Accepted Manuscript

Taphonomy and palaeohistology of ornithischian dinosaur remains from the Lower

Cretaceous bonebed of La Cantalera (Teruel, Spain)

Leire Perales-Gogenola, Javier Elorza, José Ignacio Canudo, Xabier Pereda-

Suberbiola

PII: S0195-6671(18)30380-X
DOI: https://doi.org/10.1016/j.cretres.2019.01.024
Reference: YCRES 4072

To appear in: Cretaceous Research

Received Date: 19 September 2018

Revised Date: 20 December 2018
Accepted Date: 30 January 2019

Please cite this article as: Perales-Gogenola, L., Elorza, J., Canudo, J.I., Pereda-Suberbiola, X.,
Taphonomy and palaeohistology of ornithischian dinosaur remains from the Lower Cretaceous bonebed
of La Cantalera (Teruel, Spain), Cretaceous Research, https://doi.org/10.1016/j.cretres.2019.01.024.

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1 Taphonomy and palaeohistology of ornithischian dinosaur remains from the Lower

2 Cretaceous bonebed of La Cantalera (Teruel, Spain)

4 Leire Perales-Gogenola1*, Javier Elorza2, José Ignacio Canudo3,4, Xabier Pereda-Suberbiola1

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6 (1) Departamento de Estratigrafía y Paleontología, Facultad de Ciencia y Tecnología, Universidad del País

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7 Vasco/Euskal Herriko Unibertsitatea (UPV/EHU), Apartado de Correos 644, 48080 Bilbao, Spain. E-mail:

8 leire.perales@ehu.eus*, xabier.pereda@ehu.eus

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9 (2) Departamento de Mineralogía y Petrología, Facultad de Ciencia y Tecnología, Universidad del País

10 Vasco/Euskal Herriko Unibertsitatea (UPV/EHU), Apartado de correos 644, 48080 Bilbao, Spain. E-mail:

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11 josejavier.elorza@ehu.eus
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12 (3) Grupo Aragosaurus: Recursos geológicos y paleoambientes. IUCA, Paleontología, Facultad de Ciencias,

13 Universidad de Zaragoza. 50009 Zaragoza, Spain. E-mail: jicanudo@unizar.es

14 (4) Museo de Ciencias Naturales, Universidad de Zaragoza, 50009 Zaragoza, Spain.

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16 * Corresponding author
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17

18 ABSTRACT
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19 The fossiliferous site of La Cantalera-1 (Teruel, Spain) has to date provided remains of more

20 than 30 vertebrate taxa, including dinosaurs, crocodyliforms, pterosaurs, mammals, lizards,

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21 turtles, lissamphibians and teleosteans. Located in the lower part of the Blesa Formation
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22 (lower Barremian), it is one of the richest vertebrate-bearing deposits from the Lower

23 Cretaceous of the Iberian Peninsula. In this work, taphonomic and palaeohistological studies

24 are carried out on the basis of ornithischian (Ornithopoda and Ankylosauria) dinosaur samples

25 in order to assess the diagenetic processes, to characterize the histological microstructures

26 and, if possible, to make palaeobiological inferences about the state of maturation of the

27 individuals. A variety of techniques are used in the taphonomic study, including scanning
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28 electron microscopy (SEM), cathodoluminescence (CL), X-ray diffraction (XRD) and

29 ultraviolet fluorescence (UVF). The bone of the dinosaur samples has been converted into

30 francolite (fluorapatite carbonate); the trabecular cavities are filled with semi-spherical forms

31 of goethite and two different phases of calcite. In addition, the SEM and UVF techniques

suggest the activity of coccoid-form bacteria and filaments of bacterial origin (biofilms?) in

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33 the bones, which possibly favoured fossilization. The dinosaur remains were subjected to

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34 fossil-diagenetic processes in a phreatic environment after a rapid burial, without appreciable

35 seasonality effects. On the other hand, the palaeohistological study of both skeletal and

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36 dermal bones found in La Cantalera-1 shows a community of herbivorous dinosaurs

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37 composed mostly of immature ornithopods and at least one Polacanthus-like ankylosaur, as
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38 suggested by the organizational pattern of structural collagen fibres seen in some samples.

39 The palaeobiological inferences drawn from this study support previous interpretations of a
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40 relative abundance of immature ornithischians in La Cantalera-1.

41
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42 Keywords: fossil diagenesis; bone microstructure; Ornithopoda; Ankylosauria; Barremian;

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43 Iberian Peninsula.
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45 1. Introduction

46 Our knowledge of the terrestrial ecosystems and especially the continental vertebrate

47 faunas from the Early Cretaceous of Iberia has notably increased in recent years thanks to the

48 discovery and study of rich fossiliferous outcrops (Ortega et al., 2006; Pereda-Suberbiola et

al., 2012; Merino and Buscalioni, 2013). One of the most relevant localities of this age for its

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50 great biodiversity is the bonebed of La Cantalera-1, where more than thirty vertebrate taxa

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51 have been recognized up to now (Canudo et al., 2010). This site, located near the village of

52 Josa (Teruel), has yielded a diverse accumulation of macro and micro-vertebrate fossil

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53 remains of Barremian age, including teleosteans, lissamphibians, turtles, lizards,

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54 crocodylomorphs, dinosaurs, pterosaurs and multituberculate mammals (Badiola et al., 2008;
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55 Canudo et al., 2010; Aurell et al., 2018 and references therein). Microfossils such as

56 charophytes and ostracods are very abundant at La Cantalera-1; also frequent are plant
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57 fragments and continental gastropods.

58 Dinosaurs are a significant component of the vertebrate fauna from La Cantalera-1, since
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59 they represent more than half of the identified species (Canudo et al., 2010). The dinosaurs
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60 comprise ornithopods, ankylosaurs, sauropods and theropods, the latter being the most diverse

clade in the number of species (Alonso and Canudo, 2016). Ornithopods are the most
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62 abundant dinosaur remains within the fossil assemblage (Ruiz-Omeñaca et al., 1997; Canudo
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63 et al., 2010). Based on teeth and postcranial remains, three different taxa of iguanodontian
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64 ornithopods have been identified, one of them related to Delapparentia turolensis Ruiz-

65 Omeñaca, 2011 (Gasca et al., 2014). Moreover, a small basal ornithopod is also present. With

66 regard to the ankylosaurian material, which includes isolated teeth, vertebral remains and

67 osteoderms, this has been identified as belonging to a taxon close to the genus Polacanthus

68 (Canudo et al., 2004, 2010).

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69 This work is the first palaeohistological study of dinosaur fossil bones from La Cantalera-

70 1. Ornithischian (both ornithopod and ankylosaur) remains are studied in order to ascertain

71 the mineralogy and petrology of the samples as well as to reconstruct the taphonomic history

72 of the site, to characterize the histological structures of the different tissues of the dinosaur

bones, and thus to make palaeobiological inferences. A preliminary account of the

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74 palaeohistological features observed in the ornithischian dinosaur remains from La Cantalera-

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75 1 was recently published (Perales-Gogenola et al., 2018).

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77 2. Geological setting

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78 The vertebrate site of La Cantalera-1 (Teruel) is located in the Oliete sub-basin in the
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79 northwestern marginal areas of the Maestrazgo Basin (Iberian Range) (Fig. 1). The synrift

80 sedimentation and synsedimentary extensional tectonics of the Oliete sub-basin have been
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81 summarized by Aurell et al. (2018). As noted by these authors, the Blesa Formation includes

82 an up-to-150 m-thick siliciclastic-carbonate, continental-coastal succession that represents the

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83 onset of the Early Cretaceous synrift sedimentation in the Oliete sub-basin. The early
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84 Barremian age of this unit is well constrained by the occurrence of charophytes in some of the

palustrine–lacustrine deposit intervals, and in particular by the presence of the clavatoracean

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86 Atopochara trivolvis triquetra in the lower levels of the Blesa Formation (Canudo et al., 2010,
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87 2012; see Riveline et al., 1996). Two outcrops are known at La Cantalera-1 area: La
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88 Cantalera-1 includes a rich vertebrate accumulation consisting mainly of isolated teeth and

89 disarticulated postcranial remains; eggshell fragments are also abundant (Moreno-Azanza et

90 al., 2014). La Cantalera-2 is located about 500 m south from the classic site of La Cantalera-1

91 and is an outcrop laterally equivalent to it (Gasca et al., 2014).

92 In lithological terms, La Cantalera-1 comprises grey clays deposited in the lowest part of

93 the Lower Blesa Sequence. Greyish and ochrish to reddish marls and clays with local root
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94 traces and nodulization are dominant in the lower part of this sequence, and represent distal

95 alluvial to palustrine mudflat deposits with local sheet-flood and debris-flow deposits (Aurell

96 et al., 2018). The relatively high calcium carbonate content in these facies reflects the

97 composition of the drained area, which consists of Jurassic limestones and marls. Red

pisolithic clays are also found in the lowermost part of the Lower Blesa Sequence, indicating

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99 lateritic soils on a Jurassic substratum (Aurell et al., 2018).

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100 The taphonomic evidence suggests that the fossil association of La Cantalera-1 reflects a

101 significant part of the biodiversity of a freshwater lentic ecosystem (Canudo et al., 2010). The

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102 site has been interpreted as a concentration of small, multitaxic vertebrate remains dominated

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103 by elements that are less than 5 cm in maximum dimension, i.e. a vertebrate microfossil
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104 assemblage (in the sense of Eberth and Currie, 2005). The assemblage includes partially

105 articulated remains and disarticulated vertebrate debris. It was formed as an attritional deposit
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106 of bioclasts through progressive accumulation on a poorly drained floodplain (Canudo et al.,

107 2010). In this low-energy depositional setting, preservational patterns vary and the vertebrate
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108 assemblage includes both autochthonous and parautochthonous elements, consisting almost
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109 exclusively of terrestrial and amphibious taxa that lived near the deposit area. There is no

indication of significant transport, so the fossil assemblage can be regarded as a time-

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111 averaged sample of the source community (sensu Rogers and Brady, 2010), specifically the
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112 La Cantalera-1 wetland ecosystem (Moreno-Azanza et al., 2014). The site probably represents
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113 a marshy environment with periodic droughts, resulting in an intermittent body of water that

114 periodically dried up (Canudo et al., 2010). The rich biodiversity of La Cantalera-1 may be

115 due to the concentration of vertebrate remains into restricted flooded areas during dry seasons

116 (Aurell et al., 2004). Furthermore, this small lacustrine area has been regarded as a feeding

117 area for herbivorous dinosaurs (Ruiz-Omeñaca et al., 1997) and was presumably close to a
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118 nesting area, which could explain the abundance of small-sized individuals and the presence

119 of fossil eggshells (Moreno-Azanza et al., 2014).

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121 3. Material and methods

The material studied from the La Cantalera-1 site consists of twenty ornithischian fossils,

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123 including twelve fragmentary or incomplete bones (vertebrae, ribs, ossified tendons and two

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124 long bones) corresponding to Ornithopoda and eight dermal elements (including keeled

125 scutes, small spines and ossicles; see Blows, 2001 for terminology) belonging to

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126 Ankylosauria (Table 1). This studied material comes from the erosion of the fossiliferous

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127 level and lack sings of transport. This selection was made according to the available material
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128 from the La Cantalera-1 site and the search for different palaeohistological microstructures in

129 the different skeletal elements. The minimum number of individuals is unknown but we
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130 assume that all the individuals belonged to a single population. The material is housed in the

131 Museo de Ciencias Naturales of the Universidad de Zaragoza (MPZ) (Canudo, 2018).
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132 For the palaeohistological analysis, thin sections were obtained following the standard
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133 techniques for hard histological tissues described by Chinsamy and Raath (1992). The

thickness of the sections was individually selected according to the characteristics of each
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135 piece, obtaining a thickness range of 30–50 µm. The description of the bone microstructures
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136 was undertaken using an Olympus BX41 petrographic microscope coupled to an Olympus
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137 CAMEDIA-C7070 photographic camera at the University of Zaragoza. The typological

138 classification of Francillon-Vieillot et al. (1990) was followed. The images obtained were

139 edited using Adobe Illustrator CS6®.

140 A selection of eleven petrographic thin sections of ornithischian fossil bones from La

141 Cantalera-1 was prepared for standard transmitted light petrography and carbonate staining

142 with Alizarin Red S and potassium ferricyanide (following Dickson, 1965). Polished sections
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143 were used for cathodoluminescence (CL). A number of samples were selected and examined

144 under a scanning electron microscope (SEM), and also qualitatively determined (Al, Si, Fe, P,

145 K, Ca) by energy-dispersive spectrometry (EDX) using a Jeol JSM-T6400 at the Universidad

146 del País Vasco/Euskal Herriko Unibertsitatea (UPV/EHU). All CL work employed a

Technosyn cold-cathode luminescence system, Model 8200 Mk II, mounted on an Olympus

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148 triocular research microscope with a maximum magnification capability of 400x using

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149 universal stage objectives. Standard operating conditions included an accelerating potential of

150 12 kV and a 0.5–0.6 mA beam current with a focused beam diameter of approximately 5 mm.

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151 The study of the ultraviolet fluorescence (UVF) of the fossil bone and filling phases (goethite

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152 and two calcite types) was carried out using Nikon UN2 PSE100 fluorescence power supply
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153 equipment attached to a Nikon Eclipse LV 100Pol microscope and a super high pressure

154 mercury lamp power supply as the light source at the Instituto Geológico y Minero (IGME,
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155 Madrid). XRD analyses were performed with a Phillips PW1710 diffractometer using Cu Kα

156 radiation monochromated by graphite with generator conditions of 40 kV, 20 mA, with a step
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157 size of 0.02° (º2θ) and a time per step of 1 s.

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158
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159 4. Results

160
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161 4.1. Palaeohistology

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162 The palaeohistological features of the ornithopod and ankylosaurian bones are described

163 below separately (see Fig. 2-4).

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165 4.1.1. Ornithopoda

166 Some fragmentary vertebrae (MPZ 2018/494, MPZ 2018/500 and MPZ 2018/501) and a

167 neural arch (MPZ 2018/495) were studied. The vertebra thin sections show a great percentage
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168 of trabecular bone and a small portion of compact bone. The compact tissue is formed by a

169 lamellar matrix and is variable between the samples. Some of them show bone deposited by a

170 periosteum (MPZ 2018/501; Fig. 2A) or an external avascular layer (MPZ 2018/495; Fig.

171 2B). The vascularization ranges from a laminar orientation with abundant vascular channels

(MPZ 2018/494; Fig. 2C) to a poor vascularization (MPZ 2018/501; Fig. 2A). Primary

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173 osteons (MPZ 2018/494; Fig. 2C), secondary osteons (MPZ 2018/500, MPZ 2018/495; Fig.

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174 2B and D) and Haversian bone (MPZ 2018/501; Fig. 2A) are found in different samples. In

175 general, the samples do not show periosteal zonation – except in the above-mentioned sample

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176 (MPZ 2018/501; Fig. 2A) – or LAGs (lines of arrested growth).

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177 Sample MPZ 2018/501 presents bone that was deposited by a periosteum composed of
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178 lamellar matrix with little or no vascularization (Fig. 2A). The preserved compact bone shows

179 a great density of secondary osteons, superimposed upon one another, with longitudinal
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180 vascularization and Volkmann’s channels, a typical example of Haversian bone (Francillon-

181 Vieillot et al., 1990) in which the primary lamellar matrix is almost not visible. The neural
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182 arch fragment (MPZ 2018/495; Fig. 2B and D) is composed of a larger percentage of
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183 trabecular bone than of compact bone. The compact part is composed of secondary osteons of

variable size (Fig. 2B and D). There is an avascular layer without zonation or LAGs in the
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185 most external part of the compact bone (Fig. 2B).

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186 The three fragmentary dorsal ribs (MPZ 2018/493, MPZ 2018/497 and MPZ 2018/499)
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187 show trabecular bone and fibrolamellar bone matrix. Primary osteons (MPZ 2018/492),

188 secondary osteons (MPZ 2018/497) or both types (MPZ 2018/493) are observed in different

189 samples. One of them shows weak lamination in the external cortex of the compact bone

190 (MPZ 2018/493; Fig. 2E). This cortex is presented as an avascular layer with lacunae in a

191 lamellar matrix (Fig. 2E). Lamination is not present in the rest of the compact tissue. The

192 outer part of the inner compact bone shows scattered osteons with longitudinal vascularization
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193 and lamellar matrix. There are secondary osteons within trabeculae that extend through the

194 medullary cavity, also in a llamelar matrix (Fig. 2F). The rib MPZ 2018/499 (Fig. 2G-H) has

195 a 50-50 proportion of trabecular (Fig. 2H) and compact bone (Fig. 2G), without external

196 cortex. Within the compact tissue, two different types of structure can be observed in the

internal and external faces of the rib. Two different colorations are visible in the bone (Fig.

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198 2G). It is composed of longitudinal vascularization and of secondary osteons in a lamellar-

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199 fibrolamellar matrix. There are Volkmann’s channels that connect the osteons, which have

200 well-defined resorption lines. MPZ 2018/492 (Fig. 3A-B) is an ornithopod rib, in which both

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201 the compact and trabecular bone are well preserved. The compact bone is formed by a

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202 lamellar matrix with high vascularization of simple channels in a random organization and
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203 scarce primary osteons (Fig. 3A). The transition from compact to trabecular bone is abrupt,

204 from small vascular channels to large medullary cavities (Fig. 3B).
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205 Two appendicular bones were studied, including an ornithopod ulna fragment (MPZ

206 2018/496) and an iguanodontoid fibula (MPZ 2018/502; Fig. 3C-E). The ulna (MPZ
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207 2018/496) presents a higher proportion of trabecular tissue than of compact bone; no external
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208 cortex, zonation or LAGs are recorded. The compact bone, formed by a lamellar matrix, is

composed of secondary osteons of different sizes that are overlapping due to the great density
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209

210 of vascularization (similar to Fig. 3C-D). In some parts of the section, Volkmann’s channels
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211 are seen connecting the osteons. The fibula (MPZ 2018/502; Fig. 3C-E) presents azonal
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212 compact bone with longitudinal vascularization. The compact bone represents a thicker layer

213 than the trabecular tissue. It is composed almost entirely of secondary osteons with marked

214 resorption lines. There are also Volkmann channels connecting the osteons. This is a typical

215 example of Haversian bone.

216 The studied ossified tendons (MPZ 2018/491 and MPZ 2018/498; Fig. 3F) are also an

217 example of dense Haversian tissue (Organ and Adams, 2005), with longitudinal
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218 vascularization and secondary osteons of different sizes (Fig. 3F). The concentric envelopes

219 are formed by lamellar bone and the resorption lines are visible in the secondary osteons (Fig.

220 3F). The tissue presents the same structure in the entire tendon, but some parts of the section

221 show a slightly lower density of osteons.

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223 4.1.2. Ankylosauria

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224 The dermal ossicles (MPZ 2018/506, MPZ 2018/507 and MPZ 2018/508) are formed by

225 azonal primary lamellar bone with a great complexity of collagen structural fibres, which are

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226 parallel and perpendicular to the base of the ossicle, showing a more (MPZ 2018/508; Fig.

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227 4A-D) or less (MPZ 2018/506) complex organization. The most characteristic feature of MPZ
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228 2018/508 is the particular spatial organization of the collagen structural fibres; some are

229 parallel to the base, and others perpendicular to the parallel ones, producing a pattern of bands
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230 (Fig. 4A-D). The vascularization of this particular tissue is high, with imbricated primary

231 osteons in the collagen structural fibres. Some vascular channels open to the surface of the
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232 osteoderm, especially in the basal portion (Fig. 4E).

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233 The dermal scutes are composed of trabecular bone and compact lamellar bone with

collagen structural fibres. The proportion of trabecular to compact bone is variable among the
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235 different samples. A pattern of high spatial organization of the collagen fibres is observed
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236 (MPZ 2018/509, MPZ 2018/511). The presence of osteons is also variable. Some samples
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237 show scarce scattered osteons (MPZ 2018/509), whereas others present a great density of

238 primary and secondary osteons (MPZ 2018/505; Fig. 4E). The outer cortex of the compact

239 bone is an azonal lamellar matrix.

240 The small dermal spines studied here correspond to the distal end (MPZ 2018/503; Fig.

241 4G) and the basal part (MPZ 2018/504; Fig. 4H) of the spine. Some differences in the

242 microstructure of both samples are seen. There is a gradual transition in both samples from
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243 the compact bone cortex to the trabecular cavities. This transition is more abrupt in the basal

244 part (MPZ 2018/504) than at the distal end (MPZ 2018/503). The compact bone is composed

245 of primary lamellar-fibrolamellar bone with primary osteons, wide vascular channels and

246 collagen structural fibres. Inside the trabeculae of the trabecular bone, there are some

deformed primary osteons and collagen fibres. There is neither zonation nor external wall of

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248 the compact bone well-preserved in any of the samples.

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250 4.2. Taphonomy

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251 In thin sections, the compact bone tissue shows a slight pink staining that affects both the

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252 part constituted by the secondary osteons and the primary matrix when it is treated with an
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253 Alizarin Red S stain and observed with plane-polarized light (parallel Nicols). In the primary

254 matrix, osteocyte lacunae of greater dimensions and without apparent order persist in a high
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255 proportion, as opposed to the lacunae inside the secondary osteons, where they are smaller

256 and show a concentric distribution with the lamellae of the osteons. Small, irregular fractures
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257 bleach the area of influence of the main fracture of the mineralizing fluids coming from them,
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258 whereas the Haversian channels, as well as parts of the Volkmann channels and the osteocyte

lacunae, are completely filled by opaque ore (Fig. 5A).

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259

260 The same surface with cross-polarized light (crossed Nicols) indicates the presence of a
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261 high density of secondary osteons formed by the concentric lamellae in the shape of a
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262 deformed Maltese cross, since the arms are not at 90° and the osteons have a major axis,

263 whereas the rest of the bone matrix offers a very fine interlaced arrangement (MPZ 2018/502

264 T; Fig. 5B).

265 The primary osteons in the living animal are recognized by a central channel that contains

266 two or more blood vessels, but lacks a cement line that delimits them (see Hall, 2005). When

267 the passage from compact bone tissue to cancellous (trabecular) tissue is visible, a domain of
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268 pink staining is confirmed in the compact bone and subsequent bleaching, caused by a large

269 fracture in the cancellous bone. The filling of the Haversian and Volkmann channels is

270 predominantly formed by a clean carbonate without inclusions in the compact tissue, whereas

271 in the cancellous tissue the opaque ore regularly upholsters the space of the medullary cavities

between the trabeculae and is relieved by two carbonate phases (1, 2) until it occupies it

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273 completely (Fig. 5C-E).

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274 The trabecular bone that makes up the cancellous tissue shows structural fibres by

275 birefringence (MPZ 2018/496 T and MPZ 2018/500T; Fig. 5D-F). Exceptionally, the opaque

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276 ore that covers the medullary cavities can be altered, giving rise to opaque nuclei (g,

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277 goethite?), surrounded by oxidation alteration (h, hematite) (MPZ 2018/497 L; Fig. 5G-H).
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278 Most of the thin sections observed present compact tissue with limited fracturing. When

279 fracturing occurs, it corresponds to a type of fragile fracture perpendicular to the Haversian
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280 channels, with thin replacement veins formed by remobilization of the phosphatic phase,

281 making the image cleaner to concentrate the insoluble remains at the limits of the lateral
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282 advancement (MPZ 2018/496 L; Fig. 6A). In more open fractures, replacement by iron oxides
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283 occurs in the compact bone, with irregular shapes conditioned by the original microstructure,

advancing laterally towards the interior, slightly modifying its composition, but maintaining
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285 the original microstructure (MPZ 2018/499 L; Fig. 6B). In the cancellous/trabecular tissue,
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286 the crushing produced by early compaction is intense, with an accumulation of angular
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287 fragments that occupy the empty medullary spaces with the carbonated phase (there are no

288 ores here) (MPZ 2018/510 T; Fig. 6C).

289 The filling of the medullary spaces between trabeculae that occurs in the cancellous tissue

290 follows a regular pattern. The first thing that is deposited is a thin phase of opaque ore

291 (besides the iron oxides), which covers all the available space with a growth towards the

292 central zone of the hollow, recognized by small sub-spherical forms (goethite). This is
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293 followed by a filling of two differentiated carbonated phases; the first one (1) of clean equant

294 crystals, and the second one (2), similar to the previous one but dirty in appearance, with

295 insoluble iron oxides together with organic remains (MPZ 2018/496 L; Fig. 6D).

296 A special feature occurs when the cancellous bone is also mineralized by a replacement

phase of iron oxides in bands that follow the shape of the cavity. This phase advances from

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298 contact with the opaque ore to the interior of the bone in a process of replacement; neither

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299 dissolution nor the subsequent filling (permineralization) is present, as can be seen with

300 parallel and crossed Nicols (Fig. 6E-F). This replacement, more or less concentric to the

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301 shapes of the empty spaces, appears to be cut off abruptly and irregularly when observed with

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302 a greater magnification (Fig. 6G-H). AN
303 The microstructure of the ankylosaurian osteoderms is very different from what has been

304 described in the compact and cancellous tissue of the ribs, vertebrae and long bones of
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305 ornithopods.

306 By staining with Alizarin Red S, it can be seen that the bone tissues are initially pink (p),
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307 with a subsequent bleaching stage (b) favoured by the presence of very fine fractures (Fig.
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308 7A). Initially, they are composed of a compact tissue with bands of fibres parallel to each

other, which intersect perpendicularly as a network with the scattered Volkmann channels
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310 occupied by large crystals, mostly of calcite, but with evidence of opaque ores that are very
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311 thin in relation to the ornithopod samples (MPZ 2018/509 L; Fig. 7B).
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312 It is interesting to note that the filling of the empty spaces in the cancellous tissue is

313 mostly carbonated (1), with just a remnant of the earliest phase of iron oxides (MPZ 2018/511

314 T and MPZ 2018/509 T; Fig. 7C-F).

315 Under cathodoluminescence (CL), the thin sections studied provide some details. Neither

316 compact nor cancellous tissues are luminescent, although they can be differentiated from

317 opaque ores that are blacker than tissue. In the filling, a luminescent behaviour is visible by
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318 differentiating the two recognized carbonate phases. The earlier phase formed by large

319 crystals of clean equant calcite, with parallel Nicols, shows a certain arrangement in its

320 growth, where there is a non-luminescent dark zone with straight rectilinear faces, followed

321 by alternating reddish and yellow laminar growth, and finishing with a larger irregular area of

yellowish tones. There can be considered to be regular growth with well-marked areas in this

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323 phase. In the later carbonated phase formed by calcite crystals with inclusions of insoluble

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324 remains, the luminescence is massively reddish, but not intense, with some yellow areas

325 irregularly arranged and of small size. No order can be described in the growth of carbonated

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326 cement in this later phase (MPZ 2018/496 T; MPZ 2017/497 T; Fig. 8A-D).

U
327 Under ultraviolet fluorescence (UVF), the different late modifications undergone by the
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328 bone tissue are better appreciated. It is relevant to note that, just as with parallel Nicols the

329 bone periphery and fracture zones did not show the staining in a pink tone, under UVF they
M

330 show a strong light blue luminescence that advances towards the interior of the previously

331 diagenetized bone. The filling of the trabecular spaces with goethite appears inert whereas the
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332 filling formed by clean calcite crystals from the first phase (1) is sensitive, with an intense
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333 dark blue luminescence. The second phase calcite (2) appears as non-luminescent, with some

points irregularly distributed in a blue tone (Fig. 8E-F). In some sections, the bone structure
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334

335 undergoes a greater degree of alteration, leaving the entire surface practically in a light blue
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336 tone, whereas the remaining, unaffected part appears dark coloured (Fig. 8G-H).
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337

338 5. Discussion

339

340 5.1. Palaeohistology

341

342 5.1.1. Ornithopoda

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343 Among the studied samples of Ornithopoda there is great variability among the

344 palaeohistological microstructures. Poorly organized but abundant vascularization, the

345 presence of primary osteons and the absence of zonation or an external fundamental system

346 (EFS), and a succession of LAGs very close to each other (Francillon-Vieillot et al., 1990),

constitute the pattern seen in many of the samples. This pattern relates to immature

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347

348 individuals (Chinsamy-Turan, 2005; Padian and Lamm, 2013). At the same time, the

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349 secondary remodelling as Haversian bone seen in ossified tendons, some vertebrae and the

350 long bones of other individuals indicates a more mature growth state (Fig. 2A and C, 3C-D)

SC
351 (Chinsamy-Turan, 2005).

U
352 The vertebral elements show a great proportion of trabecular bone except in one sample
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353 (MPZ 2018/501) (Fig. 2A). In general, the compact tissue does not show zonation or an

354 external cortical complex that would indicate cyclicity in its growth or a mature state. The
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355 vascularization varies from primary osteons to dense Haversian tissue. Although it could be

356 said that those individuals with greater vascular complexity, such as MPZ 2018/495 (Fig. 2B
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357 and D), would be in a state of more advanced growth than those with less complexity (e.g.,
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358 MPZ 2018/494; Fig. 2C), the only thing that can be affirmed with certainty is that they would

not have reached the adult state.

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359

360 The dorsal ribs are formed from a previous cartilage mould whereas the cervical ribs are
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361 formed from the ossification of tendinous elements anchored to the caudal portion of the
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362 original cervical rib (Cerda, 2009, Zweers et al., 1987, Wedel et al., 2000). The general

363 palaeohistology of MPZ 2018/493 is summed up as lax Haversian tissue and an avascular

364 outer layer (Fig. 2E). The absence of a cortical complex indicates a subadult growth state in

365 the individual. The presence of secondary osteons in MPZ 2018/497 points to secondary

366 remodelling of the internal tissue, which is usually increased during growth (Chinsamy-

367 Turan, 2005), but it is not possible to define the state of maturity of the individual. High
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368 vascularization of simple channels in the compact bone, seen in MPZ 2018/492 (Fig. 3A-B),

369 indicates a potentially high growth rate and, along with the absence of LAGs, is an indicator

370 of bone immaturity. Given the absence of LAGs or any other signs of a slower growth rate,

371 sample MPZ 2018/499 (Fig. 2G) can be assumed not to have reached a mature state.

Ossified tendons are anatomically associated with the neural spines of the dorsal and

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372

373 caudal vertebrae, giving support to the tail. The presence of this kind of tendon is a typical

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374 feature of Ornithopoda (Sereno, 1997). Samples MPZ 2018/491 (Fig. 3F) and MPZ 2018/498

375 are composed of dense and lax Haversian tissue, respectively. The presence of this type of

SC
376 secondary tissue usually increases with age (Chinsamy-Turan, 2005; Klein and Sander, 2008).

U
377 Secondary remodelling may also be found in subadult bones, such as in the medium-sized
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378 dryosaurid Dryosaurus (Chinsamy, 1995). Given the palaeohistological features of the studied

379 material from La Cantalera-1, most of the samples do not show signs of being at an adult
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380 stage.

381
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382 5.1.2. Ankylosauria

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383 The palaeohistological features differ with the type of dermal bone, i.e. keeled scutes,

ossicles and small spines. These differences are related to the distinct functions that these
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384

385 elements may fulfil. The ossicles act as lightweight armour, and the scutes and spines are
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386 anatomical elements that probably served for exhibition or thermoregulation (Hayashi et al.,
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387 2010).

388 In the ossicles (Fig. 4A-D), a pattern in the distribution and orientation of the collagen

389 structural fibres is observed, which is assumed to provide these dermal elements with

390 hardness for their function as defensive armour (Scheyer and Sander, 2004). It has been

391 shown that the density and distribution of these collagen fibres differ among the ankylosaurs,

392 including ankylosaurids and nodosaurids (Hayashi et al., 2010). The studied ossicles (MPZ
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393 2018/506, MPZ 2018/507 and MPZ 2018/508) are entirely composed of compact primary

394 lamellar bone, without LAGs and with abundant collagen fibres. The structure formed by

395 these fibres in MPZ 2018/508 (Fig. 4A-D) matches that described by Scheyer and Sander

396 (2004) for Polacanthus foxii, although in MPZ 2018/508 the thick portion of trabecular bone

is absent. Canudo et al. (2010) described the presence of an ankylosaur close to Polacanthus

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397

398 at La Cantalera-1 on the basis of isolated teeth. The three samples studied here show vascular

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399 channels that open to the surface of the osteoderm, probably accomplishing irrigation

400 functions for the osteoderm and surrounding tissues. These vascular channels could be an

SC
401 indicator of active growth, and of a necessity for maintenance and reparation of the tissue

U
402 (Curry, 1999; Sander et al., 2006). These channels may also indicate a role as a
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403 thermoregulator (Farlow et al., 2010).

404 With regard to MPZ 2018/509, the structural organization of the collagen fibres matches
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405 with that described for MPZ 2018/508 and therefore with the structures seen in Polacanthus

406 foxii (Scheyer and Sander, 2004). In this case, the sample presents scarcely developed
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407 trabecular tissue, and the features of the compact bone suggest that, like MPZ 2018/506, MPZ
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408 2018/507 and MPZ 2018/508, the dermal scute has not reached its mature state. The variation

seen in the palaeohistological structure from the base to the tip in the small dermal spine is
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409

410 due to the different requirements of vascularization, as seen in the dorsal dermal plates of the
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411 stegosaur Stegosaurus (Buffrénil et al., 1986).

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412 Vascularization is abundant in all the ankylosaurian samples. Continuous blood irrigation

413 would have been necessary in the reparation and maintenance of the osteoderms in

414 Ankylosauria and other thyreophorans, as is observed in Stegosaurus (Farlow et al., 2010),

415 and this is evidenced by the external appearance and the histology of the dermal bones

416 (Scheyer and Sander, 2004; Hayashi et al., 2009, 2010). Therefore, it is plausible that all types
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417 of osteoderms in Thyreophora played at least a minor role in thermoregulation (Farlow et al.,

418 2010).

419 In general, the described palaeohistological features do not indicate a mature state of

420 growth. Nevertheless, a subadult state cannot be assured either. There is a delay between the

maturation of skeletal and dermal bones in Ankylosauria (Hayashi et al., 2009). This delay in

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421

422 the maturation of dermal bones is also known in other thyreophorans, such as Stegosaurus

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423 (Hayashi et al., 2009), and in extant reptiles (Vickaryous et al., 2001; Vickaryous and Hall,

424 2008).

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425

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426 5.2. Taphonomy AN
427

428 5.2.1. Generalities

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429 Initially, a recent bone is composed by weight of 70% phosphate minerals (60%

430 hydroxyapatite and 10% other phosphate minerals), 18% collagen as the main protein, 9%
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431 water, and 3% other proteins, lipids and mucopolysaccharides (glycosaminoglycans)

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432 (Pfretzschner, 2004). During fossil diagenesis, the proteins are more or less eliminated and

replaced by inorganic substances. The hydroxyapatite [Ca5(PO4)3(OH)] is modified by

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433

434 recrystallization and by the substitution of OH- and PO43- by Cl-, F- and CO32-. In this way, it
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435 becomes a carbonate fluorapatite called francolite [Ca5(PO4,CO3)3(F)], this being the most
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436 stable mineral phase. In addition, Ca2+ in apatite can be replaced by metal ions such as Fe2+,

437 U4+, Zn2+, Mn2+, Sr2+, Ba2+ and others from the active diagenetic fluids (see Pfretzschner,

438 2004 and references therein). In extreme cases, the complete mineralogical replacement of the

439 bone by pyrite or chalcedonite may occur, or even its complete dissolution, fundamentally

440 due to the aggressiveness of the percolating ground waters (Barker et al., 1997). A recent

441 study using laser-induced breakdown spectroscopy (LIBS) has determined the presence of
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442 lanthanides (Eu, Gd, La, Nd and Sm) in some crocodile and turtle fossils from this site

443 (Anzano et al., 2017).

444 The stage of early diagenesis is considered to end when the replacement of the primordial

445 collagen by minerals is completed and the fossil-diagenetic process undergone by the bone

begins. In both stages, mineral formation can take place in the porous spaces of the bone,

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446

447 although most bones remain compact and external reagents can only enter the bone by

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448 diffusion (Pfretzschner, 2004). The Haversian channels are the main routes of diffusion, since

449 they are generally arranged parallel to the long axis of the bone and are interconnected with

SC
450 Volkmann’s channels. There does not seem to be a significant flow of fluids through the

U
451 narrow lacunae of the osteons, nor through the tiny existing canaliculi. There is an even
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452 greater obstacle to diffusion flow when the secondary osteons, generated during the

453 diagenetic process and arranged around the Haversian channels, are surrounded by a compact
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454 mineral wall known as the cement line (Hall, 2005). Diffusion can hardly extend beyond this

455 line present around each secondary osteon. As a result, diffusion through the bone is a very
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456 slow and limited process. In early diagenesis, the replacement of collagen by minerals begins
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457 with the process of gelatinization, which is strongly influenced by pH, being considerably

faster with a high pH than with a neutral pH (see the extensive work of Pfretzschner, 2004 for
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458

459 more details). The increased gelatinization of the collagen allows greater hydration of the
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460 protein, whereas fresh collagen contains only small amounts of water. The hydration of the
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461 gelatinized collagen swells the bone considerably (Walrafen and Chu, 2000). This swelling

462 causes a characteristic pattern of microcracks in the Haversian channels. As a consequence,

463 the bone material in a secondary osteon swells more quickly than in the remote regions,

464 causing tension in the cement line surrounding each secondary osteon (Pfretzschner, 2004).

465 Experimentally, the so-called recrystallization window has been established, involving

466 restricted chemical conditions and a narrow alkaline pH range, in which a bone can
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467 recrystallize from carbonated apatite to authigenic apatite (Berna et al., 2004). Thus, a small

468 pH change in the medium dictates the rules of bone conservation. A bone in sediments in

469 which the pore solution has a high pH (> 8.1) is likely to be better preserved: for instance, in a

470 solution saturated with calcite. In the transition from alkaline to neutral conditions, the

mineral component of the bone will be conserved, but affected by recrystallization. When the

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471

472 pH of the fluids retained in the sediment decreases (< 7), the bone will tend to dissolve rapidly

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473 (Berna et al., 2004).

474

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475 5.2.2. Pink stains

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476 When observed with parallel polars and stained by Alizarin Red S, the thin sections of the
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477 ornithopod and ankylosaur fossil bones from La Cantalera-1 show soft pink tones that suggest

478 the incorporation of carbonate into the initial microstructure, both in the compact bone and in
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479 the cancellous tissue (Fig. 4A, C; Fig. 6A, C, E, G). As mentioned above, the bones are

480 originally formed by hydroxyapatite [Ca5(PO4)3(OH)], and during fossil diagenesis this can
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481 change to dahllite [Ca5(PO4,CO3)3(OH)] or to francolite [Ca5(PO4,CO3)3(F)], with an

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482 important contribution of carbonate in both cases. If the existing (OH-) in the microstructure

of the dahllite is replaced by (F-) in quantities greater than 1% by weight, the compound is
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483

484 considered francolite (Hubert et al., 1996, Trueman, 1999, Elorza et al., 1999). On the other
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485 hand, the degree of substitution and mineralization within the PO4-3 network varies with the
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486 type of bone, age and burial conditions during diagenesis (Timlin et al., 2000). For all these

487 reasons, it seems logical to observe this soft pink stain, which is indicative of the presence of

488 carbonates, since the XRD analysis indicates the diagenetic transformation to francolite as the

489 final resulting mineral (Table 2). The fractures and the subsequent generation of veins

490 produce a bleaching that suggests at least one modification, with a change towards neutral

491 values in the pH, with the loss of previously acquired carbonate in the bone microstructure
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492 (Fig. 6A-B). This selective absence of coloration indicates a late recrystallization forming

493 authigenic apatite without enough carbonate, with the higher degree of crystallinity already

494 commented on by Berna et al. (2004). In Table 1, the values obtained in the samples from La

495 Cantalera-1 are compared with the francolite values given by Jarvis (1992) in his work on the

phosphatic chalks used as a standard, together with the values provided by Elorza et al. (1999)

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496

497 based on dinosaur fossils from the Late Cretaceous site of Laño (Basque-Cantabrian Region).

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498 Commonly used in the study of carbonate petrology (see Jackson et al., 2010; Rosales et

499 al., 2018 and references included in both works), epifluorescence microscopy has been used

SC
500 to determine the presence of residual organic matter in a variety of fossil marine invertebrates,

U
501 since the remnant organic matter in fossil specimens fluoresces brightly despite diagenesis,
AN
502 thereby revealing its distribution. This often allows discrimination of primary features that are

503 otherwise obscured by neomorphism. The technique is rarely employed in the study of
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504 vertebrate fossil bones and fossil eggs containing embryonic remains (Jackson et al., 2010).

505 We have not found any previous reference in the literature to cases where the diagenetic
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506 alteration generated in dinosaur bones as a product of bacterial activity has been pinpointed
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507 by UVF images. In our case, under UVF the fractures are indicated by a luminescence in a

light blue tone, which determines the presence of residual organic matter (Fig. 8E-H). It
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508

509 seems that this delayed fracturing is the result of bacterial activity, also detected by the SEM
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510 in the collagen zone, which shows the presence of widespread, more or less spherical bodies
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511 ranging in size from 100-300 nm (Fig. 9A-H). These bodies could represent the relicts of

512 nanobacterial cells (Russo et al., 2006).

513

514 5.2.3. Deformation

515 The secondary osteons display the shape of a Maltese cross with cross-polarized light, but

516 the arms do not form the usual right angle; this may be indicative of having undergone
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517 crushing due to the compaction of the lamellae or simply because of the obliquity of the

518 section. The compaction is more clearly reflected in the compact tissue by the presence of

519 small fractures without displacement (Fig. 6A-B). In the cancellous tissue, there is

520 occasionally a significant collapse and accumulation of angular fragments, similar to chaotic

sedimentary breccia. Fractures have apparently occurred after filling by iron oxides (Fig. 6C).

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521

522 The fractures are refracted when they reach the goethite α-FeO (OH) filling, changing their

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523 direction and surrounding it. That is, the bone behaves in a fragile way, whereas the filling of

524 ore and carbonate is more plastic (Fig. 7C, E, G). The small radial cracks that

SC
525 characteristically run across the cement lines of secondary osteons due to the gelatinization of

U
526 the existing collagen (Pfretzschner, 2004) are here not observed.
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527 Hubert et al. (1996) interpreted the generalized fracturing of bones as evidence of

528 trampling by large animals before they were buried. This explanation does not seem plausible
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529 because such fractures are also found in bones deposited in marine sediments. Therefore, a

530 diagenetic origin due to overload pressure should be assumed as the most plausible origin for
D

531 these structures. The compact bone parts are more affected by cracking than the cancellous
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532 bone parts, probably because the latter bone structure is more flexible under a weak initial

burial pressure than compact bone, but tends to collapse completely and break under
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533

534 compaction with a higher pressure.

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535
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536 5.2.4. Fillings

537 When bone maintains its microstructure and the fluids of the medium reach the

538 intertrabecular spaces, a filling occurs with numerous and probably rapid Eh and pH

539 fluctuations, in addition to the variation in the pore water fluid composition (Barker et al.,

540 1997; Pfretzschner, 2004). The intertrabecular mineral deposits identified in La Cantalera-1

541 seem to operate with a certain independence from each other. They preserve the histological
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542 structures and follow slightly different patterns, despite being separated from each other by

543 only a few millimetres (Fig. 9A-B). It seems that the precursor mineral is initially ferrihydrite

544 [Fe3+10O14(OH)2], which in precise diagenetic conditions becomes a dominant phase of

545 goethite α-[FeO(OH)] (Table 2). The filling of the empty spaces is completed with two

different phases of calcite (Fig. 5C-F). There is no evidence of the presence of pyrite (FeS2)

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546

547 reflected by light microscopy or by XRD. Pyrite can be formed during early diagenesis due to

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548 the favourable reducing conditions that are produced by high pH values and a low redox

549 potential (pH 8, Eh <-230mV), since the decomposition of collagen contributes H2S to the

SC
550 medium (see Pfretzschner, 2000, 2001, 2004 for more details).

U
551 By contrast, under aqueous oxidizing conditions the possible oxide precursor
AN
552 (ferrihydrite) tends to become goethite and/or hematite during early diagenesis, because these

553 phases are thermodynamically more stable (Kremer et al., 2012; see also Cudennec and
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554 Lecerf, 2006; Parenteau and Cady, 2010; Das et al., 2011). When a process of dehydration

555 occurs at low temperatures, goethite becomes hematite (Faria and Lopes, 2007), although the
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556 mineralization of bacterial aggregates does not exclude the initial formation of both hematite
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557 and goethite. The precipitation of both minerals, always starting from ferrihydrite as a

precursor, is favoured by an increase in temperature and pH. Thus, it seems that hematite is
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558

559 formed under neutral or slightly alkaline conditions (pH 7-9), whereas goethite predominates
C

560 when the pH values are outside this range, being present mostly when the concentration of
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561 ions (Fe3+) grows in equilibrium with ferrihydrite, whereas hematite is more abundant when

562 the ions (Fe3+) decrease in concentration (Schwertmann and Murad, 1983).

563 In our case, goethite (detected by XRD and SEM-EDX) is the majority component in

564 parallel laminar forms just in contact with the bone, passing to radial proto-botryoidal endings

565 (Fig. 9C-E). The presence of hematite (Fe2O3) was not detected using X-ray diffraction.

566 The older calcite is superimposed on the botryoidal forms of the diagenetic goethite (Fig.
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567 9E). Such calcite appears clean and without inclusions, whereas the second phase of calcite,

568 which often leaves empty spaces unoccupied, is characterized by its dirty appearance with

569 parallel polars due to the numerous irregular and opaque inclusions that it encompasses

570 (organic matter and oxides). The behaviour in CL is well differentiated in this sense and

determines a first oxidant phase without luminescence (comprising the beginning of calcite

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571

572 precipitation with regular growth edges), which becomes a reducing environment in a part of

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573 the clean calcite with zoned growth and all the calcite presenting inclusions, where the

574 luminescence in red is homogeneous and where it has not been possible to determine

SC
575 compositional zoning (Fig. 8A-D). This behaviour suggests a depositional environment with

U
576 rapid burial and cementing already achieved in the phreatic zone, since there is no evidence of
AN
577 microstructures typical of a vadose environment, such as meniscus, pendant or geopetal

578 cements. The filling process does not necessarily occur in the same sequence in all the
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579 cavities, which is indicative that there is not a sufficiently fluid communication between the

580 Haversian-Volkmann channels to give a single pattern. This is symptomatic of how in

D

581 compact tissue the fillings sometimes occur only with opaque ore and at other times with
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582 calcite, whereas in cancellous tissue the pattern is more uniform, with the representation of

the early phase of goethite and two later phases of calcite (Fig. 4C-F, 5D-H). It seems that
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583

584 these fillings are not spaced in time, since there are no interruptions long enough to generate
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585 contractions due to the lack of fluids (mud-crack patterns in clays). All these features are
AC

586 typical of burial in a phreatic environment, without seasonal effects that could make the water

587 sheet fluctuate (hydromorphic soil?). It is generally accepted that diagenetic goethite is

588 formed under cool/wet conditions in soils rich in organic matter, whereas hematite is formed

589 under warm/dry conditions in soils poor in organic matter (Bao et al., 1998).

590 Also unique is the advance in concentric forms, sometimes with abrupt endings, of the

591 iron oxides on the concentric lamellae of the cancellous tissue. This is indicative of a
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592 diffusion process through the bone microstructure under favourable conditions, without

593 affecting it, as occurs if the pH conditions are lower (Barker et al., 1997) (Fig. 6E-H).

594 Finally, there is evidence of subsequent microbial participation, mainly in the collagen

595 bundles and the fractures mineralized by francolite, but also during the formation of goethite

and calcites, as can be seen in the images provided by UVF and SEM (Fig. 8E-H, 9A-H). The

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596

597 observed coccoid shapes are similar in size (100-300 nm) and distribution to those described

RI
598 in the ultrastructure of tadpole soft tissue and supposed coprolithic material (Toporski et al.,

599 2002), as well as those associated with the skull of a tapejarid pterosaur (Pinheiro et al., 2012)

SC
600 and with the syndepositional fibrous cements (evinosponges) found in the Middle Triassic

U
601 dolomites of Italy (Russo et al., 2006). AN
602

603 7. Conclusions
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604

605 A taphonomic and palaeohistological study of dinosaur fossil bones from the Barremian
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606 bonebed of La Cantalera-1 (Teruel) is presented. This site is one of the most significant
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607 Lower Cretaceous vertebrate localities in Spain on account of its biodiversity, having yielded

fossil remains of more than thirty vertebrate species, including dinosaurs, crocodyliforms,
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608

609 pterosaurs, mammals, lizards, turtles, lissamphibians and teleosteans.

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610 The palaeohistological study of ornithischian samples from La Cantalera-1 shows a great
AC

611 range of microstructures among Ornithopoda, corresponding mostly to immature individuals.

612 The characteristic pattern observed in the dermal bones, especially the spatial organization of

613 collagen structural fibres, allows the presence of a Polacanthus-like ankylosaur to be

614 recognized. Based on the dermal samples, the occurrence of a second ankylosaur in La

615 Cantalera-1 cannot be ruled out. The palaeohistological results support previous

616 interpretations of the relative abundance of immature ornithischian individuals in this site,
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617 including juvenile to subadult ornithopods and it is coherent with the initial palaeoecological

618 interpretation of Cantalera-1 as feeding area (Ruiz-Omeñaca et al., 1997).

619 The petrological study indicates that the bone mineral in the dinosaur samples from La

620 Cantalera-1 has become francolite (carbonate fluorapatite), with a sufficient carbonate

contribution to stain in a pale pink tone and a regular appearance in the compact and

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621

622 cancellous (trabecular) bone tissue. Subsequent fracturing modified this composition by

RI
623 bleaching the area of influence. The filling of the intertrabecular spaces is produced by

624 hemispherical forms of fibro-radial goethite and two different phases of calcite. By means of

SC
625 scanning electron microscopy (SEM) and ultraviolet epifluorescence (UVF), bacterial activity

U
626 can be verified with the formation of coccoid carpets and filaments in the bones themselves,
AN
627 fractures and, to a lesser extent, in the filling phases. The textural relationships of the mineral

628 filling suggest that the studied remains underwent rapid burial, without appreciable seasonal
M

629 effects, and quickly reached the phreatic environment where the described fossil-diagenetic

630 processes took place.

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631
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632 Acknowledgements

This research work has been financed by the project CGL2017-85038-P of the Spanish
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633

634 Ministerio de Economía y Competitividad and the European Regional Development Fund.
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635 LPG and XPS are supported by the Gobierno Vasco/Eusko Jaurlaritza (research group IT-
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636 1044-16) and by the Universidad del País Vasco/Euskal Herriko Unibertsitatea (UPV/EHU,

637 research group PPG17/05); JIC is supported by the Gobierno de Aragón (Grupos de

638 Referencia); JE is supported by the Fundación Elorza. LPG has received a pre-doctoral grant

639 from the UPV/EHU. We thank Dr. I. Rosales (IGME, Madrid) for her invaluable help in

640 obtaining epifluorescence images. We are also grateful to Rupert Glasgow for editing the

641 English text. We thank the two anonymous reviewers and the editor (Dr. Eduardo
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642 Koutsoukos), whose valuable comments and suggestions have helped improve this

643 manuscript.

644

645 References

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646

647 Alonso, A., Canudo, J.I., 2016. On the spinosaurid theropod teeth from the early

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648 Barremian (Early Cretaceous) Blesa Formation (Spain). Historical Biology 28(6), 823–834.

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650 2017. Determination of Lanthanides in fossil samples using laser induced breakdown

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651 spectroscopy. Journal of the Chemical Society of Pakistan 39(4), 516–523.
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652 Aurell, M., Bádenas, B., Canudo, J.I., Ruiz-Omeñaca, J.I., 2004. Evolución

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654 vertebrados de La Cantalera (Josa, Teruel). Geogaceta 35, 11–14.

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666 Berna, F., Matthews, A., Weiner, S., 2004. Solubilities of bone mineral from

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769 Paleontology, Zumaia, pp. 91–94.

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772 Pfretzschner, H.U., 2000. Microcracks and fossilization of Haversian bone. Neues
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781 Rogers, R., Brady, M., 2010. Origins of microfossil bonebeds: insights from the Upper
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786 Ruiz-Omeñaca, J.I., 2011. Delapparentia turolensis nov. gen et sp., un nuevo dinosaurio

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792 Zaragoza 10, 1–48.

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794 associated with nannofossils in the Marmolada Massif: evidences of microbially mediated

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795 primary marine cements? (Middle Triassic, Dolomites, Italy). Sedimentary Geology 185, 267-
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796 –275.

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798 insular dwarfism in a new Late Jurassic sauropod dinosaur. Nature 441, 739–741.

799 Scheyer, T.M., Sander, P.M., 2004. Histology of ankylosaur osteoderms: Implications for
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800 systematics and function. Journal of Vertebrate Paleontology 24, 874–893.

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801 Schwertmann, U., Murad, E., 1983. Effect pH on the formation of goethite and hematite

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803 Sereno, P.C., 1997. The origin and evolution of dinosaurs. Annual Review of Earth and
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804 Planetary Sciences 25, 435–489.

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809 Morphologic and spectral investigation of exceptionally well-preserved bacterial biofilms

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810 from the Oligocene Enspel formation, Germany. Geochimica et Cosmochimica Acta 66,

811 1773–1791.

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814

815 mississippiensis (Archosauria, Crocodylia) with comments on the homology of osteoderms.

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816 Journal of Morphology 269, 398–422.

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819 (Ed.), The Armored Dinosaurs. Indiana University Press, Bloomington and Indianapolis, pp.
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820 318–340.

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822 water structure. Chemical Physics 258, 427–446.

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824 relationships of the sauropod dinosaur Sauroposeidon. Acta Palaeontologica Polonica 45,
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825 343-388.

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826

827 system Part I: anatomy of the cervical column in the chicken (Gallus gallus L.). Acta
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828 Morphologica Neerlands-Scandinavia 25, 135-155.

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829

830 Caption of the figures and tables

831

832 Figure 1. Geographical and geological location of La Cantalera-1 site (Lower Cretaceous,

833 Teruel, Spain). A: Stratigraphical setting of the Blesa Formation. B: Location of La Cantalera-

834 1 site within the Blesa Formation section. C: Simplified geologic map of the Iberian
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835 Peninsula, palaeogeographic sub-basins (Ol: Oliete, Pa: Las Parras, Ga: Galve, Mo: Morella,

836 Pe: Perelló, Sa: Salzedella, Pg: Peñagolosa) within the Maestrazgo Basin and active faults

837 during Early Cretaceous sedimentation and geographical location of La Cantalera-1 site near

838 the village of Josa, Teruel province. Modified from Canudo et al. (2010).

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839

840 Figure 2. Palaeohistological features seen in the fossil bones of Ornithopoda indet. from the

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841 La Cantalera-1 site (Teruel, Spain) with transversal orientation. A: Vertebra (MPZ 2018/501)

842 in transverse view with multiple layers forming the external cortical complex and secondary

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843 osteons. Scale bar: 0.5 mm. B: External portion of the compact bone of the vertebra (MPZ

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844 2018/495), showing a thin avascular external layer. Scale bar: 1 mm. C: Small vertebra (MPZ
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845 2018/494) with lamellar matrix and multiple primary osteons and blood vessels. Scale bar: 0.5

846 mm. D: Transition between compact bone and the trabecular bone of the vertebra (MPZ
M

847 2018/495), with wider cavities covered by red oxides. Crossed Nicols. Scale bar: 1 mm. E:

848 Rib (MPZ 2018/493) showing scarce vascularization and external cortex with slight
D

849 lamination. Scale bar: 0.5 mm. F: Trabecular bone of the rib (MPZ 2018/493) with great
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850 cavities covered by red iron oxides. Scale bar: 0.5 mm. G: Rib (MPZ 2018/499) with

extremely abundant longitudinal vascularization and two different colorations (1 and 2) that
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851

852 may correspond to cyclical growth. Scale bar: 1 mm. H: Trabecular bone of the rib (MPZ
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853 2018/499). Trabecular cavities completely covered by red iron oxides. Crossed Nicols. Scale
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854 bar: 1 mm.

855

856 Figure 3. Palaeohistological features seen in the fossil bones of Ornithopoda indet. from the

857 La Cantalera-1 site (Teruel, Spain) with transversal orientation. A: Great abundance of blood

858 vessels and primary osteons in the compact bone of the rib (MPZ 2018/492). Scale bar: 0.2

859 mm. B: Abrupt transition between compact bone with great vascularization and trabecular
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860 bone with wider cavities in the rib MPZ 2018/492. Scale bar: 0.2 mm. C-D: Fibula (MPZ

861 2018/502) in transverse view with parallel (F) and crossed Nicols (G) showing a lax

862 Haversian bone structure. Scale bars: 1 mm. E: Transition between the compact bone and

863 trabecular bone of the fibula (MPZ 2018/502), less abrupt than in the rib (MPZ 2018/492) and

with greater trabeculae. Scale bar: 1 mm. F: Ossified tendon (MPZ 2018/491) in transverse

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864

865 view presenting dense Haversian bone structure with secondary osteons overlapping one

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866 another. Scale bar: 0.5 mm.

867

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868 Figure 4. Palaeohistological features seen in the dermal bones of Ankylosauria indet. from the

U
869 La Cantalera-1 site (Teruel, Spain) with transversal orientation. A-D: Dermal ossicle (MPZ
AN
870 2018/508) in transverse view, external cortex seen with parallel (A) and crossed Nicols (B),

871 and internal morphology with parallel (C) and crossed Nicols (D). The ossicle is mainly
M

872 formed of collagen structural fibres, seen arranged in three different orientations (1, 2 and 3)

873 both in the cortex area (A, B) and in the internal area (C, D). E: Cortex features of dermal
D

874 ossicle (MPZ 2018/507) with crossed Nicols, a blood vessel (4) opening to the surface of the
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875 ossicle. F: Inner features of the basal part of a dermal scute (MPZ 2018/505) with crossed

Nicols, showing a structure with more osteons and small trabeculae and fewer collagen
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876

877 structural fibres than the ossicles. G: Small dermal spine (MPZ 2018/503) with a skeletal
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878 bone-like inner structure without the great organization of the collagen structural fibres. H:
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879 Basal part of a small dermal spine (MPZ 2018/504) with small trabeculae and some collagen

880 structural fibres. Scale bars: 1 mm.

881

882 Figure 5. Microstructure of Ornithopoda fossil bones from the La Cantalera-1 site (Teruel,

883 Spain) with transversal orientation. A: microstructure of compact bone with densely packed

884 Haversian systems stained in pink tones by Alizarin Red S. The small fractures (indicated by
 37
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885 the green arrow heads) are bleached. The Haversian channels are completely occupied by

886 opaque ore (goethite). Parallel Nicols. Scale bar: 0.5 mm. B: the same image as A, with a

887 visibly high density of secondary osteons. Crossed Nicols. Scale bar: 0.5 mm. C-D: passage

888 from compact bone tissue to cancellous (trabecular) tissue. The filling of the Haversian and

Volkmann channels comprises a clean carbonate in the compact tissue, whereas in the

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889

890 cancellous tissue the opaque ore is regularly relieved by two carbonate phases (1, 2) until the

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891 trabecular spaces are completely occupied. Parallel and crossed Nicols. Scale bar: 0.5 mm. E-

892 F: detail of the trabecular space filled by a goethite phase and two different phases (1 and 2)

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893 of calcite. Parallel and crossed Nicols. Scale bar: 1 mm. G-H: general view and detail of the

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894 opaque phase with a nucleus that suggests a goethite (g) composition, changing to altered
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895 hematite (h). Crossed Nicols. Scale bars: G: 1 mm, H: 0.2 mm.

896 Figure 6. Fractures and process of replacement in the microstructure of Ornithopoda fossil
M

897 bones from the La Cantalera-1 site (Teruel, Spain) with transversal orientation. A: fragile
D

898 fractures pointed out by green arrow heads, with thin replacement veins formed by
TE

899 remobilization of the phosphatic phase (francolite). Parallel Nicols. Scale bars: 1 mm. B: open

900 fracture, with iron oxide replacement that advances laterally towards the interior. Parallel
EP

901 Nicols. Scale bars: 1 mm. C: cancellous tissue, affected by the intense early compaction, with

902 the accumulation of angular fragments. Parallel Nicols. Scale bars: 1 mm. D: thin phase of
C

903 opaque ore (goethite), with a growth towards the central zone of the hollow, followed by a
AC

904 filling of two differentiated carbonated phases; the first one (1) of clean spatial crystals, and

905 the second one (2) with insoluble iron oxides together with organic remains. Scale bars: 0.5

906 mm. E-H: general appearance of mineralized cancellous bone showing a replacement phase of

907 iron oxides in concentric bands. G-H: details of the bone replacement process with abrupt

908 interruptions of the advance front. Staining with Alizarin Red S. E and G with parallel Nicols,

909 F and H with crossed Nicols. Scale bars: E-F: 1 mm and G-H: 0.5 mm.
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910

911 Figure 7. Microstructure of Ankylosauria fossil bones from the La Cantalera-1 site (Teruel,

912 Spain). A-B: compact tissue with bands of fibres parallel to each other, which intersect

913 perpendicularly as a network with the scattered Volkmann channels occupied with calcite and

opaque ore crystals. It shows a generalized pink-coloured tone (p), with a subsequent

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914

915 bleaching stage (b) favoured by the presence of very fine fractures. Staining with Alizarin Red

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916 S, parallel and crossed Nicols, respectively. Thin sections with lateral orientation. C-F:

917 general view and details where small fractures are observed; the filling of the empty spaces in

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918 the cancellous tissue is mostly carbonated (1 and 2 phases), with just a remnant of the earliest

U
919 phase of iron oxides. Thin sections with transversal orientation. Parallel (C, E) and crossed
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920 (D, F) Nicols. Scale bars: 1 mm.

921
M

922 Figure 8. Different views under cathodoluminescence (CL) and epifluorescence (UVF) of

923 Ornithopoda fossil bones from the La Cantalera-1 site (Teruel, Spain). A-D: compact and
D

924 cancellous tissues are not luminescent under CL. In the filling, the earliest carbonated phase
TE

925 formed by large crystals of clean equant calcite is shown by a non-luminescent dark zone with

straight rectilinear faces, followed by alternating reddish and yellow laminar growth and
EP

926

927 finally by a larger irregular area of yellowish tones. In the last carbonated phase, formed by
C

928 dirty calcite crystals with inclusions of insoluble remains, the luminescence is massively
AC

929 reddish, but not intense, with some yellow areas irregularly arranged and of small size. A and

930 C parallel Nicols; B and D under CL. E-F: under UVF the bone periphery and fracture zones

931 show a strong light blue luminescence that advances towards the interior of the bone. The

932 filling of the trabecular spaces with goethite appears inert whereas the filling formed by clean

933 calcite crystals (first phase) is luminescent, with an intense dark blue tone. The dirty calcite

934 (second phase) appears as non-luminescent with some points irregularly distributed in a blue
 39
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935 tone. Parallel Nicols and UVF, respectively. G-H: the bone structure may undergo a greater

936 degree of alteration, leaving the entire surface practically in a light blue tone, whereas the

937 remaining part remains in a dark violet colour. Thin sections with transversal orientation.

938 Scale bars: A-D: 0.5 mm; E-H: 0.2 mm.

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939

940 Figure 9. Different views by scanning electron microscope (SEM) of the microstructure of the

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941 bone and filling of Ornithopoda fossil bones from the La Cantalera site (Teruel, Spain). A-B:

942 general view and detail in the collagen zone, which shows the presence of spherical bodies

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943 ranging in size from 100 to 300 nm, as possible relicts of nanobacterial cells. Scale bars: A:

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944 20 mm, B: 3 mm. C-D: general view and detail of the contacts, marked by black lines, among
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945 compact bone (b), goethite (g) and calcite phase (c) fillings. Scale bars: C: 100 mm, D: 30

946 mmm. E: detail of the contact between fibro-radial goethite (g) crystals and large equant
M

947 calcite crystals. Scale bar: 10 mm. F: detail view showing the massive organic coccoid carpets

948 together with a filament with helicoidal fissures (Gallionella-like bacteria). Scale bar: 20 mm.
D

949 G-H: general view and detail of the idiomorphic calcite crystals (second phase) associated
TE

950 with bacterial activity (coccoid carpets and filaments). Scale bars: G: 100 mm, H: 20 mm.
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951

952 Table 1. Ornithischian dinosaur material from the Lower Cretaceous of La Cantalera (Teruel,
C

953 Spain) included in this study.

AC

954

955 Table 2. Francolite X-ray data from phosphatic chalks (Jarvis, 1992) used as a standard

956 together with corresponding values from the fossil bones of ankylosaurian (MPZ 2017/504;

957 MPZ 2018/506) and ornithopod dinosaurs (MPZ 2018/493) from La Cantalera (Teruel). The

958 peaks, identified by their interplanar spacings in Angstroms (A) and relative intensity (I/I0),

959 are consistent with a well-crystallized francolite. Goethite (*), quartz (**) and calcite (***)
 40
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960 are minor constituents (in red colour). In bold type, the peak more characteristic of the

961 francolite (I/Io=100). Data published by the International Centre for Diffraction Data (ICDD).

962 * Goethite 29-713; ** Quartz 33-1161.

963

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Specimen nb. Taxon Type of fossil remain

MPZ 2018/491 Ornithopoda indet. Ossified tendon
MPZ 2018/492 Ornithopoda indet. Rib
MPZ 2018/493 Ornithopoda indet. Rib
MPZ 2018/494 Ornithopoda indet. Small vertebra
MPZ 2018/495 Ornithopoda indet. Neural arch
MPZ 2018/496 Iguanodontoidea indet. Ulna

PT
MPZ 2018/497 Ornithopoda indet. Proximal rib
MPZ 2018/498 Ornithopoda indet. Ossified tendon

RI
MPZ 2018/499 Ornithopoda indet. Rib
MPZ 2018/500 Ornithopoda indet. Dorsal vertebra
MPZ 2018/501 Ornithopoda indet. Vertebra

SC
MPZ 2018/502 Ornithopoda indet. Fibula
MPZ 2018/503 Ankylosauria indet. Small dermal spine
MPZ 2018/504 Ankylosauria indet. Small dermal spine (basal part)
MPZ 2018/505 Ankylosauria indet.
U
Dermal scute (basal part)
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MPZ 2018/506 Ankylosauria indet. Dermal ossicle
MPZ 2018/507 Ankylosauria indet. Dermal ossicle
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MPZ 2018/508 Ankylosauria indet. Dermal ossicle

MPZ 2018/509 Ankylosauria indet. Dermal scute
MPZ 2018/510- Ankylosauria indet. Dermal scute (fragments)
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FRANCOLITE DINOSAUR DINOSAUR DINOSAUR DINOSAUR

In Jarvis (1992) Sample 622 Sample MPZ Sample MPZ Sample MPZ
(Elorza et al., 2018/504 2018/506 2018/493

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1999)
d(A) I/I0 hkl d(A) I/I0 d(A) I/I0 d(A) I/I0 d(A) I/I0

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8.08 6 100 7.848 3.3 8.08 8 8.11 4 8.23 7
4.19* 4.19* 4.19*
4.04 6 200 4.029 3 4.06 3 4.04 4 4.07 4

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3.87 6 111 3.848 4 3.86 4 3.85 7 3.89 9
3.45 45 2 3.427 29.7 3.44 49 3.44 43 3.45 66

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3.321** 4.9
3.17 16 102 3.153 9.7 3.17 11 3.17 11 3.17 16

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3.05 18 120; 210 3.041 12.7 3.07 16 3.06 15 3.07 11
3.04*** 3.04***

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2.79 100 212; 211 2.785 100 2.80 100 2.80 100 2.8 100
2.77 55 112 2.757 64.5 2.78 71 2.77 44 2.78 71
2.69 50 300 2.684 54.4 2.70 79 2.70 54 2.7 70

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2.62 30 202 2.610 22.2 2.62 29 2.62 22 2.63 20

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2.51 4 301 2.498 4.5 2.51 8 2.51 4 2.52 18
2.443* 2.8 2.44* 2.44* 2.44*
2.28 8 122; 212 2.275 8.5 2.29 5 2.29 7
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2.24 20 130; 310 2.234 22.6 2.25 28 2.25 23 2.25 33
2.13 6 131; 311 2.121 6.5 2.13 8 2.13 4 2.13 4
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2.06 6 113 2.058 4.9 2.06 6 2.06 4 2.06 8

2.02 2 126B
AC

1.998 4 203 1.972 13 1.999 4 1.998 4 2 6

1.931 25 222 1.929 21.4 1.937 30 1.934 23 1.938 24
1.878 12 132; 312 1.878 11.6 1.878 11 1.886 8 1.886 10
1.836 30 123; 213 1.833 25 1.837 33 1.837 27 1.839 35
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1.789 12 231; 321 1.790 13.6 1.796 15 1.795 10 1.799 16

1.762 10 140; 410 1.762 13.9 1.772 13 1.767 8 1.772 6
1.742 10 402 1.739 11.3 1.745 12 1.747 9 1.751 6

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1.724 16 4 1.718 14.5 1.722 23 1.772 17 1.772 22

RI
1.632 4 232; 322 1.629 4.5 ** **
1.604 2 133; 313 1.602 2.1 1.607 3 1.602 4

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Highlights

- First palaeohistological study of Ornithischia from La Cantalera-1 (Spain).

- Presence of Polacanthus-like ankylosaur suggested by histological features of

osteoderms.

- Mineral fill suggests the dinosaur bones underwent rapid burial in a phreatic

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- Evidence of microbial (nanobacterial) participation, possibly favouring fossilization.

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