Introduction

The Brazilian Mesozoic snake record is scarce and until now limited to Late Cretaceous (Turonian—Santonian) remains from the Adamantina Formation (Bauru Group) of the southeastern region of the country (Bertini and Bonfim-Júnior 1998; Zaher et al. 2003; Candeiro 2007; Fachini and Iori 2009; Fachini and Hsiou 2011). In contrast, the Mesozoic snake record in Argentina is significant and concentrated in the Late Cretaceous of Patagonia. It comprises several remains of primitive snakes, including the limbed form Najash rionegrina from the Cenomanian (Apesteguía and Zaher 2006; Zaher et al. 2009; Palci et al. 2013), the medium-sized snake Dinilysia patagonica from the Santonian—Campanian (Smith-Woodward 1901; Estes et al. 1970; Hecht 1982; Rage and Albino 1989; Caldwell and Albino 2002; Caldwell and Calvo 2008; Zaher and Scanferla 2012), the diverse Madtsoiidae from the Campanian—Maastrichtian (Albino 1986, 1994, 2000, 2007, 2011a; Martinelli and Forasiepi 2004), and the small “anilioid” Australophis anilioides (Gómez et al. 2008). Concerning the Madtsoiidae record, at least three genera are known in the Patagonian Cretaceous: Alamitophis (with two species, A. argentinus Albino, 1986 and A. elongatus Albino, 1994), Patagoniophis (P. parvus Albino, 1986), and Rionegrophis (R. madtsoioides Albino, 1986). Moreover, there is a probable Cretaceous madtsoiid from the Maastrichtian of Bolivia (Gayet et al. 2001) as well as probable madtsoiids or boids in the Campanian—Maastrichtian of Argentina (Albino 2000, 2011a).

In a brief communication, Hsiou et al. (2009) documented the presence of two small snake vertebrae from the Cajual Island, Alcântara Formation, early Late Cretaceous (Cenomanian) of Maranhão, northeastern Brazil, and attributed them to Madtsoiidae. Here we formally describe these remains and discuss their affinities, and we reject the previous proposal of Hsiou et al. (2009). As a whole, these new snakes represent the oldest Brazilian snake record.

Institutional abbreviations.— CPHNA-MA VT, Vertebrate Collection of the Centro de Pesquisas de História Natural e Arqueologia do Maranhão, São Luís, Maranhão State, Brazil; MACN, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, Sección Paleontología de Vertebrados, Buenos Aires, Argentina; MLP, Museo de La Plata, División de Paleontología Vertebrados, La Plata, Argentina; MPCA, Museo Provincial Carlos Ameghino, Cipolletti, Río Negro, Argentina.

Other abbreviations.—cl, centrum length; cow∼coh, condyle width similar to condyle heigth; ctw∼cth, cotyle width similar to cotyle heigth; naw, neural arch width at interzygapophyseal ridge; pr-po, distance between pre- and postzygapophyses of the same side; pr-pr, distance between prezygapophyses; zw∼ctw, zygosphene width similar to cotyle width.

Geological setting

The snake remains reported here come from the Falésia do Sismito locality (2°28′43.0”S; 44°28′10.3”W) of Cajual Island, Maranhão, northeastern Brazil (Fig. 1A). The fossiliferous locality belongs to the Itapecuru Group, which spreads over a vast area in northern Maranhão, both inland and along the shore, and ranges from Albian to early Cenomanian (Fig. 1B; Pedrão et al. 1993a–c; Rossetti 2001). In the northern border of Maranhão, the Alcântara Formation crops out at the shore exposing fossil-bearing sedimentary transitional sequences at Cajual Island. This region has been considered as part of the São Luís Basin, but a revision undertaken by Góes and Rossetti (2001) considered it contiguous to the southern inland sedimentary successions of the Grajaú basin, forming the São Luís-Grajaú Basin (Rossetti et al. 2001; Rossetti 2003).

The Laje do Coringa bone bed, another fossiliferous locality at Cajual Island, concentrates thousands of fossils in a small area (4 ha), that includes bones, teeth, and plants such as conifers and ferns, revealing Cretaceous coastal forest (Medeiros and Schultz 2002), and a remarkable continental palaeofauna with diverse vertebrate groups including dinosaurs, crocodiles, other reptiles and fishes (Vilas-Bôas and Carvalho 2001; Medeiros and Schultz 2002, 2004; Elias et al. 2007; Medeiros et al. 2007; Pereira and Medeiros 2008; Van-Tomme et al. 2008; Kellner et al. 2011; Lindoso et al. 2012). The Falésia do Sismito locality is a level of the same stratigraphic sequence; just a few hundreds metres from Laje do Coringa and some metres higher in the sedimentary sucession.

The Itapecuru deposits lie conformably over Aptian strata of the Codó and Grajaú Formations and are more than 1200 m thick in the coastal area (Rodrigues et al. 1990; Góes and Feijó 1994; Rossetti et al. 2001). The Alcântara Formation comprises layers deposited under a tide and wave dominated environment, conforming to an incised valley fill (Rossetti and Truckenbrodt 1997) and is seen in the coastal cliffs in the southern region of Alcântara.

Fig. 1.

A. Location map of Cajual Island. Asterisk shows Falésia do Sismito locality. B. Stratigraphy of São Luís-Grajaú Basin (modified from Rossetti 2001).

Palynological data from layers on São Luís island revealed an early Cenomanian age for the Cretaceous sediments cropping out along the coast, whereas the inland sequences of the Itapecuru Group are considered as Albian (Pedrão et al. 1993a–c). Klein and Ferreira (1979) also attributed a Cenomanian age to the coastal deposits of the Maranhense Gulf, based on bivalves from estuarine facies.

Material and methods

The specimens studied here are stored CPHNA-MA VT, São Luiz, Maranhão, Brazil. They were compared with specimens of Alamitophis argentinus, A. elongatus, Patagoniophis parvus, Rionegrophis madtsoioides, and Dinilysia patagonica (Appendix 1). Data from the literature, as well as figures, of Alamitophis tingamarra and Patagoniophis australiensis (Scanlon 1993, 2005), Nanowana godthelpi (Scanlon 1997), Herensugea caristiorum (Rage 1996; Rage and Werner 1999), Najash rionegrina (Apesteguía and Zaher 2006; Zaher et al. 2009; Palci et al. 2013), and Dinilysia patagonica (Rage and Albino 1989; Caldwell and Albino 2002; Scanferla and Canale 2007) were also used. Osteological nomenclature follows Auffenberg (1963), Rage (1984, 1998), Lee and Scanlon (2002), and Scanlon (2005). Systematic arrangement is based on Lee and Scanlon (2002).

Systematic palaeontology

Fig. 2.

Trunk vertebra of the snake Seismophis septentrionalis gen et sp. nov. (CPHNA-MA VT 1221) from the Cenomanian (early Late Cretaceous) of Falésia do Sismito, Cajual Island, Maranhão, northeastern Brazil. Photographs (A1–E1) and explanatory drawings (A2–E2), in anterior (A), posterior (B), lateral (C), dorsal (D), and ventral (E) views.

Fig. 3.

Midtrunk vertebra of the snake cf. Seismophis septentrionalis sp. nov. (CPHNA-MA VT 1222), from the Cenomanian (early Late Cretaceous) of Falésia do Sismito, Cajual Island, Maranhão, northeastern Brazil. Photographs (A1–E1) and explanatory drawings (A2–E2), in anterior (A), posterior (B), lateral (C), dorsal (D), and ventral (E) views.

Discussion

The holotype of Seismophis septentrionalis gen. et sp nov. (CPHNA-MA VT-1221) shares with CPHNA-MA VT-1222 the small size, zygosphene moderately thick with a rectilinear roof, absence of paracotylar foramina, presence of parazygantral foramina, and strongly marked parasagittal crests on the neural arch. The morphological similarities and subtle differences among the studied vertebrae could be attributed to intracolumnar or intraspecific variation, suggesting they parison of all characters, and so it is not possible to be sure. It is noteworthy that the locality where these vertebrae were collected, represents one of the few bone-beds from Brazil and has yielded hundreds of isolated elements, some probably reworked from previous deposits (Medeiros and Schultz 2002; Van Tomme et al. 2008; Kellner et al. 2009, 2011). For this reason, we establish that these vertebrae do not belong to the same individual. Most of the differences between both vertebrae are considered intracolumnar variation due to a more anterior position of the vertebra CPHNA-MA VT-1222 in the column, and others represent possible intraspecific variations. First, their proportions are different: the specimen CPHNA-MA VT-1222 is a higher than long vertebra, whereas the holotype of Seismophis is longer than high, showing a more depressed general aspect, and a longer neural arch and vertebral centrum than in CPHNA-MA VT-1222. In the holotype, the prezygapophyses are inclined above the horizontal plane, differing from the midtrunk vertebra CPHNA-MA VT-1222, where they are almost horizontal. The neural spine of the Seismophis holotype is low and anteroposteriorly elongate, keeping the same height all along the neural arch, unlike CPHNA-MA VT-1222, in which it is obliquely developed anteroposteriorly, and looks higher posteriorly than anteriorly. The interzygapophyseal ridge of the holotype is long and straight in lateral view. It looks curved in dorsal view because the constriction is strong. In ventral view, the subcentral ridges are sinuous in the holotype, but straight in CPHNA-MA VT-1222. Also, the haemal keel of Seismophis's holotype is much broader and flattened than in CPHNA-MA VT-1222. represent the same taxa. However, the poor preservation of the specimen CPHNA-MA VT-1222 prevents a clear comparison comparison of all characters, and so it is not possible to be sure. It is noteworthy that the locality where these vertebrae were collected, represents one of the few bone-beds from Brazil and has yielded hundreds of isolated elements, some probably reworked from previous deposits (Medeiros and Schultz 2002; Van Tomme et al. 2008; Kellner et al. 2009, 2011). For this reason, we establish that these vertebrae do not belong to the same individual. Most of the differences between both vertebrae are considered intracolumnar variation due to a more anterior position of the vertebra CPHNA-MA VT-1222 in the column, and others represent possible intraspecific variations. First, their proportions are different: the specimen CPHNA-MA VT-1222 is a higher than long vertebra, whereas the holotype of Seismophis is longer than high, showing a more depressed general aspect, and a longer neural arch and vertebral centrum than in CPHNA-MA VT-1222. In the holotype, the prezygapophyses are inclined above the horizontal plane, differing from the midtrunk vertebra CPHNA-MA VT-1222, where they are almost horizontal. The neural spine of the Seismophis holotype is low and anteroposteriorly elongate, keeping the same height all along the neural arch, unlike CPHNA-MA VT-1222, in which it is obliquely developed anteroposteriorly, and looks higher posteriorly than anteriorly. The interzygapophyseal ridge of the holotype is long and straight in lateral view. It looks curved in dorsal view because the constriction is strong. In ventral view, the subcentral ridges are sinuous in the holotype, but straight in CPHNA-MA VT-1222. Also, the haemal keel of Seismophis's holotype is much broader and flattened than in CPHNA-MA VT-1222.

Isolated snake vertebrae are very common in Mesozoic and Cenozoic deposits with vertebrate remains, and difficulties involved in vertebral identification have been widely recognized (LaDuke 1991). In this way, many fossil taxa are described based on a single vertebra because several vertebral characters can be sufficiently applicable to distinguish one taxon from another. In the last years, efforts to understand the origins and evolution of snakes resulted in several phylogenetic studies that include important vertebral characters previously seen only in morphological studies. As consequence, since then, some workers have tried to employ these vertebral characters in the study of isolated snake vertebrae in an attempt to define their phylogenetic affinities (e.g., Scanlon 2005; Albino and Montalvo 2006; Hsiou et al. 2010). In this context, both vertebrae described here display a unique combination of character states that distinguishes them from other known fossil and extant snakes. The absence of paracotylar foramina in the Seismophis holotype and CPHNA-MA VT-1222, as well as in Najash vertebrae (according to Zaher et al. 2009), distinguishes these genera from madtsoiids, where the foramina are always present (Rage 1998; Scanlon 2005). Paracotylar foramina are usually present in Dinilysia (Rage and Albino 1989) and always present in advanced Macrostomata. The absence of this foramen is considered a primitive condition (Wilson et al. 2010). Traditionally considered an apomorphy of Madtsoiidae (Albino 1986, 2007; Rage 1984, 1987, 1998; Scanlon 1992, 2005), the presence of large, paired parazygantral foramina noted in the Seismophis holotype, CPHNA-MA VT-1222, Najash specimens (see MCPA 397, Zaher et al. 2009; Palci et al. 2013), and Madtsoiidae (nonsmall specimens) is considered a derived condition (Lee and Scanlon 2002; Wilson et al. 2010). The parasagittal ridges of the neural arch observed in the holotype of Seismophis and CPHNA-MA VT-1222 are similar to the laminar crest described in precloacal vertebrae of Boa constrictor (Albino 2011b). This crest has also been observed in large madtsoiids (Madtsoia and Yurlunggur), and in large extant and extinct boids (Eunectes and Chubutophis). This morphology could be related with complex epaxial muscle insertions, which are responsible for constriction (Jayne 1982). Nevertheless, the strong development of these ridges in the holotype of Seismophis and CPHNA-MA VT-1222, connecting the lateral edge of zygosphene and the posteromedial margin of the postzygapophysis is an outstanding character that, together with the absence of paracotylar foramina and presence of parazygantral foramina constitute a combination of character states resembling these vertebrae with some vertebral remains of Najash (see Zaher et al. 2009; Palci et al. 2013). Moreover, the presence of parasagittal ridges of the neural arch combined with the prominent and sharp subcentral ridges are features only present in the Seismophis holotype and CPHNA-MA VT-1222.

The holotype of Seismophis shares with Najash (see MCPA 397; Zaher et al. 2009) the absence of prezygapophyseal process, but this condition cannot be evaluated in the specimen CPHNA-MA VT-1222, because of poor preservation of the prezygapophyses. The absence of prezygapophyseal processes is interpreted as a plesiomorphic condition, seen in several primitive fossil snakes, including Najash and Madtsoiidae (Lee and Scanlon 2002; Rieppel et al. 2002; Scanlon 2006; Zaher et al. 2009; Wilson et al. 2010; LaDuke et al. 2010). The holotype of Seismophis has a shallow posterodorsal notch in the neural arch, exposing part of the condyle in dorsal view. This feature is similar to that observed in Najash (MCPA 397; Zaher et al. 2009) and also in Dinilysia (Rage and Albino 1989; Apesteguía and Zaher 2006; Zaher et al. 2009), and it is interpreted as a plesiomorphic condition among snakes (Lee and Scanlon 2002; Wilson et al. 2010). The deep V-shaped embayment exposing much of the centrum in front of the condyle is a derived condition observed in madtsoiids and alethinophidians. It is not possible to evaluate this character in the CPHNA-MA VT-1222 midtrunk vertebra. The width between the diapophyses that approaches the width between the prezygapophyses is a plesiomorphic condition (Apesteguía and Zaher 2006; Wilson et al. 2010) seen in the Seismophis holotype and also described for posterior trunk vertebrae of Najash (MCPA 397; Zaher et al. 2009) and Madtsoiidae.

The zygapophyses of the holotype of Seismophis are well inclined above the horizontal plane, as in Najash (between 20–30° to the horizontal plane; see Zaher et al. 2009: 16). Among primitive snakes, Dinilysia also usually has this plesiomorphic condition (Lee and Scanlon 2002) frequently reaching the level of the zygosphene (Rage and Albino 1989), so that the inclination of the zygapophyses observed in the holotype of Seismophis and Najash is interpreted as an intermediate condition (Lee and Scanlon 2002). On the other hand, the zygapophyses of the CPHNA-MA VT-1222 midtrunk vertebra are almost horizontal in anterior view, relating to its location in the column or a minor variation. Also, the Seismophis holotype and posterior vertebrae of Najash share a very depressed neural arch in posterior view (see MCPA 397; Zaher et al. 2009: fig. 09), contrasting with the more elevated neural arch of the midtrunk vertebra CPHNA- MA VT-1222.

In spite of the strong resemblances between Seismophis and Najash in many characters, Seismophis has a low but well developed neural spine, with the same height all along the roof of the neural arch. On the contrary the neural spine is reduced to a low crest mostly restricted to the posterior half of the neural arch in Najash (see MCPA 397; Zaher et al. 2009: fig. 09). In addition, the holotype of Seismophis is significantly smaller than Najash, it has a comparatively longer neural arch and centrum, and the paradiapophyses are in a higher position, not surpassing the ventral edge of the cotyle as in Najash vertebrae. Thus, it clearly represents a new and distinctive genus from the South American Late Cretaceous.

Conclusions

Together, the new snake vertebrae described here represent the oldest Brazilian records of the group. The identification of a new genus and species (Seismophis septentrionalis gen. et sp. nov.) probably related to one of the most primitive snakes, Najash, corroborates the assumption that South America has been a relevant territory in the origin and early diversification of snakes since the early Late Cretaceous (Albino 2007).