme in order to standardize the
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defining characteristics of pneumaticity in sauropod vertebrae. Among these, two types
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of pneumaticity were described in titanosaurs: (1) camellate pneumaticity, which is
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characterized by the presence of camellae with generally small, angular cavities bearing
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irregular margins; and (2) camerate pneumaticity, which is characterized by the
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presence of camerae with generally larger, rounded cavities having regular margins
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(sensu Wedel, 2003a).
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In the right pleurocoel of CPPLIP 0115 there are three rounded camerae with
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well-defined margins (Fig. 5). In contrast, the pleurocoels of CPPLIP 0032, there are
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two deeper and larger camerae. The preserved elements thus demonstrate that, in this
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juvenile titanosaur, axial skeletal pneumaticity extended to the thoracic region and did
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not have a homogeneous distribution. CPPLIP 0115 is an anterior dorsal centrum with
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camerae that are smaller and shallower than those of the more posterior centrum
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CPPLIP 0032. In this respect, CPPLIP 0032 and CPPLIP 0115 differ conspicuously
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from dorsal vertebrae of adult specimens of Uberabatitan (e.g., CPPLIP 1077), which
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have only a single deep camera with well-defined margins. The juvenile vertebrae also
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differ from dorsal vertebrae of Trigonosaurus (CPPLIP 0361), which have a deep
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camera that lacks defined margins.
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The new material also differs from dorsal vertebrae of Gondwanatitan faustoi
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Kellner and Azevedo, 1999 with respect to the morphology of its pleurocoels, which in
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the latter are located on the Uppermost portions of the centra, immediately ventral to the
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neural arch, and are deep and elongated with poorly defined camerae. Similarly, the
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Early Cretaceous titanosaur Tapuiasaurus macedoi Zaher, Pol, Carvalho, Nascimento,
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Riccomini, Larson, Juárez Valieri, Silva, and Campos, 2011 has proportionally larger
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pleurocoels with poorly defined camerae (Zaher et al., 2011). The caudal centrum of the juvenile specimen does not show any pneumaticity,
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differing from some Saltasaurinae taxa (Cerda et al., 2012) and other sauropods (Wedel
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and Taylor, 2013).
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Fig. 5. Photograph (left) and interpretive drawing (right) of dorsal centrum CPPLIP 0115 in right lateral view, showing three camerae within the pleurocoel. This stage of development corresponds to morphological ontogenetic stage 3 proposed by Carballido and Sander (2014).
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Figure 5 here. 1.5 column
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6. Discussion
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The dorsal centra reported herein (CPPLIP 0032 and CPPLIP 0115) differ from
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those of other juvenile titanosaurs, such as the juvenile skeleton of Rapetosaurus (Curry
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Rogers, 2009), in which the dorsoventral diameter of the centrum is greater than its
324
width and the posterior articular cotyle is deeper. The new centra are nearly as wide as
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tall, and their cotyles are not as deep as in Rapetosaurus. The same applies to dorsal
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centra of juvenile individuals of the Jurassic macronarian Europasaurus (Carballido and
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Sander, 2014), which have more strongly concave ventral faces and posterior cotyles
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that are larger than their respective anterior condyles. Similarly, in a juvenile dorsal
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centrum of Phuwiangosaurus sirindhornae Martin, Buffetaut, and Suteethorn, 1994, the
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ventral face is also more concave, and the pleurocoel is located more posteriorly than in
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the new Serra da Galga specimen (Martin, 1994).
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Despite their generally poor preservation, it is notable that the caudal centra of
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the new specimen have less concave ventral surfaces than in those of caudals of the
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three titanosaurian genera previously described from the same region: Baurutitan,
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Trigonosaurus, and Uberabatitan. Nevertheless, with its slightly concave ventral face
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and a posterior condyle that is slightly larger than the anterior cotyle, CPPLIP 0031 is
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more similar to the most anterior preserved caudal of Rapetosaurus. Even though the juvenile elements described herein collectively preserve few
339
diagnostic features, the strongly procoelous condition of the anterior caudal centrum is a
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character of Titanosauria (Filippi et al., 2011; D’emic, 2012), and allow us to include
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CPPLIP 0031 (and all of the elements presuming they belong to the same individual) in
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this clade.
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Wilson (2002) proposed the character “anterior and middle caudal vertebrae
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procoelous” as a synapomorphy of the clade Lithostrotia (Upchurch, Barrett, and
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Dodson, 2004). However, this character appears several times outside Lithostrotia, such
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as Dreadnought schrani Lacovara et al., 2014, Mendozasaurus neguyelap González
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Riga, 2003 and Malawisaurus dixeyi Jacobs et al., 1993. Even in some lithostrotian
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titanosaurian species the procoelous condition of the anterior caudal centra are variable:
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Rincosaurus caudimirus Calvo and González Riga, 2003 has procoelous anterior
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caudals followed by a series of amphicoelous, opisthocoelous and biconvex centra, and
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Baurutitan has the first caudal biconvex - acondition that may also be present on
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Neuquensaurus (D’emic and Wilson, 2010).
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Most, if not all, Brazilian Late Cretaceous titanosaur taxa such as Baurutitan
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(Santucci and Arruda-Campos, 2011), Trigonosaurus (Mannion and Otero, 2012; Juárez
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Valieri and Ríos Díaz, 2013), and Uberabatitan are also considered to be members of
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Lithostrotia. Based on the geological and geographical context, we also suggest that the
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Peirópolis specimen has affinities with Lithostrotia. CPPLIP 0086 and 0114 possesses a
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dorsoventrally compressed centrum, a characteristic of Saltasaurinae (Powell, 2003) and
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may be related with this clade. The presence of pneumatic camerae in the dorsal centra indicates that the
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specimen was not extremely immature at death; rather, it corresponds to the
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morphological ontogenetic stage (MOS) 3 of Carballido and Sander (2014) (which was
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proposed by these authors based on their study of the ontogeny of Europasaurus). In a
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recent study, Melstrom et al. (2016) supported the hypothesis that, in neosauropods,
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vertebral pneumaticity developed early in ontogeny, first in the cervical series and later
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extending to other vertebrae.
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The Serra da Galga specimen pertains to MOS 3; furthermore, based on the
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presence of pneumatic camerae in its dorsal centra, it probably already possessed air sac
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diverticula in the thoracic region. Therefore, the titanosaurian respiratory system was
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probably completely developed at an early ontogenetic stage and a correspondingly
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small body size. This supports the hypothesis of “ontogenetic canalization” in
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titanosaurs proposed by Curry Rogers et al. (2016), who demonstrated via studies of the
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juvenile Rapetosaurus that osteologically immature titanosaurs were nearly identical in
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morphology to adults except for their size.
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The dorsal centra CPPLIP 0032 and CPPLIP 0115 bear pneumatic fossae that
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differ in morphology from those of other titanosaurian taxa found in the same region,
377
such as Trigonosaurus and Uberabatitan. This suggests that the new juvenile specimen
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may belong to a different lithostrotian species, and that the pleurocoels may become
379
progressively smaller but not change in overall shape. During growth the vertebral
380
pneumaticity of sauropod individual becomes better developed due to the expansion of
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either the cervical or abdominal air sac diverticulae (Wedel, 2003b; Salgado et al.,
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2006); a change hypothesized to reduce the weight of the skeleton and/or increase
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oxygen consumption in response to the elevated metabolic demands brought about by
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large body size. Finally, some workers have argued that sauropods show signs of gregarious
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behavior (Salgado et al., 2012). With respect to titanosaurs, it has been suggested that if
387
this behavior was not present, females at least would have aggregated periodically
388
during the ovipositional season (Chiappe et al., 2005, García et al., 2015). Price (1951)
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reported sauropods eggs within the Marília Formation, and although no juveniles have
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been found associated with these eggs, the synformational presence of both eggs and
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juveniles with adult titanosaurs suggests that animals of different ontogenetic stages
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shared a common environment.
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7. Conclusions
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In conclusion, although fragmentary, the juvenile titanosaurian specimen
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described herein to lends further support to hypotheses of isometric growth in
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titanosaurs, and may also represent a species distinct from those that have already been
399
found in the Uberaba region. Furthermore, the presence of titanosaur eggs and
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individuals of different ontogenetic stages in the area bolsters the idea that the local
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paleoenvironment was conducive to both titanosaurian nesting as well as supporting a
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taxonomically diverse sauropod fauna.
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Acknowledgments
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We thank the continuous support of all the staff of the Complexo Cultural e
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Cientifico de Peirópolis of the Universidade Federal do Triângulo Mineiro, Uberaba,
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Minas Gerais. This research was beneficiated by the financial support of the the
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Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and
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Fundação de Amparo à Pesquisa de Minas Gerais (FAPEMIG). We also thank Matthew
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C. Lamanna, Blair W. McPhee and both anonymous reviewers for comments that
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greatly improved the strength of this contribution.
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S0195-6671(16)30391-3
DOI:
10.1016/j.cretres.2017.03.029
Reference:
YCRES 3575
To appear in:
Cretaceous Research
Received Date: 15 December 2016 Revised Date:
27 March 2017
Accepted Date: 30 March 2017
Please cite this article as: Silva Junior, J.C.G., Martinelli, A.G., Ribeiro, L.C.B., Marinho, T.S., Description of a juvenile titanosaurian dinosaur from the Upper Cretaceous of Brazil, Cretaceous Research (2017), doi: 10.1016/j.cretres.2017.03.029. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Description of a juvenile titanosaurian dinosaur from the Upper
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Cretaceous of Brazil
3 Julian C. G. Silva Junior1,4*, Agustín G. Martinelli4,3, Luiz C. B. Ribeiro4, Thiago S. Marinho2,4
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Preto, Universidade de São Paulo, Av. Bandeirantes, 3900, 14040-901, Ribeirão Preto, São Paulo, Brazil
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Departamento de Ciências Biológicas, Avenida Doutor Randolfo Borges Júnior, 38064-200, Uberaba,
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Laboratório de Paleontologia de Ribeirão Preto, Faculdade de Filosofia, Ciências e Letras de Ribeirão
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Instituto de Ciências Exatas, Naturais e Educação, Universidade Federal do Triângulo Mineiro,
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Minas Gerais, Brazil.
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Grande do Sul, Ave. Bento Gonçalves 9500, Agronomia, 91540–000, Porto Alegre, Rio Grande do Sul,
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Brazil.
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Peirópolis, Estanislau Collenghi 194, 38039-755, Peirópolis, Uberaba, Minas Gerais, Brazil.
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Departamento de Paleontologia e Estratigrafia, Instituto de Geociências, Universidade Federal do Rio
Centro de Pesquisas Paleontológicas “Llwelyn Ivor Price”, Universidade Federal do Triângulo Mineiro,
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* Corresponding author: [email protected]
Abstract: We describe a juvenile specimen of a titanosaurian sauropod dinosaur
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consisting of two dorsal and three caudal vertebral centra, an ilium fragment, and an ischium
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unearthed in 1991 from Site Km 153.5 of highway BR-050 in the Serra da Galga region,
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municipality of Uberaba, state of Minas Gerais, Brazil. The outcrop at the site is assigned to the
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Serra da Galga Member of the Marília Formation (Bauru Basin: Bauru Group; Upper
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Cretaceous: Maastrichtian). Although the material is very incomplete, features such as strongly
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procoelous caudal centra suggest an affinity with the titanosaurian clade Lithostrotia. The
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extensive vertebral pneumaticity with deep pleurocoels and well-developed camerae supports
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the hypothesis that, in titanosaurs, the air sac system was already present and fully developed
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even at early ontogenetic stages.
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Keywords: Sauropoda, Titanosauria, juvenile, Marília Formation, Upper Cretaceous, ontogeny, pneumaticity
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1. Introduction
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Titanosaurs represent the last great radiation of sauropod dinosaurs, with a
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globally distributed body-fossil record dating back to at least the late Early Cretaceous
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(D’emic, 2012). They are easily differentiated from other sauropods by a characteristic
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suite of features such as anterior and middle caudal vertebrae with a ventral longitudinal
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hollow (convergent in diplodocids), a platelike ischium with no emargination distal to
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pubic peduncle, six or seven sacral vertebraeand reduction of the articular surfaces for
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the manual phalanges on the metacarpals (e.g., Salgado et al., 1997; Wilson and Sereno,
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1998; Wilson, 2002; Wilson, 2006a). In the Cretaceous fossil record of Brazil
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titanosaurs represent the dinosaur clade with the highest taxonomic abundance (Kellner,
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1999; Novas, 2009; Bittencout and Langer, 2011), with ten species formally described
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to date. Of these, Baurutitan britoi Kellner, Campos, and Trotta 2005, Trigonosaurus
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pricei Campos, Kellner, Bertini and Santucci 2005, and Uberabatitan ribeiroi Salgado
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and Carvalho 2008 have been found in the region of Uberaba, in the state of Minas
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Gerais, in Upper Cretaceous rocks belonging to the Bauru Group of the Bauru Basin.
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Fossils of juvenile sauropod individuals are rare, possibly because their small
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size made them more susceptible to taphonomic processes such as weathering,
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scavenging, and transport (Behrensmeyer et al., 1979; Carpenter and McIntosh, 1994).
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Although most juvenile sauropod specimens consist of fragmentary material (Peterson
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and Gilmore, 1902; Britt and Naylor, 1994; Martin, 1994; Foster, 2005; Candeiro et al.,
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2011), there are some notable
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titanosauriform described by Schwarz et al. (2007) and Carballido et al. (2012), a
exceptions, such as the enigmatic probable
ACCEPTED MANUSCRIPT juvenile of the titanosaur Alamosaurus sanjuanensis Gilmore, 1922 (Lehman and
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Coulson, 2002), some juvenile remains of Europasaurus holgeri Sander, Mateus and
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Knötschke, 2006 (Carballido and Sander, 2014), a juvenile Rapetosaurus krausei Curry
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Rogers and Forster, 2001 (Curry Rogers, 2009), the recent records of a juvenile
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specimen of Barosaurus March, 1890 (Melstrom et al., 2016), and a putative record
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from the Lower Cretaceous of Brazil (Ghilardi et al., 2016).
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Here we describe a juvenile specimen of a titanosaurian sauropod dinosaur from
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the Marilia Formation, Bauru Basin, Brazil. This is the first juvenile specimen
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recovered from this formation and the most complete occurrence of a juvenile sauropod
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from Brazil.
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2. Geological Context
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The material here was recovered from an exposure of the Serra da Galga
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Member of the Marília Formation (Upper Cretaceous: Maastrichtian) of the Bauru
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Group in the Bauru Basin (Fernandes and Coimbra, 1998, 2008; Dias-Brito et al., 2001;
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Paula e Silva, 2003). The Bauru Basin covers most of the western plateau of the state of
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São Paulo and also extends to the Triângulo Mineiro (i.e., the westernmost portion of
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Minas Gerais state), southern Goiás state, and southeastern Mato Grosso and northern
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Mato Grosso do Sul states (Ribeiro and Carvalho, 2009) (Fig. 1).
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The subsurface of the Bauru Basin is composed of basalts of the Serra Geral
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Formation that are overlain by 300 m of sedimentary rocks that pertain to two
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chronologically correlated units, the Caiuá Group and the Bauru Group (Fernandes and
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Coimbra, 1998, 2008). The Caiuá Group includes the Rio Paraná, Goio Erê, and Santo
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Anastácio formations, which are composed of thin to very thin aeolian sandstones, that
ACCEPTED MANUSCRIPT were deposited in a paleodesert that extended across the inner portion of the Bauru
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Basin during the Early Cretaceous (Fernandes and Coimbra, 2008). The Bauru Group is
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composed of the Vale do Rio do Peixe, Araçatuba, Presidente Prudente, São José do Rio
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Preto, Uberaba and Marília formations (sensu Fernandes, 2004). However, some
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authors disagree with this stratigraphic proposal. For example, Batezelli (2015) divided
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the Bauru Group into the Araçatuba, Uberaba, Adamantina, and Marília formations
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(Soares et al., 1980), with the latter including the Vale do Rio do Peixe, São José do Rio
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Preto and Presidente Prudente formations of Fernandes (2004).
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The Marília Formation consists of fining-upward cycles, including matrix-
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supported conglomerates with intra- and extraformational clasts, fine to very coarse
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sandstones, and rare mudstones (Menegazzo et al., 2016). The formation is divided into
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three members: the Serra da Galga, Ponte Alta, and Echaporã members, with the former
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cropping out exclusively in the Uberaba region. The Serra da Galga Member stands out
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as one of the most important paleontological units in the entire Bauru Group, having
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produced approximately 15 formally described fossil vertebrate taxa that collectively
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include fishes, frogs, lizards, turtles, crocodyliforms, and dinosaurs (sauropods and
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theropods, the latter including birds) (see Martinelli and Teixeira, 2015, and references
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therein). The Serra da Galga Member has also yielded remains of invertebrates (e.g.,
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ostracods, gastropods, bivalves) and charophytes.
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Figure 1 here. 1.5 column
Fig. 1. Geological map of the Bauru Basin in Brazil. Modified from Fernandes and Coimbra (1996).
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3. Materials and Methods
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The specimens were recovered in 1991 from a site about 500 m from the
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outcrops where the type materials of Uberabatitan were found. The remains are housed
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at the Centro de Pesquisas Paleontológicas “Llwelyn Ivor Price” (CPPLIP) of the
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Universidade Federal do Triângulo Mineiro (UFTM). Throughout the description of the vertebrae we employ the terminology
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proposed by Wedel (2003) for the classification of pneumatic features, and the
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terminology proposed by Wilson (2006b) for the anatomical structures. Anterior and
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posterior are used in place of cranial and caudal, respectively.
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Institutional abbreviations. CPPLIP: Centro de Pesquisas Paleontológicas Llwellyn
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Ivor Price.
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4. Systematic paleontology
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SAUROPODA Marsh 1878
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MACRONARIA Wilson and Sereno 1998
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TITANOSAURIFORMES Salgado, Coria and Calvo 1997
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TITANOSAURIA Bonaparte and Coria 1993
Gen. et sp. Indet
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Figures: 5 figures
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Referred material: The material consists of two dorsal centra (CPPLIP 0032 and
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CPPLIP 0115), three caudal centra (CPPLIP 0031, CPPLIP 0086, and CPPLIP 0114), a
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partial right ilium (CPPLIP 0029), and a partial right ischium (CPPLIP 0034).
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Locality and horizon: Serra da Galga Member of the Marília Formation (Maastrichtian),
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in the Serra da Galga region at kilometer 153.5 of the highway BR-050, in the
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municipality of Uberaba, Minas Gerais state, Brazil.
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4.1 Taphonomic observations
The outcrop where the specimen was found no longer exist, it was destroyed
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during a highway expansion, so only limited information regarding the stratigraphic
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environment could be recovered. However, it was found close to the outcrop where
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Uberabatitan was discovered within a braided fluvial system on a conglomeratic level,
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and the corresponding stratigraphy can be seen in Salgado and Carvalho, 2008.
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Fossils discovered in the Serra da Galga Member of the Marília Formation
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mostly consist of disarticulated fragments, possibly related to strong seasonal
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fluctuations in sedimentary cycles (Garcia et al., 1999). The high degree of abrasion,
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including fractured and rounded surfaces, indicates that these taphonomic features were
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generated during transport in high-energy environments (Behrensmeyer, 1975;
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Behrensmeyer et al., 1979). This conclusion is supported by the transportability scheme
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introduced by Voorhies (1969), who demonstrated that elements of the axial column
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and pelvic girdle (his groups 1 and 2) display the highest potential for transport in
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fluvial systems – a situation that potentially accounts for the taphonomic signature of,
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e.g., the juvenile titanosaur taphocenosis.
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ACCEPTED MANUSCRIPT Due to their close association in the field, corresponding size, and similar
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preservation, the elements are considered to belong to a single titanosaurian individual.
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The specimens are fragmentary, indicating possible prediagenetic transport, a
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hypothesis that is reinforced by the fact that the neural arches were not found
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associated. These are delicate structures that could have been easily destroyed or
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disarticulated in immature animals (Martin, 1994).
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4.2 Descriptions and Comparisons
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Dorsal vertebrae: CPPLIP 0032 (Fig. 2A–E) is a well-preserved opisthocoelous
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dorsal centrum, lacking only a small portion of its right anterior face. The lateral faces
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are short with deep pleurocoels on both sides. The floor of the neural canal is deep and
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strongly concave, a feature commonly observed in juvenile sauropods, in which the
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neural canal is more conspicuously developed than in adults (Britt and Naylor, 1994). A
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small orifice, located roughly at the anterior portion of the neural canal, was made
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artificially during the preparation of the material. The contact surfaces with the neural
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arch show a pattern of ridges and grooves, indicating that the neurocentral suture was
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unfused, a typical feature of juveniles (Martin, 1994).
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Dorsal centrum CPPLIP 0115 (Fig. 2F–J), the centrum is poorly preserved and
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heavily eroded on its left lateral face, but the right pleurocoel is preserved, measuring 28
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mm anteroposteriorly and 15 mm dorsoventrally. The right contact surface for the
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neural arch is poorly preserved, as is the neural canal.
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In both CPPLIP 0032 and CPPLIP 0115, the centrum is much less ventrally
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concave than in dorsal centra of the Patagonian saltasaurine titanosaur Neuquensaurus
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australis Lydekker, 1893 (Salgado et al., 2005). However, the new juvenile centra are
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similar to the middle dorsal centra of Overosaurus paradasorum Coria, Filippi,
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Chiappe, García, and Arcucci, 2013. In lateral view, the ventral limits of the anterior
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condyles are slightly more pronounced than those of the posterior cotyles, but without
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the ventral crest present in Overosaurus (Coria et al., 2013). The pleurocoels are located on the anterior-most portion of the centrum as in
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Bonatitan reigi Martinelli and Forasiepi, 2004. CPPLIP 0032 is also similar to dorsal
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centra of Trigonosaurus in that both pleurocoels occupy the dorsal-most portion of the
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centrum.
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CPPLIP 0032 and CPPLIP 0115 differ from the dorsal centra of a juvenile
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specimen of the diplodocid Brontosaurus parvus (Tschopp et al., 2015) with respect to
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the ventral extension of the condyles and cotyles, which do not surpass the ventral
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margins of the main body of the centra in the latter. Furthermore, the pleurocoels of
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Brontosaurus are located on the posterior portion of the centrum, connected to the
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cotyle.
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Figure 2 here. 2-column
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Fig. 2. Juvenile Titanosauria indet. from the Serra da Galga Member of the Marília Formation. Dorsal centrum CPPLIP 0032 in anterior (A), posterior (B), left lateral (C), right lateral (D), and dorsal (E) views. Dorsal centrum CPPLIP 0115 in anterior (F), posterior (G), left lateral (H), right lateral (I), and dorsal (J) views.
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Caudal vertebrae: CPPLIP 0031 (Fig. 3A–D) is a well-preserved procoelous
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caudal vertebral centrum. Based on these measurements, and comparisons with the
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other two preserved caudal centra, this centrum clearly pertained to an anterior caudal
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vertebra. The lateral faces are short, with the posterior condyle occupying one-third of
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the anteroposterior length of the centrum. The contact surfaces for the neural arch are
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well defined and short, reinforcing the identification of the vertebra as an anterior
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caudal.
ACCEPTED MANUSCRIPT CPPLIP 0114 (Fig. 3E–F) is a very poorly preserved caudal centrum. The
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posterior condyle is broken and the lateral faces are short. The contact surface of the
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neural arch is not preserved and its right portion is fragmented. The neural canal is very
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large, which may indicate that the centrum belonged to another anterior caudal vertebra,
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but one that was positioned more posteriorly than CPPLIP 0031.
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CPPLIP 0086 (Fig. 3G–H) is another fragmentary caudal centrum that is similar
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in size to CPPLIP 0114. The contact surfaces for the neural arch are poorly preserved,
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as are both lateral sides of the centrum. The neural canal is large and well preserved. Its
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diameter and proportions indicate that the centrum was also positioned near CPPLIP
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0031, and therefore probably represents part of another anterior caudal.
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The absence of the neural arches precludes the identification of the position of
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both CPPLIP 0086 and CPPLIP 0114. However, assuming that they belong to the same
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individual as CPPLIP 0031, it is probable that they derive from the middle section of
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the caudal series insofar as they are not much smaller than the latter centrum. Relative
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to the anterior centrum, which shows a strongly procoelous condition and a robust
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condyle, the condyles and the cotyles of both mid caudal are only slightly developed.
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TABLE 1. Vertebral measurements (mm). The values followed by a * represents complete structures.
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Identification
Element Maximum Maximum Maximum
Condyle
Condyle Cotyle Cotyle
Lenght
width
Height
Height
Width
Height Width
CPPLIP 0032
Dorsal
62
60
48
37
52
46*
55*
CPPLIP 0115
Dorsal
62
60
66
43
51
32
63
CPPLIP 0031
Caudal
70*
59*
50*
46*
75*
49*
90*
CPPLIP 0086
Caudal
47
43
30
34
54
35
55
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Caudal
47
40
24
32
55
32
59
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The caudal centra clearly differ from those of Baurutitan due primarily to the
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absence of a pronounced rim framing the posterior condyle, the lack of a deep
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depression in its central portion, and the absence of a ‘heart-shaped’ anterior cotyle.
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This latter feature also differentiates the centra from those of Bonitasaura salgadoi
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Apesteguía, 2004. The new caudals also differ from those of Trigonosaurus in having
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lateral and ventral margins that are less concave and bounded by the condyle. Despite
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the fact that the transverse processes are not fully preserved in CPPLIP 0031, they are
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similar to those of Neuquensaurus in being positioned anteriorly on the centrum.
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Fig. 3. Juvenile Titanosauria indet. from the Serra da Galga Member of the Marília Formation. Caudal centrum CPPLIP 0031 in right lateral (A), left lateral (B), dorsal (C), and ventral (D) views. Caudal centrum CPPLIP 0114 in ventral (E) and dorsal (F) views. Caudal centrum CPPLIP 0086 in ventral (G) and dorsal (H) views.
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Figure 3 here. 2-column
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Ilium: CPPLIP 0034 (Fig. 4A–B) is a fragment of a right ilium. It measures 134
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mm in maximum length and 84 mm in preserved height. The proximal portion of the
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pubic peduncle is preserved; it is robust and anteroposteriorly flattened. A small portion
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of the preacetabular process is also present as a thin lamina.
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Ischium: CPPLIP 0029 (Fig. 4C–D) is an almost complete right ischium that
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measures 208 mm in greatest length and 120 mm in preserved height. It has a semilunar
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shape in medial and lateral views. The iliac peduncle is short and its anterior face is
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concave where it forms part of the acetabulum. The pubic peduncle is not preserved.
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TABLE 2. Pelvic girdle measurements (mm)
Element
Preserved Length
CPPLIP 0034
Ilium
134
CPPLIP 0029
Ischium
208
Preserved Height 84
120
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Identification
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The ilium is too fragmented for comparisons, However the ischium, although
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heavily abraded, is a narrow, lamina-like structure, similar in appearance to those of
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Neuquensaurus and Saltasaurus loricatus Bonaparte and Powell, 1980. The iliac
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peduncle appears to have been relatively gracile and less robust than in Rapetsaurus or
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Nequensaurus.
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Fig. 4. Juvenile Titanosauria indet. from the Serra da Galga Member of the Marília Formation. Right lium CPPLIP 0034 in lateral (A) and medial (B) views. Right ischium CPPLIP 0029 in medial (C) and lateral (D) views.
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Figure 4 here. 2-column
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4.3 Pneumaticity
Postcranial pneumaticity in sauropod dinosaurs has been the subject of much
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investigation in recent years (Cerda et al., 2012; Wedel and Taylor, 2013).
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Pneumatization of the axial skeleton would have dramatically reduced its total mass and
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undoubtedly helped sauropods reach their massive body sizes (Wedel, 2009). Vertebral
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laminae (the series of thin, bony struts connecting the major vertebral landmarks) are
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thus best conceived of as a correlate of axial pneumaticity in saurischians, bounding
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negative space filled by pneumatic diverticula (Wilson, 1999). Wedel (2003a) introduced a classificatory scheme in order to standardize the
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defining characteristics of pneumaticity in sauropod vertebrae. Among these, two types
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of pneumaticity were described in titanosaurs: (1) camellate pneumaticity, which is
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characterized by the presence of camellae with generally small, angular cavities bearing
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irregular margins; and (2) camerate pneumaticity, which is characterized by the
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presence of camerae with generally larger, rounded cavities having regular margins
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(sensu Wedel, 2003a).
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In the right pleurocoel of CPPLIP 0115 there are three rounded camerae with
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well-defined margins (Fig. 5). In contrast, the pleurocoels of CPPLIP 0032, there are
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two deeper and larger camerae. The preserved elements thus demonstrate that, in this
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juvenile titanosaur, axial skeletal pneumaticity extended to the thoracic region and did
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not have a homogeneous distribution. CPPLIP 0115 is an anterior dorsal centrum with
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camerae that are smaller and shallower than those of the more posterior centrum
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CPPLIP 0032. In this respect, CPPLIP 0032 and CPPLIP 0115 differ conspicuously
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from dorsal vertebrae of adult specimens of Uberabatitan (e.g., CPPLIP 1077), which
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have only a single deep camera with well-defined margins. The juvenile vertebrae also
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differ from dorsal vertebrae of Trigonosaurus (CPPLIP 0361), which have a deep
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camera that lacks defined margins.
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The new material also differs from dorsal vertebrae of Gondwanatitan faustoi
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Kellner and Azevedo, 1999 with respect to the morphology of its pleurocoels, which in
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the latter are located on the Uppermost portions of the centra, immediately ventral to the
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neural arch, and are deep and elongated with poorly defined camerae. Similarly, the
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Early Cretaceous titanosaur Tapuiasaurus macedoi Zaher, Pol, Carvalho, Nascimento,
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Riccomini, Larson, Juárez Valieri, Silva, and Campos, 2011 has proportionally larger
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pleurocoels with poorly defined camerae (Zaher et al., 2011). The caudal centrum of the juvenile specimen does not show any pneumaticity,
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differing from some Saltasaurinae taxa (Cerda et al., 2012) and other sauropods (Wedel
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and Taylor, 2013).
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Fig. 5. Photograph (left) and interpretive drawing (right) of dorsal centrum CPPLIP 0115 in right lateral view, showing three camerae within the pleurocoel. This stage of development corresponds to morphological ontogenetic stage 3 proposed by Carballido and Sander (2014).
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Figure 5 here. 1.5 column
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6. Discussion
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The dorsal centra reported herein (CPPLIP 0032 and CPPLIP 0115) differ from
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those of other juvenile titanosaurs, such as the juvenile skeleton of Rapetosaurus (Curry
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Rogers, 2009), in which the dorsoventral diameter of the centrum is greater than its
324
width and the posterior articular cotyle is deeper. The new centra are nearly as wide as
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tall, and their cotyles are not as deep as in Rapetosaurus. The same applies to dorsal
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centra of juvenile individuals of the Jurassic macronarian Europasaurus (Carballido and
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Sander, 2014), which have more strongly concave ventral faces and posterior cotyles
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that are larger than their respective anterior condyles. Similarly, in a juvenile dorsal
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centrum of Phuwiangosaurus sirindhornae Martin, Buffetaut, and Suteethorn, 1994, the
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ventral face is also more concave, and the pleurocoel is located more posteriorly than in
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the new Serra da Galga specimen (Martin, 1994).
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Despite their generally poor preservation, it is notable that the caudal centra of
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the new specimen have less concave ventral surfaces than in those of caudals of the
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three titanosaurian genera previously described from the same region: Baurutitan,
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Trigonosaurus, and Uberabatitan. Nevertheless, with its slightly concave ventral face
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and a posterior condyle that is slightly larger than the anterior cotyle, CPPLIP 0031 is
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more similar to the most anterior preserved caudal of Rapetosaurus. Even though the juvenile elements described herein collectively preserve few
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diagnostic features, the strongly procoelous condition of the anterior caudal centrum is a
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character of Titanosauria (Filippi et al., 2011; D’emic, 2012), and allow us to include
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CPPLIP 0031 (and all of the elements presuming they belong to the same individual) in
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this clade.
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Wilson (2002) proposed the character “anterior and middle caudal vertebrae
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procoelous” as a synapomorphy of the clade Lithostrotia (Upchurch, Barrett, and
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Dodson, 2004). However, this character appears several times outside Lithostrotia, such
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as Dreadnought schrani Lacovara et al., 2014, Mendozasaurus neguyelap González
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Riga, 2003 and Malawisaurus dixeyi Jacobs et al., 1993. Even in some lithostrotian
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titanosaurian species the procoelous condition of the anterior caudal centra are variable:
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Rincosaurus caudimirus Calvo and González Riga, 2003 has procoelous anterior
350
caudals followed by a series of amphicoelous, opisthocoelous and biconvex centra, and
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Baurutitan has the first caudal biconvex - acondition that may also be present on
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Neuquensaurus (D’emic and Wilson, 2010).
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Most, if not all, Brazilian Late Cretaceous titanosaur taxa such as Baurutitan
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(Santucci and Arruda-Campos, 2011), Trigonosaurus (Mannion and Otero, 2012; Juárez
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Valieri and Ríos Díaz, 2013), and Uberabatitan are also considered to be members of
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Lithostrotia. Based on the geological and geographical context, we also suggest that the
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Peirópolis specimen has affinities with Lithostrotia. CPPLIP 0086 and 0114 possesses a
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dorsoventrally compressed centrum, a characteristic of Saltasaurinae (Powell, 2003) and
359
may be related with this clade. The presence of pneumatic camerae in the dorsal centra indicates that the
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specimen was not extremely immature at death; rather, it corresponds to the
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morphological ontogenetic stage (MOS) 3 of Carballido and Sander (2014) (which was
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proposed by these authors based on their study of the ontogeny of Europasaurus). In a
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recent study, Melstrom et al. (2016) supported the hypothesis that, in neosauropods,
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vertebral pneumaticity developed early in ontogeny, first in the cervical series and later
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extending to other vertebrae.
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The Serra da Galga specimen pertains to MOS 3; furthermore, based on the
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presence of pneumatic camerae in its dorsal centra, it probably already possessed air sac
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diverticula in the thoracic region. Therefore, the titanosaurian respiratory system was
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probably completely developed at an early ontogenetic stage and a correspondingly
371
small body size. This supports the hypothesis of “ontogenetic canalization” in
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titanosaurs proposed by Curry Rogers et al. (2016), who demonstrated via studies of the
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juvenile Rapetosaurus that osteologically immature titanosaurs were nearly identical in
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morphology to adults except for their size.
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The dorsal centra CPPLIP 0032 and CPPLIP 0115 bear pneumatic fossae that
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differ in morphology from those of other titanosaurian taxa found in the same region,
377
such as Trigonosaurus and Uberabatitan. This suggests that the new juvenile specimen
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may belong to a different lithostrotian species, and that the pleurocoels may become
379
progressively smaller but not change in overall shape. During growth the vertebral
380
pneumaticity of sauropod individual becomes better developed due to the expansion of
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either the cervical or abdominal air sac diverticulae (Wedel, 2003b; Salgado et al.,
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2006); a change hypothesized to reduce the weight of the skeleton and/or increase
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oxygen consumption in response to the elevated metabolic demands brought about by
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large body size. Finally, some workers have argued that sauropods show signs of gregarious
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behavior (Salgado et al., 2012). With respect to titanosaurs, it has been suggested that if
387
this behavior was not present, females at least would have aggregated periodically
388
during the ovipositional season (Chiappe et al., 2005, García et al., 2015). Price (1951)
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reported sauropods eggs within the Marília Formation, and although no juveniles have
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been found associated with these eggs, the synformational presence of both eggs and
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juveniles with adult titanosaurs suggests that animals of different ontogenetic stages
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shared a common environment.
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7. Conclusions
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In conclusion, although fragmentary, the juvenile titanosaurian specimen
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described herein to lends further support to hypotheses of isometric growth in
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titanosaurs, and may also represent a species distinct from those that have already been
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found in the Uberaba region. Furthermore, the presence of titanosaur eggs and
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individuals of different ontogenetic stages in the area bolsters the idea that the local
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paleoenvironment was conducive to both titanosaurian nesting as well as supporting a
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taxonomically diverse sauropod fauna.
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Acknowledgments
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We thank the continuous support of all the staff of the Complexo Cultural e
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Cientifico de Peirópolis of the Universidade Federal do Triângulo Mineiro, Uberaba,
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Minas Gerais. This research was beneficiated by the financial support of the the
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Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and
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Fundação de Amparo à Pesquisa de Minas Gerais (FAPEMIG). We also thank Matthew
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C. Lamanna, Blair W. McPhee and both anonymous reviewers for comments that
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greatly improved the strength of this contribution.
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