Cranial anatomy of the Late Jurassic dwarf sauropod Europasaurus holgeri (Dinosauria, Camarasauromorpha): ontogenetic changes and size dimorphism

Abstract

Sauropods were the most successful herbivorous group of dinosaurs during the Mesozoic era. Despite their supremacy as reflected in the fossil record, sauropod skulls are very rare and current knowledge of skull anatomy is based on just a few taxa. Juvenile skull bones are even rarer than adult skulls; thus, our understanding of their morphology and ontogenetic changes is limited. The recent discovery of several adult and juvenile specimens of a Late Jurassic taxon from Germany, Europasaurus holgeri, extends our knowledge of sauropod skull anatomy. A total of 123 skull bones, representing at least 14 skulls, were examined, described and compared to other taxa. The skull material includes several individuals of various ontogenetic stages. Because size alone is not sufficient to determine the morphological ontogenetic stage (MOS), sizeindependent characters were used to stage the bone elements. Detailed studies of the skull bones proved that the material represents two morphotypes, independent of ontogenetic stage. Since the original description of Europasaurus, new skull material has been found, and an updated skull reconstruction of an adult individual is presented here. All the autapomorphic characters of Europasaurus recognized in the skull (i.e. anteroposteriorly long and lateromedially narrow frontal; presence of postparietal fenestra; large participation of the jugal to the ventral rim of the skull and the orbit; presence of a postparietal foramen and single optic foramen) are plesiomorphic characters of basal sauropodomorphs and/ or present in embryos and juvenile sauropods. Therefore, we consider that in Europasaurus these characters evolved through paedomorphosis, which resulted in the dwarf condition of this taxon.

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Cranial anatomy of the Late Jurassic dwarf
sauropod Europasaurus holgeri (Dinosauria,
Camarasauromorpha): ontogenetic changes and size
dimorphism
Jean Sebastian Marpmanna, José Luis Carballidob, P. Martin Sandera & Nils Knötschkec
a Steinmann Institute, Division of Palaeontology, University of Bonn, Nussallee 8, 53115
Bonn, Germany
b Consejo Nacional de Investigaciones Científicas y Técnicas, Museo Paleontológico Egidio
Feruglio, Fontana 140, 29100 Trelew, Argentina
c Dinosaurier-Freilichtmuseum Münchehagen, Alte Zollstrasse 5, 31547 Rehburg-Loccum,
Germany
Published online: 27 Mar 2014.
To cite this article: Jean Sebastian Marpmann, José Luis Carballido, P. Martin Sander & Nils Knötschke (2014): Cranial
anatomy of the Late Jurassic dwarf sauropod Europasaurus holgeri (Dinosauria, Camarasauromorpha): ontogenetic changes
and size dimorphism, Journal of Systematic Palaeontology, DOI: 10.1080/14772019.2013.875074
To link to this article: http://dx.doi.org/10.1080/14772019.2013.875074
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Cranial anatomy of the Late Jurassic dwarf sauropod Europasaurus holgeri
(Dinosauria, Camarasauromorpha): ontogenetic changes and size dimorphism
Jean Sebastian Marpmann
a
, Jos
e Luis Carballido
b
*, P. Martin Sander
a
and Nils Kn€
otschke
c
a
Steinmann Institute, Division of Palaeontology, University of Bonn, Nussallee 8, 53115 Bonn, Germany;
b
Consejo Nacional de
Investigaciones Cient
ıficas y T
ecnicas, Museo Paleontol
ogico Egidio Feruglio, Fontana 140, 29100 Trelew, Argentina;
c
Dinosaurier-
Freilichtmuseum M€
unchehagen, Alte Zollstrasse 5, 31547 Rehburg-Loccum, Germany
(Received 3 June 2013; accepted 24 October 2013)
Sauropods were the most successful herbivorous group of dinosaurs during the Mesozoic era. Despite their supremacy as
reflected in the fossil record, sauropod skulls are very rare and current knowledge of skull anatomy is based on just a few
taxa. Juvenile skull bones are even rarer than adult skulls; thus, our understanding of their morphology and ontogenetic
changes is limited. The recent discovery of several adult and juvenile specimens of a Late Jurassic taxon from Germany,
Europasaurus holgeri, extends our knowledge of sauropod skull anatomy. A total of 123 skull bones, representing at least
14 skulls, were examined, described and compared to other taxa. The skull material includes several individuals of various
ontogenetic stages. Because size alone is not sufficient to determine the morphological ontogenetic stage (MOS), size-
independent characters were used to stage the bone elements. Detailed studies of the skull bones proved that the material
represents two morphotypes, independent of ontogenetic stage. Since the original description of Europasaurus, new skull
material has been found, and an updated skull reconstruction of an adult individual is presented here. All the
autapomorphic characters of Europasaurus recognized in the skull (i.e. anteroposteriorly long and lateromedially narrow
frontal; presence of postparietal fenestra; large participation of the jugal to the ventral rim of the skull and the orbit;
presence of a postparietal foramen and single optic foramen) are plesiomorphic characters of basal sauropodomorphs and/
or present in embryos and juvenile sauropods. Therefore, we consider that in Europasaurus these characters evolved
through paedomorphosis, which resulted in the dwarf condition of this taxon.
Keywords: Macronaria; ontogeny; maturity; dimorphism; dwarfism; island rule; heterocrony; Late Jurassic
Introduction
Sauropods are the largest terrestrial vertebrates and most
successful herbivorous non-avian dinosaurs to have ever
existed (e.g. Upchurch et al. 2004; Sander et al. 2010;
Clauss 2011; Hummel & Clauss 2011). They achieved a
global distribution and spanned the Late Triassic (Buffe-
taut et al. 2000; Yates & Kitching 2003) to the very end
of the Cretaceous (Fastovsky & Weishampel 2005;
Schulte et al. 2010). These colossal animals, which could
attain body lengths of more than 40 m (Sander & Clauss
2008; Sander et al. 2010) and weigh 100 tonnes
(Upchurch et al. 2004; Sander & Clauss 2008; Sander
et al. 2010), are characterized by massive bodies with pil-
lar-like limbs, extremely elongated necks and tails, and
small skulls (Upchurch et al. 2004; Fastovsky & Weish-
ampel 2005, Chure et al. 2010).
Approximately 175 valid sauropod genera are known to
date (Upchurch et al. 2011), with few specimens preserv-
ing cranial remains (Mannion & Upchurch 2010). Find-
ings of sauropod embryos, hatchlings or juveniles are
even less common (Carpenter & McIntosh 1994;
Upchurch et al. 2004; Foster 2005). So far, young sauro-
pod individuals are known from only a few specimens
worldwide, yet a large number of descriptions have been
made in the 21st century (see Table 1). Due to the lack of
juvenile sauropod skulls, no extensive growth series exists
for their cranial bones. Thus, morphological changes in
ontogeny are not fully understood, and major morphologi-
cal transformations are difficult to interpret (e.g. Carbal-
lido & Sander 2014; Wedel & Taylor 2013). Additional
difficulties include evaluating the phylogenetic affinities
of juvenile specimens (Schwarz et al. 2007; Carballido
et al. 2012).
Usually, small bones of sauropod dinosaurs are consid-
ered parts of juvenile specimens. But the diminutive Euro-
pasaurus holgeri from Kimmeridgian shallow marine
sediments of northern Germany (Sander et al. 2006, fig.
1) is a classical example of an island dwarf or phyletic
nanoid (Sander et al. 2006; Benton et al. 2010; Stein et al.
2010), which most likely evolved by a heterochronic pro-
cess (Sander et al. 2006; Benton et al. 2010; Stein et al.
*Corresponding author. Email: jcarballido@mef.org.ar
ÓThe Trustees of the Natural History Museum, London 2014. All Rights Reserved.
Journal of Systematic Palaeontology, 2014
http://dx.doi.org/10.1080/14772019.2013.875074
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2010). An heterochrony resulted in miniaturization is
known as paedomorphosis, i.e. the retention of juvenile
characters of ancestors (Alberch et al. 1979). Evidence to
support the dwarf status of Europasaurus was provided
by the histological study of several long bones carried out
by Sander et al. (2006). The histology revealed different
growth stages including juveniles, subadults and fully
grown individuals.
Europasaurus is the only sauropod with several indi-
viduals that have skull elements representing various
ontogenetic stages. Recently, a complete description and
re-evaluation of the axial skeleton suggested the presence
of two different morphotypes, which mainly differ in size
and stage of skeletal maturity (Carballido & Sander
2014). Here we provide a detailed description of each
skull bone recovered to date, as well as the ontogenetic
stage for each of these bones. The focus of this study is to
evaluate the cranial material of the most complete collec-
tion of disarticulated skull bones of a single sauropod
taxon and to establish a detailed growth series to ascertain
the morphological changes during sauropod cranial ontog-
eny, as well as potentially to detect postcranial dimor-
phism in the skull material. Furthermore, the presence of
new autapomorphic characters are discussed as well as
the recognition of three different morphological ontoge-
netic stages (MOS) in both morphotypes (see Carballido
& Sander 2014) and the presence of numerous paedomor-
phic characters that result from dwarfing. Europasaurus
Table 1. List of better-documented juvenile sauropods and preserved regions (skull, axial, appendicular). Juvenile material is tentatively
staged as Em (embryonic), EJ (early juvenile) and LJ (late juvenile), mainly based on referred publications.
Taxon Ontogenetic stage Material Most relevant references
Sauropoda
Tazoudasaurus EJ Axial and appendicular Allain & Aquesbi (2008)
Eusauropoda
Barapasaurus LJ Appendicular bones Bandyopadhyay et al. (2010)
Patagosaurus LJ Skull, axial and appendicular Coria (1994)
Chebsaurus LJ Skull, axial and appendicular Mahammed et al. (2005)
Neosauropoda
Haplocanthosaurus LJ Axial and appendicular bones Hatcher (1903)
Macronaria
Bellusaurus LJ Skull, axial and appendicular Dong (1990)
Europasaurus EJ–LJ Skull, axial and appendicular Klein & Sander (2008); Carballido &
Sander (2014)
Camarasaurus LJ Complete specimen Gilmore (1925)
Camarasaurus Em Premaxilla Britt & Naylor (1994)
Camarasaurus LJ Skull, axial and appendicular Ikejiri et al. (2005)
Camarasaurus LJ Axial and appendicular Foster (2005)
Titanosauriformes
Brachiosaurus? EJ Almost complete postcranial skeleton Schwarz et al. (2007); Carballido et al. (2011)
Titanosauria
Titanosauria indet. Em Skull (rest mainly un-ossified) Salgado et al. (2005); Garc
ıa et al. (2010)
Phuwiangosaurus EJ–LJ Axial and appendicular Martin (1994); Martin et al. (1994);
Martin et al. (1999)
‘Astrodon’ LJ Skull, axial and appendicular Carpenter & Tidwell (2005); D’Emic (2012)
Alamosaurus LJ Axial and appendicular Lehman & Coulson (2002)
Rocasaurus LJ Axial and appendicular Salgado & Azpilicueta, 2000
Rincosaurus LJ Axial and appendicular Calvo & Gonz
ales Riga (2003)
Bonitasaura LJ Skull, axial and appendicular Apestegu
ıa (2004); Gallina (2011);
Gallina & Apestegu
ıa (2011)
Bonatitan LJ Skull, axial and appendicular Martinelli & Forasiepi (2004)
Rapetosaurus LJ Skull, axial and appendicular Curry Rogers & Forster (2001, 2004, 2009)
Lirainosaurus ? Isolated teeth D
ıez D
ıaz et al. (2012)
Saltasaurus LJ Skull, axial and appendicular Powell (1992)
Diplodocoidea
Diplodocidae
Diplodocidae indet. EJ–LJ Axial Woodruff & Fowler (2012); Wedel &
Taylor (2013)
Diplodocus LJ Almost complete skull Whitlock et al. (2010)
Diplodocus? LJ Caudal vertebrae Foster (2005)
Apatosaurus LJ Axial and appendicular bones Foster (2005)
Rebbachisauridae
cf. Zapalasaurus Axial and appendicular bones Sagado et al. (2012)
2 J. S. Marpmann et al.
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holgeri has been described as a basal macronarian (Sander
et al. 2006), a position recently recovered by Ksepka &
Norell (2010), Carballido et al. (2011a,b) and Carballido
& Sander (2014). Nevertheless, Europasaurus was recov-
ered by D’Emic (2012) as a basal brachiosaurid due to the
presence of some synapomorphic characters of this group
in this taxon, but noting that the missing data could
strongly influence this position (see also Mannion et al.
2013). Although a new phylogenetic analysis lies outside
the scope of this contribution, detailed comparisons with
basal macronarians (e.g. Camarasaurus) and brachiosaur-
ids (e.g. Giraffatitan,Abydosaurus) are here provided.
Institutional abbreviations
CM: Carnegie Museum of Natural History, Pittsburgh, PA,
USA; CLH: Cuesta Lonsal Herrero, Galve, Spain;
DFMMh/FV: Dinosaurier-Freilichtmuseum M€
unchehagen/
Verein zur F€
orderung der Nieders€
achsischen Pal€
aontologie
e.V., Rehburg – Loccum, OT M€
unchehagen, Germany;
MACN: Museo Argentino de Ciencias Naturales
‘Bernardino Rivadavia,’ Buenos Aires, Argentina; MfN:
Museum f€
ur Naturkunde – Leibniz-Institut f€
ur Evolutions
und Biodiversit€
atsforschung an der Humboldt-Universit€
at
zu Berlin, Germany; MNN GAD: Musee National du
N

ıger, N

ıger; NMB: Staatliches Naturhistorisches Museum
Braunschweig, Braunschweig, Germany; PMU: Palaeonto-
logical Museum, Uppsala, Sweden; SMA: auriermuseum
Aathal, Aathal-Seegr€
aben, near Zurich, Switzerland;
BYUVP: Brigham Young University Vertebrate Palaeon-
tology,Provo,UT,USA;YPM: Yale Peabody Museum of
Natural History, New Haven, CT, USA.
Systematic palaeontology
Saurischia Seeley, 1887
Sauropodomorpha von Huene, 1932
Eusauropoda Upchurch, 1995
Neosauropoda Bonaparte, 1986
Macronaria Wilson & Sereno, 1998
Camarasauromorpha Salgado et al., 1997
Genus Europasaurus Mateus et al. in Sander et al.
2006
Europasaurus holgeri Mateus et al. in Sander et al.
2006
(Figs 1–14)
Holotype. DFMMh/FV 291: disarticulated left premax-
illa (DFMMh/FV 291.18), right maxilla (DFMMh/FV
291.17); right quadratojugal (DFMMh/FV 291.25), frag-
ment of a braincase (DFMMh/FV 291.15), left laterosphe-
noid–orbitosphenoid complex (DFMMh/FV 291.16),
right surangular (DFMMh/FV 291.10), left prearticular
(DFMMh/FV 291.24), left dentary (DFMMh/FV 291.11),
teeth (DFMMh/FV 291), cervical and sacral vertebrae,
and cervical and dorsal ribs assigned to one individual.
Referred material. The referred material represents at
least 14 individuals, but probably several more. The mini-
mum number of individuals is based on the number of sin-
gle dentary rami and size differences.
Horizon and locality. Late Jurassic, middle Kimmerid-
gian marine carbonate rocks, bed 93 of section at Langen-
berg Quarry, Lower Saxony basin, Oker near Goslar,
Lower Saxony, Germany.
Emended diagnosis. Europasaurus holgeri is diagnosed
from the following characters based on the holotype and
referred specimens: (1) anteroposteriorly long and latero-
medially narrow frontal with a very deep orbital rim
causing an extreme reduction of the frontal–prefrontal
and frontal–nasal articulations; (2) absence of quadrato-
jugal–maxilla contact and large participation of the jugal
to form the ventral margin of the skull; (3) extensive
ventral participation of the jugal to the orbit; (4) pres-
ence of postparietal foramen (convergently acquired in
some diplodocoids); (5) single optic foramen; (6) ante-
rior cervical vertebrae without an anterior centrodiapo-
physeal lamina; (7) cervical vertebrae with well-
developed prespinal and postspinal laminae (convergent
with Isisaurus; Wilson & Upchurch 2003); (8) scapular
acromion with a prominent posterior projection; and (9)
transverse width of astragalus twice its dorsoventral
height and anteroposterior length.
Remarks. The present emended diagnosis is fairly simi-
lar to that proposed by Carballido & Sander (2014) with
the addition of two autapomorphic characters (characters
3 and 5). Autapomorphic characters 8 and 9 were listed as
autapomorphies by Mateus et al. in Sander et al. (2006),
and are included here as well. The new materials revealed
that the nasal process of the premaxilla is not anterolater-
ally oriented (see below), whereas the presence of a notch
is a widespread character (Carballido & Sander 2014).
Therefore, these two characters are no longer considered
as autapomorphies of Europasaurus.
Description
Ontogenetic stages and morphotypes
A reliable method to determine the ontogenetic age of an
individual is to histologically sample long bones and ribs
(e.g. Klein & Sander 2008; Sander et al. 2011; Cerda
et al. 2014); size alone is not a good proxy for age (e.g.
Brochu 1996; Sander & Klein 2005; Wedel & Taylor
2013). However, this method is not applicable to the rela-
tively narrow and delicate skull bones. Like the axial ele-
ments described by Carballido & Sander (2014), the skull
elements of Europasaurus cannot be properly linked to
certain long bones (either ribs or limbs). Therefore,
Cranial anatomy of the Late Jurassic dwarf sauropod Europasaurus holgeri 3
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different ontogenetic information than that offered by his-
tology must be used. Following Carballido & Sander
(2014), size-independent characters were used for deter-
mining the different MOS of each skull bone. Bone sur-
face texture has proven to be a useful criterion to stage the
bones and determine a relative age (see Varricchio 1997;
Tumarkin-Deratzian 2009). Bones of an ontogenetically
young individual, as studied in other dinosaur groups
(Sampson et al. 1997), have rough, very porous and possi-
bly striated bone surfaces (Varricchio 1997), which is typ-
ical for a fast-growing tissue. As an individual ages, the
porosity or vascularity of the bone surface decreases;
therefore, changes in bone texture can be applied to onto-
genetic stages (Varricchio 1997; Tumarkin-Deratzian
2009). Other size-independent characters are used, but are
specific for each skull bone and will be mentioned with
the description of their respective skull element.
The MOS corresponds to the relative age class of the
individual bone element. As the degree of vascularization
is used for all the elements, this character allows standard-
ization of the MOS amongst different skull bones. Three
main MOS were defined for Europasaurus: MOS 1 repre-
sents the youngest stage, presumably of juvenile animals;
MOS 2 is used for intermediate stages; and MOS 3 is the
oldest recognized stage, which, at least for most of the ele-
ments, indicates that the animal reached adulthood. These
three MOS are applicable to all bones in this study, and
are comparable amongst all bone types. In addition,
because some skull elements could be staged into more
than three MOS, sub-stages were introduced (e.g. MOS
1.1, MOS 1.2). Not all of the three MOS are always repre-
sented in every bone type. See Online Supplementary
Material for a complete list of the skull material and its
principal measurements.
MOS 1. This is characterized by a highly vascularized
bone surface (hvbs) with small canals penetrating the
bone surface at a low angle. It is typical for individuals
still actively growing (e.g. Benton et al. 2010). A similar
surface texture is present in the actively growing pleuro-
coels of juvenile sauropods (Carballido et al. 2012; Car-
ballido & Sander 2014). Bones of very young individuals
also show well-defined striations on the bone surface.
Only material from the DFMMh/FV collection is referable
to this growth stage. A total of 25 skull bones were
assigned to MOS 1.
MOS 2. The intermediate growth stage shows a partially
vascularized bone surface combined with characters of
presumably fully grown individuals (e.g. distinctive struc-
tures for articulations with other bones). This growth stage
is represented in at least 22 skull bones.
MOS 3. This is characterized by a generally smooth bone
surface with pronounced, rugose articular facets. Further
secondary characters are bone specific and will therefore
be described individually for each bone type. This stage is
exemplified in at least 62 skull bones, presumably repre-
senting the adult growth stage of Europasaurus.
Different morphotypes. Examining the material and
recognizing different MOS have revealed that two differ-
ent morphotypes are present amongst the Europasaurus
samples, the presence of which was also recognized in the
axial skeleton (Carballido & Sander 2014) and is identi-
fied when size differences are observed amongst elements
that share the same MOS. Therefore, the two morphotypes
found within the Europasaurus material represent two
size classes. The morphotypes were distinguished as mor-
photype A (small) and morphotype B (large). In general,
morphotype B elements are 30–55% larger than those of
morphotype A. Independent of ontogenetic stage, bones
of morphotype A are more ‘gracile’, whereas those of
morphotype B are more ‘robust’ in appearance. Bones of
morphotype B, with 27 elements, are under-represented,
while material of morphotype A is represented by 65
elements.
Skull reconstruction. Based on the complete informa-
tion provided here, it was possible to reassemble bone ele-
ments, presumably of adult growth stages, graphically
into a new skull reconstruction of Europasaurus holgeri
(Fig. 1). This reconstruction attempts to account for the
different MOS as well as the two different morphotypes.
The method used for reconstructing the skull is discussed
at the end of the following description.
Skull roof bones
Of the bones of the skull roof, only the prefrontal and
scleral ossicles are missing (Fig. 1). Furthermore, several
elements cannot be compared due to the fact that they are
too fragmented. These elements are one complete maxilla
and four maxillary fragments from the DFMMh/FV collec-
tion; one maxilla from the NMB collection; one complete
nasal and two fragments from the DFMMh/FV collection;
and five lacrimal fragments, three from the DFMMh/FV
collection and two elements from the NMB collection.
Premaxilla. Eight premaxillae (Fig. 2) have been identi-
fied amongst the Europasaurus material (DFMMh/FV
032, 061, 291.18, 652.2, 831, 703.5, 890.8, 982). None is
completely preserved; nevertheless, DFMMh/FV 032
(which only lacks most of the nasal process) and
DFMMh/FV 831 (of which the ventral body of the pre-
maxilla is not preserved but all of its nasal process is pres-
ent) provide the most complete information on the
premaxillary anatomy of Europasaurus (Fig. 2A–D). The
following description is mainly based on these last two
elements, except when explicitly mentioned.
In lateral view, the premaxilla of Europasaurus has a
rectangular shape, which gives the skull a bulldog-like
4 J. S. Marpmann et al.
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muzzle shape similar to that of Camarasaurus (Madsen
et al. 1995), although the muzzle is more elongated dorso-
ventrally (Fig. 1). The nasal process of the premaxilla was
initially restored as inclined anteriorly (Sander et al.
2006), and therefore considered an autapomorphic charac-
ter of this taxon. Based on new and better-preserved pre-
maxillae, the new reconstruction presented here (Figs 1,
2) indicates that the nasal process is oriented with a more
vertical inclination, similar to that of Camarasaurus but
not as posteriorly inclined as in Euhelopus. Therefore, the
former autapomorphic character was excluded from the
diagnosis of this taxon (see Emended diagnosis above).
The ventral starting point of the nasal process is postero-
dorsally oriented whereas, at the height of the subnarial
foramen, the nasal process points in the dorsal direction
until it contacts the nasal. This orientation gives the nasal
process a step-like shape. When observed in lateral view,
the nasal process starts turning dorsally at the same height
of the fourth premaxillary and first maxillary tooth
(Fig. 2A, C). The development of the step in the premax-
illa of Europasaurus is thus similar to the condition
observed in some specimens of Camarasaurus (e.g. Mad-
sen et al. 1995, fig. 1; SMA 0002/02) and in Euhelopus
(Mateer & McIntosh 1985; PMU 233). Nevertheless, this
step is less developed in some specimens of Camarasau-
rus, such as the complete juvenile skull (CM 11338). In
contrast, the premaxilla of the brachiosaurids Giraffatitan
and Abydosaurus, as well as the premaxilla of the skull
Figure 1. Europasaurus holgeri skull reconstruction in A, left lateral; B, occipital; and C, dorsal views. Reconstruction modified from
Sander et al. (2006) on the basis of the new bones recently recovered and new observations. White bones correspond to known ele-
ments, whereas missing elements are lined. See text for a complete discussion on modified regions with respect to the previous skull
reconstruction. Abbreviations: an, angular; aof, antorbital fenestra; ar, articular; asaf, anterior surangular foramen; boc, basioccipital;
bpt, basipterygoid process; d, dentary; en, external naris; eoc, exoccipital; f, frontal; itf, infratemporal fenestra; j, jugal; l, lacrimal; m,
maxilla; n, nasal, nvf, neurovascular foramen; orb, orbit; oc, occipital condyle; os, orbitosphenoid; p, parietal; paof, preantorbital
fenestra; pf, parietal fenestra; pt, palatine; pm, premaxilla; po, postorbital; pop, paroccipital process; ppf, postparietal fenestra; prf, pre-
frontal; ppr, parasphenoid rostrum; psaf, posterior surangular foramen; pt, pterygoid; ptf, post-temporal fenestra; q, quadrate, qj, quad-
ratojugal; sa, surangular; snf, subnarial foramen; soc, supraoccipital; sq, squamosal; stf, supratemporal fenestra; v, vomer. Scale bar
represents 5 cm.
Cranial anatomy of the Late Jurassic dwarf sauropod Europasaurus holgeri 5
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referred to as Brachiosaurus sp. by Carpenter & Tidwell
(1998), have a well-developed step. In these taxa, the
inflection point of the nasal process is at the height of the
last maxillary tooth, which is positioned further posteri-
orly than in Europasaurus,Camarasaurus or Euhelopus
(MB.R. 2223.1; Chure et al. 2010; USNM 5730; PMU
233). As a consequence, the external narial fenestra in the
aforementioned brachiosaurids is retracted and its poste-
rior edge exceeds the last maxillary tooth. In
Europasaurus, the external narial fenestra was recon-
structed as larger than the antorbital fenestra, being almost
as large as the orbit. This character is also present in other
basal camarasauromorphs (Camarasaurus,Giraffatitan,
Abydosaurus,Malawisaurus; Janensch 1935–1936; Mad-
sen et al. 1995; Gomani 2005; Chure et al. 2010) and dif-
fers from the reduced and extremely retracted external
narial fenestra of titanosaurs (Rapetosaurus,Nemegtosau-
rus,Tapuiasaurus; Curry Rogers & Forster 2004; Wilson
Figure 2. Europasaurus holgeri premaxillae. A, C, DFMMh/FV 032 (right) in A, lateral and C, medial views. B, D, DFMMh/FV 831
(right) in B, lateral and D, medial views. E–H, lateral views of the elements; E, DFMMh/FV 982 (reversed left); F, DFMMh/FV
291.18; G, DFMMh/FV 831 (reversed left); H, DFMMh/FV 061 (reversed left). Abbreviations: 4th t, fourth premaxillary tooth; dmp,
dorsomedial process; en, external naris; naa, nasal articulation; nf, nutrient foramen; nvf, neurovascular foramen; snf, subnarial foramen;
vmp, ventromedial process. Scale bars represent 2 cm.
6 J. S. Marpmann et al.
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2005; Zaher et al. 2011). A small but well-developed fora-
men is present in all premaxillae of Europasaurus. This
foramen lies below the ventromedial process of the pre-
maxilla, next to the subnarial foramen. We interpret it as a
neurovascular foramen, which is well developed in Euro-
pasaurus (Fig. 2A).
In medial view, four large alveoli can be observed with
their nutrition foramina preserved beneath them. The
interdental plate union forms the nutrition foramina.
Through the nutrition foramina a second generation of
replacement teeth can be observed in the second and
fourth alveolus of specimen DFMMh/FV 032. The teeth
of Europasaurus are D-shaped and spatulate, although to
a lesser extent than those of Camarasaurus and more
basal sauropods. The general morphology seems to be an
intermediate between the teeth of Camarasaurus and that
observed amongst titanosauriforms. The mesial sides of
the teeth show small denticles. A complete and detailed
description of the teeth lies outside the scope of this publi-
cation and is being prepared by V. R
egent and P. M.
Sander (R
egent 2011). The premaxilla symphysis is not as
broad as in Camarasaurus and is rather dorsoventrally
long and anteroposteriorly narrow. The articular facet of
the premaxilla for the maxilla is wider dorsally than ven-
trally and becomes thinner ventrally (Fig. 2A–D). In
medial view a concave articular facet is developed
between the ventromedial and dorsomedial processes of
the premaxilla. This facet serves as an articular facet for
the premaxillary process of the maxilla, which is not pre-
served in any of the recovered maxillae.
Ontogenetic changes. The MOS are identified by several
size-independent characters: bone surface structure, the
increasingly erect nasal process and anterior snout region,
and the tendency for the muzzle to become relatively
wider during ontogeny (the last character is also used for
other sauropods; Whitlock et al. 2010). Relative muzzle
width is measured as the anteroposterior length of the pre-
maxillary body divided by its lateromedial width (mea-
sured at the premaxillary–maxillary suture); note that in
this ratio lower values indicate greater relative width. The
anteroposterior length of the vertical part of the nasal pro-
cess decreases in relation to the premaxillary body (Britt
& Naylor 1994). Except for specimen DFMMh/FV 831,
all premaxillae lack most of the dorsal part of the nasal
process. The three recognized MOS are present in the pre-
served premaxillae.
DFMMh/FV 982 represents MOS 1 (Fig. 2E). The tiny
and incomplete bone shows an hvbs structure. The pre-
maxillary body inclines at a shallow angle before it bends
dorsally towards the nasal process. The muzzle region is
relatively short and, notably, is relatively slender. The
proximal end of the nasal process is relatively long com-
pared to the premaxillary body. This premaxilla is pre-
sumed to be a juvenile of morphotype A.
DFMMh/FV 291.18 represents the MOS 2 (Fig. 2F).
The second oldest premaxilla is much larger than the
aforementioned specimen. The lateral side is striated,
while the medial side still shows an hvbs structure. As in
DFMMh/FV 982, the muzzle region is relatively short
and lateromedially slender. The nasal process is slightly
elongated posterodorsally, and its ventral region is rela-
tively long, compared to the preserved premaxillary body.
This premaxilla is assigned to morphotype A.
DFMMh/FV 061 represents an intermediate MOS (2–3)
(Fig. 2H). This premaxilla has a remarkable overall
resemblance to the premaxilla of an embryonic specimen
of Camarasaurus sp. (Britt & Naylor 1994, figs 16.1–
16.2; BYUVP 8967), but is also highly reminiscent of the
premaxillae of Tornieria africana (Remes 2009,fig.2;
MB.R. 2343 and MB.R. 2346). CT scanning revealed that
the premaxilla DFMMh/FV 061 bears the distinct Europa-
saurus premature replacement teeth, and not the more
cylindrical teeth of diplodocids. The bone surface is
mostly fully developed with little vascularization laterally
and medially to the nasal process. Its premaxillary body is
much more robust than that of the other elements. Based
on the MOS of this element and the significantly different
shape, DFMMh/FV 061 is considered a premaxilla of
morphotype B.
Five elements, which show some variation, are pre-
served of MOS 3. DFMMh/FV 831 (MOS 3.1; Fig. 2B,
D) has the most completely preserved nasal process, but
most of its premaxillary body is missing. Bone surface
texture is smooth. The erectness of the nasal process
extends more posteriorly. The proximal end of the nasal
process is anteroposteriorly short relative to the premaxil-
lary body. DFMMh/FV 831 represents a presumed adult
stage of morphotype A. DFMMh/FV 032 (MOS 3.2;
Fig. 2A, C) has the most complete premaxilla body, with
a decreasing anteroposterior length of the nasal process to
the premaxillary body. Its bone surface structure looks
fully developed, lacking any vascularization. The nasal
process becomes steeper, and the muzzle becomes rela-
tively wider compared to the younger elements of mor-
photype A, with which this element is associated. Three
specimens represent MOS 3.3. DFMMh/FV 652.2 is the
largest of these, with parts of the nasal process preserved
as well as its premaxilla body. The nasal process is antero-
posteriorly short compared to the premaxilla body, which
is the widest amongst all elements. Bone surface structure
is overall very smooth and the nasal process shifts even
more posterodorsally. It represents the largest known pre-
maxilla of morphotype A. DFMMh/FV 703.5 is repre-
sented only by the vertical rim of the nasal process and is
still embedded in the rock matrix. The curvature of the
nasal process is almost identical to that of DFMMh/FV
652.2 and shows a smooth bone surface structure. There-
fore, DFMMh/FV 703.5 might be of the same ontogenetic
stage of morphotype A. Element DFMMh/FV 890.8 is a
Cranial anatomy of the Late Jurassic dwarf sauropod Europasaurus holgeri 7
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fragment of the anterolateral margin of the premaxilla
body. The bone surface is comparable to that of DFMMh/
FV 652.2 and might be of morphotype A as well.
Maxilla. Six maxillae were discovered amongst the
Europasaurus material (Fig. 3). DFMMh/FV 291.17 is
the best preserved, corresponding to the holotype material
(Fig. 3). Therefore, the maxilla description is mainly
based on this specimen. A small anterodorsal part is miss-
ing, which articulates with the premaxilla and builds the
posterior rim of the subnarial foramen. The maxilla has a
large body with two main processes, the nasal process and
a dichotomous posterior process, formed by the lacrimal
process in dorsal direction and the jugal process in the
posterior direction (Fig. 3B). The maxilla of Europasau-
rus, like most sauropods, has a short and weakly devel-
oped lacrimal process, except Rapetosaurus (Curry
Rogers & Forster 2004). The nasal process is long and
well developed. The posterior edge of the nasal process,
up to the beginning of the lacrimal articulation (Fig. 3),
surrounds the anteroventral part of the antorbital fenestra
(Fig. 1). The posterodorsally oriented nasal process forms
an angle of 120with the tooth row. The lacrimal process
is well developed and is pointed dorsally, strongly resem-
bling the lacrimal process development of Euhelopus
(PMU 233; Mateer &McIntosh 1985, fig. 5). In some
specimens of Camarasaurus and Abydosaurus the lacri-
mal process is expanded dorsally and is not as pointed as
is in Europasaurus and Euhelopus (Madsen et al. 1995,
fig. 9; Chure et al. 2010, fig. 3). In contrast, the subadult
specimens of Camarasaurus (CM 11338) and Giraffatitan
(Janensch 1935–1936, fig. 42; MB.R.2233.1) have a lacri-
mal process that is neither pointed nor expanded. In Euro-
pasaurus the lacrimal and nasal processes are close to
each other, resulting in an anteroposteriorly short tear-
shaped antorbital fenestra (Figs 1, 3). This fenestra is
approximately three times as high as it is wide. Those of
Camarasaurus,Giraffatitan,Abydosaurus and Euhelopus
are about twice as high as they are wide. The antorbital
fenestra is positioned anteriorly to the last maxillary tooth,
as is common for basal sauropods (Patagosaurus,Joba-
ria; MACN 934; MNNTIG 5) and some camarasauro-
morphs like Camarasaurus (Madsen et al. 1995;CM
11338; SMA 0002/02) and Euhelopus (PMU 233). The
brachiosaurids Giraffatitan,Abydosaurus and Brachio-
saurus sp. have a posteriorly retracted antorbital fenestra.
In these taxa, the posterior edge of the antorbital fenestra
is positioned posteriorly to the last maxillary tooth (MB.
R.2223.1; Chure et al. 2010; USNM 5730). In derived
titanosaurs the antorbital fenestra is positioned even fur-
ther posteriorly from the last maxillary teeth (e.g. Rapeto-
saurus,Tapuiasaurus; Curry Rogers & Forster 2004;
Zaher et al. 2011). In Europasaurus a small and laterome-
dial flat opening can be seen below the antorbital fenestra,
which is interpreted as the preantorbital fenestra, a syna-
pomorphic character of Neosauropoda (Wilson & Sereno
1998). The preantorbital fenestra is completely opened in
derived titanosaurs and diplodocoids (e.g. Diplodocus,
Tapuiasaurus), while in Europasaurus (Fig. 3A), as well
as Camarasaurus and Euhelopus, the preantorbital fenes-
tra is located beneath the antorbital fenestra; in
Figure 3. Europasaurus holgeri right maxilla (DFMMh/FV 291.17) in A, lateral and B, medial views. Abbreviations: 1st t, first tooth;
12th? t, twelfth tooth; aof, antorbital fenestra; ec, ectopterygoid articulation; en, external naris; et, erupted tooth (eighth?); ja, jugal artic-
ulation; la, lacrimal articulation; na, nasal articulation; paof, preantorbital fenestra; sy, symphysys. Scale bar represents 1 cm.
8 J. S. Marpmann et al.
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Giraffatitan and Abydosaurus the preantorbital fenestra is
more anteriorly positioned with respect to the antorbital
fenestra, but in a similar position with respect to the tooth
row.
In medial view, the tooth row is poorly preserved, so
the number of maxillary teeth present in Europasaurus is
difficult to ascertain (Fig. 3B). Based on visible teeth and
the alveolus, and the distance between them, the estimated
number of teeth for the maxilla is 12–13. Basal sauropods
usually have more than 12 teeth (16 in Jobaria: Sereno
et al. 1999; 14–15 in Atlasaurus: Monbaron et al. 1999).
Some macronarians, such as Camarasaurus and Euhelo-
pus, have between nine and 10 maxillary teeth (Madsen
et al. 1995; Wilson & Upchurch 2009). Brachiosaurids
have a variable number of teeth (12 in Giraffatitan:
Janensch 1935–1936; 14–15 in Brachiosaurus sp.: Car-
penter & Tidwell 1998;10in Abydosaurus: Chure et al.
2010). The tooth row of Europasaurus takes up more than
70% of the total length of the maxillary body. Only
replacement teeth can be observed in the element
DFMMh/FV 291.17, visible through the nutrition foram-
ina and broken surfaces. All show three or four small den-
ticles on their mesial sides. While the anterior (non-
erupted) teeth seem to be aligned vertically with respect
to the tooth row, the single erupted tooth is slightly poste-
riorly inclined. The crown shape of this tooth is slightly
posteriorly twisted (around 15), much less than Abydo-
saurus or Giraffatitan (30–45; D’Emic 2012; Mannion
et al. 2013). In fact, most of the preserved teeth of Euro-
pasaurus have straight crowns, and only a few having
marginally twisted crowns (R
egent 2011).
Ontogenetic changes. Of the six preserved maxillae, the
large specimen DFMMh/FV 291.17 is nearly complete,
and is classified as MOS 3 due to its smooth bone surface
structure and well-developed processes and articular fac-
ets. The element is attributed to morphotype A. The MOS
and the morphotype are the same for the incomplete max-
illa NMB-2207-R. Although the position of these maxil-
lary bone fragments (DFMMh/FV 077, DFMMh/FV 218,
DFMMh/FV 911 and DFMMh/FV 1046) can be deter-
mined, they cannot be staged or assigned to any
morphotype.
Nasal. Three nasals are preserved amongst the Europa-
saurus material (Fig. 4). One almost complete and unde-
formed left nasal was recently discovered (DFMMh/FV
1150.1; Fig. 4), and is the basis for most of the descrip-
tion. Two nasal fragments were identified as the posterior
part of a right nasal (DFMMh/FV 1037.13), and as the
anterior section of another right nasal (DFMMh/FV
867.4).
Posteriorly the nasal becomes overlapped by the fron-
tal, both bones being extremely narrow in this section.
Neither of the nasals is complete in this section, although
a small facet for the articulation with the frontal and the
prefrontal is observed in DFMMh/FV 1150.1 (Fig. 4A).
The nasal–frontal articulation is mediolaterally narrow,
evident in both the frontal and the nasal (Fig. 4; see
below). The dorsolateral edge of the nasal has a rough sur-
face, which is interpreted as the contact of the nasal with
the prefrontal. The ventrolateral process, which articulates
with the lacrimal and the nasal process of the maxilla (e.g.
Camarasaurus; Madsen et al. 1995;Figs 1, 4), is almost
completely intact. The nasal–lacrimal articulation is dis-
cernible in lateral view and covers most of the posterior
edge of the ventrolateral process (Fig. 4A, B), whereas the
articulation for the nasal process of the maxilla is slightly
preserved on the ventral edge of the ventrolateral process
of the nasal (Fig. 4B). If the lateroventral process is
almost vertically oriented, as in Figures 1 and 4 and fol-
lows the orientation of this process in other sauropods
(e.g. Camarasaurus,Giraffatitan; Janensch 1935–1936,
supplement 7; Madsen et al. 1995, figs 1, 5), the premaxil-
lary process of the nasal is horizontally directed before
turning ventrally. In contrast, in Giraffatitan the nasal is
dorsally directed. The morphology of the newly recovered
nasal is clearly different from that previously recon-
structed by Sander et al. (2006, fig. 1b), which seems to
follow the nasal morphology of Giraffatitan.
Ontogenetic changes. The three preserved nasals proba-
bly belong to fully grown individuals, as indicated by their
smooth bone surface structure, and they are accordingly
staged as MOS 3. The nasals fit perfectly into the above-
mentioned premaxillary process and the frontal of
Figure 4. Europasaurus holgeri right nasal (DFMMh/FV
1150.1) in A, lateral and B, dorsal views. Abbreviations: fa, fron-
tal articulation; la, lacrimal articulation; ma, maxilla articulation;
pfa, prefrontal articulation. Scale bar represents 1 cm.
Cranial anatomy of the Late Jurassic dwarf sauropod Europasaurus holgeri 9
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DFMMh/FV 552, which further underlines the assumption
that they belong to fully grown individuals, and possibly
the same morphotype (A). Further comparisons and onto-
genetic inferences are not possible.
Jugal. Three jugals are preserved amongst the Europa-
saurus material (Fig. 5): two are almost complete
(DFMMh/FV 292 and 100.4) and the third is preserved as
the basal part of the postorbital process (DFMMh/FV
908). The following description is mainly based on ele-
ment DFMMh/FV 100.4, a nearly complete specimen that
only lacks a small anterior part of the maxillary process
and the tip of the quadatojugal process (Fig. 5A, B).
The jugal, which is greatly reduced in camarasauro-
morphs, is a long and well-developed bone in Europasau-
rus. Comparing this element to other related sauropods
(e.g. Camarasaurus,Giraffatitan and Abydosaurus) is dif-
ficult because the jugal of Europasaurus is more
reminiscent of those of basal sauropodomorphs. The jugal
of Europasaurus contributes to the infratemporal fenestra,
the orbit and the ventral margin of the skull, but does not
contribute to the antorbital fenestra.
The posteroventral or quadratojugal process of the jugal
is extremely fragile and narrow, showing an articular scar
along its ventromedial side, which extends from the poste-
rior acute tip to almost the mid-length of the maxillar pro-
cess, just below the anteroventral side of the posterodorsal
or postorbital process. The quadratojugal process and the
postorbital process diverge from each other at an angle of
75, forming the anteroventral margin of the infratempo-
ral fenestra (Figs 1, 5A, B).
The postorbital process articulates with the postorbital
through an anteriorly long surface, which extends along
the third dorsal edge of the postorbital process of the
jugal. The centre between the dorsal part of the postorbital
process and the posterodorsal edge of the maxillary
Figure 5. Europasaurus holgeri jugals. A, B, DFMMh/FV 100.4 (left) in A, lateral and B, medial views. C, D, DFMMh/FV 292
(reversed right) in C, lateral and D, medial views. E, DFMMh/FV 908 (reversed right) in lateral view. F, reconstruction of the different
MOS detected amongst preserved jugals in lateral view; white line indicates free ventral margin of the element. Abbreviations: itf, infra-
temporal fenestra; la, lacrimal articulation; ma, maxilla articulation; orb, orbit; poa, postorbital articulation; pop, postorbital process;
qjp, quadratojugal process. Scale bar represents 1 cm.
10 J. S. Marpmann et al.
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process forms a rounded concavity, which contributes to
the ventral margin of the orbit. In this respect the jugal of
Europasaurus is also more similar to those of basal sauro-
podomorphs (e.g. Riojasaurus,Massospondylus; Gow
et al. 1990; Bonaparte & Pumares 1995), compared to the
jugals with reduced ventral participation in the orbit of
most sauropods (e.g. Camarasaurus,Giraffatitan;
Janensch 1935–1936; Madsen et al. 1995). Similarly, a
large participation of the jugal to the orbit was recently
described for titanosaur embryos (Salgado et al. 2005;
Garc
ıa et al. 2010), but has not been observed in any adult
titanosaur described so far (e.g. Rapetosaurus,Nemgto-
saurus,Tapuiasaurus; Nowinski 1971; Curry Rogers &
Forster 2004; Zaher et al. 2011).
The well-developed maxillary process of the jugal con-
tacts both the maxilla and the lacrimal. The anterolateral
side of the maxillary process of the jugal contacts the
medial side of the maxilla. Therefore, about half of the
maxillary process of the jugal is covered by the maxilla
(Fig. 5A). The medial side of the maxillary process of the
jugal shows a small sigmoidal scar. The indented lateral
side of the maxillary process of the jugal fits perfectly in
the medial side of the jugal process of the maxilla, result-
ing in a stiffer articulation between the elements.
The jugal–quadratojugal articulation occurs solely on
the ventral margin of the jugal (Fig. 5B), and not on its
posterior margin (as is seen in Camarasaurus). Therefore,
Europasaurus has the derived state that is characteristic
of macronarians more derived than Camarasaurus (Curry
Rogers 2005; Mannion et al. 2013). The jugal–quadratoju-
gal and jugal–maxilla articulations leave a wide gap in the
centre of the jugal bone. Thus, the jugal contributes to the
ventral rim of the skull (Figs 1, 5A, B). In the adult, the
length of this free ventral margin is at least a quarter of its
total anteroposterior length. A large participation of the
jugal to the ventral margin of the skull is a widespread
character amongst sauropods more basal than Shunosau-
rus (Chatterjee & Zheng 2002; e.g. Plateosaurus,Masso-
spondylus,Mussaurus,Melanorosaurus; Galton 1984,
1985; Sues et al. 2004; Pol & Powell 2007; Yates 2007).
In more derived forms jugal participation to the ventral
margin of the skull is precluded by the direct maxilla–
quadratojugal contact (e.g. Mamenchisaurus,Turiasau-
rus,Camarasaurus,Nemegtosaurus; Nowinski 1971;
Madsen et al. 1995; Ouyang & Ye 2002; Royo Torres &
Upchurch 2012), or is extremely reduced as in Giraffati-
tan (Janensch 1935–1936). Amongst camarasauromorphs
a reduced participation of the jugal has been described
only for Giraffatitan and reconstructed for Malawisaurus
(Gomani 2005; Royo Torres & Upchurch 2012) and Aby-
dosaurus (Chure et al. 2010, fig. 3B). Of these taxa only
Giraffatitan has an undoubted minor participation of the
jugal to the ventral margin of the skull (MB.R. 2223.1).
For Malawisaurus, Gomani (2005, fig. 31) published only
a general reconstruction, and this character was not
specified. In Abydosaurus, this participation could be the
result of breakage, as it is observed in the right lateral
view, but absent in left lateral view (Chure et al. 2010,
fig. 3). If present the contribution of the jugal to the ven-
tral margin of the skull in Abydosaurus is as reduced as in
Giraffatitan. Therefore, the large participation of the jugal
to the ventral rim of the skull is here interpreted as an
autapomorphic character of Europasaurus, resulting in a
reversion to the plesiomorphic character of basal
sauropodomorphs.
As in Camarasaurus (Madsen et al. 1995) and most
camarasauromorphs, the jugal does not contribute to the
antorbital fenestra in Europasaurus (Figs 1, 5A, B), differ-
ing from the large participation of the jugal in the antorbi-
tal fenestra of diplodocoid sauropods (e.g. Diplodocus;
CM 11255; Upchurch 1998; Whitlock 2011) and the tita-
nosaur Tapuiasaurus (Zaher et al. 2011). A reduced par-
ticipation of the jugal to the antorbital fenestra was
described for some titanosauriforms such as Giraffatitan
(Janensch 1935–1936),Abydosaurus (Chure et al. 2010)
and Rapetosaurus (Curry Rogers & Forster 2004). In
Europasaurus the jugal is completely excluded from the
antorbital fenestra, as in Nemegtosaurus (Nowinski 1971)
and Camarasaurus (Madsen et al. 1995).
Ontogenetic changes. Two elements are of MOS 1
(DFMMh/FV 292 and 908) and one element is of MOS 3
(DFMMh/FV 100.4). No intermediate MOS have been
identified yet amongst the preserved jugals of Europasau-
rus. Size-independent characters are the structure of the
bone surface, the articular facets on the processes, the
length and ratio of the free space of the ventral margin of
the jugal that contributes to the ventral rim of the skull,
the shape of the curvature between postorbital and quadra-
tojugal process, and the angle of the curvature of the dor-
sal margin that forms the ventral margin of the orbit.
The bone surface structure of DFMMh/FV 292
(Fig. 5C, D), which is only a few centimetres long, is
highly vascularized with striations showing small grooves
and canals penetrating the bone surface at a low angle,
and is therefore staged as MOS 1. The articular facets of
the maxillary, the postorbital as well as the quadratojugal
process are not yet well developed. The postorbital pro-
cess has a small and smooth edge on its lateral side. The
free ventral margin has a length of 11.3 mm and contrib-
utes 33% to the total length of the jugal. The curvature
between the postorbital and the quadratojugal processes is
J-shaped and the angle of the dorsal margin shows an
inclination of 20. DFMMh/FV 292 is associated with
morphotype A.
DFMMh/FV 908 (Fig. 5E) has the same bone surface
structure as DFMMh/FV 292, including a pronounced
edge on the lateral side of the postorbital process. Even
though the postorbital process is about 55% larger in
DFMMh/FV 908 than in DFMMh/FV 292, both have
Cranial anatomy of the Late Jurassic dwarf sauropod Europasaurus holgeri 11
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typical bone surface structures of juveniles (Fig. 5). Given
the similar size of the basal postorbital process of the jugal
of DFMMh/FV 292 and DFMMh/FV 100.4 (described
below), the surface structure of this jugal is considered to
be a bone of the larger morphotype B.
DFMMh/FV 100.4 is assigned to MOS 3 (Fig. 5A, B).
Bone surface structure is rather plain on the lateral side
and rugose on the articular facets of all processes, espe-
cially the maxillary and postorbital ones. This jugal shows
a small ridge for the articulation with the lacrimal along
the anterodorsal margin. The free ventral margin is
18.8 mm long and contributes 25% to the total length of
the jugal (Fig. 5A, B); therefore, it contributes proportion-
ally less than the jugal staged as MOS 1. The curvature
between the postorbital and the quadratojugal processes is
more L-shaped, and the angle of the dorsal margin shows
an inclination of about 40. This bone seems to be an adult
specimen of morphotype A.
Lacrimal. There can be no detailed description of the
lacrimal because only fragments have been found, in both
the DFMMh/FV and NMB collections. The correct posi-
tion within the skull is only known for specimen
DFMMh/FV 994 and the two elements of NMB-2207-R.
The correct position of the other specimens (DFMMh/FV
521, DFMMh/FV 858.2) remains unknown.
Ontogenetic changes. Judging by the bone surfaces of
DFMMh/FV 994, DFMMh/FV 521 and DFMMh/FV
858.2, they seem to belong to fully grown animals and are
attributed to MOS 3. However, due to their fragmentary
nature, the association of DFMMh/FV 521 and DFMMh/
FV 858.2 is highly uncertain. The lacrimal elements asso-
ciated with other bones in the NMB-2207-R specimen are
of morphotype A, but the morphotype for the DFMMh/
FV lacrimals cannot be determined with certainty.
Frontal. The frontal of Europasaurus (Fig. 6) is known
from four individuals (DFMMh/FV 162, 552, 389 and
907, all being left except for 552 which corresponds to a
right frontal). Whereas in Camarasaurus the paired fron-
tals and parietals are rarely found disarticulated (Madsen
et al. 1995), this is not true for Europasaurus in which all
the frontals were found disarticulated and were probably
never tightly sutured or fused with any other skull bone
(see Discussion). As can be inferred from the visible artic-
ulation surfaces of the frontals, and by comparison to
other sauropods (e.g. Giraffatitan,Camarasaurus; MB.
R.2223.1; CM 11338), the frontal contacts the parietal
posteriorly and posterolaterally, the postorbital posterolat-
erally, the prefrontal anterolaterally, the nasal anterome-
dially, and the laterosphenoid and orbitosphenoid
ventrally (Figs 1, 6A, B). The smooth interdigitating fron-
tal–frontal suture is transversely long. This suture deter-
mines the longest axis of the frontal. The frontal is
anteroposteriorly longer than it is lateromedially wide.
This is an unusual character for a eusauropod dinosaur
(Wilson 2002) and is therefore interpreted as an additional
autapomorphic character. Similar proportions were
recently described for a titanosaur embryo (Garc
ıa et al.
2010).
The frontal–frontal contact is completely preserved in
two of the frontals (DFMMh/FV 162, 552; Fig. 6), and
both have an edge that is completely straight, without any
sign of fenestration, even in their posterior ends. Thus the
planar frontal–frontal articulation differs from the inter-
digitated shape of Giraffatitan or Camarasaurus. Addi-
tionally, the frontals are excluded from the so-called
frontoparietal fenestra (also the pineal fenestra; Madsen
et al. 1995), which in Europasaurus is only surrounded by
the parietals and here referred to as the parietal fenestra.
The presence of a similar fenestra was reported for
the dicraeosaurids Amargasaurus and Dicraeosaurus
(Salgado & Calvo 1992;Paulina Carabajal et al. in press),
the diplodocid Apatosaurus (Balanoff et al. 2010), some
specimens of Camarasaurus (Madsen et al. 1995), and
recently for titanosaur embryos (Salgado et al. 2005;
Garc
ıa et al. 2010). The posterior surface of the frontal,
which mainly articulates with the parietal, forms an angle
of about 100with the frontal–frontal suture axis. Addi-
tionally, the frontal also articulates with the parietal
throughout half of its posterolateral edge, whereas the dis-
tal half of this surface articulates with the frontal process
of the postorbital (not preserved), as is also observed in
other sauropods (e.g. Camarasaurus,Giraffatitan;CM
11338; MB.R.2223.1). Therefore, the posterior edge of
the frontal does not form the anterior margin of the supra-
temporal fenestra because the parietal and postorbital pre-
cludes its participation, a widespread character amongst
sauropods more derived than Shunosaurus (e.g. Wilson
2002), with a reversion probably in Turiasaurus (Royo
Torres & Upchurch 2012).
The orbital margin is not very long and does not bear
any sign of ornamentation. While some camarasauro-
morphs (e.g. Camarasaurus,Nemegtosaurus; Madsen
et al. 1995; Wilson 2005) show an ornamented margin,
Europasaurus is more similar to the completely smooth
frontal of Giraffatitan (MB.R.2223.1). The orbital rim
deeply penetrates the frontal. This concavity is well visi-
ble in dorsal or ventral view (Fig. 6). The deep penetration
of the orbital rim into the skull roof results in very reduced
contacts for the prefrontal and the nasal. The general con-
dition in sauropods is that the anterior edge of the frontal
contacts the nasal and the prefrontal, forming an anterior
articulation surface that is almost equally wide as the wid-
est section of this bone. In contrast, in the frontals of
Europasaurus, the articulation surface for the nasal and
prefrontal is about half the width of the widest area of the
bone (Fig. 6). The prefrontal (not preserved) was firmly
interdigitated by a deep articular facet with the frontal.
Although the frontal–prefrontal articulation is extremely
12 J. S. Marpmann et al.
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reduced in Europasaurus, and thus has previously been
regarded as an autapomorphic character of this taxon
(Sander et al. 2006), the frontal–nasal articulation is also
very reduced. This reduction is the result of the deep
indentation of the rim of the orbit into the frontal. The
combination of a long and narrow frontal with a deep
orbital rim and narrow articulation surface for the prefron-
tal and nasal is considered here to be an autapomorphic
character of Europasaurus.
In ventral view three separated concavities can be dis-
tinguished: the orbital, nasal and cranial cavities
(Fig. 6B). The orbital cavity is separated from the nasal
cavity by a well-developed ridge that extends posteriorly
from the deep insertion of the prefrontal to the anterior
end of the rugose articular surface for the laterosphenoid–
orbitosphenoid. This crest diverges from the frontal–fron-
tal axis articulation in an angle that varies between 20(in
DFFMh/FV 552) and almost 45(in DFFMh/FV162). The
articulation between the frontal and the laterosphenoid–
orbitosphenoid precludes any connection between the cra-
nial cavity and the orbital cavity. The cranial cavity is
connected with the nasal cavity by a small gap, which is
slightly convex ventrally. This gap leads to a dorsal cavity
that gives way for the olfactory bulb, which is separated
from the brain cavity. Besides their position, these cavities
also differ from each other in their size, the orbital cavity
being the largest as in other sauropods (e.g. Nigersaurus,
Camarasaurus,Giraffatitan,Phuwiangosaurus,Rapeto-
saurus; Janensch 1935–1936; Madsen et al. 1995; Curry
Rogers & Forster 2004; Sereno et al. 2007; Suteethorn
et al. 2009). In Europasaurus the cranial cavity is small
and shallow, while the orbital cavity is about twice the
size. Whereas the large size of the orbital cavity seems to
be a widespread character amongst sauropods, the sizes of
the brain cavity and nasal cavity in the frontal show some
variation amongst taxa. The frontal of Europasaurus,with
a small brain cavity and middle-sized nasal cavity, resem-
bles other non-titanosaur camarasauromorphs such as
Camarasaurus and Phuwiangosaurus (Madsen et al.
1995; Suteethorn et al. 2009). However, as the cranial
cavity forms, the frontals of titanosaurs seem to have an
extensive participation that covers more than half of the
anteroposterior region of the frontal (e.g. Rapetosaurus,
Bonitasaura; Curry Rogers & Forster 2004; Gallina &
Apestegu
ıa 2011). In titanosaurs the nasal cavity is
reduced and confined to the anteriormost part of the fron-
tal (e.g. Rapetosaurus; Curry Rogers & Forster 2004),
whereas in diplodocoids (e.g. Nigersaurus; Sereno et al.
2007) the nasal cavity seems to be equally as large as the
cranial cavity. Thus, the relative size of these cavities in
Europasaurus, as well as other basal camarasauromorphs
(e.g. Camarasaurus,Giraffatitan,Phuwiangosaurus), is
provisionally regarded as a plesiomorphic character for
basal camarasauromorphs, since the same shape is
observed in non-neosauropod sauropods (e.g. Spinophoro-
saurus; Knoll et al. 2012; GCP-CV-4229).
Ontogenetic changes. Of the four frontals preserved,
three are MOS 1 and one is MOS 3, and no intermediate
stage could be determined. Size-independent characters
used are: the structure of the bone surface; the sharpness
of the orbitonasal ridge separating the posterior part of the
orbital cavity, nasal cavity and braincase region on the
ventral side; and the bending depth of the curvature of the
posterior part of the orbital cavity on the ventral side. The
morphotypes are differentiated by the difference in the
angle in which the orbital rim opens laterally. The angle is
measured from the medial suture to the central point of
the orbital rim (Fig. 6). Importantly, both morphotypes
are distinguished from all other sauropods in which the
orbital rim does not open as much anterolaterally (an auta-
pomorphic character of Europasaurus).
Figure 6. Europasaurus holgeri frontals. A, B, DFMMh/FV 552
(right) in A, dorsal and B, ventral views. C, D, dorsal views of
the elements; C, DFMMh/FV 162 (left); D, DFMMh/FV 389
(right). Abbreviations: brc, brain cavity; f-f a, frontal–frontal
articulation surface; na, nasal articulation; nac, narial cavity;
orb, orbit; orbc, orbital cavity; pa, parietal articulation; poa, post-
orbital articulation; prfa, prefrontal surface articulation. Scale
bar represents 1 cm.
Cranial anatomy of the Late Jurassic dwarf sauropod Europasaurus holgeri 13
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Currently two stages are recognized amongst the ele-
ments assigned to MOS 1. DFMMh/FV 907 (MOS 1.1)
preserves the anterior region between the medial suture
and the medial process for the prefrontal. Ontogenetically,
this element is the youngest Europasaurus frontal to have
been found. The dorsal and the ventral bone surface show
an hvbs structure. The orbitonasal ridge is not very promi-
nent but rather rounded, and shows a relatively flat bulge.
The curvature of the orbital cavity appears very shallow.
Determining the morphotype is not as obvious as with the
other three elements because of its fragmentary state.
Given its small size in combination with the described
size-independent characters, this fragmentary frontal
probably belongs to morphotype B (see DFMMh/FV 162).
MOS 1.2 is represented by two elements (DFMMh/FV
162 and 389). DFMMh/FV 162 is an almost complete
frontal (Fig. 6C); the dorsal side consists mainly of an
hvbs structure with several striations. The orbitonasal
ridge is sharper and more developed than in DFMMh/FV
907 and is very similar to DFMMh/FV 389. The posterior
part of the orbital cavity is deeper than in DFMMh/FV
907, but still quite shallow. Despite the autapomorphic
characters of Europasaurus being present, some aspects
of the morphology of the frontal are different. In
DFMMh/FV 389 and DFMMh/FV 552 the orbital rim
opens at 45anterolaterally, measured between the mar-
gin of the medial suture and the middle of the lateral
orbital opening, whereas the orbital rim opens slightly
more laterally in DFMMh/FV 162; the contact with the
nasal is more lateromedially extended; and the articular
facet for the anterolateral process of the parietal opens at
25anterolaterally, measured from the posterior margin,
and is inclined at a shallow angle posteroventrally. The
most lateral point extends further laterally than in
DFMMh/FV 389, leading to a larger posterior section of
the orbital cavity. No hook-shaped structure is visible on
the posterolateral margin. The angle at which the orbital
rim opens laterally, the articular facet for the parietal, and
the missing hook-shaped structure are characteristics that
differ exceedingly from DFMMh/FV 389 and DFMMh/
FV 552. Therefore, this frontal is not assigned to morpho-
type A but to morphotype B. DFMMh/FV 389 only lacks
the lateral process for the prefrontal and was reconstructed
on the posteromedial margin (Fig. 6D). The bone surface
structure, the sharpness of the ridge, and the depth of the
posterior part of the orbital cavity are very similar to
DFMMh/FV 162. The size-independent characteristics
lead to the assumption that DFMMh/FV 389 and
DFMMh/FV 162 are of a similar age but of different size
(Fig. 6C, D). Their morphology is very different from
each other; however, the orbital rim opens at 45in the
anterolateral direction, and therefore more anterior than in
DFMMh/FV 162. Furthermore, the contact for the nasal is
short, and the articular facet for the anterolateral process
of the parietal opens at 35anterolaterally, and is inclined
at a steep angle posteroventrally. The most lateral point
does not extend as far laterally as in DFMMh/FV 162,
leading to a smaller posterior part of the orbital cavity. A
hook-shaped structure is visible on the posterolateral mar-
gin that would fit the depression of the anteromedial pro-
cess of a parietal. The morphotype for this frontal is A.
DFMMh/FV 552 represents MOS 3 (Fig. 5A, B). Bone
surface structure shows almost no striation and no visible
vascularization, and has an overall smooth appearance.
The ventral ridge is very sharp and strongly pronounced,
and the depression of the posterior part of the orbital cav-
ity is very deep, as is expected in an adult individual.
Except for its similar large size to DFMMh/FV 162, mor-
phology is the same as in DFMMh/FV 389 with the same
angles and morphological characteristics that define mor-
photype A.
Parietal. Five isolated parietals identified as Europasau-
rus have been found (Fig. 7), including a left and right
parietal (DFMMh/FV 581.2 and 581.3) that undoubtedly
belong to the most complete braincase DFMMh/FV
581.1, representing a single specimen. These two parietals
are nearly complete, except for a small medial portion
that would prevent their middle sections from contacting
each other. The following description is mainly based on
these two osteologically mature parietals (see below),
because they are not only the most complete elements but
also articulate with the complete preserved braincase as
mentioned above.
In dorsal view the parietals are anteroposteriorly narrow
(Fig. 7A, B), whereas in posterior view they have a rectan-
gular shape. Their height is almost half of the length of
their total lateromedial width (Fig. 1B). The dorsoventral
height of the parietals is slightly larger than the height of
the foramen magnum. This difference is not as major as it
is in most sauropods (e.g. Camarasaurus,Giraffatitan),
but it is clearly different from the dorsoventrally short
parietals of derived titanosaurs (Nemegtosaurus,Rapeto-
saurus; Nowinski 1971; Curry Rogers & Forster 2004).
The ventral side of the posterolateral process of the
parietal articulates with the supraoccipital at its medial
half and therefore covers all the dorsolateral margin of the
supraoccipital. The ventral margin of the posterolateral
process expands further laterally beyond the supraoccipi-
tal–exoccipital contact. This condition prevents any con-
tact of the squamosal with the supraoccipital and differs
from the condition seen in diplodocids (Calvo & Salgado
1995; Upchurch 1998; Remes 2006). The parietal forms
the dorsolateral part of the post-temporal fenestra
(Fig. 1B). Medioventrally, the post-temporal fenestra is
surrounded by the exoccipital and laterally by the squa-
mosal (Fig. 1B), a widespread character amongst non-
flagelicaudatan sauropods (Upchurch 1998; Wilson 2002;
Upchurch et al. 2004; Whitlock 2011). Amongst macro-
narian neosauropods, the exclusion of the parietal from
14 J. S. Marpmann et al.
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the post-temporal fenestra has been reported only for
some titanosaurs such as Nemegtosaurus and Malawisau-
rus (Wilson 2005). The anterior planes of the posterolat-
eral processes of the parietals articulate with the prootics
ventrally; these processes form the posterior wall of the
supratemporal fenestrae. The medial and anterior margins
of the supratemporal fenestrae are formed dorsally by the
parietals and ventrally by the laterosphenoid. The left
parietal (DFMMh/FV 581.2) contacts the left laterosphe-
noid on the medial side of the parietal, whereas the antero-
lateral process of the parietal matches the lateral process
of the laterosphenoid. The supratemporal fenestra of
Europasaurus is around 2.5 times wider lateromedially
than long anteroposteriorly (Fig. 7A, B). Therefore, the
supratemporal fenestra is anteroposteriorly short, as can
be seen in most sauropods (e.g. Spinophorosaurus,
Camarasaurus,Giraffatitan), but differs from Shunosau-
rus (Chatterjee & Zheng 2002) and basal sauropodo-
morphs. The dorsal distance that separates the
supratemporal fenestrae is only slightly larger (1.1) than
the long axis of the fenestra. Similar proportions are
observed in some specimens of Camarasaurus (Madsen
et al. 1995, fig. 25; SMA 0002/02). The dorsal distance
between the supratemporal fenestrae observed in the juve-
nile specimen of Camarasaurus (CM 11338) is propor-
tionally larger than that observed in Europasaurus and
other Camarasaurus specimens. This difference amongst
Camarasaurus specimens indicates that there must be
some ontogenetic or even specific variations amongst this
taxon, although based on Europasaurus ontogenetic evi-
dence the former hypothesis is supported. In flagellicauda-
tan diplodocoids, the supratemporal fenestrae are
separated from each other (with a distance that is around
as twice as long as the longest axis of the fenestrae); how-
ever, a supratemporal fenestra in rebbachisaurids seems to
be absent, as in Nigersaurus (Sereno et al. 2007), or very
reduced, as in Limaysaurus (Calvo & Salgado 1995; Sal-
gado et al. 2004). Similar proportions to those observed in
Europasaurus appear to be present in basal sauropods
(Spinophorosaurus,Mamenchisaurus,Jobaria; GCP-CV-
4229; Ouyang & Ye 2002, Fig. 5, MNNTIG4). In contrast,
the distance that separates both supratemporal fenestrae in
Giraffatitan is just half of the length of the long axis of
the supratemporal fenestra (MB.R.2223.1). This also
holds true for Abydosaurus (Chure et al. 2010). The dis-
tance between both supratemporal fenestrae in the skull
referred to as Brachiosaurus sp. (Carpenter & Tidwell
1998; USNM5730) is almost the same as the lateromedial
length, and is thus relatively wider than in Giraffatitan.
Therefore, the shape of the parietals in Europasaurus is
more reminiscent of other sauropods, but not of Giraffati-
tan or Abydosaurus.
Besides the supratemporal fenestra, two other fenestrae
are surrounded by the parietals, the parietal fenestra and
the postparietal fenestra. The parietal fenestra is discern-
ible as a small concavity, especially in dorsal view of the
left parietal. The exact size or shape of this fenestra is
unknown because of missing bone fragments that prevent
the parietals from contacting medially (Fig. 7A). The
presence of another fenestra, the postparietal fenestra, is
also evident when both parietals are manually articulated
with the braincase. In dicraeosaurid sauropods (e.g. Suu-
wassea,Amargasaurus; Salgado & Calvo 1992; Harris
Figure 7. Europasaurus holgeri parietals. A, B, DFMMh/FV
291.2 (left) and DFMMh/FV 291.3 (right) in A, dorsal and B,
ventral views. C, D, right parietal (DFFNh/FV 883) in C, dorsal
and D, ventral views. E, F, reversed left parietal (DFMMh/FV
169) in E, dorsal and F, ventral views. G, reconstruction of the
different MOS detected amongst preserved parietals in dorsal
view. Grey zone in A corresponds to broken surface, recon-
structed in the base of broken edged and articulation of parietals
into the braincase (DFMMh/FV 291.1). Abbreviations: brc, brain
cavity; fa, frontal articulation; lsa, laterosphenoid articulation;
pf, parietal fenestra; poa, postorbital articulation; proa, prootic
articulation; soa, supraoccipital articulation; stf, supratemporal
fenestra. Scale bar represents 1 cm.
Cranial anatomy of the Late Jurassic dwarf sauropod Europasaurus holgeri 15
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2006), this fenestra is surrounded by the parietals dorsally
and the supraoccipital ventrally, as in Europasaurus. The
postparietal fenestra is easily visible in posterior view of
the skull (see Fig. 1 and below). The occurrence of a post-
parietal fenestra is an unusual character for a non-dicraeo-
saurid sauropod (e.g. Salgado & Calvo 1992; Upchurch
1998; Wilson 2002). Its presence was recognized as a syn-
apomorphic character of dicraeosaurids (e.g. Salgado &
Calvo 1992; Upchurch 1998; Wilson 2002; Whitlock
2011). Amongst non-dicraeosaurid sauropods, the post-
parietal fenestra was only described for the basal sauropod
Spinophorosaurus (Knoll et al. 2012) and an indetermi-
nate titanosaur from the Late Cretaceous of Argentina
(Paulina-Carabajal & Salgado 2007). Therefore, its pres-
ence in Europasaurus is interpreted as an autapomorphic
character of this taxon, convergently acquired in Spino-
phorosaurus and, amongst neosauropods, in dicraeosaur-
ids and probably some derived titanosaurs.
Ontogenetic changes. Recognized size-independent
characters include the structure of the bone surface, the
structure of the articular facet of the distal part on the
anteroventral plane of the posterolateral process, the
absence or presence of a depression at the proximal end of
the anteroventral plane of the posterolateral process, the
development of the frontoparietal contact, the width of
the supratemporal fenestra in relation to the total width of
the parietal (both measured lateromedially), and the depth
of the brain cavity. The width (lateromedially measured)
of the supratemporal fenestra in relation to the length
(anteroposteriorly measured) is not a distinctive character
since the openings differ greatly from each other even in
the two parietals that belong to the same braincase.
Two elements are interpreted as being MOS 1
(DFMMh/FV 1078 and 169; Fig. 7G, H). DFMMh/FV
1078 is the smallest parietal with an hvbs structure, and
on the ventral side the part that encloses the brain cavity
is very shallow and shows no ridges. The laterally longer
posterolateral process has a rugose structure. The articular
facet for the squamosal does not seem to be well devel-
oped in the distal part on the anteroventral plane of the
posterolateral process, and neither is the articular facet for
the laterosphenoid. The development of these articular
facets is a sign for a rather loose connection of these
bones. The lack of a depression at the proximal end of the
anteroventral plane of the posterolateral process also
shows that there was a very loose connection with the
supraoccipital–prootic notch, which explains the disar-
ticulated nature of the specimen. No depression for the
hook of the frontal is visible, either because it is still in a
juvenile stage or because it belongs to morphotype B, in
which the frontal does not have the hook-shaped structure.
Considering this specimen undoubtedly belongs to an
ontogenetically young individual, determining the mor-
photype is rather difficult. The size difference with
DFMMh/FV 169 is not significant, and the morphology is
very similar in the two specimens, except for the slightly
more developed articular facet for the squamosal in the
parietal DFMMh/FV 1078. Therefore, the parietal
DFMMh/FV 1078 cannot be associated with either
morphotype.
The other element, staged MOS 1 as well, is DFMMh/
FV 169 (Fig. 7G, H). This very fragile parietal is slightly
larger than DFMMh/FV 1078, yet both have the same
bone surface structure, as well as the incomplete anterolat-
eral process. Additionally, this specimen lacks parts of the
posterior region of the medial margin. The articular facet
on the posterolateral process is less rugose than on the
smallest parietal of DFMMh/FV 1078, making it even
more loosely connected to the squamosal. A depression
for the supraoccipital cannot be found at the ventral side
of the parietal (Fig. 7). The anterior side for the contact to
the frontal also lacks a depression. The width of the supra-
temporal fenestra is slightly larger than half the width of
the parietal. Parietal DFMMh/FV 169 probably represents
a diminutive specimen of morphotype A but, as in
DFMMh/FV 1078, the characters are not reliable enough
to determine the morphotype.
DFMMh/FV 883 represents the MOS 2 (Fig. 7E, F).
This partially incomplete parietal is the largest and most
robust parietal, especially in its posterolateral process.
Some spots with a vascularized bone surface structure are
visible in the medial region on the ventral side. The rest of
the bone surface is very rugose and the articulation for the
squamosal shows well-pronounced facets to allow a tight
connection. The anterolateral process is short, as in
DFMMh/FV 169 and DFMMh/FV 1078, but the distal
part of the process is almost complete. Compared to the
posterolateral process, the anterolateral process is rather
short. Parietal DFMMh/FV 883 lacks the depression on
the ventral side, and judging by the preserved parts, it
seems that there was none, which is similar to the poten-
tially juvenile specimens. The parts enclosing the brain
cavity are shallow, as in DFMMh/FV 169 and DFMMh/
FV 1078. The frontoparietal contact is not well developed.
The width of the supratemporal fenestra is slightly smaller
than half the width of the parietal, and therefore the supra-
temporal fenestra is relatively wider than that measured in
the parietals staged as MOS 1. This large parietal, which
had not finished growing, is probably a subadult of mor-
photype B and would have become even larger.
Two elements are assigned to MOS 3: DFMMh/FV
581.2 and DFMMh/FV 581.3 (Fig. 7A–D). Both parietals
have a highly rugose bone surface structure lacking any
vascularization. The only differences between the speci-
mens are the stouter appearance of DFMMh/FV 581.3 in
the lateromedial direction and the different shapes of the
supratemporal openings. Both have relatively long antero-
lateral processes compared to the more juvenile stages
above. These processes seem to have had a good
16 J. S. Marpmann et al.
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articulation with the laterosphenoids. The articular facets
on the posterolateral processes are well developed, show-
ing ridges and grooves for a strong connection to the squa-
mosals. Both show deep depressions at the proximal ends
of the anteroventral plane of the posterolateral processes,
which are needed for a firm contact with the notch of the
supraoccipital–prootic region. The sections that contribute
to the brain cavity are deep and winding, giving the brain
more space. This corresponds to the ontogenetic change
from juvenile to adult, although the brain cavity is propor-
tionally larger in juveniles. This specimen has a compara-
tively wider supratemporal fenestra, indicating that the
relative distance that separates the supratemporal fenes-
trae tend to decrease through ontogeny. The anterior
regions for the frontoparietal contact show well-devel-
oped contacts for the hook-shaped structures described in
morphotype A of the frontals, suggesting that DFMMh/
FV 581.2 (Fig. 7) and DFMMh/FV 581.3 are both part of
morphotype A. When parietals DFMMh/FV 581.2 and
DFMMh/FV 581.3 are put together, the presence of the
postparietal foramen in the skull can be regarded as an
autapomorphic character.
Postorbital. Five right postorbitals (DFMMh/FV 095,
097, 098, 380, 555/1) and one left postorbital (DFMMh/
FV 096) from Europasaurus were studied (Fig. 8). This
triradiate bone is interpreted as a fused postorbital and
postfrontal (Upchurch et al. 2004), also described as post-
orbital þpostfrontal by Janensch (1935–1936).Asin
other sauropods, the postorbital participates in forming
the lateral margin of the supratemporal fenestra, the ante-
rior edge of the infratemporal fenestra, and the posterior
border of the orbit (Fig. 1A). The postorbital has three
processes: the ventral or jugal process, which is the lon-
gest and most gracile process; the posterior or squamosal
process; and the anterior or parietal–laterosphenoid pro-
cess, which is the most robust of the processes (Fig. 8A).
The maximum anteroposterior length of this element is
measured from the anterior to the posterior process in dor-
sal view. This distance is slightly longer than half of the
dorsoventral height of the jugal process of the postorbital.
A postorbital of similar robustness is present in Camara-
saurus (Madsen et al. 1995; CM11338) and Euhelopus
(Mateer & McIntosh 1985; PMU 233). The postorbital of
Giraffatitan is more gracile (anteroposterior length is less
than half of the dorsoventral height; Janensch 1935–1936;
MB.R. 2223.1). The squamosal process is tapered at its
distal end and contacts the concave sulcus of the squamo-
sal medially. The anterior process is deflected medially to
support the lateral process of the laterosphenoid and the
anterolateral process of the parietal. The gracile jugal pro-
cess is anteroventrally oriented and articulates with the
postorbital process of the jugal.
Ontogenetic changes. Size-independent characters used
are the bone surface structure and the depression on the
medial side, where the three processes come together,
which is very deep in adult specimens. Nonetheless, the
shape of the jugal process, a contribution of the postorbital
to the orbital opening, is not a reliable character in Euro-
pasaurus, because the orbit remains relatively large
throughout ontogeny. Two elements are considered MOS
1 and four elements MOS 3. The postorbitals contain no
intermediate MOS.
MOS 1 is observed in DFMMh/FV 555/1. This element
is rather gracile in appearance compared to the more
robust, presumably adult elements. As DFMMh/FV 555/1
is rather small with an hvbs structure and no depression
on the medial side, it probably is a juvenile. Overall mor-
phology is similar to morphotype A adult specimens
DFMMh/FV 095 and DFMMh/FV 096; thus, we assign
the same morphotype to DFMMh/FV 555/1. DFMMh/FV
380 is of about the same size as the ontogenetically older
DFMMh/FV 095 and DFMMh/FV 096, but shows juve-
nile characters such as an hvbs structure and the absence
of the depression on the medial side. Therefore, it is
assigned to MOS 1 of the larger morphotype B.
DFMMh/FV 095 and DFMMh/FV 096 are associated
with MOS 3.1. These two elements vary only slightly in
morphology, and both show a finished surface structure
with medial depressions. Specimen DFMMh/FV 096
attaches very well to the other skull bones of the adult
morphotype A, which are all visualized in the new skull
reconstruction. DFMMh/FV 097 and DFMMh/FV 098
represent MOS 3.2. These two elements show a very
rugose surface. While DFMMh/FV 097 has the rugose
surface predominantly on its medial side, DFMMh/FV
098 also has a rugose surface on the ventral side down
toward the base of the jugal process, which is mostly
absent. Both show an extensive deep depression situated
medially in DFMMh/FV 097. Element DFMMh/FV 097
Figure 8. Europasaurus holgeri left postorbital (DFMMh/FV
96) in A, lateral and B, medial views. Abbreviations: itf, infra-
temporal fenestra; ja, jugal articulation; ls-pa, laterosphenoid
and parietal articulation surface; orb, orbit; sqa, squamosal artic-
ulation; stf, supratemporal fenestra. Scale bar represents 1 cm.
Cranial anatomy of the Late Jurassic dwarf sauropod Europasaurus holgeri 17
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varies the most from the other postorbitals, but seems to
be deformed diagenetically rather than representing
another morphotype. Since DFMMh/FV 097 is deformed
and broken and DFMMh/FV 098 is incomplete, it is diffi-
cult to determine the morphotype beyond the staging.
Squamosal. Four isolated squamosals have been discov-
ered (DFMMh/FV 657 is a right element, while 993, 1004
and 712.2 are left squamosals), but only one specimen
(DFMMh/FV 712.2) is almost complete (Fig. 9). The lat-
ter only lacks a small distal fragment of the ventral pro-
cess, and the following description is mainly based on this
nearly complete element. The squamosal is a triradiate
bone with a large ventral process that contacts the quad-
rate, an anterior process in which the postorbital is
inserted, and a medial process that mainly articulates with
the parietal and exoccipital–paroccipital–opisthotic com-
plex. In size and shape, the squamosal fits very well with
the complete braincase DFMMh/FV 581.1.
As described by Madsen et al. (1995) for Camarasau-
rus, the squamosal has the shape of a question mark in
lateral view. Its anterior process supports the posterior
process of the postorbital and both form the temporal
bar. The articular facet for the postorbital is broad, with
a maximum length of around 2.27 cm and a maximum
height of 1.36 cm. The ventral margin of this articular
facet is well marked by a lateral expansion that serves as
ventral support for the postorbital. The squamosal forms
a small posterolateral margin of the supratemporal fenes-
tra, which is mainly formed by the parietal and postor-
bital (Fig. 1).
The medial process of the squamosal is robust and artic-
ulates mainly with the exoccipital–paroccipital–opisthotic
complex through its entire posteroventral margin. It is
also completely inset in the concave dorsal margin of the
exoccipital–paroccipital–opisthotic complex, covering
most of the complex and laterally bounding the post-tem-
poral fenestra. The exact position and size of the post-tem-
poral fenestra remains unknown because no squamosal
was found in articulation with the almost completely pre-
served braincase. Posteromedially, the squamosal contacts
the posterolateral process of the parietal, forming a broad
overlapping surface. The parietals are included in forming
the post-temporal fenestra (see above), since the squamo-
sal does not expand medially. If present, this medial
expansion would exclude the parietals from the post-tem-
poral fenestrae, observed in other sauropods (e.g. Negme-
tosaurus,Apatosaurus; Wilson 2005; Balanoff et al.
2010).
The ventral process of the squamosal is long and grac-
ile. In lateral view, its anterior edge is slightly convex,
whereas its posterior border is mainly straight and only
curves posteriorly at the ventral end. The anterior margin
of the ventral process of the squamosal builds the upper
posterior part of the infratemporal fenestra. The squamo-
sal is, besides the postorbital, the element that contributes
most to the shape of the infratemporal fenestra (Fig. 1).
Ontogenetic changes. Size-independent characters con-
sist of the bone surface structure and the shape of the
articular facets. Morphotype determination depends on
the size in correlation with the bone surface structure,
especially of the medial process. Three elements are MOS
1 and one element is MOS 3. The squamosal has no inter-
mediate MOS.
Four specimens represent MOS 1. While specimens
DFMMh/FV 657, 993 and 1004 all show an hvbs structure
with depressions and articular facets already accentuated,
given their surface and size, the first and the third seem to
be juveniles of morphotype A. DFMMh/FV 993 also
shows an hvbs structure, but with striated articular facets.
It is even larger than the MOS 3 squamosal of morphotype
A, suggesting that this specimen is a juvenile of the larger
morphotype B.
Element DFMMh/FV 712.2 is interpreted as being
MOS 3. The bone surface is only slightly vascularized in
some spots, but looks mostly finished. The articular facets
are very rugose and the squamosal fits very well onto the
braincase of DFMMh/FV 581.1. Therefore, this squamo-
sal is assigned to morphotype A.
Quadratojugal. Three quadratojugals have been found.
Only a completely preserved right quadratojugal pertains
to the holotype material (DFMMh/FV 291.25; Fig. 10).
Quadratojugals DFMMh/FV 785.2 and DFMMh/FV 734
each consist of a different right element, preserving the
posterior half and the anterior half, respectively. The
Figure 9. Europasaurus holgeri left squamosal (DFMMh/FV
712.2) in A, lateral and B, medial views. Abbreviations: itf,
infratemporal fenestra; poa, postorbital articulation; popa, para-
occipital process articulation; qa, quadrate articulation. Scale bar
represents 1 cm.
18 J. S. Marpmann et al.
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complete quadratojugal (DFMMh/FV 291.25) can be
manually articulated with the quadrate DFMMh/FV 062,
indicating an individual of similar size and proportions.
As in other sauropods, when viewed in lateral view, the
quadratojugal is L-shaped with a horizontally long process
(the anterior process) and a short vertical process (the dor-
sal process) (Fig. 10). The length of the dorsal process is
around three-quarters that of the anterior process. In Euro-
pasaurus the quadratojugal forms the lateroventral margin
of the infratemporal fenestra (Figs 1A, 10). The quadrato-
jugal articulates with the squamosal (dorsolaterally), the
quadrate (medially), and the jugal (anteriorly) (Figs 1,
10). Based on the reconstruction of the skull (Fig. 1) and
the articulation of the quadratojugal with the surrounding
bones, the anterior process of the quadratojugal is hori-
zontally aligned with the tooth row (Fig. 1), as in Camara-
saurus (Madsen et al. 1995), instead of being inclined, as
in Giraffatitan and Abydosaurus (Janensch 1935–1936;
Chure et al. 2010).
The dorsal process is sigmoidal, following the same
shape observed in the lateral edge of the quadrate. While
the dorsal part of the squamosal process is narrow and del-
icate, its ventral section is stouter and anteroposteriorly
wider. This expansion or wider zone articulates with the
lateroventral margin of the lateral outline of the quadrate
(Fig. 10B). Half of the lateral surface of the squamosal
process of the quadratojugal serves as an articular plane
for the squamosal (Fig. 10A). The articulation between
these two bones starts at the same point in which the dor-
sal process changes its orientation, from dorsal towards
posterodorsal (Fig. 10A). In medial view, the articulation
of the quadratojugal with the quadrate is clearly distin-
guishable as a rough surface, which extends through
almost all the medial surface of the vertical process
(Fig. 10). Therefore, as was noted above, the quadratoju-
gal articulates with the quadrate, medially, and with the
squamosal, laterally.
The anterior process of the quadratojugal is straight on
its dorsal outline, as is observed in most other sauropods
(e.g. Camarasaurus,Brachiosaurus; Janensch 1935–
1936; Madsen et al. 1995). The ventral margin has a
marked ventral expansion that forms a prominent ventral
keel (Fig. 10), which is present in both quadratojugals pre-
serving this section of the bone (DFMMh/FV 291.25 and
734). A ventral expansion was recently described as a syn-
apomorphic character of Brachiosauridae (D’Emic 2012),
and scored associated with the derived state (presence of
ventral projection) only in Europasaurus,Giraffatitan and
Abydosaurus (D’Emic 2012, chapter 9). The ventral
expansion of the latter two of these taxa has a slightly
developed and more rounded ventral expansion than that
of Europasaurus. A similar ventral rounded expansion to
that of Giraffatitan (Janensch 1935–1936, fig. 21) and
Abydosaurus (Chure et al. 2010, fig. 3) is present in some
specimens of Camarasaurus (Madsen et al. 1995, fig. 19;
SMA 0002/02). In addition, a similar, although much
more developed, ventral expansion is present in the ante-
rior ramus of the quadratojugal of Tapuiasaurus (Zaher
et al. 2011, fig. 1). A rounded and slightly developed ven-
tral expansion is also present in Nemegtosaurus (Wilson
2005, fig. 3), which is more similar to that of Giraffatitan
than Europasaurus or Tapuiasaurus. Therefore, the pres-
ence of a ventral expansion in the quadratojugal seems to
have a broader distribution amongst camarasauromorph
sauropods and is not only restricted to taxa of the clade
Brachiosauridae. The articulation for the jugal can be
observed in medial view and is formed as a thin scar that
extends up to the level of the ventral expansion.
Ontogenetic changes. Size-independent characters used
are the bone surface structure and the articular facets.
Since the incomplete specimens are both from different
parts of the bone, they can only be compared to the com-
plete quadratojugal. It is difficult to predict if the shape of
Figure 10. Europasaurus holgeri right quadratojugal (DFMMh/
FV 291.25) in A, lateral and B, medial views. Abbreviations: itf,
infratemporal fenestra; ja, jugal articulation; qa, quadrate articu-
lation surface; sqa, squamosal articulation surface; vb, ventral
bulge. Scale bar represents 1 cm.
Cranial anatomy of the Late Jurassic dwarf sauropod Europasaurus holgeri 19
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the keel-like tip on its anteroventral margin and the form
of the vertical process are ontogenetic differences or fea-
tures that differ between morphotypes. Two elements are
presumably MOS 2 and one element is MOS 3. No ele-
ment was determined to be a juvenile.
MOS 2 is represented by two elements (DFMMh/FV
734 and DFMMh/FV 785.2). DFMMh/FV 734 is pre-
served as the anterior part of the horizontal branch with a
smooth bone surface structure, but a rounded tip of the
keel. It is the same size as DFMMh/FV 291.25, but
the keel does not look complete developed compared to
the stage three specimen. DFMMh/FV 785.2 is signifi-
cantly smaller than DFMMh/FV 291.25, but shows a
straight rather than a sigmoidal vertical process (cf.
Madsen et al. 1995, fig. 19; DNM 28 and DNM 975),
although the articular facets are well developed and the
bone surface structure has a smooth surface. Considering
too much material is missing in both elements, it is hard
to assign them to a specific stage. But both look slightly
younger than the MOS 3 specimen, and thus for now they
will be assigned MOS 2. The different features of
DFMMh/FV 734 and DFMMh/FV 785.2 probably mean
that they are both of the other morphotype.
MOS 3 is assigned to DFMMh/FV 291.25. This com-
plete element fits very well into the squamosal DFMMh/
FV 712.2. Bone surface structure is smooth and has a fin-
ished appearance. The vertical process is sigmoidal and
the horizontal rather straight, while articular facets on
both are well accentuated and rugose. The keel-like tip is
pointed and lateromedially sharp. It is regarded as being
of morphotype A.
Palate
Neither a palatine nor a vomer has been found from the
palate area. As the quadrate is most commonly referred to
as being part of the palate region, this scheme will be used
here, too. Of the 13 preserved palate elements amongst
the Europasaurus material, the quadrates are listed first,
because the quadrate is a bone that connects several skull
regions, including the palate region, with those of the
skull roof. The description follows an anterior direction
starting at the quadrate.
Quadrate. In total, six isolated quadrates from Europa-
saurus were collected (DFMMh/FV 057, 058, 062, 062.1,
972.2, 1032.2) (Fig. 11). The following description is
mainly based on the largest and best-preserved element
(DFMMh/FV 062), which fits well onto braincase
DFMMh/FV 581.1 and squamosal DFMMh/FV 712.2.
Quadrate DFMMh/FV 062 is well preserved and its
general shape is reminiscent of quadrates of other rela-
tively basal macronarians (e.g. Camarasaurus,Giraffati-
tan; Janensch 1935–1936; Madsen et al. 1995). The
articular surfaces for the squamosal, quadratojugal and
pterygoid are well defined (Fig. 11). A well-developed
Figure 11. Europasaurus holgeri left quadrate (DFMMh/FV 062) in A, lateral, B, medial and C, posterolateral views. Abbreviations:
lapl, lateral plate; ptw, pterygoid wing; qf, quadrate fossa; qja, quadratojugal articulation; sqa, squamosal articulation. Scale bar repre-
sents 1 cm.
20 J. S. Marpmann et al.
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shaft is present along the entire length, which is dorsally
and ventrally expanded to form the head as well as the
articular surface of the quadrate. The pterygoid wing runs
along the medial side of the quadrate in an anterior direc-
tion (Fig. 11). A narrow lamina-like process, referred to
as the lateral plate, extends laterally from the shaft to con-
tact the squamosal and the quadratojugal (Fig. 11A). The
lateral surface of the lateral plate has a scar that extends
throughout the surfaces and serves as a contact for the
quadratojugal (ventrally) and the squamosal (dorsally).
Due to the squamosal–quadratojugal contact along the lat-
eral margin of the quadrate, the quadrate is excluded from
the infratemporal fenestra. The dorsal head of the quadrate
has a triangular shape in cross section. The posteriorly ori-
ented apex forms the dorsal margin of a robust posterior
crest.
The quadrate fossa is deep and posteriorly directed.
Ventrally, this fossa begins at the same level as the ventral
edge of the pterygoid process. The lateral plate, squamo-
sal and quadratojugal together form the lateral edge of the
quadrate fossa. The medial wall is formed by a robust
crest, which is posteriorly directed and extends throughout
the height of the quadrate. In posterior view, this crest
stretches dorsolaterally from the ventromedial corner of
the quadrate to the dorsomedial end.
The pterygoid wing is well developed and anteriorly
expanded (Fig. 11). Its dorsal edge is anteroventrally
directed from the quadrate head down to the middle of the
quadrate, where the ventral edge acquires a strong ventral
orientation. The single articulation facet for the pterygoid
is large and covers most of the medial side of the ptery-
goid wing except for the more dorsal margin. In posterior
view the ventral articular surface of the quadrate, which
articulates with the articular in the mandibles, is dorsolat-
erally oriented (Fig. 11), but forms two almost horizontal
facets that are separated by a marked step.
Ontogenetic changes. Size-independent characters for
staging the quadrates are bone surface structure, depth of
the quadrate fossa, and the curvature between the process
for the articular and the pterygoid wing. DFMMh/FV
972.2 is assigned to morphotype B while all the others,
apart from DFMMh/FV 062.1, can be assigned to mor-
photype A. One element is described as MOS 1, three as
MOS 2, and two as MOS 3.
DFMMh/FV 062.1 represents MOS 1. Bone surface
structure is highly vascularized. The quadrate fossa is
shallow. The curvature between the process for the articu-
lar and the pterygoid wing is not very pronounced.
Although identification as a quadrate is indisputable, its
morphology differs from all the other quadrates at the
posterodorsal margin. At this margin, there is a crest
instead of a concave indentation. Except for this crest,
morphology is reminiscent of the other Europasaurus
quadrates. The crest might be a juvenile character that is
not preserved in older ontogenetic stages. The assignment
of the quadrate to Europasaurus is currently uncertain but
it will be regarded as belonging to Europasaurus for the
time being.
Three sub-stages were recognized in MOS 2. MOS 2.1
is represented by element DFMMh/FV 1032.2. This com-
plete specimen shows a moderately vascularized bone sur-
face structure. The quadrate fossa and the curvature are
both shallow. The second sub-stage (MOS 2.2) is repre-
sented by DFMMh/FV 057. This almost complete speci-
men shows a moderately vascularized bone surface
structure with most surfaces finished. The posterior plane
of the squamosal process, however, is highly vascularized,
showing that this part is still growing. DFMMh/FV 057
has a shallow quadrate fossa, but the curvature cuts in
more deeply. The third stage, MOS 2.3, represented by
DFMMh/FV 058, has a similar bone surface structure as
in DFMMh/FV 057, except for the posterior plane of the
squamosal process. The quadrate fossa is deeper, as is the
degree of curvature.
The third MOS is represented by two elements
(DFMMh/FV 062 and DFMMh/FV 972.2). The bone sur-
face structure of these two elements is smooth and appears
finished. The articular facets are well defined and rugose,
and the quadrate fossa is very deep, as is the curvature.
The quadrate fits very well to squamosal DFMMh/FV
712.2 and quadratojugal DFMMh/FV 291.25. In
DFMMh/FV 972.2, the quadrate fossa is very deep, but
the curvature here is shallow to almost non-existent. Since
one putative diplodocoid dorsal vertebra has also been
found in the quarry (JLC pers. obs.), the question arises if
DFMMh/FV 972.2 could be assigned to another sauropod
taxon. But since the quadrate fossa is really deep in con-
trast to the condition seen in diplodocoids, such as Diplod-
ocus or Apatosaurus (Whitlock et al. 2010), it is more
likely a quadrate of an adult of morphotype B.
Pterygoid. The pterygoid is usually the largest element
of the sauropod palate (Fig. 12). Seven pterygoids are pre-
served, including five left (DFMMh/FV 100.2, 244, 554.6,
748, 965.4) and two right (DFMMh/FV 196, 964) ele-
ments. The pterygoid of Europasaurus is a large element
with three different processes. One of these processes is
an anteriorly directed wing that contacts the contralateral
pterygoid (the anterior pterygoid wing). A second process
is lateroventrally directed for contacting the ectopterygoid
(the lateroventral pterygoid process), and the third process
is a posteriorly directed wing, which gives support to the
basipterygoid process of the braincase and the quadrate
(the posterior pterygoid wing). These three processes lead
to the characteristic triradiate shape of the pterygoid
(Fig. 12).
The anterior pterygoid wing is the longest and most
prominent process of the pterygoid. The pterygoid con-
tacts with its contralateral through a medially directed
Cranial anatomy of the Late Jurassic dwarf sauropod Europasaurus holgeri 21
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expansion, which starts below the posterior pterygoid
wing and diminishes into the dorsal surface of the anterior
pterygoid wing. Anteriorly to this expansion the facet for
the interpterygoid articulation cannot be clearly distin-
guished because of the state of preservation. However, as
in most sauropods, this facet was probably extended more
anteriorly, up to the level of the pterygoid–vomer articula-
tion. The vomer articular facet in the anterior pterygoid
wing is well marked and recognized as an anteroventral
depression on the lateral side of the anterior pterygoid
wing (Fig. 12). The exact place where the palatine articu-
lates on the medial side of the anterior pterygoid wing
cannot be defined, but as in most sauropods, this surely
covers most of the ventrolateral side of this process except
the facet for the vomer.
The lateroventral pterygoid wing is the smallest but
most robust of the three processes of the pterygoid. The
lateroventral process is a short expansion that supports the
ectopterygoid. The articulation surface for the ectoptery-
goid extends nearly the entire length of the process as a
marked longitudinal canal in which the ectopterygoid is
inset.
The posterior pterygoid wing (or quadrate process) is a
middle-sized process that gives support to the basiptery-
goid process of the parabasisphenoid, dorsally, and con-
tacts the quadrate lateroventrally. In dorsal view the
posterior process and the anterior pterygoid wing diverge
from each other at an angle slightly larger than 90, result-
ing in a curved shape of the pterygoid (Fig. 12). The
basipterygoid pit (fossa basipterygoideus) is a small round
depression observed in the anterodorsal surface of the pro-
cess. This facet is inset in a medially facing, concave sur-
face of the process. The convex lateral surface of the
posterior pterygoid wing has a rugose surface, especially
ventrally, that articulates with the medial surface of the
pterygoid wing of the quadrate (Fig. 12).
Ontogenetic changes. Size-independent characters used
are bone surface structure, elevation of the blunt, tooth-
like projection anterior to the basipterygoid pit, curvature
of the medial side of the quadrate process, depth of the
basipterygoid pit, form of the anterodorsal margin of the
quadrate process, and the medial margin of the basiptery-
goid pit. The absence or presence of the latter is used to
define the morphotype. One element is assigned stage 1,
two to stage 2, and one to stage 3.
DFMMh/FV 196 (MOS 1) is represented only by a
small fragment. The bone has an hvbs structure with stria-
tions in the longitudinal direction. The tooth-like projec-
tion is moderately developed. There is no curvature on the
medial side, but a rather flat surface. The basipterygoid pit
is not very deep. The anterodorsal margin is rounded and
the medial margin is lacking, suggesting that the element
is of morphotype B.
Two different substages are recognized amongst the
elements interpreted as MOS 2. The incomplete DFMMh/
FV 244 (MOS 2.1) shows a partially vascularized bone
surface. The tooth-like projection is small, the curvature
is slightly concave, and the basipterygoid pit is shallow.
The anterodorsal margin is not as sharp as in stage 3, but
the medial margin is still rounded. This pterygoid is the
youngest element of morphotype A amongst the ptery-
goids. DFMMh/FV 554.6 (MOS 2.2) preserves about the
same part as DFMMh/FV 244. It has a partially vascular-
ized bone surface, a small tooth-like projection, and a con-
cave curvature. The basipterygoid pit is deep and the
anterodorsal margin is not as sharp as in stage 3, while the
medial margin is already sharp. This pterygoid is the sec-
ond oldest element of morphotype A amongst the
pterygoids.
The third stage (MOS 3) was recognized in DFMMh/
FV 100.2 (Fig. 12). The bone surface structure of this
almost complete specimen is smooth, and the articular
facets are very rugose. The tooth-like projection is well
developed, and the curvature is concave. The basiptery-
goid pit is very deep. Both the anterodorsal margin and
the medial margin are sharp. This pterygoid is of a pre-
sumably fully grown animal of morphotype A and fits
quite well with the quadrate DFMMh/FV 062.
Ectopterygoid. The ectopterygoid is a rather simple ele-
ment, which contacts with the pterygoid, palatine and
maxilla (Fig. 12). Three ectopterygoids are preserved
(DFMMh/FV 748, 965.4, 966). Two processes form the
L-shaped ectopterygoid: a narrow anterolaterally directed
process which contacts posteriorly with the maxilla, and a
Figure 12. Europasaurus holgeri left pterygoid (DFMMh/FV
100.2) and manually articulated ectopterygoid (DFMMh/FV
748) in medial view. Abbreviations: aptw, anterior pterygoid
wing; ec, ectopterygoid; lvptx, lateroventral pterygoid wing; ma,
maxillar articulation; pptw, posterior pterygoid wing. Scale bar
represents 1 cm.
22 J. S. Marpmann et al.
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vertically expanded flange which contacts with the ptery-
goid. The anterolateral process is mainly oval-shaped in
cross section. Its posterior end is expanded to form the
facet for the articulation with the palatine process of the
maxilla. Two differently positioned articular facets are
observed at this posterior end, a posterodistal and an ante-
rodistally facet, giving a firm attachment of the palate to
the maxilla. This process is posteriorly expanded to form
the process that is inserted into the lateroventral pterygoid
process of the pterygoid. Through the posterior half of the
lateral side of the ectopterygoid, a rugose and slightly
expanded surface marks the area of contact with the pala-
tine. This area is mainly extended through the posterodor-
sal side of the ectopterygoid vertical expansion, and only
slightly exposed in the anterolateral process.
Ontogenetic changes. All three preserved elements show
rather rugose bone surfaces with little vascularization and
well-pronounced articular facets. While DFMMh/FV 748
has an elongated lateral shaft and a claw-like medial
flange with a concave medial margin, DFMMh/FV 965.4
shows a rather stout lateral shaft and the blade-like medial
flange has a straight medial rim. They probably belong to
two morphotypes: DFMMh/FV 748 is presumably mor-
photype A, and DFMMh/FV 965.4 morphotype B. The
third specimen, DFMMh/FV 966, is rather incomplete,
but shows characters that resemble those of morphotype
B. Specimen DFMMh/FV 748 fits well in the articular
facet of pterygoid DFMMh/FV 100.2 and therefore might
be of the same, presumably adult, stage. The morphotype
B specimens belong at least to stage 2, but they could pos-
sibly be older.
Braincase and occiput
Several bones from the braincase of Europasaurus holgeri
are preserved, most as isolated elements. Of the braincase
and occiput region, only the stapes are missing, which so
far have been reported in few sauropods (Shunosaurus,
Camarasaurus; Zheng 1991; Madsen et al. 1995). The
braincase description is mainly based on a newly pre-
pared, almost complete, and excellently preserved speci-
men (DFMMh/FV 581.1). Most of the bone sutures of
DFMMh/FV 581.1 are completely closed, but some are
still discernible. The same specimen preserves both parie-
tals (DFMMh/FV 581.2 and 581.3), which are not fused
with the braincase or the frontals (see above). For descrip-
tive purposes, the braincase is oriented with the dorsal sur-
face of the occipital condyle horizontally positioned,
which is coincident with a horizontal position of the lat-
eral semicircular canal (Schmitt 2012). Further informa-
tion from individual braincase bones is based on isolated
elements, which also provides evidence of ontogenetic
changes.
Supraoccipital. Two of the six preserved supraoccipitals
(Fig. 13) are fused with surrounding skull elements in the
braincases (DFMMh/FV 581.1 and 1077). The other four
supraoccipitals were found isolated (DFMMh/FV 041,
723, 724 and 867.3), all being complete except specimen
DFMMh/FV 724. The isolated supraoccipitals do not
show enough reliable characters amongst each other to
make strong arguments for any staging from the ontoge-
netic perspective or to support any kind of morphotype
differences. The fused supraoccipitals and surrounding
bones likely belong to morphologically mature animals
(subadult or adult specimens).
The supraoccipital is a massive single bone that forms
the posterior roof of the endocranial cavity. The sutures
between this bone and the exoccipitals are closed, but are
still visible in occipital view (Fig. 13A). The supraoccipi-
tal is only slightly higher (2.71 cm) than the occipital con-
dyle (2.36 cm), which seems to be a consequence of the
relatively small foramen magnum of Europasaurus.
Whereas the exoccipitals surround 72% of the external
edges of the foramen magnum, the supraoccipital sur-
rounds 25% and the basioccipital, 3%. The supraoccipital
contacts the prootic anteriorly, leaving a shallow suture at
the union. Laterally throughout its height the supraoccipi-
tal articulates with the parietal in an almost vertical con-
tact, which terminates ventrally in a small but well-
marked notch. This notch gives support to the ventral pro-
cess of the parietal. A small foramen is present in the
deepest part of the notch, which opens internally into the
brain cavity. This foramen, the external occipital fenestra
for the caudal middle cerebral vein (Witmer & Ridgely
2009), mainly pierces the supraoccipital but its posterior
opening is dorsally bounded by the parietal (Fig. 13A).
Thus, as in other sauropods (e.g. Apatosaurus,Camara-
saurus; Witmer et al. 2008; Balanoff et al. 2010), the
external occipital fenestra is in the line of the suture
between the supraoccipital and the parietals. Laterodor-
sally, the supraoccipital is highly fused with the prootic,
which forms the ventral support for the parietal. Ventro-
laterally, the supraoccipital articulates with the exoccipi-
tal–opisthotic complex. The ventral surface of the
supraoccipital can be observed in the isolated supraoccipi-
tals (e.g. DFMMh/FV 867.3), being square-shaped and
with two well-defined facets. The anterior facet articulates
with the prootic, whereas the posterior facet articulates
with the exoccipital.
A lateromedially narrow but well-developed and poste-
riorly projected nuchal crest is present. In occipital view,
this crest is triangular (Fig. 13A). Starting as a wide pro-
jection, close to the foramen magnum, the crest ends in a
thin lamina at its dorsal end. When the parietals of this
braincase are articulated with the supraoccipital (see
above), a small but well-distinguishable posterior opening
is formed between the dorsal margin of the supraoccipital
and the ventral edge of the parietals (Fig. 13A). We
Cranial anatomy of the Late Jurassic dwarf sauropod Europasaurus holgeri 23
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