A new rebbachisaurid (Sauropoda: Diplodocoidea) from the middle Cretaceous of northern Brazil

Accepted Manuscript A new rebbachisaurid (Sauropoda: Diplodocoidea) from the middle Cretaceous of northern Brazil Rafael Matos Lindoso, Manuel Alfredo Araújo Medeiros, Ismar de Souza Carvalho, Agostinha Araújo Pereira, Ighor Dienes Mendes, Fabiano Vidoi Iori, Eliane Pinheiro Sousa, Silvia Helena Souza Arcanjo, Taciane Costa Madeira Silva PII:

S0195-6671(18)30206-4

DOI:

https://doi.org/10.1016/j.cretres.2019.104191

Article Number: 104191 Reference:

YCRES 104191

To appear in:

Cretaceous Research

Received Date: 30 May 2018 Revised Date:

1 July 2019

Accepted Date: 23 July 2019

Please cite this article as: Lindoso, R.M., Medeiros, M.A.A., Carvalho, I.d.S., Pereira, A.A., Mendes, I.D., Iori, F.V., Sousa, E.P., Souza Arcanjo, S.H., Madeira Silva, T.C., A new rebbachisaurid (Sauropoda: Diplodocoidea) from the middle Cretaceous of northern Brazil, Cretaceous Research, https:// doi.org/10.1016/j.cretres.2019.104191. 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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A new rebbachisaurid (Sauropoda: Diplodocoidea) from the middle

2

Cretaceous of northern Brazil

3 Rafael Matos Lindosoa,c*, Manuel Alfredo Araújo Medeirosb, Ismar de Souza Carvalhoc,

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Agostinha Araújo Pereirad, Ighor Dienes Mendese, Fabiano Vidoi Iorif, Eliane Pinheiro

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Sousag, Silvia Helena Souza Arcanjob, Taciane Costa Madeira Silvab

RI PT

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7 8

a

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Pesquisa, Pós-Graduação e Inovação - PRPGI, Av. Colares Moreira, 477, Renascença,

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Instituto Federal de Educação, Ciência e Tecnologia do Maranhão, Pró-Reitoria de

São Luís, MA, CEP: 65.075-441, Brazil; e-mail: [email protected]

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b

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s/n, CEP: 65.085-580, São Luís, MA, Brazil; e-mail: [email protected];

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[email protected], [email protected]

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c

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CEP: 21.949-900, Cidade Universitária, Ilha do Fundão, Rio de Janeiro, RJ, Brazil; e-

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mail: [email protected]

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d

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Centro,

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[email protected]

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e

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Biodiversidade e Biologia Evolutiva, CCS/IB, CEP: 21.941-902, Cidade Universitária,

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Ilha do Fundão, Rio de Janeiro, RJ, Brazil; e-mail: [email protected]

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f

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Garisto, CEP: 15.890-000, Uchoa, SP, Brazil; e-mail: [email protected];

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Universidade Federal do Maranhão, Campus do Bacanga, Avenida dos Portugueses,

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Universidade Federal do Rio de Janeiro, Departamento de Geologia, CCMN/IGEO,

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Centro de Pesquisa de História Natural e Arqueologia do Maranhão, Rua do Giz, 59, São

Luís,

Maranhão,

Brazil;

e-mail:

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CEP:65.010-680,

Universidade Federal do Rio de Janeiro, Programa de Pós-Graduação em

Museu de Paleontologia Pedro Candolo, Estação Cultura, Praça Farmacêutico Bruno

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g

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Universitária Paulo VI, CEP: 65.055-970 São Luís, MA, Brazil; e-mail:

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[email protected]

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*Corresponding author. Tel. +55(98)98868-7462; [email protected]

Universidade

Estadual

do

Maranhão,

Departamento

Biologia,

Cidade

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de

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Abstract

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São Luís Basin, Alcântara Formation, Itapeuasaurus cajapioensis gen. et sp. nov., is

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described, the first from this temporal interval in northern Brazil. It is characterized by

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the presence of large and deep fossae on ventro-lateral aspect of the dorsal neural arch

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split by laminae obliquely oriented; posterior centrodiapophyseal lamina forked

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ventrally forming the dorsal edge of the centrodiapophyseal fossa; dorsal and ventral

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components of anterior caudal transverse process thinner than the usual bony bar. This

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latter

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centrodiapophyseal fossa accessory lamina. The phylogenetic analysis performed herein

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identifies the subclade Nigersaurinae as a South American – African/European clade,

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suggesting a vicariant event before Cenomanian times. In addition, continental

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vertebrate taxa recorded in the Alcântara Formation offer support to a minor

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evolutionary change after major vicariant event in Western Gondwana.

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Keywords: Sauropoda; Diplodocoidea; Rebbachisauridae; Alcântara Formation; Brazil

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associated

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the

presence

of

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A new genus and species of Rebbachisauridae sauropod from the Cenomanian of the

1 Introduction

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One of the most interesting subjects concerning the Mesozoic continental faunas

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is the identification of events of vicariance and dispersal throughout the history of

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Gondwana. In this sense, Rebbachisauridae is paleobiogeographically relevant, a clade

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formed by all diplodocoids more closely related to Rebbachisaurus garasbae than to 2

ACCEPTED MANUSCRIPT Diplodocus longus (sensu Salgado et al., 2004). Their records have been useful for

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ascertaining the moment of definitive separation between South America and Africa

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(Carballido et al., 2010). Recently, phylogenetic analysis has emphasized a marked

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provincialism among members of Rebbachisauridae, with some of them restricted to

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Europe and northern Africa (e.g. Nigersaurus, Demandasaurus, Rebbachisaurus) and

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others only composed by Upper Cretaceous South American taxa (e.g. Limaysaurus,

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Cathartesaura, Nopcsaspondylus, El Chocon rebbachisaurid) (Sereno et al., 2007;

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Whitlock, 2011; Fanti et al., 2013; Wilson and Allain, 2015; Mannion et al., 2019). This

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group of neosauropods also reveals extreme adaptations for herbivory and high

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temperatures in habitats at tropical and subtropical paleolatitudes (Ibiricu et al., 2017;

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Sereno et al., 2007).

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In South America, Rebbachisauridae is diverse and frequently recorded in an

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interval extending from the Barremian to Turonian, particularly in Argentina.

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Additionally, their remains are composed mainly of postcranial elements (Calvo and

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Salgado, 1995; Bonaparte, 1996; Calvo, 1999; Salgado et al., 2004; Gallina and

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Apesteguía, 2005; Apesteguía, 2007; Carballido et al., 2010, 2012; Haluza et al., 2012;

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Ibiricu et al., 2012, 2013). This diversity has been also complemented by a few cranial

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remains (Calvo and Salgado, 1995; Carabajal et al., 2016; Canudo et al., 2018). Other

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records of Rebbachisauridae in South America occur only in northern-northeastern

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Brazil (Carvalho et al., 2003; Medeiros and Schultz, 2004; Castro et al., 2007; Medeiros

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et al., 2014).

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In the São Luís Basin, Cretaceous outcrops are mainly Cenomanian in age

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(Klein and Ferreira, 1979; Pedrão et al., 1993). For over 20 years, the most important

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fossiliferous outcrop in this basin has been the Laje do Coringa bone-bed, which records

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the Alcântara Formation (lower Cenomanian), at Cajual Island, São Marcos Bay

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ACCEPTED MANUSCRIPT (Corrêa-Martins, 1996; Medeiros and Schultz, 2001, 2002) (Fig. 1). Therein, a

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noteworthy paleocommunity including crocodyliforms, fishes, dinosaurs, plants

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remains, invertebrates, and pterosaurs has been recorded (Medeiros et al., 1995, 1996,

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2014; Corrêa-Martins, 1996; Vilas-Bôas et al., 1999; Vilas-Bôas and Carvalho, 2001;

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Medeiros and Schultz, 2001, 2002; Elias et al., 2007; Pereira and Medeiros, 2008;

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Araújo et al., 2011; Lindoso et al., 2012, 2013a).

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The Alcântara Formation records both Titanosauria and Diplodocoidea remains,

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although the former is less frequent in the Laje do Coringa bone bed (Medeiros et al.,

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2007, 2014). The fragmentary state of these materials has precluded the proposition of

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any nominal species, except for a few teeth tentatively assigned to Malawisaurus (Freire

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et al., 2007). Some rebbachisaurid remains (e.g. caudal vertebrae/neural spine) have

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been tentatively assigned to a more specific taxonomic level, cf. Limaysaurus tessonei

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(Medeiros and Schultz, 2004).

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In the Parnaíba sedimentary Province (which also include the São Luís Basin to

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the north), Diplodocoidea remains has been found in a better preservation state, with a

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unique nominal species described so far, Amazonsaurus maranhensis Carvalho et al.,

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2003. This rebbachisaurid was described based on a partial postcranial skeleton in

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Lower Cretaceous (Aptian-Albian) strata of the Itapecuru Formation, southern

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Maranhão State, northern Brazil (Carvalho et al., 2003). Many common taxa are

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recorded in the Alcântara and Itapecuru formations (e.g. Theropoda and fishes),

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suggesting a homogeneous paleocommunity inhabiting the northeastern Brazil

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throughout the Albian and early Cenomanian (Medeiros and Schultz, 2002; Medeiros et

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al., 2007, 2014).

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In the present study, a new genus and species of rebbachisaurid dinosaur is

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described from lower Cenomanian strata of Brazil, the first nominal diplodocoid from

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the Alcântara Formation. It comes from a new fossiliferous locality in Maranhão State

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and may help to increase our understanding concerning this sauropod group during the

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mid-Cretaceous worldwide.

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2 Geological setting

The São Luís Basin is a marginal basin located in the north portion of South

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Please, include the Fig. 1 near here.

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America. It has a total area of 18.000 km2 and its genesis is related to the Equatorial

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Atlantic opening initiated during the Late Jurassic and Early Cretaceous (Szatimari et

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al., 1987; Carvalho, 2001a; Góes and Rossetti, 2001). This basin represents one sub-

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basin on a larger intracratonic sedimentary area, the Parnaíba Province, tectonically

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reactivated in the Mesozoic during the South America and Africa breakup (Góes, 1995;

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Góes and Coimbra, 1996; Góes and Rossetti, 2001). The São Luís Basin is limited by

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the following structural arches: the Xambioá-Alto Parnaíba Antecline to the south, the

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Capim Arch to the northwest, and the Rio Parnaíba Lineament to the east (Góes, 1995).

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The sedimentary record of the São Luís Basin can be divided into three

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depositional sequences sensu Rossetti (2001): S1, S2 and S3. The S1 sequence

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accumulated during the upper Aptian and lower Albian, and includes about 450 m of

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sandstones, shales and limestones deposited in shallow marine, lacustrine and fluvio-

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deltaic environments that make up the Grajaú and Codó formations. The S2 sequence,

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lower-middle Albian, consists of about 500 m of sandstone and pelitic deposits

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attributed to shallow marine and fluvio-deltaic environments that make up the Itapecuru

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Formation (Campbell, 1949) or Undifferentiated Unit (Rossetti and Truckenbrodt,

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1997).

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The S3 sequence accumulated between the middle Albian and the Upper

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Cretaceous. It comprises 600-800 m of sandstones and pelitic deposits referred to the

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Alcântara and Cujupe formations (Rossetti and Truckenbrodt, 1997; Paz and Rossetti,

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2001). The new sauropod described herein comes from a new locality in the Itapeua

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beach, Cajapió municipality, northern Maranhão State, Brazil (Fig. 1). This locality is

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part of the Alcântara Formation, São Luís Basin (Medeiros et al., 2015). Its sedimentary

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succession includes around 2,5 m of reddish argillaceous levels at the base, being

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immediately overlaid by centimetric levels of fine to medium siltic sandstones,

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laterized, where dinosaur bones and teeth remains are found. These layers are

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superposed by reddish argillite strata intercalated by greenish siltite mottled with

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reddish coloring. Additionally, mud crack, fluidization and elephant skin structures are

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observed in plan view (Medeiros et al., 2015). The diplodocoid remains comes from

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greenish argillaceous siltic levels 20 cm thickness (Fig. 2B). The Alcântara Formation

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records a diverse biota comprising plants, fishes, turtles, dinosaurs, pterosaurs,

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vertebrate and invertebrate ichnofossils (Medeiros and Vilas-Bôas, 1999; Carvalho,

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2001b; Dutra and Malabarba, 2001; Medeiros and Schultz, 2001; Moraes-Santos and

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Carvalho, 2001; Elias et al., 2007; Freire et al., 2007; Pereira and Medeiros, 2008;

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Lindoso et al., 2012, 2013a; Medeiros et al., 2014).

148 149

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Please, include the Fig. 2 near here.

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3 Material and methods

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Universidade Federal do Maranhão (UFMA). They were localized by a fisherman on a

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beach in the Cajapió municipality, Maranhão State, subsequently being recovered by a

The fossils described herein are housed at the fossil collection of the

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ACCEPTED MANUSCRIPT team of Paleontologists of the Universidade Federal do Maranhão (UFMA),

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Universidade Federal do Rio de Janeiro (UFRJ), Centro de Pesquisa de História Natural

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e Arqueologia do Maranhão (CPHNAMA) and Universidade Estadual do Maranhão

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(Fig. 2A). As the specimen was exposed on the intertidal area, it was necessary to

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develop a stabilization technique under flood conditions, using wire, splints and

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impermeable polyurethane foam, before and after the total removal of each bony

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element, which often took more than one daily tide cycle (Medeiros et al., 2015).

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Considering the tidal cycles and the stabilization technique, the effective working time

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was reduced to less than 4 hours per day.

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Mechanical conventional techniques of fossil preparation were performed at the

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laboratory of the CPHNAMA. The phylogenetic analysis conducted herein is detailed in

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a specific section. For the nomenclature of vertebral laminae and fossae we followed

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Wilson (1999), Wilson et al. (2011) and Carballido et al. (2012).

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169 4 Systematic paleontology

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SAURISCHIA Seeley, 1887

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SAUROPODOMORPHA Huene, 1932

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SAUROPODA Marsh, 1878

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DIPLODOCOIDEA Marsh, 1884 (sensu Upchurch, 1995)

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REBBACHISAURIDAE Bonaparte, 1997

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Itapeuasaurus cajapioensis, gen. et sp. nov.

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(Figs. 3-9)

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Diagnosis. Rebbachisauridae distinguished by the following combination of characters

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on the dorsal and caudal vertebrae (autapomorphies are marked with an asterisk):

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ACCEPTED MANUSCRIPT Presence of three shallow pneumatic fossae disposed vertically on the dorsal surface of

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the neural arch, which are separated by the spinoprezygapophyseal lamina and

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spinopostzygapophyseal accessory lamina; large and deep fossae on the ventro-lateral

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aspect of the dorsal neural arch split by laminae obliquely oriented*; posterior

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centrodiapophyseal lamina forked ventrally forming the dorsal edge of the

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centrodiapophyseal fossa*; dorsal and ventral components of anterior caudal transverse

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process thinner than the usual bony bar associated to the presence of a

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prezygapophyseal

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centrodiapophyseal fossa accessory lamina*.

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Holotype. An incomplete dorsal neural arch (UFMA. 1.10.1960-01); three anterior

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caudal vertebrae (UFMA. 1.10.1960-03, 1.10.1960-04, UFMA. 1.10.1960-05); and two

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middle caudal vertebrae (UFMA. 1.10.1960-07, 1.10.1960-08).

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Paratype. A summit of dorsal neural spine (UFMA. 1.10.1960-02); an anterior caudal

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vertebra (UFMA. 1.10.1960-06); two chevrons (UFMA. 1.10.1960-10, 1.10.1960-11);

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an incomplete ischium (UFMA. 1.10.1960-09)

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Stratigraphic horizon. Alcântara Formation, São Luís Basin, lower Upper Cretaceous

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(Cenomanian).

and

prezygodiapophyseal

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lamina

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centrodiapophyseal

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4.1 Comparative description

Dorsal vertebrae. Two elements comprise the dorsal vertebrae of Itapeuasaurus

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cajapioensis. However, only the most well preserved is described herein (Fig. 3).

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UFMA 1.10.1960-01 represents a large, partially preserved middle-posterior dorsal

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neural arch. Most of the neural spine and right costal articulations are not preserved.

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The left parapophysis is missing and only the base of the right diapophysis is preserved.

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The left diapophysis is almost completely preserved; it is broad and laminar, forming an

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angle of almost 90 degrees relative to the neural spine. Although the centrum is missing,

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large fossae on the ventrolateral aspect of neural arch are deep and internally partitioned

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by a thin, obliquely oriented lamina (Fig. 3D). Its unusual position does not allow

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comparisons with other rebbachisaurids. In UFMA 1.10.1960-01, the parapophysis is above the zygapophysis level, a

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position observed in Rebbachisaurus, Nigersaurus, Histriasaurus and Demandasaurus

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(Dalla Vecchia, 1999; Sereno et al., 2007; Fernández-Baldor et al., 2011; Wilson and

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Allain, 2015), but not shared with Comahuesaurus and Limaysaurus [=Rebbachisaurus

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tessonei] (Calvo and Salgado, 1995; Carballido et al., 2012). In these latter

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rebbachisaurids, the parapophysis is far below the level of the zygapophysis. Otherwise,

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the leveling parapophysis/zygapophysis is present in the Rebbachisauridae MMCH-Pv

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49/17 (Haluza et al., 2012).

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The lateral aspect of neural arch display two fossae (centrodiapophyseal fossa,

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cdf; parapophyseal centrodiapophyseal fossa, pacdf; fig. 3C), which differ from all

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others rebbachisaurids known. For example, in Katepensaurus the parapophyseal

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centroprezygapophyseal fossa (pacprf) and (pacdf) are subdivided by laminae (Ibiricu

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et al., 2013; fig. 7C), and in Histriasaurus it forms a complex latticework of thin bone

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laminae (Dalla Vecchia, 1998; fig. 9C). Otherwise, Limaysaurus, Nopcsaspondylus,

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Nigersaurus and Demandasaurus present a reduction in complexity in these fossae

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(Nopcsa, 1902, fig. 2; Calvo and Salgado, 1995, fig. 8D; Sereno et al., 2007, fig. 3C;

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Fernández-Baldor et al., 2011, fig. 9B). In UFMA 1.10.1960-01, the posterior

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centrodiapophyseal lamina (pcdl) is forked in the middle region of the neural arch

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toward the centrum. These two new laminae form the border of the cdf and partially the

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pacdf. We consider it an autapomorphy for Itapeuasaurus cajapioensis.

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Please, include the Fig. 3 near here.

234 The surface framed by the prespinal (prsl), prezygoparapophyseal (prpl), and

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spinodiapophyseal (spdl) laminae is well delimited by three shallow fossae disposed

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vertically, increasing in size toward the apex (Fig. 4B). These fossae are subdivided by

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the spinoprezygapophyseal lamina (sprl) and spinopostzygapophyseal accessory lamina

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(spzal). Limaysaurus tessonei possesses apparently the same complex of fossae/lamina,

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but at a number of two (Calvo and Salgado, 1995; fig. 8). Although Nigersaurus also

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have dorsal vertebrae with paired pneumatic spaces at the base of the neural spines,

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Sereno et al. (1999) does not offer information regarding its compartmentalization. In

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Rebbachisaurus, the pneumatic fossae are irregularly distributed along the inferior

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margin of the diapophysis, margin of the spinodiapophyseal lamina and neural spine

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(Wilson and Allain, 2015; figs. 8B, 9).

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The neural canal is almost circular in anterior and slightly elliptical in posterior

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view. It is bordered by the medial centroprezygapophyseal lamina (med. cprl) into a

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large fossa in a drop shape in anterior view (centroprezygapophyseal fossa - cprf). Both

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the med. cprl and the intraprezygapophyseal lamina (tprl) border the subfossa

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centroprezygapophyseal dorsal (s-cprf-d, sensu Carballido et al., 2012; fig. 4B), which

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is large in Itapeuasaurus cajapioensis. (Fig. 3A). In fact, the complex lamina/fossae in

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the infraprezygapophyseal region of UFMA 1.10.1960-01 is distinct from all other

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Rebbachisauridae known.

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Please, include the Fig. 4 near here.

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ACCEPTED MANUSCRIPT Caudal vertebrae. Six caudal vertebrae almost complete are preserved (four

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anterior and two middle). The most anterior of them, UFMA 1.10.1960-03 is 540 mm

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high being 95% complete (Table 1; Fig. 5). The centrum is anteroposteriorly short,

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subcircular in shape, with lateral and ventral sides concave. The ventral concavity has a

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mediolateral direction without the presence of lateral ridges. There is no sign of lateral

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pneumatic cavities and both articular faces are amphicoelous. Subcircular anterior

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caudal centrum is present in Cathartesaura, but along with amphiplatyan articular faces

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(Gallina and Apesteguía, 2005).

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The neural arch is reduced and positioned on the anterior half of the centrum. In

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UFMA 1.10.1960-03 the neural spine is slightly inclined posteriorly (Fig. 5C).

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Otherwise, the neural arch in anterior caudals of Limaysaurus is twice higher than the

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height of the centra (Calvo and Salgado, 1995: 22) and in Cathartesaura a neural spine

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S-shaped is present (Gallina and Apesteguía, 2005; fig. 3A).

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The transverse process is a laminar complex dorsoventrally short and slightly

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oriented upward (a slight variation from the morphological type ‘complex’ termed by

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Gallina and Otero, 2009). Instead, in Histriasaurus the transverse process is laterally

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and backwardly directed (Dalla Vecchia, 1998). In UFMA 1.10.1960-03 both the dorsal

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and ventral component of the transverse process are laminar rather than bar shaped; the

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ventral component is parallel to the dorsal one rather than oblique as in most

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rebbachisaurids (e.g. Katepensaurus, Limaysaurus, Rebbachisaurus, Cathartesaura).

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The isolated anterior caudal vertebrae from Kem Kem bed (NHMUK R36636) bears

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limited similarities with UFMA 1.10.1960-03, including dorsal and ventral components

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parallel to each other in its dorsolateral plan. Most laminar anterior caudal transverse

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processes put UFMA 1.10.1960-03 apart from diplodocids, which have dorsal

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components well developed (bony bars). Although Comahuesaurus shares with

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Itapeuasaurus cajapioensis a transverse process dorsoventrally short and dorsolaterally

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deflected, the centroprezygapophyseal fossa (cprf) does not span the entire length of the

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dorsal and ventral components of the transverse process (see Carballido et al., 2012; fig.

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6A). A thin ‘web’ of bone between the dorsal and ventral components is absent in

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UFMA 1.10.1960-03; instead, a large prezygapophyseal centrodiapophyseal fossa

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(prcdf) is compartmentalized medially by two short laminae. The first one is positioned

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more

290

centrodiapophyseal fossa lamina [prcdfl] (Fig. 5A). As in Katepensaurus, the prcdfl

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arises from the dorsolateral margin of the centrum and isolates the dorsomedial corner

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of the prcdf. However, this lamina continues a trajectory under the dorsal component (=

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prezygodiapophyseal lamina [prdl]) performing an arc until contacting the ventral

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component (Fig. 5A). The second lamina, herein termed prezygodiapophyseal

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centrodiapophyseal fossa accessory lamina (prcdfal), is positioned more internally into

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the prcdf, vertically oriented. This lamina arises from the base of the ventral component

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toward the prdl (Fig. 5A). The presence and symmetrical arrangement of prcdfl and

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prcdfal in anterior caudal vertebrae of Itapeuasaurus cajapioensis is herein considered

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an autapomorphy. This condition is not present in others rebbachisaurids (see Pereda

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Suberbiola et al., 2003; Fernández-Baldor et al., 2011; Fernández-Baldor, 2012). For

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example, in the Isle of Wight rebbachisaurid anterior caudal vertebra (MIWG 5384),

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both right and left prcdf are asymmetrically compartmentalized (see Mannion et al.,

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2011: fig 1A).

into

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oriented

(prezygapophyseal

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The neural spine possesses spinodiapophyseal lamina (spdl), pre- and postspinal

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lamina (prsl and posl) well developed. The spinodiapophyseal laminae are posteriorly

306

convex and anteriorly concave, which results in an anterior bending of these laminae,

12

ACCEPTED MANUSCRIPT present in Amazonsaurus and Rebbachisaurus garasbae (Carvalho et al., 2003; Wilson

308

and Allain, 2015), but diverging in R. tessonei (Calvo and Salgado, 1995). According to

309

Sereno et al. (2007), Nigersaurus has a characteristic flaring of the lateral lamina at mid

310

length. In Demandasaurus and the Isle of Wight rebbachisaurid anterior caudal vertebra

311

(MIWG 5384), the lateral lamina is marked by the small wing-like projections near the

312

top of the neural spine (Fernández-Baldor et al., 2011; Mannion et al., 2011; Pereda

313

Suberbiola et al., 2003). The distal third of the neural spine has a ‘petal-shape’ as a

314

consequence of the expansion of the spinodiapophyseal lamina which is also present in

315

R. garasbae (Wilson and Allain, 2015; fig. 9) (Fig. 5). In distal view, the

316

spinodiapophyseal lamina (spdl), prsl and posl form the tetraradiate character typical of

317

Rebbachisauridae (Calvo and Salgado, 1995; Salgado et al., 2004). However, the lateral,

318

anterior and posterior rami are proportional in length.

M AN U

SC

RI PT

307

The pre- and postspinal laminae bifurcate at the median region of the neural

320

spine, continuing toward the neurocentral junction, participating of the formation of the

321

prezygapophysis

322

postzygapophysis (medial spinopostzygapophyseal lamina [med. spol]). This character

323

is absent in A. maranhensis, partially present in R. garasbae and anterior caudal

324

vertebrae of rebbachisaurids from central Patagonia, UNPSJB-PV 580 and UNPSJB-PV

325

1004/2. In anterior caudal vertebrae of Katepensaurus this character is also distinct,

326

although the specimen UNPSJB-PV 1007/8 may have pre- and postspinal bifurcate

327

lamina once excluded possible diagenetic obliteration or deformation (Ibiricu et al.,

328

2013; fig. 10 C).

TE D

319

spinoprezygapophyseal

lamina

[med.

sprl])

and

AC C

EP

(medial

329 330

Please, include the Fig. 5 near here.

331

13

ACCEPTED MANUSCRIPT In the anterior caudal UFMA 1.10.1960-04 the centrum is amphicoelous. The

333

neural arch is low, which supports prezygapophysis well developed and not wide apart,

334

with its articular facets oriented medially. It is placed beyond the anterior margin of the

335

centrum (Fig. 6). This condition is distinct from Dicraeosaurus, Amazonsaurus and

336

from the isolated neural arch MCF-PVPH-633.

337 338

Please, include the Fig. 6 near here.

SC

339

RI PT

332

UFMA 1.10.1960-05 is 84 mm long, missing the distal half of neural spine, most

341

of the transverse process and posterior articular surface (Fig. 7). As in the anterior

342

caudal ones, the centrum is anteroposteriorly short, whit lateral sides slightly concave.

343

The ventral side is anteroposteriorly excavated; two discrete articular eruptions close to

344

the anterior edge of centrum is herein interpreted as the haemal articular surfaces. They

345

are ca. 5 cm apart, suggesting opened haemal articulations (not bridged).

TE D

M AN U

340

As in UFMA 1.10.1960-04, the pedicel is reduced, situated on anterior half of

347

the centrum. The prezygapophysis are placed beyond the anterior margin of the slightly

348

amphicoelous centrum, and there is no prezygodiapophyseal centrodiapophyseal fossa

349

(prcdf). The base of the transverse process preserved indicates a fusion of the dorsal

350

and ventral components in a single bony bar. Between the well-developed

351

postzygapophysis, there is a deep groove, which indicates the existence of a forked

352

postspinal laminae. The articular facets of the postzygapophysis form a shallow,

353

elliptic-elongated concavity (Fig. 7 B, C).

AC C

EP

346

354

In its medium region, the neural spine is pentaradiate in cross-section due the

355

absence of lateral lamina in the proximal half. This topography results of the medial

356

spinoprezygapophyseal (med.sprl), prespinal (prsl) and postspinal (posl) laminae. In

14

ACCEPTED MANUSCRIPT 357

Amazonsaurus (MN 4555-V), instead, the caudal vertebrae neural spine is more

358

laminar.

359 360

Please, include the Fig. 7 near here.

RI PT

361

UFMA 1.10.1960-07 is 42,4 mm long and is markedly compressed laterally. It is

363

interpreted herein as a middle caudal vertebra (Fig. 8). The centrum is amphicoelous,

364

possessing the lateral faces slightly concave; the ventral one, instead, exhibit a deep

365

notch anteroposteriorly oriented. The ventral margin of the posterior articular surface is

366

slightly bulky than the anterior one, probably as a result of the presence of the haemal

367

articular surfaces. In Katepensaurus (UNPSJB-PV 1004) and Cathartesaura, the middle

368

caudal centra are similar to UFMA 1.10.1960-07, but the formers are more rectangular

369

in lateral view and have lower neural spines. These differences clearly reflect distinct

370

positions in the caudal series, thus precluding direct comparisons.

TE D

M AN U

SC

362

The neural arch is positioned on the anterior half of centrum; in this specimen,

372

the transverse process is absent (a common aspect in posterior caudal vertebrae). The

373

neural canal is higher than wide and the pre- and postzygapophysis have a laminar

374

aspect. In lateral view, UFMA 1.10.1960-07 is similar to mid-posterior caudal vertebrae

375

of Amazonsaurus (MN 4560-V), but slightly more compressed in anterior/posterior

376

view. The neural spine is slightly oriented posteriorly, only the prsl and posl being

377

preserved.

AC C

EP

371

378

UFMA 1.10.1960-07 differs from Comahuesaurus (MOZ-PV 6634) by the

379

presence of a ridge on the lateral faces of the centrum, as well as a more excavated

380

ventral surface. Caudal lateral ridges are also present in Demandasaurus (Pereda

381

Suberbiola et al., 2003). The mid- caudals of Zapalasaurus (Pv-6127-MOZ), mainly the

15

ACCEPTED MANUSCRIPT 382

numbers 5 and 6, are remarkably similar to those of Itapeuasaurus cajapioensis, but

383

exhibits a slightly greater angle between the prezygapophysis and the neural spine

384

(Salgado et al., 2006; fig. 2: 5-6). This latter condition, plus the presence of a lateral

385

knob at the base of the neural arch, distances Histriasaurus from UFMA 1.10.1960-07.

387

RI PT

386 Please, include the Fig. 8 near here.

388

UFMA 1.10.1960-08 represents a second middle caudal vertebra, posterior to

390

UFMA 1.10.1960-07 in the caudal series (Fig. 9). The centrum is 109,5 mm long and

391

170,5 mm, the lateral face being strongly excavated and the ventral face slightly

392

concave. The neurocentral junction is placed on anterior half of the centrum. The

393

prezygapophysis is laminar and surpass the anterior edge of the centrum. As in UFMA

394

1.10.1960-07, there is no an evident transverse process. The neural spine is low and

395

laterally compressed, without evidence of lateral laminae (ll).

TE D

M AN U

SC

389

UFMA 1.10.1960-08 differs from the middle caudals of Limaysaurus and

397

Demandasaurus in having a wider angle between the postzygapophysis and the

398

centrum, and from Comahuesaurus by a smaller neurocentral junction (Fig. 9B). The

399

mid-posterior caudal vertebra of Amazonsaurus (MN 4560-V) is more robust, with

400

equivalent prezygapophysis (Carvalho et al., 2003; fig. 11). In the specimen Nos IG-1,

401

the centrum has a spool shape, with a lateral knob (lk) at the base of the neural arch

402

(Dalla Vecchia, 1998; fig. 17A), aspects not present in UFMA 1.10.1960-08. In

403

Tataouinea, the postzygapophysis are more developed, and the prezygapophysis are

404

slightly oriented upward (Fanti et al., 2015; fig. 13A). The specimen UNPSJB-PV 1004

405

and mid-posterior caudal vertebrae of Zapalasaurus exhibit a neural spine more

AC C

EP

396

16

ACCEPTED MANUSCRIPT 406

expanded than UFMA 1.10.1960-08 (Salgado et al., 2006; fig. 5, 7, 8; Ibiricu et al.,

407

2012; fig. 7).

408 409

Please, include the Fig. 9 near here.

411

RI PT

410 5 Discussion

412 5.1 Phylogenetic Analysis

SC

413

Rebbachisauridae was defined as all diplodocoids more closely related to

416

Rebbachisaurus garasbae than to Diplodocus longus (Wilson [pers. comm.] in Salgado

417

et al., 2004). Recent analysis has recovered Amazonsaurus as the most ‘basal’ member

418

of this clade, with the European/African Histriasaurus its sister taxon. Histriasaurus

419

forms a polytomy with the South American Zapalasaurus at the base of

420

Rebbachisauridae and Comahuesaurus is also placed outside of Khebbashia

421

(Limaysaurinae + Nigersaurinae) (see Whitlock, 2011; Carballido et al., 2012; Wilson

422

and Allain, 2015; Fanti et al., 2015; Mannion et al., 2019).

TE D

M AN U

414 415

Nigersaurinae, a clade defined as Nigersaurus not Limaysaurus by Whitlock

424

(2011), is formed by African (Nigersaurus, Rebbachisaurus, Tataouinea) and European

425

(Demandasaurus) taxa (see Wilson and Allain, 2015; Mannion et al., 2019).

426

Rebbachisauridae also includes Limaysaurinae (Cathartesaura + Limaysaurus). In order

427

to ascertain the probable phylogenetic relationships of Itapeuasaurus cajapioensis, a

428

phylogenetic analysis was carried out based on the matrix proposed by Wilson and

429

Allain (2015). This analysis included a few changes in the characters 119 (from Salgado

430

et al., 2006), 124 (from Mcintosh, 1990), 131 (from Wilson, 2002), 132 (from Whitlock,

431

2011), 141 (from Wilson et al., 1999) (Appendix A).

AC C

EP

423

17

ACCEPTED MANUSCRIPT A parsimony analysis was carried out using the software TNT v. 1.1 (Goloboff

433

et al., 2008a, b). The matrix consists of the compiled data from Wilson and Allain

434

(2015) using a data set of 171 characters scored in 27 taxa, plus the inclusion of

435

Itapeuasaurus cajapioensis. Additionally, a heuristic tree search of 1,000 replicates of

436

Wagner Trees with random addition sequences was performed, followed by TBR

437

branch-swapping. The initial search produced 334 most parsimonious trees (MPTs) of

438

282 steps (consistency index [CI] = 0.663, retention index [RI] = 0.810). The strict

439

consensus of this analysis recovered a polytomy at the base of Rebbachisauridae (Fig.

440

10). However, when an agreement subtree analysis is performed, Itapeuasaurus

441

cajapioensis is grouped together with Demandasaurus and Nigersaurus in

442

Nigersaurinae (Fig. 11). In our resulting topology, Histriasaurus and Rebbachisaurus

443

were excluded and Amazonsaurus, Zapalasaurus and Comahuesaurus recovered as

444

successive outgroups to Khebbashia.

Please, include the Figs. 10 and 11 near here.

447 448

5.2 Taxonomy

EP

446

TE D

445

M AN U

SC

RI PT

432

Itapeuasaurus cajapioensis is the best preserved diplodocoid sauropod from the

450

Alcântara Formation, Cenomanian of the São Luís Basin. We consider it as a

451

Diplodocoidea primarily by the neural arch in the dorsal vertebrae being tall and neural

452

spines very elongated both in dorsal and caudal vertebrae, being tetraradiate in cross-

453

section. Its attribution to Rebbachisauridae is mainly based on dorsal and ventral

454

components of the transverse process supported by a reduced ‘web’ of bone (sensu

455

Gallina and Otero, 2009), summit of the anterior caudal neural spine ‘petal-shaped’ (see

456

Wilson and Allain, 2015; fig. 12) as well as absence of hyposphene-hypantrum in

AC C

449

18

ACCEPTED MANUSCRIPT posterior dorsals (see Calvo and Salgado, 1995). Additionally, the presence of fossae

458

split by an obliquely oriented internal pneumatic fossa lamina on the dorsals neural

459

arch, posterior centrodiapophyseal lamina forked on the dorsal vertebrae and caudal

460

transverse processes thinner than the usual bony bar characterize it as a new genus and

461

species of Rebbachisauridae.

RI PT

457

In Brazil, rebbachisaurids are scarce and only recorded in the Albian-

463

Cenomanian strata of the São Luís and Parnaíba basins (Alcântara and Itapecuru

464

formations, respectively). Until now, solely one nominal species has been described,

465

Amazonsaurus maranhensis, from Aptian-Albian Itapecuru Formation (Carvalho et al.,

466

2003). Isolated and fragmentary rebbachisaurids records include materials of few

467

diagnostic value (e.g. fragments of tetraradiate neural spine) from the Alcântara

468

Formation as well as in underlying Undifferentiated Unit deposits (a designation used

469

for Itapecuru Formation by some authors as Rossetti and Truckenbrodt, 1997),

470

lower/middle Albian in age (Medeiros and Schultz 2004; Castro et al., 2007). Most of

471

the caudal centra from the Alcântara Formation (e.g. Laje do Coringa bone bed) have

472

been related to Limaysaurus sp. (Medeiros and Schultz, 2004), but the authors admit

473

that this generic assignment is weakly sustained because of the lack of diagnostic

474

features (M.A. Medeiros, pers. comm., 2015).

475 476

5.3 Spatiotemporal context

478

M AN U

TE D

EP

AC C

477

SC

462

Prior studies have supported a North America origin for Diplodocoidea, with the

479

surge of diversification in Flagellicaudata occurring in the Kimmeridgian of North

480

America, Europe and Africa, and Tithonian of South and North America (Whitlock,

481

2011). Recently, discoveries in East Asia have challenged current paleobiogeographic

19

ACCEPTED MANUSCRIPT 482

hypotheses concerning the origin and dispersion of Diplodocoidea, estimating an early

483

Middle Jurassic age for the earliest members of the clade (Xu et al., 2018). New discoveries also have improved our knowledge regarding spatiotemporal

485

context of Rebbachisauridae. After extinction of most flagellicaudatan taxa in the Late

486

Jurassic, Rebbachisauridae became the latest-surviving dipodocoids occupying both

487

Laurasian and Gondwanan landmasses during the Early Cretaceous (Wilson and Allain,

488

2015). The earliest record of this clade is Maraapunisaurus, now dated as Upper

489

Jurassic of North America (Morrison Formation) (Carpenter, 2018). Moreover, the

490

Lower Cretaceous Xenoposeidon from Hastings Group of England represents the

491

successive earliest rebbachisaurid known (Taylor, 2018).

M AN U

SC

RI PT

484

The presence of Diplodocoidea in the early Middle – Late Jurassic interval of

493

North America and Asia suggests a global distribution of this clade before the breakup

494

of Pangea. Furthermore, the discovery of the dicraeosaurid Lingwulong shenqi in China

495

indicates that many advanced sauropods lineages originated c. 15 million years earlier

496

than previously hypothesized (Xu et al., 2018). According to Carpenter (2018), it is

497

probable that the migration of rebbachisaurids has occurred between North America and

498

Europe during the latest Late Jurassic and earliest Early Cretaceous, reaching South

499

America via Europe and Africa. This scenario has now confronted time-calibrated

500

phylogeny for a South American root of Rebbachisauridae radiation (see Fanti et al.,

501

2015).

EP

AC C

502

TE D

492

Recently, Rebbachisaurus has been positioned as sister taxon to Nigersaurus and

503

Demandasaurus in the subclade Rebbachisaurinae by Wilson and Allain (2015) (herein

504

termed Nigersaurinae following recommendation of Mannion et al., 2019) or as sister

505

taxon to Demandasaurus and Tataouinea by Fanti et al. (2015). In both cases,

506

Nigersaurinae is a subclade restricted to Europe and northern Africa. In fact, the oceanic

20

ACCEPTED MANUSCRIPT barrier that would have prevented the closer relationship between African and European

508

faunas seems to have been bridged by an intercontinental land passage by means of

509

carbonate platforms in the Tethyan seaway known as the Apulian Route (Canudo et al.,

510

2009; Dalla Vecchia, 2002; Fernández-Baldor et al., 2011; Sereno et al., 2007;

511

Holwerda et al., 2018). According to Fernández-Baldor et al., (2011), although the

512

Apulian Route may never have been a continuous land corridor between south Europe

513

and northern Africa, islands appear to have been sufficiently closer to allow faunal

514

interchange. In the present study, the clade formed by Itapeuasaurus cajapioensis and

515

Demandasaurus suggests that Nigersaurinae was not restricted only to Europe and

516

northern Africa, but also included South American taxa. Similarly, Fanti et al. (2015)

517

also suggest a more widely distributed Nigersaurinae lineage.

M AN U

SC

RI PT

507

In Western Gondwana, especially in the northeastern Brazil, paleobiogeographic

519

patterns are more complex than previously thought. Recent models have suggested the

520

presence of epicontinental seaways on the rift valleys along the Recôncavo-Tucano-

521

Jatobá and Cariri-Potiguar trends during the Aptian (Arai, 1999, 2009, 2014; Maisey,

522

2000). Maisey (2011) postulated one of these probably separated northeastern Brazil

523

from the rest of South America, but it remained connected with Africa. For this author,

524

another seaway may have left northern Brazil apart from both South America and

525

Africa. As a result, dispersal and vicariance of Early Cretaceous biota of northeastern

526

Brazil do not reflect a conspicuous and unambiguous unique ‘event’ of breakup between

527

South America and Africa, but complex isolation episodes in parts of Western

528

Gondwana (Maisey, 2011).

AC C

EP

TE D

518

529

The earlier marine incursions along the Equatorial-South Atlantic continental

530

margin of Brazil has been widely recognized as Aptian in age. Undoubted evidences

531

come from Macro- and microfossils records of Sergipe and Parnaíba basins: from the

21

ACCEPTED MANUSCRIPT 532

first one, the oldest ammonite assemblages are representatives of the early

533

douvilleiceratid lineage (e.g. Epicheloniceras–Eodouvilleiceras) and characterize a

534

middle Aptian age, some may even suggest a late early Aptian (e.g. Dufrenoyia

535

justinae) (Bengtson et al., 2007).

536

the Sergipe Basin confirms a well-developed open connection with low-latitude western

537

Tethyan regions during the late Aptian – late Albian (Koutsoukos, 1992). By the late

538

Coniacian – early Santonian times, the final structural detachment of South America

539

and Africa occurred and consequently the establishment of deep-oceanic conditions in

540

the northern South Atlantic (Koutsoukos, 1998). In the Parnaíba Basin, Maranhão State,

541

marine isopods record is also late Aptian in age (Lindoso et al., 2013b). All these

542

records show faunal Tethyan affinities. In the Cenomanian, however, a permanent

543

oceanic connection seems to have developed, in part as a result of eustatic sea level

544

rising with repeated flooding by ocean waters across most of Saharan region (Maisey,

545

1991).

TE D

M AN U

SC

RI PT

Foraminifera record from oldest marine deposits in

The fossil record of the Alcântara Formation has revealed remarkable

547

similarities between the continental faunas of northeastern Brazil and northern Africa

548

during the lower Cenomanian, mainly when compared to the material from southeast

549

Morocco (Medeiros and Schultz, 2001, 2002; Medeiros et al., 2014). The fishes

550

assemblage recorded in the Laje do Coringa bone bed is the most striking element of

551

correlation (see Cavin and Dutheil, 1999; Cavin et al., 2010), although theropod

552

dinosaurs (e.g. Carcharodontosaurus, Spinosaurus) are also remarkable. Despite some

553

taxa are restricted to the Alcântara Formation (e.g. Atlanticopristis equatorialis,

554

Equinoxiodus alcantarensis, Coringasuchus anisodontis and Oxalaia quilombensis), the

555

similarities of vertebrate taxa recorded in this lithostratigraphic unit with those of Africa

556

has been claimed as a Gondwanan heritage. For Medeiros et al. (2014), it might be

AC C

EP

546

22

ACCEPTED MANUSCRIPT 557

attributed to minor evolutionary changes of the biota after the breakup of South

558

America and Africa. The presence of a new genus and species of rebbachisaurid in the Alcântara

560

Formation closely related to Demandasaurus is another evidence that South America

561

and Africa still shared a faunistic identity during the early Late Cretaceous. Thus, the

562

present data fits well with previous statement of a greater similarity among South

563

America and Africa mid-Cretaceous continental fauna than amongst the southern and

564

northern South American ones (Medeiros and Schultz, 2002; Medeiros et al., 2007,

565

2014). Before the early Late Cretaceous, dinosaur faunas were relatively cosmopolitan.

566

The isolation of continental landmasses by oceanic barriers led to marked

567

provincialisms (Sereno et al., 1994, 1996).

M AN U

SC

RI PT

559

Since most Alcântara Formation sauropod sampling comes from the Laje do

569

Coringa bone bed, and the skeletal remains collected therein are reworked, fractured and

570

abraded, they are unsuitable for assessing relative diversities. Taphonomic bias is an

571

important factor to be considered in the Laje do Coringa vertebrate assemblage which

572

includes skeletal remains transported and re-deposited (Holz, 2003).

TE D

568

Nonetheless, diplodocoid isolated caudal centra are far more numerous than

574

those of titanosaurs, and they certainly would not belong to a single individual. Instead,

575

the fossils from Laje do Coringa represent a sample of a paleocommunity (see Medeiros

576

et al., 2014). However, we consider the Alcântara Formation vertebrate record

577

insufficient to make confident sinecological assessments. The complex pneumaticy

578

observed in Itapeuasaurus cajapioensis could be an adaptation for the high

579

temperatures in tropical to subtropical paleolatitudes during the early Late Cretaceous

580

(Fig. 12) (see Ibiricu et al., 2017).

AC C

EP

573

581

23

ACCEPTED MANUSCRIPT 582

Please, include the Fig. 11 near here.

583 584

6 Conclusion

Itapeuasaurus cajapioensis represents the northernmost record of Diplodocoidea

587

in South America and the second nominal Rebbachisauridae for the middle-Cretaceous

588

of Brazil, expanding our knowledge regarding the diversity of this clade in Western

589

Gondwana. Its set of autapomorphies confirm the pneumatic complexity inherent to this

590

neosauropod

591

Nigersaurinae as a South American – African/European clade more than an exclusively

592

African and European taxa during Cenomanian times. Although this scenario is

593

consistent with previous paleontological data recorded in the lower Upper Cretaceous of

594

the São Luís Basin, recent phylogenetic approaches within Rebbachisauridae precludes

595

a reliable paleobiogeographic hypothesis at this moment. Finally, by now it seems clear

596

that rebbachisaurids outnumbered titanosaurs in the early Late Cretaceous in northern

597

South America right before the steep decline of Rebbachisauridae. New information on

598

several aspects of this remarkable community that lived in northern Brazil depends on

599

better preserved specimens that may be found in the future.

601 602

phylogenetic

analysis

SC

The

performed

herein

identifies

EP

TE D

M AN U

group.

AC C

600

RI PT

585 586

Acknowledgements

We would like to thank Dr. Philip Mannion for criticisms, comments and English

603

improvement addressed to the final version of this manuscript. We are very grateful to

604

Dr. Eduardo Koutsoukos for his valuable comments on the paleobiogeography of

605

Western Gondwana, and the anonymous reviewer for criticisms and comments. We also

606

would like to thank Robertônio Brito (UFMA), Mosart Rogério Soares, João Francisco

607

Martins Costa, Taísa Pinheiro, Cláudia Cristina Soares, Nalva Cilene Soares, Max 24

ACCEPTED MANUSCRIPT William, Etiane Carvalho, Rosileia Alcofarado and the executive authorities for the

609

support during the fieldwork in Cajapió municipality. This manuscript is part of the first

610

author’s post-doctoral research (CNPq – 402602/2015-3) at the Universidade Federal do

611

Rio de Janeiro (UFRJ). Logistical support was offered by the Centro de Pesquisa de

612

História Natural e Arqueologia do Maranhão (CPHNAMA) and Instituto Federal de

613

Educação, Ciência e Tecnologia do Maranhão (IFMA). This manuscript received

614

financial support of Conselho Nacional de Desenvolvimento Científico e Tecnológico

615

(CNPq), Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de

616

Janeiro (FAPERJ) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior

617

(CAPES).

M AN U

SC

RI PT

608

618 References

621

Arai, M., 1999. A transgressão marinha mesocretácea: sua implicação no paradigma da

622

reconstituição paleogeográfica do Cretáceo no Brasil, in: SIMPÓSIO SOBRE O

623

CRETÁCEO DO BRASIL, 5, Serra Negra, Boletim, Rio Claro, UNESP, Rio

624

Claro, pp. 577–582.

EP

626

Arai, M., 2009. Paleogeografia do Atlântico Sul no Aptiano: um novo modelo a partir de dados micropaleontológicos recentes. Bol. Geociências Petrobras 17, 331–351.

AC C

625

TE D

619 620

627

Arai, M., 2014. Aptian/Albian (Early Cretaceous) paleogeography of the South

628

Atlantic: a paleontological perspective. Brazilian J. Geol. 44, 339–350.

629 630

https://doi.org/10.5327/Z2317-4889201400020012.

Apesteguía, S., 2007. The sauropod diversity of the La Amarga Formation (Barremian),

631

Neuquén

632

https://doi.org/10.1016/J.GR.2007.04.007.

633

(Argentina).

Gondwana

Res.

12,

533–546.

Araújo, K.C.O., Sommer, M.G., Medeiros, M.A.A., Girnos, E.C., Schimdt, I.D., 2011. 25

ACCEPTED MANUSCRIPT 634

Lenhos de Coníferas do Mesocretáceo do Norte do Maranhão Brasil. Rev. Bras.

635

Paleontol. 14, 29–38. https://doi.org/10.4072/rbp.2011.1.03. Bengtson, P., Koutsoukos, E.A.M., Kakabadze, M.V., Zucon, M.H., 2007. Ammonite

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RI PT

887

dinosaurs.

Sereno, P.C., Dutheil, D.B., Larochene, M., Larsson, H.C.E., Lyon, G.H., Magwene,

890

P.M., Sidor, C.A., Varricchio, D.J., Wilson, J.A., 1996. Predatory Dinosaurs from

891

the Sahara and Late Cretaceous faunal differentiation. Science 272, 986–991.

892

Sereno, P.C., Wilson, J.A., Witmer, L.M., Whitlock, J.A., Maga, A., Ide, O., Rowe,

895 896 897 898

M AN U

894

T.A., 2007. Structural Extremes in a Cretaceous Dinosaur. PLoS One e1230. Szatimari, P., Françolin, J.B.L., Zanotto, O., Wolff, S., 1987. Evolução tectônica da margem equatorial brasileira. Rev. Bras. Geociências 180–188. Taylor, M.P., 2018. Xenoposeidon is the earliest known rebbachisaurid sauropod dinosaur. PeerJ 6:e5212. https://doi.org/DOI 10.7717/peerj.5212.

TE D

893

SC

889

Vilas-Bôas, I., Carvalho, I.S., 2001. Répteis marinhos (mosasauria e plesiosauria) do

900

Cretáceo Superior da Bacia de São Luís (Maranhão, Brasil), in: Rossetti, D.F.,

901

Góes, A.M., Truckenbrodt, W. (Eds.), O Cretáceo na Bacia de São Luís-Grajaú.

902

Museu Paraense Emílio Goeldi, Coleção Friedrich Katzer, pp. 223–233.

AC C

EP

899

903

Vilas-Bôas, I., Carvalho, I.S., Medeiros, M.A., Pontes, H., 1999. Dentes de

904

Carcharodontosaurus (Dinosauria, Tyrannosauridae [sic]) do Cenomaniano, Bacia

905

de São Luís (Norte do Brasil). Acad. Bras. Ciências 71, 846–847.

906

Whitlock, J.A., 2011. A phylogenetic analysis of Diplodocoidea (Saurischia:

907

Sauropoda). Zool. J. Linn. Soc. 161, 872–915. https://doi.org/10.1111/j.1096-

908

3642.2010.00665.x

36

ACCEPTED MANUSCRIPT 909 910

Wilson, J.A., 2002. Sauropod dinosaur phylogeny: critique and cladistic analysis. Zool. J. Linn. Soc. 217–276. Wilson, J.A., Allain, R., 2015. Osteology of Rebbachisaurus garasbae La Ibiricu vocat,

912

1954, a diplodocoid (Dinosauria, Sauropoda) from the early Late Cretaceous–aged

913

Kem Kem beds of southeastern Morocco. J. Vertebr. Paleontol. 33 pages.

RI PT

911

Wilson, J.A., Martinez, R.N., Alcober, O., 1999. Distal tail segment of a titanosaur

915

(Dinosauria, Sauropoda) from the Upper Cretaceous of Mendoza, Argentina. J.

916

Vertebr. Paleontol. 19, 591–594.

917

SC

914

Wilson, J.A., 1999. A nomenclature for vertebral laminae in sauropods and other saurischian

dinosaurs.

J.

Vertebr.

919

10.1080/02724634.1999.10011178.

Paleontol.

M AN U

918

19:4,

639-653.

doi:

Wilson J.A., D’Emic M.D., Ikejiri T., Moacdieh E.M., Whitlock J.A., 2011. A

921

nomenclature for vertebral fossae in sauropods and other saurischian dinosaurs.

922

PLoS ONE 6(2): e17114. doi:10.1371/journal.pone.0017114.

TE D

920

Xu, X., Upchurch, P., Mannion, P.D., Barrett, P.M., Regalado-Fernandez, O.R., Mo, J.,

924

Ma, J., Liu, H., 2018. A new Middle Jurassic diplodocoid suggests an earlier

925

dispersal and diversification of sauropod dinosaurs. Nat. Commun. 9, 2700.

926

https://doi.org/10.1038/s41467-018-05128-1.

928 929 930 931

AC C

927

EP

923

Captions

Fig. 1. Location of Itapeua beach, Cajapió municipality, northern Maranhão

932

State, Brazil. The sauropod silhouette indicates the area where the material was

933

collected.

934

Fig. 2. Photographs of the excavation and geological context of Itapeuasaurus

935

cajapioensis at Cajapió municipality, northern Maranhão State. A) View of the Itapeua 37

ACCEPTED MANUSCRIPT 936

beach during the removal of the material between tidal cycles; B) Section of an outcrop

937

of the Alcântara Formation (São Luís Basin) at Itapeua beach revealing reddish/greenish

938

pelitic deposits. Fig. 3. Holotype of I. cajapioensis. Dorsal vertebra (UFMA1.10.1960-01) in

940

anterior (A), posterior (B), right lateral (C) and latero-ventral views (D). The scale bar

941

represents 10 cm.

RI PT

939

Fig. 4. Holotype of I. cajapioensis. Dorsal vertebra (UFMA1.10.1960-01) in

943

anterior (A) and detail of the right base of the neural spine (B) views. The scale bar

944

represents 5 cm.

SC

942

Fig. 5. Holotype of I. cajapioensis. Anterior caudal vertebra (UFMA 1.10.1960-

946

03) in anterior (A), posterior (B) and left lateral (C) views. The scale bar represents 5

947

cm.

M AN U

945

Fig. 6. Holotype of I. cajapioensis. Anterior caudal vertebra (UFMA 1.10.1960-

949

04) in anterior (A), posterior (B) and right lateral (C) views. The scale bar represents 5

950

cm.

TE D

948

Fig. 7. Holotype of I. cajapioensis. Anterior caudal vertebra (UFMA 1.10.1960-

952

05) in anterior (A), posterior (B) and right lateral (C) views. The scale bar represents 5

953

cm.

Fig. 8. Holotype of I. cajapioensis. Middle caudal vertebra (UFMA 1.10.1960-

AC C

954

EP

951

955

07) in anterior (A), posterior (B) and left lateral (C) views. The scale bar represents 5

956

cm.

957 958

Fig. 9. Holotype of I. cajapioensis. Middle caudal vertebra (UFMA 1.10.196008) in anterior (A) and right lateral posterior (B) views. The scale bar represents 5 cm.

959

Fig. 10. Phylogenetic relationship among Neosauropoda, including the results

960

for Itapeuasaurus cajapioensis. The diagram reflects a strict consensus of 334 most

38

ACCEPTED MANUSCRIPT 961

parsimonious trees of 282 steps (MPTs). Abbreviations: c, characters; CI, consistency

962

index; MPT, most parsimonious trees; RI, retention index; t, taxa; TL, tree length. Fig. 11. Phylogenetic relationship among Neosauropoda based on agreement

964

subtree produced in TNT. The resulting topology shows Itapeuasaurus cajapioensis

965

grouped together with members of Nigersaurinae.

RI PT

963

Fig. 12. Paleoenvironmental context of Itapeuasaurus cajapioensis. In the

967

background, the Equatorial Atlantic Ocean had already represented a selective barrier

968

on the paleocommunities from the Northeastern Brazil and Northern Africa. Art by

969

Deverson Pepi.

971

Table 1. Measurements of the holotype of Itapeuasaurus cajapioensis. (in mm).

M AN U

970

SC

966

An ‘*’ indicates an incomplete measurement.

972

TE D

Anatomical Abbreviations

973 974 975 976

acpl, anterior centroparapophyseal lamina; cprf, centroprezygapophyseal fossa; di,

diapophysis;

978

centroprezygapophyseal lamina; med.sprl, medial spinoprezygapophyseal lamina; nc,

979

neural

980

centrodiapophyseal fossa; pcdl, posterior centrodiapophyseal lamina; pf, pneumatic

981

fossa; pfl, pneumatic fossa lamina; prcdf, prezygapophyseal centrodiapophyseal fossa,

982

prcdfl,

983

prezygodiapophyseal

984

prezygodiapophyseal lamina; prsl, prespinal lamina; prpl, prezygoparapophyseal

985

lamina; prz, prezygapophysis; posl, postspinal lamina; poz, postzygapophysis; spdl,

986

spinodiapophyseal

987

spinoprezygapophyseal lamina; spzal, spinopostzygapophyseal accessory lamina; s-

ns,

neural

AC C

canal;

cdf,

EP

977

prezygapophyseal

centrodiapophyseal

spine;

pa,

lamina;

parapophysis;

centrodiapophyseal

centrodiapophyseal

sprf,

fossa;

fossa

med.cprl,

pacdf,

fossa

parapophyseal

lamina;

accessory

spinoprezygapophyseal

medial

lamina;

fossa;

prcdfal, prdl,

sprl,

39

ACCEPTED MANUSCRIPT 988

cprf-d, subfossa centroprezygapophyseal dorsal; tp, transverse process; tprl,

989

intraprezygapophyseal lamina.

AC C

EP

TE D

M AN U

SC

RI PT

990

40

ACCEPTED MANUSCRIPT

Neural Neural Neural Neural Neural Neural arch, arch, spine, spine, canal canal greatest height greatest height width height transverse transverse width width UFMA.10.1960-01 135,5* 240* 46,9 45,8 UFMA.10.1960-03 82,9 130,5 112,7* 260* 110 78,4 400* 26,8 21,06 UFMA.10.1960-04 82,2* 118,8* 113,6* 190* 63,3 27,1* 31,6 UFMA.10.1960-05 82,4 120,1 100,6* 104,2 49,2 37,5 130* 30,7 21,03 UFMA.10.1960-07 95,9* 47,9* 95,4* 48,1 40,4 9,1 170* 22,5 27,4 UFMA.10.1960-08 111,8* 58,6 87,5 33 38,6 17,4 12,7 Table 1. Measurements of the holotype of Itapeuasaurus cajapioensis gen. et sp. nov. (in mm). An ‘*’ indicates an incomplete measurement.

M AN U

SC

RI PT

Centrum height

TE D

Centrum width

EP

Centrum length

AC C

Specimen