- Email: [email protected]
The titanosaurian dinosaur Atsinganosaurus velauciensis (Sauropoda) from the Upper Cretaceous of southern France: New material, phylogenetic affinities, and palaeobiogeographical implications
Accepted Manuscript The titanosaurian dinosaur Atsinganosaurus velauciensis (Sauropoda) from the Upper Cretaceous of southern France: New material, phylogenetic affinities, and palaeobiogeographical implications Verónica Díez Díaz, Géraldine Garcia, Xabier Pereda Suberbiola, Benjamin JentgenCeschino, Koen Stein, Pascal Godefroit, Xavier Valentin PII:
S0195-6671(18)30042-9
DOI:
10.1016/j.cretres.2018.06.015
Reference:
YCRES 3908
To appear in:
Cretaceous Research
Received Date: 31 January 2018 Revised Date:
2 May 2018
Accepted Date: 20 June 2018
Please cite this article as: Díez Díaz, Veró., Garcia, Gé., Pereda Suberbiola, X., Jentgen-Ceschino, B., Stein, K., Godefroit, P., Valentin, X., The titanosaurian dinosaur Atsinganosaurus velauciensis (Sauropoda) from the Upper Cretaceous of southern France: New material, phylogenetic affinities, and palaeobiogeographical implications, Cretaceous Research (2018), doi: 10.1016/j.cretres.2018.06.015. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
1
ACCEPTED MANUSCRIPT The titanosaurian dinosaur Atsinganosaurus velauciensis (Sauropoda) from the
2
Upper Cretaceous of southern France: new material, phylogenetic affinities, and
3
palaeobiogeographical implications
4
Verónica Díez Díaz 1,2, Géraldine Garcia 3, Xabier Pereda Suberbiola 4, Benjamin Jentgen-
5
Ceschino 5,6, Koen Stein 5,7, Pascal Godefroit 7, and Xavier Valentin 3,8
RI PT
1
6
1
7
43, 10115 Berlin, Germany;
8
2
Humboldt Universität, Berlin, Germany;
9
3
Laboratoire de Paléontologie, Evolution, Paléoécosystèmes et Paléoprimatologie (PALEVOPRIM,
M AN U
SC
Museum für Naturkunde, Leibniz-Institut für Evolutions-und Biodiversitätsforschung, Invalidenstraße
10
UMR7262 CNRS INEE), Université de Poitiers, 6, rue Michel-Brunet, 86073 Poitiers cedex, France;
11
4
12
Estratigrafía y Paleontología, Apartado 644, 48080 Bilbao, Spain;
13
5
Earth System Science – AMGC, Vrije Universiteit Brussel, Pleinlaan 2, 1050 Brussels, Belgium;
14
6
Evolution & Diversity Dynamics Lab, Liège University, Allée du six Août, 14, 4000 Liège, Belgium;
15
7
Directorate ‘Earth and History of Life’, Royal Belgian Institute of Natural Sciences, 1000 Brussels,
16
Belgium;
17
8
TE D
Universidad del País Vasco/Euskal Herriko Unibertsitatea, Facultad de Ciencia y Tecnología, Dpto.
EP
Palaios Association, 86300 Valdivienne, France.
AC C
18 19
Abstract
20
New remains of the titanosaurian sauropod Atsinganosaurus velauciensis from its Upper
21
Cretaceous type horizon and type locality in Velaux-La Bastide Neuve (Bouches-du-Rhône
22
Department, Provence) in southern France are described. This locality is considered to be
23
upper Campanian (Argiles et Grès à Reptiles Formation, Aix-en-Provence Basin). The new
24
material consists of skull fragments, including a partial braincase, isolated teeth, elements of
2
ACCEPTED MANUSCRIPT the axial skeleton (cervical, dorsal and caudal vertebrae, ribs), and appendicular bones
26
(scapula, humeri, ulna, metacarpals, ilia, ischia, femur, tibia, metatarsal). Histological
27
investigation shows that the analysed individuals were mature. The emended diagnosis of
28
Atsinganosaurus velauciensis includes a pubic peduncle of the ilium with a posterior concave
29
surface in its distal half, surrounded by two sharp ridges. Equations for predicting body mass
30
and size in sauropods suggest a body size up to 12 meters and a body mass of at least 3.5-5
31
tonnes for the largest individuals.
32
A phylogenetic analysis including 29 sauropod taxa was performed, with the European
33
titanosaurs Atsinganosaurus, Ampelosaurus, Lirainosaurus, Lohuecotitan, Paludititan (Late
34
Cretaceous) and Normanniasaurus (Early Cretaceous) all scored in the same analysis for the
35
first time. Atsinganosaurus and Ampelosaurus form a clade that is phylogenetically proximal to
36
Lirainosaurus within Lithostrotia – a clade here named Lirainosaurinae nov. – whereas
37
Lohuecotitan and Paludititan form a clade towards the base of Lithostrotia. Normanniasaurus
38
is resolved outside Lithostrotia, but within Titanosauria. From a palaeobiogeographical
39
perspective, the phylogenetic results suggest that European titanosaurs belong to at least
40
three distinct lineages and that two lithostrotian lineages were present during the latest
41
Cretaceous in the European archipelago.
42
Key Words: Atsinganosaurus, Lirainosaurinae, Titanosauria, Late Cretaceous, France,
43
palaeobiogeography
SC
M AN U
TE D
EP
AC C
44
RI PT
25
45
INTRODUCTION
46
Recent studies have shown that the biodiversity of European titanosaurian sauropods was
47
quite high during the Late Cretaceous, especially between the Campanian and early
48
Maastrichtian (see e.g. Díez Díaz et al., 2015, 2016; Fondevilla, 2017; Vila et al., 2012, 2016).
3
ACCEPTED MANUSCRIPT Five titanosaurian taxa have been described in Europe so far: Lirainosaurus astibiae, from the
50
upper Campanian of Laño and Chera, Spain (Sanz et al., 1999; Company et al., 2009; Díez Díaz
51
et al., 2011, 2012a, 2013a, 2013b, 2015); Lohuecotitan pandafilandi, from the upper
52
Campanian-lower Maastrichtian of Lo Hueco, Spain (Díez Díaz et al., 2016); Atsinganosaurus
53
velauciensis, from the upper Campanian of Velaux-La Bastide Neuve, France (Garcia et al.,
54
2010); Ampelosaurus atacis, from the lower Maastrichtian of Bellevue, France (Le Loeuff, 1995,
55
2005); and Paludititan nalatzensis, from the lower Maastrichtian of Nǎlaţ-Vad, Romania (Csiki
56
et al., 2010). However, their diversity was likely even higher:
59
SC
58
1) The status of Magyarosaurus, from the Maastrichtian of Romania, is still uncertain, and a revision of all the recovered material is needed (see Csiki et al., 2010).
M AN U
57
RI PT
49
2) Numerous isolated or poorly preserved titanosaurian remains were found in the Upper Cretaceous of southeastern France and northeastern Spain during the second half of
61
the 19th century and the 20th century. These remains were assigned to the species
62
Titanosaurus indicus and Hypselosaurus priscus (Matheron, 1869; Depéret, 1899;
63
Lapparent and Aguirre, 1956, 1957; Masriera and Ullastre, 1988), both now considered
64
nomina dubia (Le Loeuff, 1993; Wilson and Upchurch, 2003). This material also needs a
65
detailed revision.
68 69
EP
67
3) At several sites of Spain and southern France cranial, dental and appendicular elements representing more than one titanosaurian morphotype have been found
AC C
66
TE D
60
(Vila et al., 2012; Díez Díaz et al., 2012b, 2014, 2015; Páramo et al., 2015a, b).
Thus, at least seven titanosaurian taxa have so far been identified from the Campanian-
70
Maastrichtian of Europe. Detailed studies and comprehension of these last sauropod faunas,
71
especially in the Ibero-Armorican Island, is of great importance for understanding dinosaur
72
biodiversity in Europe, just before the Cretaceous-Palaeogene (K-Pg) event (see Csiki-Sava et
4
ACCEPTED MANUSCRIPT 73
al., 2015, Vila et al., 2016; Fondevilla et al., 2016) that led to the extinction of all non-avian
74
dinosaurs.
75
Atsinganosaurus velauciensis is represented by several partially articulated specimens, some of which were described by Garcia et al. (2010). In 2009 and 2012, renewed excavation
77
campaigns at the Velaux-La Bastide Neuve locality (Provence, France) led to the recovery of
78
more material (Figure 1). The specimens described in this publication derive from sequence 2
79
(Cincotta et al., 2015), as do the holotype and referred specimens of this taxon described in
80
Garcia et al. (2010). This sequence occurs in the Argiles et Grès à Reptiles Formation (Aix-en-
81
Provence Basin), which is upper Campanian. Dinosaur specimens represent 38% of the
82
vertebrate remains collected during the 2009 and 2012 campaigns in Velaux-La Bastide Neuve
83
(Cincotta et al. 2015), with most of these representing titanosaurs. The vertebrate fauna is
84
abundant and diversified including rhabdodontid dinosaurs (Matheronodon provincialis
85
[Godefroit et al. 2017] and Rhabdodon priscus), ankylosaurian remains, theropod teeth, the
86
ontogenetic cranial and postcranial elements of the eusuchian crocodyliform Allodaposuchus
87
precedens (Martin et al. 2016) , pleurodiran and cryptodiran turtle shells, an azhdarchid
88
pterosaur (Vullo et al. in press), hybodont shark teeth, and mawsoniid bones. Sequence 2
89
constitutes a coarse-grained conglomeratic sandstone lens. The fossil material was transported
90
over rather short distances and accumulated together within a river channel, in a fluvial
91
environment (Cincotta et al., 2015).
SC
M AN U
TE D
EP
AC C
92
RI PT
76
The discovery of abundant titanosaurian cranial and postcranial remains provides new
93
information on the French titanosaur Atsinganosaurus velauciensis, thereby facilitating the
94
emendation of its diagnosis, better definition of its morphological features, and more precise
95
assessment of its phylogenetic affinities. This will, in turn, enhance our understanding of the
96
palaeobiogeographical history of Late Cretaceous sauropod faunas.
97
5
ACCEPTED MANUSCRIPT 98
METHODOLOGY
99
Taxonomic description We use “Romerian” terms (Wilson, 2006) for anatomical structures (e.g. “centrum”, not
101
“corpus”) and their orientations (e.g. “anterior”, not “cranial’”). The landmark-based
102
terminology for vertebral laminae (Wilson, 1999) and fossae (Wilson et al., 2011) is used in the
103
discussion of vertebral anatomy and in Figures 3-5. For the identification of the caudal
104
vertebrae we follow suggestions made by Díez Díaz et al. (2013a). All measurements are
105
provided in Tables 1-5.
SC
For brevity and clarity, Atsinganosaurus velauciensis is mainly compared with
M AN U
106
RI PT
100
European titanosaurian taxa: Ampelosaurus atacis from Bellevue (Aude, France; Le Loeuff,
108
1995, 2005), Normanniasaurus genceyi from Le Havre (Normandy, France; Le Loeuff et al.,
109
2013), Lirainosaurus astibiae from Laño (Condado de Treviño, Spain; Sanz et al., 1999; Díez
110
Díaz et al., 2011, 2013a, b) and Chera (Valencia, Spain; Company et al., 2009; Díez Díaz et al.,
111
2015), Lohuecotitan pandafilandi from Lo Hueco (Cuenca, Spain; Díez Díaz et al., 2016),
112
Paludititan nalatzensis from Nǎlat-Vad (Haţeg Basin, Romania; Csiki et al., 2010), and the
113
material from the Haţeg Basin (Romania) referred to Magyarosaurus dacus (Nopcsa, 1915;
114
Huene, 1932) housed in the NHMUK. All the comparisons, except for Normanniasaurus genceyi
115
and Paludititan nalatzensis, are based on first-hand observations by the senior author (VDD).
116
However, several comparisons have been made with other titanosaurs on the basis of
117
important anatomical and phylogenetically important features that will help to distinguish
118
Atsinganosaurus and the other European taxa from other members within Titanosauria.
119
Histological methods
120
In order to determine the ontogenetic stage of the new specimens, we sampled humeri and
121
femora housed in the collection in the Moulin Seigneurial of Velaux (MMS/VBN.09.126,
AC C
EP
TE D
107
6
ACCEPTED MANUSCRIPT
MMS/VBN.09.A.018, and MMS/VBN.00.12 – see table 6). In addition, we also sampled two
123
very long (± 200 cm) and slender bony elements (MMS/VBN.09.51a and b), hypothesized to be
124
cervical ribs. The long bone specimens were core-sampled (diameter of 1 cm) at or near the
125
mid-shaft in posterior or anterior position, according to the standardized core location, when
126
possible (Stein and Sander 2009; Sander et al., 2011). A fragment of the rib was also sectioned
127
longitudinally and transversely to look for tendon fibres. Most of the cores broke during the
128
drilling process because of their low mineralization, but were glued and restored before thin
129
sectioning. All thin sections were prepared using standard lapidary methods with a thickness of
130
40 µm. Observations were made with an Olympus petrographic microscope, BX50F-3 model,
131
equipped with 5x and 10x objectives. Pictures were taken with a Leica camera and processed
132
in Leica Application suite.
133
Phylogenetic analysis
134
To establish the relationships of Atsinganosaurus, a phylogenetic analysis was performed using
135
the data matrix proposed by Salgado et al. (2015). This data matrix was analyzed using TNT 1.1
136
(Goloboff et al., 2008) to find the most parsimonious trees (MPTs). For the first time, all the
137
European taxa were included in the same analysis: Sallam et al. (2018) scored all the European
138
titanosaurs from the Campanian-Maastrichtian of Europe, but this is the first time that
139
Normannaisaurus is also included in the analysis. We have scored from first hand the European
140
titanosaurs Atsinganosaurus, Ampelosaurus, Lirainosaurus and Lohuecotitan, and
141
Normanniasaurus and Paludititan from the literature. We have also scored the titanosauriform
142
Malarguesaurus (González Riga et al., 2009) first-hand in order to enhance the resolution of
143
the relationships of basal forms. We used a heuristic tree search performing 1000 replications
144
of Wagner trees (using random addition sequences) followed by tree bisection reconnection
145
(TBR) as swapping algorithm, saving 100 trees per replicate. All characters were treated as
146
unordered and unweighted.
AC C
EP
TE D
M AN U
SC
RI PT
122
7
ACCEPTED MANUSCRIPT Institutional Abbreviations: FAM, Fox-Amphoux-Métisson, Mairie de Fox-Amphoux (Fox-
148
Amphoux Council), Fox-Amphoux, France; MCNA, Museo de Ciencias Naturales de
149
Álava/Arabako Natur Zientzien Museoa, Vitoria-Gasteiz, Spain; MDE, Musée des Dinosaures,
150
Espéraza, France; MMS/VBN, Musée Moulin Seigneurial /Velaux-La Bastide Neuve, Bouches-
151
du-Rhône, France; NHMUK, Natural History Museum, London, United Kingdom; UP, Université
152
de Poitiers, Vienne, France.
153
Anatomical Abbreviations: acdl, anterior centrodiapophyseal lamina; acpl, anterior
154
centroparapophyseal lamina; ADW, anterodorsal pterygoid wing; AVW, anteroventral
155
ectopterygoid wing; Bo, basioccipital; Bs, basisphenoid; cpol, centropostzygapophyseal lamina;
156
cprl, centroprezygapophyseal lamina; D, diapophysis; ICA, internal carotid artery; iped,
157
ischiadic peduncle; Ls+Os, laterosphenoid-orbitosphenoid complex; NS, neural spine; PA,
158
parapophysis; pcdl, posterior centrodiapophyseal lamina; pcpl, posterior centroparapophyseal
159
lamina; PO, postzygapophysis; pocdf, postzygocentrodiapophyseal fossa; podl,
160
postzygodiapophyseal lamina; posdf, postzygospinodiapophyseal fossa; posl, postspinal
161
lamina; pped, pubic peduncle; PR, prootic; prdl, posterior centrodiapophyseal lamina; PRE,
162
prezygapophysis; prsl, prespinal lamina; PVW, posteroventral quadrate wing; sdf,
163
spinodiapophyseal fossa; spof, spinopostzygapophyseal fossa; spol, spinopostzygapophyseal
164
lamina; sprf, spinoprezygapophyseal fossa; sprl, spinoprezygapophyseal lamina.
166
SC
M AN U
TE D
EP
AC C
165
RI PT
147
SYSTEMATIC PALAEONTOLOGY
167
Dinosauria Owen, 1842
168
Saurischia Seeley, 1887
169
Sauropoda Marsh, 1878
8
ACCEPTED MANUSCRIPT Titanosauriformes Salgado, Coria and Calvo, 1997
171
Titanosauria Bonaparte and Coria, 1993
172
Lithostrotia Upchurch, Barrett and Dodson, 2004
173
Lirainosaurinae new taxon
174
RI PT
170
Etymology. After the Spanish titanosaur Lirainosaurus astibiae.
176
Definition. Lirainosaurinae is phylogenetically defined as Lirainosaurus astibiae, Ampelosaurus
177
atacis, their common ancestor, and all of its descendants.
M AN U
178 179
SC
175
Atsinganosaurus velauciensis Garcia, Amico, Fournier, Thouand and Valentin, 2010
TE D
180
Holotype. UP/VBN.93.01.a–d: four articulated posterior dorsal vertebrae, housed in the
182
collections of the Université de Poitiers, France.
183
Referred specimens. Université de Poitiers, France: UP/VBN.93.12a–c: three cervical vertebrae;
184
UP/VBN.93.11: scapula; UP/VBN.93.10: metatarsal; UP/VBN.93.03-08: caudal vertebrae.
185
Musée Moulin Seigneurial /Velaux-La Bastide Neuve, France: MMS/VBN.02.03, 22 and 53:
186
teeth; MMS/VBN.02.78a–b: scapulocoracoid; MMS/VBN.02.99: isolated dorsal vertebra;
187
MMS/VBN.02.82: sacrum; MMS/VBN.02.109: tibia; MMS/VBN.02.110: caudal vertebra.
188
Musée Moulin Seigneurial /Velaux-La Bastide Neuve, France: MMS/VBN.00.12: humerus;
189
MMS/VBN.00.01-03: three caudal vertebrae.
AC C
EP
181
9
ACCEPTED MANUSCRIPT Muséum d’Histoire Naturelle d’Aix-en-Provence, France (donated by X. Valentin):
191
VBN.93.MHNA.99.21: tooth; VBN.93.MHNA.99.52: humerus; VBN.93.MHNA.99.32-34: caudal
192
vertebrae.
193
Type locality. La Bastide Neuve, Velaux; Aix-en-Provence Basin, Bouches-du-Rhône, France
194
(Figure 1A).
195
Type horizon. ‘Begudian’ (local stage) sandstones, upper Campanian, Upper Cretaceous (Garcia
196
et al. 2010, Cincotta et al., 2015).
SC
RI PT
190
197
Newly referred material. MMS/VBN.09.41: occipital condyle; MMS/VBN.09.167: braincase
199
fragment; MMS/VBN.09.158a: left pterygoid; MMS/VBN.93.33, MMS/VBN.12.A.006,
200
MMS/VBN.12.A.007, and MMS/VBN.12.B.014: four teeth; UP/VBN.93.13a and b,
201
MMS/VBN.09.D.007a, MMS/VBN.12.A.004, MMS/VBN.12.B.010, MMS/VBN.12.B.015: six
202
cervical vertebrae; UP/VBN.93.02, MMS/VBN.93.32, UP/VBN.09.157: three dorsal vertebrae;
203
MMS/VBN.93.31a, MMS/VBN.93.32b, MMS/VBN.00.14, MMS/VBN.00.15, MMS.VBN.09.46,
204
MMS/VBN.09.54, MMS/VBN.09.159b, MMS/VBN.09.D.003, MMS/VBN.09.D.009,
205
MMS/VBN.09.D.010, MMS/VBN.09.D.011, MMS/VBN.12.33, MMS/VBN.12.B.013a,
206
MMS.VBN.12.B.013b, MMS/VBN.12.B.018, MMS/VBN.12.C.003, MMS/VBN.12.C.004:
207
seventeen caudal vertebrae; MMS/VBN. 93.31b and MMS/VBN.93.32b: two haemal arches;
208
MMS/VBN.09.51a and b: two cervical ribs; MMS/VBN.09.D.07b and MMS/VBN.09.D.007c: two
209
dorsal ribs; MMS/VBN.09.66: sacral rib; MMS/VBN.09.124D: scapula; MMS/VBN.09.A.018: left
210
humerus; MMS/VBN.12.P.06a: right ulna; MMS/VBN.09.D.001: radius; MMS/VBN.09.113,
211
UP/VBN.93.09: two metacarpals; MMS/VBN.12.32: ilion; MMS/VBN.09.51c: right ischium;
212
MMS/VBN.09.126: right femur; MMS/VBN.02.90: left tibia; MMS/VBN.09.132: fibula.
AC C
EP
TE D
M AN U
198
10
ACCEPTED MANUSCRIPT 213
The fossil material is labelled and housed in the municipality palaeontological and
214
archaeological structures of Velaux, under the care of the research association Palaios, and is
215
property of the department CD (Conseil Départemental) 13.
216 Emended diagnosis. Pubic peduncle of the ilium with a posterior concave surface in its distal
218
half, surrounded by two sharp ridges. Recovered local autapomorphies from the phylogenetic
219
analysis: i) anterior and middle cervical vertebrae without pleurocoels (character #22), ii) ratio
220
between the anteroposterior length/height of posterior face of the posterior cervical
221
vertebrae higher than 3 (character #29), and iii) prominent ulnar olecraneon process,
222
projecting above the proximal articulation (character #61). None of the features of the former
223
diagnosis from Garcia et al. (2010) can longer be regarded as diagnostic for Atsinganosaurus
224
velauciensis.
M AN U
SC
RI PT
217
225 DESCRIPTION
227
Skull
228
Three skull fragments (Fig. 2) have been unearthed: an occipital condyle (MMS/VBN.09.41), a
229
right portion of the braincase (MMS/VBN.09.167), and a probable left pterygoid
230
(MMS/VBN.09.158a)
231
Occipital condyle. MMS/VBN.09.41 (Figure 2E) is a robust occipital condyle with a rounded
232
outline. The neck is not preserved, and the foramen for the hypoglossal nerve (XII) can only be
233
seen on the right side in dorsolateral view. It is a single opening, as seen in most titanosaurian
234
taxa (Paulina Carabajal, 2012; Poropat et al., 2016).
235
Braincase. MMS/VBN.09.167 seems to be a right fragment of a braincase, with portions of the
236
basioccipital, basisphenoid, prootic, and laterosphenoid (Figure 2A and B). However, this is a
AC C
EP
TE D
226
11
ACCEPTED MANUSCRIPT tentative identification, as no sutures are visible – there is a high level of fusion between the
238
bones – and all the foramina for the cranial nerves and fenestrae are collapsed. However,
239
some structures can be identified: grooves for the trigeminal (V) and facial (VII) nerves, and the
240
crista prootica in lateral view; the channel for the internal carotid artery in the basisphenoid;
241
and several grooves along the medial surface of the prootic, probably related with brain or
242
cranial nerve structures. The grooves for cranial nerves V and VII more closely resemble those
243
on the partial braincase MCNA 7439, referred to Lirainosaurus (Díez Díaz et al., 2011), than
244
those observed on the specimen FAM 03.064 from Fox-Amphoux-Métisson referred to
245
Titanosauria indet. (Díez Díaz et al., 2012b). Besides this, no more detailed comparisons can be
246
made due to the poor preservation of the specimen from Velaux.
247
Pterygoid. MMS/VBN.09.158a is a fragmentary skull bone that probably belongs to a left
248
pterygoid (Figure 2C and D). It is a flat triradiate element, the ends of which are not completely
249
preserved. Pterygoids have only been described in the titanosaurs Nemegtosaurus (Nowinski,
250
1971), Quaesitosaurus (Kurzanov and Bannikov, 1983), Rapetosaurus (Curry Rogers and
251
Forster, 2004), Tapuiasaurus (Zaher et al., 2011, Wilson et al., 2016), and Sarmientosaurus
252
(Martínez et al., 2016). MMS/VBN.09.158a shares its general morphology with them, like its
253
plate-like morphology (with its three processes coplanar), that seems to be a diagnostic
254
character within Titanosauria (Poropat et al., 2016). The lateral surface of MMS/VBN.09.158a
255
is slightly convex, and the medial one is flat. The anterodorsal pterygoid wing is the longest of
256
the three wings because of its preservation. It narrows distally, and forms an angle of 90° with
257
the anteroventral ectopterygoid wing. The anteroventral ectopterygoid wing becomes more
258
robust towards its distal end, forming an anterior bulge for the contact with the ectopterygoid.
259
In lateral view, at the junction between the three wings, a broken surface probably
260
corresponds to the lateral depression for contact with the palatine. The posteroventral
261
quadrate wing is not complete and poorly preserved. It forms an angle of ca. 130° with the
262
anterodorsal wing. Laterally, a shallow depression on the posteroventral quadrate wing marks
AC C
EP
TE D
M AN U
SC
RI PT
237
12
ACCEPTED MANUSCRIPT
the contact with the quadrate. No pterygoid remains have been described in other European
264
titanosaurians so far.
265
Teeth
266
Four new teeth have been found (MMS/VBN.12.A.006 and 07, MMS/VBN.12.B.014 and
267
MMS/VBN.93.33) (Figure 2F, Table 1). They are similar to those previously described in
268
Atsinganosaurus (see Garcia et al., 2010 and Díez Díaz et al., 2013c). They are peg-like, with
269
cylindrical crowns and a tapered tip. The lingual surface is flat, and the labial one convex. The
270
apex is slightly inclined lingually. An apical wear facet is present, with and angle of 60° in
271
relation with the apicobasal axis of the crown. This angle is similar to the ones calculated for
272
most of the titanosaurian teeth found in the Ibero-Armorican Island (see Díez Díaz et al. 2012a,
273
b, 2014). The enamel is smooth, with smooth longitudinal lines. The mesial and distal ridges
274
are more prominent in the distal third of the crown. There are no denticles or carinae present.
275
They clearly differ from other titanosaurian teeth described from the Ibero-Armorican Island
276
(see Díez Díaz et al. 2013c and 2014 for a more detailed comparison). These new teeth have a
277
similar SI (SI mean of the sample: 4.49) as the other teeth ascribed to Atsinganosaurus (SI
278
mean: 4.15; see Díez Díaz et al., 2013c). MMS/VBN.12.A.006 has a more slender and slightly
279
more labiolingually compressed crown than the other preserved teeth of Atsinganosaurus.
280
Cervical vertebrae
281
Six cervical vertebrae have been recovered, belonging to the anterior, middle and posterior
282
sections of the neck. All of them display the same general morphology as those originally
283
described by Garcia et al. (2010) (Figure 3A-C and E, Table 2). The centra are opisthocoelous,
284
with camellate internal texture, characteristic for Titanosauriformes (Upchurch, 1998; Wilson,
285
2002; Wedel, 2003; Upchurch et al., 2004; D'Emic, 2012). The prezygapophyses extend
286
anterior to the anterior tip of the condyle, contrary to some derived lithostrotians (Poropat et
287
al., 2016). Analyzing the changes on the EI we can elucidate a pattern in the cervical series: the
AC C
EP
TE D
M AN U
SC
RI PT
263
13
ACCEPTED MANUSCRIPT
centra shorten their length through the anterior to middle cervicals, becoming longer again in
289
the posterior ones, being even more transversally compressed than the first ones (although
290
this could be also due to preservation).
291
Anterior cervical vertebra. MMS/VBN.12.A.004, MMS/VBN.12.B.015 and MMS/VBN.09.D.007a
292
(this one found associated with two dorsal ribs) are anterior cervical vertebrae (Figure 3D, F
293
and G). The first one is the best preserved, but the main features are shared by all elements.
294
The left side of MMS/VBN.12.A.004 (Figure 3G) misses the tuberculum of the cervical rib, but
295
this structure is preserved in the right side of the specimen, together with a fragment of the
296
cervical rib (see below for a more detailed description). The centrum is long and has a sub-
297
quadrangular cross-section, especially its posterior half. The posterior ventral surface is flat,
298
whereas the anterior one is concave. The lateral surfaces, which are flat posteriorly and
299
concave anteriorly, do not present pneumatic foramina, contrary to Lohuecotitan (Díez Díaz et
300
al., 2016) and Magyarosaurus (NHMUK R. 4898). None of the specimens preserve the
301
postzygapophyses. The diapophyses and parapophyses are located on the anterior half of the
302
centrum. The parapophysis is located below the centrum. The dorsal surface of the
303
parapophysis is not excavated, but a shallow fossa is present on the lateral surface of the
304
centrum, above the parapophysis, in MMS/VBN.12.B.010 (Fig. 4C and C’). The prezygapophysis
305
is wide and robust, anterodorsally directed, and does not diverge too much from the centrum.
306
The neural spine is not completely preserved in any of them; it seems to be a single, laterally
307
compressed structure with a simple lamination. The lamination is the same that presumably
308
can be found in most sauropod cervical vertebrae: acpl, pcpl, pcdl, prdl in the centra, and podl,
309
sprl and spol in the spine. No acdl, prsl or posl are present. The fossae between these laminae
310
are very shallow with the exception of the spof, which is narrow and deep.
311
Middle to posterior cervical vertebrae. UP/VBN.93.13a and b were found in anatomical
312
connection. Because they are still embedded in the matrix, most of the structures on their
AC C
EP
TE D
M AN U
SC
RI PT
288
14
ACCEPTED MANUSCRIPT
right side cannot be seen. Both present the same general morphology, also together with the
314
anterior cervicals, but these are smaller and more slender. The cross-section of the centra is
315
more circular. The ventral surfaces of the centra are concave anteriorly and flat posteriorly, as
316
in Ampelosaurus. The diapophyses and parapophyses are better developed laterally, and the
317
parapophyses are slightly ventrally placed with respect to the centra. Both are still located on
318
the anterior half of the centra. The tubercula and capitula are preserved, but not the cervical
319
ribs. The prezygapophyses are only preserved in UP/VBN.93.13b; they are short and wide, and
320
directed anterodorsally. The postzygapophyses are broad, teardrop-shaped structures, whose
321
articulations are directed ventrally and slightly laterally. The single neural spines are higher,
322
and have a triangular outline in lateral view. There is a rugose thickening in the distal half of
323
the neural spine, maybe for tendinous attachment. The laminae and fossae complexes are
324
more developed than on the anterior cervicals: besides the laminae also present in the
325
anterior cervicals, the single cprl and cpol can be seen, together with an accessory lamina that
326
divides vertically a shallow posterior fossa below the pcdl. Shallow fossae are developed on
327
the dorsal surfaces of the parapophyses and below the diapophyses; on the lateral surfaces of
328
the centra, two additional fossae (anterior and posterior – the latter divided by an accessory
329
lamina) are present. The fossae on the neural spines are deeper than in the other European
330
titanosaurs (but not like the ones present in the Argentinean taxon Mendozasaurus, that are
331
even delimited by sharp-lipped laminae [González Riga et al., 2018]), like the triangular pocdf
332
between the pcdl and the podl, the sdf above the podl, and the spof.
333
Posterior cervical vertebra. Garcia et al. (2010) described three posterior cervical vertebrae:
334
UP/VBN.93.12a–c . Besides the new cervical found, we figure these three vertebrae again,
335
detailing the lamina and fossae complexes (Figure 3A-C and E). The new posterior cervical,
336
MMS/VBN.12.B.010 (Figure 4), is the smallest of the sample and the most posterior one, as
337
indicated by its shorter and lower centrum and its higher neural spine. In general terms, this
338
vertebra presents the same features as the other five cervicals. Although there is some
AC C
EP
TE D
M AN U
SC
RI PT
313
15
ACCEPTED MANUSCRIPT taphonomic deformation, we suggest that the centrum had a circular cross-section. The
340
ventral face of the centrum is also anteriorly concave and posteriorly flat. The ribs are missing,
341
but the diapophyses and parapophyses are preserved and ventrally directed. In this specimen,
342
the parapophyses are more anteriorly located on the centrum than the diapophyses, which are
343
located in the middle part of the centrum. The prezygapophyses are not well-preserved, but it
344
can be inferred that they were more anterodorsally directed than on the anterior cervicals.
345
Only the right postzygapophysis is preserved and dorsolaterally directed. There is also a rugose
346
thickening on the distal half of the neural spine, directed posterodorsally from the
347
postzygapophysis. The laminae are thicker than in the other cervicals, and the fossae are
348
slightly shallower than on the middle to posterior cervicals, with the exception of the lateral
349
pneumatic foramina, which are better developed on this vertebra. The posterior cervical
350
vertebra MDE C3-265, referred to Ampelosaurus, also has lateral pneumatic foramina. In
351
addition, the anterior side of the neural spine of MMS/VBN.12 B.010 has two sprls that define
352
a deep and narrow sprf between themselves. The posterior spof is similarly deep and narrow,
353
delimited by the spols. Ampelosaurus (MDE C3-265) also possesses a deep spof; however, this
354
fossa is much wider than in Atsinganosaurus, as is its neural spine overall. The cervicals of
355
Ampelosaurus also present a prsl (Le Loeuff, 2005).
SC
M AN U
TE D
EP
356
RI PT
339
The conservative pattern of the lamina and fossa complexes within the cervical series is noteworthy. This pattern is not present on the dorsal and sacral vertebrae, and different
358
patterns may occur in the same (right and left features) or in different individuals. This also
359
occurs in the vertebrae of Atsinganosaurus described by Garcia et al. (2010), and in the
360
titanosauriform Giraffatitan brancai (Wedel and Taylor, 2013; VDD pers. obs.).
361
Cervical ribs
362
A fragmentary cervical rib, probably a right one, is associated with MMS/VBN.12 A.004 (Figure
363
3G). The preserved fragment is slender, with the same width along most of its length (ca. 1.6
AC C
357
16
ACCEPTED MANUSCRIPT
cm). The lateral face is flat. However, we cannot infer the section of the specimen because it is
365
still hidden in the rock matrix. The preserved length is ca. 30 cm.
366
Dorsal vertebrae
367
None of the new dorsal vertebrae are completely preserved, but they closely resemble those
368
already described by Garcia et al. (2010) (see also Díez Díaz et al., 2013a, fig. 9C for the
369
laminae and fossae complexes and the comparison of UP/VBN.93.01b with other European
370
titanosaurs) (Figure 5A-C; Table 2). MMS/VBN.93.32 (Figure 5A) is an anterior neural arch
371
lacking the spine, UP/VBN.09.157 (Figure 5B) is a poorly preserved centrum with the base of
372
the neural arch, and UP/VBN.93.02 (Figure 5C) is a fragment of the left half of a middle to
373
posterior dorsal (in which the neural canal is not clearly visible, as it is obliterated). The dorsal
374
centra are opisthocoelous, with lateral eyed-shaped pleurocoels (set within a fossa), as in
375
other European titanosaurian taxa except Paludititan (Csiki et al., 2010; Díez Díaz et al., 2013a,
376
fig. 9). UP/VBN.09.157 likely had a ventral keel, unlike other European taxa. The inner
377
structure of the centra cannot be observed in any of the specimens, although the camellate
378
internal tissue is present in the anterior neural arch MMS/VBN.93.32. In this latter specimen,
379
the prezygapophyses are short and directed anterodorsally, but its posterior surface is
380
completely eroded. The neural canal is small and circular. The prezygapophyses are better
381
developed and laterally directed in Lirainosaurus (MCNA 7445; Díez Díaz et al., 2013a).
382
Although their distal ends are missing, the diapophyses are oriented dorsolaterally. Some
383
laminae can be seen in this specimen: single cprl, the base of the left sprl, pcdl, and podl. The
384
left pocdf and posdf are deep. The main difference between this specimen and Lirainosaurus
385
(MCNA 7445) is the presence of an acdl in the latter. In UP/VBN.93.02, the diapophyses appear
386
to be better developed and more robust. The postzygapophyses are small and their articular
387
surfaces face ventrally. The cpols are single, slender and vertical laminae. A pocdf is also
388
developed between the pcdl, the cpol, and the broken podl, and the posdf is shallower. In this
AC C
EP
TE D
M AN U
SC
RI PT
364
17
ACCEPTED MANUSCRIPT
specimen, only the base of the neural spine is preserved. In UP/VBN.09.157, a different lamina
390
pattern can be seen: together with the pcdl, an acdl is present and between them a triangular
391
fossa is present. In addition, as no matrix is present between the cpol and the pcdl, we observe
392
that the pocdf was so deep that it reached the inner structure of the neural arch, confirming
393
that these dorsal vertebrae were highly pneumatized. These lamina and fossa complexes are
394
also present in a posterior dorsal of Ampelosaurus (MDE C3-247). As in UP/VBN.93.02, the
395
posterior dorsals of Lirainosaurus are devoid of an acdl. However, the lateral pneumatic
396
foramina of this Iberian titanosaur are smaller. The main differences with the dorsal vertebrae
397
of Lohuecotitan are found on the ventral surface of the centrum, the laminae and fossae
398
complexes, and the development of the diapophyses (Díez Díaz et al., 2016, fig. 2. C-E).
399
Paludititan does not present a podl, but in general, its laminae and fossae complexes are more
400
complex than those of Atsinganosaurus.
401
Dorsal and sacral ribs
402
Two dorsal ribs (Figure 5D-G) were found associated with the anterior cervical vertebra
403
MMS/VBN.09.D.07a. They are flat (plank-like) and slender, although an important level of
404
crushing should be taken into account. One of them (the longest one: MMS/VBN.07.D.07b,
405
preserved length 58.5 cm) shows part of its tuberculum and capitulum separated by a
406
concavity. The preserved length of the other (MMS/VBN.09.D.007c) is 56 cm. No evidences on
407
pneumaticity can be assessed because of their preservation.
408
Only one fragmentary sacral rib (MMS/VBN.09.66) was recovered. It is probably one of first
409
ones from the left side, because of the development of a transverse foramen. In the sacrum
410
described by García et al. (2010), only the first three preserved sacrals present a transverse
411
foramen between the centra and the ribs. This element is anteroposteriorly compressed and
412
its acetabular arm is not completely preserved. Both costovertebral junctions with the
413
diapophysis and the parapophysis are preserved, although their ends are broken off. The
AC C
EP
TE D
M AN U
SC
RI PT
389
18
ACCEPTED MANUSCRIPT
capitulum is more slender than the tuberculum, which is bifurcated distally. The area between
415
the tuberculum and the capitulum (the transverse foramen sensu Wilson, 2011) is highly
416
concave.
417
Sacrum
418
The sacrum MMS/VBN.02.82 (Figure 6) was already described by Garcia et al. (2010), so here
419
we will point out some details that are not present in the former work.The ventral surfaces of
420
the sacral vertebrae present a ventral keel (Figure 6C). This sacrum is a robust and well-fused
421
specimen, as stated by huge fusion of the centra and neural spines, but also the presence of
422
thickened flat dorsal surfaces in the tuberculum of the sacral ribs. These surfaces are well-
423
differentiated from the rest of the sacral rib (Figure 6A and D). The laminae and fossae
424
complexes do not have the same patterns through all the sacral series, and are not even
425
symmetrical. A supraspinous rod (Figure 6A) runs distally through all the neural spines, as seen
426
in many other derived sauropods (see e.g. Cerda et al., 2015, fig. 7). Indeed, this rod could be a
427
diagnostic feature within Titanosauria (Poropat et al., 2016).
428
Caudal vertebrae
429
Seventeen new caudal vertebrae have been recovered (Figures 7 and 8, Table 2). All of them
430
are procoelous (with some exceptions in the posterior caudal vertebrae, that become slightly
431
amphicelous, like in MMS/VBN.93.32a [Figure 7V-X], UP/VBN.93.03 and UP/VBN.93.04 [Figure
432
8F-G]), a condition typically found in Lithostrotia (e.g. Salgado et al., 1997; Upchurch et al.,
433
2004; D’Emic, 2012). The presence of non-procoelous posterior caudal vertebrae
434
(amphicoelous, opisthocoelous and biconvex) has been found in other lithostrotian
435
titanosaurs, like Rinconsaurus caudamirus (Calvo and González Riga, 2003; VDD, pers. obs.) or
436
Opisthocoelicaudia skarzynskii (Borsuk-Białynicka, 1977). Their neural arches are placed
437
anteriorly on their centra, as in Titanosauriformes (e.g. Salgado et al., 1997; Wilson, 2002;
438
Upchurch et al., 2004), and are vertically oriented as in most lithostrotians (Carballido et al.,
AC C
EP
TE D
M AN U
SC
RI PT
414
19
ACCEPTED MANUSCRIPT 2017). As in most somphospondylans, these caudals do not present a hyposphenic ridge
440
(Upchurch et al., 2004, Carballido et al., 2011).
441
Anterior caudal vertebrae. Six anterior caudal vertebrae are preserved (MMS/VBN.93.31a
442
[Figure 7J-K], MMS/VBN.00.14 [Figure 7A-E], MMS/VBN.00.15 [Figure 7F-I], MMS.VBN.09.46,
443
MMS/VBN.09.54 [Figure 8B], MMS/VBN.12.C.004 [Figure 8A]). The broken surfaces of
444
MMS/VBN.09.54 allow observation of the camellate internal tissue of the centrum. None of
445
them have transverse processes, instead possessing lateral bulges located dorsally on the
446
centrum, close to the junction with the neural arch. This, together with the simple neural
447
spine, indicates a relatively more posterior position along the anterior caudal series, probably
448
close to the middle section of the tail. The centra are strongly procoelous with a well-
449
developed condyle, which is not constricted unlike in Lirainosaurus (Díez Díaz et al., 2013a) and
450
Lohuecotitan (Díez Díaz et al., 2016). In addition, this condyle is located in the middle of the
451
posterior articulation, which is not the case in Normanniasaurus and Paludititan, whose
452
condyles are dorsally displaced on the centra. The centrum of MMS/VBN.12 B.004 is sub-
453
quadrangular in cross-section, as in the caudal vertebrae found in Chera (Spain) and referred
454
to an indeterminate titanosaurian distinct from Lirainosaurus (see Díez Díaz et al., 2015), but
455
unlike other European titanosaurs. However, it is important to highlight that this is the only
456
similarity with the caudals of the second taxon from Chera. Longitudinal ridges are present in
457
the most anterior caudals (Figure 7D and H), and become less developed in the next ones in
458
the series. No longitudinal ridges or midline grooves are developed along the ventral face of
459
the posterior anterior centra (Figure 7Q), this is also the case in Lirainosaurus. The articular
460
surface for the the haemal arches is poorly preserved. MMS/VBN.12 B.004 lacks the right
461
prezygapophysis and the neural spine. The prezygapophyses of both specimens are directed
462
slightly anterodorsally, and the one of MMS/VBN.09.54 is broader. The neural spine is an
463
anteroposteriorly short, transversely-compressed, and slightly posterodorsally-directed
464
lamina. It is proportionally lower than the neural spines of the anterior caudals of
AC C
EP
TE D
M AN U
SC
RI PT
439
20
ACCEPTED MANUSCRIPT Lohuecotitan, and does not present the interzygapophyseal fossa seen in Normanniasaurus.
466
The postzygapophyses are triangular surfaces located posteriorly on the neural spine. They
467
closely resemble those described by Garcia et al. (2010). We consider that MMS/VBN.02.110 is
468
an anterior caudal because of the presence of transverse processes.
469
Anterior to middle caudal vertebrae. Three fragmentary middle caudals have been recovered:
470
MMS/VBN.09.D.009, MMS/VBN.09.D.011, MMS/VBN.12.B.018. Their morphology (procoelous
471
centra, low neural arches, and long and horizontal prezygapophyses) is not particularly
472
noteworthy within Titanosauria. Their ventral surfaces do not present any longitudinal ridges
473
or midline grooves, like in the anterior caudal vertebrae.
474
Posterior caudal vertebrae. Eight posterior caudal vertebrae have been found:
475
MMS/VBN.93.32a (Figure 7V-X), MMS/VBN.09.159.b (Figure 8E), MMS/VBN.09.D.003 (Figure
476
7R-U), MMS/VBN.09.D.010, MMS/VBN.12.B.013a, MMS/VBN.12.B.013b, MMS/VBN.12.C.003
477
(Figure 8C), MMS/VBN.12.33. Only MMS/VBN.12 B.013a and b were found associated. These
478
vertebrae are procoelous (with some exceptions, as seen above), unlike the shorter and
479
amphiplatyan centra on the posterior caudals of Paludititan. Their condyle is less developed
480
than on the anterior caudals, unlike in Lirainosaurus and Lohuecotitan, in which the posterior
481
caudals still have a constricted condyle located slightly dorsally on the posterior articular
482
surface of the centra (Díez Díaz et al., 2013a, fig. 6; Díez Díaz et al., 2016, fig. 3). The centra are
483
longer than the anterior caudals, but shorter dorsoventrally. The ventral surface of
484
MMS/VBN.09.159b is flat, and its articular surface for the haemal arches is prominent as in
485
Lohuecotitan (Díez Díaz et al., 2016). A ridge marks the junction between the neural arch and
486
the centrum, as also observed on the middle and posterior caudal vertebrae of Alamosaurus
487
(Gilmore, 1946), Ampelosaurus (Le Loeuff, 2005), Andesaurus (Mannion and Calvo, 2011),
488
Baurutitan (Kellner et al., 2005), Narambuenatitan (Filippi et al., 2011), and Normanniasaurus
489
(Le Loeuff et al., 2013). The neural spine is only preserved in MMS/VBN.12 B.013a; it is a
AC C
EP
TE D
M AN U
SC
RI PT
465
21
ACCEPTED MANUSCRIPT simple, laterally compressed lamina, more anteroposteriorly extended than in the anterior
491
caudals. In the other posterior caudals, the neural arch is incipient. The prezygapophyses are
492
long and slender, and almost horizontal. The postzygapophyses are located on the
493
posterodorsal tip of the neural spine, forming a triangular articular surface. These vertebrae
494
are different from the posterior caudals described by Garcia et al. (2010). However, because of
495
its dorsoventral compression and the presence of articulations for the haemal arches,
496
VBN.93.MHNA.99.33 is probably a middle to posterior caudal vertebra. We consider
497
MMS/VBN.93.3-8, described by Garcia et al. (2010), as distal caudal vertebrae because of their
498
typical spool-like morphology and the absence of neural arches. These six caudals were found
499
almost articulated.
500
Haemal arches
501
MMS/VBN.93.31b (Figure 7L-M) and MMS/VBN.93.32b (Figure 8Y-Z) are two haemal arches
502
found associated with the caudal vertebrae MMS/VBN.93.31a and MMS/VBN.93.32a
503
respectively. Both are open Y-shaped, as in most macronarians (Wilson, 2002; Curry Rogers,
504
2005; Mannion and Calvo, 2011; Otero et al., 2012). The haemal canal does not reach the
505
middle of the total length of both arches, contrary to the ones referred to Paludititan. The
506
distal blades are transverselly flattened distally, contrary to Lirainosaurus. Although the
507
proximal articular faces are not completely preserved it is visible that they are not divided in
508
two articular faces, as the ones of Lohuecotitan.
509
Pectoral girdle
510
Scapula. Besides the fragmentary scapulocoracoid (MMS/VBN.02.78a–b, Figure 9A-B) and the
511
scapula (MMS/VBN.93.11, Figure 9C), previously described by Garcia et al. (2010), another
512
fragmentary right scapula (Figure 9D) has been found, which likely belonged to a juvenile
513
individual (MMS/VBN.09.124D). It consists of the proximal third of the scapular blade and part
514
of the acromial blade. Its medial surface is concave (no ridges or prominences present),
AC C
EP
TE D
M AN U
SC
RI PT
490
22
ACCEPTED MANUSCRIPT
whereas its lateral side is convex, with a rounded and longitudinal ventral ridge. No triangular
516
processes on the ventral margin are present.
517
Forelimb
518
Humerus. MMS/VBN.00.12 (Figure 10A-D) is a right humerus, and MMS/VBN.09.A.018 (Figure
519
10E-H, Table 3) a left one This second one has poorly preserved proximal and distal edges and
520
deltopectoral crest. Their diaphyses are slender and anteroposteriorly compressed. The
521
posterior surface is convex, and the anterior one concave. No bulges or tuberosities are
522
present in the posterior surface of the proximal third of MMS/VBN.09.A.018, contrary to
523
MMS/VBN.00.12, which presents a tuberosity close to the lateral margin of the posterior
524
surface, at approximately the level of the distal tip of the deltopectoral crest. This tuberosity
525
was probably for the insertion of m. latissimus dorsi (Borsuk-Bialynicka, 1977; Otero, 2010;
526
D’Emic, 2012) No other prominences or ridges are visible or present in the anterior and
527
posterior surfaces of these specimens. The distal edge of the deltopectoral crest is located
528
above the middle of the diaphysis, as in Lirainosaurus, Ampelosaurus, and Magyarosaurus (Le
529
Loeuff, 2005; Díez Díaz et al. 2013b; VDD pers. obs.). The deltopectoral crest doubles its
530
thickness distally, and it is slightly deflected medially. The diaphysis of this specimen seems
531
more slender than in other European titanosaurs. A more detailed comparison is not possible
532
due to the preservation of the proximal and distal ends of the specimen. However, the
533
slenderness of the diaphysis (ECC [eccentricity index, sensu Wilson and Carrano, 1999]: 3.76)
534
and the relative development and position of the deltopectoral crest resemble the condition in
535
MMS/VBN.00.12 (ECC: 3.14), described by Garcia et al. (2010) as belonging to Atsinganosaurus
536
(figure 6A). VBN.93.MHNA.99.52 is a fragmentary right humerus (Figure 10I-J) that was not
537
described by Garcia et al. (2010). The anterior surface is not well-preserved, the proximal end
538
is eroded and the distal extremity is lost. The posterior surface is better preserved, but no
539
special features can be seen.
AC C
EP
TE D
M AN U
SC
RI PT
515
23
ACCEPTED MANUSCRIPT
Ulna. MMS.VBN.12.P.06a is a slender right ulna (Figure 10K-P), Table 3), with a broad proximal
541
end. This end has a triradiate outline (forming an angle of almost 90° between the longest
542
arms, which are not completely preserved), although its articular surface is not preserved. The
543
posterior process is well-developed. The olecranon process is better developed than in
544
Lirainosaurus and the ulna C3-1296 of Ampelosaurus, more closely resembling the condition in
545
C3-1490. The well-developed proximal processes delimit three shallow surfaces that extend
546
along the diaphysis up to the distal extremity, which is only slightly expanded and not
547
completely preserved (the presence of an anteromedial fossa for the reception of the radius
548
cannot be assessed).
549
Radius. MMS/VBN.09.D.001 (Figure 10Q-R) is a fragmentary diaphysis of a radius, and has a
550
cylindrical cross-section. No more features can be described due to its poor preservation.
551
Metacarpals. Only two metacarpals I (MMS/VBN.09.113 and UP/VBN.93.09) have been
552
recovered (Figure 11, Table 4); the second specimen is much smaller, likely belonging to an
553
immature individual. Both specimens are poorly preserved, and their proximal and distal ends
554
are missing. MMS/VBN.09.113 was probably a left metacarpal, as suggested by the position of
555
its articular surface for metacarpal II. The diaphyses are long and anteroposteriorly
556
compressed, as in Bonatitan (Salgado et al., 2015) and Rapetosaurus (Curry Rogers, 2009),
557
contrasting with the metacarpals of Magyarosaurus, which have a more rounded cross-
558
section. Metacarpal I of Epachthosaurus (Martínez et al., 2004) is more robust, and its
559
diaphysis is not compressed. The diaphyses are straight, as in the derived titanosaurs
560
Bonatitan, Epachthosaurus, Rapetosaurus, and Opisthocoelicaudiinae (Apesteguía, 2005) and
561
unlike the bowed morphology in the basal taxa Andesaurus (Mannion and Calvo, 2011),
562
Antarctosaurus (Huene, 1929), Argyrosaurus (Mannion and Otero, 2012), and Malawisaurus
563
(Gomani, 2005). The proximal and distal ends are mediolaterally expanded; the proximal end is
564
also anteroposteriorly compressed, as in other titanosaurs, e.g. Andesaurus and Rapetosaurus.
AC C
EP
TE D
M AN U
SC
RI PT
540
24
ACCEPTED MANUSCRIPT Pelvic girdle
566
Ilium. One fragmentary right ilium is preserved (MMS/VBN.12.32) (Figure 12A-B). It consists of
567
the dorsal part of the acetabulum, ventral fragments of the pre- and postacetabular processes
568
of the iliac blade, and the pubic peduncle. The preacetabular process is slightly horizontal
569
(more than in other titanosaurs) and laterally projected, and has a ventral ridge that ends
570
above the acetabulum, contrary to the ilia of Lirainosaurus and Lohuecotitan, which have a
571
vertical preacetabular lobe. The postacetabular process is vertical. The pubic peduncle
572
(anteroposterior length: 7.8 cm; transversal length: 8.7 cm) is robust, becomes broader
573
towards its distal end, and has a C-shaped cross-section. The posterior surface of the distal half
574
of the peduncle is particularly concave and surrounded by two sharp ridges. This morphology is
575
not known in any other titanosaur, and is consequently considered as an autapomorphy of
576
Atsinganosaurus. The lateral ridge extends through the dorsal edge of the acetabulum and
577
runs through the ventral edge of the preacetabular lobe. There is no triangular hollow at the
578
base of the pubic peduncle, contrary to Lirainosaurus (Díez Díaz et al., 2013b). The acetabulum
579
is not as strongly concave as it is in Paludititan. Both ilia are pneumatized, as in Lirainosaurus
580
(Díez Díaz et al., 2013b), Diamantinasaurus (Poropat et al. 2015) and derived titanosaurs (see
581
Cerda et al., 2012). However, this could be a synapomorphy of a more inclusive clade than just
582
Titanosauria, as Euhelopus also has pneumatized ilia (see Wilson and Upchurch, 2009;
583
Mannion et al., 2013).
584
Ischium. One right ischium (MMS/VBN.09.51c) has been recovered (Figure 12C-E, Table 5). The
585
iliac peduncle is incompletely preserved, its distal edge is missing. The plate-like morphology of
586
this element, and the absence of an emargination along the anterior margin of the ischiadic
587
blade, are common features in titanosaurs (Wilson, 2002; Upchurch et al., 2004; González Riga
588
et al., 2009). The acetabular margin is almost flat, as also observed in Ampelosaurus (Le Loeuff,
589
2005, Fig. 4.17), and it is not well differentiated from the iliac peduncle. This feature is
AC C
EP
TE D
M AN U
SC
RI PT
565
25
ACCEPTED MANUSCRIPT interesting to analyze more carefully, as an acute acetabular margin is a diagnostic feature
591
within Lithostrotia (see D’Emic, 2012). Both Atsinganosaurus and Ampelosaurus are grouped
592
together in our phylogenetic analysis (see below), so maybe we are talking about a diagnostic
593
feature within these French taxa. The iliac peduncle is slender and well developed, contrasting
594
with the wider and more robust peduncles in Ampelosaurus and Paludititan. The pubic
595
peduncle is poorly preserved, but seems continuous with the anteroventral edge of the
596
ischium. The ischia of Ampelosaurus and Paludititan are boomerang-shaped and their pubic
597
peduncle is well differentiated from their distal blade. At the base of the iliac peduncle, a
598
lateral tubercle (with a groove associated, as in Titanosauriformes [Poropat et al., 2016]) is
599
present near the posterior edge of the proximal part of the blade. This lateral ridge could
600
correspond to the bulge interpreted by Borsuck-Białynicka (1977) as the attachment point for
601
m. flexor tibialis internus III (see also Poropat et al., 2015). This lateral tubercle or tuberosity
602
seems to be a diagnostic feature within Titanosauria (Carballido et al., 2017). At about the
603
middle of the ischiadic blade, near its ventral margin, a lateral ridge is present. The ischiadic
604
blade is a straight plate, whose thickness decreases towards its distal edge.
605
Hindlimb
606
Femur. MMS/VBN.09.126 is the diaphysis of a right femur (Figure 13A-B, Table 3). Its proximal
607
and distal extremities are not preserved, but a low and poorly developed fourth trochanter is
608
present posteromedially, as in Lirainosaurus and Ampelosaurus, and contrasting with the more
609
centrally-situated fourth trochanter in Lohuecotitan. The diaphysis seems wider than in the
610
Spanish taxa, but more lateromedially developed than in Ampelosaurus (e.g. C3-87).
611
Tibia. MMS/VBN.02.90 is a left tibia (Figure 13C-H, Table 3). This bone was previously
612
identified as a metacarpal by Garcia et al. (2010), but it is highly similar as MMS/VBN.02.109
613
(although this last specimen is larger [Figure 13K-P]). This bone is slender, with an expanded
614
proximal third and a distal extremity with a triangular outline in distal view. Both articular
AC C
EP
TE D
M AN U
SC
RI PT
590
26
ACCEPTED MANUSCRIPT
surfaces are poorly preserved, but the shallow surface of the anterolaterally-projected cnemial
616
crest can be observed. No “tuberculum fibularis” can be seen in the internal face of the
617
cnemial crest. A second cnemial crest is absent too, as is the case of most somphospondylans
618
and diplodocoids (Mannion et al., 2013). Its proximal end appears compressed as in
619
Lirainosaurus, contrasting with the more rounded ones in Lohuecotitan and Ampelosaurus.
620
Distally, a prominent anteromedial ridge delimits two concave surfaces, as in Lirainosaurus
621
(MCNA 2203).
622
Fibula. MMS/VBN.09.132 is the proximal third of a fibula (Figure 13I-J, Table 3). It is more
623
expanded than the diaphysis and slightly lateromedially compressed, as in Lirainosaurus and
624
Ampelosaurus, and unlike in Lohuecotitan. Its lateral surface is convex, whereas its poorly
625
preserved medial surface is flat to slightly concave. The lateral trochanter is not preserved.
626
Metatarsal. The left metatarsal I (UP/VBN.93.10; Figure 14, Table 4) was only briefly described
627
by Garcia et al. (2010). It is a robust element, with expanded proximal and distal edges. Its
628
shaft is more slender than in other titanosaurs (e.g. Rapetosaurus, Epachthosaurus [Martínez
629
et al., 2014], Bonitasaura [Gallina and Apesteguía, 2015], Notocolossus [González Riga et al.,
630
2016], or Mendozasaurus [González Riga et al., 2018]). Its proximal surface is quadrangular in
631
outline. The proximal and distal medial surfaces are slightly concave for articulation with
632
metacarpal II. The distal articular surface is poorly preserved, but apparently had a comma-
633
shaped outline. In lateral view, a ridge extends from the middle of the shaft down to the
634
posterior edge of the distal articular surface. It also presents a prominent ventrolateral
635
expansion along its distal half, such that the distal end expands further laterally than the
636
proximal end.
AC C
EP
TE D
M AN U
SC
RI PT
615
637 638
HISTOLOGICAL OBSERVATIONS
27
ACCEPTED MANUSCRIPT 639
All Atsinganosaurus sections display a similar bone histology, dominated by heavy remodelling
640
of the primary bone and several cross-cutting generations of secondary osteons (sensu Stein et
641
al., 2010 and Mitchell et al., 2017; Figure 15A-B). No pristine in situ trabecular structures can be identified because the transition
643
between the medullary cavity and the innermost cortex is abrupt and goes from broken
644
trabeculae (sometimes embedded in sediments [Figure 15C]) to crushed, distorted secondary
645
osteons.
SC
RI PT
642
The secondary osteons are mature, rounded to elliptical in shape, and composed of
647
successive layers of alternating bone lamellae (as seen under cross polarized light, type two
648
osteons sensu Ascenzi and Bonucci, 1968; Figure 15A). The elliptical osteons have the long axis
649
preferentially oriented parallel to the periosteal surface in transverse section, a feature also
650
seen in other titanosaurs (e.g. Phuwiangosaurus sirindhornae and Ampelosaurus atacis in Klein
651
et al., 2009 and Klein et al., 2012a respectively). In long bones of A. velauciensis, four to five
652
generations of secondary osteons can be recognized in the innermost cortex, five to six
653
generations in the mid-cortex and four to six generations in the outer cortex (see Table 6
654
below for details – Fig. 15B). No open resorption cavities were observed in the innermost
655
cortex in any of the samples. Instead, the innermost cortex is often characterized by irregular
656
secondary osteons which are found with broken trabeculae. MMS/VBN.09.126 and
657
MMS/VBN.09.A.018 are the best sections showing the broken trabeculae.
TE D
EP
AC C
658
M AN U
646
All samples except MMS/VBN.09.A.018 show some patches of primary tissue. These
659
patches are mostly confined to the outer cortex. However, no unambiguous primary vascular
660
canals can be seen in any of these patches. It is possible that the outermost µm of the cortical
661
samples are missing because of weathering or mechanical preparation.
662 663
Following Klein and Sander (2008) and Stein et al. (2010), the studied specimens match the Histologic Ontogenetic Stage (HOS) 14 because of the complete remodelled type H bone
28
ACCEPTED MANUSCRIPT 664
tissue of the cortices (Fig. 15A, E and F). Dense secondary osteons are clearly visible even
665
macroscopically as purple dots in Fig. 15E. Given the multiple cross-cutting secondary osteon
666
generations throughout the cortex, the Remodelling Stages (RS) (sensu Mitchell et al., 2017)
667
are ranging from RS 13 to 14. Longitudinal sections (Figure 15D-F) were made to complement data from the
RI PT
668
transverse sections, in particular to verify any preferential orientation of the secondary
670
osteons. Their oval shape in transverse section could be either the result of a section plane at a
671
slight angle to the ideal transverse section (Mitchell et al., 2017) or of the 3D geometry of the
672
osteons not correlating to the long bone axis. The osteonal boundaries are more difficult to
673
see, and so are the different cross-cutting generations. The cortices yield a widespread
674
remodelled histology with very elongated secondary osteons meaning they are mainly
675
oriented along the long bone axis (purple lines in Fig. 15F). Some secondary osteons have an
676
ellipsoid appearance, which implies they are oriented oblique to the long bone axis.
M AN U
The histology of a putative cervical rib (MMS/VBN.09.51a and b) is characterized by
TE D
677
SC
669
strong remodelling features, and only a small part of the original ossified tendon matrix is still
679
present (Figure 16). Numerous tensile secondary osteons (sensu Ascenzi and Bonuci, 1968)
680
with smooth cement lines make up the most significant part of the tissue, some of them
681
showing cross-cutting relations. However, interstitially, small areas remain unremodelled and
682
show densely packed collagen fibre bundles, similar to those in the ossified tendons of
683
hadrosaurs (Adams and Organ, 2005; Organ and Adams, 2005) and elongated cervical ribs of
684
other sauropod dinosaurs (Cerda, 2009; Klein et al., 2012b).
685
AC C
EP
678
In a longitudinal section (Figure 16), the longitudinal vascular canals of the secondary
686
osteons are dominant features, and the osteons have longitudinally oriented osteocyte
687
lacunae with faint but numerous branching canaliculi. In between the longitudinally oriented
29
ACCEPTED MANUSCRIPT 688
osteons, fibre bundles with fibrocyte lacunae can be observed. These features complement the
689
cross sectional view and are furthermore reminiscent of ossified tendons.
690
Taking into account the strongly elongated morphology, parallel occurrence in the sediment and ossified tendinous histology of the two described elements, there can be little
692
doubt that they represent the ossified tendons of sauropod cervical ribs.
RI PT
691
693
695
PHYLOGENETIC ANALYSIS
SC
694
The result of this phylogenetic analysis with 29 sauropod taxa yielded a single MPT of 166 steps, with a consistency index (CI) of 0.572 and a retention index (RI) of 0.665 (Figure 17).
697
The general topology is similar to the one obtained by Salgado et al. (2015), but with two main
698
differences: i) the diagnosis of Lithostrotia has been resolved, with Malawisaurus placed in a
699
more derived position than Andesaurus (and therefore within Titanosauria); ii) the derived
700
clade Saltasauridae has been divided, with Opisthocoelicaudiinae regarded as a more basal
701
group than Saltasaurinae (this split can be also seen in the analysis of Sallam et al. 2018).
702
Another notable difference with previous phylogenetic analyses is the recovery of
703
Lognkosauria within Rinconsauria. Similar results were obtained by González Riga et al. (2018),
704
resolving Lognkosauria as the sister taxon of Rinconsauria. The phylogenetic relationships of
705
this clade seem more difficult to solve, as it has been placed as a basal clade within Lithostrotia
706
(Calvo et al., 2007, González Riga et al., 2009), or as more derived lithostrotians (González Riga
707
et al., 2016) related with Aeolosaurini (González Riga and Ortiz, 2014) or with Rinconsauria
708
(Salgado et al., 2015). However, this discussion is beyond the scope of this paper; herein, we
709
focus on the relationships between the European taxa.
710 711
AC C
EP
TE D
M AN U
696
European taxa were almost completely neglected in previous titanosaurian phylogenies: Sallam et al. (2018) include all of the Late Cretaceous European taxa, but before
30
ACCEPTED MANUSCRIPT
this work only few included Lirainosaurus and Ampelosaurus together (see e.g. Powell, 2003;
713
Curry Rogers, 2005), and most of the time separately or scored only from the literature (see
714
e.g. González Riga, 2003; Upchurch et al., 2004; Bonaparte et al., 2006; Calvo et al., 2007;
715
González Riga et al., 2009; Hocknull et al., 2009; Csiki et al., 2010). As previously suggested by
716
Bonaparte et al. (2006), González Riga et al. (2009), Gallina and Apesteguía, (2011), Salgado et
717
al. (2015), and Sallam et al. (2018), the present analysis recovers Lirainosaurus as a member of
718
Lithostrotia, whereas it was regarded as a derived titanosaur more closely related to
719
Saltasauridae by Upchurch et al. (2004), Calvo et al. (2007), Csiki et al. (2010), and Filippi et al.
720
(2011), or even a member of the saltasaurid clade by Hocknull et al. (2009) and Díez Díaz et al.
721
(2013d). In our analysis, Lirainosaurus appears as a lithostrotian closely related to a clade
722
formed by the French titanosaurs Ampelosaurus and Atsinganosaurus. This clade is here
723
named Lirainosaurinae nov. Both French titanosaurs have been included in a few analyses
724
(only together in Sallam et al. (2018)), and their relationships have not been well studied (e.g.
725
Powell, 2003; Curry Rogers, 2005; Sallam et al. 2018). Díez Díaz et al. (2013d) suggested that
726
French titanosaurs were basal lithostrotians and that Lirainosaurus a member of
727
Opisthocoelicaudiinae. However, Díez Díaz (2013) scored these three titanosaurs in two
728
previously published matrices (Bonaparte et al., 2006; González Riga et al., 2009), and in both
729
phylogenetic hypotheses the three taxa appeared closely related. Lohuecotitan and Paludititan
730
are grouped together as basal lithostrotians. The phylogenetic affinities of Paludititan are not
731
well resolved (Csiki et al., 2010), and Lohuecotitan has only been scored in Díez Díaz et al.
732
(2016) and Sallam et al. (2018), so few comments can be made here, besides the lack of
733
affinities of Lirainosaurus with the French taxa. The Early Cretaceous French taxon
734
Normanniasaurus is nested within Titanosauria, but not within Lithostrotia.
AC C
EP
TE D
M AN U
SC
RI PT
712
735 736
DISCUSSION
31
ACCEPTED MANUSCRIPT
After the detailed study and comparison of the specimens published by Garcia et al. (2010) and
738
the ones described in this work, an emended diagnosis of A. velauciensis is suggested. The new
739
diagnosis focuses on the ilium: pubic peduncle of the ilium with a posterior concave surface in
740
its distal half, surrounded by two sharp ridges. Three isolated humeri (the most recurring non-
741
axial bone in the site) have been found, so at least three individuals of Atsinganosaurus are
742
present at Velaux-La-Bastide Neuve. However, besides the holotype, no other remains were
743
found associated or articulated, so their referral to each individual it is not possible. It should
744
be noted that further titanosaurian remains have been found at Velaux-La Bastide Neuve and
745
they present several divergences (especially humeri and an ulna) with the holotype and
746
material referred to Atsinganosaurus velauciensis by Garcia et al. (2010). The remains ascribed
747
to this possible new taxon were most of them found in the same level as the ones belonging to
748
Atsinganosaurus, with the exception of one almost complete sacrum and a humerus, that
749
were recovered from a second level (2 meters above the former one). This new material is
750
currently under study.
751
Estimation of Body Size and Mass for Atsinganosaurus velauciensis
752
As we have recovered several humeri and femora we can hypothesize the body size and mass
753
for Atsinganosaurus. For the body mass and size we have used the equations proposed by
754
Seebacher (2001) for size, and Packard et al. (2009) and Campione and Evans (2012) for mass,
755
in which M(g) = 3.352PerH+F2,125, M(kg) = 214.44L(m)1.46, and logM(g) = 2.754logPerH+F −
756
1.097, where M: body mass, PerH+F: sum of the perimeters of the humerus and femur in mm,
757
L: body length. With the smallest humerus and femur we obtain a size of 6.45 meters, and a
758
mass of 2.46 tonnes (sensu Packard et al., 2009) and 3.2 tonnes (sensu Campione and Evans,
759
2012), whereas with the largest specimens the results are 14.54 meters, and 3.661 tonnes
760
(sensu Packard et al., 2009) and 5.26 tonnes (sensu Campione and Evans, 2012).
AC C
EP
TE D
M AN U
SC
RI PT
737
32
ACCEPTED MANUSCRIPT 761
We tentatively propose a body length of ca. 8-12 meters for the adults of Atsinganosaurus, or as much as 14 meters for the largest individuals, and a body mass of ca.
763
3.5-5 tonnes. Although it is a sauropod of small size, it probably doubled (or even tripled) the
764
length of Lirainosaurus (4 meters and 2-4 tonnes, Díez Díaz et al., 2013b).
765
Ontogeny and Dwarfism
766
In general, all sampled specimens of A. velauciensis show very similar histological features.
767
Clearly, the samples do not represent a growth series and are all of comparable developmental
768
stages. The histology of A. velauciensis is comparable to that of the small European titanosaurs
769
Lirainosaurus astibiae (adult specimen descriptions in Company, 2011, fig. 5) and
770
Magyarosaurus dacus (Stein et al., 2010).
SC
M AN U
771
RI PT
762
Heavy remodelling is the main histological pattern in the long bones of A. velauciensis. This mature histology suggests that these individuals were fully grown. Considering the
773
reduced size of the femur and humeri, the remodelling process would have begun early in the
774
ontogeny of this titanosaur compared to non-titanosaurian sauropods, at a rate that surpassed
775
the apposition rate. This is consistent with the histology of juveniles of the titanosaur
776
Rapetosaurus krausei (Rogers et al., 2016). If the haversian bone deposition rate is assumed to
777
be constant throughout ontogeny (Mitchell and Sander, 2014), the combination of a slow
778
apposition rate with heavy remodelling prior to the final size involves some kind of size
779
reduction and/or insular dwarfism comparable to other titanosaurs in the Cretaceous
780
European archipelago (e.g. Lirainosaurus astibiae, Magyarosaurus dacus; Company, 2011;
781
Stein et al., 2010).
AC C
EP
TE D
772
782 783
Palaeobiogeographical considerations
33
ACCEPTED MANUSCRIPT 784
Our new phylogenetic results shed light on the palaeobiogeographical patterns of the
785
titanosaurian faunas from the Ibero-Armorican Island. With these results we can suggest two
786
different scenarios:
787
1) Csiki-Sava et al. (2015) commented that European titanosaurs do not seem to have a southern influence, but in our analysis we have found that Lohuecotitan and
789
Paludititan are grouped together close to the basal African lithostrotian Malawisaurus.
790
Works on the Cretaceous titanosaurian faunas from Africa (see Gorscak et al. 2014,
791
2017; Lamanna et al., 2017; and works in progress) will help to clarify soon the
792
relationships of these faunas with the Late Cretaceous European ones. Indeed, the
793
titanosaur Mansourasaurus from the Late Cretaceous of Egypt seems to be closely
794
related to Lohuecotitan (Sallam et al., 2018), supporting sauropod dispersal between
795
Europe and Africa in the terminal Cretaceous. Therefore, a Gondwanan influence
796
cannot be discarded; this has been also previously posited for other groups of reptiles
797
(Pereda Suberbiola, 2009).
SC
M AN U
TE D
798
RI PT
788
2) The case of the more derived lithostrotians Lirainosaurus and the French taxa
800
Ampelosaurus and Atsinganosaurus is likely different. This group, here named
801
Lirainosaurinae, could lead to a possible endemicity in the Ibero-Armorican Island, and
802
that is why Lirainosaurus (late Campanian) and the French titanosaurs (late
804
AC C
803
EP
799
Campanian-early Maastrichtian) appear to be closely related. As Pereda et al. (2009)
and Mannion and Upchurch (2011) suggested, Late Cretaceous European dinosaurs
805
could be relictual lineages of Laurasian faunas, and Lirainosaurinae could be a good
806
example of this. It is also possible that the late Maastrichtian taxa found in the
807
Pyrenean region (northern Spain and southern France) and southeastern France (i.e.
808
Vitrolles la Plaine, Valentin et al., 2012) evolved from these titanosaurs known from
809
late Campanian–early Maastrichtian faunas.
34
ACCEPTED MANUSCRIPT 810
These hypotheses represent a solid foundation for future phylogenetic and
811
palaeobiogeographical analyses incorporating the Cretaceous European titanosaurian faunas,
812
following on from palaeobiogeographic analyses primarily focused on titanosaurs from
813
elsewhere (e.g. Gorscak et al. 2016; Poropat et al. 2016).
RI PT
814 CONCLUSIONS
816
In this work we describe new titanosaurian cranial and postcranial remains found in the Upper
817
Cretaceous site of Velaux-La Bastide Neuve (southern France), which are referred to
818
Atsinganosaurus velauciensis. This new material has allowed us to better define the
819
morphological features of this taxon and emend its diagnosis, thereby helping us to better
820
understand the sauropod faunas that inhabited the Ibero-Armorican Island.
M AN U
SC
815
Long bones of Atsinganosaurus velauciensis are heavily remodelled (HOS 14, RS
822
ranging from stage 13 to 14). The sampled specimens of A. velauciensis were fully grown. The
823
small size but mature nature of the specimens might be linked to insular dwarfism, as seen in
824
Magyarosaurus or Lirainosaurus. However, Atsinganosaurus was larger than these two taxa, as
825
shown by its hypothesized body size and mass: ca. 8-12 meters for the adults, or as much as 14
826
meters for the largest individuals, and ca. 3.5-5 tonnes.
EP
AC C
827
TE D
821
A phylogenetic analysis with 29 sauropod taxa was performed, with the European
828
titanosaurs Atsinganosaurus, Ampelosaurus, Lirainosaurus, Lohuecotitan, Paludititan (Late
829
Cretaceous) and Normanniasaurus (Early Cretaceous) all scored for the same analysis for the
830
first time. Atsinganosaurus and Ampelosaurus form a clade closely related to Lirainosaurus
831
within Lithostrotia, whereas Lohuecotitan and Paludititan are grouped together as basal
832
lithostrotians. Lirainosaurinae is defined here for the first time as Lirainosaurus astibiae,
833
Ampelosaurus atacis, their common ancestor, and all of its descendants. Atsinganosaurus
35
ACCEPTED MANUSCRIPT 834
velauciensis appears within this clade, as sister taxon of Ampelosaurus. As for
835
Normanniasaurus, it is nested within Titanosauria but not within Lithostrotia. From a palaeobiogeographical perspective, the phylogenetic results suggest that
837
European titanosaurs belong to at least three distinct lineages and that two lithostrotian
838
lineages were present during the latest Cretaceous in the European archipelago. Although the
839
“African origin” of the latest Cretaceous re-invasion of Europe is not well-supported by other
840
groups of tetrapods (see Mannion and Upchurch, 2011 and references therein), the results
841
obtained in this work and the one published by Sallam et al. (2018) shed some light on one
842
possible dispersal route between North Africa and Europe during the Cenomanian–Campanian.
843
More works on the African titanosaurs are needed to test if these African faunas are closely
844
related with other South American titanosaurian clades, as previously hypothesized by
845
Mannion and Upchurch (2011). On the other hand, Lirainosaurinae could be a relictual lineage
846
of Laurasian sauropod faunas. To assess these hypotheses more inclusive (with more Late
847
Cretaceous Laurasian taxa, together with the African and European ones) phylogenetic and
848
paleobiogeographical should be done.
SC
M AN U
TE D
849
RI PT
836
The diversity of the titanosaurian faunas from the Late Cretaceous of Europe, and more specifically from the Ibero-Armorican Island, has been an important research issue since
851
the last years of the 19th century (see e.g. Le Loeuff, 1993), always suggesting a higher
852
diversity than previously thought. According to the findings of these last years, especially in
853
Spain, France, and Romania, this diversity has been increased to, at least, seven titanosaurian
854
taxa in the Campanian-Maastrichtian of Europe. However, new findings and reanalyses of
855
previously published material will no doubt increase this further.
AC C
EP
850
856 857
ACKNOWLEDGMENTS
36
ACCEPTED MANUSCRIPT
M. Moreno-Azanza (Universidade Nova de Lisboa, Portugal) helped in the development of the
859
phylogenetic analysis. VDD would like to thank V. Fondevilla (ICP, Spain) for the useful
860
discussions on titanosaurian faunas and stratigraphy. We would like to acknowledge A.
861
Montaufier for the photographs (with financial support of the Lisea-Vinci group), and C. Zafra
862
for editing the figures. We thank J. C. Corral and J. Alonso (Museo de Ciencias Naturales de
863
Álava/Arabako Natur Zientzien Museoa, Vitoria-Gasteiz, Spain), B. Madarieta (Museo Vasco de
864
Historia de la Medicina y de las Ciencias of Leioa, Spain), F. Ortega (Grupo de Biología
865
Evolutiva, Universidad Nacional de Educación a Distancia, Spain), J. Le Loeuff (Musée des
866
Dinosaures d’Espéraza, France), P. Barrett (Natural History Museum, U.K.), and B. González
867
Riga (IANIGLA, CRICyT, Mendoza, Argentina) for access to collections under their care. The Willi
868
Hennig Society sponsors the use of the TNT cladistics software. Research work of XPS was
869
supported by the Ministerio de Economía y Competitividad of Spain (MINECO, project
870
CGL2017-85038-P), the European Regional Development Fund, the Gobierno Vasco/Eusko
871
Jaurlaritza (research group IT-1044-16) and the Universidad del País Vasco (UPV/EHU, research
872
group PPG17/05), and works of BJ by the FRIA grant. BJ-C thanks J. Laval for producing the thin
873
sections for histological purposes, V. Fischer for his useful critics on the long bone histology
874
part, and J. Jentgen for having helped a lot to produce the histological figures. We are greatly
875
indebted to P.M. Mannion (UCL, UK) and S.F. Poropat (Swinburne University of Technology,
876
Hawthorn, Australia), which provided useful comments that helped improving this work. This
877
work has been developed thanks to the collaboration between Palaios (research association in
878
which XV is the president), the University of Poitiers, the Velaux Municipality (J.-P. Maggi and
879
L. Melhi) with its heritage, culture and technical services (M. Calvier, and S. Chauvet), the
880
environment department from CD 13 (M. Bourrelly, T. Tortosa, G. Michel, N. Mouly, and S.
881
Amico), the ‘Service Départemental d’Incendie et de Secours’ (SDIS 13), and numerous
882
volunteers during the field campaigns in 2009 and 2012. This work was supported by the
883
Ministry of Education and Communication (research grant VR1013 to Palaios association), the
AC C
EP
TE D
M AN U
SC
RI PT
858
37
ACCEPTED MANUSCRIPT 884
Bouches du Rhône department CD 13 proposals MAPADGAC23112010-1 and
885
MAPADGAC16012014-1-AAPC).
886 REFERENCES
888
Adams, J., Organ, C.L. 2005. Histologic determination of ontogenetic patterns and processes in
889
hadrosaurian ossified tendons. Journal of Vertebrate Paleontology 25(3), 614-622.
RI PT
887
SC
890
Apesteguía, S. 2005. The evolution of the titanosaurian metacarpus. In: Tidwell, V., Carpenter,
892
K. (Eds.), Thunder-Lizards. The Sauropodomorph Dinosaurs. Indiana University Press,
893
Bloomington and Indianapolis pp. 321-345.
M AN U
891
894
Ascenzi, A., Bonucci, E. 1968. The compressive properties of single osteons. The Anatomical
896
Record: Advances in Integrative Anatomy and Evolutionary Biology 161(3), 377-391.
897
TE D
895
Bonaparte, J.F., Coria, R.A. 1993. Un nuevo y gigantesco saurópodo titanosaurio de la
899
Formación Río Limay (Albiano-Cenomanio) de la Provincia del Neuquén, Argentina.
900
Ameghiniana 30, 271-282.
AC C
901
EP
898
902
Bonaparte, J.F., González Riga, B.J., Apesteguía, S. 2006. Ligabuesaurus leanzai gen. and sp.
903
nov. (Dinosauria, Sauropoda), a new titanosaur from the Lohan Cura Formation (Aptian, Lower
904
Cretaceous) of Neuquén, Patagonia, Argentina. Cretaceous Research 27, 364–376.
905
38
ACCEPTED MANUSCRIPT
Borsuk-Białynicka, M. 1977. A new camarasaurid sauropod Opisthocoelicaudia skarzynskii gen.
907
n., sp. n. from the Upper Cretaceous of Mongolia. Palaeontologia Polonica 37, 5–64.
908
Calvo, J.O., Porfiri, J.D., González-Riga, B.J., Kellner, A.W.A. 2007. A new Cretaceous terrestrial
909
ecosystem from Gondwana with the description of a new sauropod dinosaur. Anais da
910
Academia Brasileira de Ciências 79(3), 529-541.
911
RI PT
906
Campione, N.E., Evans, D.C. 2012. A universal scaling relationship between body mass and
913
proximal limb bone dimensions in quadrupedal terrestrial tetrapods. BMC Biology 10(1), 60.
SC
912
M AN U
914
Carballido, J.L., Pol, D., Otero, A., Cerda, I.A., Salgado, L., Garrido, A.C., Ramezani, J., Cúneo,
916
N.R., Krause, J.M. 2017 A new giant titanosaur sheds light on body mass evolution among
917
sauropod dinosaurs. Proceedings of the Royal Society of London B 284, 20171219.
TE D
915
918
Carballido, J.L., Rauhut, O.W.M., Pol, D., Salgado, L. 2011. Osteology and phylogenetic
920
relationships of Tehuelchesaurus benitezii (Dinosauria, Sauropoda) from the Upper Jurassic of
921
Patagonia. Zoological Journal of the Linnean Society 163, 605-662. DOI: 10.1111/j.1096-
922
3642.2011.00723.x
AC C
923
EP
919
924
Cerda, I.A. 2009. Consideraciones sobre la histogénesis de las costillas cervicales en los
925
dinosaurios saurópodos. Ameghiniana 46, 193-198.
926
39
ACCEPTED MANUSCRIPT 927
Cerda, I.A., Casal, G.A., Martinez, R.D., Ibiricu, L.M. 2015 Histological evidence for a
928
supraspinous ligament in sauropod dinosaurs. Royal Society Open Science 2, 150369. DOI:
929
10.1098/rsos.150369
RI PT
930 931
Cerda, I.A., Salgado, L., Powell, J.E. 2012. Extreme postcranial pneumaticity in sauropod
932
dinosaurs from South America. Paläontologische Zeitschrift 86(4), 441-449.
SC
933
Cincotta, A., Yans, Y., Godefroit, P., Garcia, G., Dejax, J., Benammi, M., Amico, S., Valentin, X.
935
2015. Integrated paleoenvironmental reconstruction and taphonomy of a unique Upper
936
Cretaceous vertebrate–bearing locality (Velaux, southeastern France). PlosOne.
937
DOI:10.1371/journal.pone.0134231
938
M AN U
934
Company, J., Pereda Suberbiola, X., Ruiz-Omeñaca, J.I. 2009. Nuevos restos fósiles del
940
dinosaurio Lirainosaurus (Sauropoda, Titanosauria) en el Cretácico Superior (Campaniano-
941
Maastrichtiano) de la Península Ibérica. Ameghiniana 46(2), 391-405.
EP
942
TE D
939
Csiki, Z., Codrea, V., Jipa-Murzea, C., Godefroit, P. 2010. A partial titanosaur (Sauropoda,
944
Dinosauria) skeleton from the Maastrichtian of Nălaţ-Vad, Haţeg, Basin, Romania. Neues
945
Jahrbuch für Geologie und Paläontologie Abhandlungen 258(3), 297-324.
946
AC C
943
947
Csiki-Sava, Z., Buffetaut, E., Ösi, A., Pereda-Suberbiola, X., Brusatte, S.L. 2015. Island life in the
948
Cretaceous - faunal composition, biogeography, evolution, and extinction of land-living
949
vertebrates on the Late Cretaceous European archipelago. ZooKeys 469, 1-161. DOI:
950
10.3897/zookeys.469.8439
951
40
ACCEPTED MANUSCRIPT 952
Curry Rogers, K. 2005. Titanosauria. A phylogenetic overview. In: Curry Rogers, K., Wilson, J.A.
953
(Eds.), The Sauropods: Evolution and Paleobiology. University of California Press, Berkeley pp.
954
50-103.
955 Curry Rogers, K. 2009. The postcranial osteology of Rapetosaurus krausei (Sauropoda:
957
Titanosauria) from the Late Cretaceous of Madagascar. Journal of Vertebrate Paleontology
958
29(4), 1046-1086.
RI PT
956
SC
959
Curry Rogers, K.A., Forster, C. 2004. The skull of Rapetosaurus krausei (Sauropoda:
961
Titanosauria) from the Late Cretaceous of Madagascar. Journal of Vertebrate Paleontology 24,
962
121–144.
M AN U
960
963
D'Emic, M.D. 2012. The early evolution of titanosauriform sauropod dinosaurs. Zoological
965
Journal of the Linnean Society 166, 624-671. DOI: http://dx.doi.org/10.1111/j.1096-
966
3642.2012.00853.x
967
TE D
964
D’Emic, M.D., Wilson, J.A., Williamson, T.E. 2011. A sauropod dinosaur pes from the latest
969
Cretaceous of North America and the validity of Alamosaurus sanjuanensis (Sauropoda,
970
Titanosauria). Journal of Vertebrate Paleontology 31, 1072-1079.
AC C
971
EP
968
972
Depéret, C. 1899. Aperçu sur la géologie du Chaînon de Saint-Chinian. Bulletin de la
973
Société Géologique de France 3(27), 686-709.
974 975
Díez Díaz, V. 2013. Revisión del dinosaurio saurópodo Lirainosaurus astibiae
41
ACCEPTED MANUSCRIPT 976
(Titanosauria) del Cretácico Superior de la Península Ibérica. Comparación con otros
977
titanosaurios del suroeste de Europa. Hipótesis filogenética y paleobiogeográfica. Unpublished
978
Ph.D Thesis (306 pp). Universidad del País Vasco/EHU, Bilbao, Bilbao.
979 Díez Díaz, V., Pereda Suberbiola, X., Sanz, J.L. 2011. Braincase anatomy of the sauropod
981
dinosaur Lirainosaurus astibiae (Titanosauria) from the Late Cretaceous of the Iberian
982
Peninsula. Acta Paleontologica Polonica 56, 521-533.
SC
983
RI PT
980
Díez Díaz, V., Pereda Suberbiola, X., Sanz, J.L. 2012a. Juvenile and adult teeth of the
985
titanosaurian dinosaur Lirainosaurus (Sauropoda) from the Late Cretaceous of Iberia. Geobios
986
45, 265-274.
M AN U
984
987
Díez Díaz, V., Garcia, G., Knoll, F., Pereda Suberbiola, X., Valentin, X. 2012b. New cranial
989
remains of titanosaurian sauropod dinosaurs from the Late Cretaceous of Fox-Amphoux-
990
Métisson (Var, SE France). Proceedings of the Geologists' Association 123, 626-637.
TE D
988
991
Díez Díaz, V., Pereda Suberbiola, X., Sanz, J.L. 2013a. The axial skeleton of the titanosaur
993
Lirainosaurus astibiae (Dinosauria: Sauropoda) from the latest Cretaceous of Spain. Cretaceous
994
Research 43, 145-160.
AC C
995
EP
992
996
Díez Díaz, V., Pereda Suberbiola, X., Sanz, J.L. 2013b. Appendicular skeleton and dermal
997
armour of the Late Cretaceous titanosaur Lirainosaurus astibiae (Dinosauria: Sauropoda) from
998
Spain. Palaeontologia Electronica 16(2), 19A, 18p.
999 1000
Díez Díaz, V., Tortosa, T., Le Loeuff, J. 2013c. Sauropod diversity in the Latest Cretaceous of
1001
south-western Europe: The lessons of odontology. Annales de Paléontologie 99(2), 119-129.
42
ACCEPTED MANUSCRIPT 1002 Díez Díaz, V., Garcia, G., Pereda Suberbiola, X., Valentin, X., Sanz, J.L. 2013. Phylogenetic
1004
relationships of the titanosaurian dinosaurs from the Late Cretaceous of the Ibero-Armorican
1005
Island. In: Torcida Fernández-Baldor, F.; Huerta, P. (Eds.). Abstract book of the VI International
1006
Symposium about Dinosaurs Palaeontology and their Environment pp. 60-62.
1007
RI PT
1003
Díez Díaz, V., Ortega, F., Sanz, J.L. 2014. Titanosaurian teeth from the Late Cretaceous of “Lo
1009
Hueco” (Cuenca, Spain). Cretaceous Research 51, 285-291.
SC
1008
1010
Díez Díaz, V., Pereda Suberbiola, X., Company, J. 2015. Puesta al día de la diversidad de
1012
titanosaurios (Sauropoda) del Cretácico Superior de España. Spanish Journal of Palaeontology
1013
30(2), 293-306.
M AN U
1011
1014
Díez Díaz, V., Mocho, P., Páramo, A., Escaso, F., Marcos-Fernández, F., Sanz, J.L., Ortega, F.
1016
2016. A new titanosaur (Dinosauria, Sauropoda) from the Upper Cretaceous of Lo Hueco
1017
(Cuenca, Spain). Cretaceous Research 68, 49-60.
TE D
1015
EP
1018
Filippi, L.S., García, R.A., Garrido, A.C. 2011. A new titanosaur sauropod dinosaur from the
1020
Upper Cretaceous of North Patagonia, Argentina. Acta Palaeontologica Polonica 56(3), 505-
1021
520.
1022
AC C
1019
1023
Fondevilla, V. 2017. Registre geològic, paleoambients i susscesió dels darrers dinosaures del
1024
sud-oest europeu. Unpublished Ph.D. Thesis (338 pp). Universitat Autònoma de Barcelona.
1025 1026
Fondevilla, V., Vila, B., Oms, O., Galobart, À. 2016. Skin impressions of the last European
1027
dinosaurs. Geological Magazine 154(2), 393-398. DOI: 10.1017/S0016756816000868
43
ACCEPTED MANUSCRIPT 1028 1029
Gallina, P.A., Apesteguía, S. 2011. Cranial anatomy and phylogenetic position of the
1030
titanosaurian sauropod Bonitasaura salgadoi. Acta Palaeontologica Polonica 56(1), 45-60.
1031 Gallina, P.A., Apesteguía, S. 2015. Postcranial anatomy of Bonitasaura salgadoi (Sauropoda,
1033
Titanosauria) from the Late Cretaceous of Patagonia, Journal of Vertebrate Paleontology 35(3),
1034
e924957. DOI: 10.1080/02724634.2014.924957
SC
1035
RI PT
1032
Garcia, G., Vianey-Liaud, M. 2001. Dinosaur eggshells as new biochronological markers in Late
1037
Cretaceous continental deposits. Palaeogeography, Palaeoclimatology, Palaeoecology 169,
1038
153-164.
M AN U
1036
1039
Garcia, G., Amico, S., Fournier, F., Thouand, E., Valentin, X. 2010. A new titanosaur genus
1041
(Dinosauria, Sauropoda) from the Late Cretaceous of southern France and its
1042
paleobiogeographic implications. Bulletin de la Société Géologique de France
1043
181, 269-277.
EP
1044
TE D
1040
Gilmore, C.W. 1946. Reptilian fauna of the North Horn Formation of central Utah. United
1046
States Geological Survey Professional Paper 210C, 1-52.
1047
AC C
1045
1048
Godefroit, P., Garcia, G., Gomez, B., Stein, K., Cincotta, A., Lefevre, U., Valentin, X. 2017.
1049
Extreme tooth enlargement in a new Late Cretaceous rhabdodontid dinosaur from Southern
1050
France. Scientific reports 7, 13098. DOI:10.1038/s41598-017-13160-2
1051 1052
Goloboff, P., Farris, J., Nixon, K. 2008. TNT, a free program for phylogenetic analysis. Cladistics
1053
24, 774-786.
44
ACCEPTED MANUSCRIPT 1054 1055
Gomani, E.M. 2005. Sauropod dinosaurs from the Early Cretaceous of Malawi, Africa.
1056
Palaeontologia Electronica 8(1.27A), 1-37.
1057 González Riga, B.J. 2003. A new titanosaur (Dinosauria, Sauropoda) from the Upper
1059
Cretaceous of Mendoza Province, Argentina. Ameghiniana 40, 155-172.
RI PT
1058
1060
González Riga, B.J., Ortiz David, L. 2014. A new titanosaur (Dinosauria, Sauropoda) from the
1062
Upper Cretaceous (Cerro Lisandro Formation) of Mendoza Province, Argentina. Ameghiniana
1063
51(1), 3-25.
M AN U
SC
1061
1064
González Riga, B.J., Previtera, E., Pirrone, C.A. 2009. Malarguesaurus florenciae gen. et sp.
1066
nov., a new titanosauriform (Dinosauria, Sauropoda) from the Upper Cretaceous of Mendoza,
1067
Argentina. Cretaceous Research 30, 135-148. DOI: 10.1016/j.cretres.2008.06.006
1068
TE D
1065
González Riga, B.J., Lamanna, M.C., Ortiz David, L.D., Calvo, J.O., Coria, J.P. 2016. A gigantic
1070
new dinosaur from Argentina and the evolution of the sauropod hind foot. Scientific Reports 6,
1071
19165. DOI: 10.1038/srep19165.
AC C
1072
EP
1069
1073
González Riga, B.J., Mannion, P.D., Poropat, S.F., Ortiz David, L., Coria, J.P. 2018. Osteology of
1074
the Late Cretaceous Argentinean sauropod dinosaur Mendozasaurus neguyelap: implications
1075
for basal titanosaur relationships. Zoological Journal of the Linnean Society. DOI:
1076
10.1093/zoolinnean/zlx103
1077
45
ACCEPTED MANUSCRIPT 1078
Gorscak, E., O'Connor, P.M. 2016. Time-calibrated models support congruency between
1079
Cretaceous continental rifting and titanosaurian evolutionary history. Biology Letters 12,
1080
20151047. DOI: 10.1098/rsbl.2015.1047
1081 Gorscak, E., O'Connor, P.M. , Roberts, E.M., Stevens, N.J. 2017 The second titanosaurian
1083
(Dinosauria: Sauropoda) from the middle Cretaceous Galula Formation, southwestern
1084
Tanzania, with remarks on African titanosaurian diversity. Journal of Vertebrate Paleontology
1085
37, 4. DOI: 10.1080/02724634.2017.1343250
SC
RI PT
1082
1086
Gorscak, E., O’Connor, P.M., Stevens, N.J., Roberts, E M. 2014. The basal titanosaurian
1088
Rukwatitan bisepultus (Dinosauria, Sauropoda) from the middle Cretaceous Galula Formation,
1089
Rukwa Rift Basin, southwestern Tanzania. Journal of Vertebrate Paleontology 34, 1133–1154.
M AN U
1087
1090
Hocknull, S.A., White, M.A., Tischler, T.R., Cook, A.G., Calleja, N.D., Sloan, T., Elliott, D.A. 2009.
1092
New Mid-Cretaceous (Latest Albian) Dinosaurs from Winton, Queensland, Australia. PLoS ONE
1093
4(7), e6190. DOI: 10.1371/journal.pone.0006190
TE D
1091
EP
1094
Huene, F.v. 1929. Los Saurisquios y Ornithisquios del Cretáceo Argentino. Anales del Museo La
1096
Plata 2, 1- 196.
1097
AC C
1095
1098
Huene, F.v. 1932. Die fossil Reptil-Ordnung Saurischia, ihre Entwicklung und Geschichte.
1099
Monographien zur Geologie und Palaeontologie 4, 1-361.
1100 1101
Kellner, A.W.A., Campos, D. de A., Trotta, M.N.F. 2005. Description of a titanosaurid caudal
1102
series from the Bauru group, Late Cretaceous of Brazil. Arquivos do Museu Nacional, Rio de
1103
Janeiro 63(3), 529-564.
46
ACCEPTED MANUSCRIPT 1104 1105
Klein, N., Sander, M. 2008. Ontogenetic stages in the long bone histology of sauropod
1106
dinosaurs. Paleobiology 34, 247-263. DOI: 10.1666/0094-8373(2008)034[0247:OSITLB]2.0.CO;2
1107 Klein, N., Sander, M., Suteethorn, V. 2009. Bone histology and its implications for the life
1109
history and growth of the Early Cretaceous Phuwiangosaurus sirindhornae. Special Publications
1110
of the Geological Society of London 315, 217-228. DOI: 10.1144/SP315.15
RI PT
1108
SC
1111
Klein, N., Sander, P. M., Stein, K., Le Loeuff, J., Carballido J.L. , Buffetaut E. 2012a. Modified
1113
laminar bone in Ampelosaurus atacis and other titanosaurs (Sauropoda): implications for life
1114
history and physiology. PLoS ONE 7, e36907. DOI: 10.1371/journal.pone.0036907
M AN U
1112
1115
Klein, N., Christian, A., Sander, P.M. 2012b. Histology shows that elongated neck ribs in
1117
sauropod dinosaurs are ossified tendons. Biology Letters. DOI: 10.1098/rsbl.2012.0778
1118
TE D
1116
Kurzanov, S.M., Bannikov, A.F. 1983. A new sauropod from the Upper Cretaceous of Mongolia.
1120
Palaeontological Journal 2, 91–97.
1121
EP
1119
Lamanna, M.C., Gorscak, E., Díez Díaz, V., Schwarz, D., El-Dawoudi, I. 2017. Reassessment Of A
1123
Partial Titanosaurian Sauropod Dinosaur Skeleton From The Upper Cretaceous (Campanian)
1124
Quseir Formation Of The Kharga Oasis, Egypt. XV Annual Meeting of the European Association
1125
of Vertebrate Palaeontologists. Zitteliana p. 50.
AC C
1122
1126 1127
Lapparent, A.F.de, Aguirre, E. 1956. Algunos yacimientos de Dinosaurios en el Cretácico
1128
Superior de la Cuenca de Tremp. Estudios geológicos 31-32, 377-382.
1129
47
ACCEPTED MANUSCRIPT 1130
Lapparent, A.F.de, Aguirre, E. 1957. Presencia de dinosaurios en el Cretáceo superior de la
1131
Cuenca de Tremp (prov. de Lérida, España). Notas y Comunicaciones del Instituto Geológico y
1132
Minero de España 47, 1-6.
1133 Le Loeuff, J. 1993. European titanosaurids. Revue de Paleobiologie 7, 105–117.
RI PT
1134 1135
Le Loeuff, J. 1995. Ampelosaurus atacis (nov. gen., nov. sp.) un nouveau Titanosauridae
1137
(Dinosauria, Sauropoda) du Crétacé supérieur de la Haute Vallée de l'Aude (France). Comptes
1138
Rendus de l'Académie des Sciences Paris 321(IIa), 693-699.
M AN U
1139
SC
1136
1140
Le Loeuff, J. 2005. Osteology of Ampelosaurus atacis (Titanosauria) from Southern France. In:
1141
Tidwell, V., Carpenter, K. (Eds.), Thunder-Lizards. The Sauropodomorph Dinosaurs. Indiana
1142
University Press, Bloomington and Indianapolis pp. 115-137.
TE D
1143
Le Loeuff, J., Suteethorn, S., Buffetaut, E. 2013. A new sauropod dinosaur from the Albian of Le
1145
Havre (Normandy, France). Oryctos 10, 23-30.
1146
EP
1144
Mannion, P.D., Calvo, J.O. 2011. Anatomy of the basal titanosaur (Dinosauria, Sauropoda)
1148
Andesaurus delgadoi from the mid-Cretaceous (Albian-early Cenomanian) Río Limay
1149
Formation, Neuquén Province, Argentina: implications for titanosaur systematics. Zoological
1150
Journal of the Linnean Society 163(1), 155-181. DOI: 10.1111/j.1096-3642.2011.00699
1151
AC C
1147
1152
Mannion, P.D., Otero, A. 2012. A reappraisal of the Late Cretaceous Argentinean sauropod
1153
dinosaur Argyrosaurus superbus, with a description of a new titanosaur genus. Journal of
1154
Vertebrate Paleontology 32, 614-638. DOI: 10.1080/02724634.2012.660898
1155
48
ACCEPTED MANUSCRIPT 1156
Mannion, P.D., Upchurch, P. 2011. A re-evaluation of the ‘mid-Cretaceous sauropod hiatus’
1157
and the impact of uneven sampling of the fossil record on patterns of regional dinosaur
1158
extinction. Palaeogeography, Palaeoclimatology, Palaeoecology 299, 529–540.
1159 Mannion, P.D., Upchurch, P., Barnes, R.N., Mateus, O. 2013. Osteology of the Late Jurassic
1161
Portuguese sauropod dinosaur Lusotitan atalaiensis (Macronaria) and the evolutionary history
1162
of basal titanosauriforms. Zoological Journal of the Linnean Society 168, 98–206.
RI PT
1160
SC
1163
Marsh, O.C. 1878. Principal characters of American Jurassic dinosaurs. Part I. American Journal
1165
of Science 16, 411-416.
M AN U
1164
1166
Martin, J., Delfino, M., Garcia, G., Godefroit, P., Berton, S., Valentin, X. 2016. New specimens of
1168
Allodaposuchus precedens from France: intraspecific variability and the diversity of European
1169
Late Cretaceous eusuchians. Zoological Journal of the Linnean Society 176, 607–631.
1170
TE D
1167
Martínez, R.D., Giménez, O., Rodríguez, J., Luna, M., Lamanna, M.C. 2004. An articulated
1172
specimen of the basal titanosaurian (Dinosauria: Sauropoda) Epachthosaurus sciuttoi from the
1173
Early Late Cretaceous Bajo Barreal Formation of Chubut Province, Argentina. Journal of
1174
Vertebrate Paleontology 24(1), 107-120.
AC C
1175
EP
1171
1176
Martínez, R.D.F., Lamanna, M.C., Novas, F.E., Ridgely, R.C., Casal, G.A., Martínez, J.E., Vita, J.R.,
1177
Witmer, L.M. 2016. A Basal Lithostrotian Titanosaur (Dinosauria: Sauropoda) with a Complete
1178
Skull: Implications for the Evolution and Paleobiology of Titanosauria. PLoS ONE 11(4),
1179
e0151661. DOI: 10.1371/journal.pone.0151661.
1180
49
ACCEPTED MANUSCRIPT 1181
Masriera, A., Ullastre, J. 1988. Nuevos datos sobre las capas maestrichtienses con Septorella:
1182
su presencia al norte del Montsec (Pirineo catalán). Acta Geológica Hispánica 23, 1-77.
1183 Matheron, P. 1869. Note sur les reptiles fossiles des dépôts fluvio-lacustres crétacés du basin à
1185
lignite de Fuveau. Bulletin de la Societe Geologique de France 26, 781–795.
RI PT
1184
1186
Mitchell, J., Sander, P.M., Stein, K. 2017. Can secondary osteons be used as ontogenetic
1188
indicators in sauropods? Extending the histological ontogenetic stages into senescence.
1189
Paleobiology 43, 321-342. DOI: 10.1017/pab.2016.47
M AN U
1190
SC
1187
1191
Nopcsa, F. 1915. Die Dinosaurier der Siebenbürgischen Landsteile Ungarns. Mitteilungen aus
1192
dem Jahrbuche der Königlich Ungarischen Geologischen Reichsanstalt 23, 3-24.
1193
Nowinski, A. 1971. Nemegtosaurus mongoliensis n. gen. n. sp. (Sauropoda) from the
1195
uppermost Cretaceous of Mongolia. Palaeontologia Polonica 25, 57–81.
1196
TE D
1194
Organ, C.L., and Adams, J. 2005. The histology of ossified tendon in dinosaurs. Journal of
1198
Vertebrate Paleontology 25(3), 602-613.
AC C
1199
EP
1197
1200
Otero, A. 2010. The appendicular skeleton of Neuquensaurus, a Late Cretaceous saltasaurine
1201
sauropod from Patagonia, Argentina. Acta Palaeontologica Polonica 55(3), 399–426.
1202 1203
Otero, A., Gallina, P.A., Canale, J.I., Haluza, A., 2012. Sauropod haemal arches: morphotypes,
1204
new classification and phylogenetic aspects. Historical Biology: An International Journal of
1205
Paleobiology 24(3), 243e256. DOI: 10.1080/08912963.2011.618269
50
ACCEPTED MANUSCRIPT 1206 1207
Owen, R. 1842. Report on British fossil reptiles. Reports of the British Association for the
1208
Advancement of Science II, 60-204.
1209 Packard, G.C., Boardman, T.J., Birchard, G.F. 2009. Allometric equations for predicting body
1211
mass in dinosaurs. Journal of Zoology 279(1), 102-110.
SC
1212
RI PT
1210
Páramo, A., Ortega, F., Sanz, J.L. 2015a. Two types of appendicular bones of titanosaurs
1214
(Dinosauria, Sauropoda) from Lo Hueco (Fuentes, Cuenca). In: 63rd Symposium for Vertebrate
1215
Palaeontology and Comparative Anatomy 24th Symposium of Palaeontological Preparation
1216
and Conservation with the Geological Curators' Group (Abstract Book) p. 100.
M AN U
1213
1217
Páramo, A., Ortega, F., Sanz, J.L. 2015b. Preliminar assessment of the morphological variability
1219
of appendicular bones of titanosaurs (Dinosauria, Sauropoda) from Lo Hueco (Fuentes,
1220
Cuenca). In: Reolid, M. (Ed.), Libro de resúmenes de las XXXI Jornadas de Paleontología de la
1221
Sociedad Española de Paleontología pp. 225-226.
EP
1222
TE D
1218
Paulina Carabajal, A. 2012. Neuroanatomy of titanosaurid dinosaurs from the Upper
1224
Cretaceous of Patagonia, with comments on endocranial variability within Sauropoda. The
1225
Anatomical Record 295; 2141–2156.
1226
AC C
1223
1227
Pereda-Suberbiola, X. 2009. Biogeographical affinities of Late Cretaceous continental tetrapods
1228
of Europe: a review. Bulletin de la Société Géologique de France 180(1), 57-71.
1229
51
ACCEPTED MANUSCRIPT 1230
Poropat, S.F., Upchurch, P., Mannion, P.D., Hocknull, S.A., Kear, B.P., Sloan, T., Sinapius, G.H.K.,
1231
Elliott, D.A. 2015. Revision of the sauropod dinosaur Diamantinasaurus matildae Hocknull et
1232
al. 2009 from the middle Cretaceous of Australia: implications for Gondwanan titanosauriform
1233
dispersal. Gondwana Research 27, 995–1033.
RI PT
1234 Poropat, S.F., Mannion, P.D., Upchurch, P., Hocknull, S.A., Kear, B.P., Kundrát, M., Tischler, T.T.,
1236
Sloan, T., Sinapius, G.H.K., Elliott, J.A., Elliott, D.A. 2016. New Australian sauropods shed light
1237
on Cretaceous dinosaur palaeobiogeography. Scientific Reports 6; 34467.
SC
1235
1238
Powell, J.E. 2003. Revision of South American titanosaurid dinosaurs: palaeobiological,
1240
palaeobiogeographical and phylogenetic aspects. Records of the Queen Victoria Museum 111,
1241
1-173.
M AN U
1239
1242
Salgado, L., Coria, R.A., Calvo, J.O. 1997. Evolution of titanosaurid sauropods I: Phylogenetic
1244
analysis based on the postcranial evidence. Ameghiniana 34(1), 3-32.
1245
TE D
1243
Salgado, L., Apesteguía, S., Heredia, S.E. 2005. A new specimen of Neuquensaurus australis, a
1247
Late Cretaceous saltasaurine titanosaur from North Patagonia. Journal of Vertebrate
1248
Paleontology 25(3), 623-634.
AC C
1249
EP
1246
1250
Salgado, L., Gallina, P.A., Paulina Carabajal, A. 2015. Redescription of Bonatitan reigi
1251
(Sauropoda: Titanosauria), from the Campanian–Maastrichtian of the Río Negro Province
1252
(Argentina), Historical Biology: An International Journal of Paleobiology. DOI:
1253
10.1080/08912963.2014.894038
1254
52
ACCEPTED MANUSCRIPT 1255
Sallam, H.M., Gorscak, E., O’Connor, P.M., El-Dawoudi, I.A., El-Sayed, S., Saber, S., Kora, M.A.,
1256
Sertich, J.J.W., Seiffert, E.R., Lamanna, M.C. 2018. New Egyptian sauropod reveals Late
1257
Cretaceous dinosaur dispersal between Europe and Africa. Nature Ecology & Evolution.
1258
DOI: 10.1038/s41559-017-0455-5
RI PT
1259 Sander P.M., Klein N., Stein K., Wings O. 2011. Sauropod bone histology and its implications for
1261
sauropod biology. In: Klein N., Remes K., Gee C. T. & Sander P. M. (Eds). Biology of the
1262
sauropod dinosaurs: understanding the life of giants. Bloomington, Indiana University Press pp.
1263
276-302.
SC
1260
M AN U
1264
Sanz, J.L., Powell, J.E., Le Loeuff, J., Martínez, R., Pereda-Suberbiola, X. 1999. Sauropod remains
1266
from the Upper Cretaceous of Laño (Northecentral Spain). Titanosaur phylogenetic
1267
relationships. Estudios del Museo de Ciencias Naturales de Álava 14(Número Especial 1), 235-
1268
255.
1269
TE D
1265
Seebacher, F. 2001. A New Method to Calculate Allometric Length-Mass Relationships of
1271
Dinosaurs. Journal of Vertebrate Paleontology 21(1), 51-60.
1272
EP
1270
Seeley, H.G. 1887. On the classification of the fossil animals commonly called Dinosauria.
1274
Proceedings of the Royal Society London 43(printed 1888), 165-171.
1275
AC C
1273
1276
Stein K., Csiki Z., Rogers K.C., Weishampel D. B., Redelstorff R., Carballido J. L., Sander P.M.
1277
2010. Small body size and extreme cortical bone remodelling indicate phyletic dwarfism in
1278
Magyarosaurus dacus (Sauropoda: Titanosauria), PNAS 107, 9258-9263. DOI:
1279
10.1073/pnas.1000781107
1280
53
ACCEPTED MANUSCRIPT 1281
Upchurch, P. 1998. The phylogenetic relationships of sauropod dinosaurs. Zoological Journal of
1282
the Linnean Society 124, 43-103.
1283 Upchurch, P., Barrett, P., Dodson, P. 2004. Sauropoda. In: Weishampel, D.B., Dodson, P.,
1285
Osmólska, H. (Eds.), The Dinosauria, second ed. University of California Press, Berkeley pp. 259-
1286
324.
RI PT
1284
1287
Valentin, X., Godefroit, P., Tabuce, R., Vianey-Liaud, M., Wu, W., Garcia, G. 2012. First
1289
Maastrichtian vertebrate assemblage from Provence (Vitrolles La Plaine, France). In: Godefroit,
1290
P. (Ed.), Bernissart Dinosaurs and Early Cretaceous Terrestrial Ecosystems. Indiana University
1291
Press pp. 583-597.
M AN U
SC
1288
1292
Vila, B., Galobart, À., Canudo, J.I., Le Loeuff, J., Dinarés-Turell, J., Riera, V., Oms, O.,
1294
Tortosa, T., Gaete, R. 2012. The diversity of sauropod dinosaurs and their first taxonomic
1295
succession from the latest Cretaceous of southwestern Europe: clues to demise and extinction.
1296
Palaeogeography, Palaeoclimatology, Palaeoecology 350-352, 19-38. DOI:
1297
10.1016/j.palaeo.2012.06.008
EP
1298
TE D
1293
Vila, B., Sellés, A.G., Brusatte, S.L. 2016. Diversity and faunal changes in the latest Cretaceous
1300
dinosaur communities of south-western Europe. Cretaceous Research 57, 552–64.
1301
AC C
1299
1302
Vullo, R., Garcia, G., Godefroit, P., Cincotta, A., Valentin, X. In press. Mistralazhdarcho maggii
1303
gen. et sp. nov., a new azhdarchid pterosaur from the Upper Cretaceous of southeastern
1304
France. Journal of Vertebrate Paleontology.
1305
54
ACCEPTED MANUSCRIPT 1306
Wedel, M.J. 2003. The evolution of vertebral pneumaticity in sauropod dinosaurs. Journal of
1307
Vertebrate Paleontology 23(2), 344-357.
1308 Wedel, M.J., Taylor, M.P. 2013. Caudal Pneumaticity and Pneumatic Hiatuses in the Sauropod
1310
Dinosaurs Giraffatitan and Apatosaurus. PLoS ONE 8(10), e78213. DOI:
1311
10.1371/journal.pone.0078213
RI PT
1309
1312
Wilson, J.A. 1999. A nomenclature for vertebral laminae in sauropods and other saurischian
1314
dinosaurs. Journal of Vertebrate Paleontology 19, 639-653.
SC
1313
M AN U
1315 1316
Wilson, J.A. 2002. Sauropod dinosaur phylogeny: critique and cladistic analysis. Zoological
1317
Journal of the Linnean Society 136, 217-276.
1318
Wilson, J.A. 2006. Anatomical nomenclature of fossil vertebrates: standardized terms or lingua
1320
franca? Journal of Vertebrate Paleontology 26, 511-518.
TE D
1319
1321
Wilson, J.A. 2011. Anatomical terminology for the sacrum of sauropod dinosaurs. Contrib.
1323
Mus. Paleontol. Univ. Michigan 32, 59-69.
EP
1322
AC C
1324 1325
Wilson, J.A., Carrano, M.T. 1999. Titanosaurs and the origin of “wide-gauge” trackways: a
1326
biomechanical and systematic perspective on sauropod locomotion. Paleobiology 25, 252-267.
1327 1328
Wilson, J.A., Upchurch, P. 2003. A revision of Titanosaurus Lydekker (Dinosauria-Sauropoda),
1329
the first dinosaur genus with a “Gondwanan” distribution. Journal of Systematic Palaeontology
1330
1, 125-160.
1331
55
ACCEPTED MANUSCRIPT 1332
Wilson, J.A., Upchurch, P. 2009. Redescription and reassessment of the phylogenetic affinities
1333
of Euhelopus zdanskyi (Dinosauria: Sauropoda) from the Early Cretaceous of China. Journal of
1334
Systematic Palaeontology 7, 199–239.
1335 Wilson, J.A., D'Emic, M.D., Ikejiri, T., Moacdieh, E.M., Withlock, J.A. 2011. A nomenclature for
1337
vertebral fossae in sauropods and other saurischian dinosaurs. PLoS One 6(2), e17114. DOI:
1338
10.1371/journal.pone.0017114
RI PT
1336
SC
1339
Wilson, J.A., Pol, D., Carvalho, A.B., Zaher, H. 2016. The skull of the titanosaur Tapuiasaurus
1341
macedoi (Dinosauria: Sauropoda), a basal titanosaur from the Lower Cretaceous of Brazil.
1342
Zoological Journal of the Linnean Society 178(3), 611-662. DOI: 10.1111/zoj.12420.
M AN U
1340
1343
Zaher, H., Pol, D., Carvalho, A.B., Nascimento, P.M., Riccomini, C., Larson, P., Juárez-Valieri, R.,
1345
Pires-Domingues, R., da Silva Jr., de Almeida Campos, N.J.D. 2011. A complete skull of an early
1346
Cretaceous Sauropod and the evolution of advanced Titanosaurians. PLoS ONE 6(2), e16663.
TE D
1344
1347
1350
FIGURE LEGENDS
AC C
1349
EP
1348
1351
Figure 1. (A) Simplified geological map of the Aix-en-Provence Basin (Bouches-du-Rhône,
1352
France). Arrow indicates the location of the Velaux-La Bastide Neuve site. (B) Map indicating
1353
the repartition of vertebrate specimens collected since 1993 including some important
1354
titanosaurian bones (without the institutional abbreviations) and the concentration of bones
1355
collected in 2009 (a) and 22012 (b).
1356
56
ACCEPTED MANUSCRIPT Figure 2. Cranial remains of the titanosaur Atsinganosaurus velauciensis. Right fragment of a
1358
braincase (MMS/VBN.09.167) in (A) lateral and (B) medial views. Left pterygoid
1359
(MMS/VBN.09.158a) in (C) medial and (D) lateral views. Occipital condyle (MMS/VBN.09.41 ) in
1360
(E) right lateral view. Tooth (MMS/VBN.12.A.006) in (F) labial view. Abbreviations as in the
1361
text.
RI PT
1357
1362
Figure 3. Cervical vertebrae of the titanosaur Atsinganosaurus velauciensis. Posterior cervical
1364
vertebrae, previously described by Garcia et al. (2010), in left lateral view: (A) UP/VBN.93.12a
1365
(B), UP/VBN.93.12b, and (C) UP/VBN.93.12c. (D) Anterior cervical vertebra
1366
(MMS/VBN.12.B.015), with parts of the subsequent centrum ventrally associated to it in left
1367
lateral view. Posterior view of (E) UP/VBN.93.12a and (F) MMS/VBN.12.B.015. (G) Anterior
1368
cervical vertebra (MMS/VBN.12.A.004), with a fragment of the cervical rib, in right lateral view.
1369
Abbreviations as in the text.
M AN U
TE D
1370
SC
1363
Figure 4. Posterior cervical vertebra (MMS/VBN.12.B.010), and interpretative drawings, of the
1372
titanosaur Atsinganosaurus velauciensis in (A, A’) left lateral, (B, B’) anterior, (C, C’) right
1373
lateral, and (D, D’) posterior views. Abbreviations as in the text.
AC C
1374
EP
1371
1375
Figure 5. Fragmentary dorsal vertebrae and ribs of the titanosaur Atsinganosaurus
1376
velauciensis. (A) fragment of an anterior dorsal neural arch (MMS/VBN.93.32) in anterior view,
1377
(B) fragmentary dorsal vertebra (UP/VBN.09.157) in right lateral view, and (C) fragmentary
1378
middle to posterior dorsal vertebra (MMS/VB.93.02) in posterolateral view. Dorsal ribs
1379
MMS/VBN.07.D.07b in (D) lateral and (E) medial views, and MMS/VBN.07.D.07a in in (F) lateral
1380
and (G) medial views. Abbreviations as in the text.
57
ACCEPTED MANUSCRIPT 1381
Figure 6. Sacrum (MMS/VBN.02.82) of the titanosaur Atsinganosaurus velauciensis, previously
1383
described by Garcia et al. (2010), in (A) right lateral, (B) anterior, (C) slightly ventrolateral, and
1384
(D) posterior views.
RI PT
1382
1385
Figure 7. Caudal vertebrae and haemal arches of the titanosaur Atsinganosaurus velauciensis.
1387
Anterior caudal vertebra (MMS/VBN. 00.14) in (A) left lateral, (B) anterior, (C) posterior, (D)
1388
ventral, and (E) dorsal views. Anterior caudal vertebra (MMS/VBN. 00.15) in (F) left lateral, (G)
1389
anterior, (H) ventral, and (I) dorsal views. Anterior caudal vertebra (MMS/VBN.93.31a) in (J)
1390
left lateral and (K) anterior views. Haemal arch (MMS/VBN. 93.31b) in (L) anterior and (M)
1391
posterior views. Anterior caudal vertebra (MMS/VBN. 02.110) in (N) left lateral, (O) anterior,
1392
(P) posterior, and (Q) ventral views. Middle to posterior caudal vertebra (MMS/VBN.09.D.003)
1393
in (R) left lateral, (S) anterior, (T) posterior, and (U) ventral views. Posterior (distal) caudal
1394
vertebra (MMS/VBN.93.32a) in (V) right lateral, (W) anterior, and (X) posterior views. Haemal
1395
arch (MMS/VBN.93.32b) in (Y) anterior and (Z) posterior views.
M AN U
TE D
EP
1396
SC
1386
Figure 8. Caudal vertebrae of the titanosaur Atsinganosaurus velauciensis. (A) anterior caudal
1398
vertebra (MMS/VBN.12.C.004) in left lateral view, (B) fragmentary anterior caudal vertebra
1399
(MMS/VBN.09.54) in left lateral view, (C) posterior caudal vertebra (MMS/VBN.12.C.003) in
1400
right lateral view, (D) fragmentary posterior caudal vertebra (MMS/VBN.09.D.010) in left
1401
lateral view, (E) posterior caudal vertebra (MMS/VBN.09.159.b) in right lateral view, (F)
1402
posterior caudal vertebra (UP/VBN.93.03), in left lateral view, (G) posterior caudal vertebra
1403
(UP/VBN.93.04), in right lateral view, (H) posterior caudal vertebra (UP/VBN.93.05), in right
1404
lateral view, (I) fragmentary posterior caudal vertebra (UP/VBN.93.06), in right lateral view (J)
AC C
1397
58
ACCEPTED MANUSCRIPT 1405
posterior caudal vertebra UP/VBN.93.07), in right lateral view, and (K) posterior caudal
1406
vertebra (UP/VBN.93.08), in right lateral view. F-K were previously described by Garcia et al.
1407
(2010).
RI PT
1408 Figure 9. Scapular girdle remains of the titanosaur Atsinganosaurus velauciensis. Fragmentary
1410
left scapulocoracoid (MMS/VBN.02.78a–b) in (A) lateral and (B) medial views. (C) Left scapula
1411
(MMS/VBN.93.11) in medial view. (D) Right juvenile scapula (MMS/VBN.09.124D) in lateral
1412
view.
SC
1409
M AN U
1413
Figure 10. Forelimb remains of the titanosaur Atsinganosaurus velauciensis. Right humerus
1415
(MMS/VBN.00.12), previously described by Garcia et al. (2010), in (A) anterior, (B) medial, (C)
1416
posterior, and (D) lateral views. Left humerus (MMS/VBN.09.A.018) in (E) anterior, (F) medial,
1417
(G) posterior, and (H) lateral views. Right humerus (VBN.93.MHNA.99.52) in (I) anterior and (J)
1418
posterior views. Right ulna (MMS.VBN.12.P.06a) in (K) proximal (medial towards top), (L)
1419
medial, (M) posterior, (N) lateral, (O) distal (lateral towards top), and (P) anterior views.
1420
Fragmentary radius (MMS/VBN.09.D.001) in (Q) anterior/posterior? and (R)
1421
posterior/anterior? views.
EP
AC C
1422
TE D
1414
1423
Figure 11. Metacarpal remains of the titanosaur Atsinganosaurus velauciensis. Left metacarpal
1424
I (MMS/VBN.09.113) in (A) dorsal, (B) posterior, (C) medial, and (D) lateral views. Left
1425
metacarpal I (UP/VBN.93.09) in (E) dorsal, (F) posterior, (G) medial, and (H) lateral views.
1426
59
ACCEPTED MANUSCRIPT 1427
Figure 12. Pelvic girdle of the titanosaur Atsinganosaurus velauciensis. Fragment of a right
1428
ilium (MMS/VBN.12.32) in (A) lateral and (B) ventromedial views. Right ischium
1429
(MMS/VBN.09.51c) in (C) lateral,(D), posterior, and (E) medial views. Abbreviations as in the
1430
text.
RI PT
1431
Figure 13. Hind limb remains of the titanosaur Atsinganosaurus velauciensis. Diaphysis of a
1433
right femur (MMS/VBN.09.126) in (A) anterior and (B) posterior views. Left tibia
1434
(MMS/VBN.02.90) in (C) proximal (lateral towards bottom), (D) lateral, (E) anterior, (F) medial,
1435
(G) distal (medial towards top), and (H) posterior views. Proximal third of a fibula
1436
(MMS/VBN.09.132) in (I) lateral and (J) medial views. Left tibia (MMS/VBN.02.109) in (K)
1437
proximal (lateral towards bottom), (L) lateral, (M) anterior, (N) medial, (O) distal (medial
1438
towards top), and (P) posterior views.
TE D
1439
M AN U
SC
1432
Figure 14. Left metatarsal I (MMS/VBN.93.10), previously described by Garcia et al. (2010), of
1441
the titanosaur Atsinganosaurus velauciensis in (A) dorsal, (B) distal, (C) medial, (D) proximal, (E)
1442
ventral (dorsal toward bottom), and (F) lateral (dorsal towards top) views.
AC C
1443
EP
1440
1444
Figure 15. Micro- and macrohistology of the titanosaur Atsinganosaurus velauciensis. A-C and
1445
E: transverse sections. D and F: longitudinal sections. (A) heavy remodelling of the cortex
1446
(MMS/VBN.09.A.018). (B) zoom with multiple secondary osteon generations indicated by
1447
numbers (MMS/VBN.09.A.018). (C) broken trabeculae trapped in sediments at the base of the
1448
core (MMS/VBN.09.A.018). (D) longitudinal section of MMS/VBN.09.126. (E-F) macrohistology
1449
of MMS/VBN.09.126 in radial and longitudinal section respectively. Scale bars: A-B = 0.5 mm,
1450
C-D = 1 mm, E-F = 1 cm.
60
ACCEPTED MANUSCRIPT 1451 Figure 16. Neck rib histology of the titanosaur Atsinganosaurus velauciensis. (A) overview of
1453
the two ribs in their storage unit, with inset illustrating the sectioning planes. The arrow in A,
1454
D, and E indicates the longitudinal axis. (B) composite image (plane polarized light and cross
1455
polars) with an overview of the histology of the sauropod cervical ribs in cross section. Note
1456
the patches of longitudinally running collagen fibre bundles. (C) composite image (in plane
1457
polarized light and cross polars) of the secondary osteons and fibre bundles in cross section at
1458
high magnification. Note the cross cutting relationships of some of the secondary osteons. (D)
1459
overview (plane polarized light) of the histology of the cervical ribs in longitudinal section. (E)
1460
detail of D. Note the strong longitudinal orientation of the osteons and osteocyte lacunae, as
1461
well as the fibre bundles with fibrocytes. Abbreviations: cl, cementing line; fb, fibre bundles;
1462
so, secondary osteon.
M AN U
SC
RI PT
1452
TE D
1463
Figure 17. Phylogenetic hypothesis. Only one MPT of 166 steps was obtained from the Salgado
1465
et al. (2015) data matrix, with a consistency index (CI) of 0.572 and a retention index (RI) of
1466
0.665. The European taxa are highlighted in the cladogram. The obtained nodes are (1)
1467
Titanosauriformes, (2) Titanosauria, (3) Lithostrotia, (4) Opisthocoelicaudiinae, (5)
1468
Saltasaurinae, (6) Aeolosaurinae, (7) Rinconsauria, (8) Lognkosauria, and (9) Lirainosaurinae.
AC C
1469
EP
1464
1470
TABLE LEGENDS
1471
Table 1. Measurements (in mm) of the teeth of the titanosaur Atsinganosaurus velauciensis.
1472
Abbreviations: Ø m-d: maximum mesiodistal width; Ø lb-ln: maximum labiolingual width; SI:
1473
slenderness index (Upchurch, 1998): length of the tooth crown divided by its maximum
61
ACCEPTED MANUSCRIPT 1474
mesiodistal width; CI: compression index (Díez Díaz et al., 2013c): maximum labiolingual width
1475
divided by the maximum mesiodistal width of the crown.
1476 Table 2. Measurements (in mm) of the vertebrae of the titanosaur Atsinganosaurus
1478
velauciensis. Abbreviations: A, anterior; M, middle; P, posterior; D, distal; EI (Elongation index)
1479
(Upchurch, 1998): anteroposterior length of the centrum (without the condyle) divided by the
1480
midline width of the cotyle.
RI PT
1477
SC
1481
Table 3. Measurements (in mm) of the fore and hindlimb remains of the titanosaur
1483
Atsinganosaurus velauciensis. Abbreviations: Max. width Prox. end: maximum width of the
1484
proximal end; Max. width distal end: maximum width of the distal end; Min. AP Width:
1485
minimum anteroposterior width; Min. Cir. Diaph.: minimum circumference of the diaphysis;
1486
Min. Transv. Width: minimum transversal width; ECC (eccentricity index) (Wilson and Carrano,
1487
1999): mid-shaft mediolateral width divided by the anteroposterior width.
TE D
1488
M AN U
1482
Table 4. Measurements (in mm) of the metacarpal and metatarsal remains of the titanosaur
1490
Atsinganosaurus velauciensis. Abbreviations: AP, anteroposterior; ML, mediolateral.
1491
EP
1489
Table 5. Measurements (in mm) of the ischium of the titanosaur Atsinganosaurus velauciensis.
1493
Abbreviations: PP, pubic peduncle.
1494 1495
AC C
1492
Table 6. Histological data summary of Atsinganosaurus velauciensis.
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
MMS/VBN.12.A.006 MMS/VBN.12.B.14 MMS/VBN.12.A.07 MMS/VBN.93.33
Crown length Ø m-d Ø lb-ln SI CI 190 33 23 5.76 0.69 180 45 4 160 37 33 4.32 0.89 150 39 3.85 -
ACCEPTED MANUSCRIPT
Centrum length Centrum length Vertebral Centrum height Centrum width Neural arch Neural spine (w/condyle) (wo/condyle) Heigth (posterior) (posterior) heigth heigth 352.5 330 195 220 230 185 255 280 -
333.5 270 175 195 200 155 235 252 220
240 300 310 220 260 185 192
74 51 85 90 60 82 63 50
69 44 85 90 50 72 61 34
1270.7 -
1017.1 -
-
130
75
86 91 83 85 102 90 94 121 123 97 97 125 113 90 99 76 75 71
60 77 67 74 70 74 103 84 98 102 83 86 109 92 77 74 86 68 70 59
107 143 104 133 85 74 66 71 54 64 54 60 44
62 39 35 65 53 56 48 47 45 29 59 31 38 40 34 24
28 90 95 36 51 58 62 50 46 54 48 61 45 26 30 21
AC C
EP
M AN U
CAUDALS MMS/VBN.93.31a (A) MMS/VBN.00.14 (A) MMS/VBN.00.15 (A) MMS/VBN.09.46 (A) MMS/VBN.09.54 (A) MMS/VBN.12.C.004 (A) MMS/VBN.09.D.011 (A-M?) MMS/VBN.12.B.018 (A-M?) MMS/VBN.09.D.009 (M?) MMS/VBN.12.B.013a (P) MMS/VBN.12.B.013b (P) MMS/VBN.09.D.03 (P) MMS/VBN.09.D.010 (P) MMS/VBN.09.159.b (P) MMS/VBN.12.C.003 (P) MMS/VBN.12.33 (P) UP/VBN.93.3 (P-D) UP/VBN.93.4 (P-D) UP/VBN.93.5 (P-D) UP/VBN.93.6 (D) UP/VBN.93.7 (D) UP/VBN.93.8 (D)
TE D
MMS/VBN.02.99 UP/VBN.09.157
120 200 210 118 100 78 90
3.91 3.98 2.29 2.22 3.10 3.26 4.13 6.47
-
275.7 -
-
57 70 40 68 41 36 48 23 25 35 33 30 19 24 16
51 32 22 50 17 14 21 7 21 14 9 0 7 3
2.14 0.86 0.71 2.06 1.37 1.28 1.65 1.66 1.87 2.02 1.92 1.26 1.64 2.62 2.33 2.81
SC
DORSALS
171 25 2050 147 185 102 126
RI PT
CERVICALS MMS/VBN.12.A.004 (A) MMS/VBN.12.B.015 (A) MMS/VBN.09.D.007a (A) UP/VBN.93.13a (M) UP/VBN.93.13b (M) MMS/VBN.12.B.10 (P) UP/VBN.93.12a (P) UP/VBN.93.12b (P) UP/VBN.93.12c (P)
EI
ACCEPTED MANUSCRIPT
Min. Cir. Diaph.
Max. width Prox.end
Max. width distal end
21 17
3.14 3.76
23.31 16.94
-
-
57.96
30.22
1.92
22.58
272
57
29
1.97
-
709
90.42
57.95
562
112
43
TIBIAE MMS/VBN.02.90 MMS/VBN.02.109
322 530
50.14 81.85
21.2 38.66
FIBULA MMS/VBN.09.132
221
47
390
RADIUS MMS/VBN.09.D.01
29
AC C
FEMORA MMS/VBN.00.12 MMS/VBN.09.126
SC
ULNA MMS/VBN.12.P.06a
M AN U
66 64
EP
555 480
RI PT
ECC
55.16
43.75
-
-
1.56 2.60
45.67 40.67
-
-
2.37 2.12
37.3 63.22
106.61 64.23
72 38.7
-
-
-
TE D
Preserved length Min. Transv. Width Min. AP Width HUMERI MMS/VBN.00.12 MMS/VBN.09.A.018
1.62
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
Length AP width diaphisis LM width diaphisis AP width Prox. Art. LM width Prox. Art. AP width Dist. Art. LM width Dist. Art. MMS/VBN.93.09 87 13 17 22 32 MMS/VBN.09.113 180 14 27 23 60 27 43 UP/VBN.93.10 120 46 27 71 31 60 60
AC C
EP
TE D
M AN U
SC
RI PT
MANUSCRIPT Preserved length ACCEPTED PP articular surface Distal edge width MMS/VBN.09.51c 345 105
Preserved lentgh (mm) ±570 470 555
ACCEPTED MANUSCRIPT Bone tissue type 2ry osteon generations in the inner,mid,outer cortex respectively
Core location Posterior side, above the mid-shaft Posterior side, in the mid-shaft Anterior side, in the mid-shaft
H H H
5,6,4 5,5,6 4,5,4
AC C
EP
TE D
M AN U
SC
RI PT
A. velauciensis sample Bone MMS/VBN.09.126 Right femur MMS/VBN.09.A.018 Left humerus MMS/VBN.00.12 Right humerus
HOS,RS 14,13+ 14.14 14.13
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
S0195-6671(18)30042-9
DOI:
10.1016/j.cretres.2018.06.015
Reference:
YCRES 3908
To appear in:
Cretaceous Research
Received Date: 31 January 2018 Revised Date:
2 May 2018
Accepted Date: 20 June 2018
Please cite this article as: Díez Díaz, Veró., Garcia, Gé., Pereda Suberbiola, X., Jentgen-Ceschino, B., Stein, K., Godefroit, P., Valentin, X., The titanosaurian dinosaur Atsinganosaurus velauciensis (Sauropoda) from the Upper Cretaceous of southern France: New material, phylogenetic affinities, and palaeobiogeographical implications, Cretaceous Research (2018), doi: 10.1016/j.cretres.2018.06.015. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
1
ACCEPTED MANUSCRIPT The titanosaurian dinosaur Atsinganosaurus velauciensis (Sauropoda) from the
2
Upper Cretaceous of southern France: new material, phylogenetic affinities, and
3
palaeobiogeographical implications
4
Verónica Díez Díaz 1,2, Géraldine Garcia 3, Xabier Pereda Suberbiola 4, Benjamin Jentgen-
5
Ceschino 5,6, Koen Stein 5,7, Pascal Godefroit 7, and Xavier Valentin 3,8
RI PT
1
6
1
7
43, 10115 Berlin, Germany;
8
2
Humboldt Universität, Berlin, Germany;
9
3
Laboratoire de Paléontologie, Evolution, Paléoécosystèmes et Paléoprimatologie (PALEVOPRIM,
M AN U
SC
Museum für Naturkunde, Leibniz-Institut für Evolutions-und Biodiversitätsforschung, Invalidenstraße
10
UMR7262 CNRS INEE), Université de Poitiers, 6, rue Michel-Brunet, 86073 Poitiers cedex, France;
11
4
12
Estratigrafía y Paleontología, Apartado 644, 48080 Bilbao, Spain;
13
5
Earth System Science – AMGC, Vrije Universiteit Brussel, Pleinlaan 2, 1050 Brussels, Belgium;
14
6
Evolution & Diversity Dynamics Lab, Liège University, Allée du six Août, 14, 4000 Liège, Belgium;
15
7
Directorate ‘Earth and History of Life’, Royal Belgian Institute of Natural Sciences, 1000 Brussels,
16
Belgium;
17
8
TE D
Universidad del País Vasco/Euskal Herriko Unibertsitatea, Facultad de Ciencia y Tecnología, Dpto.
EP
Palaios Association, 86300 Valdivienne, France.
AC C
18 19
Abstract
20
New remains of the titanosaurian sauropod Atsinganosaurus velauciensis from its Upper
21
Cretaceous type horizon and type locality in Velaux-La Bastide Neuve (Bouches-du-Rhône
22
Department, Provence) in southern France are described. This locality is considered to be
23
upper Campanian (Argiles et Grès à Reptiles Formation, Aix-en-Provence Basin). The new
24
material consists of skull fragments, including a partial braincase, isolated teeth, elements of
2
ACCEPTED MANUSCRIPT the axial skeleton (cervical, dorsal and caudal vertebrae, ribs), and appendicular bones
26
(scapula, humeri, ulna, metacarpals, ilia, ischia, femur, tibia, metatarsal). Histological
27
investigation shows that the analysed individuals were mature. The emended diagnosis of
28
Atsinganosaurus velauciensis includes a pubic peduncle of the ilium with a posterior concave
29
surface in its distal half, surrounded by two sharp ridges. Equations for predicting body mass
30
and size in sauropods suggest a body size up to 12 meters and a body mass of at least 3.5-5
31
tonnes for the largest individuals.
32
A phylogenetic analysis including 29 sauropod taxa was performed, with the European
33
titanosaurs Atsinganosaurus, Ampelosaurus, Lirainosaurus, Lohuecotitan, Paludititan (Late
34
Cretaceous) and Normanniasaurus (Early Cretaceous) all scored in the same analysis for the
35
first time. Atsinganosaurus and Ampelosaurus form a clade that is phylogenetically proximal to
36
Lirainosaurus within Lithostrotia – a clade here named Lirainosaurinae nov. – whereas
37
Lohuecotitan and Paludititan form a clade towards the base of Lithostrotia. Normanniasaurus
38
is resolved outside Lithostrotia, but within Titanosauria. From a palaeobiogeographical
39
perspective, the phylogenetic results suggest that European titanosaurs belong to at least
40
three distinct lineages and that two lithostrotian lineages were present during the latest
41
Cretaceous in the European archipelago.
42
Key Words: Atsinganosaurus, Lirainosaurinae, Titanosauria, Late Cretaceous, France,
43
palaeobiogeography
SC
M AN U
TE D
EP
AC C
44
RI PT
25
45
INTRODUCTION
46
Recent studies have shown that the biodiversity of European titanosaurian sauropods was
47
quite high during the Late Cretaceous, especially between the Campanian and early
48
Maastrichtian (see e.g. Díez Díaz et al., 2015, 2016; Fondevilla, 2017; Vila et al., 2012, 2016).
3
ACCEPTED MANUSCRIPT Five titanosaurian taxa have been described in Europe so far: Lirainosaurus astibiae, from the
50
upper Campanian of Laño and Chera, Spain (Sanz et al., 1999; Company et al., 2009; Díez Díaz
51
et al., 2011, 2012a, 2013a, 2013b, 2015); Lohuecotitan pandafilandi, from the upper
52
Campanian-lower Maastrichtian of Lo Hueco, Spain (Díez Díaz et al., 2016); Atsinganosaurus
53
velauciensis, from the upper Campanian of Velaux-La Bastide Neuve, France (Garcia et al.,
54
2010); Ampelosaurus atacis, from the lower Maastrichtian of Bellevue, France (Le Loeuff, 1995,
55
2005); and Paludititan nalatzensis, from the lower Maastrichtian of Nǎlaţ-Vad, Romania (Csiki
56
et al., 2010). However, their diversity was likely even higher:
59
SC
58
1) The status of Magyarosaurus, from the Maastrichtian of Romania, is still uncertain, and a revision of all the recovered material is needed (see Csiki et al., 2010).
M AN U
57
RI PT
49
2) Numerous isolated or poorly preserved titanosaurian remains were found in the Upper Cretaceous of southeastern France and northeastern Spain during the second half of
61
the 19th century and the 20th century. These remains were assigned to the species
62
Titanosaurus indicus and Hypselosaurus priscus (Matheron, 1869; Depéret, 1899;
63
Lapparent and Aguirre, 1956, 1957; Masriera and Ullastre, 1988), both now considered
64
nomina dubia (Le Loeuff, 1993; Wilson and Upchurch, 2003). This material also needs a
65
detailed revision.
68 69
EP
67
3) At several sites of Spain and southern France cranial, dental and appendicular elements representing more than one titanosaurian morphotype have been found
AC C
66
TE D
60
(Vila et al., 2012; Díez Díaz et al., 2012b, 2014, 2015; Páramo et al., 2015a, b).
Thus, at least seven titanosaurian taxa have so far been identified from the Campanian-
70
Maastrichtian of Europe. Detailed studies and comprehension of these last sauropod faunas,
71
especially in the Ibero-Armorican Island, is of great importance for understanding dinosaur
72
biodiversity in Europe, just before the Cretaceous-Palaeogene (K-Pg) event (see Csiki-Sava et
4
ACCEPTED MANUSCRIPT 73
al., 2015, Vila et al., 2016; Fondevilla et al., 2016) that led to the extinction of all non-avian
74
dinosaurs.
75
Atsinganosaurus velauciensis is represented by several partially articulated specimens, some of which were described by Garcia et al. (2010). In 2009 and 2012, renewed excavation
77
campaigns at the Velaux-La Bastide Neuve locality (Provence, France) led to the recovery of
78
more material (Figure 1). The specimens described in this publication derive from sequence 2
79
(Cincotta et al., 2015), as do the holotype and referred specimens of this taxon described in
80
Garcia et al. (2010). This sequence occurs in the Argiles et Grès à Reptiles Formation (Aix-en-
81
Provence Basin), which is upper Campanian. Dinosaur specimens represent 38% of the
82
vertebrate remains collected during the 2009 and 2012 campaigns in Velaux-La Bastide Neuve
83
(Cincotta et al. 2015), with most of these representing titanosaurs. The vertebrate fauna is
84
abundant and diversified including rhabdodontid dinosaurs (Matheronodon provincialis
85
[Godefroit et al. 2017] and Rhabdodon priscus), ankylosaurian remains, theropod teeth, the
86
ontogenetic cranial and postcranial elements of the eusuchian crocodyliform Allodaposuchus
87
precedens (Martin et al. 2016) , pleurodiran and cryptodiran turtle shells, an azhdarchid
88
pterosaur (Vullo et al. in press), hybodont shark teeth, and mawsoniid bones. Sequence 2
89
constitutes a coarse-grained conglomeratic sandstone lens. The fossil material was transported
90
over rather short distances and accumulated together within a river channel, in a fluvial
91
environment (Cincotta et al., 2015).
SC
M AN U
TE D
EP
AC C
92
RI PT
76
The discovery of abundant titanosaurian cranial and postcranial remains provides new
93
information on the French titanosaur Atsinganosaurus velauciensis, thereby facilitating the
94
emendation of its diagnosis, better definition of its morphological features, and more precise
95
assessment of its phylogenetic affinities. This will, in turn, enhance our understanding of the
96
palaeobiogeographical history of Late Cretaceous sauropod faunas.
97
5
ACCEPTED MANUSCRIPT 98
METHODOLOGY
99
Taxonomic description We use “Romerian” terms (Wilson, 2006) for anatomical structures (e.g. “centrum”, not
101
“corpus”) and their orientations (e.g. “anterior”, not “cranial’”). The landmark-based
102
terminology for vertebral laminae (Wilson, 1999) and fossae (Wilson et al., 2011) is used in the
103
discussion of vertebral anatomy and in Figures 3-5. For the identification of the caudal
104
vertebrae we follow suggestions made by Díez Díaz et al. (2013a). All measurements are
105
provided in Tables 1-5.
SC
For brevity and clarity, Atsinganosaurus velauciensis is mainly compared with
M AN U
106
RI PT
100
European titanosaurian taxa: Ampelosaurus atacis from Bellevue (Aude, France; Le Loeuff,
108
1995, 2005), Normanniasaurus genceyi from Le Havre (Normandy, France; Le Loeuff et al.,
109
2013), Lirainosaurus astibiae from Laño (Condado de Treviño, Spain; Sanz et al., 1999; Díez
110
Díaz et al., 2011, 2013a, b) and Chera (Valencia, Spain; Company et al., 2009; Díez Díaz et al.,
111
2015), Lohuecotitan pandafilandi from Lo Hueco (Cuenca, Spain; Díez Díaz et al., 2016),
112
Paludititan nalatzensis from Nǎlat-Vad (Haţeg Basin, Romania; Csiki et al., 2010), and the
113
material from the Haţeg Basin (Romania) referred to Magyarosaurus dacus (Nopcsa, 1915;
114
Huene, 1932) housed in the NHMUK. All the comparisons, except for Normanniasaurus genceyi
115
and Paludititan nalatzensis, are based on first-hand observations by the senior author (VDD).
116
However, several comparisons have been made with other titanosaurs on the basis of
117
important anatomical and phylogenetically important features that will help to distinguish
118
Atsinganosaurus and the other European taxa from other members within Titanosauria.
119
Histological methods
120
In order to determine the ontogenetic stage of the new specimens, we sampled humeri and
121
femora housed in the collection in the Moulin Seigneurial of Velaux (MMS/VBN.09.126,
AC C
EP
TE D
107
6
ACCEPTED MANUSCRIPT
MMS/VBN.09.A.018, and MMS/VBN.00.12 – see table 6). In addition, we also sampled two
123
very long (± 200 cm) and slender bony elements (MMS/VBN.09.51a and b), hypothesized to be
124
cervical ribs. The long bone specimens were core-sampled (diameter of 1 cm) at or near the
125
mid-shaft in posterior or anterior position, according to the standardized core location, when
126
possible (Stein and Sander 2009; Sander et al., 2011). A fragment of the rib was also sectioned
127
longitudinally and transversely to look for tendon fibres. Most of the cores broke during the
128
drilling process because of their low mineralization, but were glued and restored before thin
129
sectioning. All thin sections were prepared using standard lapidary methods with a thickness of
130
40 µm. Observations were made with an Olympus petrographic microscope, BX50F-3 model,
131
equipped with 5x and 10x objectives. Pictures were taken with a Leica camera and processed
132
in Leica Application suite.
133
Phylogenetic analysis
134
To establish the relationships of Atsinganosaurus, a phylogenetic analysis was performed using
135
the data matrix proposed by Salgado et al. (2015). This data matrix was analyzed using TNT 1.1
136
(Goloboff et al., 2008) to find the most parsimonious trees (MPTs). For the first time, all the
137
European taxa were included in the same analysis: Sallam et al. (2018) scored all the European
138
titanosaurs from the Campanian-Maastrichtian of Europe, but this is the first time that
139
Normannaisaurus is also included in the analysis. We have scored from first hand the European
140
titanosaurs Atsinganosaurus, Ampelosaurus, Lirainosaurus and Lohuecotitan, and
141
Normanniasaurus and Paludititan from the literature. We have also scored the titanosauriform
142
Malarguesaurus (González Riga et al., 2009) first-hand in order to enhance the resolution of
143
the relationships of basal forms. We used a heuristic tree search performing 1000 replications
144
of Wagner trees (using random addition sequences) followed by tree bisection reconnection
145
(TBR) as swapping algorithm, saving 100 trees per replicate. All characters were treated as
146
unordered and unweighted.
AC C
EP
TE D
M AN U
SC
RI PT
122
7
ACCEPTED MANUSCRIPT Institutional Abbreviations: FAM, Fox-Amphoux-Métisson, Mairie de Fox-Amphoux (Fox-
148
Amphoux Council), Fox-Amphoux, France; MCNA, Museo de Ciencias Naturales de
149
Álava/Arabako Natur Zientzien Museoa, Vitoria-Gasteiz, Spain; MDE, Musée des Dinosaures,
150
Espéraza, France; MMS/VBN, Musée Moulin Seigneurial /Velaux-La Bastide Neuve, Bouches-
151
du-Rhône, France; NHMUK, Natural History Museum, London, United Kingdom; UP, Université
152
de Poitiers, Vienne, France.
153
Anatomical Abbreviations: acdl, anterior centrodiapophyseal lamina; acpl, anterior
154
centroparapophyseal lamina; ADW, anterodorsal pterygoid wing; AVW, anteroventral
155
ectopterygoid wing; Bo, basioccipital; Bs, basisphenoid; cpol, centropostzygapophyseal lamina;
156
cprl, centroprezygapophyseal lamina; D, diapophysis; ICA, internal carotid artery; iped,
157
ischiadic peduncle; Ls+Os, laterosphenoid-orbitosphenoid complex; NS, neural spine; PA,
158
parapophysis; pcdl, posterior centrodiapophyseal lamina; pcpl, posterior centroparapophyseal
159
lamina; PO, postzygapophysis; pocdf, postzygocentrodiapophyseal fossa; podl,
160
postzygodiapophyseal lamina; posdf, postzygospinodiapophyseal fossa; posl, postspinal
161
lamina; pped, pubic peduncle; PR, prootic; prdl, posterior centrodiapophyseal lamina; PRE,
162
prezygapophysis; prsl, prespinal lamina; PVW, posteroventral quadrate wing; sdf,
163
spinodiapophyseal fossa; spof, spinopostzygapophyseal fossa; spol, spinopostzygapophyseal
164
lamina; sprf, spinoprezygapophyseal fossa; sprl, spinoprezygapophyseal lamina.
166
SC
M AN U
TE D
EP
AC C
165
RI PT
147
SYSTEMATIC PALAEONTOLOGY
167
Dinosauria Owen, 1842
168
Saurischia Seeley, 1887
169
Sauropoda Marsh, 1878
8
ACCEPTED MANUSCRIPT Titanosauriformes Salgado, Coria and Calvo, 1997
171
Titanosauria Bonaparte and Coria, 1993
172
Lithostrotia Upchurch, Barrett and Dodson, 2004
173
Lirainosaurinae new taxon
174
RI PT
170
Etymology. After the Spanish titanosaur Lirainosaurus astibiae.
176
Definition. Lirainosaurinae is phylogenetically defined as Lirainosaurus astibiae, Ampelosaurus
177
atacis, their common ancestor, and all of its descendants.
M AN U
178 179
SC
175
Atsinganosaurus velauciensis Garcia, Amico, Fournier, Thouand and Valentin, 2010
TE D
180
Holotype. UP/VBN.93.01.a–d: four articulated posterior dorsal vertebrae, housed in the
182
collections of the Université de Poitiers, France.
183
Referred specimens. Université de Poitiers, France: UP/VBN.93.12a–c: three cervical vertebrae;
184
UP/VBN.93.11: scapula; UP/VBN.93.10: metatarsal; UP/VBN.93.03-08: caudal vertebrae.
185
Musée Moulin Seigneurial /Velaux-La Bastide Neuve, France: MMS/VBN.02.03, 22 and 53:
186
teeth; MMS/VBN.02.78a–b: scapulocoracoid; MMS/VBN.02.99: isolated dorsal vertebra;
187
MMS/VBN.02.82: sacrum; MMS/VBN.02.109: tibia; MMS/VBN.02.110: caudal vertebra.
188
Musée Moulin Seigneurial /Velaux-La Bastide Neuve, France: MMS/VBN.00.12: humerus;
189
MMS/VBN.00.01-03: three caudal vertebrae.
AC C
EP
181
9
ACCEPTED MANUSCRIPT Muséum d’Histoire Naturelle d’Aix-en-Provence, France (donated by X. Valentin):
191
VBN.93.MHNA.99.21: tooth; VBN.93.MHNA.99.52: humerus; VBN.93.MHNA.99.32-34: caudal
192
vertebrae.
193
Type locality. La Bastide Neuve, Velaux; Aix-en-Provence Basin, Bouches-du-Rhône, France
194
(Figure 1A).
195
Type horizon. ‘Begudian’ (local stage) sandstones, upper Campanian, Upper Cretaceous (Garcia
196
et al. 2010, Cincotta et al., 2015).
SC
RI PT
190
197
Newly referred material. MMS/VBN.09.41: occipital condyle; MMS/VBN.09.167: braincase
199
fragment; MMS/VBN.09.158a: left pterygoid; MMS/VBN.93.33, MMS/VBN.12.A.006,
200
MMS/VBN.12.A.007, and MMS/VBN.12.B.014: four teeth; UP/VBN.93.13a and b,
201
MMS/VBN.09.D.007a, MMS/VBN.12.A.004, MMS/VBN.12.B.010, MMS/VBN.12.B.015: six
202
cervical vertebrae; UP/VBN.93.02, MMS/VBN.93.32, UP/VBN.09.157: three dorsal vertebrae;
203
MMS/VBN.93.31a, MMS/VBN.93.32b, MMS/VBN.00.14, MMS/VBN.00.15, MMS.VBN.09.46,
204
MMS/VBN.09.54, MMS/VBN.09.159b, MMS/VBN.09.D.003, MMS/VBN.09.D.009,
205
MMS/VBN.09.D.010, MMS/VBN.09.D.011, MMS/VBN.12.33, MMS/VBN.12.B.013a,
206
MMS.VBN.12.B.013b, MMS/VBN.12.B.018, MMS/VBN.12.C.003, MMS/VBN.12.C.004:
207
seventeen caudal vertebrae; MMS/VBN. 93.31b and MMS/VBN.93.32b: two haemal arches;
208
MMS/VBN.09.51a and b: two cervical ribs; MMS/VBN.09.D.07b and MMS/VBN.09.D.007c: two
209
dorsal ribs; MMS/VBN.09.66: sacral rib; MMS/VBN.09.124D: scapula; MMS/VBN.09.A.018: left
210
humerus; MMS/VBN.12.P.06a: right ulna; MMS/VBN.09.D.001: radius; MMS/VBN.09.113,
211
UP/VBN.93.09: two metacarpals; MMS/VBN.12.32: ilion; MMS/VBN.09.51c: right ischium;
212
MMS/VBN.09.126: right femur; MMS/VBN.02.90: left tibia; MMS/VBN.09.132: fibula.
AC C
EP
TE D
M AN U
198
10
ACCEPTED MANUSCRIPT 213
The fossil material is labelled and housed in the municipality palaeontological and
214
archaeological structures of Velaux, under the care of the research association Palaios, and is
215
property of the department CD (Conseil Départemental) 13.
216 Emended diagnosis. Pubic peduncle of the ilium with a posterior concave surface in its distal
218
half, surrounded by two sharp ridges. Recovered local autapomorphies from the phylogenetic
219
analysis: i) anterior and middle cervical vertebrae without pleurocoels (character #22), ii) ratio
220
between the anteroposterior length/height of posterior face of the posterior cervical
221
vertebrae higher than 3 (character #29), and iii) prominent ulnar olecraneon process,
222
projecting above the proximal articulation (character #61). None of the features of the former
223
diagnosis from Garcia et al. (2010) can longer be regarded as diagnostic for Atsinganosaurus
224
velauciensis.
M AN U
SC
RI PT
217
225 DESCRIPTION
227
Skull
228
Three skull fragments (Fig. 2) have been unearthed: an occipital condyle (MMS/VBN.09.41), a
229
right portion of the braincase (MMS/VBN.09.167), and a probable left pterygoid
230
(MMS/VBN.09.158a)
231
Occipital condyle. MMS/VBN.09.41 (Figure 2E) is a robust occipital condyle with a rounded
232
outline. The neck is not preserved, and the foramen for the hypoglossal nerve (XII) can only be
233
seen on the right side in dorsolateral view. It is a single opening, as seen in most titanosaurian
234
taxa (Paulina Carabajal, 2012; Poropat et al., 2016).
235
Braincase. MMS/VBN.09.167 seems to be a right fragment of a braincase, with portions of the
236
basioccipital, basisphenoid, prootic, and laterosphenoid (Figure 2A and B). However, this is a
AC C
EP
TE D
226
11
ACCEPTED MANUSCRIPT tentative identification, as no sutures are visible – there is a high level of fusion between the
238
bones – and all the foramina for the cranial nerves and fenestrae are collapsed. However,
239
some structures can be identified: grooves for the trigeminal (V) and facial (VII) nerves, and the
240
crista prootica in lateral view; the channel for the internal carotid artery in the basisphenoid;
241
and several grooves along the medial surface of the prootic, probably related with brain or
242
cranial nerve structures. The grooves for cranial nerves V and VII more closely resemble those
243
on the partial braincase MCNA 7439, referred to Lirainosaurus (Díez Díaz et al., 2011), than
244
those observed on the specimen FAM 03.064 from Fox-Amphoux-Métisson referred to
245
Titanosauria indet. (Díez Díaz et al., 2012b). Besides this, no more detailed comparisons can be
246
made due to the poor preservation of the specimen from Velaux.
247
Pterygoid. MMS/VBN.09.158a is a fragmentary skull bone that probably belongs to a left
248
pterygoid (Figure 2C and D). It is a flat triradiate element, the ends of which are not completely
249
preserved. Pterygoids have only been described in the titanosaurs Nemegtosaurus (Nowinski,
250
1971), Quaesitosaurus (Kurzanov and Bannikov, 1983), Rapetosaurus (Curry Rogers and
251
Forster, 2004), Tapuiasaurus (Zaher et al., 2011, Wilson et al., 2016), and Sarmientosaurus
252
(Martínez et al., 2016). MMS/VBN.09.158a shares its general morphology with them, like its
253
plate-like morphology (with its three processes coplanar), that seems to be a diagnostic
254
character within Titanosauria (Poropat et al., 2016). The lateral surface of MMS/VBN.09.158a
255
is slightly convex, and the medial one is flat. The anterodorsal pterygoid wing is the longest of
256
the three wings because of its preservation. It narrows distally, and forms an angle of 90° with
257
the anteroventral ectopterygoid wing. The anteroventral ectopterygoid wing becomes more
258
robust towards its distal end, forming an anterior bulge for the contact with the ectopterygoid.
259
In lateral view, at the junction between the three wings, a broken surface probably
260
corresponds to the lateral depression for contact with the palatine. The posteroventral
261
quadrate wing is not complete and poorly preserved. It forms an angle of ca. 130° with the
262
anterodorsal wing. Laterally, a shallow depression on the posteroventral quadrate wing marks
AC C
EP
TE D
M AN U
SC
RI PT
237
12
ACCEPTED MANUSCRIPT
the contact with the quadrate. No pterygoid remains have been described in other European
264
titanosaurians so far.
265
Teeth
266
Four new teeth have been found (MMS/VBN.12.A.006 and 07, MMS/VBN.12.B.014 and
267
MMS/VBN.93.33) (Figure 2F, Table 1). They are similar to those previously described in
268
Atsinganosaurus (see Garcia et al., 2010 and Díez Díaz et al., 2013c). They are peg-like, with
269
cylindrical crowns and a tapered tip. The lingual surface is flat, and the labial one convex. The
270
apex is slightly inclined lingually. An apical wear facet is present, with and angle of 60° in
271
relation with the apicobasal axis of the crown. This angle is similar to the ones calculated for
272
most of the titanosaurian teeth found in the Ibero-Armorican Island (see Díez Díaz et al. 2012a,
273
b, 2014). The enamel is smooth, with smooth longitudinal lines. The mesial and distal ridges
274
are more prominent in the distal third of the crown. There are no denticles or carinae present.
275
They clearly differ from other titanosaurian teeth described from the Ibero-Armorican Island
276
(see Díez Díaz et al. 2013c and 2014 for a more detailed comparison). These new teeth have a
277
similar SI (SI mean of the sample: 4.49) as the other teeth ascribed to Atsinganosaurus (SI
278
mean: 4.15; see Díez Díaz et al., 2013c). MMS/VBN.12.A.006 has a more slender and slightly
279
more labiolingually compressed crown than the other preserved teeth of Atsinganosaurus.
280
Cervical vertebrae
281
Six cervical vertebrae have been recovered, belonging to the anterior, middle and posterior
282
sections of the neck. All of them display the same general morphology as those originally
283
described by Garcia et al. (2010) (Figure 3A-C and E, Table 2). The centra are opisthocoelous,
284
with camellate internal texture, characteristic for Titanosauriformes (Upchurch, 1998; Wilson,
285
2002; Wedel, 2003; Upchurch et al., 2004; D'Emic, 2012). The prezygapophyses extend
286
anterior to the anterior tip of the condyle, contrary to some derived lithostrotians (Poropat et
287
al., 2016). Analyzing the changes on the EI we can elucidate a pattern in the cervical series: the
AC C
EP
TE D
M AN U
SC
RI PT
263
13
ACCEPTED MANUSCRIPT
centra shorten their length through the anterior to middle cervicals, becoming longer again in
289
the posterior ones, being even more transversally compressed than the first ones (although
290
this could be also due to preservation).
291
Anterior cervical vertebra. MMS/VBN.12.A.004, MMS/VBN.12.B.015 and MMS/VBN.09.D.007a
292
(this one found associated with two dorsal ribs) are anterior cervical vertebrae (Figure 3D, F
293
and G). The first one is the best preserved, but the main features are shared by all elements.
294
The left side of MMS/VBN.12.A.004 (Figure 3G) misses the tuberculum of the cervical rib, but
295
this structure is preserved in the right side of the specimen, together with a fragment of the
296
cervical rib (see below for a more detailed description). The centrum is long and has a sub-
297
quadrangular cross-section, especially its posterior half. The posterior ventral surface is flat,
298
whereas the anterior one is concave. The lateral surfaces, which are flat posteriorly and
299
concave anteriorly, do not present pneumatic foramina, contrary to Lohuecotitan (Díez Díaz et
300
al., 2016) and Magyarosaurus (NHMUK R. 4898). None of the specimens preserve the
301
postzygapophyses. The diapophyses and parapophyses are located on the anterior half of the
302
centrum. The parapophysis is located below the centrum. The dorsal surface of the
303
parapophysis is not excavated, but a shallow fossa is present on the lateral surface of the
304
centrum, above the parapophysis, in MMS/VBN.12.B.010 (Fig. 4C and C’). The prezygapophysis
305
is wide and robust, anterodorsally directed, and does not diverge too much from the centrum.
306
The neural spine is not completely preserved in any of them; it seems to be a single, laterally
307
compressed structure with a simple lamination. The lamination is the same that presumably
308
can be found in most sauropod cervical vertebrae: acpl, pcpl, pcdl, prdl in the centra, and podl,
309
sprl and spol in the spine. No acdl, prsl or posl are present. The fossae between these laminae
310
are very shallow with the exception of the spof, which is narrow and deep.
311
Middle to posterior cervical vertebrae. UP/VBN.93.13a and b were found in anatomical
312
connection. Because they are still embedded in the matrix, most of the structures on their
AC C
EP
TE D
M AN U
SC
RI PT
288
14
ACCEPTED MANUSCRIPT
right side cannot be seen. Both present the same general morphology, also together with the
314
anterior cervicals, but these are smaller and more slender. The cross-section of the centra is
315
more circular. The ventral surfaces of the centra are concave anteriorly and flat posteriorly, as
316
in Ampelosaurus. The diapophyses and parapophyses are better developed laterally, and the
317
parapophyses are slightly ventrally placed with respect to the centra. Both are still located on
318
the anterior half of the centra. The tubercula and capitula are preserved, but not the cervical
319
ribs. The prezygapophyses are only preserved in UP/VBN.93.13b; they are short and wide, and
320
directed anterodorsally. The postzygapophyses are broad, teardrop-shaped structures, whose
321
articulations are directed ventrally and slightly laterally. The single neural spines are higher,
322
and have a triangular outline in lateral view. There is a rugose thickening in the distal half of
323
the neural spine, maybe for tendinous attachment. The laminae and fossae complexes are
324
more developed than on the anterior cervicals: besides the laminae also present in the
325
anterior cervicals, the single cprl and cpol can be seen, together with an accessory lamina that
326
divides vertically a shallow posterior fossa below the pcdl. Shallow fossae are developed on
327
the dorsal surfaces of the parapophyses and below the diapophyses; on the lateral surfaces of
328
the centra, two additional fossae (anterior and posterior – the latter divided by an accessory
329
lamina) are present. The fossae on the neural spines are deeper than in the other European
330
titanosaurs (but not like the ones present in the Argentinean taxon Mendozasaurus, that are
331
even delimited by sharp-lipped laminae [González Riga et al., 2018]), like the triangular pocdf
332
between the pcdl and the podl, the sdf above the podl, and the spof.
333
Posterior cervical vertebra. Garcia et al. (2010) described three posterior cervical vertebrae:
334
UP/VBN.93.12a–c . Besides the new cervical found, we figure these three vertebrae again,
335
detailing the lamina and fossae complexes (Figure 3A-C and E). The new posterior cervical,
336
MMS/VBN.12.B.010 (Figure 4), is the smallest of the sample and the most posterior one, as
337
indicated by its shorter and lower centrum and its higher neural spine. In general terms, this
338
vertebra presents the same features as the other five cervicals. Although there is some
AC C
EP
TE D
M AN U
SC
RI PT
313
15
ACCEPTED MANUSCRIPT taphonomic deformation, we suggest that the centrum had a circular cross-section. The
340
ventral face of the centrum is also anteriorly concave and posteriorly flat. The ribs are missing,
341
but the diapophyses and parapophyses are preserved and ventrally directed. In this specimen,
342
the parapophyses are more anteriorly located on the centrum than the diapophyses, which are
343
located in the middle part of the centrum. The prezygapophyses are not well-preserved, but it
344
can be inferred that they were more anterodorsally directed than on the anterior cervicals.
345
Only the right postzygapophysis is preserved and dorsolaterally directed. There is also a rugose
346
thickening on the distal half of the neural spine, directed posterodorsally from the
347
postzygapophysis. The laminae are thicker than in the other cervicals, and the fossae are
348
slightly shallower than on the middle to posterior cervicals, with the exception of the lateral
349
pneumatic foramina, which are better developed on this vertebra. The posterior cervical
350
vertebra MDE C3-265, referred to Ampelosaurus, also has lateral pneumatic foramina. In
351
addition, the anterior side of the neural spine of MMS/VBN.12 B.010 has two sprls that define
352
a deep and narrow sprf between themselves. The posterior spof is similarly deep and narrow,
353
delimited by the spols. Ampelosaurus (MDE C3-265) also possesses a deep spof; however, this
354
fossa is much wider than in Atsinganosaurus, as is its neural spine overall. The cervicals of
355
Ampelosaurus also present a prsl (Le Loeuff, 2005).
SC
M AN U
TE D
EP
356
RI PT
339
The conservative pattern of the lamina and fossa complexes within the cervical series is noteworthy. This pattern is not present on the dorsal and sacral vertebrae, and different
358
patterns may occur in the same (right and left features) or in different individuals. This also
359
occurs in the vertebrae of Atsinganosaurus described by Garcia et al. (2010), and in the
360
titanosauriform Giraffatitan brancai (Wedel and Taylor, 2013; VDD pers. obs.).
361
Cervical ribs
362
A fragmentary cervical rib, probably a right one, is associated with MMS/VBN.12 A.004 (Figure
363
3G). The preserved fragment is slender, with the same width along most of its length (ca. 1.6
AC C
357
16
ACCEPTED MANUSCRIPT
cm). The lateral face is flat. However, we cannot infer the section of the specimen because it is
365
still hidden in the rock matrix. The preserved length is ca. 30 cm.
366
Dorsal vertebrae
367
None of the new dorsal vertebrae are completely preserved, but they closely resemble those
368
already described by Garcia et al. (2010) (see also Díez Díaz et al., 2013a, fig. 9C for the
369
laminae and fossae complexes and the comparison of UP/VBN.93.01b with other European
370
titanosaurs) (Figure 5A-C; Table 2). MMS/VBN.93.32 (Figure 5A) is an anterior neural arch
371
lacking the spine, UP/VBN.09.157 (Figure 5B) is a poorly preserved centrum with the base of
372
the neural arch, and UP/VBN.93.02 (Figure 5C) is a fragment of the left half of a middle to
373
posterior dorsal (in which the neural canal is not clearly visible, as it is obliterated). The dorsal
374
centra are opisthocoelous, with lateral eyed-shaped pleurocoels (set within a fossa), as in
375
other European titanosaurian taxa except Paludititan (Csiki et al., 2010; Díez Díaz et al., 2013a,
376
fig. 9). UP/VBN.09.157 likely had a ventral keel, unlike other European taxa. The inner
377
structure of the centra cannot be observed in any of the specimens, although the camellate
378
internal tissue is present in the anterior neural arch MMS/VBN.93.32. In this latter specimen,
379
the prezygapophyses are short and directed anterodorsally, but its posterior surface is
380
completely eroded. The neural canal is small and circular. The prezygapophyses are better
381
developed and laterally directed in Lirainosaurus (MCNA 7445; Díez Díaz et al., 2013a).
382
Although their distal ends are missing, the diapophyses are oriented dorsolaterally. Some
383
laminae can be seen in this specimen: single cprl, the base of the left sprl, pcdl, and podl. The
384
left pocdf and posdf are deep. The main difference between this specimen and Lirainosaurus
385
(MCNA 7445) is the presence of an acdl in the latter. In UP/VBN.93.02, the diapophyses appear
386
to be better developed and more robust. The postzygapophyses are small and their articular
387
surfaces face ventrally. The cpols are single, slender and vertical laminae. A pocdf is also
388
developed between the pcdl, the cpol, and the broken podl, and the posdf is shallower. In this
AC C
EP
TE D
M AN U
SC
RI PT
364
17
ACCEPTED MANUSCRIPT
specimen, only the base of the neural spine is preserved. In UP/VBN.09.157, a different lamina
390
pattern can be seen: together with the pcdl, an acdl is present and between them a triangular
391
fossa is present. In addition, as no matrix is present between the cpol and the pcdl, we observe
392
that the pocdf was so deep that it reached the inner structure of the neural arch, confirming
393
that these dorsal vertebrae were highly pneumatized. These lamina and fossa complexes are
394
also present in a posterior dorsal of Ampelosaurus (MDE C3-247). As in UP/VBN.93.02, the
395
posterior dorsals of Lirainosaurus are devoid of an acdl. However, the lateral pneumatic
396
foramina of this Iberian titanosaur are smaller. The main differences with the dorsal vertebrae
397
of Lohuecotitan are found on the ventral surface of the centrum, the laminae and fossae
398
complexes, and the development of the diapophyses (Díez Díaz et al., 2016, fig. 2. C-E).
399
Paludititan does not present a podl, but in general, its laminae and fossae complexes are more
400
complex than those of Atsinganosaurus.
401
Dorsal and sacral ribs
402
Two dorsal ribs (Figure 5D-G) were found associated with the anterior cervical vertebra
403
MMS/VBN.09.D.07a. They are flat (plank-like) and slender, although an important level of
404
crushing should be taken into account. One of them (the longest one: MMS/VBN.07.D.07b,
405
preserved length 58.5 cm) shows part of its tuberculum and capitulum separated by a
406
concavity. The preserved length of the other (MMS/VBN.09.D.007c) is 56 cm. No evidences on
407
pneumaticity can be assessed because of their preservation.
408
Only one fragmentary sacral rib (MMS/VBN.09.66) was recovered. It is probably one of first
409
ones from the left side, because of the development of a transverse foramen. In the sacrum
410
described by García et al. (2010), only the first three preserved sacrals present a transverse
411
foramen between the centra and the ribs. This element is anteroposteriorly compressed and
412
its acetabular arm is not completely preserved. Both costovertebral junctions with the
413
diapophysis and the parapophysis are preserved, although their ends are broken off. The
AC C
EP
TE D
M AN U
SC
RI PT
389
18
ACCEPTED MANUSCRIPT
capitulum is more slender than the tuberculum, which is bifurcated distally. The area between
415
the tuberculum and the capitulum (the transverse foramen sensu Wilson, 2011) is highly
416
concave.
417
Sacrum
418
The sacrum MMS/VBN.02.82 (Figure 6) was already described by Garcia et al. (2010), so here
419
we will point out some details that are not present in the former work.The ventral surfaces of
420
the sacral vertebrae present a ventral keel (Figure 6C). This sacrum is a robust and well-fused
421
specimen, as stated by huge fusion of the centra and neural spines, but also the presence of
422
thickened flat dorsal surfaces in the tuberculum of the sacral ribs. These surfaces are well-
423
differentiated from the rest of the sacral rib (Figure 6A and D). The laminae and fossae
424
complexes do not have the same patterns through all the sacral series, and are not even
425
symmetrical. A supraspinous rod (Figure 6A) runs distally through all the neural spines, as seen
426
in many other derived sauropods (see e.g. Cerda et al., 2015, fig. 7). Indeed, this rod could be a
427
diagnostic feature within Titanosauria (Poropat et al., 2016).
428
Caudal vertebrae
429
Seventeen new caudal vertebrae have been recovered (Figures 7 and 8, Table 2). All of them
430
are procoelous (with some exceptions in the posterior caudal vertebrae, that become slightly
431
amphicelous, like in MMS/VBN.93.32a [Figure 7V-X], UP/VBN.93.03 and UP/VBN.93.04 [Figure
432
8F-G]), a condition typically found in Lithostrotia (e.g. Salgado et al., 1997; Upchurch et al.,
433
2004; D’Emic, 2012). The presence of non-procoelous posterior caudal vertebrae
434
(amphicoelous, opisthocoelous and biconvex) has been found in other lithostrotian
435
titanosaurs, like Rinconsaurus caudamirus (Calvo and González Riga, 2003; VDD, pers. obs.) or
436
Opisthocoelicaudia skarzynskii (Borsuk-Białynicka, 1977). Their neural arches are placed
437
anteriorly on their centra, as in Titanosauriformes (e.g. Salgado et al., 1997; Wilson, 2002;
438
Upchurch et al., 2004), and are vertically oriented as in most lithostrotians (Carballido et al.,
AC C
EP
TE D
M AN U
SC
RI PT
414
19
ACCEPTED MANUSCRIPT 2017). As in most somphospondylans, these caudals do not present a hyposphenic ridge
440
(Upchurch et al., 2004, Carballido et al., 2011).
441
Anterior caudal vertebrae. Six anterior caudal vertebrae are preserved (MMS/VBN.93.31a
442
[Figure 7J-K], MMS/VBN.00.14 [Figure 7A-E], MMS/VBN.00.15 [Figure 7F-I], MMS.VBN.09.46,
443
MMS/VBN.09.54 [Figure 8B], MMS/VBN.12.C.004 [Figure 8A]). The broken surfaces of
444
MMS/VBN.09.54 allow observation of the camellate internal tissue of the centrum. None of
445
them have transverse processes, instead possessing lateral bulges located dorsally on the
446
centrum, close to the junction with the neural arch. This, together with the simple neural
447
spine, indicates a relatively more posterior position along the anterior caudal series, probably
448
close to the middle section of the tail. The centra are strongly procoelous with a well-
449
developed condyle, which is not constricted unlike in Lirainosaurus (Díez Díaz et al., 2013a) and
450
Lohuecotitan (Díez Díaz et al., 2016). In addition, this condyle is located in the middle of the
451
posterior articulation, which is not the case in Normanniasaurus and Paludititan, whose
452
condyles are dorsally displaced on the centra. The centrum of MMS/VBN.12 B.004 is sub-
453
quadrangular in cross-section, as in the caudal vertebrae found in Chera (Spain) and referred
454
to an indeterminate titanosaurian distinct from Lirainosaurus (see Díez Díaz et al., 2015), but
455
unlike other European titanosaurs. However, it is important to highlight that this is the only
456
similarity with the caudals of the second taxon from Chera. Longitudinal ridges are present in
457
the most anterior caudals (Figure 7D and H), and become less developed in the next ones in
458
the series. No longitudinal ridges or midline grooves are developed along the ventral face of
459
the posterior anterior centra (Figure 7Q), this is also the case in Lirainosaurus. The articular
460
surface for the the haemal arches is poorly preserved. MMS/VBN.12 B.004 lacks the right
461
prezygapophysis and the neural spine. The prezygapophyses of both specimens are directed
462
slightly anterodorsally, and the one of MMS/VBN.09.54 is broader. The neural spine is an
463
anteroposteriorly short, transversely-compressed, and slightly posterodorsally-directed
464
lamina. It is proportionally lower than the neural spines of the anterior caudals of
AC C
EP
TE D
M AN U
SC
RI PT
439
20
ACCEPTED MANUSCRIPT Lohuecotitan, and does not present the interzygapophyseal fossa seen in Normanniasaurus.
466
The postzygapophyses are triangular surfaces located posteriorly on the neural spine. They
467
closely resemble those described by Garcia et al. (2010). We consider that MMS/VBN.02.110 is
468
an anterior caudal because of the presence of transverse processes.
469
Anterior to middle caudal vertebrae. Three fragmentary middle caudals have been recovered:
470
MMS/VBN.09.D.009, MMS/VBN.09.D.011, MMS/VBN.12.B.018. Their morphology (procoelous
471
centra, low neural arches, and long and horizontal prezygapophyses) is not particularly
472
noteworthy within Titanosauria. Their ventral surfaces do not present any longitudinal ridges
473
or midline grooves, like in the anterior caudal vertebrae.
474
Posterior caudal vertebrae. Eight posterior caudal vertebrae have been found:
475
MMS/VBN.93.32a (Figure 7V-X), MMS/VBN.09.159.b (Figure 8E), MMS/VBN.09.D.003 (Figure
476
7R-U), MMS/VBN.09.D.010, MMS/VBN.12.B.013a, MMS/VBN.12.B.013b, MMS/VBN.12.C.003
477
(Figure 8C), MMS/VBN.12.33. Only MMS/VBN.12 B.013a and b were found associated. These
478
vertebrae are procoelous (with some exceptions, as seen above), unlike the shorter and
479
amphiplatyan centra on the posterior caudals of Paludititan. Their condyle is less developed
480
than on the anterior caudals, unlike in Lirainosaurus and Lohuecotitan, in which the posterior
481
caudals still have a constricted condyle located slightly dorsally on the posterior articular
482
surface of the centra (Díez Díaz et al., 2013a, fig. 6; Díez Díaz et al., 2016, fig. 3). The centra are
483
longer than the anterior caudals, but shorter dorsoventrally. The ventral surface of
484
MMS/VBN.09.159b is flat, and its articular surface for the haemal arches is prominent as in
485
Lohuecotitan (Díez Díaz et al., 2016). A ridge marks the junction between the neural arch and
486
the centrum, as also observed on the middle and posterior caudal vertebrae of Alamosaurus
487
(Gilmore, 1946), Ampelosaurus (Le Loeuff, 2005), Andesaurus (Mannion and Calvo, 2011),
488
Baurutitan (Kellner et al., 2005), Narambuenatitan (Filippi et al., 2011), and Normanniasaurus
489
(Le Loeuff et al., 2013). The neural spine is only preserved in MMS/VBN.12 B.013a; it is a
AC C
EP
TE D
M AN U
SC
RI PT
465
21
ACCEPTED MANUSCRIPT simple, laterally compressed lamina, more anteroposteriorly extended than in the anterior
491
caudals. In the other posterior caudals, the neural arch is incipient. The prezygapophyses are
492
long and slender, and almost horizontal. The postzygapophyses are located on the
493
posterodorsal tip of the neural spine, forming a triangular articular surface. These vertebrae
494
are different from the posterior caudals described by Garcia et al. (2010). However, because of
495
its dorsoventral compression and the presence of articulations for the haemal arches,
496
VBN.93.MHNA.99.33 is probably a middle to posterior caudal vertebra. We consider
497
MMS/VBN.93.3-8, described by Garcia et al. (2010), as distal caudal vertebrae because of their
498
typical spool-like morphology and the absence of neural arches. These six caudals were found
499
almost articulated.
500
Haemal arches
501
MMS/VBN.93.31b (Figure 7L-M) and MMS/VBN.93.32b (Figure 8Y-Z) are two haemal arches
502
found associated with the caudal vertebrae MMS/VBN.93.31a and MMS/VBN.93.32a
503
respectively. Both are open Y-shaped, as in most macronarians (Wilson, 2002; Curry Rogers,
504
2005; Mannion and Calvo, 2011; Otero et al., 2012). The haemal canal does not reach the
505
middle of the total length of both arches, contrary to the ones referred to Paludititan. The
506
distal blades are transverselly flattened distally, contrary to Lirainosaurus. Although the
507
proximal articular faces are not completely preserved it is visible that they are not divided in
508
two articular faces, as the ones of Lohuecotitan.
509
Pectoral girdle
510
Scapula. Besides the fragmentary scapulocoracoid (MMS/VBN.02.78a–b, Figure 9A-B) and the
511
scapula (MMS/VBN.93.11, Figure 9C), previously described by Garcia et al. (2010), another
512
fragmentary right scapula (Figure 9D) has been found, which likely belonged to a juvenile
513
individual (MMS/VBN.09.124D). It consists of the proximal third of the scapular blade and part
514
of the acromial blade. Its medial surface is concave (no ridges or prominences present),
AC C
EP
TE D
M AN U
SC
RI PT
490
22
ACCEPTED MANUSCRIPT
whereas its lateral side is convex, with a rounded and longitudinal ventral ridge. No triangular
516
processes on the ventral margin are present.
517
Forelimb
518
Humerus. MMS/VBN.00.12 (Figure 10A-D) is a right humerus, and MMS/VBN.09.A.018 (Figure
519
10E-H, Table 3) a left one This second one has poorly preserved proximal and distal edges and
520
deltopectoral crest. Their diaphyses are slender and anteroposteriorly compressed. The
521
posterior surface is convex, and the anterior one concave. No bulges or tuberosities are
522
present in the posterior surface of the proximal third of MMS/VBN.09.A.018, contrary to
523
MMS/VBN.00.12, which presents a tuberosity close to the lateral margin of the posterior
524
surface, at approximately the level of the distal tip of the deltopectoral crest. This tuberosity
525
was probably for the insertion of m. latissimus dorsi (Borsuk-Bialynicka, 1977; Otero, 2010;
526
D’Emic, 2012) No other prominences or ridges are visible or present in the anterior and
527
posterior surfaces of these specimens. The distal edge of the deltopectoral crest is located
528
above the middle of the diaphysis, as in Lirainosaurus, Ampelosaurus, and Magyarosaurus (Le
529
Loeuff, 2005; Díez Díaz et al. 2013b; VDD pers. obs.). The deltopectoral crest doubles its
530
thickness distally, and it is slightly deflected medially. The diaphysis of this specimen seems
531
more slender than in other European titanosaurs. A more detailed comparison is not possible
532
due to the preservation of the proximal and distal ends of the specimen. However, the
533
slenderness of the diaphysis (ECC [eccentricity index, sensu Wilson and Carrano, 1999]: 3.76)
534
and the relative development and position of the deltopectoral crest resemble the condition in
535
MMS/VBN.00.12 (ECC: 3.14), described by Garcia et al. (2010) as belonging to Atsinganosaurus
536
(figure 6A). VBN.93.MHNA.99.52 is a fragmentary right humerus (Figure 10I-J) that was not
537
described by Garcia et al. (2010). The anterior surface is not well-preserved, the proximal end
538
is eroded and the distal extremity is lost. The posterior surface is better preserved, but no
539
special features can be seen.
AC C
EP
TE D
M AN U
SC
RI PT
515
23
ACCEPTED MANUSCRIPT
Ulna. MMS.VBN.12.P.06a is a slender right ulna (Figure 10K-P), Table 3), with a broad proximal
541
end. This end has a triradiate outline (forming an angle of almost 90° between the longest
542
arms, which are not completely preserved), although its articular surface is not preserved. The
543
posterior process is well-developed. The olecranon process is better developed than in
544
Lirainosaurus and the ulna C3-1296 of Ampelosaurus, more closely resembling the condition in
545
C3-1490. The well-developed proximal processes delimit three shallow surfaces that extend
546
along the diaphysis up to the distal extremity, which is only slightly expanded and not
547
completely preserved (the presence of an anteromedial fossa for the reception of the radius
548
cannot be assessed).
549
Radius. MMS/VBN.09.D.001 (Figure 10Q-R) is a fragmentary diaphysis of a radius, and has a
550
cylindrical cross-section. No more features can be described due to its poor preservation.
551
Metacarpals. Only two metacarpals I (MMS/VBN.09.113 and UP/VBN.93.09) have been
552
recovered (Figure 11, Table 4); the second specimen is much smaller, likely belonging to an
553
immature individual. Both specimens are poorly preserved, and their proximal and distal ends
554
are missing. MMS/VBN.09.113 was probably a left metacarpal, as suggested by the position of
555
its articular surface for metacarpal II. The diaphyses are long and anteroposteriorly
556
compressed, as in Bonatitan (Salgado et al., 2015) and Rapetosaurus (Curry Rogers, 2009),
557
contrasting with the metacarpals of Magyarosaurus, which have a more rounded cross-
558
section. Metacarpal I of Epachthosaurus (Martínez et al., 2004) is more robust, and its
559
diaphysis is not compressed. The diaphyses are straight, as in the derived titanosaurs
560
Bonatitan, Epachthosaurus, Rapetosaurus, and Opisthocoelicaudiinae (Apesteguía, 2005) and
561
unlike the bowed morphology in the basal taxa Andesaurus (Mannion and Calvo, 2011),
562
Antarctosaurus (Huene, 1929), Argyrosaurus (Mannion and Otero, 2012), and Malawisaurus
563
(Gomani, 2005). The proximal and distal ends are mediolaterally expanded; the proximal end is
564
also anteroposteriorly compressed, as in other titanosaurs, e.g. Andesaurus and Rapetosaurus.
AC C
EP
TE D
M AN U
SC
RI PT
540
24
ACCEPTED MANUSCRIPT Pelvic girdle
566
Ilium. One fragmentary right ilium is preserved (MMS/VBN.12.32) (Figure 12A-B). It consists of
567
the dorsal part of the acetabulum, ventral fragments of the pre- and postacetabular processes
568
of the iliac blade, and the pubic peduncle. The preacetabular process is slightly horizontal
569
(more than in other titanosaurs) and laterally projected, and has a ventral ridge that ends
570
above the acetabulum, contrary to the ilia of Lirainosaurus and Lohuecotitan, which have a
571
vertical preacetabular lobe. The postacetabular process is vertical. The pubic peduncle
572
(anteroposterior length: 7.8 cm; transversal length: 8.7 cm) is robust, becomes broader
573
towards its distal end, and has a C-shaped cross-section. The posterior surface of the distal half
574
of the peduncle is particularly concave and surrounded by two sharp ridges. This morphology is
575
not known in any other titanosaur, and is consequently considered as an autapomorphy of
576
Atsinganosaurus. The lateral ridge extends through the dorsal edge of the acetabulum and
577
runs through the ventral edge of the preacetabular lobe. There is no triangular hollow at the
578
base of the pubic peduncle, contrary to Lirainosaurus (Díez Díaz et al., 2013b). The acetabulum
579
is not as strongly concave as it is in Paludititan. Both ilia are pneumatized, as in Lirainosaurus
580
(Díez Díaz et al., 2013b), Diamantinasaurus (Poropat et al. 2015) and derived titanosaurs (see
581
Cerda et al., 2012). However, this could be a synapomorphy of a more inclusive clade than just
582
Titanosauria, as Euhelopus also has pneumatized ilia (see Wilson and Upchurch, 2009;
583
Mannion et al., 2013).
584
Ischium. One right ischium (MMS/VBN.09.51c) has been recovered (Figure 12C-E, Table 5). The
585
iliac peduncle is incompletely preserved, its distal edge is missing. The plate-like morphology of
586
this element, and the absence of an emargination along the anterior margin of the ischiadic
587
blade, are common features in titanosaurs (Wilson, 2002; Upchurch et al., 2004; González Riga
588
et al., 2009). The acetabular margin is almost flat, as also observed in Ampelosaurus (Le Loeuff,
589
2005, Fig. 4.17), and it is not well differentiated from the iliac peduncle. This feature is
AC C
EP
TE D
M AN U
SC
RI PT
565
25
ACCEPTED MANUSCRIPT interesting to analyze more carefully, as an acute acetabular margin is a diagnostic feature
591
within Lithostrotia (see D’Emic, 2012). Both Atsinganosaurus and Ampelosaurus are grouped
592
together in our phylogenetic analysis (see below), so maybe we are talking about a diagnostic
593
feature within these French taxa. The iliac peduncle is slender and well developed, contrasting
594
with the wider and more robust peduncles in Ampelosaurus and Paludititan. The pubic
595
peduncle is poorly preserved, but seems continuous with the anteroventral edge of the
596
ischium. The ischia of Ampelosaurus and Paludititan are boomerang-shaped and their pubic
597
peduncle is well differentiated from their distal blade. At the base of the iliac peduncle, a
598
lateral tubercle (with a groove associated, as in Titanosauriformes [Poropat et al., 2016]) is
599
present near the posterior edge of the proximal part of the blade. This lateral ridge could
600
correspond to the bulge interpreted by Borsuck-Białynicka (1977) as the attachment point for
601
m. flexor tibialis internus III (see also Poropat et al., 2015). This lateral tubercle or tuberosity
602
seems to be a diagnostic feature within Titanosauria (Carballido et al., 2017). At about the
603
middle of the ischiadic blade, near its ventral margin, a lateral ridge is present. The ischiadic
604
blade is a straight plate, whose thickness decreases towards its distal edge.
605
Hindlimb
606
Femur. MMS/VBN.09.126 is the diaphysis of a right femur (Figure 13A-B, Table 3). Its proximal
607
and distal extremities are not preserved, but a low and poorly developed fourth trochanter is
608
present posteromedially, as in Lirainosaurus and Ampelosaurus, and contrasting with the more
609
centrally-situated fourth trochanter in Lohuecotitan. The diaphysis seems wider than in the
610
Spanish taxa, but more lateromedially developed than in Ampelosaurus (e.g. C3-87).
611
Tibia. MMS/VBN.02.90 is a left tibia (Figure 13C-H, Table 3). This bone was previously
612
identified as a metacarpal by Garcia et al. (2010), but it is highly similar as MMS/VBN.02.109
613
(although this last specimen is larger [Figure 13K-P]). This bone is slender, with an expanded
614
proximal third and a distal extremity with a triangular outline in distal view. Both articular
AC C
EP
TE D
M AN U
SC
RI PT
590
26
ACCEPTED MANUSCRIPT
surfaces are poorly preserved, but the shallow surface of the anterolaterally-projected cnemial
616
crest can be observed. No “tuberculum fibularis” can be seen in the internal face of the
617
cnemial crest. A second cnemial crest is absent too, as is the case of most somphospondylans
618
and diplodocoids (Mannion et al., 2013). Its proximal end appears compressed as in
619
Lirainosaurus, contrasting with the more rounded ones in Lohuecotitan and Ampelosaurus.
620
Distally, a prominent anteromedial ridge delimits two concave surfaces, as in Lirainosaurus
621
(MCNA 2203).
622
Fibula. MMS/VBN.09.132 is the proximal third of a fibula (Figure 13I-J, Table 3). It is more
623
expanded than the diaphysis and slightly lateromedially compressed, as in Lirainosaurus and
624
Ampelosaurus, and unlike in Lohuecotitan. Its lateral surface is convex, whereas its poorly
625
preserved medial surface is flat to slightly concave. The lateral trochanter is not preserved.
626
Metatarsal. The left metatarsal I (UP/VBN.93.10; Figure 14, Table 4) was only briefly described
627
by Garcia et al. (2010). It is a robust element, with expanded proximal and distal edges. Its
628
shaft is more slender than in other titanosaurs (e.g. Rapetosaurus, Epachthosaurus [Martínez
629
et al., 2014], Bonitasaura [Gallina and Apesteguía, 2015], Notocolossus [González Riga et al.,
630
2016], or Mendozasaurus [González Riga et al., 2018]). Its proximal surface is quadrangular in
631
outline. The proximal and distal medial surfaces are slightly concave for articulation with
632
metacarpal II. The distal articular surface is poorly preserved, but apparently had a comma-
633
shaped outline. In lateral view, a ridge extends from the middle of the shaft down to the
634
posterior edge of the distal articular surface. It also presents a prominent ventrolateral
635
expansion along its distal half, such that the distal end expands further laterally than the
636
proximal end.
AC C
EP
TE D
M AN U
SC
RI PT
615
637 638
HISTOLOGICAL OBSERVATIONS
27
ACCEPTED MANUSCRIPT 639
All Atsinganosaurus sections display a similar bone histology, dominated by heavy remodelling
640
of the primary bone and several cross-cutting generations of secondary osteons (sensu Stein et
641
al., 2010 and Mitchell et al., 2017; Figure 15A-B). No pristine in situ trabecular structures can be identified because the transition
643
between the medullary cavity and the innermost cortex is abrupt and goes from broken
644
trabeculae (sometimes embedded in sediments [Figure 15C]) to crushed, distorted secondary
645
osteons.
SC
RI PT
642
The secondary osteons are mature, rounded to elliptical in shape, and composed of
647
successive layers of alternating bone lamellae (as seen under cross polarized light, type two
648
osteons sensu Ascenzi and Bonucci, 1968; Figure 15A). The elliptical osteons have the long axis
649
preferentially oriented parallel to the periosteal surface in transverse section, a feature also
650
seen in other titanosaurs (e.g. Phuwiangosaurus sirindhornae and Ampelosaurus atacis in Klein
651
et al., 2009 and Klein et al., 2012a respectively). In long bones of A. velauciensis, four to five
652
generations of secondary osteons can be recognized in the innermost cortex, five to six
653
generations in the mid-cortex and four to six generations in the outer cortex (see Table 6
654
below for details – Fig. 15B). No open resorption cavities were observed in the innermost
655
cortex in any of the samples. Instead, the innermost cortex is often characterized by irregular
656
secondary osteons which are found with broken trabeculae. MMS/VBN.09.126 and
657
MMS/VBN.09.A.018 are the best sections showing the broken trabeculae.
TE D
EP
AC C
658
M AN U
646
All samples except MMS/VBN.09.A.018 show some patches of primary tissue. These
659
patches are mostly confined to the outer cortex. However, no unambiguous primary vascular
660
canals can be seen in any of these patches. It is possible that the outermost µm of the cortical
661
samples are missing because of weathering or mechanical preparation.
662 663
Following Klein and Sander (2008) and Stein et al. (2010), the studied specimens match the Histologic Ontogenetic Stage (HOS) 14 because of the complete remodelled type H bone
28
ACCEPTED MANUSCRIPT 664
tissue of the cortices (Fig. 15A, E and F). Dense secondary osteons are clearly visible even
665
macroscopically as purple dots in Fig. 15E. Given the multiple cross-cutting secondary osteon
666
generations throughout the cortex, the Remodelling Stages (RS) (sensu Mitchell et al., 2017)
667
are ranging from RS 13 to 14. Longitudinal sections (Figure 15D-F) were made to complement data from the
RI PT
668
transverse sections, in particular to verify any preferential orientation of the secondary
670
osteons. Their oval shape in transverse section could be either the result of a section plane at a
671
slight angle to the ideal transverse section (Mitchell et al., 2017) or of the 3D geometry of the
672
osteons not correlating to the long bone axis. The osteonal boundaries are more difficult to
673
see, and so are the different cross-cutting generations. The cortices yield a widespread
674
remodelled histology with very elongated secondary osteons meaning they are mainly
675
oriented along the long bone axis (purple lines in Fig. 15F). Some secondary osteons have an
676
ellipsoid appearance, which implies they are oriented oblique to the long bone axis.
M AN U
The histology of a putative cervical rib (MMS/VBN.09.51a and b) is characterized by
TE D
677
SC
669
strong remodelling features, and only a small part of the original ossified tendon matrix is still
679
present (Figure 16). Numerous tensile secondary osteons (sensu Ascenzi and Bonuci, 1968)
680
with smooth cement lines make up the most significant part of the tissue, some of them
681
showing cross-cutting relations. However, interstitially, small areas remain unremodelled and
682
show densely packed collagen fibre bundles, similar to those in the ossified tendons of
683
hadrosaurs (Adams and Organ, 2005; Organ and Adams, 2005) and elongated cervical ribs of
684
other sauropod dinosaurs (Cerda, 2009; Klein et al., 2012b).
685
AC C
EP
678
In a longitudinal section (Figure 16), the longitudinal vascular canals of the secondary
686
osteons are dominant features, and the osteons have longitudinally oriented osteocyte
687
lacunae with faint but numerous branching canaliculi. In between the longitudinally oriented
29
ACCEPTED MANUSCRIPT 688
osteons, fibre bundles with fibrocyte lacunae can be observed. These features complement the
689
cross sectional view and are furthermore reminiscent of ossified tendons.
690
Taking into account the strongly elongated morphology, parallel occurrence in the sediment and ossified tendinous histology of the two described elements, there can be little
692
doubt that they represent the ossified tendons of sauropod cervical ribs.
RI PT
691
693
695
PHYLOGENETIC ANALYSIS
SC
694
The result of this phylogenetic analysis with 29 sauropod taxa yielded a single MPT of 166 steps, with a consistency index (CI) of 0.572 and a retention index (RI) of 0.665 (Figure 17).
697
The general topology is similar to the one obtained by Salgado et al. (2015), but with two main
698
differences: i) the diagnosis of Lithostrotia has been resolved, with Malawisaurus placed in a
699
more derived position than Andesaurus (and therefore within Titanosauria); ii) the derived
700
clade Saltasauridae has been divided, with Opisthocoelicaudiinae regarded as a more basal
701
group than Saltasaurinae (this split can be also seen in the analysis of Sallam et al. 2018).
702
Another notable difference with previous phylogenetic analyses is the recovery of
703
Lognkosauria within Rinconsauria. Similar results were obtained by González Riga et al. (2018),
704
resolving Lognkosauria as the sister taxon of Rinconsauria. The phylogenetic relationships of
705
this clade seem more difficult to solve, as it has been placed as a basal clade within Lithostrotia
706
(Calvo et al., 2007, González Riga et al., 2009), or as more derived lithostrotians (González Riga
707
et al., 2016) related with Aeolosaurini (González Riga and Ortiz, 2014) or with Rinconsauria
708
(Salgado et al., 2015). However, this discussion is beyond the scope of this paper; herein, we
709
focus on the relationships between the European taxa.
710 711
AC C
EP
TE D
M AN U
696
European taxa were almost completely neglected in previous titanosaurian phylogenies: Sallam et al. (2018) include all of the Late Cretaceous European taxa, but before
30
ACCEPTED MANUSCRIPT
this work only few included Lirainosaurus and Ampelosaurus together (see e.g. Powell, 2003;
713
Curry Rogers, 2005), and most of the time separately or scored only from the literature (see
714
e.g. González Riga, 2003; Upchurch et al., 2004; Bonaparte et al., 2006; Calvo et al., 2007;
715
González Riga et al., 2009; Hocknull et al., 2009; Csiki et al., 2010). As previously suggested by
716
Bonaparte et al. (2006), González Riga et al. (2009), Gallina and Apesteguía, (2011), Salgado et
717
al. (2015), and Sallam et al. (2018), the present analysis recovers Lirainosaurus as a member of
718
Lithostrotia, whereas it was regarded as a derived titanosaur more closely related to
719
Saltasauridae by Upchurch et al. (2004), Calvo et al. (2007), Csiki et al. (2010), and Filippi et al.
720
(2011), or even a member of the saltasaurid clade by Hocknull et al. (2009) and Díez Díaz et al.
721
(2013d). In our analysis, Lirainosaurus appears as a lithostrotian closely related to a clade
722
formed by the French titanosaurs Ampelosaurus and Atsinganosaurus. This clade is here
723
named Lirainosaurinae nov. Both French titanosaurs have been included in a few analyses
724
(only together in Sallam et al. (2018)), and their relationships have not been well studied (e.g.
725
Powell, 2003; Curry Rogers, 2005; Sallam et al. 2018). Díez Díaz et al. (2013d) suggested that
726
French titanosaurs were basal lithostrotians and that Lirainosaurus a member of
727
Opisthocoelicaudiinae. However, Díez Díaz (2013) scored these three titanosaurs in two
728
previously published matrices (Bonaparte et al., 2006; González Riga et al., 2009), and in both
729
phylogenetic hypotheses the three taxa appeared closely related. Lohuecotitan and Paludititan
730
are grouped together as basal lithostrotians. The phylogenetic affinities of Paludititan are not
731
well resolved (Csiki et al., 2010), and Lohuecotitan has only been scored in Díez Díaz et al.
732
(2016) and Sallam et al. (2018), so few comments can be made here, besides the lack of
733
affinities of Lirainosaurus with the French taxa. The Early Cretaceous French taxon
734
Normanniasaurus is nested within Titanosauria, but not within Lithostrotia.
AC C
EP
TE D
M AN U
SC
RI PT
712
735 736
DISCUSSION
31
ACCEPTED MANUSCRIPT
After the detailed study and comparison of the specimens published by Garcia et al. (2010) and
738
the ones described in this work, an emended diagnosis of A. velauciensis is suggested. The new
739
diagnosis focuses on the ilium: pubic peduncle of the ilium with a posterior concave surface in
740
its distal half, surrounded by two sharp ridges. Three isolated humeri (the most recurring non-
741
axial bone in the site) have been found, so at least three individuals of Atsinganosaurus are
742
present at Velaux-La-Bastide Neuve. However, besides the holotype, no other remains were
743
found associated or articulated, so their referral to each individual it is not possible. It should
744
be noted that further titanosaurian remains have been found at Velaux-La Bastide Neuve and
745
they present several divergences (especially humeri and an ulna) with the holotype and
746
material referred to Atsinganosaurus velauciensis by Garcia et al. (2010). The remains ascribed
747
to this possible new taxon were most of them found in the same level as the ones belonging to
748
Atsinganosaurus, with the exception of one almost complete sacrum and a humerus, that
749
were recovered from a second level (2 meters above the former one). This new material is
750
currently under study.
751
Estimation of Body Size and Mass for Atsinganosaurus velauciensis
752
As we have recovered several humeri and femora we can hypothesize the body size and mass
753
for Atsinganosaurus. For the body mass and size we have used the equations proposed by
754
Seebacher (2001) for size, and Packard et al. (2009) and Campione and Evans (2012) for mass,
755
in which M(g) = 3.352PerH+F2,125, M(kg) = 214.44L(m)1.46, and logM(g) = 2.754logPerH+F −
756
1.097, where M: body mass, PerH+F: sum of the perimeters of the humerus and femur in mm,
757
L: body length. With the smallest humerus and femur we obtain a size of 6.45 meters, and a
758
mass of 2.46 tonnes (sensu Packard et al., 2009) and 3.2 tonnes (sensu Campione and Evans,
759
2012), whereas with the largest specimens the results are 14.54 meters, and 3.661 tonnes
760
(sensu Packard et al., 2009) and 5.26 tonnes (sensu Campione and Evans, 2012).
AC C
EP
TE D
M AN U
SC
RI PT
737
32
ACCEPTED MANUSCRIPT 761
We tentatively propose a body length of ca. 8-12 meters for the adults of Atsinganosaurus, or as much as 14 meters for the largest individuals, and a body mass of ca.
763
3.5-5 tonnes. Although it is a sauropod of small size, it probably doubled (or even tripled) the
764
length of Lirainosaurus (4 meters and 2-4 tonnes, Díez Díaz et al., 2013b).
765
Ontogeny and Dwarfism
766
In general, all sampled specimens of A. velauciensis show very similar histological features.
767
Clearly, the samples do not represent a growth series and are all of comparable developmental
768
stages. The histology of A. velauciensis is comparable to that of the small European titanosaurs
769
Lirainosaurus astibiae (adult specimen descriptions in Company, 2011, fig. 5) and
770
Magyarosaurus dacus (Stein et al., 2010).
SC
M AN U
771
RI PT
762
Heavy remodelling is the main histological pattern in the long bones of A. velauciensis. This mature histology suggests that these individuals were fully grown. Considering the
773
reduced size of the femur and humeri, the remodelling process would have begun early in the
774
ontogeny of this titanosaur compared to non-titanosaurian sauropods, at a rate that surpassed
775
the apposition rate. This is consistent with the histology of juveniles of the titanosaur
776
Rapetosaurus krausei (Rogers et al., 2016). If the haversian bone deposition rate is assumed to
777
be constant throughout ontogeny (Mitchell and Sander, 2014), the combination of a slow
778
apposition rate with heavy remodelling prior to the final size involves some kind of size
779
reduction and/or insular dwarfism comparable to other titanosaurs in the Cretaceous
780
European archipelago (e.g. Lirainosaurus astibiae, Magyarosaurus dacus; Company, 2011;
781
Stein et al., 2010).
AC C
EP
TE D
772
782 783
Palaeobiogeographical considerations
33
ACCEPTED MANUSCRIPT 784
Our new phylogenetic results shed light on the palaeobiogeographical patterns of the
785
titanosaurian faunas from the Ibero-Armorican Island. With these results we can suggest two
786
different scenarios:
787
1) Csiki-Sava et al. (2015) commented that European titanosaurs do not seem to have a southern influence, but in our analysis we have found that Lohuecotitan and
789
Paludititan are grouped together close to the basal African lithostrotian Malawisaurus.
790
Works on the Cretaceous titanosaurian faunas from Africa (see Gorscak et al. 2014,
791
2017; Lamanna et al., 2017; and works in progress) will help to clarify soon the
792
relationships of these faunas with the Late Cretaceous European ones. Indeed, the
793
titanosaur Mansourasaurus from the Late Cretaceous of Egypt seems to be closely
794
related to Lohuecotitan (Sallam et al., 2018), supporting sauropod dispersal between
795
Europe and Africa in the terminal Cretaceous. Therefore, a Gondwanan influence
796
cannot be discarded; this has been also previously posited for other groups of reptiles
797
(Pereda Suberbiola, 2009).
SC
M AN U
TE D
798
RI PT
788
2) The case of the more derived lithostrotians Lirainosaurus and the French taxa
800
Ampelosaurus and Atsinganosaurus is likely different. This group, here named
801
Lirainosaurinae, could lead to a possible endemicity in the Ibero-Armorican Island, and
802
that is why Lirainosaurus (late Campanian) and the French titanosaurs (late
804
AC C
803
EP
799
Campanian-early Maastrichtian) appear to be closely related. As Pereda et al. (2009)
and Mannion and Upchurch (2011) suggested, Late Cretaceous European dinosaurs
805
could be relictual lineages of Laurasian faunas, and Lirainosaurinae could be a good
806
example of this. It is also possible that the late Maastrichtian taxa found in the
807
Pyrenean region (northern Spain and southern France) and southeastern France (i.e.
808
Vitrolles la Plaine, Valentin et al., 2012) evolved from these titanosaurs known from
809
late Campanian–early Maastrichtian faunas.
34
ACCEPTED MANUSCRIPT 810
These hypotheses represent a solid foundation for future phylogenetic and
811
palaeobiogeographical analyses incorporating the Cretaceous European titanosaurian faunas,
812
following on from palaeobiogeographic analyses primarily focused on titanosaurs from
813
elsewhere (e.g. Gorscak et al. 2016; Poropat et al. 2016).
RI PT
814 CONCLUSIONS
816
In this work we describe new titanosaurian cranial and postcranial remains found in the Upper
817
Cretaceous site of Velaux-La Bastide Neuve (southern France), which are referred to
818
Atsinganosaurus velauciensis. This new material has allowed us to better define the
819
morphological features of this taxon and emend its diagnosis, thereby helping us to better
820
understand the sauropod faunas that inhabited the Ibero-Armorican Island.
M AN U
SC
815
Long bones of Atsinganosaurus velauciensis are heavily remodelled (HOS 14, RS
822
ranging from stage 13 to 14). The sampled specimens of A. velauciensis were fully grown. The
823
small size but mature nature of the specimens might be linked to insular dwarfism, as seen in
824
Magyarosaurus or Lirainosaurus. However, Atsinganosaurus was larger than these two taxa, as
825
shown by its hypothesized body size and mass: ca. 8-12 meters for the adults, or as much as 14
826
meters for the largest individuals, and ca. 3.5-5 tonnes.
EP
AC C
827
TE D
821
A phylogenetic analysis with 29 sauropod taxa was performed, with the European
828
titanosaurs Atsinganosaurus, Ampelosaurus, Lirainosaurus, Lohuecotitan, Paludititan (Late
829
Cretaceous) and Normanniasaurus (Early Cretaceous) all scored for the same analysis for the
830
first time. Atsinganosaurus and Ampelosaurus form a clade closely related to Lirainosaurus
831
within Lithostrotia, whereas Lohuecotitan and Paludititan are grouped together as basal
832
lithostrotians. Lirainosaurinae is defined here for the first time as Lirainosaurus astibiae,
833
Ampelosaurus atacis, their common ancestor, and all of its descendants. Atsinganosaurus
35
ACCEPTED MANUSCRIPT 834
velauciensis appears within this clade, as sister taxon of Ampelosaurus. As for
835
Normanniasaurus, it is nested within Titanosauria but not within Lithostrotia. From a palaeobiogeographical perspective, the phylogenetic results suggest that
837
European titanosaurs belong to at least three distinct lineages and that two lithostrotian
838
lineages were present during the latest Cretaceous in the European archipelago. Although the
839
“African origin” of the latest Cretaceous re-invasion of Europe is not well-supported by other
840
groups of tetrapods (see Mannion and Upchurch, 2011 and references therein), the results
841
obtained in this work and the one published by Sallam et al. (2018) shed some light on one
842
possible dispersal route between North Africa and Europe during the Cenomanian–Campanian.
843
More works on the African titanosaurs are needed to test if these African faunas are closely
844
related with other South American titanosaurian clades, as previously hypothesized by
845
Mannion and Upchurch (2011). On the other hand, Lirainosaurinae could be a relictual lineage
846
of Laurasian sauropod faunas. To assess these hypotheses more inclusive (with more Late
847
Cretaceous Laurasian taxa, together with the African and European ones) phylogenetic and
848
paleobiogeographical should be done.
SC
M AN U
TE D
849
RI PT
836
The diversity of the titanosaurian faunas from the Late Cretaceous of Europe, and more specifically from the Ibero-Armorican Island, has been an important research issue since
851
the last years of the 19th century (see e.g. Le Loeuff, 1993), always suggesting a higher
852
diversity than previously thought. According to the findings of these last years, especially in
853
Spain, France, and Romania, this diversity has been increased to, at least, seven titanosaurian
854
taxa in the Campanian-Maastrichtian of Europe. However, new findings and reanalyses of
855
previously published material will no doubt increase this further.
AC C
EP
850
856 857
ACKNOWLEDGMENTS
36
ACCEPTED MANUSCRIPT
M. Moreno-Azanza (Universidade Nova de Lisboa, Portugal) helped in the development of the
859
phylogenetic analysis. VDD would like to thank V. Fondevilla (ICP, Spain) for the useful
860
discussions on titanosaurian faunas and stratigraphy. We would like to acknowledge A.
861
Montaufier for the photographs (with financial support of the Lisea-Vinci group), and C. Zafra
862
for editing the figures. We thank J. C. Corral and J. Alonso (Museo de Ciencias Naturales de
863
Álava/Arabako Natur Zientzien Museoa, Vitoria-Gasteiz, Spain), B. Madarieta (Museo Vasco de
864
Historia de la Medicina y de las Ciencias of Leioa, Spain), F. Ortega (Grupo de Biología
865
Evolutiva, Universidad Nacional de Educación a Distancia, Spain), J. Le Loeuff (Musée des
866
Dinosaures d’Espéraza, France), P. Barrett (Natural History Museum, U.K.), and B. González
867
Riga (IANIGLA, CRICyT, Mendoza, Argentina) for access to collections under their care. The Willi
868
Hennig Society sponsors the use of the TNT cladistics software. Research work of XPS was
869
supported by the Ministerio de Economía y Competitividad of Spain (MINECO, project
870
CGL2017-85038-P), the European Regional Development Fund, the Gobierno Vasco/Eusko
871
Jaurlaritza (research group IT-1044-16) and the Universidad del País Vasco (UPV/EHU, research
872
group PPG17/05), and works of BJ by the FRIA grant. BJ-C thanks J. Laval for producing the thin
873
sections for histological purposes, V. Fischer for his useful critics on the long bone histology
874
part, and J. Jentgen for having helped a lot to produce the histological figures. We are greatly
875
indebted to P.M. Mannion (UCL, UK) and S.F. Poropat (Swinburne University of Technology,
876
Hawthorn, Australia), which provided useful comments that helped improving this work. This
877
work has been developed thanks to the collaboration between Palaios (research association in
878
which XV is the president), the University of Poitiers, the Velaux Municipality (J.-P. Maggi and
879
L. Melhi) with its heritage, culture and technical services (M. Calvier, and S. Chauvet), the
880
environment department from CD 13 (M. Bourrelly, T. Tortosa, G. Michel, N. Mouly, and S.
881
Amico), the ‘Service Départemental d’Incendie et de Secours’ (SDIS 13), and numerous
882
volunteers during the field campaigns in 2009 and 2012. This work was supported by the
883
Ministry of Education and Communication (research grant VR1013 to Palaios association), the
AC C
EP
TE D
M AN U
SC
RI PT
858
37
ACCEPTED MANUSCRIPT 884
Bouches du Rhône department CD 13 proposals MAPADGAC23112010-1 and
885
MAPADGAC16012014-1-AAPC).
886 REFERENCES
888
Adams, J., Organ, C.L. 2005. Histologic determination of ontogenetic patterns and processes in
889
hadrosaurian ossified tendons. Journal of Vertebrate Paleontology 25(3), 614-622.
RI PT
887
SC
890
Apesteguía, S. 2005. The evolution of the titanosaurian metacarpus. In: Tidwell, V., Carpenter,
892
K. (Eds.), Thunder-Lizards. The Sauropodomorph Dinosaurs. Indiana University Press,
893
Bloomington and Indianapolis pp. 321-345.
M AN U
891
894
Ascenzi, A., Bonucci, E. 1968. The compressive properties of single osteons. The Anatomical
896
Record: Advances in Integrative Anatomy and Evolutionary Biology 161(3), 377-391.
897
TE D
895
Bonaparte, J.F., Coria, R.A. 1993. Un nuevo y gigantesco saurópodo titanosaurio de la
899
Formación Río Limay (Albiano-Cenomanio) de la Provincia del Neuquén, Argentina.
900
Ameghiniana 30, 271-282.
AC C
901
EP
898
902
Bonaparte, J.F., González Riga, B.J., Apesteguía, S. 2006. Ligabuesaurus leanzai gen. and sp.
903
nov. (Dinosauria, Sauropoda), a new titanosaur from the Lohan Cura Formation (Aptian, Lower
904
Cretaceous) of Neuquén, Patagonia, Argentina. Cretaceous Research 27, 364–376.
905
38
ACCEPTED MANUSCRIPT
Borsuk-Białynicka, M. 1977. A new camarasaurid sauropod Opisthocoelicaudia skarzynskii gen.
907
n., sp. n. from the Upper Cretaceous of Mongolia. Palaeontologia Polonica 37, 5–64.
908
Calvo, J.O., Porfiri, J.D., González-Riga, B.J., Kellner, A.W.A. 2007. A new Cretaceous terrestrial
909
ecosystem from Gondwana with the description of a new sauropod dinosaur. Anais da
910
Academia Brasileira de Ciências 79(3), 529-541.
911
RI PT
906
Campione, N.E., Evans, D.C. 2012. A universal scaling relationship between body mass and
913
proximal limb bone dimensions in quadrupedal terrestrial tetrapods. BMC Biology 10(1), 60.
SC
912
M AN U
914
Carballido, J.L., Pol, D., Otero, A., Cerda, I.A., Salgado, L., Garrido, A.C., Ramezani, J., Cúneo,
916
N.R., Krause, J.M. 2017 A new giant titanosaur sheds light on body mass evolution among
917
sauropod dinosaurs. Proceedings of the Royal Society of London B 284, 20171219.
TE D
915
918
Carballido, J.L., Rauhut, O.W.M., Pol, D., Salgado, L. 2011. Osteology and phylogenetic
920
relationships of Tehuelchesaurus benitezii (Dinosauria, Sauropoda) from the Upper Jurassic of
921
Patagonia. Zoological Journal of the Linnean Society 163, 605-662. DOI: 10.1111/j.1096-
922
3642.2011.00723.x
AC C
923
EP
919
924
Cerda, I.A. 2009. Consideraciones sobre la histogénesis de las costillas cervicales en los
925
dinosaurios saurópodos. Ameghiniana 46, 193-198.
926
39
ACCEPTED MANUSCRIPT 927
Cerda, I.A., Casal, G.A., Martinez, R.D., Ibiricu, L.M. 2015 Histological evidence for a
928
supraspinous ligament in sauropod dinosaurs. Royal Society Open Science 2, 150369. DOI:
929
10.1098/rsos.150369
RI PT
930 931
Cerda, I.A., Salgado, L., Powell, J.E. 2012. Extreme postcranial pneumaticity in sauropod
932
dinosaurs from South America. Paläontologische Zeitschrift 86(4), 441-449.
SC
933
Cincotta, A., Yans, Y., Godefroit, P., Garcia, G., Dejax, J., Benammi, M., Amico, S., Valentin, X.
935
2015. Integrated paleoenvironmental reconstruction and taphonomy of a unique Upper
936
Cretaceous vertebrate–bearing locality (Velaux, southeastern France). PlosOne.
937
DOI:10.1371/journal.pone.0134231
938
M AN U
934
Company, J., Pereda Suberbiola, X., Ruiz-Omeñaca, J.I. 2009. Nuevos restos fósiles del
940
dinosaurio Lirainosaurus (Sauropoda, Titanosauria) en el Cretácico Superior (Campaniano-
941
Maastrichtiano) de la Península Ibérica. Ameghiniana 46(2), 391-405.
EP
942
TE D
939
Csiki, Z., Codrea, V., Jipa-Murzea, C., Godefroit, P. 2010. A partial titanosaur (Sauropoda,
944
Dinosauria) skeleton from the Maastrichtian of Nălaţ-Vad, Haţeg, Basin, Romania. Neues
945
Jahrbuch für Geologie und Paläontologie Abhandlungen 258(3), 297-324.
946
AC C
943
947
Csiki-Sava, Z., Buffetaut, E., Ösi, A., Pereda-Suberbiola, X., Brusatte, S.L. 2015. Island life in the
948
Cretaceous - faunal composition, biogeography, evolution, and extinction of land-living
949
vertebrates on the Late Cretaceous European archipelago. ZooKeys 469, 1-161. DOI:
950
10.3897/zookeys.469.8439
951
40
ACCEPTED MANUSCRIPT 952
Curry Rogers, K. 2005. Titanosauria. A phylogenetic overview. In: Curry Rogers, K., Wilson, J.A.
953
(Eds.), The Sauropods: Evolution and Paleobiology. University of California Press, Berkeley pp.
954
50-103.
955 Curry Rogers, K. 2009. The postcranial osteology of Rapetosaurus krausei (Sauropoda:
957
Titanosauria) from the Late Cretaceous of Madagascar. Journal of Vertebrate Paleontology
958
29(4), 1046-1086.
RI PT
956
SC
959
Curry Rogers, K.A., Forster, C. 2004. The skull of Rapetosaurus krausei (Sauropoda:
961
Titanosauria) from the Late Cretaceous of Madagascar. Journal of Vertebrate Paleontology 24,
962
121–144.
M AN U
960
963
D'Emic, M.D. 2012. The early evolution of titanosauriform sauropod dinosaurs. Zoological
965
Journal of the Linnean Society 166, 624-671. DOI: http://dx.doi.org/10.1111/j.1096-
966
3642.2012.00853.x
967
TE D
964
D’Emic, M.D., Wilson, J.A., Williamson, T.E. 2011. A sauropod dinosaur pes from the latest
969
Cretaceous of North America and the validity of Alamosaurus sanjuanensis (Sauropoda,
970
Titanosauria). Journal of Vertebrate Paleontology 31, 1072-1079.
AC C
971
EP
968
972
Depéret, C. 1899. Aperçu sur la géologie du Chaînon de Saint-Chinian. Bulletin de la
973
Société Géologique de France 3(27), 686-709.
974 975
Díez Díaz, V. 2013. Revisión del dinosaurio saurópodo Lirainosaurus astibiae
41
ACCEPTED MANUSCRIPT 976
(Titanosauria) del Cretácico Superior de la Península Ibérica. Comparación con otros
977
titanosaurios del suroeste de Europa. Hipótesis filogenética y paleobiogeográfica. Unpublished
978
Ph.D Thesis (306 pp). Universidad del País Vasco/EHU, Bilbao, Bilbao.
979 Díez Díaz, V., Pereda Suberbiola, X., Sanz, J.L. 2011. Braincase anatomy of the sauropod
981
dinosaur Lirainosaurus astibiae (Titanosauria) from the Late Cretaceous of the Iberian
982
Peninsula. Acta Paleontologica Polonica 56, 521-533.
SC
983
RI PT
980
Díez Díaz, V., Pereda Suberbiola, X., Sanz, J.L. 2012a. Juvenile and adult teeth of the
985
titanosaurian dinosaur Lirainosaurus (Sauropoda) from the Late Cretaceous of Iberia. Geobios
986
45, 265-274.
M AN U
984
987
Díez Díaz, V., Garcia, G., Knoll, F., Pereda Suberbiola, X., Valentin, X. 2012b. New cranial
989
remains of titanosaurian sauropod dinosaurs from the Late Cretaceous of Fox-Amphoux-
990
Métisson (Var, SE France). Proceedings of the Geologists' Association 123, 626-637.
TE D
988
991
Díez Díaz, V., Pereda Suberbiola, X., Sanz, J.L. 2013a. The axial skeleton of the titanosaur
993
Lirainosaurus astibiae (Dinosauria: Sauropoda) from the latest Cretaceous of Spain. Cretaceous
994
Research 43, 145-160.
AC C
995
EP
992
996
Díez Díaz, V., Pereda Suberbiola, X., Sanz, J.L. 2013b. Appendicular skeleton and dermal
997
armour of the Late Cretaceous titanosaur Lirainosaurus astibiae (Dinosauria: Sauropoda) from
998
Spain. Palaeontologia Electronica 16(2), 19A, 18p.
999 1000
Díez Díaz, V., Tortosa, T., Le Loeuff, J. 2013c. Sauropod diversity in the Latest Cretaceous of
1001
south-western Europe: The lessons of odontology. Annales de Paléontologie 99(2), 119-129.
42
ACCEPTED MANUSCRIPT 1002 Díez Díaz, V., Garcia, G., Pereda Suberbiola, X., Valentin, X., Sanz, J.L. 2013. Phylogenetic
1004
relationships of the titanosaurian dinosaurs from the Late Cretaceous of the Ibero-Armorican
1005
Island. In: Torcida Fernández-Baldor, F.; Huerta, P. (Eds.). Abstract book of the VI International
1006
Symposium about Dinosaurs Palaeontology and their Environment pp. 60-62.
1007
RI PT
1003
Díez Díaz, V., Ortega, F., Sanz, J.L. 2014. Titanosaurian teeth from the Late Cretaceous of “Lo
1009
Hueco” (Cuenca, Spain). Cretaceous Research 51, 285-291.
SC
1008
1010
Díez Díaz, V., Pereda Suberbiola, X., Company, J. 2015. Puesta al día de la diversidad de
1012
titanosaurios (Sauropoda) del Cretácico Superior de España. Spanish Journal of Palaeontology
1013
30(2), 293-306.
M AN U
1011
1014
Díez Díaz, V., Mocho, P., Páramo, A., Escaso, F., Marcos-Fernández, F., Sanz, J.L., Ortega, F.
1016
2016. A new titanosaur (Dinosauria, Sauropoda) from the Upper Cretaceous of Lo Hueco
1017
(Cuenca, Spain). Cretaceous Research 68, 49-60.
TE D
1015
EP
1018
Filippi, L.S., García, R.A., Garrido, A.C. 2011. A new titanosaur sauropod dinosaur from the
1020
Upper Cretaceous of North Patagonia, Argentina. Acta Palaeontologica Polonica 56(3), 505-
1021
520.
1022
AC C
1019
1023
Fondevilla, V. 2017. Registre geològic, paleoambients i susscesió dels darrers dinosaures del
1024
sud-oest europeu. Unpublished Ph.D. Thesis (338 pp). Universitat Autònoma de Barcelona.
1025 1026
Fondevilla, V., Vila, B., Oms, O., Galobart, À. 2016. Skin impressions of the last European
1027
dinosaurs. Geological Magazine 154(2), 393-398. DOI: 10.1017/S0016756816000868
43
ACCEPTED MANUSCRIPT 1028 1029
Gallina, P.A., Apesteguía, S. 2011. Cranial anatomy and phylogenetic position of the
1030
titanosaurian sauropod Bonitasaura salgadoi. Acta Palaeontologica Polonica 56(1), 45-60.
1031 Gallina, P.A., Apesteguía, S. 2015. Postcranial anatomy of Bonitasaura salgadoi (Sauropoda,
1033
Titanosauria) from the Late Cretaceous of Patagonia, Journal of Vertebrate Paleontology 35(3),
1034
e924957. DOI: 10.1080/02724634.2014.924957
SC
1035
RI PT
1032
Garcia, G., Vianey-Liaud, M. 2001. Dinosaur eggshells as new biochronological markers in Late
1037
Cretaceous continental deposits. Palaeogeography, Palaeoclimatology, Palaeoecology 169,
1038
153-164.
M AN U
1036
1039
Garcia, G., Amico, S., Fournier, F., Thouand, E., Valentin, X. 2010. A new titanosaur genus
1041
(Dinosauria, Sauropoda) from the Late Cretaceous of southern France and its
1042
paleobiogeographic implications. Bulletin de la Société Géologique de France
1043
181, 269-277.
EP
1044
TE D
1040
Gilmore, C.W. 1946. Reptilian fauna of the North Horn Formation of central Utah. United
1046
States Geological Survey Professional Paper 210C, 1-52.
1047
AC C
1045
1048
Godefroit, P., Garcia, G., Gomez, B., Stein, K., Cincotta, A., Lefevre, U., Valentin, X. 2017.
1049
Extreme tooth enlargement in a new Late Cretaceous rhabdodontid dinosaur from Southern
1050
France. Scientific reports 7, 13098. DOI:10.1038/s41598-017-13160-2
1051 1052
Goloboff, P., Farris, J., Nixon, K. 2008. TNT, a free program for phylogenetic analysis. Cladistics
1053
24, 774-786.
44
ACCEPTED MANUSCRIPT 1054 1055
Gomani, E.M. 2005. Sauropod dinosaurs from the Early Cretaceous of Malawi, Africa.
1056
Palaeontologia Electronica 8(1.27A), 1-37.
1057 González Riga, B.J. 2003. A new titanosaur (Dinosauria, Sauropoda) from the Upper
1059
Cretaceous of Mendoza Province, Argentina. Ameghiniana 40, 155-172.
RI PT
1058
1060
González Riga, B.J., Ortiz David, L. 2014. A new titanosaur (Dinosauria, Sauropoda) from the
1062
Upper Cretaceous (Cerro Lisandro Formation) of Mendoza Province, Argentina. Ameghiniana
1063
51(1), 3-25.
M AN U
SC
1061
1064
González Riga, B.J., Previtera, E., Pirrone, C.A. 2009. Malarguesaurus florenciae gen. et sp.
1066
nov., a new titanosauriform (Dinosauria, Sauropoda) from the Upper Cretaceous of Mendoza,
1067
Argentina. Cretaceous Research 30, 135-148. DOI: 10.1016/j.cretres.2008.06.006
1068
TE D
1065
González Riga, B.J., Lamanna, M.C., Ortiz David, L.D., Calvo, J.O., Coria, J.P. 2016. A gigantic
1070
new dinosaur from Argentina and the evolution of the sauropod hind foot. Scientific Reports 6,
1071
19165. DOI: 10.1038/srep19165.
AC C
1072
EP
1069
1073
González Riga, B.J., Mannion, P.D., Poropat, S.F., Ortiz David, L., Coria, J.P. 2018. Osteology of
1074
the Late Cretaceous Argentinean sauropod dinosaur Mendozasaurus neguyelap: implications
1075
for basal titanosaur relationships. Zoological Journal of the Linnean Society. DOI:
1076
10.1093/zoolinnean/zlx103
1077
45
ACCEPTED MANUSCRIPT 1078
Gorscak, E., O'Connor, P.M. 2016. Time-calibrated models support congruency between
1079
Cretaceous continental rifting and titanosaurian evolutionary history. Biology Letters 12,
1080
20151047. DOI: 10.1098/rsbl.2015.1047
1081 Gorscak, E., O'Connor, P.M. , Roberts, E.M., Stevens, N.J. 2017 The second titanosaurian
1083
(Dinosauria: Sauropoda) from the middle Cretaceous Galula Formation, southwestern
1084
Tanzania, with remarks on African titanosaurian diversity. Journal of Vertebrate Paleontology
1085
37, 4. DOI: 10.1080/02724634.2017.1343250
SC
RI PT
1082
1086
Gorscak, E., O’Connor, P.M., Stevens, N.J., Roberts, E M. 2014. The basal titanosaurian
1088
Rukwatitan bisepultus (Dinosauria, Sauropoda) from the middle Cretaceous Galula Formation,
1089
Rukwa Rift Basin, southwestern Tanzania. Journal of Vertebrate Paleontology 34, 1133–1154.
M AN U
1087
1090
Hocknull, S.A., White, M.A., Tischler, T.R., Cook, A.G., Calleja, N.D., Sloan, T., Elliott, D.A. 2009.
1092
New Mid-Cretaceous (Latest Albian) Dinosaurs from Winton, Queensland, Australia. PLoS ONE
1093
4(7), e6190. DOI: 10.1371/journal.pone.0006190
TE D
1091
EP
1094
Huene, F.v. 1929. Los Saurisquios y Ornithisquios del Cretáceo Argentino. Anales del Museo La
1096
Plata 2, 1- 196.
1097
AC C
1095
1098
Huene, F.v. 1932. Die fossil Reptil-Ordnung Saurischia, ihre Entwicklung und Geschichte.
1099
Monographien zur Geologie und Palaeontologie 4, 1-361.
1100 1101
Kellner, A.W.A., Campos, D. de A., Trotta, M.N.F. 2005. Description of a titanosaurid caudal
1102
series from the Bauru group, Late Cretaceous of Brazil. Arquivos do Museu Nacional, Rio de
1103
Janeiro 63(3), 529-564.
46
ACCEPTED MANUSCRIPT 1104 1105
Klein, N., Sander, M. 2008. Ontogenetic stages in the long bone histology of sauropod
1106
dinosaurs. Paleobiology 34, 247-263. DOI: 10.1666/0094-8373(2008)034[0247:OSITLB]2.0.CO;2
1107 Klein, N., Sander, M., Suteethorn, V. 2009. Bone histology and its implications for the life
1109
history and growth of the Early Cretaceous Phuwiangosaurus sirindhornae. Special Publications
1110
of the Geological Society of London 315, 217-228. DOI: 10.1144/SP315.15
RI PT
1108
SC
1111
Klein, N., Sander, P. M., Stein, K., Le Loeuff, J., Carballido J.L. , Buffetaut E. 2012a. Modified
1113
laminar bone in Ampelosaurus atacis and other titanosaurs (Sauropoda): implications for life
1114
history and physiology. PLoS ONE 7, e36907. DOI: 10.1371/journal.pone.0036907
M AN U
1112
1115
Klein, N., Christian, A., Sander, P.M. 2012b. Histology shows that elongated neck ribs in
1117
sauropod dinosaurs are ossified tendons. Biology Letters. DOI: 10.1098/rsbl.2012.0778
1118
TE D
1116
Kurzanov, S.M., Bannikov, A.F. 1983. A new sauropod from the Upper Cretaceous of Mongolia.
1120
Palaeontological Journal 2, 91–97.
1121
EP
1119
Lamanna, M.C., Gorscak, E., Díez Díaz, V., Schwarz, D., El-Dawoudi, I. 2017. Reassessment Of A
1123
Partial Titanosaurian Sauropod Dinosaur Skeleton From The Upper Cretaceous (Campanian)
1124
Quseir Formation Of The Kharga Oasis, Egypt. XV Annual Meeting of the European Association
1125
of Vertebrate Palaeontologists. Zitteliana p. 50.
AC C
1122
1126 1127
Lapparent, A.F.de, Aguirre, E. 1956. Algunos yacimientos de Dinosaurios en el Cretácico
1128
Superior de la Cuenca de Tremp. Estudios geológicos 31-32, 377-382.
1129
47
ACCEPTED MANUSCRIPT 1130
Lapparent, A.F.de, Aguirre, E. 1957. Presencia de dinosaurios en el Cretáceo superior de la
1131
Cuenca de Tremp (prov. de Lérida, España). Notas y Comunicaciones del Instituto Geológico y
1132
Minero de España 47, 1-6.
1133 Le Loeuff, J. 1993. European titanosaurids. Revue de Paleobiologie 7, 105–117.
RI PT
1134 1135
Le Loeuff, J. 1995. Ampelosaurus atacis (nov. gen., nov. sp.) un nouveau Titanosauridae
1137
(Dinosauria, Sauropoda) du Crétacé supérieur de la Haute Vallée de l'Aude (France). Comptes
1138
Rendus de l'Académie des Sciences Paris 321(IIa), 693-699.
M AN U
1139
SC
1136
1140
Le Loeuff, J. 2005. Osteology of Ampelosaurus atacis (Titanosauria) from Southern France. In:
1141
Tidwell, V., Carpenter, K. (Eds.), Thunder-Lizards. The Sauropodomorph Dinosaurs. Indiana
1142
University Press, Bloomington and Indianapolis pp. 115-137.
TE D
1143
Le Loeuff, J., Suteethorn, S., Buffetaut, E. 2013. A new sauropod dinosaur from the Albian of Le
1145
Havre (Normandy, France). Oryctos 10, 23-30.
1146
EP
1144
Mannion, P.D., Calvo, J.O. 2011. Anatomy of the basal titanosaur (Dinosauria, Sauropoda)
1148
Andesaurus delgadoi from the mid-Cretaceous (Albian-early Cenomanian) Río Limay
1149
Formation, Neuquén Province, Argentina: implications for titanosaur systematics. Zoological
1150
Journal of the Linnean Society 163(1), 155-181. DOI: 10.1111/j.1096-3642.2011.00699
1151
AC C
1147
1152
Mannion, P.D., Otero, A. 2012. A reappraisal of the Late Cretaceous Argentinean sauropod
1153
dinosaur Argyrosaurus superbus, with a description of a new titanosaur genus. Journal of
1154
Vertebrate Paleontology 32, 614-638. DOI: 10.1080/02724634.2012.660898
1155
48
ACCEPTED MANUSCRIPT 1156
Mannion, P.D., Upchurch, P. 2011. A re-evaluation of the ‘mid-Cretaceous sauropod hiatus’
1157
and the impact of uneven sampling of the fossil record on patterns of regional dinosaur
1158
extinction. Palaeogeography, Palaeoclimatology, Palaeoecology 299, 529–540.
1159 Mannion, P.D., Upchurch, P., Barnes, R.N., Mateus, O. 2013. Osteology of the Late Jurassic
1161
Portuguese sauropod dinosaur Lusotitan atalaiensis (Macronaria) and the evolutionary history
1162
of basal titanosauriforms. Zoological Journal of the Linnean Society 168, 98–206.
RI PT
1160
SC
1163
Marsh, O.C. 1878. Principal characters of American Jurassic dinosaurs. Part I. American Journal
1165
of Science 16, 411-416.
M AN U
1164
1166
Martin, J., Delfino, M., Garcia, G., Godefroit, P., Berton, S., Valentin, X. 2016. New specimens of
1168
Allodaposuchus precedens from France: intraspecific variability and the diversity of European
1169
Late Cretaceous eusuchians. Zoological Journal of the Linnean Society 176, 607–631.
1170
TE D
1167
Martínez, R.D., Giménez, O., Rodríguez, J., Luna, M., Lamanna, M.C. 2004. An articulated
1172
specimen of the basal titanosaurian (Dinosauria: Sauropoda) Epachthosaurus sciuttoi from the
1173
Early Late Cretaceous Bajo Barreal Formation of Chubut Province, Argentina. Journal of
1174
Vertebrate Paleontology 24(1), 107-120.
AC C
1175
EP
1171
1176
Martínez, R.D.F., Lamanna, M.C., Novas, F.E., Ridgely, R.C., Casal, G.A., Martínez, J.E., Vita, J.R.,
1177
Witmer, L.M. 2016. A Basal Lithostrotian Titanosaur (Dinosauria: Sauropoda) with a Complete
1178
Skull: Implications for the Evolution and Paleobiology of Titanosauria. PLoS ONE 11(4),
1179
e0151661. DOI: 10.1371/journal.pone.0151661.
1180
49
ACCEPTED MANUSCRIPT 1181
Masriera, A., Ullastre, J. 1988. Nuevos datos sobre las capas maestrichtienses con Septorella:
1182
su presencia al norte del Montsec (Pirineo catalán). Acta Geológica Hispánica 23, 1-77.
1183 Matheron, P. 1869. Note sur les reptiles fossiles des dépôts fluvio-lacustres crétacés du basin à
1185
lignite de Fuveau. Bulletin de la Societe Geologique de France 26, 781–795.
RI PT
1184
1186
Mitchell, J., Sander, P.M., Stein, K. 2017. Can secondary osteons be used as ontogenetic
1188
indicators in sauropods? Extending the histological ontogenetic stages into senescence.
1189
Paleobiology 43, 321-342. DOI: 10.1017/pab.2016.47
M AN U
1190
SC
1187
1191
Nopcsa, F. 1915. Die Dinosaurier der Siebenbürgischen Landsteile Ungarns. Mitteilungen aus
1192
dem Jahrbuche der Königlich Ungarischen Geologischen Reichsanstalt 23, 3-24.
1193
Nowinski, A. 1971. Nemegtosaurus mongoliensis n. gen. n. sp. (Sauropoda) from the
1195
uppermost Cretaceous of Mongolia. Palaeontologia Polonica 25, 57–81.
1196
TE D
1194
Organ, C.L., and Adams, J. 2005. The histology of ossified tendon in dinosaurs. Journal of
1198
Vertebrate Paleontology 25(3), 602-613.
AC C
1199
EP
1197
1200
Otero, A. 2010. The appendicular skeleton of Neuquensaurus, a Late Cretaceous saltasaurine
1201
sauropod from Patagonia, Argentina. Acta Palaeontologica Polonica 55(3), 399–426.
1202 1203
Otero, A., Gallina, P.A., Canale, J.I., Haluza, A., 2012. Sauropod haemal arches: morphotypes,
1204
new classification and phylogenetic aspects. Historical Biology: An International Journal of
1205
Paleobiology 24(3), 243e256. DOI: 10.1080/08912963.2011.618269
50
ACCEPTED MANUSCRIPT 1206 1207
Owen, R. 1842. Report on British fossil reptiles. Reports of the British Association for the
1208
Advancement of Science II, 60-204.
1209 Packard, G.C., Boardman, T.J., Birchard, G.F. 2009. Allometric equations for predicting body
1211
mass in dinosaurs. Journal of Zoology 279(1), 102-110.
SC
1212
RI PT
1210
Páramo, A., Ortega, F., Sanz, J.L. 2015a. Two types of appendicular bones of titanosaurs
1214
(Dinosauria, Sauropoda) from Lo Hueco (Fuentes, Cuenca). In: 63rd Symposium for Vertebrate
1215
Palaeontology and Comparative Anatomy 24th Symposium of Palaeontological Preparation
1216
and Conservation with the Geological Curators' Group (Abstract Book) p. 100.
M AN U
1213
1217
Páramo, A., Ortega, F., Sanz, J.L. 2015b. Preliminar assessment of the morphological variability
1219
of appendicular bones of titanosaurs (Dinosauria, Sauropoda) from Lo Hueco (Fuentes,
1220
Cuenca). In: Reolid, M. (Ed.), Libro de resúmenes de las XXXI Jornadas de Paleontología de la
1221
Sociedad Española de Paleontología pp. 225-226.
EP
1222
TE D
1218
Paulina Carabajal, A. 2012. Neuroanatomy of titanosaurid dinosaurs from the Upper
1224
Cretaceous of Patagonia, with comments on endocranial variability within Sauropoda. The
1225
Anatomical Record 295; 2141–2156.
1226
AC C
1223
1227
Pereda-Suberbiola, X. 2009. Biogeographical affinities of Late Cretaceous continental tetrapods
1228
of Europe: a review. Bulletin de la Société Géologique de France 180(1), 57-71.
1229
51
ACCEPTED MANUSCRIPT 1230
Poropat, S.F., Upchurch, P., Mannion, P.D., Hocknull, S.A., Kear, B.P., Sloan, T., Sinapius, G.H.K.,
1231
Elliott, D.A. 2015. Revision of the sauropod dinosaur Diamantinasaurus matildae Hocknull et
1232
al. 2009 from the middle Cretaceous of Australia: implications for Gondwanan titanosauriform
1233
dispersal. Gondwana Research 27, 995–1033.
RI PT
1234 Poropat, S.F., Mannion, P.D., Upchurch, P., Hocknull, S.A., Kear, B.P., Kundrát, M., Tischler, T.T.,
1236
Sloan, T., Sinapius, G.H.K., Elliott, J.A., Elliott, D.A. 2016. New Australian sauropods shed light
1237
on Cretaceous dinosaur palaeobiogeography. Scientific Reports 6; 34467.
SC
1235
1238
Powell, J.E. 2003. Revision of South American titanosaurid dinosaurs: palaeobiological,
1240
palaeobiogeographical and phylogenetic aspects. Records of the Queen Victoria Museum 111,
1241
1-173.
M AN U
1239
1242
Salgado, L., Coria, R.A., Calvo, J.O. 1997. Evolution of titanosaurid sauropods I: Phylogenetic
1244
analysis based on the postcranial evidence. Ameghiniana 34(1), 3-32.
1245
TE D
1243
Salgado, L., Apesteguía, S., Heredia, S.E. 2005. A new specimen of Neuquensaurus australis, a
1247
Late Cretaceous saltasaurine titanosaur from North Patagonia. Journal of Vertebrate
1248
Paleontology 25(3), 623-634.
AC C
1249
EP
1246
1250
Salgado, L., Gallina, P.A., Paulina Carabajal, A. 2015. Redescription of Bonatitan reigi
1251
(Sauropoda: Titanosauria), from the Campanian–Maastrichtian of the Río Negro Province
1252
(Argentina), Historical Biology: An International Journal of Paleobiology. DOI:
1253
10.1080/08912963.2014.894038
1254
52
ACCEPTED MANUSCRIPT 1255
Sallam, H.M., Gorscak, E., O’Connor, P.M., El-Dawoudi, I.A., El-Sayed, S., Saber, S., Kora, M.A.,
1256
Sertich, J.J.W., Seiffert, E.R., Lamanna, M.C. 2018. New Egyptian sauropod reveals Late
1257
Cretaceous dinosaur dispersal between Europe and Africa. Nature Ecology & Evolution.
1258
DOI: 10.1038/s41559-017-0455-5
RI PT
1259 Sander P.M., Klein N., Stein K., Wings O. 2011. Sauropod bone histology and its implications for
1261
sauropod biology. In: Klein N., Remes K., Gee C. T. & Sander P. M. (Eds). Biology of the
1262
sauropod dinosaurs: understanding the life of giants. Bloomington, Indiana University Press pp.
1263
276-302.
SC
1260
M AN U
1264
Sanz, J.L., Powell, J.E., Le Loeuff, J., Martínez, R., Pereda-Suberbiola, X. 1999. Sauropod remains
1266
from the Upper Cretaceous of Laño (Northecentral Spain). Titanosaur phylogenetic
1267
relationships. Estudios del Museo de Ciencias Naturales de Álava 14(Número Especial 1), 235-
1268
255.
1269
TE D
1265
Seebacher, F. 2001. A New Method to Calculate Allometric Length-Mass Relationships of
1271
Dinosaurs. Journal of Vertebrate Paleontology 21(1), 51-60.
1272
EP
1270
Seeley, H.G. 1887. On the classification of the fossil animals commonly called Dinosauria.
1274
Proceedings of the Royal Society London 43(printed 1888), 165-171.
1275
AC C
1273
1276
Stein K., Csiki Z., Rogers K.C., Weishampel D. B., Redelstorff R., Carballido J. L., Sander P.M.
1277
2010. Small body size and extreme cortical bone remodelling indicate phyletic dwarfism in
1278
Magyarosaurus dacus (Sauropoda: Titanosauria), PNAS 107, 9258-9263. DOI:
1279
10.1073/pnas.1000781107
1280
53
ACCEPTED MANUSCRIPT 1281
Upchurch, P. 1998. The phylogenetic relationships of sauropod dinosaurs. Zoological Journal of
1282
the Linnean Society 124, 43-103.
1283 Upchurch, P., Barrett, P., Dodson, P. 2004. Sauropoda. In: Weishampel, D.B., Dodson, P.,
1285
Osmólska, H. (Eds.), The Dinosauria, second ed. University of California Press, Berkeley pp. 259-
1286
324.
RI PT
1284
1287
Valentin, X., Godefroit, P., Tabuce, R., Vianey-Liaud, M., Wu, W., Garcia, G. 2012. First
1289
Maastrichtian vertebrate assemblage from Provence (Vitrolles La Plaine, France). In: Godefroit,
1290
P. (Ed.), Bernissart Dinosaurs and Early Cretaceous Terrestrial Ecosystems. Indiana University
1291
Press pp. 583-597.
M AN U
SC
1288
1292
Vila, B., Galobart, À., Canudo, J.I., Le Loeuff, J., Dinarés-Turell, J., Riera, V., Oms, O.,
1294
Tortosa, T., Gaete, R. 2012. The diversity of sauropod dinosaurs and their first taxonomic
1295
succession from the latest Cretaceous of southwestern Europe: clues to demise and extinction.
1296
Palaeogeography, Palaeoclimatology, Palaeoecology 350-352, 19-38. DOI:
1297
10.1016/j.palaeo.2012.06.008
EP
1298
TE D
1293
Vila, B., Sellés, A.G., Brusatte, S.L. 2016. Diversity and faunal changes in the latest Cretaceous
1300
dinosaur communities of south-western Europe. Cretaceous Research 57, 552–64.
1301
AC C
1299
1302
Vullo, R., Garcia, G., Godefroit, P., Cincotta, A., Valentin, X. In press. Mistralazhdarcho maggii
1303
gen. et sp. nov., a new azhdarchid pterosaur from the Upper Cretaceous of southeastern
1304
France. Journal of Vertebrate Paleontology.
1305
54
ACCEPTED MANUSCRIPT 1306
Wedel, M.J. 2003. The evolution of vertebral pneumaticity in sauropod dinosaurs. Journal of
1307
Vertebrate Paleontology 23(2), 344-357.
1308 Wedel, M.J., Taylor, M.P. 2013. Caudal Pneumaticity and Pneumatic Hiatuses in the Sauropod
1310
Dinosaurs Giraffatitan and Apatosaurus. PLoS ONE 8(10), e78213. DOI:
1311
10.1371/journal.pone.0078213
RI PT
1309
1312
Wilson, J.A. 1999. A nomenclature for vertebral laminae in sauropods and other saurischian
1314
dinosaurs. Journal of Vertebrate Paleontology 19, 639-653.
SC
1313
M AN U
1315 1316
Wilson, J.A. 2002. Sauropod dinosaur phylogeny: critique and cladistic analysis. Zoological
1317
Journal of the Linnean Society 136, 217-276.
1318
Wilson, J.A. 2006. Anatomical nomenclature of fossil vertebrates: standardized terms or lingua
1320
franca? Journal of Vertebrate Paleontology 26, 511-518.
TE D
1319
1321
Wilson, J.A. 2011. Anatomical terminology for the sacrum of sauropod dinosaurs. Contrib.
1323
Mus. Paleontol. Univ. Michigan 32, 59-69.
EP
1322
AC C
1324 1325
Wilson, J.A., Carrano, M.T. 1999. Titanosaurs and the origin of “wide-gauge” trackways: a
1326
biomechanical and systematic perspective on sauropod locomotion. Paleobiology 25, 252-267.
1327 1328
Wilson, J.A., Upchurch, P. 2003. A revision of Titanosaurus Lydekker (Dinosauria-Sauropoda),
1329
the first dinosaur genus with a “Gondwanan” distribution. Journal of Systematic Palaeontology
1330
1, 125-160.
1331
55
ACCEPTED MANUSCRIPT 1332
Wilson, J.A., Upchurch, P. 2009. Redescription and reassessment of the phylogenetic affinities
1333
of Euhelopus zdanskyi (Dinosauria: Sauropoda) from the Early Cretaceous of China. Journal of
1334
Systematic Palaeontology 7, 199–239.
1335 Wilson, J.A., D'Emic, M.D., Ikejiri, T., Moacdieh, E.M., Withlock, J.A. 2011. A nomenclature for
1337
vertebral fossae in sauropods and other saurischian dinosaurs. PLoS One 6(2), e17114. DOI:
1338
10.1371/journal.pone.0017114
RI PT
1336
SC
1339
Wilson, J.A., Pol, D., Carvalho, A.B., Zaher, H. 2016. The skull of the titanosaur Tapuiasaurus
1341
macedoi (Dinosauria: Sauropoda), a basal titanosaur from the Lower Cretaceous of Brazil.
1342
Zoological Journal of the Linnean Society 178(3), 611-662. DOI: 10.1111/zoj.12420.
M AN U
1340
1343
Zaher, H., Pol, D., Carvalho, A.B., Nascimento, P.M., Riccomini, C., Larson, P., Juárez-Valieri, R.,
1345
Pires-Domingues, R., da Silva Jr., de Almeida Campos, N.J.D. 2011. A complete skull of an early
1346
Cretaceous Sauropod and the evolution of advanced Titanosaurians. PLoS ONE 6(2), e16663.
TE D
1344
1347
1350
FIGURE LEGENDS
AC C
1349
EP
1348
1351
Figure 1. (A) Simplified geological map of the Aix-en-Provence Basin (Bouches-du-Rhône,
1352
France). Arrow indicates the location of the Velaux-La Bastide Neuve site. (B) Map indicating
1353
the repartition of vertebrate specimens collected since 1993 including some important
1354
titanosaurian bones (without the institutional abbreviations) and the concentration of bones
1355
collected in 2009 (a) and 22012 (b).
1356
56
ACCEPTED MANUSCRIPT Figure 2. Cranial remains of the titanosaur Atsinganosaurus velauciensis. Right fragment of a
1358
braincase (MMS/VBN.09.167) in (A) lateral and (B) medial views. Left pterygoid
1359
(MMS/VBN.09.158a) in (C) medial and (D) lateral views. Occipital condyle (MMS/VBN.09.41 ) in
1360
(E) right lateral view. Tooth (MMS/VBN.12.A.006) in (F) labial view. Abbreviations as in the
1361
text.
RI PT
1357
1362
Figure 3. Cervical vertebrae of the titanosaur Atsinganosaurus velauciensis. Posterior cervical
1364
vertebrae, previously described by Garcia et al. (2010), in left lateral view: (A) UP/VBN.93.12a
1365
(B), UP/VBN.93.12b, and (C) UP/VBN.93.12c. (D) Anterior cervical vertebra
1366
(MMS/VBN.12.B.015), with parts of the subsequent centrum ventrally associated to it in left
1367
lateral view. Posterior view of (E) UP/VBN.93.12a and (F) MMS/VBN.12.B.015. (G) Anterior
1368
cervical vertebra (MMS/VBN.12.A.004), with a fragment of the cervical rib, in right lateral view.
1369
Abbreviations as in the text.
M AN U
TE D
1370
SC
1363
Figure 4. Posterior cervical vertebra (MMS/VBN.12.B.010), and interpretative drawings, of the
1372
titanosaur Atsinganosaurus velauciensis in (A, A’) left lateral, (B, B’) anterior, (C, C’) right
1373
lateral, and (D, D’) posterior views. Abbreviations as in the text.
AC C
1374
EP
1371
1375
Figure 5. Fragmentary dorsal vertebrae and ribs of the titanosaur Atsinganosaurus
1376
velauciensis. (A) fragment of an anterior dorsal neural arch (MMS/VBN.93.32) in anterior view,
1377
(B) fragmentary dorsal vertebra (UP/VBN.09.157) in right lateral view, and (C) fragmentary
1378
middle to posterior dorsal vertebra (MMS/VB.93.02) in posterolateral view. Dorsal ribs
1379
MMS/VBN.07.D.07b in (D) lateral and (E) medial views, and MMS/VBN.07.D.07a in in (F) lateral
1380
and (G) medial views. Abbreviations as in the text.
57
ACCEPTED MANUSCRIPT 1381
Figure 6. Sacrum (MMS/VBN.02.82) of the titanosaur Atsinganosaurus velauciensis, previously
1383
described by Garcia et al. (2010), in (A) right lateral, (B) anterior, (C) slightly ventrolateral, and
1384
(D) posterior views.
RI PT
1382
1385
Figure 7. Caudal vertebrae and haemal arches of the titanosaur Atsinganosaurus velauciensis.
1387
Anterior caudal vertebra (MMS/VBN. 00.14) in (A) left lateral, (B) anterior, (C) posterior, (D)
1388
ventral, and (E) dorsal views. Anterior caudal vertebra (MMS/VBN. 00.15) in (F) left lateral, (G)
1389
anterior, (H) ventral, and (I) dorsal views. Anterior caudal vertebra (MMS/VBN.93.31a) in (J)
1390
left lateral and (K) anterior views. Haemal arch (MMS/VBN. 93.31b) in (L) anterior and (M)
1391
posterior views. Anterior caudal vertebra (MMS/VBN. 02.110) in (N) left lateral, (O) anterior,
1392
(P) posterior, and (Q) ventral views. Middle to posterior caudal vertebra (MMS/VBN.09.D.003)
1393
in (R) left lateral, (S) anterior, (T) posterior, and (U) ventral views. Posterior (distal) caudal
1394
vertebra (MMS/VBN.93.32a) in (V) right lateral, (W) anterior, and (X) posterior views. Haemal
1395
arch (MMS/VBN.93.32b) in (Y) anterior and (Z) posterior views.
M AN U
TE D
EP
1396
SC
1386
Figure 8. Caudal vertebrae of the titanosaur Atsinganosaurus velauciensis. (A) anterior caudal
1398
vertebra (MMS/VBN.12.C.004) in left lateral view, (B) fragmentary anterior caudal vertebra
1399
(MMS/VBN.09.54) in left lateral view, (C) posterior caudal vertebra (MMS/VBN.12.C.003) in
1400
right lateral view, (D) fragmentary posterior caudal vertebra (MMS/VBN.09.D.010) in left
1401
lateral view, (E) posterior caudal vertebra (MMS/VBN.09.159.b) in right lateral view, (F)
1402
posterior caudal vertebra (UP/VBN.93.03), in left lateral view, (G) posterior caudal vertebra
1403
(UP/VBN.93.04), in right lateral view, (H) posterior caudal vertebra (UP/VBN.93.05), in right
1404
lateral view, (I) fragmentary posterior caudal vertebra (UP/VBN.93.06), in right lateral view (J)
AC C
1397
58
ACCEPTED MANUSCRIPT 1405
posterior caudal vertebra UP/VBN.93.07), in right lateral view, and (K) posterior caudal
1406
vertebra (UP/VBN.93.08), in right lateral view. F-K were previously described by Garcia et al.
1407
(2010).
RI PT
1408 Figure 9. Scapular girdle remains of the titanosaur Atsinganosaurus velauciensis. Fragmentary
1410
left scapulocoracoid (MMS/VBN.02.78a–b) in (A) lateral and (B) medial views. (C) Left scapula
1411
(MMS/VBN.93.11) in medial view. (D) Right juvenile scapula (MMS/VBN.09.124D) in lateral
1412
view.
SC
1409
M AN U
1413
Figure 10. Forelimb remains of the titanosaur Atsinganosaurus velauciensis. Right humerus
1415
(MMS/VBN.00.12), previously described by Garcia et al. (2010), in (A) anterior, (B) medial, (C)
1416
posterior, and (D) lateral views. Left humerus (MMS/VBN.09.A.018) in (E) anterior, (F) medial,
1417
(G) posterior, and (H) lateral views. Right humerus (VBN.93.MHNA.99.52) in (I) anterior and (J)
1418
posterior views. Right ulna (MMS.VBN.12.P.06a) in (K) proximal (medial towards top), (L)
1419
medial, (M) posterior, (N) lateral, (O) distal (lateral towards top), and (P) anterior views.
1420
Fragmentary radius (MMS/VBN.09.D.001) in (Q) anterior/posterior? and (R)
1421
posterior/anterior? views.
EP
AC C
1422
TE D
1414
1423
Figure 11. Metacarpal remains of the titanosaur Atsinganosaurus velauciensis. Left metacarpal
1424
I (MMS/VBN.09.113) in (A) dorsal, (B) posterior, (C) medial, and (D) lateral views. Left
1425
metacarpal I (UP/VBN.93.09) in (E) dorsal, (F) posterior, (G) medial, and (H) lateral views.
1426
59
ACCEPTED MANUSCRIPT 1427
Figure 12. Pelvic girdle of the titanosaur Atsinganosaurus velauciensis. Fragment of a right
1428
ilium (MMS/VBN.12.32) in (A) lateral and (B) ventromedial views. Right ischium
1429
(MMS/VBN.09.51c) in (C) lateral,(D), posterior, and (E) medial views. Abbreviations as in the
1430
text.
RI PT
1431
Figure 13. Hind limb remains of the titanosaur Atsinganosaurus velauciensis. Diaphysis of a
1433
right femur (MMS/VBN.09.126) in (A) anterior and (B) posterior views. Left tibia
1434
(MMS/VBN.02.90) in (C) proximal (lateral towards bottom), (D) lateral, (E) anterior, (F) medial,
1435
(G) distal (medial towards top), and (H) posterior views. Proximal third of a fibula
1436
(MMS/VBN.09.132) in (I) lateral and (J) medial views. Left tibia (MMS/VBN.02.109) in (K)
1437
proximal (lateral towards bottom), (L) lateral, (M) anterior, (N) medial, (O) distal (medial
1438
towards top), and (P) posterior views.
TE D
1439
M AN U
SC
1432
Figure 14. Left metatarsal I (MMS/VBN.93.10), previously described by Garcia et al. (2010), of
1441
the titanosaur Atsinganosaurus velauciensis in (A) dorsal, (B) distal, (C) medial, (D) proximal, (E)
1442
ventral (dorsal toward bottom), and (F) lateral (dorsal towards top) views.
AC C
1443
EP
1440
1444
Figure 15. Micro- and macrohistology of the titanosaur Atsinganosaurus velauciensis. A-C and
1445
E: transverse sections. D and F: longitudinal sections. (A) heavy remodelling of the cortex
1446
(MMS/VBN.09.A.018). (B) zoom with multiple secondary osteon generations indicated by
1447
numbers (MMS/VBN.09.A.018). (C) broken trabeculae trapped in sediments at the base of the
1448
core (MMS/VBN.09.A.018). (D) longitudinal section of MMS/VBN.09.126. (E-F) macrohistology
1449
of MMS/VBN.09.126 in radial and longitudinal section respectively. Scale bars: A-B = 0.5 mm,
1450
C-D = 1 mm, E-F = 1 cm.
60
ACCEPTED MANUSCRIPT 1451 Figure 16. Neck rib histology of the titanosaur Atsinganosaurus velauciensis. (A) overview of
1453
the two ribs in their storage unit, with inset illustrating the sectioning planes. The arrow in A,
1454
D, and E indicates the longitudinal axis. (B) composite image (plane polarized light and cross
1455
polars) with an overview of the histology of the sauropod cervical ribs in cross section. Note
1456
the patches of longitudinally running collagen fibre bundles. (C) composite image (in plane
1457
polarized light and cross polars) of the secondary osteons and fibre bundles in cross section at
1458
high magnification. Note the cross cutting relationships of some of the secondary osteons. (D)
1459
overview (plane polarized light) of the histology of the cervical ribs in longitudinal section. (E)
1460
detail of D. Note the strong longitudinal orientation of the osteons and osteocyte lacunae, as
1461
well as the fibre bundles with fibrocytes. Abbreviations: cl, cementing line; fb, fibre bundles;
1462
so, secondary osteon.
M AN U
SC
RI PT
1452
TE D
1463
Figure 17. Phylogenetic hypothesis. Only one MPT of 166 steps was obtained from the Salgado
1465
et al. (2015) data matrix, with a consistency index (CI) of 0.572 and a retention index (RI) of
1466
0.665. The European taxa are highlighted in the cladogram. The obtained nodes are (1)
1467
Titanosauriformes, (2) Titanosauria, (3) Lithostrotia, (4) Opisthocoelicaudiinae, (5)
1468
Saltasaurinae, (6) Aeolosaurinae, (7) Rinconsauria, (8) Lognkosauria, and (9) Lirainosaurinae.
AC C
1469
EP
1464
1470
TABLE LEGENDS
1471
Table 1. Measurements (in mm) of the teeth of the titanosaur Atsinganosaurus velauciensis.
1472
Abbreviations: Ø m-d: maximum mesiodistal width; Ø lb-ln: maximum labiolingual width; SI:
1473
slenderness index (Upchurch, 1998): length of the tooth crown divided by its maximum
61
ACCEPTED MANUSCRIPT 1474
mesiodistal width; CI: compression index (Díez Díaz et al., 2013c): maximum labiolingual width
1475
divided by the maximum mesiodistal width of the crown.
1476 Table 2. Measurements (in mm) of the vertebrae of the titanosaur Atsinganosaurus
1478
velauciensis. Abbreviations: A, anterior; M, middle; P, posterior; D, distal; EI (Elongation index)
1479
(Upchurch, 1998): anteroposterior length of the centrum (without the condyle) divided by the
1480
midline width of the cotyle.
RI PT
1477
SC
1481
Table 3. Measurements (in mm) of the fore and hindlimb remains of the titanosaur
1483
Atsinganosaurus velauciensis. Abbreviations: Max. width Prox. end: maximum width of the
1484
proximal end; Max. width distal end: maximum width of the distal end; Min. AP Width:
1485
minimum anteroposterior width; Min. Cir. Diaph.: minimum circumference of the diaphysis;
1486
Min. Transv. Width: minimum transversal width; ECC (eccentricity index) (Wilson and Carrano,
1487
1999): mid-shaft mediolateral width divided by the anteroposterior width.
TE D
1488
M AN U
1482
Table 4. Measurements (in mm) of the metacarpal and metatarsal remains of the titanosaur
1490
Atsinganosaurus velauciensis. Abbreviations: AP, anteroposterior; ML, mediolateral.
1491
EP
1489
Table 5. Measurements (in mm) of the ischium of the titanosaur Atsinganosaurus velauciensis.
1493
Abbreviations: PP, pubic peduncle.
1494 1495
AC C
1492
Table 6. Histological data summary of Atsinganosaurus velauciensis.
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
MMS/VBN.12.A.006 MMS/VBN.12.B.14 MMS/VBN.12.A.07 MMS/VBN.93.33
Crown length Ø m-d Ø lb-ln SI CI 190 33 23 5.76 0.69 180 45 4 160 37 33 4.32 0.89 150 39 3.85 -
ACCEPTED MANUSCRIPT
Centrum length Centrum length Vertebral Centrum height Centrum width Neural arch Neural spine (w/condyle) (wo/condyle) Heigth (posterior) (posterior) heigth heigth 352.5 330 195 220 230 185 255 280 -
333.5 270 175 195 200 155 235 252 220
240 300 310 220 260 185 192
74 51 85 90 60 82 63 50
69 44 85 90 50 72 61 34
1270.7 -
1017.1 -
-
130
75
86 91 83 85 102 90 94 121 123 97 97 125 113 90 99 76 75 71
60 77 67 74 70 74 103 84 98 102 83 86 109 92 77 74 86 68 70 59
107 143 104 133 85 74 66 71 54 64 54 60 44
62 39 35 65 53 56 48 47 45 29 59 31 38 40 34 24
28 90 95 36 51 58 62 50 46 54 48 61 45 26 30 21
AC C
EP
M AN U
CAUDALS MMS/VBN.93.31a (A) MMS/VBN.00.14 (A) MMS/VBN.00.15 (A) MMS/VBN.09.46 (A) MMS/VBN.09.54 (A) MMS/VBN.12.C.004 (A) MMS/VBN.09.D.011 (A-M?) MMS/VBN.12.B.018 (A-M?) MMS/VBN.09.D.009 (M?) MMS/VBN.12.B.013a (P) MMS/VBN.12.B.013b (P) MMS/VBN.09.D.03 (P) MMS/VBN.09.D.010 (P) MMS/VBN.09.159.b (P) MMS/VBN.12.C.003 (P) MMS/VBN.12.33 (P) UP/VBN.93.3 (P-D) UP/VBN.93.4 (P-D) UP/VBN.93.5 (P-D) UP/VBN.93.6 (D) UP/VBN.93.7 (D) UP/VBN.93.8 (D)
TE D
MMS/VBN.02.99 UP/VBN.09.157
120 200 210 118 100 78 90
3.91 3.98 2.29 2.22 3.10 3.26 4.13 6.47
-
275.7 -
-
57 70 40 68 41 36 48 23 25 35 33 30 19 24 16
51 32 22 50 17 14 21 7 21 14 9 0 7 3
2.14 0.86 0.71 2.06 1.37 1.28 1.65 1.66 1.87 2.02 1.92 1.26 1.64 2.62 2.33 2.81
SC
DORSALS
171 25 2050 147 185 102 126
RI PT
CERVICALS MMS/VBN.12.A.004 (A) MMS/VBN.12.B.015 (A) MMS/VBN.09.D.007a (A) UP/VBN.93.13a (M) UP/VBN.93.13b (M) MMS/VBN.12.B.10 (P) UP/VBN.93.12a (P) UP/VBN.93.12b (P) UP/VBN.93.12c (P)
EI
ACCEPTED MANUSCRIPT
Min. Cir. Diaph.
Max. width Prox.end
Max. width distal end
21 17
3.14 3.76
23.31 16.94
-
-
57.96
30.22
1.92
22.58
272
57
29
1.97
-
709
90.42
57.95
562
112
43
TIBIAE MMS/VBN.02.90 MMS/VBN.02.109
322 530
50.14 81.85
21.2 38.66
FIBULA MMS/VBN.09.132
221
47
390
RADIUS MMS/VBN.09.D.01
29
AC C
FEMORA MMS/VBN.00.12 MMS/VBN.09.126
SC
ULNA MMS/VBN.12.P.06a
M AN U
66 64
EP
555 480
RI PT
ECC
55.16
43.75
-
-
1.56 2.60
45.67 40.67
-
-
2.37 2.12
37.3 63.22
106.61 64.23
72 38.7
-
-
-
TE D
Preserved length Min. Transv. Width Min. AP Width HUMERI MMS/VBN.00.12 MMS/VBN.09.A.018
1.62
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
Length AP width diaphisis LM width diaphisis AP width Prox. Art. LM width Prox. Art. AP width Dist. Art. LM width Dist. Art. MMS/VBN.93.09 87 13 17 22 32 MMS/VBN.09.113 180 14 27 23 60 27 43 UP/VBN.93.10 120 46 27 71 31 60 60
AC C
EP
TE D
M AN U
SC
RI PT
MANUSCRIPT Preserved length ACCEPTED PP articular surface Distal edge width MMS/VBN.09.51c 345 105
Preserved lentgh (mm) ±570 470 555
ACCEPTED MANUSCRIPT Bone tissue type 2ry osteon generations in the inner,mid,outer cortex respectively
Core location Posterior side, above the mid-shaft Posterior side, in the mid-shaft Anterior side, in the mid-shaft
H H H
5,6,4 5,5,6 4,5,4
AC C
EP
TE D
M AN U
SC
RI PT
A. velauciensis sample Bone MMS/VBN.09.126 Right femur MMS/VBN.09.A.018 Left humerus MMS/VBN.00.12 Right humerus
HOS,RS 14,13+ 14.14 14.13
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT