Natural or artificial cranial endocasts of sauropod dinosaurs are known for Camarasaurus (Ostrom and Mook, 1921; Ostrom and McIntosh, 1996; Zheng, 1996; Chatterjee and Zheng, 2005; Witmer et al., 2008), Tornieria and Dicraeosaurus (Janensch, 1935), Diplodocus (Holland, 1906; Osborn, 1912; Galton, 1985; Zheng, 1996; Witmer et al., 2008), Shunosaurus (Zheng, 1996; Chatterjee and Zheng, 2002), Nigersaurus (Sereno et al., 2007), Giraffatitan (“Brachiosaurus” in Janensch, 1935; Knoll and Schwarz-Wings, 2009), Apatosaurus (Balanoff et al., 2010), Amargasaurus (Paulina Carabajal, 2011), and Spinophorosaurus (Knoll et al., 2012). Within titanosaurs, cranial endocasts are only known for Jainosaurus (Huene and Matley, 1933; Wilson, 2009) and Bonatitan (Paulina Carabajal, 2009); whereas brief descriptions of the endocranial anatomy or the inner ear exist for Antarctosauruswichmannianus (Huene, 1929; Powell 2003), Saltasaurus (Powell, 2003), Rapetosaurus (Curry Rogers and Forster, 2004), and a few unnamed titanosaurids from Patagonia (Paulina Carabajal and Salgado, 2007; García et al., 2008; Paulina Carabajal et al., 2008).
Bonatitanreigi was a small-sized titanosaur sauropod from the Upper Cretaceous of Rio Negro Province (Martinelli and Forasiepi, 2004). This taxon is closely related to Saltasaurus, a titanosaur from the northern Argentina (Powell, 2003). Two braincases are preserved for Bonatitan, both corresponding to subadult individuals as suggested by visible sutures that are otherwise obscured by fusion in most adult dinosaurs (Currie, 1997). The braincase identified as MACN-RN 821 (Museo Argentino de Cs. Nat. “Bernardino Rivadavia”, Buenos Aires, Argentina) is complete and the sediment filling the endocranial cavity was almost completely removed mechanically permitting direct observation of endocranial traits (Fig. 1). Preliminary studies on the paleoneurology of this taxon were based on a latex endocast (Paulina Carabajal, 2009). This study includes inner ear reconstructions based on CT scans (Figs. 1–3).
Antarctosaurus wichmannianus is a mid-size titanosaur from the Upper Cretaceous of Río Negro province, north Patagonia (Huene, 1929). The preserved braincase (MACN 6904) is almost complete and was previously described by Powell (2003). However, the hardness of the sediment inside the endocranial cavity prevents further mechanical preparation, and, therefore, this study of the endocranial cavity was based only on the CT scans (Figs. 4 and 5).
The unnamed titanosaur MGPIFD-GR 118 (Museo de Geología y Paleontología, General Roca, Río Negro, Argentina) corresponds to an isolated and almost complete braincase from the Upper Cretaceous of Rio Negro Province, which was previously described, together with the inner ear morphology (Paulina Carabajal and Salgado, 2007). The sediment filling the endocranial cavity was mechanically removed and a latex endocast was made for this study (Fig. 6).
There are no other described Argentinean sauropod endocasts, although new discoveries of titanosaur braincases have dramatically increased in the past decade (e.g., Calvo and Gonzalez Riga, 2004; Martinelli and Forasiepi, 2004; Calvo and Kellner, 2006; García et al., 2008; Filippi and Garrido, 2008; Filippi et al., 2011). In this study a detailed description of the endocranial morphology of Bonatitan, Antarctosaurus, and the unnamed titanosaurid MGPIFD-GR 118 is provided, including the first observations on the inner ear morphology of the two first taxa.
MATERIAL AND METHODS
X-ray CT scans of the braincases of Bonatitan (MACN-RN 821) and Antarctosaurus (MACN 6904) were performed at the Hospital Alejandro Posadas, city of Buenos Aires, using a Toshiba Aquilion 64 Multidetector medical tomographer. The slices were taken at 0.5 mm intervals. Virtual three-dimensional inner ear and cranial endocasts were obtained and visualized using the software Mimics (version 12.0) and Geomagic at the University of Alberta Paleontology lab. Additionally, latex cranial endocasts of MACN-RN 821 and MGPIFD-GR 118 were made by the author.
Comparisons with other sauropod endocasts (see taxa and specimens listed in Table 1) were based in the following materials by first hand observation: Amargasaurus (MACN-N 15), Camarasaurus (Paleo-Vertebrate Collection, Gunma Museum of Natural History, Japan [GMNH]-PV 101), Saltasaurus (Instituto Miguel Lillo, Tucumán, Argentina [PVL] 4017-161, PVL 4017-162), and the unnamed titanosaurs MUCPV-334 (Museo de la Universidad Nacional del Comahue, Neuquén, Argentina), MPCA-PV-80 (Museo Provincial “Carlos Ameghino”, Cipolletti, Río Negro, Argentina), MML-194 (Museo Municipal de Lamarque, Río Negro, Argentina), and MAU-Pv-AG-446/5 (Museo Municipal “Argentino Urquiza”, Rincón de los Sauces, Neuquén, Argentina); and published descriptions of: Apatosaurus (Brigham Young University, Paleontology collections, Provo, USA [BYU] 17096; Balanoff et al., 2010), Camarasaurus (Dinosaur National Monument, Colorado, USA [DNM] 28; Zheng, 1996), Dicraeosaurus (Collection of fossil Reptilia, Museum fur Naturkunde, Berlin, Germany [MB.R].1917, MMBR.1916.1 (endocast of MBR.2379.1-3); Janensch 1935), Diplodocus (Carnegie Museum of Natural History, Pittsburgh, USA [CM] 11161; Chatterjee and Zheng, 2002; Witmer et al., 2008), Nigersaurus (Sereno et al, 2007), Spinophorosaurus (Grupo Cultural Paleontológico de Elche, Museo Paleontológico de Elche, Elche, Spain [GCP]-CV 4229; Knoll et al., 2012), Jainosaurusseptentrionalis (“Antarctosaurus” ISI R 162; Huene and Matley, 1933; Chatterjee and Rudra, 1996; Geological Survey of India, Hyderabad, India [GSI K] 27/497; Wilson et al., 2009), Giraffatitan (“Brachiosaurus” MB.R. 1919, MB.R. 2180.22.1-4; Knoll and Schwarz-Wings, 2009), Lirainosaurus (Museo de Ciencias naturals de Alava, Alava, vitoria-Gasteiz, Spain [MCNA] 13913; Díez Díaz et al., 2011), Nemegtosaurus (Palaeobiological Institute of the Polish Academy of Sciences, Warsaw [Z.Pal.]N.MgDI/9; Wilson, 2005), Quaesitosaurus (Palaeontological Institute, Russian Academy of Sciences, Moscow, Russia [PIN] 3906/2; Kursanov and Bannikov, 1983), and Rapetosaurus (FMNH PR 2184; Curry Rogers and Forster 2004).
Table 1. Distribution of endocranial traits within Sauropoda
asc vs. psc
References: CN XII, cranial nerve XII number of foramina; ic.e.f, external foramen of the internal carotid respect the basipterygoid process; CN VI/Pit, cranial nerve VI and pituitary fossa relationship; vasc, vascular element: mcv, middle cerebral vein; ocv, orbitocerebral vein; soa, supraorbital artery; asc, anterior semicircular canal; psc, posterior semicircular canal.
personal observation, - missing or damaged, ? unknown until further studies.
In Pitekunsaurus, there are two internal openings for CN XII but a single external opening lateral to the oc.
As mentioned by other authors (e.g., Hopson, 1980; Balanoff et al., 2010), the sauropod cranial endocast does not reflect the shape of the brain (soft tissues), but the morphology of the endocranial space, which also reflects structures such as meninges and venous sinuses. As proposed by Witmer et al. (2008) to facilitate discussion I will refer to the digital casts of structures as if they were the structures themselves (e.g., “olfactory bulb” instead of “olfactory bulb (ob) cavity endocast”).
Titanosauria: Bonaparte and Coria, 1993; Saltasaurinae: Powell, 1992; Bonatitan reigi: Martinelli and Forasiepi, 2004; Studied material: Digital and latex cranial endocasts of MACN-RN 821 (Figs. 1–3; Locality and horizon: Bajo de Santa Rosa, Rio Negro province; Allen Formation (Campanian-Maastrichtian) (Martinelli and Forasiepi, 2004).
The cranial endocast of Bonatitan is 59 mm in total anteroposterior length measured from the olfactory tract (ot) to the foramen magnum, and 45 mm in maximum dorsoventral depth (Fig. 2A). It is relatively short and deep as in most sauropods (Hopson, 1979). The greatest mediolateral breadth of the endocranial space lies across the cerebral hemispheres (cers) of the forebrain and is 37 mm, whereas the narrowest point lies in the hindbrain just posterior to the cerebellum. The dural expansion (dural peak), which corresponds to the space occupied by the longitudinal venous sinus (see Witmer et al., 2008; Knoll et al., 2012 and discussion herein), is slightly taller than the forebrain. The volume of the endocranial cast (excluding the pituitary space) is 25 mL.
The outstanding features of the forebrain include the olfactory tracts and bulbs of cranial nerve (CN) I, the cerebral hemispheres, optic nerves (CN II), and the pituitary body.
The olfactory tract is almost nonexistent (3 mm long and 18 mm wide) and the olfactory bulbs are short and slightly divergent anteriorly, as in other titanosaurids. The olfactory bulbs are approximately 8 mm long and 7 mm wide, and oval-shaped in dorsal view (Fig. 1). They are relatively small if compared with the cerebral volume.
The optic nerves (CN II) exit the endocranial cavity through a pair of large, circular foramina enclosed by the orbitosphenoids (osph), which are transversely separated by 13 mm of bone. The passages for these nerves are short (5 mm long) and 6.5 mm in diameter. They extend posteromedially to converge at the midline of the anteroventral margin of the main body of the diencephalon. Here, the medial walls of the osph form a marked oval depression that is similar to the impression left by the optic chiasm in extant birds (Breazile, 1979). A well-marked depression for the optic chiasm is also observed in the endocranial cavities of Saltasaurus (PVL 4017-161) and the unnamed taxon MGPIFD-GR 118.
The cerebral hemispheres are well developed anteroposteriorly and transversely. The lateral extent of the cers reaches the lateral semicircular canal (lsc) of the inner ear in dorsal view of the endocast, as in Apatosaurus (Balanoff et al, 2010). However, the dorsal longitudinal sinus is also well developed, obscuring the dorsal shape of the hemispheres.
Also part of the diencephalon, the pituitary body descends from the ventral surface of the endocast and exhibits extreme hyperdevelopment, as in other sauropods (Balanoff et al., 2010). The infundibular stalk is short and 13 mm wide. Below the infundibulum, the pituitary fossa is more or less cylindrical and posteroventrally projected, forming an angle of 55° with the base of the medulla oblongata (Fig. 2A). The pituitary fossa is divided in two sections by a constriction below the pituitary veins. This constriction indicates the height of the dorsum sellae and is separating the spaces occupied by the anterior pituitary body dorsally (adenohypophysis) and the posterior pituitary body (neurohypophysis) ventrally. The separation of the pituitary fossa in two sections is also well marked in MGPIFD-GR 118, MPCA-PV80, and Saltasaurus (Figs. 6A, 7B, and 8B).
The internal carotid arteries enter the lower section of the pituitary fossa through separate foramina. The passages for the arteries are 36 mm long and have a diameter of about 4.5 mm. They diverge from the midline in an angle of 25° in posterior view of the endocast. As in other titanosaurids, the external foramina for the internal carotid arteries open medially to the basipterygoid processes (btps), suggesting a derived condition within sauropods (Paulina Carabajal, 2009; Table 1).
In the floor of the endocranial cavity, there is a single foramen behind the dorsum sellae that was identified as for the basilar artery (bas) for Plateosaurus (Galton, 1985), the unnamed titanosaurid MML-194 (García et al., 2008), Giraffatitan (Janensch, 1935-36; Knoll and Schwarz-Wings, 2009), and Spinophorosaurus (Knoll et al., 2012). In Bonatitan, the digital endocast shows a median passage, enclosed by the basisphenoid, running from the mentioned foramen in the floor of the endocranial cavity and entering the posterior wall of the pituitary fossa (Fig. 3). This passage is completely obliterated in larger specimens such as MPCA-PV 80 (Fig. 5). Balanoff et al. (2010) identify this passage in Apatosaurus as the “craniopharyngeal canal, which is an adult remnant of the embryonic hypophyseal fenestra.” However, the embryonic hypophyseal fenestra leads the passage of the hypophysis (pituitary) and pituitary vein, corresponding in the adult to the foramen for the infundibular stalk. Knoll et al. (2012) also mentioned a median canal that connects the pituitary space with the braincase cavity in Spinophorosaurus, which may have been for the bas. The bas is formed by the anastomosis of the caudal branches of the caudal encephalic arteries, after reaching the endocranial floor, in extant birds and crocodiles (Sedlmayr, 2002). This suggests that the retention of an open passage for the bas in most prosauropod (it is absent in a juvenile Massospondylus, Witmer pers. comm.) and sauropod dinosaurs is probably attributable to developmental processes that remain to be understood due to the lack of complete ontogenetic series in most of the groups.
There are two pairs of vascular foramina (these vascular foramina could transmit exiting vessels as likely as entering vessels) related to the pituitary fossa that are clearly visible in the endocast. Two foramina open rostrally dorsal to the constriction that separates the pituitary fossa, corresponding to vessels irrigating or draining the anterodorsal portion of the pituitary body. These foramina (labeled as “1”) are more transversely separated that the second pair of foramina (labeled as “2”), which are ventral to the constriction and have short anteroventrally projected passages (Figs. 2A and 3).
Posteriorly in the basicranium, below the occipital condyle (oc), there is a single fenestra between the basal tubera that connects internally with the pituitary fossa (Figs. 1C and 2A). A similar opening is observed in the basicranium of Narambuenatitan (Filippi et al., 2011), Pitekunsaurus (Filippi and Garrido, 2008), Saltasaurus (Powell, 2003), and the unnamed titanosaurid MPCA-PV-80 (Fig. 7B). In Pitekunsaurus, however, the sediment is filling the opening and is not possible to determine if there is a connection or not with the pituitary fossa. A small, poorly defined and ventrally facing circular depression between the oc and the basal tubera is a feature present in several neosauropods (Wilson et al., 2009), which suggests that the closure of this passage could be ontogeny dependent.
The visible mesencephalic structures in a dinosaur endocast consist of the optic lobes and cranial nerves III and IV (Franzosa, 2004). The optic lobes are not clearly defined in Bonatitan, or in the other studied titanosaurids.
Cranial nerve III is posterior to and aligned with CN II, whereas CN IV is anterodorsal to CN III (Fig. 2A). The distance between CN II and CN III is larger than the distance between CN III and CN IV as in the endocast of Saltasaurus (Fig. 8B) and Giraffatitan (Knoll and Schwarz-Wings, 2009). In Antarctosaurus (Fig. 5A) and the unnamed titanosaurid MCF-PVPH 765 (Fig. 6A), the distances between CN II and III, and CN III and IV are subequal, as in Shunosaurus and Diplodocus. In Apatosaurus, Camarasaurus, and Nigersaurus, the distance between CN II and CN III is shorter than the distance between CN III and CN IV.
In Bonatitan, The passage for the orbitocerebral vein (ocv) (see Witmer et al., 2008; “anterior cerebral vein” in Knoll and Schwarz-Wings, 2009) is difficult to follow in the CT scans except for the proximal and distal ends (Figs. 2B and 3). This vessel is dorsal to CN IV, as in Antarctosaurus, Saltasaurus, Quaesitosaurus (Kursanov and Bannikov, 1983), MCF-PVPH 765, Camarasaurus, and Diplodocus (Witmer et al., 2008) (Table 1). In Apatosaurus, a different vascular passage, more closely related with CN II, was identified as the “supraorbital artery” (Balanoff et al., 2010).
In Bonatitan, there is no marked impression of the medial laterosphenoid pillar (see Wilson et al., 2009) separating midbrain from hindbrain, unlike the deep impression left by a robust pillar in MCF-PVPH 765 and MGPIFD-GR 118. The laterosphenoid pillar is not robust in Saltasaurus (PVL 4017-161, PVL 4017-162) suggesting that the development of this reinforcement is not characteristic of saltasaurines.
The visible features in this region of the cranial endocast include the cerebellum, medulla oblongata, and cranial nerves V–XII.
The highest point in the endocast, the dural expansion or “dural peak,” is aligned with the posterior wall of the infundibular stalk (Figs. 1A and 2A). The same landmark is posterior to the infundibular stalk in the titanosaurid MGPIFD-GR 118 (Fig. 6A).
As in other sauropods, CN V foramen is the largest. The passage runs transversely from the endocranial cavity and is 8 mm long and has a maximum diameter of 7 mm. The size and form of the trigeminal root is congruent with the presence of a large, single ganglion, as mentioned for Giraffatitan and other sauropods (Witmer et al., 2008; Knoll and Schwarz-Wings, 2009).
There is a vascular element dorsal to CN V, the middle cerebral vein (mcv), laterally projected from the lateral sinus (Figs. 2 and 3). The external opening for this passage is not visible in the braincase, located behind the crista antotica and near the laterosphenoid-frontal sutural contact. The mcv was identified in other few sauropods (Knoll and Schwarz-Wings, 2009; Balanoff et al., 2010). This vessel probably leaves the endocranial cavity through the CN V foramen in most titanosaurs (Table 1).
Cranial nerve VI has a small passage that runs laterally to the pituitary fossa, as in other titanosaurids and unlike other studied sauropods where CN VI penetrates the pituitary fossa (Table 1). Cranial nerve VII is small in diameter and located posterior to CN V.
Inside the endocranial cavity, the metotic foramen (for CN IX-X and the jugular vein) is a semilunar slit, strongly compressed anteroposteriorly and 6 mm long, located posteriorly to CN VII. The endocast shows a vertical ridge running from the dorsal border of the metotic foramen, which probably corresponds to a vessel related to the dorsal sagittal venous sinus (Fig. 3).
In Bonatitan, there is a single passage for the branches of CN XII, as in the other studied titanosaurids except in Pitekunsaurus (which has two internal openings but a single external foramen, pers. obs.) and Rapetosaurus (Curry Rogers and Forster, 2004) (Table 1).
Titanosauria: Bonaparte and Coria, 1993; Antarctosaurus wichmannianus: Huene, 1929; Studied material: Digital endocast of MACN 6904 (Fig. 5); Locality and horizon: General Roca area, Río Negro province; Anacleto Formation (Campanian) (Huene, 1929; Upchurch et al., 2004).
The digital cranial endocast of Antarctosaurus is complete, measuring 85 mm in total anteroposterior length, 46 mm in maximum dorsoventral depth and 57 mm wide across the cers (Figs. 4B and 5B). The dural expansion is taller than the cers, although not as much as the deep dural expansion observed in the endocast of Jainosaurus septentrionalis (Huene and Matley, 1933; Wilson et al., 2009, Fig. 7A). The volume of the endocranial cast of Antarctosaurus is 70–75 mL, which is slightly larger than the volume of MGPIFD-GR 118.
In Antarctosaurus, the ot and bulbs are short and horizontally projected. The shape of the obs is not clearly discernible in the digital endocast.
The pituitary body is 32 mm long and forms an angle of 85° with the base of the medulla oblongata (Fig. 5A). As in other titanosaurids, the internal carotid arteries enter the distal end of the pituitary fossa ventrolaterally through separated foramina. The passage for the carotid is 22.8 mm long and has a diameter of approximately 2.2mm. There are no discernible pituitary veins associated with the pituitary fossa in the endocast.
Cranial nerve II is large and separated from its counterpart by 15mm of bone.
As in Bonatitan, the optic lobes of Antarctosaurus are not discernible in the endocast. Cranial nerve III is posterior and aligned to CN II. Whereas CN IV is dorsal to CN III and has a smaller diameter (Fig. 5A). The distance between CN II and III is more or less the same distance between CN III and IV, as in MCF-PVPH 765 and MGPIFD-GR 118.
The foramen for the ocv is located dorsal to CN IV near the laterosphenoid-frontal suture. Only the right passage for this vein was able to be reconstructed in the digital endocast (Fig. 5A). This passage is small in diameter and slightly posterolaterally projected. The mcv, located dorsally to CN V in Bonatitan, is absent in Antarctosaurus (see Table 1).
Cranial nerve V is large and horizontally co-planar with CN II and III. The passage for CN VI cannot be followed in the CT scans. However, the position of the external foramen on the lateral surface of the basisphenoid indicates that this nerve does not penetrate the pituitary fossa, as in the other studied titanosaurs (Table 1). Cranial nerve VII is small and located posteroventrally to CN V (Fig. 5A).
The large metotic foramen is for CN IX-XI. The endocast shows two small branches, one dorsal, and another ventral merging together before leaving the braincase trough the metotic foramen, suggesting that CN XI has a separated internal opening. Within the studied titanosaurs, a separated CN XI is only observed in MPCA-PV-80 (Fig. 7A). There is a single root for the branches of CN XII in the endocast.
Titanosauria: Bonaparte and Coria, 1993; Unnamed taxon: MGPIFD-GR 118; Studied material: Latex endocast of MGPIFD-GR 118 (Fig. 6); Locality and horizon: Salitral Ojo de Agua, Rio Negro province; Allen Formation (Campanian-Maastrichtian) (Paulina Carabajal and Salgado, 2007).
The cranial endocast is complete, measuring 80 mm in total anteroposterior length, 61 mm in maximum dorsoventral depth and 51mm transversely at the level of the cers. The volume of the cranial endocast is 64 mL. The dural expansion is slightly taller than the cers (Fig. 6A), as observed in Antarctosaurus and Bonatitan, although not as tall as the observed in the endocast of Jainosaurus (Wilson et al., 2005).
The olfactory tract is almost nonexistent and the olfactory bulbs are short, as in other titanosaurids (Fig. 6A,B).
The pituitary fossa is somewhat anteroposteriorly compressed. As in Bonatitan and MPCA-PV-80, there is a marked constriction separating the pituitary fossa in two sections. As in Bonatitan and Antarctosaurus, the tip of the pituitary fossa is posteriorly projected just anterior to the inner ear in lateral view on the endocast (Fig. 6A).
The passages and openings for the internal carotid arteries are unknown as the ventral section of the basicranium is missing (Fig. 6A).
The external opening for Cranial nerve II is separated from its counterpart by 12 mm of bone. The roots of this nerve converge within an oval depression in the medial wall of the osph (Fig. 6C) probably occupied by the optic chiasm (Breazile, 1979).
Cranial nerve III is posterior and aligned to CN II, whereas CN IV is posterodorsal to CN III. Unlike the ratio observed in Bonatitan, in MGPIFD-GR 118 the distances between CN II and III and between CN III and IV are subequal, as in Antarctosaurus and MCF-PVPH 765 (Fig. 6A). The diameters of CN III and IV are similar. The ocv, located dorsally to CN IV in Bonatitan and MCF-PVPH 765, is not present suggesting that in this specimen the vein leaves the endocranial cavity through the CN IV foramen.
Laterally, there is a marked longitudinal depression on the endocast that corresponds to the impression left by the prominent pillar of the laterosphenoid (Fig. 6A). This impression is also present in MCF-PVPH 765 (Fig. 8A), but is very shallow in Bonatitan and Saltasaurus.
As in other sauropods, the foramen for CN V is large. The passage for this nerve is transversely projected. Dorsal to the root of CN V, a longitudinal ridge runs dorsally towards the dural expansion, suggesting the presence of a well developed sphenoparietal sinus (Witmer et al., 2008), as observed in Bonatitan (Figs. 2A and 3). In the braincase of this specimen, there is no separated foramen for the mcv; therefore, this vessel exits the endocranial cavity through the trigeminal foramen, as is most titanosaurs (Table 1).
In the ventral aspect of the hindbrain, CN VI is transversely separated from its counterpart by 8 mm. This distance is slightly shorter than the distance between CN II foramina, which seems to be a repeated ratio within the studied titanosaurids. As observed in the basicranium (Paulina Carabajal and Salgado, 2007), CN VI does not penetrates the pituitary fossa. Cranial nerve VII has a small diameter compared to CN V.
The metotic foramen is oval shaped and has a maximum diameter of 10mm. In the endocast, there is a short ridge dorsal to the metotic foramen, probably a cast for a vessel connecting with the dorsal longitudinal sinus (Fig. 5A). As in most titanosaurids, there is a single opening for the roots of CN XII (Table 1).
The left inner ears of both Antarctosaurus and Bonatitan were digitally reconstructed (Fig. 9A,B,E,F). The general inner ear morphology corresponds to that described in other sauropods (Hopson, 1979; Galton, 1985; Paulina Carabajal and Salgado, 2007; Paulina Carabajal et al., 2008; Witmer et al., 2008; Knoll and Schwarz-Wings, 2009; Knoll et al., 2012), in which the lagena (lag) has a simple conical shape, the anterior semicircular canal (asc) is larger than the posterior semicircular canal (psc) and the lateral semicircular canal (lsc) is smaller than the other two.
In Bonatitan, the lag is simple, conical and medioventrally inclined below the oval window. The asc is slightly larger and taller than the psc (Fig. 9A). The angle between the asc and psc is approximately 90° (Fig. 9E). This is the same condition observed in Diplodocus (Galton, 1985), MCF-PVPH-765 (Paulina Carabajal and Salgado, 2007; Fig. 9G), and MGPIFD-GR 118 (Paulina Carabajal et al., 2008; Fig. 9H). The lsc is smaller than the other two canals. It is circular in arc shape, with an internal diameter of 4 mm, and a diameter of the tube of 2.6mm (Fig. 9E).
In Antarctosaurus, the width of the labyrinth is 25 mm. The lag is simple, conical and ventrolaterally projected. The asc is slightly larger in size than the psc, and is slightly taller (Fig. 9B). The angle formed between the asc and psc is 100° (Fig. 9F). The lsc is more robust than the other two canals. It is circular in arc shape and has an internal diameter of 14 mm, and a diameter of the tube of approximately 4 mm.
Inner Ear Variation
The studied titanosaurids such as Antarctosaurus, Bonatitan, Jainosaurus (Knoll et al., 2012, Fig. 6), MGPIFD-GR 118 (Paulina Carabajal and Salgado, 2007) and MCF-PVPH 765 (Paulina Carabajal et al., 2008), show a bony labyrinth with robust semicircular canals and an asc that is subequal in size with the psc. Whereas, the titanosauriform Giraffatitan (Clarke, 2005; Knoll and Schwarz-Wings, 2009; Knoll et al., 2012, Fig. 6) has an asc that is almost two times the size of the psc (Fig. 10). The rest of the sauropods with known inner ear have a larger asc, such as the basal sauropod Spinophorosaurus (Knoll et al., 2012) and Diplodocus (Witmer et al., 2008). The same condition is shared by prosauropods such as Massospondylus (Sereno et al., 2007, Fig. 1), suggesting that the robustness of the semicircular canals and the reduction of the asc are characteristics of Titanosauria.
The length of the lag is subequal to the height of the vestibule in the titanosaurs Jainosaurus, Bonatitan, Antarctosaurus, and the unnamed titanosaurids MCF-PVPH 765 and MGPIFD-GR 118. In non-titanosaurids, the lag is shorter than the vestibular part as in Spinophorosaurus, Nigersaurus, Diplodocus, Giraffatitan, and Camarasaurus (Witmer et al., 2008; Knoll et al., 2012). The lag housed the cochlear tube, which had the function of capturing sounds. Therefore, the length of this structure is directly related with the length of the sensory epithelium, a measurement that is used to estimate auditory capacity (Witmer and Ridgely, 2009). The titanosaur inner ear would have been able of capturing sounds of a relatively wide range of high frequencies (greater than 1 kHz), but not to the extent of living birds (see Paulina Carabajal and Salgado, 2007 and references cited therein). Characteristically, the inner ear of titanosaurs presents shorter semicircular canals with larger diameter than the other sauropods.
The morphology of the sauropod endocranial cavity is characterized by being globose and transversely wide, with no meningeal vessel traces as seen in derived maniraptoran dinosaurs. Endocranially, there is no medullar eminence on the cavity floor, nor floccular recess (with few exceptions) on the anterior aspect of the vestibular eminence. The dorsum sellae is tall and projected dorsally over the level of the floor of the endocranial cavity. The pituitary fossa is enlarged compared with other saurischian dinosaurs and posteroventrally projected. As mentioned by Sereno et al. (2007), the cerebral portion of the endocast extends laterally about as far as the lateral margin of the lsc. The cranial nerves follow the same general pattern, with aligned CN II, III, V–XII. Cranial nerve IV is generally dorsal to CN III or II, and there is single foramen for CN V, except in Shunosaurus, which have a separated ophthalmic branch of the trigeminal nerve (Zheng, 1996).
Tall Dorsum Sellae and Enlarged Pituitary Fossa
The neurological implications of a tall dorsum sellae, which is dorsally projected within the endocranial cavity, are not clear, although seems to be related to the enlargement of the pituitary gland. In other extinct tetrapods such as dicynodonts, the relative development of the dorsum sellae has been directly related with an enlargement of the pituitary gland (Surkov and Benton, 2004). Some authors suggested that the pituitary gland has a positive allometric relationship with body size; and because of this, it is extremely large in sauropods (Edinger, 1942; Sander et al., 2010). But, is the enlarged pituitary body related only with the body size? In humans and small mammals (Elster et al., 1991; Pankakoski and Tahka, 1982; Tsunoda and Okuda, 1997), the size of the pituitary gland varies with age and sex, between younger and older, and between female and male subjects. The size of the pituitary gland increases during the maturity of the individual, but the most striking changes are during pregnancy when the gland reaches its maximal height just after birth (Elster et al., 1991). The large pituitary fossa in sauropods may have been prepared to hold a pituitary grand during the whole life of the individual, or by the other hand, to hold an enlarged gland during the reproductive season. The last, probably related to a fast period of reproduction, but also with the production of large amounts of eggs (15–30) as observed in each nest at the Aucamahuevo site (Chiappe et al., 2004; pers. obs.). However, extant reptiles that lay large amount of eggs, such as crocodiles and turtles, have extremely reduced pituitary glands (pers. obs.). The functional significance of the pituitary enlargement in sauropods is still obscure in view of the multiple functions of this endocrine gland.
Absence of Floccular Recess
A small floccular recess is present in the endocranial cavity of prosauropods such as Adeopapposaurus (Martínez, 2009), Plateosaurus (Galton 1985), and Massospondylus (Gow, 1990). Galton and Knoll (2006) reported a floccular recess in the braincase of a possible sauropod, although this material is very fragmentary and thus, informatively ambiguous. More recently, small floccular recesses in the endocranial cavity of Nigersaurus (Witmer et al., 2008) and Giraffatitan (Knoll and Schwarz-Wings, 2009) were reported. In the titanosaurid MCF-PVPH-765, the floccular recess is absent but the vestibular eminence shows a circular area crossed by several small foramina, indicating the close relationship between this part of the cerebellum and the labyrinth of the inner ear (Paulina Carabajal et al., 2008). Based on the neuroscience of extant species, Witmer et al. (2003) suggested that the flocculus was associated with coordinating inputs from the periphery and vestibular apparatus to enhance the vestibulo-ocular reflexes. Thus, the reduction or absence of the flocculus in sauropods is consistent with the reduction of the semicircular canals, which also are intimately connected with coordinating eye movements. In saurischians, the presence and relative development of the floccular process of the cerebellum seems to be related with the degree of bipedalism (Chatterjee and Zheng, 2002; Paulina Carabajal, 2009).
Titanosaurid Cranial Endocast
Titanosaurid cranial endocasts have extremely short ots and small obs (in the titanosaurs studied, the ob cavities represent less than 6% of the endocranial cavity volume). There is no floccular process, nor pineal and postparietal foramina in the skull roof. The cers are well developed anteroposteriorly, and the distance between CN IV (midbrain) and the base of the ot represents the length of the cers. This distance is subequal to the rest of the cranial endocast length (hindbrain). In other sauropods such as Spinophorosaurus (Knoll et al., 2012), Shunosaurus, Camarasaurus (Zheng, 1996), Diplodocus (Hopson, 1979), Apatosaurus (Balanoff et al., 2010), Dicraeosaurus (Janensch, 1936), and Giraffatitan (Knoll and Schwarz-Wings, 2009), the distance between CN IV and ot is less than half the rest of the endocast length. In this sense, CN IV is relatively closer to CN I in other sauropods than in titanosaurids, and only Nigersaurus (Sereno et al., 2007) shows a similar disposition of the cers and CN IV. Unlike Camarasaurus, Diplodocus (Witmer et al., 2008) and dicraeosaurids (Paulina Carabajal pers. obs.), the endocrania of the patagonian titanosaurs do not show the large vascular sinuses that form prominent furrows, recesses and openings on the endocranial surface.
In titanosaurids, the olfactory bulbs are horizontally projected, similar to what is observed in the diplodocoid Nigersaurus (Sereno et al. 2007), but unlike the relatively longer and strongly dorsally angled obs in Shunosaurus (Zheng, 1996), Camarasaurus (Zheng, 1996), Diplodocus (Hopson, 1979), and Spinophorosaurus (Knoll et al., 2012). In those taxa, the anterodorsal projection of the obs is a result of the strong caudal retraction of the nasal cavity and the telescoping of the braincase (Sereno et al. 2007; Witmer et al., 2008).
In all the titanosaurids studied, CN VI passes lateral to the pituitary fossa, as in the titanosauriforms Giraffatitan (Knoll and Schwarz-Wings, 2009) and the unnamed taxon TMM 40435 (Tidwell and Carpenter, 2003). Cranial nerve VI penetrates the pituitary fossa in most other non titanosaurid forms, indicating a possible diagnostic characteristic for Titanosauria (Wilson and Upchurch, 2003) (Table 1).
In the titanosaurids studied, the length of the hindbrain (measured from CN V to CN XII) is equal to the length of forebrain (without the ot) plus the midbrain (from CN I to CN IV), indicating a shortening of the hindbrain in the group. Also, the dorsal border of the post-cerebellar hindbrain is coplanar horizontally with the ot and the inner ear is located below the imaginary horizontal plane over the medulla. In Camarasaurus, Diplodocus, Nigersaurus (Sereno et al., 2007), and probably Apatosaurus (Balanoff et al., 2010), the same plane crosses the asc. In prosauropods such as Plateosarus (Galton, 1985) and Massospondylus, and the basal sauropods Shunosaurus (Zheng, 1996) and Spinophorosaurus (Knoll et al., 2012), the dorsal border of the medulla oblongata is ventral to the ot, and the horizontal plane over the medulla crosses the semicircular canals. This suggests that the alignment of the forebrain and hindbrain is a derived condition within Sauropods.
Sauropodomorphs have a relatively simple inner ear, with short lag and elliptic semicircular canals (Knoll et al., 2012), of which the asc is larger than the psc, and the lsc is smaller than the other two (Galton, 1985). The angle formed between the asc and psc is approximately 100°.
Titanosaurids have more robust semicircular canals and common trunk than the rest of the sauropods, but the most striking morphological change is the reduction of the asc, which is barely larger than the psc (Fig. 10). As mentioned by Sereno et al. (2007), the development of large semicircular canals has been associated with behavioral patterns that require agility. Short and small semicircular canals in sauropods suggest then a decrease in the compensatory movements of eyes and head (Witmer et al., 2008). Therefore, shorter and thicker semicircular canals in titanosaurids indicate a diminished gaze stabilization mechanism of this family within Sauropoda. The only non-Cretaceous titanosauriform with known inner ear is Giraffatitan, and it has larger asc (Knoll and Schwarz-Wings, 2009), with similar proportions than the basal Jurassic sauropod Spinophorosaurus (Knoll et al., 2012). Within non-titanosaur forms, only Camarasaurus exhibits an asc that is not markedly larger than the psc. This comparisons show that all the Jurassic and Lower Cretaceous forms including basal sauropods, diplodocids, dicraeosaurids, and basal titanosauriforms have a labyrinth with slender semicircular canals and a larger asc. Whereas, the Upper Cretaceous titanosaurids from south America have a labyrinth with relatively more robust canals, and an asc that is slightly larger than the psc. This tendency to the reduction of the semicircular canals in titanosaurids (Fig. 10) is probably related with the lack of floccular process, suggesting a decreased range of movements of the head for this clade of sauropods.
As mentioned by other authors (Balanoff et al., 2010), the endocranial morphology of sauropod dinosaurs is not that conservative as previously stated. The variation in the endocranial morphology of sauropods responds to differences in the angle between the forebrain, midbrain, and hindbrain (more precisely the cephalic flexure), the relative length and orientation of the olfactory tract and bulbs, and the development of the dorsal sagittal venous sinuses (e.g., dural peak).
Based on the study of the cranial endocasts of Antarctosaurus, Bonatitan, Jainosaurus, and other unnamed titanosaurids, the titanosaur neuroanatomy consists of a mosaic of characters (Table 1) such as short ot and bulbs that are horizontally projected, absence of the floccular process, pituitary fossa posteroventrally projected, and an inner ear with robust lagena and semicircular canals, and anterior and posterior semicircular canals that are subequal in size. Unlike most sauropods, in the titanosaur basicranium CN VI does not penetrate the pituitary fossa whereas the external foramen of the internal carotid artery opens on the medial aspect of the basipterygoid process, indicating two possible diagnostic characteristics for Titanosauria. The phylogenetic implications of these endocranial characters will be tested on further phylogenetic analyses.
The evolutionary pattern observed within Sauropoda responds basically to the anteroposterior shortening of the midbrain, and the reduction of the asc of the inner ear. This last trait going from the slender and large asc present in the Jurassic taxa to the more robust and subequal in size asc and psc observed in the Cretaceous titanosaurid forms.
The author thank A. Kramarz (MACN) for permitting the CT scanning and study of two of the specimens, and especially to Dr. M. Zamboni (Jefe Interino Servicio de Diagnóstico por Imágenes) and his collaborators at the Alejandro Posadas Hospital (Buenos Aires) for their time and kind help generating the CT scans. She is deeply grateful to I. Cerda (MPCA) for his help during the CT scanning process and transportation of the materials, and to C. Holliday (University of Missouri) for checking the grammar and discussing several aspects in the last version of the manuscript. P.J. Currie and E. Koppelhus (University of Alberta) supported her trip to Canada, and V. Arbour (U of A) instructed her in the use of the software Mimics. She also thank J. Porfiri (MUC-PV), L. Filippi (MAU-Pv-AG), D. Cabaza (MML), and J. Powell (PVL) for allowing her access to the specimens under their care. Finally, she thank L. Witmer (Ohio University) and another anonymous reviewer for their comments, which greatly improved this manuscript.