1. Introduction
The fossil Lagerstätte of Las Hoyas has yielded a rich floral and faunal continental assemblage (Sanz et al. Reference Sanz, Wenz, Yebenes, Estes, Martínez-Delclòs, Jimenez-Fuentes, Diéguez, Buscalioni, Barbadillo and Via1988; Escaso, Sanz & Ortega, Reference Escaso, Sanz and Ortega2005). Among the most significant taphonomic features of the vertebrate specimens of this site are their articulation and preservation (e.g. mineralization of soft tissue) (Briggs et al. Reference Briggs, Wilby, Pérez-Moreno, Sanz and Fregenal-Martínez1997). However, the Las Hoyas beds also contain isolated vertebrate remains, such as teeth, ribs, feathers and fish scales. Isolated elements are uncommon and only a dozen reptile teeth have been recovered. Most of them may be referred to crocodiles and the remainder to pterosaurs and theropod dinosaurs.
The Las Hoyas subbasin is located in the Serranía de Cuenca (La Huérguina Formation, upper Barremian), southwestern Iberian ranges, eastern Spain (Fregenal & Meléndez, Reference Fregenal-Martínez, Meléndez, Gierlowski-Kordesch and Kelts2000). The sequence including the Las Hoyas fossiliferous deposits is composed of laminated limestone and rare marlstone levels (Fig. 1a). These deposits were produced in the context of a continental (freshwater) subtropical carbonate wetland that overlies a low-relief karstic terrain (Buscalioni et al. Reference Buscalioni, Fregenal, Bravo, Poyato-Ariza, Sanchíz, Báez, Cambra Moo, Martín Closas, Evans and Marugán Lobón2008). The Las Hoyas biota mainly consists of obligate aquatic organisms (e.g. osteichthyan fishes, decapod crustaceans, belostomid insects, charophytes, the aquatic plant Montsechia) (Buscalioni et al. Reference Buscalioni, Fregenal, Bravo, Poyato-Ariza, Sanchíz, Báez, Cambra Moo, Martín Closas, Evans and Marugán Lobón2008) (Fig. 1b–d). The amphibious forms (crocodiles, turtles and lissamphibians) are much less abundant, and the facultative ones (terrestrial/arboreal forms such as insects, lizards and basal birds) are rather rare. Large animals such as dinosaurs are exceptional in the assemblage, and correspond to the incidental ecological category (Buscalioni & Fregenal, Reference Buscalioni, Fregenal, Barrett and Evans2006). The terrestrial macroflora is dominated by conifers (Cheirolepidiaceae) and ferns (Mantoniacea and Schizaeaceae) (Escaso, Sanz & Ortega, Reference Escaso, Sanz and Ortega2005) (Fig. 1b).
The Las Hoyas Lagerstätte (upper Barremian, La Huérguina Formation, Cuenca). (a) Example of section displaying the fossiliferous laminated deposits; (b) remains of the fern Weichselia reticulata, in association with a small fragment of the aquatic plant Montsechia vidali; (c) specimen of the aquatic belostomid insect Iberonepa romerali, adult stage (paratype ADR0268I); (d) specimen of the semionotid fish Lepidotes tanyrhis (holotype MCCM LH-7410). Scale bars in (b, c) equal 1 cm. Scale bar in (d) marked in 1 cm increments. For further information, see http://www.yacimientolashoyas.es.
To date, the only published evidence of pterosaurs at Las Hoyas corresponds to an isolated track (LH-6500). This track (Fig. 2a) was first attributed to a Pteraichnus-like footprint (Lockley et al. Reference Lockley, Logue, Moratalla, Hunt, Schultz and Robinson1995), then tentatively to a turtle (Moratalla et al. Reference Moratalla, Lockley, Buscalioni, Fregenal-Martínez, Meléndez, Ortega, Pérez-Moreno, Pérez-Asensio, Sanz and Schultz1995), and thereafter it has repeatedly been regarded as a pterosaur manus track (Wright et al. Reference Wright, Barrett, Lockley, Cook, Lucas, Kirkland and Estep1998; Lockley & Meyer, Reference Lockley and Meyer2000). However, according to aspects of its morphology (e.g. digit orientation and proportion, posterior surrounding bulge) and size (it is 30 cm wide), this track may be a theropod footprint, displaying a peculiar ‘asymmetric’ pattern of preservation (Fig. 2a). Furthermore, some theropod trackways from Las Hoyas also contain footprints with the same morphological features and taphonomic preservation (Fig. 2b). Thus, the teeth described in this paper are the first convincing evidence of the presence of pterosaurs at Las Hoyas.
Tracks from the upper Barremian of Las Hoyas (La Huérguina Formation, Cuenca). (a) Tridactyl theropod footprint (LH-6500), previously identified as a pterosaur track. Besides its large size, note also the prominent posterior bulge, left by a heavy animal. Such features are not consistent with a pterosaurian origin. In addition to the digit distal acumination, digit proportion and interdigital angles, these characters are more congruent with a theropod footprint; (b) theropod trackway showing similar footprints. Scale bar in (a) in 1 cm increments, totalling 5 cm.
2. Description of the teeth and comparisons
The material studied (housed in the Museo de las Ciencias de Castilla–La Mancha, Cuenca) consists of four teeth (Fig. 3). They can be separated into two morphotypes which are regarded here as two distinct taxa. The first morphotype is represented by the specimens LH-28572 and LH-15448 (Fig. 3a, b). LH-28572 is 4.7 mm long and shows its lingual(?) face. The crown is very slender and weakly recurved (convex mesial carina and concave distal one). It is laterally compressed and its base is constricted. The crown is inflated just above this constriction. The enamel is very finely folded, giving an irregular, granular surface. Both mesial and distal edges are obtusely angled near the base. Below these angles, both edges are rectilinear and the crown is devoid of enamel. Sharp carinae, especially the distal one, are better developed in the wider part of the crown. There is a very shallow depression in the medial zone of the basal part of the crown. Some very slight, apically concave, growth rings are present. The second tooth of this morphotype (LH-15448) is slightly larger (5.8 mm long) and more robust than LH-28572. It shows its convex labial face. The crown has the same curvature and enamel pattern. The basal constriction is less marked, especially in the mesial part of the crown.
Pterodactyloid teeth from the upper Barremian of Las Hoyas (La Huérguina Formation, Cuenca). As they are included in the lithographic limestone, only one face is available for description. a, a′: LH-28572, indeterminate Istiodactylidae tooth in lingual(?) view; b, b′: LH-15448, indeterminate Istiodactylidae tooth in labial view; c, c′: LH-17264, indeterminate Ornithocheiridae tooth in labial view; d, d′: LH-21451, indeterminate Ornithocheiridae tooth in labial view. Scale bars equal 1 mm (a, a′, b, b′) and 1 cm (c, c′, d, d′).
Among pterodactyloids, these two specimens from Las Hoyas are very similar in shape and size to the teeth of Haopterus gracilis, a medium-sized pterosaur from the Barremian Yixian Formation in China (Wang & Lü, Reference Wang and Lü2001). Haopterus has slender, labiolingually compressed, slightly recurved teeth that do not attain a length of 10 mm. As observed in LH-28572 and LH-15448, their crown is slightly inflated and has a basal constriction (Wang & Lü, Reference Wang and Lü2001). Haopterus, originally described as Pterodactylidae, has been recently reinterpreted as either the sister group of Ornithocheiroidea (Andres & Ji, Reference Andres and Ji2008) or the basalmost Ornithocheiroidea (Lü et al. Reference Lü, Unwin, Xu and Zhang2008). Finally, the most recent study concludes that Haopterus is a basal Istiodactylidae (Lü, Xu & Ji, Reference Lü, Xu and Ji2008). LH-28572 and LH-15448 are therefore assigned to this family. Some of the small pterodactyloid teeth from the Barremian of Vallipón (Teruel) described by Ruiz-Omeñaca, Canudo & Cuenca-Bescós (Reference Ruiz-Omeñaca, Canudo and Cuenca-Bescós1998, figs 1, 2a–i) are very similar to the Las Hoyas specimens and may represent the same taxon. A few teeth from Galve (Teruel), described by Sánchez-Hernández, Benton & Naish (Reference Sánchez-Hernández, Benton and Naish2007, fig. 5c) as Ornithocheiridae ‘morphotype 3’, might also belong to the same form. These authors also reported another kind of teeth (‘morphotype 4’) which they assigned to an indeterminate Istiodactylidae. The tooth figured by Sánchez-Hernández, Benton & Naish (Reference Sánchez-Hernández, Benton and Naish2007, fig. 5d) is broader at its base than the Las Hoyas specimens. Istiodactylids, first described from the mid-Early Cretaceous of southern England (Howse, Milner & Martill, Reference Howse, Milner, Martill, Martill and Naish2001), are also well known from deposits of similar age in northeastern China (Lü, Xu & Ji, Reference Lü, Xu and Ji2008).
The other two teeth represent the second morphotype (Fig. 3c, d). The specimen LH-17264, like the others, is partly included in the matrix, and shows its labial face. The tooth is large (37 mm long), relatively slender, labiolingually compressed and probably occupied an anterior position in the jaw. It is markedly curved mesiodistally (mesially convex), and also shows slight labiolingual curvature (labially convex). In lateral view, a very thin enamel layer is apparent on the apical half of the crown. Ornamentation is present on the entire crown but is very weak. It consists of slight, irregular, longitudinal folds. Some very slight growth folds, concave toward the apex, are present near the base. A poorly marked distal carina is present on the enamelled part of the crown. The mesial edge is rounded and devoid of carina. The apex shows a small wear facet oriented distally. The specimen LH-21451 (17 mm long) corresponds to an incomplete crown in labial view. Its morphology and enamel pattern are similar to those of LH-17264, and it may also be an anterior tooth. However, it is less curved and devoid of ornamentation. Two mesial and distal carinae are present, but they are blunt and poorly marked. The crown section is oval around its base. The apex is worn.
The most parsimonious interpretation would be that these two large specimens, rather similar in morphology to the anteriormost teeth of Haopterus, derive from the same taxon as LH-28572 and LH-15448. However, the teeth of istiodactylids are relatively small and generally do not exceed 10 mm in length. Furthermore, the significant difference in tooth size between the two morphotypes described here clearly indicates that two distinct toothed pterosaurs occur at Las Hoyas. By their general morphology, size and enamel pattern, the two large pterosaur teeth of Las Hoyas LH-17264 and LH-21451 must be assigned to the widespread family Ornithocheiridae ( = Anhangueridae). They display the same dental morphotypes (I and III) as those defined by Wellnhofer & Buffetaut (Reference Wellnhofer and Buffetaut1999) on the basis of teeth from the Cenomanian of Morocco. In Western Europe, a Barremian ornithocheirid (Caulkicephalus trimicrodon) was recently described from the English Wessex Formation (Steel et al. Reference Steel, Martill, Unwin and Winch2005). However, its teeth are unknown and a direct comparison with the Las Hoyas material is not possible. In Spain, the Barremian ornithocheirid-like teeth described by Ruiz-Omeñaca, Canudo & Cuenca-Bescós (Reference Ruiz-Omeñaca, Canudo and Cuenca-Bescós1998) and Sánchez-Hernández, Benton & Naish (Reference Sánchez-Hernández, Benton and Naish2007) are smaller and morphologically distinct. In China (Liaoning), ornithocheirids are only represented by Liaoningopterus gui from the Aptian Jiufotang Formation (Wang & Zhou, Reference Wang and Zhou2003). Anterior teeth of this taxon can reach a length of up to 81 mm and are rather similar to our specimens (slender crown, mesiodistal curvature). LH-17264 and LH-21451 are also very close to the teeth of various ornithocheirids (e.g. Anhanguera, Coloborhynchus) from the Crato and Santana formations in Brazil (Kellner & Tomida, Reference Kellner and Tomida2000; Unwin & Martill, Reference Unwin, Martill, Martill, Bechly and Loveridge2007).
3. Discussion and conclusions
The discovery of pterosaurs at Las Hoyas is remarkable for several reasons: (1) they are not preserved as articulated skeletons; (2) their remains represent a very small fraction of the assemblage (< 1 ‰); (3) they correspond to medium-large individuals. The discovery of isolated teeth is uncommon at Las Hoyas, where most organisms are found in an at least partially articulated state. Furthermore, exceptional preservation tends to occur only in small- to medium-sized individuals, denoting both a taphonomic and a palaeoecological size bias (Buscalioni & Fregenal, Reference Buscalioni, Fregenal, Barrett and Evans2006). All these observations suggest that pterosaurs were incidental forms within the Las Hoyas ecosystem. The scarcity and poor preservation of pterosaurs at Las Hoyas are two points that are similar to the taphonomic conditions observed at Cerin. Indeed, the Kimmeridgian lithographic limestones of this French Lagerstätte have yielded only a few isolated pterosaur bones, whereas other reptiles are more abundant and much better preserved, for reasons that remain unclear (Buffetaut et al. Reference Buffetaut, Bernier, Barale, Bourseau, Gaillard, Gall and Wenz1990).
The teeth found at Las Hoyas are comparable with those of the pterosaur taxa from the Early Cretaceous Lagerstätten of Brazil (Crato and Santana formations) and China (Yixian and Jiufotang formations). In terms of palaeoenvironment and biostratigraphy, the Chinese localities are the most similar to that of Las Hoyas. The Barremian–early Aptian freshwater deposits of Liaoning have yielded a diverse pterosaur fauna, including two pterodactyloids (the istiodactylid Haopterus and the ornithocheirid Liaoningopterus), which might have been taxonomically and palaeoecologically close to the Las Hoyas forms. Wang et al. (Reference Wang, Kellner, Zhou and Campos2005) and Martín-Closas & Wang (Reference Martín-Closas and Wang2008) underlined the broad faunal and floral exchanges and palaeobiogeographic affinities between Eastern Asia and Europe: as in many other latest Jurassic–Early Cretaceous groups, the closest relatives of some pterosaurs (Feilongus and Nurhachius) from the Barremian–Aptian of Liaoning may be found in Western Europe. Palaeoenvironmentally, the La Huérguina Formation is interpreted as a complex wetland ecosystem composed of alluvial plain, channels, ponds and shallow lakes, and palustrine marshy areas (Buscalioni et al. Reference Buscalioni, Fregenal, Bravo, Poyato-Ariza, Sanchíz, Báez, Cambra Moo, Martín Closas, Evans and Marugán Lobón2008). The apparent absence of pterosaur body remains at Las Hoyas is intriguing since its biota is highly comparable in palaeoecological structure with that of Jehol in China (Zhou, Barrett & Hilton, Reference Zhou, Barrett and Hilton2003). As in Liaoning (Wang et al. Reference Wang, Kellner, Zhou and Campos2005), birds are much more abundant than pterosaurs at Las Hoyas. Conversely, the more coastal deposits of the Crato and Santana formations have yielded numerous pterosaur specimens, while bird remains are extremely rare in these Brazilian Lagerstätten (Naish, Martill & Merrick, Reference Naish, Martill, Merrick, Martill, Bechly and Loveridge2007). This would tend to confirm the hypothesis of Wang et al. (Reference Wang, Kellner, Zhou and Campos2005) about the spatial distribution of avian and pterosaur faunas during the Early Cretaceous; these authors argued that birds would have been more abundant in terms of number of specimens (and taxonomically more diverse?) in inland areas (e.g. continental wetlands), whereas pterosaur populations would have been mainly concentrated in coastal areas. However, it is worth noting that several new pterosaur taxa have been described from the Yixian and Jiufotang formations since 2005 and that the pterosaur fauna recovered from the Jehol Biota now represents the most rich and diverse assemblage (hundreds of specimens and more than 20 species) known from anywhere at any time. This observation is at variance with the hypothesis formulated by Wang et al. (Reference Wang, Kellner, Zhou and Campos2005) and shows that such palaeoecological conclusions must be regarded with caution.
Acknowledgements
We thank the two anonymous reviewers for their constructive suggestions and critical comments. This article is a contribution to the Spanish project CGL2005-01121 of the Ministerio de Ciencia e Innovación.
