Neurocranial Osteology and Neuroanatomy of a Late
Cretaceous Titanosaurian Sauropod from Spain
(Ampelosaurus sp.)
Fabien Knoll1*, Ryan C. Ridgely2, Francisco Ortega3, Jose Luis Sanz4, Lawrence M. Witmer2
1 Departamento de Paleobiologı́a, Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Cientı́ficas, Madrid, Spain, 2 Department of Biomedical
Sciences, Heritage College of Osteopathic Medicine, Ohio University, Athens, Ohio, United States of America, 3 Departamento de Fı́sica Matemática y de Fluidos, Facultad
de Ciencias, Universidad Nacional de Educación a Distancia, Madrid, Spain, 4 Departamento de Biologı́a, Facultad de Ciencias, Universidad Autónoma de Madrid, Madrid,
Spain
Abstract
Titanosaurians were a flourishing group of sauropod dinosaurs during Cretaceous times. Fossils of titanosaurians have been
found on all continents and their remains are abundant in a number of Late Cretaceous sites. Nonetheless, the cranial
anatomy of titanosaurians is still very poorly known. The Spanish latest Cretaceous locality of ‘‘Lo Hueco’’ yielded a relatively
well preserved, titanosaurian braincase, which shares a number of phylogenetically restricted characters with Ampelosaurus
atacis from France such as a flat occipital region. However, it appears to differ from A. atacis in some traits such as the
greater degree of dorsoventral compression and the presence of proatlas facets. The specimen is, therefore, provisionally
identified as Ampelosaurus sp. It was CT scanned, and 3D renderings of the cranial endocast and inner-ear system were
generated. Our investigation highlights that, although titanosaurs were derived sauropods with a successful evolutionary
history, they present a remarkably modest level of paleoneurological organization. Compared with the condition in the
basal titanosauriform Giraffatitan brancai, the labyrinth of Ampelosaurus sp. shows a reduced morphology. The latter feature
is possibly related to a restricted range of head-turning movements.
Citation: Knoll F, Ridgely RC, Ortega F, Sanz JL, Witmer LM (2013) Neurocranial Osteology and Neuroanatomy of a Late Cretaceous Titanosaurian Sauropod from
Spain (Ampelosaurus sp.). PLoS ONE 8(1): e54991. doi:10.1371/journal.pone.0054991
Editor: Richard J. Butler, Ludwig-Maximilians-Universität München, Germany
Received July 9, 2012; Accepted December 21, 2012; Published January 23, 2013
Copyright: ß 2013 Knoll et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This is a contribution to the research project CGL2009-12143 (Ministerio de Economı́a y Competitividad, Madrid), of which FK, who is currently
supported by the Ramón y Cajal Program, is Principal Investigator. LMW and RCR acknowledge funding support from the United States National Science
Foundation (IBN-9601174, IBN-0343744, IOB-0517257, IOS-1050154) and the Ohio University Heritage College of Osteopathic Medicine. The Ohio Supercomputing
Center also provided support. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: knoll@mncn.csic.es
The aim of the present paper is to present a detailed osteological
description as well as digital reconstructions of the endocast and
endosseous labyrinth of the inner ear based on CT scanning of a
significant sauropod cranial specimen from Lo Hueco: a well
preserved, though somewhat incomplete, braincase.
Introduction
In 2007, in the course of the construction of a high-speed rail
track connecting Madrid with Valencia, an exceptional fossil site
was discovered in the Villalba de la Sierra Formation at a locality
named ‘‘Lo Hueco,’’ near the village of Fuentes, Castile-La
Mancha, Spain. Over the course of several months, a large-scale
emergency excavation allowed thousands of specimens of plants,
invertebrates, and vertebrates of late Campanian-early Maastrichtian age to be saved [1]. Together with crocodiles, the
sauropods represent the largest part of the biomass at Lo Hueco.
The large number of sauropod elements from Lo Hueco (many of
which are in articulation) are yet to be fully prepared and
described, but preliminary observations suggest that more than
one titanosaurian species is present. Among this rich sauropod
collection, only a very limited number of cranial elements were
collected: two braincases (likely to represent distinct taxa) and a
number of isolated teeth. This is not surprising given the fragility
of the skull in sauropods. The skull elements are extremely
important remains as the cranial anatomy of titanosaurian
sauropods is currently very poorly known, except for a few
remarkable exceptions (see in particular [2–7]).
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Repository Abbreviations
ANS, Academy of Natural Sciences, Philadelphia, PA, USA;
FAM, Mairie de Fox-Amphoux, Fox-Amphoux, France; FGGUB:
Facultatea de Geologie şi Geofizică a Universită ii din Bucureşti,
Bucharest, Romania; GSI: Geological Survey of India, Kolkata,
India; MCCM: Museo de las Ciencias de Castilla-La Mancha,
Cuenca, Spain; MCNA: Museo de Ciencias Naturales de Álava,
Vitoria, Spain; MDE: Musée des Dinosaures, Espéraza, France;
MNHN: Muséum National d’Histoire Naturelle, Paris, France;
PIN: Paleontologicheskii Institut, Rossiiskaya Akademiya Nauk,
Moscow, Russia; TMM: Texas Memorial Museum, Austin, TX,
USA; Z. PAL: Instytut Paleobiologii, Polska Akademia Nauk,
Warsaw, Poland.
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Neurocranium of a Spanish Titanosaurian
indeterminate titanosauriform from the Early Cretaceous of
Texas, USA (TMM 40435 [18]: fig. 2A). Our paleoneurological
comparisons will, therefore, be extended to Jainosaurus septentrionalis
(Huene et Matley, 1933) (GSI K27/497, [19]: fig. 6, [20]: fig. 7)
from the Maastrichtian of India, as well as to further Gondwanan
titanosaurians and even more remotely related taxa, when
relevant.
To produce a three-dimensional reconstruction of the endocast
of the cranial cavity and endosseous labyrinth of the inner ear, the
specimen was scanned on a Yxlon CT Compact (Yxlon
International, Hamburg, Germany) with a voltage of 180 kV
and a current of 2.8 mA. The inter-slice spacing was of 0.20 mm.
The in-plane pixel size was about 0.147 mm. The raw scan data
were reconstructed using a bone algorithm. Data were output
from the scanner in DICOM format and then imported into Avizo
7.0.1 (VSG, Burlington, MA, USA) for viewing, analysis, and
visualization. The resulting 3D models were then imported into
the 3D modeling software Maya 2012 (Autodesk, San Rafael, CA,
USA) for artifact removal, final rendering, and generation of the
illustrations. The 3D PDFs in the Supporting Information were
Materials and Methods
The osteology of the specimen, MCCM-HUE-8741 (Fig. 1), will
be contrasted with all the comparable Laurasian Late Cretaceous
(Santonian-Maastrichtian) titanosaur specimens known so far.
From Europe, these include the braincases of Lirainosaurus astibiae
Sanz et al., 1999 [8] from Spain (MCNA 7439, [9]: figs. 2–4) and
Ampelosaurus atacis Le Loeuff, 1995 [10] from France (MDE C3–
761, [11]: fig. 4.2), as well as three braincases of indeterminate
titanosaurians from France (Mechin private collection 225,
[12]:unnumb. pl.; MNHN unnumb., [13]: fig. 2, pls 5–6;
FAM 03.064, [14]) and another from Romania (FGGUB 1007,
[15]: fig. 15, [16]: fig. 2.10). From Asia, these consist of the caudal
portion of the skulls of Nemegtosaurus mongoliensis Nowinski, 1971
[17] (Z. PAL MgD-I/9, [6]: figs. 7–11, [17]: figs. 4–5, pls 12–13)
and Quaesitosaurus orientalis Bannikov et Kurzanov vide Kurzanov et
Bannikov, 1983 [2] (PIN 3906/2, [6]: fig. 18, [2]: fig. 2), both from
Mongolia. Additional comparisons with taxa from areas south of
the Tethys will also be made where pertinent.
Our knowledge of the paleoneuroanatomy of the Laurasian
titanosauriforms rests on a single physical endocast of an
Figure 1. Photographs of the braincase of the titanosaurian sauropod Ampelosaurus sp. (MCCM-HUE-8741) from the Cretaceous of
Fuentes, Spain. In dorsal (A), ventral (B), rostral (C), caudal (D), and left lateral (E) views. Abbreviations: BO, basioccipital; BS, basisphenoid; EO-OP,
exoccipital-opisthotic/otoccipital; F, frontal; LS, laterosphenoid; OS, orbitosphenoid; P, parietal; PR, prootic; SO, supraoccipital. Scale bar equals 5 cm.
doi:10.1371/journal.pone.0054991.g001
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Figure 2. Volume-rendered CT-based images of the braincase of the titanosaurian sauropod Ampelosaurus sp. (MCCM-HUE-8741)
from the Cretaceous of Fuentes, Spain. In dorsal (A), ventral (B), rostral (C), caudal (D), and left lateral (E) views. Scale bar equals 5 cm.
doi:10.1371/journal.pone.0054991.g002
generated by exporting the 3D models from Maya into Deep
Exploration 5.5 (Right Hemisphere, San Ramon, CA, USA) and
then Adobe Acrobat 9 Pro Extended (Adobe Systems Inc., San
Jose, CA, USA). The data are archived at the Departamento de
Paleobiologı́a of the Museo Nacional de Ciencias Naturales-CSIC
(Madrid, Spain) and at WitmerLab at Ohio University (Athens,
OH, USA).
small part of the basioccipital and some of the basisphenoidparasphenoid) are missing. As a result, structures such as the
basipterygoid processes cannot be appraised in any manner. The
orbitosphenoid, which perhaps was incompletely ossified, is poorly
preserved and has sunk into the cranial cavity. Nevertheless, the
specimen does not appear to have suffered significantly from
taphonomic deformation, as demonstrated, for instance, by its
unaltered bilateral symmetry.
Frontal. The left frontal is complete. The rostrolateral corner
of the right frontal is missing, but the break suggests that this
happened during the excavation. The lateral margin of the frontal
is remarkably sinuous, with two processes: one rostrolaterally and
the other more caudolaterally. The rostral border of the
rostrolateral process shows a large groove, for the articulation of
the prefrontal, whereas the caudolateral process possibly articulated with the postorbital. The rostral margin is also pointed (close
to the central axis), although in a much more subtle way. The
dorsal surface of each frontal is uneven: it is convex along the
central axis in the caudal half and concave elsewhere except in the
zone of the rostrolateral process, where it is approximately flat.
The ventral side of the frontal is marked by a large hemispheric
depression whose lateral margin shapes into the two above-
Results
Osteology
MCCM-HUE-8741 (Figures 1, 2, S1, S2, S3) was discovered in
August 2007 in the lowest part of the fossiliferous succession (G1;
see [1]). It is of overall small size (length in the median axis:
100.8 mm; maximal width of the left, best preserved lateral half:
64.3 mm). Almost no sutures are visible. This is probably due to
the fact that this is a mature titanosaurian in which the bones have
largely fused together. Difficulties in discriminating sutures are
exacerbated by the iron oxides that have penetrated the bone,
concealing the bony surface and forming hard concretions in
places that cannot be removed without jeopardizing the integrity
of the specimen. Portions of the ventral half of the braincase (i.e., a
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Neurocranium of a Spanish Titanosaurian
Figure 3. Surface-rendered CT-based images of the cranial endocast and endosseous labyrinth of the titanosaurian sauropod
Ampelosaurus sp. (MCCM-HUE-8741) from the Cretaceous of Fuentes, Spain. In right lateral (A), caudal (B), dorsal (C), and ventral (D) views.
Abbreviations: CER, cerebrum; DE, dural expansion; III, oculomotor nerve; IX, glossopharyngeal nerve; LAB, labyrinth; MO, medulla oblongata; OT,
olfactory tract; PFO, pituitary fossa; V, trigeminal nerve; VI, abducens nerve; VII, facial nerve; X-XI, vagoaccessory nerve; XII, hypoglossal nerve. Scale
bar equals 5 cm.
doi:10.1371/journal.pone.0054991.g003
The ventral orientation of the frontals in MCCM-HUE-8741 is
less prominent and, in particular, its dorsal surface does not show
any strong ventral curvature. Although closer in morphology, the
frontal of MCCM-HUE-8741 is also distinct from that of the
specimen from Fox-Amphoux FAM 03.064 ([14]: figs. 2–5).
Specifically, the latter has a continuously convex rostral edge and a
straight lateral margin. In contrast, the frontal of Ampelosaurus atacis
([11]: fig. 4.2) resembles that of the specimen from Lo Hueco. It
shows, in particular, the extensive contribution to the roof of the
orbit and its correlated hemispheric depression on the ventral
surface. However, the frontal of this species is not identical to that
of MCCM-HUE-8741. For instance, the caudal border of the
orbital roof is much more ventral in A. atacis ([11]: fig. 4.2E) than
mentioned processes, which together constitute the roof of the
orbit. The rostromedial part of the ventral surface is separated
from this depression by a strong crest that runs caudally from the
rostrolateral zone toward the midline of the united frontals,
separating the orbital and narial portions of the braincase. The left
frontal is 57.3 mm long and 64.3 mm wide.
The frontals of MCCM-HUE-8741 differ greatly from those of
the Transylvanian titanosaurian braincase FGGUB 1007 ([15]: fig.
15). In the latter specimen, the lateral margin of the frontal is
roughly straight, whereas in the Lo Hueco specimen the
participation of the frontal in the orbital margin distinctly stands
out laterally. Also, in the Transylvanian specimen, the frontals are
oriented strongly ventrally from the articulation with the parietal.
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Neurocranium of a Spanish Titanosaurian
rostromedially low, rounded outgrowths. In contrast, the conjoined parietals of Ampelosaurus atacis ([11]: fig. 4.2A) look similar in
morphology to that of MCCM-HUE-8741. Le Loeuff ([11]:119–
120) noted similarities between the parietal of A. atacis and that of
Antarctosaurus wichmannianus, which does resemble that of the
specimen from Lo Hueco in its arcuate dorsal crest ([21]:pl. 28
fig. 2, [22]:pls 63, 64 fig. e). The parietal of MCCM-HUE-8741 is
also very close to that of the specimen from Fox-Amphoux ([14]:
figs. 2–5), which possibly bore a similarly shaped crest. The
parietal of MCCM-HUE-8741 is distinct from that of Nemegtosaurus
mongoliensis ([6]: fig. 7, [17]: fig. 4a, pl. 13 fig. 1), which bears a
prominent dorsal crest that is not nearly as biarcuate. The
conjoined parietals of N. mongoliensis also show a short, flat median
suture ([6]: fig. 7).
Supraoccipital. The precise morphology of the supraoccipital cannot be ascertained due to imperfect preservation. It appears
to have been strongly convex and may have born a median nuchal
crest (for ligament insertion), at least in its more dorsal part. It is
presently pierced by two irregular apertures dorsally in its suture
with the parietal. The participation of the supraoccipital to the
foramen magnum cannot be known for sure, but it did not exceed
the most dorsal quarter to judge from the position of the proatlas
facets, which are typically borne by the exoccipitals. The
supraoccipital is only 10.1 mm deep (dorsoventrally) and
16.5 mm long (rostrocaudally).
The supraoccipital of MCCM-HUE-8741 resembles that of the
fragmentary titanosaur braincase described by Le Loeuff et al.
[12] which has a massive nuchal crest, though this is a fairly widely
distributed character in dinosaurs in general and in sauropods in
particular. A strong nuchal crest is also present in the supraoccipital of Ampelosaurus atacis ([11]: fig. 4.2D).
Otoccipital. There is no way to distinguish the exoccipital
from the opisthotic, and they presumably are co-ossified into a
single complex (otoccipital), as is typical in archosaurs. Each
otoccipital no doubt makes up most of the lateral margin of the
foramen magnum. It is marked by a small protuberance in its
dorsomedial area: the facet for the proatlas articulation. This bulge
distorts the edge of the foramen magnum and thereby gives the
latter a pyriform outline (21.1619.1 mm). Whereas the medial
otoccipital is strongly convex, the paroccipital process has a rather
flat occipital surface. The latter, which is fusiform in section, is
oriented ventrally and slightly caudally. Its state of preservation
distally does not allow affirming if it originally bore a nonarticulating ventral processes as in many titanosaurs, such as
Rapetosaurus krausei ([3]: fig. 19) and Saltasaurus loricatus ([22]: fig. 19).
The proximoventral margin of the otoccipital bears a groove-like
depression, whose ventral border is the tuberal crest (crista
tuberalis). CT scan data suggest that this furrow accommodated
the single hypoglossal nerve (XII) as it left the braincase. The
tuberal crest is extremely sharp and prominent. CT data reveal
that it overhangs proximally the jugular foramen (foramen
jugulare), which formed the exit of the vagoaccessory nerves (X–
XI), and that the oval window (fenestra ovalis = fenestra vestibuli)
opens just rostral to the latter. The better-preserved left otoccipital
is 49.4 mm wide.
Compared with that of MCCM-HUE-8741, the paroccipital
process of the braincase presented by Le Loeuff et al. [12] is much
stouter. Thus, it is much higher at its base than the foramen
magnum is wide ([12]:unnumb. pl.), whereas the height of the
paroccipital process of the specimen from Lo Hueco is roughly
similar to the transverse diameter of the foramen magnum. The
specimen described by Le Loeuff et al. [12] bears a small
protuberance at about midheight of the exoccipital. This
somewhat recalls that seen in MCCM-HUE-8741, though it is
Figure 4. Surface-rendered CT-based image of the endosseous
labyrinth of the right inner ear of the titanosaurian sauropod
Ampelosaurus sp. (MCCM-HUE-8741) from the Cretaceous of
Fuentes, Spain. In lateral view. Orientation was determined with the
lateral semicircular canal held roughly horizontal. Abbreviations: CRC,
crus commune; CSC, caudal ( = posterior, inferior) semicircular canal; FV,
fenestra vestibuli ( = oval window); LSC, lateral ( = horizontal) semicircular canal; RSC, rostral ( = anterior, superior) semicircular canal; VE,
vestibule of inner ear. Scale bar equals 1 cm.
doi:10.1371/journal.pone.0054991.g004
in the specimen from Lo Hueco and its lateral margin is not
embayed ([11]: fig. 4.2A–B). The frontal of MCCM-HUE-8741 is
clearly distinct from that of Nemegtosaurus mongoliensis ([6]: fig. 7),
which has a fairly flat dorsal surface and mostly convex lateral
margin marked with discrete transverse wrinkles. The frontal of N.
mongoliensis ([6]: fig. 7) also bears a rostromedial depression, which
is absent in MCCM-HUE-8741. The latter concavity is also
present in Quaesitosaurus orientalis [6].
Parietal. The dorsal margin of the conjoined parietals is
marked by a v-shaped crest. The midpoint of this prominence
contacts the supraoccipital caudally, whereas laterally the parietal
sends two occipital wings. These extensions are not fully preserved,
but they would have bordered the upper temporal fenestrae
caudally, at least in their medial half. The caudal border of each
occipital wing would have constituted the dorsal margin of the
post-temporal fenestrae, but there is no evidence of these openings,
suggesting they were either absent or situated laterally to the
occiput as preserved. An aperture of angular outline is visible on
the midline of the cranial roof near the frontoparietal contact. Its
position is consistent with its identification as a pineal foramen (but
see below). As preserved, the parietal is 79.6 mm wide.
The parietals of MCCM-HUE-8741 are clearly different from
the unfused ones of the juvenile titanosaurian braincase FGGUB
1007 ([15]: fig. 15). The latter are extremely unusual in bearing
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Neurocranium of a Spanish Titanosaurian
not situated on the margin of the foramen magnum but slightly
more distally. Similar protuberances are also found in the
Dongargaon specimen ([23]: fig. 2) from the Maastrichtian of
India and that from Balochistan ([24]: fig. 2C), Maastrichtian of
Pakistan, as well as in other sauropods (e.g., Spinophorosaurus
nigerensis [25]: fig. 3B, S1, S2, S3). In contrast, no such feature is
seen on the otoccipital of Lirainosaurus astibiae ([9]: fig. 2A),
Ampelosaurus atacis ([11]: fig. 4.2D), and the specimen reported by
Allain ([13]:pl. 6 fig. 1A). The paroccipital process of the latter
specimen is oriented also more strongly caudally than that of the
Lo Hueco specimen. The otoccipital of MCCM-HUE-8741 is
clearly distinct from that of Nemegtosaurus mongoliensis ([6]: fig. 7,
[17]: fig. 5a), whose paroccipital process is proportionally higher
(dorsoventrally) and more ventrally inclined. In addition, the
otoccipital of N. mongoliensis ([6]: fig. 7) does not bear any
noticeable proatlas facet. It displays, however, a prominent ridge
that extends from the dorsolateral margin of the foramen magnum
onto the paroccipital process, but subsides at the midlength of it. A
comparable elongate prominence is present in Quaesitosaurus
orientalis ([6]: fig. 18), whose paroccipital process has a tapered
prong distoventrally ([6]: fig. 18). In both N. mongoliensis and Q.
orientalis, the foramen magnum is oval with the long axis oriented
dorsoventrally ([2]: fig. 2a, [6]: figs. 9, 18, [17]: fig. 5a, pl. 12 fig. 2).
Basioccipital. The basioccipital of the specimen from Lo
Hueco is remarkable in having an occipital condyle that is much
broader laterally than high in caudal view. Thus, the occipital
condyle is wide (a little wider than the foramen magnum), but it is
dorsoventrally low. The non-hemispherical form of the occipital
condyle, which appears to be genuine given the lack of any
indication of effective taphonomic compression, might have
favored the dorsoventral and mediolateral motions of the head
over those in the diagonal. The lowness of the condyle is
responsible for a condylar neck whose lateral surfaces are very
convex dorsoventrally, whereas the ventral side is much flatter.
Therefore, the occipital condyle is not well separated from its neck
ventrally. However, and despite the wideness of the neck, the
occipital condyle stands out from it laterally (best seen on the
better-preserved left size). The irregular surface of the occipital
condyle is at least partly related to the loss of the original
cartilaginous covering. No participation of the otoccipital in the
occipital condyle is evident, but almost all sutures are obliterated.
A part of the left basal tuber is visible at this level, which means
that the complete braincase was especially low (the skull as a whole
may have been high, though). Probably only the dorsal half or so
of the preserved basal tuber was made up by the basioccipital. It is
oriented laterally, and its lateral surface appears to have been
rugose, which is common in titanosaurians. The occipital condyle
is 28.6 mm wide and 15.8 mm deep. The tubera:condyle width
ratio of MCCM-HUE-8741 is very high (at least 2.33).
Like MCCM-HUE-8741, Ampelosaurus atacis has a transversely
ovoid occipital condyle ([11]: fig. 4.2D). The juvenile titanosaurian
braincase FGGUB 1007 ([15]: fig. 15) also has a somewhat
laterally elongate occipital condyle, but it appears more rounded
ventrally. The basioccipital of Lirainosaurus astibiae ([9]: figs. 2–3) is
clearly different from that of the specimen from Lo Hueco. For
instance, the occipital condyle is much taller (more hemispherical)
in L. astibiae than in MCCM-HUE-8741. The ventral border of the
articular surface of the occipital condyle stands out from the neck
in a very marked way in L. astibiae, whereas this border is almost in
continuity with the neck in the specimen from Lo Hueco. In
addition, the basal tubera of L. astibiae are significantly more
ventrally extended than those of the specimen from Lo Hueco,
hinting at a deeper braincase in the former. They are also
positioned much more caudally, more or less at the vertical level of
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the occipital condyle, whereas they are approximately at the
vertical level of the supraoccipital in MCCM-HUE-8741. The
basioccipital of the titanosaurian braincase reported by Allain [13]
is also clearly different from that of MCCM-HUE-8741. For
instance, in that specimen the occipital condyle is a bit deformed,
but subtriangular in outline, not ovoid as in the Lo Hueco
specimen. Its neck is also a little longer in proportion, the articular
surface of the condyle extends ventrally beyond the ventral border
of the neck and, above all, the ventrolateral sides of the neck are
concave. The basal tubera have a more habitual (more ventral)
position. In fact, the basal tubera emerge at a variable level in
sauropods. Thus, the camarasaurid Camarasaurus lentus ([26]: fig.
23A), the dicraeosaurid Dicraeosaurus hansemanni ([27]: fig. 96), and
other species (including most titanosaurians) have more ventral
basal tubera than does MCCM-HUE-8741, which is similar in this
respect to some species such as the brachiosaurid Giraffatitan brancai
([27]: figs. 5, 7), two other basal titanosauriforms ([18]: fig. 1B, D,
[28]: fig. 3A, D), and the titanosaurians Mongolosaurus haplodon
([29]: fig. 2A) and Tapuiasaurus macedoi ([7]: fig. 1D). In MCCMHUE-8741, the neck of the occipital condyle does not show the
possibly autapomorphic ventral groove described by Dı́ez Dı́az
et al. [14] in FAM 03.064. The basioccipital of MCCM-HUE8741 differs unmistakably from that of Nemegtosaurus mongoliensis in
the relative size and the outline of the occipital condyle. Thus, in
N. mongoliensis, the occipital condyle is more than twice as broad as
the foramen magnum and its dorsal surface is distinctly concave in
the midline, whereas the ventral surface is convex in caudal view
([6]: fig. 9, [17]: fig. 5a, pl. 12 fig. 2). Whereas the difference in
relative size of the occipital condyle between MCCM-HUE-8741
and Quaesitosaurus orientalis is less marked than it is between the
former and N. mongoliensis, the difference in shape is more marked,
as Q. orientalis has a fairly hemispheric occipital condyle ([2]: fig.2,
[6]: fig. 18). The condyle width:height ratio of MCCM-HUE-8741
(1.81) are only approximated among sauropods by that of A. atacis
(1.79) and that of an indeterminate titanosaurian braincase (1.86)
described by Paulina-Carabajal and Salgado ([30]: fig. 2D),
whereas the tubera:condyle width ratios (which cannot be
ascertained in MDE C3–761 ) is close to that of the titanosaurian
Bonatitan reigi (2.24) ([29]:tab. 1).
Basiphenoid-parasphenoid. Based on CT scan data, this
bone complex (parabasisphenoid) would constitute the floor of the
preserved braincase from the rostral edge of the basioccipital to the
rostral wall of the pituitary fossa. The ventral half or so of the
preserved basal tuber is probably made up by the basisphenoid.
The pituitary fossa is ovoid in section, wider than long, and the
dorsum sellae is caudoventrally inclined. Very close to the pituitary
fossa, on both sides of it, the basisphenoid is pierced by a small
foramen caudally. CT scan data substantiate that it was for the
abducens nerve (VI), which therefore did not enter the pituitary
fossa in contrast to what is generally observed in most sauropods
[31]. In its middle part, the basisphenoid-parasphenoid is about
40.3 mm wide. The section of the pituitary fossa is 6.9 mm wide
and 3.7 mm long.
As in MCCM-HUE-8741 and most sauropods, the pituitary
fossa seems to have been inclined caudoventrally in Ampelosaurus
atacis ([11]: fig. 4.2) and Lirainosaurus astibiae ([9]: figs. 2–4). This
was also the case in the specimen reported by Allain [13], to judge
from the strongly caudoventrally oriented basisphenoid-parasphenoid.
Orbitosphenoid. The orbitosphenoid, which is rostral to the
pituitary fossa and laterosphenoid, is poorly preserved and
displaced dorsally. The left orbitosphenoid better preserves the
border of a single median aperture for the optic nerve (II). The
orbitosphenoid also ventrally borders the origin of the olfactory
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Neurocranium of a Spanish Titanosaurian
and endosseous labyrinth (Figures 3, 4, S1, S2, S3). Due to the
imperfect preservation of the braincase (displacement of the
orbitosphenoids into the cranial cavity, etc.), the rostroventral part
of the endocast is missing. As a consequence, the exact position
and configuration of the optic (II) nerve could not be determined.
For the sake of ease of description, we will refer to the
reconstructed digital casts of bone-bounded spaces that housed
soft-tissue structures as if they were the structures themselves (e.g.,
‘‘trigeminal nerve’’ instead of ‘‘digital cast of trigeminal canal’’).
Brain. As a consequence of the dorsoventral compression of
the braincase, the endocast has moderate pontine and cerebral
flexures (about 40u). As in Jainosaurus septentrionalis ([19]: fig. 6, [20]:
fig. 7) and most other non-avian archosaurs, the hindbrain and
midbrain are relatively poorly outlined in the endocast due to
former meningeal coverings and apparently substantial dural
venous sinuses, which obscure details of the optic lobes and the
cerebellum. In contrast with TMM 40435 ([18]: fig. 2A) and a few
other taxa such as cf. Cetiosaurus oxoniensis ([37]: fig. 6) and
Giraffatitan brancai ([27]:pl. 13 figs. 1–2), no ‘‘nub’’ betraying the
location of the cerebellum can be discerned. As in TMM 40435
[18] and many other archosaurs, the hindbrain is especially
narrow at the level of the otic capsules in MCCM-HUE-8741.
The cerebral region is separated from the hindbrain-midbrain
complex through a marked constriction caused by the laterosphenoid pillar in the endocranial cavity. In contrast with the
subset caudal to this pillar, the cerebral region of the brain is also
relatively well defined. In fact, it forms two reniform swellings in
dorsal view. The concavity of each one faces medially, resulting in
a median depression, a little off-centered caudally. We interpret
this morphology as being due to paired longitudinal dural venous
sinuses that coursed dorsolaterally through the cerebral region, as
previously described for Diplodocus longus ([31]: fig. 6.9D). The cleft
between these pronounced venous swellings is very deep and
broad suggesting that the two cerebral hemispheres were very little
inflated and must have been extremely modest. This configuration
is markedly different from that seen in the other few sauropods
with thin dural covering of the cerebral regions. Thus, in the
rebbachisaurid Nigersaurus taqueti ([38]: figs. 1F, S4) and the
titanosaurians Antarctosaurus wichmannianus ([39]: fig. 5B) and
Bonatitan reigi ([39]: fig. 2B), there is no median longitudinal
indentation in the cerebral region. This is especially worth
mentioning for the latter two taxa because their braincase is not
fundamentally different in overall morphology from MCCMHUE-8741 ([22]:pls 62–63, [40]: figs. 7–8). Rostrally, the cerebral
region prolongs into the olfactory tracts, whose dorsal aspect could
be reconstructed as it was roofed by the frontal. The caudalmost
part of the cerebral region of the Spanish specimen is topped by
only a moderate dural expansion. This is at odds with Jainosaurus
septentrionalis ([19]: fig. 6, [20]: fig. 7) in which this venous feature is
responsible for a sharp process on the endocast, about dorsal to the
putative location of the optic lobes. However, relatively much
more substantial dural expansions are known in the diplodocoid
sauropods Dicraeosaurus hansemanni ([27]:pl. 13 figs. 6–7) and
Diplodocus longus ([31]: fig. 6.9). In MCCM-HUE-8741, the small
median opening in the skull roof near the frontoparietal contact is
responsible for a swelling on the endocast that is evocative of a
pineal system. It is in the exact position where the pineal gland is
expected to have evaginated, between the forebrain and the
midbrain. However, the state of the bony margins of the aperture
in MCCM-HUE-8741 calls its genuineness and its identification as
a pineal foramen into question. Actually, the bone roofing this
region in sauropods is commonly very thin and damaged (see
discussion about the ‘‘pineal hypothesis’’ in sauropods in [31]:pp.
79–80). The pituitary fossa is incomplete distally, but was directed
tracts (I), by flooring the wide rostral aperture of the braincase.
The remaining border of the olfactory tract aperture (laterally and
dorsally) was constituted by the frontals. As preserved, the
orbitosphenoid extends rostrally from the pituitary fossa
17.5 mm along its median axis.
The original configuration of the orbitosphenoid of MCCMHUE-8741 was no doubt similar to that seen in Ampelosaurus atacis
([11]: fig. 4.2B–C), with a single conjoined optic foramen and a
broad, but low, olfactory aperture. A single optic foramen seems to
be homoplastically distributed in sauropods as it also appears to be
present in the basal eusauropod Shunosaurus lii ([32]: fig. 7B) and
Giraffatitan brancai ([27]: figs. 5–6), whereas Dicraeosaurus hansemanni
([27]: figs. 136–137), Camarasaurus lentus ([26]: fig. 24A), and
Nemegtosaurus mongoliensis ([6]: fig. 8) have two distinct openings.
Prootic. The prootic is a dorsoventrally high but rostrocaudally short bone. It is bordered largely by the basisphenoid
ventrally, the laterosphenoid rostrally, the parietal dorsally, and
the otoccipital caudally. The prootic is marked by a robust and
sharp otosphenoidal crest (crista otosphenoidalis = crista prootica),
which runs rostroventrally from the basis of the paroccipital
process to contact the basal tuber and most probably continued
ventrally to reach the basipterygoid process. This crest borders
caudally the large trigeminal foramen. The rostrocaudal distance
between the otosphenoidal crest and the antotic crest (crista
antotica) of the laterosphenoid (which corresponds approximately
with the caudal and rostral limits of the prootic) is 10.6 mm at the
level of the trigeminal foramen.
The otosphenoidal crest of MCCM-HUE-8741 is sharper and
more prominent than that of Ampelosaurus atacis ([11]: fig. 4.2B, E).
This difference, however, is more marked with Lirainosaurus astibiae
([9]: figs. 3A, 4C), the specimen reported by Allain [13], and FAM
03.064 ([14]: figs. 4–5).
Laterosphenoid. The laterosphenoid of MCCM-HUE-8741
is well preserved on the left side. It is bordered ventrally by the
basisphenoid, rostrally by the orbitosphenoid, dorsally by the
frontal and the parietal, and caudally by the prootic. The
laterosphenoid is characterized by a lamellar and slightly arcuate
capitate process that projects laterally and fits along the
caudolateral border of the frontal. In so doing, it participates to
the separation of the adductor chamber from the orbital cavity.
The ventromedial continuation of the capitate process, the antotic
crest, apparently constituted most of the rostral margin of a large,
somewhat heart-shaped pit at the bottom of which opens the
trigeminal foramen. Rostrally to the latter, on the suture with the
basiphenoid, a small foramen provided exit to the oculomotor (III)
and, possibly, the trochlear nerves (IV), too. The left laterosphenoid is 33.3 mm wide and 19.8 mm long.
The comparisons of the laterosphenoid of MCCM-HUE-8741
with that of the other Laurasian Late Cretaceous titanosaurian
braincases, in which this element is either lacking or fused
indistinctly with surrounding bones like the orbitosphenoid, are
difficult or impossible. However, MCCM-HUE-8741 appears in
this respect much closer to Ampelosaurus atacis ([11]: fig. 4.2B) than
to the specimen reported by Allain [13], which presents a stronger
capitate process.
Neuroanatomy
The first virtual cranial cavity endocast of a dinosaur (a
theropod) was generated from CT scans more than a decade ago
[33–34]. This method was first applied to a sauropod some years
later ([35]: fig. 25), nearly a century after the first published
detailed figuration of a physical endocast made from a specimen of
this group ([36]: fig. 16A). In the present case, the processing of the
CT data resulted in a very close rendering of the cranial endocast
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Neurocranium of a Spanish Titanosaurian
dorsoventrally elongated foramen in (or mostly constituted by) the
otoccipital, the metotic fissure (fissura metotica). However, it
possibly left the braincase through a small aperture of its own, the
occipital recess (recessus scalae tympani), which is located at the
ventral end of the otoccipital, about where the tuberal crest
subsides. Hence, MCCM-HUE-8741 might shows an unusual
configuration in which the glossopharyngeal nerve appears to be
separate from and ventral to the vagoaccesory nerve, in contrast to
the condition known in other sauropods (see e.g.,
[20,25,31,39,41,43]), in which the glossopharyngeal and vagoaccesory nerves are more closely arranged.
The vagoaccesory nerve (X-XI) leaves the braincase through a
moderately-sized jugular foramen that is located immediately
caudally to the oval window. Tidwell and Carpenter ([18]: fig. 2A)
identified an independent accessory nerve (XI) at mid-distance
between the fissura metotica/jugular foramen and a single
hypoglossal foramen. This is most probably incorrect as this
stands out in sharp contrast with the general condition, in which
the accessory nerve (XI) has joined the vagus (X) (see e.g., [44]).
The hypoglossal nerve (XII) has a single root entering the
braincase wall (otoccipital) very close to the rim of the foramen
magnum. This situation suggests it is homologous with the
caudalmost hypoglossal root of other sauropods. Such a configuration is highly remarkable because most sauropods, other than
titanosaurians (including Jainosaurus septentrionalis ([20]: figs. 4, 7)),
have two hypoglossal roots ([31,39]). The basal titanosauriform
Giraffatitan brancai has also two roots ([27]: fig. 116). We interpret
the putative accessory nerve of TMM 40435 ([18]: fig. 2A) as
actually a rostral root of the hypoglossal nerve, which suggests that
this specimen is from a primitive, non-titanosaurian, titanosauriform.
Inner ear. A beautiful rendering of the right labyrinth could
be arrived at, whereas merely the vestibule and base of the lagena
were reconstructed on the left side. The semicircular canals are
contracted, i.e. the radius of the arc they describe is small and,
therefore, they are highly curved. The longest semicircular canal
(but only moderately so) is the rostral one and the lateral
semicircular canal is the shortest, which is the most common
configuration in vertebrates [45–46]. The semicircular system of
MCCM-HUE-8741 shows also a plesiomorphic morphology in
that the planes delimited by each semicircular canal do not
intersect; that is, neither of the vertical semicircular canals passes
ventral to the lateral one and not any of the former extends behind
or ahead of their common leg (crus commune) [47]. The latter
presents a blunt apex. Another archaic character is that the
ampullae of the semicircular canals are not discernibly inflated,
which is to weigh against the sizeable vestibule. The rostral
semicircular canal is oriented at an angle of about 45u with the
midline of the endocast. The angle between the rostral and lateral
semicircular canals is about 85u (85u in Spinophorosaurus nigerensis,
100u in Giraffatitan brancai), that between the two vertical
semicircular canals is about 75u (75u in S. nigerensis, 80u in G.
brancai), and that between the posterior and lateral semicircular
canals is about 95u (100u in S. nigerensis, 95u in G. brancai). The
lagena (cochlear duct) is extremely short, not extending ventrally
beyond the oval window. The latter draws indeed a dorsoventrally
elongate oval.
The labyrinth of MCCM-HUE-8741 is largely reminiscent of
that of other titanosaurians such as Bonatitan reigi and Antarctosaurus
wichmannianus ([39]: fig. 9). It is markedly different from that of the
basal sauropod Spinophorosaurus nigerensis ([25]: fig. 5, S1, S2, S3).
More surprisingly, the labyrinth of MCCM-HUE-8741 is equally
distinct from that of the basal titanosauriform Giraffatitan brancai
([27]: figs. 119–126). These differences, which rest in part on the
strongly caudally as indicated by the sturdily inclined dorsum
sellae. This is reminiscent of the condition in the titanosaurian
Bonatitan reigi ([39]: figs. 1–3) and many other archosaurs.
In striking contrast with more basal sauropods such as
Spinophorosaurus nigerensis ([25]: fig. 4, S1, S2, S3), there is no
evidence of a complex endocranial venous system that is highly
anastomotic and partly invades the laterosphenoid laterally and
the occiput caudally, but this absence is possibly due to issues
pertaining to both preservation and the resulting quality of the CT
scan data. According to Kurzanov and Bannikov ([2]:p. 95), in
Quaesitosaurus orientalis the middle cerebral vein is accommodated
by an arcuate groove on the inner surface of the braincase before
passing through the wall of it. This configuration is reminiscent of
a variety of sauropods (e.g., cf. Cetiosaurus oxoniensis ([37]: fig. 6),
Dicraeosaurus hansemanni ([27]:pl. 13 fig. 6–7), Giraffatitan brancai
([41]: figs. 1–2) and indeed many other archosaurs, but not any
titanosaurian (see e.g., [39]), and thus its presence in Q. orientalis
merits confirmation.
Cranial nerves. A single nerve trunk emerges from the
lateral side of the hypophyseal peduncle. Given the displacement
of the orbitosphenoid in MCCM-HUE-8741, it is difficult to
determine whether this single aperture is just for the oculomotor
(III) nerve or potentially also for the trochlear (IV) nerve. Both
conditions are found among sauropods. For example, in Jainosaurus
septentrionalis ([19]: fig. 6, [20]: fig. 7), Camarasaurus lentus ([31]: fig.
6.8), and many other sauropods, these two nerves are more or less
close to one another, but not fused. However, this combined
oculomotor-trochlear aperture does occur in taxa such as
Nigersaurus taqueti ([38]: fig. 1, S4), Suuwassea emilieae (specimen
ANS 21122), Dicraeosaurus hansemanni ([27]:pl.13 figs. 6–7), and
Diplodocus longus ([31]: fig. 6.9). It remains a possibility that the
trochlear nerve emerges more dorsally, between the laterosphenoid and orbitosphenoid, as seen in other taxa.
More caudally on the brainstem, the trigeminal nerve (V) comes
into view. As usual in archosaurs, it is the largest of the cranial
nerves. The roughly heart-shaped outline of the trigeminal
foramen is related to the division of this nerve into rostral
(ophthalmic, V1) and caudal (maxillomandibular, V2,3) rami. In
Jainosaurus septentrionalis ([19]: fig. 6, [20]: fig. 7), the trigeminal
foramen presents a very unusual slit-like internal outline.
The abducens nerve (VI) emerges from the ventral surface of
the brainstem, courses rostroventrally and, as far as it can be
observed, passes lateral to the pituitary fossa. This is in contrast
with the general condition in sauropods (see e.g., cf. Cetiosaurus
oxoniensis ([37]: fig. 6), Diplodocus longus ([31]: fig. 6.9), Giraffatitan
brancai ([41]: fig. 1)) in which the abducens nerve enters the
pituitary space. The same primitive pattern is seen in TMM 40435
([18]: fig. 2A), but not in titanosaurians [39], and thus MCCMHUE-8741 conforms to the derived condition observed in this
clade.
The facial nerve (VII) emerges caudal to the trigeminal nerve
(V) and passes ventrolaterally. The situation of the facial nerve
with respect to the trigeminal nerve is identical in MCCM-HUE8741 and Bonatitan reigi ([39]: fig.2). In other taxa, the facial nerve
may be closer to the trigeminal nerve (e.g., cf. Cetiosaurus oxoniensis
([37]: fig. 6) or in the vicinity of the otic region (e.g., Camarasaurus
lentus ([31]: fig. 6.8)). As in other sauropods and reptiles in general
(see [42]), the facial nerve of MCCM-HUE-8741 is of very small
diameter.
A great deal of caution needs to be exercised in inferring the
course of the glossopharyngeal nerve (IX). Our tentative interpretation of the CT scan data is that this nerve emerges from the
brain stem and penetrates the braincase wall together with the
vagoaccesory nerve (X-XI) and the internal jugular vein through a
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Neurocranium of a Spanish Titanosaurian
significantly more elongate semicircular canals in S. nigerensis and
G. brancai, are discussed below.
Spain of a sauropod species close (or identical) to one from
approximately contemporaneous sediments in south-western
France (at present almost 500 km farther northeast) is actually
not unexpected. The Iberian Massif island (on which Lo Hueco is
situated) and the emerged area of the Ebro Massif (where Bellevue,
the type locality of A. atacis, is located) were admittedly separated
by a shallow strait in early Campanian time [49]. However, this
seaway had disappeared by the late Maastrichtian due to marine
retreats, removing a serious barrier to the interchange of large land
vertebrates between the Iberian Massif and the French Craton
through the Ebro Massif and the Corsica-Sardinia Block [50].
From a paleoneuroanatomical viewpoint and if we take our
reconstruction (which is unavoidably a simplified and somewhat
distorted reflection of the genuine neuroanatomy) at face value,
the endocast of MCCM-HUE-8741 is as dissimilar from that of a
more basal form such as Spinophorosaurus nigerensis [25] as it is
reminiscent of other titanosaurians [39]. The cerebral region
appears to have been covered by a tight dural envelope that
accommodated a potentially simple venous system, for the most
part reduced to longitudinal sinuses. This results in an ‘‘unadorned’’ and straightforwardly interpretable endocast (as far as
the cerebral region is concerned at least). In addition, even though
the cranial nerves present roughly the configuration seen in other
sauropods, there are derived features that appear to characterize
titanosaurians, such as the abducens nerve (VI) that passes lateral
to the pituitary fossa rather than entering it and the hypoglossal
nerve (XII) that exits the skull via a single foramen [39]. These
features are at variance with most saurischians, including
Giraffatitan brancai, which is a basal titanosauriform [41]. In
contrast with Spinophorosaurus nigerensis and Giraffatitan brancai but
similar to other sauropods such as Camarasaurus lentus ([38]: S5F–
G), the labyrinth shows a dramatic reduction of the magnitude of
the vestibular system such that the rostral semicircular canal is not
much longer than the caudal canal.
The functional significance of the differential development of
the semicircular canals in sauropods has been recently brought up
by Knoll et al. [25]. It has long been hypothesised (see e.g.,
[51]:pp. 19, 161) that the greater the radius of the semicircular
canals, the greater the locomotor agility of its holder. Again
recently, Cox and Jeffery [52] showed that the canal radii were
positively correlated with agility of locomotion in mammals. The
same authors [53] demonstrated that the semicircular canal
morphology in some mammals is arranged primarily for perceiving head movements and then secondarily for sending their
impulses for compensatory eye movements (vestibulo-ocular
reflex). A number of reports have suggested relationships between
semicircular canal morphology and locomotor agility in birds as
well. For instance, Hadžiselimović and Savković [54] have
demonstrated that the canals are short and thick with poorly
marked ampullae in clumsy fliers. In contrast, few investigations
have focused on the possible correlation between morphology of
the semicircular canals and behavioral pattern in reptiles (see in
particular [55]). Inasmuch as no sauropod would qualify as a
physically nimble animal, the development of the semicircular
canals in any given taxon may be more probably related, inter alia,
with the natural range of turning movements of its head.
Discussion
The specimen from Lo Hueco is especially remarkable in its
dorsoventral compression, most of which seems to be natural,
although there is little doubt that some deformation occurred
postmortem. Dorsoventral compression of the braincase is an
uncommon character in sauropods (and saurischians as a whole),
but it is shared with the titanosaurian braincases of the Isisaurusmorph sensu Wilson et al. [20]. This is in contrast with other
European Late Cretaceous titanosaurian braincases, such as
FGGUB 1007 ([15]: fig. 15), which is short and deep. The
titanosaurian braincases of the Isisaurus-morph also resemble
MCCM-HUE-8741 in having an occipital condyle that is strongly
deflected ventrally relative to the skull roof (frontals and parietals)
so that the long axis of the occipital condyle approximates the
plane of the occiput (paroccipital processes and supraoccipital). In
contrast, the long axis of the occipital condyle and the plane of the
skull roof are subparallel in taxa such as Nemegtosaurus mongoliensis
[6].
Although the number of sauropod braincases from the Late
Cretaceous European archipelago found to date is limited, it shows
a significant diversity. As evidenced by the comparisons above, the
specimen from Lo Hueco resembles the braincase of Ampelosaurus
atacis MDE C3–761 ([11]: fig. 4.2). This last specimen is yet to be
described in detail but, as far as these two braincases can be
compared, they are fairly similar. Naturally, they present a
number of characters that are more or less widely distributed in
titanosaurians including fused frontals, a frontal with a medial
convexity on the dorsal surface, a contribution of the frontal to the
margin of the upper temporal fenestra, a rostrocaudally short
upper temporal fenestra (and therefore weak jaw adductors) that
faces dorsolaterally, a rostral portion of parietal that is relatively
broad and a caudal portion that is inclined caudally with a marked
dorsal crest and laterally extended occipital wings, and other
features. But, more significantly, both MCCM-HUE-8741 and
MDE C3–761 have a flat occiput with transversely oriented
paroccipital processes. According to Curry Rogers ([48]:appx 2.1),
such an occipital plate is known only in one other titanosaurian in
her character/taxon matrix: Jainosaurus septentrionalis. However,
MCCM-HUE-8741 is easily distinguished from J. septentrionalis,
whose occipital condyle is hemispheric and with a long axis
subparallel to the skull roof [20]. MCCM-HUE-8741 therefore
appears closer in morphology to A. atacis than to any other
titanosaurian, especially any other specimens from the SantonianMaastrichtian from north of the Tethys known so far. The sizes of
MCCM-HUE-8741 and MDE C3–761 are also commensurate.
However, there appear also to be differences between MCCMHUE-8741 and MDE C3–761. Thus, the latter is less dorsoventrally compressed and lacks proatlas facets. Also, the frontal orbital
margin of MDE C3–761 is not embayed, whereas there is a
rostrolateral and a caudolateral prong on the frontal in MCCMHUE-8741. In view of the above-mentioned similarities, we judge
that a provisional attribution of MCCM-HUE-8741 to the genus
Ampelosaurus is reasonable. However, we find it difficult to assess
the significance of the differences between MCCM-HUE-8741
and MDE C3–761 given our extremely poor knowledge of
intraspecific variation in cranial morphology among sauropods in
general and titanosaurians in particular. Hence, the former is
better left at this time in open nomenclature as Ampelosaurus sp.
Incidentally, strongly spatulate teeth alike those of A. atacis were
discovered at Lo Hueco ([1]:p. 1275). The presence in mid-eastern
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Supporting Information
Figure S1 Interactive visualization made from the CT
scan of the braincase of the sauropod dinosaur Ampelosaurus sp. (MCCM-HUE-8741) from the Late Cretaceous of Fuentes, Spain (small file).
(PDF)
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Neurocranium of a Spanish Titanosaurian
Interactive visualization made from the CT
scan of the braincase of the sauropod dinosaur Ampelosaurus sp. (MCCM-HUE-8741) from the Late Cretaceous of Fuentes, Spain (medium file).
(PDF)
0392-P11 issued by the Dirección General de Patrimonio y Museos of the
Junta de Comunidades de Castilla-La Mancha. All necessary permits were
obtained for the described study, which complied with all relevant
regulations. R. Allain (Muséum national d’Histoire naturelle, Paris)
provided access to the titanosaurian cranial material under his care. V.
Dı́ez Dı́az (Universidad del Paı́s Vasco, Bilbao) supplied unpublished
photographs of MDE C3–761. M. D. D’Emic (Stony Brook University,
Stony Brook) and P. D. Mannion (Imperial College London, London)
provided useful comments on the manuscript.
Figure S2
Interactive visualization made from the CT
scan of the braincase of the sauropod dinosaur Ampelosaurus sp. (MCCM-HUE-8741) from the Late Cretaceous of Fuentes, Spain (large file).
(PDF)
Figure S3
Author Contributions
Conceived and designed the experiments: FK LMW. Performed the
experiments: FK LMW RCR. Analyzed the data: FK LMW RCR.
Contributed reagents/materials/analysis tools: FO JLS LMW RCR.
Wrote the paper: FK LMW.
Acknowledgments
The August-December 2007 excavations at Lo Hueco, in which FK, FO,
and JLS took part, were carried out according to the authorization 04-
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