Introduction

More than 20 sauropod genera are known from substantial portions of both the cranial and postcranial skeleton (Upchurch et al. 2004). Titanosaurs, the predominant sauropods during the Late Cretaceous, are mainly represented by postcranial material; their cranial elements are rather scarce, especially in association with postcranial remains. Rapetosaurus krausei from Madagascar is the first described titanosaur with associated cranial and postcranial bones (Curry Rogers and Forster 2001). In recent years, the cranial material of several titanosaurs has been described (Table 1) and offers new information about the titanosaurian skull (Wilson 2005). In the Late Cretaceous of Europe, only two braincases have been described, one of them of Ampelosaurus atacis (Le Loeuff 2005) and the other from an indeterminate titanosaur (Le Loeuff et al. 1989), both from southern France. Additional partial skulls found in Europe, including a juvenile specimen from Transylvania (Weishampel et al. 1991), a braincase from Provence (Allain 1998) and several partial skulls from Cuenca in Spain (Barroso-Barcenilla et al. 2009), have not yet been fully described.

Lirainosaurus is the only Iberian titanosaur known to date. This small to medium-sized sauropod (about 8–10 m in length) is the largest-sized component of the Laño vertebrate assemblage (Pereda Suberbiola et al. 2000). Sanz et al. (1999) erected Lirainosaurus astibiae from a fragment of skull, isolated teeth and a set of postcranial elements. Here we describe in detail two braincases of Lirainosaurus astibiae. One of the skull fragments, which consists of an incomplete braincase, is one of the paratypes of the species (Sanz et al. 1999). Additional material recovered in Laño, including a second braincase, is also referable to Lirainosaurus.

The features characterising Lirainosaurus and supporting its placement within the Titanosauria and less inclusive clades are identified. Moreover, the affinities of Lirainosaurus with other European titanosaurs and the implications of this study are also discussed.

Institutional abbreviations.—FGGUB, Facultatea de Geologie si Geofizica, Universitatea din Bucuresti, Bucarest, Romania; ISI, Indian Statistical Institute, Calcuta, India; MACN, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, Buenos Aires, Argentina; MAU, Museo Municipal “Argentino Urquiza”, Rincón de los Sauces, Neuquén, Argentina; MCF, Museo Carmen Funes, Plaza Huincul, Neuquén, Argentina; MCNA, Museo de Ciencias Naturales de Álava/Arabako Natur Zientzien Museoa, Vitoria-Gasteiz, Spain; MDE, Musée des Dinosaures, Espéraza, France; MGPIFD-GR, Museo de Geología y Paleontología del Instituto de Formación Docente Continua de General Roca, Río Negro, Argentina; MML, Museo Municipal de Lamarque, Río Negro, Argentina; MNHN, Muséum National d'Histoire Naturelle, Paris, France; MPCA-PV, Museo Provincial “Carlos Ameghino”, Cipolletti, Río Negro, Argentina; MRS-PV, Museo de Rincón de los Sauces, Neuquén, Argentina; MUPCPv, Museo de Geología y Paleontología de la Universidad Nacional del Comahue, Argentina; PIN, Russian Academy of Sciences, Moscow, Russia; PVL, Instituto Miguel Lillo, Tucumán, Argentina; UA, Université d'Antananarivo, Madagascar; ZPAL, Institute of Paleobiology, Polish Academy of Sciences, Warszawa, Poland.

Table 1.

Titanosaurian braincases. European taxa are emphasized.

Geological setting

Lano is located in a sand quarry between the villages of Lano and Albaina, in the Condado de Treviño, an enclave of Burgos Province inside the Basque Country (Fig. 1). From a geological point of view, Laño and the adjacent region lie within the southern part of the Basque-Cantabrian Region, in the northern Iberian Peninsula (Astibia et al. 1987; Baceta et al. 1999; Berreteaga 2008). Laño has yielded a diverse continental vertebrate assemblage of Late Cretaceous (probable late Campanian to early Maastrichtian) age, including remains of bony fish, amphibians, lizards, snakes, turtles, crocodilians, pterosaurs, dinosaurs and mammals (Astibia et al. 1990, 1999; Pereda Suberbiola et al. 2000). The continental fossiliferous beds (L1A, L1B, and L2) of the Laño quarry were deposited in an alluvial system composed primarily of fluvial sands and silts. The sedimentary structures are consistent with channel areas within an extensive braided river (Astibia et al. 1990, 1999).

Fig. 1.

Titanosaurian record of Europe based on cranial remains, and map showing the location of the Laño quarry (star).

The fossils of Lirainosaurus astibiae come from the three fossiliferous strata of Laño. They correspond to a number of different individuals. As a whole, the remains of L. astibiae are quite homogenous and show little osteological variation, indicating that they probably belong to the same species.

Besides Laño, titanosaurian material referred to Lirainosaurus has been described from two other Iberian localities (Company et al. 2009; Ortega and Pérez García 2009), but it does not include skull remains.

Systematic palaeontology

Fig. 2.

The titanosaurian sauropod Lirainosaurus astibiae Sanz, Powell, Le Loeuff, Martinez, and Pereda Suberbiola, 1999 from the Late Cretaceous of Laño (northern Spain), paratypic braincase (MCNA 7439). Stereopairs in posterior (A) and anterior (B) views.

Fig. 3.

The titanosaurian sauropod Lirainosaurus astibiae Sanz, Powell, Le Loeuff, Martinez, and Pereda Suberbiola, 1999 from the Late Cretaceous of Laño (northern Spain), paratypic braincase (MCNA 7439). Stereopairs in right lateral (A) and left lateral (B) views.

Fig. 4.

The titanosaurian sauropod Lirainosaurus astibiae Sanz, Powell, Le Loeuff, Martinez, and Pereda Suberbiola, 1999 from the Late Cretaceous of Lano (northern Spain), paratypic braincase (MCNA 7439). Interpretive line drawings in posterior (A), anterior (B), and right lateral (C) views. Grey area indicates iron oxides.

Fig. 5.

The titanosaurian sauropod Lirainosaurus astibiae Sanz, Powell, Le Loeuff, Martinez, and Pereda Suberbiola, 1999 from the Late Cretaceous of Lano (northern Spain), referred braincase (MCNA 13913). Stereopairs in posterior (A) and anterior (B) views.

Fig. 6.

The titanosaurian sauropod Lirainosaurus astibiae Sanz, Powell, Le Loeuff, Martinez, and Pereda Suberbiola, 1999 from the Late Cretaceous of Laño (northern Spain), referred braincase (MCNA 13913). Stereopairs in right lateral view.

Discussion

The braincases of Lirainosaurus are not completely ossified, and lack the dorsal braincase elements (laterosphenoid and orbithospenoid), which means they could have belonged to subadult individuals. The occipital condyle is postera ventrally oriented, as occurs in most sauropods (Upchurch et al. 2004). Both specimens of Laño lack a recess in the basisphenoid, which is regarded as a synapomorphy of the Neosauropoda (Wilson 2002).

Lirainosaurus cannot be referred to the Diplodocoidea as it lacks synapomorphies of this clade, e.g., the basal region of the basipterygoid processes do not form a markedly acute angle to the skull roof (Harris 2006). In addition, the occipital condyle of Lirainosaurus is not oriented ventrally (Upchurch 1995) and the basipterygoid processes are not directed anteriorly, as commonly in diplodocids (Calvo and Salgado 1995). Unlike the Dicraeosauridae, Lirainosaurus does not present a “leaf”-like dorsolaterally-directed process on the crista prootica (Salgado and Calvo 1992; Upchurch 1998; Wilson 2002; Upchurch et al. 2004; Harris 2006); the angle between the basipterygoid processes is approximately 40°, while it is approximately 20° in the Dicraeosauridae (Salgado and Calvo 1992; Upchurch 1995, 1998; Wilson 2002; Upchurch et al. 2004). The area between the bases of the basipterygoid processes is shallowly concave in Lirainosaurus, whereas dicraeosaurids present a long narrow pit extending caudally beneath the rostral part of the braincase (Upchurch 1998; Upchurch et al. 2004; Harris 2006). In Lirainosaurus, the basal tubera breadth is much broader than the occipital condyle, whereas in the Dicraeosauridae it is narrower (Wilson 2002).

The anatomy and position of the foramina of the braincases MCNA 7439 and MCNA 13913 indicate that both belong to the Titanosauria. At least three of the morphological attributes observed in titanosaurian braincases (Paulina Carabajal et al. 2008) are present in Lirainosaurus: the complete fusion between the prootic and the exoccipital-opisthotic complex; a single trigeminal foramen that is large and located just below the crista antotica; and an oval metotic foramen that is as large as the exit of cranial nerve V, which is visible in lateral view. In addition, both braincases share several features with other titanosaurian braincases, i.e., the presence of a dorsal concave surface in the occipital condyle, and its posteroventral orientation. The median cavity for the pons variolii is commonly present in titanosaurian braincases, such as in Jainosaurus septentrionalis (Chatterjee and Rudra 1996), Rapetosaurus krauset (Curry Rogers and Forster 2004) and an indeterminate titanosaur from Patagonia (Paulina-Carabajal and Salgado 2007). MCNA 7439 also shares with other titanosaurs a high ratio (more than 1.2) between the mediolateral width of the paired basal tubera and the mediolateral width of the occipital condyle (Upchurch et al. 2004). Wilson (2005) noted that the braincases of derived titanosaurs, such as Nemegtosaurus, Quaesitosaurus, and Jainosaurus septentrionalis (Wilson et al. 2009), have a novel contact between the quadrate and the basal tubera. This feature cannot be confirmed in the braincases of Lirainosaurus.

As in Antarctosaurus (Huene 1929), Saltasaurus (Powell 1992,2003), Jainosaurus (Chatterjee and Rudra 1996; Wilson et al. 2009), Rapetosaurus (Curry Rogers and Forster 2004), Bonatitan (Martinelli and Forasiepi 2004); Nemegtosaurus (Wilson 2005), an indeterminate titanosaur from Patagonia (Garcia et al. 2008), and Phuwiangosaurus (Suteethorn et al. 2009), the occipital condyle of Lirainosaurus is heart-shaped to hemispherical, the neck of the occipital condyle has a concave dorsal surface, and the positions of the cranial foramina are similar in all specimens. In all of them but Saltasaurus the occipital condyle is posteroventrally oriented, and the basal tubera diverge from the midline. The rugose surface of the distal ends of the basal tubera is observed in Rapetosaurus, Phuwiangosaurus and the Patagonian titanosaur (García et al. 2008). Moreover, the basal tubera of Lirainosaurus are robust, as in Rapetosaurus (Curry Rogers and Forster 2004) and the Patagonian titanosaur (García et al. 2008), while in the other titanosaurs they are more or less sheet-like. This last condition is generally observed in titanosauriforms, including the basal forms (Curry Rogers and Forster 2001; Upchurch et al. 2004).

Fig. 7.

The titanosaurian sauropod Lirainosaurus astibiae Sanz, Powell, Le Loeuff, Martinez, and Pereda Suberbiola, 1999 from the Late Cretaceous of Lano (northern Spain), referred braincase (MCNA 13913). Interpretive photographs in dorsal (A), ventral (B) and posterior (C) views.

The most striking difference between the braincases of Lirainosaurus and the above mentioned titanosaurs is the absence of a basioccipital depression between the foramen magnum and the basal tubera, a feature that is seen in several neosauropods (Wilson 2002), and a median subcondylar foramen. In Lirainosaurus, the surface of the basioccipital below the occipital condyle and between the basal tubera does not show any median subcondylar foramen, unlike Saltasaurus, Rapetosaurus, Nemegtosaurus, and Phuwiangosaurus (Powell 1992: fig. 1; Powell 2003: pl. 19; Curry Rogers and Forster 2004: figs. 23, 24; Wilson 2005: fig.11; Suteethorn et al. 2009: fig. 9), but the closure of this foramen could be related with the ontogeny (Ariana Paulina Carabajal, personal communication 2010). Some of the characters discussed above are summarised in Table 2.

Fig. 8.

The titanosaurian sauropod Lirainosaurus astibiae Sanz, Powell, Le Loeuff, Martínez, and Pereda Suberbiola, 1999 from the Late Cretaceous of Laño (northern Spain), referred braincase (MCNA 13913). Interpretive drawings in anterior (A) and right lateral (B) views.

Lirainosaurus can also be compared with a few titanosaurian braincases described so far from Europe (see Introduction and Table 1): two braincases from southern France, one belonging to Ampelosaurus (Le Loeuff et al. 1989; Le Loeuff 2005), and one juvenile specimen from Romania (Weishampel et al. 1991). The latter, a small braincase associated with a skull roof that has been assigned to Magyarosaurus dacus by Weishampel et al. (1991), is in need of revision (Zoltan Csiki, personal communication 2008). Lack of fusion between the floor and the walls of the braincase indicates the immaturity of the individual (Weishampel et al. 1991). The position of the cranial foramina seems similar to that observed in Lirainosaurus, but the basal tubera are more rounded in both Laño specimens than in the Transylvanian skull. The occipital condyle of MCNA 7439 resembles that of a partial skull of Ampelosaurus atacis from the Campagne-sur-Aude locality (Aude Departement) of Languedoc, France in that it is roughly hemispherical and has a dorsal concavity (Le Loeuff 2005). With regard to the braincase of an indeterminate titanosaur Patrick and Annie Méchin private collection, cast in MDE) from the Var Department of Provence, France (Le Loeuff et al. 1989), the position of the metotic foramen and the foramen for cranial nerve V is similar to the same foramina in both specimens from Laño.

Table 2.

Distribution of various character states among the titanosaurs discussed in the text.

Lirainosaurus exhibits two features that have never been described in other titanosaurian braincases from Europe and elsewhere: the absence of median subcondylar foramina, recesses, depressions or pits in the basioccipital, below the occipital condyle and between the basal tubera; and the presence of a foramen in the distal surface of each basal tubera. The first feature could be due to ontogenetic growth (the braincases are not fully grown but are regarded as from subadult individuals). The significance of the last feature is currently unclear, but could be related to basicranial pneumacity. It is here regarded as an autapomorphic trait of L. astibiae.

The comparative anatomy of the titanosaurian braincases currently known in Europe (some of them yet unpublished) supports the idea of a high diversity during the Late Cretaceous, with at least four or five different species—including Lirainosaurus astibiae and Ampelosaurus atacis— present in the Campanian-Maastrichtian of the European archipelago (VDD, work currently in progress), as already suggested by Le Loeuff (1993, 1998) on the basis of the postcranial material.

Lirainosaurus astibiae has been included in several phylogenetic analyses, but there is not a consensus about its position within the Titanosauria (see Sanz et al. 1999; Wilson 2002; Upchurch et al. 2004; Díez Díaz et al. 2009, and references therein). Nevertheless, there is a consensus about its membership to the Lithostrotia (Upchurch et al. 2004). According to the phylogenetic analyses made by Sanz et al. (1999) and Calvo et al. (2007), Lirainosaurus is a member of the Eutitanosauria (“all titanosaurs closer to Saltasaurus than to Epachthosaurus”; see Salgado 2003: 20). Some authors had assigned Lirainosaurus to the Saltasauridae on the basis of vertebral features, but there is no strong evidence of its membership to this clade (Company et al. 2009).

No phylogenetic analysis based only on cranial features has been published to date, probably because of the small number of titanosaurian braincases discovered until now, and their striking features. Lirainosaurus and Rapetosaurus share some cranial features—like the rugose surface of the distal ends of the basal tubera, and their robustness—that are not seen in the majority of the titanosaurian braincases known until now. Some differences between Lirainosaurus and Saltasaurus, like the orientation of the occipital condyle and the morphology of the basal tubera, could indicate that Lirainosaurus is not a saltasaurine titanosaur, although we do not know if these features have a phylogenetic significance. Even though these results are preliminary, they are consistent with previous interpretations (e.g., Calvo et al. 2007) regarding Lirainosaurus as a non-saltasaurine eutitanosaur.

Conclusion

This work provides the first detailed description of two braincases (one paratype and one referred specimen) of the titanosaurian sauropod Lirainosaurus astibiae from the Lano locality (Iberian Peninsula). Lirainosaurus exhibits one feature that is unknown in other titanosaurian braincases: the presence of a foramen in the distal surface of each basal tubera. This feature is here regarded as diagnostic of L. astibiae. The absence of median subcondylar foramina, recesses, depressions or pits in the basioccipital may be another autapomorphy of L. astibiae, although explanation as an ontogenetic growth feature cannot be excluded. Other features observed in the two braincases, mainly the complete fusion between the prootic and the exoccipital-opisthotic complex, the position of the cranial foramina, and the shape and orientation of the occipital condyle, suggests that Lirainosaurus is a derived titanosaur.