1. Introduction
The Early Cretaceous Las Hoyas Lagerstätte is famous for its rich and diverse wetland assemblage including numerous plant, invertebrate and vertebrate taxa (Sanz et al. Reference Sanz, Wenz, Yebenes, Estes, Martínez-Delclòs, Jimenez-Fuentes, Diéguez, Buscalioni, Barbadillo and Via1988, Reference Sanz, Fregenal-Martínez, Meléndez, Ortega, Briggs and Crowther2001; Fregenal-Martínez & Meléndez, Reference Fregenal-Martínez, Meléndez, Gierlowski-Kordesch and Kelts2000; Escaso, Sanz & Ortega, Reference Escaso, Sanz and Ortega2005; Buscalioni & Fregenal-Martínez, Reference Buscalioni and Fregenal-Martínez2010). In this upper Barremian locality, tetrapods are mostly articulated and occasionally preserve soft tissue and histological structures (Briggs et al. Reference Briggs, Wilby, Pérez-Moreno, Sanz and Fregenal-Martínez1997; Gupta et al. Reference Gupta, Cambra-Moo, Briggs, Love, Fregenal-Martínez and Summons2008; Bailleul et al. Reference Bailleul, Ségalen, Buscalioni, Cambra-Moo and Cubo2011). The tetrapods found at Las Hoyas belong to Salientia, Caudata, Albanerpetontidae, Scincomorpha, Chelonia, Pterosauria, Crocodyliformes, and Dinosauria (including Aves) (Buscalioni & Fregenal-Martínez, Reference Buscalioni and Fregenal-Martínez2010). Most of the recorded species are small-sized forms (ranging from 5 to 30 cm in total length), except for the dinosaur and pterosaur taxa. Small (subadult to adult) individuals are largely dominant in the assemblage, whereas large ones are exceptional. Considering that body size plays a relevant role in the ecology of wetlands (van der Valk, Reference van der Valk2006), the large species have been interpreted as incidental, i.e. species occasionally found in wetlands (Buscalioni & Fregenal-Martínez, Reference Buscalioni, Fregenal-Martínez, Barrett and Evans2006, Reference Buscalioni and Fregenal-Martínez2010). Pterosaurs are known from isolated teeth, and a fragmentary skull and mandible. They have been referred to as indeterminate istiodactylids and ornithocheirids (Vullo et al. Reference Vullo, Buscalioni, Marugán-Lobón and Moratalla2009), and a new tapejarid taxon, Europejara olcadesorum, was recently erected (LH-9413; Vullo et al. Reference Vullo, Marugán-Lobón, Kellner, Buscalioni, Gomez, de la Fuente and Moratalla2012). The non-avian dinosaur record is composed of footprints and two species each known from a single individual: the ornithomimosaur Pelecanimimus polyodon (LH-7777; Pérez-Moreno et al. Reference Pérez-Moreno, Sanz, Buscalioni, Moratalla, Ortega and Rasskin-Gutman1994), and the carcharodontosaur Concavenator corcovatus (LH-6666; Ortega, Escaso & Sanz, Reference Ortega, Escaso and Sanz2010). Dinosaur and crocodile footprints are concentrated at the base of each unit, and they are associated with facies from drier periods (Buscalioni & Fregenal-Martínez, Reference Buscalioni and Fregenal-Martínez2010). The Las Hoyas dinosaur footprints are frequently distorted and were produced by rather large theropods (Vullo et al. Reference Vullo, Buscalioni, Marugán-Lobón and Moratalla2009).
Here, we describe an exquisitely preserved specimen with integument impressions. The fossil is an isolated but fully articulated lower hindlimb of a medium sized iguanodontian ornithopod. This discovery represents the first clear occurrence of an ornithischian dinosaur at Las Hoyas and complements the palaeoecological reconstruction and trophic network of this ancient wetland.
2. Description
The material studied (specimen LH-30677 housed in the Museo de las Ciencias de Castilla-La Mancha, Cuenca) consists of an incomplete but fully articulated right hindlimb (Figs. 1, 2; see Table 1 for measurements). The femur is missing, as well as the proximal extremities of both the tibia and fibula. While the latter two bones are exposed in anterior view, all pes elements (i.e. tarsals, metatarsals, and phalanges) are visible in ventral view. The phalangeal formula of this tridactyl pes is clearly recognizable: 0-3-4-5-0. The maximal length of the foot is about 32 cm.
*Preserved lengths
The tibia shaft is slightly crushed anteroposteriorly, and the distal extremity is hidden by the overlying metatarsals. The calcaneum is in contact with the distal end of the fibula. The ventral surface is convex. The astragalus is fully hidden. Two flat, oval-shaped bones adjacent to the proximal ends of the metatarsals III and IV are probably the distal tarsals III and IV, respectively. Four metatarsals are present (I–IV). Although most of the metatarsal I is hidden, this bone is notably reduced when compared to the functional II–IV metatarsals. The first metatarsal shows a stylus-like shape, and distally reaches the middle part of the metatarsal II. The metatarsal II is the shortest of the three functional metatarsals. The proximal articular surface has a rectangular outline with concave medial and straight lateral edges. In ventral view, the shaft is compressed. The shaft of metatarsal II curves gently medially towards its distal end. The proximal end of the metatarsal II anteriorly overlaps that of the metatarsal III with a tab of bone on the craniomedial margin. The metatarsal III is the longest and most robust bone of the metatarsus, being 30% and 20% longer than metatarsals II and IV, respectively. It displays a strong ventral crest developed from the proximal extremity to the middle of the medial border, and a median crest that reaches the distal articulation. The proximal crest delimits a medial surface where the metatarsal II is ventrally lying, while the metatarsal III anteriorly overlaps the proximal end of the metatarsal IV. The shaft of the metatarsal IV is robust, and shows a slight lateral curvature. The metatarsal IV bears a proximal medial crest, and the proximal articular surface extends lateromedially.
The proximal phalange is the largest one in all three digits. The proximal phalange of the digit II has an elongate rectangular shape, while those of the digits III and IV are more robust. More distal phalanges become progressively shorter before culminating in the pedal unguals. The unguals are relatively elongate with a blunt, rounded distal extremity. Some slight brownish integument impressions are preserved around the digits II, III and IV. However, no scale-like structures can be observed. Examination of the specimen under ultraviolet light reveals two types of integumentary structures: (1) whitish structures at the ungual tips which may correspond to the hoof-like claws; and (2) dark structures around each digit which may correspond to the toe pads.
3. Discussion and conclusions
The fossil record of basal iguanodonts (i.e. non-hadrosaurid members of Iguanodontia; McDonald, Reference McDonald2012a ) is well documented in the Early Cretaceous of Western Europe, with most of the material coming from England (Norman, Reference Norman and Batten2011), Belgium (Norman, Reference Norman1980), Germany (Norman, Reference Norman1987), France (Martin & Buffetaut, Reference Martin and Buffetaut1992) and Spain (for an exhaustive review of the Spanish occurrences, see Ruiz-Omeñaca, Canudo & Cuenca-Bescós, Reference Ruiz-Omeñaca, Canudo and Cuenca-Bescós1998). Until recently, almost all iguanodontian remains found in the Early Cretaceous of Europe had been assigned to the classic genus Iguanodon. At present, this group has an intricate taxonomy because of the erection of several new genera and species during the last five years: Mantellisaurus Paul, Reference Paul and Carpenter2007; Dollodon Paul, Reference Paul2008; Owenodon Galton, Reference Galton2009; Barilium Norman, Reference Norman2010 (objective senior synonym of Torilion Carpenter & Ishida, Reference Carpenter and Ishida2010); Hypselospinus Norman, Reference Norman2010 (objective senior synonym of Wadhurstia Carpenter & Ishida, Reference Carpenter and Ishida2010); Proplanicoxa Carpenter & Ishida, Reference Carpenter and Ishida2010; Sellacoxa Carpenter & Ishida, Reference Carpenter and Ishida2010; Kukufeldia McDonald, Barrett & Chapman, Reference McDonald, Barrett and Chapman2010 and Delapparentia Ruiz-Omeñaca, Reference Ruiz-Omeñaca2011. According to Norman (Reference Norman and Batten2011) and McDonald (Reference McDonald2012b ), Iguanodon bernissartensis and Mantellisaurus atherfieldensis are the only two taxa of large-bodied iguanodonts present in the Barremian–Aptian of Belgium and England, Dollodon bampingi being considered a junior synonym of the latter by these authors.
Concerning the foot anatomy of basal iguanodonts such as Iguanodon and Mantellisaurus, there are only a few detailed descriptions of associated, sometimes fully articulated, pes elements. The holotypic material of Mantellisaurus atherfieldensis (NHMUK R5764) includes almost all pes elements (Hooley, Reference Hooley1925; Norman, Reference Norman1986, Reference Norman and Batten2011). The Bernissart specimen assigned to Mantellisaurus atherfieldensis (IRNSB 1551) also provides information on the foot anatomy of this taxon. The well-preserved, articulated specimen NHMUK R1829 from the Barremian of the Isle of Wight, referable to Mantellisaurus atherfieldensis (Norman, Reference Norman and Batten2011), was originally described by Owen (Reference Owen1858a , Reference Owen b ) then re-figured by Naish & Martill (Reference Naish, Martill, Batten and Naish2001) as Iguanodon sp. Another well-preserved specimen (NHMUK R28685), also from the Barremian of Isle of Wight, was described by Hulke (Reference Hulke1882) as Iguanodon seelyi, a junior synonym of Iguanodon bernissartensis following Norman (Reference Norman and Batten2011) and McDonald (Reference McDonald2012b ). The foot anatomy of Iguanodon bernissartensis is also well-known on the basis of the material from Bernissart, especially thanks to the description of the holotype IRNSB 1534 by Norman (Reference Norman1980).
As underlined by Norman (Reference Norman and Batten2011), the hindlimb bones, including the lower leg elements, are not particularly distinctive. However, some differences can be noted between Mantellisaurus and Iguanodon regarding the size, proportion, and morphology of the various pes bones. The large species Iguanodon bernissartensis has a foot made of robust elements. The metatarsal I is reduced and laterally flattened. The length of the metatarsal III ranges from 270 to 350 mm among the specimens from Bernissart (Norman, Reference Norman1980), this length roughly corresponds to 1.5 to 2 times the value observed in the Las Hoyas specimen. The smaller taxon Mantellisaurus atherfieldensis has a more gracile foot, with more slender bones. The metatarsal I (preserved in NHMUK R1829) is narrow and has a rod-like shape, similar to the condition observed in LH-30677. In Mantellisaurus atherfieldensis, the metatarsal III is 280 mm in length. The phalangeal formula and the way in which the metatarsals II to IV are arranged in LH-30677 are the same as those in Mantellisaurus and Iguanodon. Until more material is recovered, the Las Hoyas iguanodont is tentatively assigned to Mantellisaurus atherfieldensis because of the relative proportions of the foot. However, some slight differences can be noted in the Las Hoyas specimen: the foot is more lightly built; the metatarsal IV is relatively enlarged in relation to the narrow metatarsal II; and the unguals are relatively small compared to other phalanges. Such differences may be ontogenetic, but could also suggest that the Las Hoyas iguanodont represents a new, smaller taxon.
The specimen LH-30677 was collected in situ from a taphonomically controlled area named ‘Magenta’. The fossil was apparently isolated and was showing the top part of the metatarsal III embedded in a thick (~7 cm) slab. Although no additional material has been recovered from around this specimen to date, the rest of the skeleton might be preserved in the still unexcavated part of the ‘Magenta’ area. This hindlimb was probably separated from the fleshy carcass and was buried before it could be scattered. Complete to sub-complete isolated limbs remaining in articulation and preserved more or less far away from the rest of the skeleton (or inversely a nearly complete articulated skeleton missing some limbs, e.g. the crocodyliform Susisuchus from the Cretaceous Crato Formation in Brazil; Salisbury et al. Reference Salisbury, Frey, Martill and Buchy2003) are relatively frequent in the fossil record. This kind of preservation, corresponding to the taphonomic subclass IIB defined by Holz & Barberena (Reference Holz and Barberena1994), often occurs when subaerial processes lead to mummification (i.e. dehydrated carcasses). Mummification is not unusual at Las Hoyas (e.g. the albanerpetontid Celtedens; McGowan & Evans, Reference McGowan and Evans1995) and that phenomenon might be linked to the occurrence of some extreme temperatures during the warm and dry seasons (Buscalioni & Fregenal-Martínez, Reference Buscalioni and Fregenal-Martínez2010).
More or less well-preserved iguanodont remains are not rare in lower stratigraphic sequences (Rambla de Las Cruces I) of the La Huérguina Formation (Buscalioni et al. Reference Buscalioni, Fregenal, Bravo, Poyato-Ariza, Sanchíz, Báez, Cambra-Moo, Martín-Closas, Evans and Marugán-Lobón2008). Some isolated vertebrae and a femur were reported from the nearby locality of Buenache de la Sierra (see Ruiz-Omeñaca, Canudo & Cuenca-Bescós, Reference Ruiz-Omeñaca, Canudo and Cuenca-Bescós1998). LH-30677 represents the first discovery of an ornithopod dinosaur in the Las Hoyas limestone and the third non-avian dinosaur body fossil. As mentioned above, the only occurrences of non-avian dinosaurs at Las Hoyas correspond to a few medium-sized dinosaur footprints (15 to 35 cm in length) and two well-preserved skeletons, corresponding to 2–2.5 m (Pelecanimimus) and 6 m (Concavenator) long animals. The Las Hoyas iguanodont would correspond to an individual about 5.5 to 6 m long. This bias (i.e. the very low relative abundance of medium to large-sized animals) has also been noted for the Late Jurassic locality of Guimarota (Martin, Reference Martin, Martin and Krebs2000), suggesting that heavy dinosaurs probably avoided the soft substrate of such a coastal palaeoenvironment. The Las Hoyas deposits have been interpreted as a rather isolated carbonate shallow subtropical lake located in a complex wetland system (Buscalioni & Fregenal-Martínez, Reference Buscalioni and Fregenal-Martínez2010). Thus, a similar hypothesis can be applied for the muddy palaeoenvironment of Las Hoyas. This rareness supports the notion of facultative to incidental categories, i.e. organisms that may be found in wetlands and in the terrestrial surrounding environments, or only occasionally found, respectively (Buscalioni & Fregenal-Martínez, Reference Buscalioni and Fregenal-Martínez2010). Thus, considering the Las Hoyas iguanodont as a facultative organism is not surprising considering the large number of terrestrial plants (e.g. ferns and conifers mostly represented by Weichselia and Frenelopsis, respectively) present in that palaeoecosystem (Gomez et al. Reference Gomez, Martín-Closas, Méon, Thévenard and Barale2001). Lastly, an ornithopod dinosaur such as Mantellisaurus may have represented a valuable prey item for the top predator Concavenator, thus fulfilling the reconstruction of the trophic chain of this ancient ecosystem.
Acknowledgements
This article is a contribution to Project CGL2009-11838BTE of the Spanish Ministerio de Ciencia e Innovación and the Junta de Castilla-La Mancha.