Bull. Soc. géol. France, 2012, t. 183, no 6, pp. 525-528

An early azhdarchid pterosaur from the Lower Cretaceous of the eastern Paris basin ERIC BUFFETAUT

Key-words. – Pterosauria, Azhdarchidae, Vertebra, Early Cretaceous, Albian, Sables verts, Cambridge Greensand, France, Phosphate. Abstract. – A pterosaur vertebra from the Early Cretaceous (Albian) Sables verts of Grandpré (Ardennes, northeastern France) is characterised by its elongation, its very low neural arch confluent with the centrum, and the presence of a tuba vertebralis. It is referred to the family Azhdarchidae and is one of the earliest well-attested records of this group. The pterosaur diversity of the Sables verts is higher than previously recognised.

Un ptérosaure azhdarchidé très ancien dans le Crétacé inférieur de l’Est du bassin de Paris

Mots-clés. – Pterosauria, Azhdarchidae, Vertèbre, Crétacé inférieur, France. Résumé. – Une vertèbre de ptérosaure des Sables verts du Crétacé inférieur (Albien) de Grandpré (Ardennes, Nord-Est de la France) se caractérise par son élongation, son arc neural très bas confluent avec le centrum et la présence d’un tuba neuralis. Elle est rapportée à la famille des Azhdarchidae, dont elle constitue un des plus anciens représentants bien attestés. La diversité des ptérosaures des Sables verts est plus élevée qu’on ne le pensait jusqu’ici.

INTRODUCTION the Early Cretaceous Greensand (Sables verts)ofthatarea. During the “phosphate rush” of the late 19th century, abun- Azhdarchids were one of the most widespread groups of dant fossils (including plants, invertebrates and vertebrates) pterosaurs during the Late Cretaceous [Witton and Naish, were found whilst mining nodules for fertiliser, in exactly 2008]. It is generally accepted that they originated in the the same way as the Cenomanian Cambridge Greensand Early Cretaceous, if not earlier, but their fossil record be- fossils in England [Unwin, 2001; Buffetaut, 2006)]. Pterosaur fore the Cenomanian is extremely scanty, as Late Jurassic or remains obtained in this way were first reported by Barrois Early Cretaceous records are disputable [Witton and Naish, [1875], and referred by Sauvage [1882] to Pterodactylus 2008], although a cervical vertebra from the Berriasian of sedgwicki, a Cambridge Greensand taxon erected by Owen Romania does seem to belong to an azhdarchid [Dyke et al., [1859]. 2011]. As a result, Early Cretaceous azhdarchids tend to ap- pear as “ghost lineages” in pterosaur phylogenies [e.g. The Sables verts of the eastern Paris basin are generally Unwin, 2006]. considered to have been deposited in a calm shallow marine The present paper describes an isolated cervical verte- environment during the early Albian [Magniez-Jannin and bra from the Albian Sables verts of the eastern Paris basin, Demonfaucon, 1980]. With a few exceptions, most the ver- which appears to belong to an azhdarchid and is thus one of tebrate remains they have yielded are isolated bones, which the oldest known records of that group. may be related to phosphate extraction techniques [see Buffetaut, 2006].

GEOGRAPHICAL AND GEOLOGICAL SETTING The specimen was found in the palaeontological collection DESCRIPTION of University Paris 6 (formerly the palaeontological collec- tion of the Sorbonne). Its label indicates that it was part of The specimen (Collection paléontologique de l’Université the Toucas collection. Aristide Toucas (1843-1911) was a Paris 6, UPMC-080) is a relatively well preserved cervical French palaeontologist mainly remembered for his work on vertebra, lacking mostly parts of the neural spine (fig. 1). rudists [see Pervinquière, 1912]. A scrap of paper kept to- Its posterior part is embedded in a phosphate nodule. Be- gether with the fossil indicates that it comes from Grandpré, cause of the hardness of the nodule and of the fact that there a village in département Ardennes, in the Argonne region is no clear discontinuity between it and the phosphatic fos- of eastern France, which in the 19th century was one of the sil, only very limited preparation could be carried out, so main centres for the exploitation of phosphate nodules from that few details are visible in the phosphate-covered areas.

CNRS, UMR 8538, Laboratoire de Géologie de l’Ecole Normale Supérieure, 24 rue Lhomond, 75231 Paris Cedex 05, France. Manuscript accepted on April 9, 2012

Bull. Soc. géol. Fr., 2012, no 6 526 BUFFETAUT E.

The most striking feature of the vertebra is its elonga- a short bony ridge is separated from the prezygapophysis by tion relative to its breadth (total length: 70 mm; minimum a groove, which may correspond to the passage of the verte- width: 16 mm). Both ends of the centrum are transversely bral artery. Posteriorly, details of the ventral surface of the expanded, the posterior end more so than the anterior end centrum are obscured by phosphatic matrix. (posterior width: 33 mm; anterior width: 26 mm). The nar- The posterior end of the vertebra is enclosed in a rowest part of the centrum is at about the level of the poste- rounded phosphate nodule which seems to approximately rior third of its length. The neural spine is not clearly follow the outline of the articular condyle. The posterior separated from the centrum; its dorsal part is broken or opening of the neural canal is completely obscured by ma- worn off along its whole length, but to judge from the slope trix, but it appears that that region was limited dorsally by a of its flanks, it must have been quite low and roof-shaped, posteriorly concave rim. Laterally, the postzygapophyses albeit taller at its anterior and posterior ends. The anterior are partly preserved, and on the left side a well defined, end of the vertebra shows, ventrally, the concave articular slightly hooked epipophysis is visible. Just below it, the area for the preceding centrum, which is much wider than dorsal rim of a posteriorly facing zygapophysial facet is high and roughly triangular in shape. Above it is a slightly visible. sloping smooth surface. Dorsal to that, the opening of the The vertebra is broken in two nearly at mid-length, thus neural canal is visible, although somewhat obscured by ma- showing the phosphate-filled inner cavity. At this level, the trix. Depressions on both sides of it correspond to ma- vertebra is nearly circular in cross-section (fig. 2). The trix-filled pneumatic foramina. The whole area is overhung outer bony wall is extremely thin, hardly reaching 1 mm at by the roof-like dorsal sides of the confluent centrum and its thickest. The vertebra thus appears as a hollow, very neural spine. On both sides, the low prezygapophyses are thin-walled bony tube, 17 mm in diameter. No bony broken. trabeculae are clearly visible inside the vertebra (fig. 2, tf), The ventral face of the centrum shows a weak but a bony tube with paper-thin walls is present in the dor- hypapophysis, followed posteriorly over a short distance by sal half of the internal space of the vertebra, just below the a very low and blunt median ridge. Laterally, on both sides, region corresponding to the neural arch. It is about 2.5 mm in diameter and certainly housed the spinal cord. This struc- ture corresponds to what was described by Martill et al. [1998] as the tuba vertebralis in Arambourgiania philadelphiae, from the Late Cretaceous (Maastrichtian) of Jordan. How this tube was attached to the external wall of the vertebra from Grandpré is unclear.

COMPARISONS AND IDENTIFICATION

The vertebra from Grandpré is markedly different from the vertebra from the Sables verts of Louppy (Meuse) reported by Barrois [1875] and described and illustrated by Sauvage [1882]. That vertebra, kept at the Natural History Museum of Lille, was identified by Sauvage [1882] as Pterodactylus sedgwicki, and referred to Ornithocheirus by Buffetaut et al. [1989]. Its centrum is much shorter relative to its width than that of the vertebra from Grandpré, and its neural arch is clearly distinct from the dorsoventrally flattened, rather than cylindrical, centrum. The morphological differences between these two cervical vertebrae from the Sables verts clearly cannot be ascribed to different positions in the verte- bral column, and there is no doubt that more than one group of pterosaurs is present in the Albian of northeastern France. Elongate cervical vertebrae have been described in sev- eral groups of pterosaurs [Howse, 1986], but apparently azhdarchid vertebrae differ from those of other groups in several characters, which are observable in the specimen from Grandpré. In particular, the marked regression of the FIG. 1. – Cervical vertebra of an azhdarchid pterosaur from the Albian Sa- bles verts of Grandpré (Ardennes, northeastern France). Palaeontological neural spine, which forms only a low roof-like ridge, and collection of University Paris 6, Toucas collection, UPMC-080. A: ventral especially the advanced confluence between the centrum view. B: dorsal view. C: left lateral view. D: cranial view. Scale bar: 10 and the neural arch, seem to characterise the cervical verte- mm. e: epipophysis; h: hypapophysis; ns: neural spine; pf: pneumatic fora- men; pn: phosphate nodule. brae of azhdarchids. Another group of Azhdarchoidea, the FIG.1.–Vertèbre cervicale d’un ptérosaure azhdarchidé des Sables verts Tapejaridae, apparently shows fairly similar cervical verte- albiens de Grandpré (Ardennes, Nord-Est de la France). Collection pa- brae, which, however, do not show the remarkable elonga- léontologique de l’Université Paris 6, collection Toucas, UPMC-080. A : tion seen in azhdarchids. A further azhdarchid character vue ventrale. B : vue dorsale. C : vue latérale gauche. D : vue craniale. Barré d’échelle : 10 mm. e : epipophyse; h : hypapophyse; ns : épine neu- mentioned by Watabe et al. [2009] is the “double peak” rale; pf : foramen pneumatique; pn : nodule phosphaté. neural spine, more elevated at its anterior and posterior

Bull. Soc. géol. Fr., 2012, no 6 AN EARLY AZHDARCHID PTEROSAUR (PARIS BASIN) 527 ends than at its mid-point, a condition not seen in other comparisons have been made between such vertebrae from pterosaurs with elongate cervical vertebrae, in which the the Cambridge Greensand, kept in the Sedgwick Museum height of the neural spine is almost constant all along its (Cambridge, UK), and the vertebra from Grandpré. There length. This general morphology is seen, for instance, in appears to be several types of elongate cervical vertebrae the vertebrae of Azhdarcho lancicollis [Nessov, 1984], from the Cambridge Greensand. Some differ from the spec- Quetzalcoatlus [Howse, 1986], Arambourgiania philadel- imen from Grandpré in being less elongate and having the phiae [Martill et al., 1998], the azharchid (probably neural arch more clearly distinct from the centrum, owing Bakonydraco) from Iharkút in Hungary [Äsi et al., 2005], to the presence of a pair of longitudinal ridges, running and the unnamed azhdarchids from Laño in Spain from the prezygapophysis to the postzygapophysis, which [Buffetaut, 1999], from Cruzy in France [Buffetaut, 2001], are not present in the specimen from Grandpré. The ventral from the Dinosaur Park Formation of Alberta [Godfrey and surface of the centrum tends to be flat rather than trans- Currie, 2005] and from Late Cretaceous localities in Mon- versely convex as in the French specimen. A further differ- golia [Watabe et al., 2009]. The uncrushed vertebra from ence is the presence of a pneumatic foramen on the lateral Grandpré shows this morphology quite clearly and closely face of the centrum, which does not seem to be present on resembles well preserved Late Cretaceous azhdarchid verte- the French specimen (and does not occur in azhdarchids). brae, notably specimen TMP 92.83.7 from Alberta (Tyrrell Other vertebrae from the Cambridge Greensand resemble Museum of Palaeontology, Drumheller) figured by Godfrey more closely the vertebra from Grandpré. They show a sim- and Currie [2005, Fig. 16.1], with which it agrees in nearly ilar arrangement of pneumatic foramina around the opening every respect except size, as confirmed by direct compari- of the neural canal, and in some broken specimens a tuba son. On the basis of these similarities, the specimen from vertebralis is visible. Because a complete, well-preserved Grandpré is referred to the family Azhdarchidae. cervical series has not yet been described in detail in Furthermore, the internal structure of the vertebra from azhdarchids, it is difficult to decide whether morphological Grandpré, made visible by the break at mid-length, is also differences among the elongate cervical vertebrae from the in agreement with the condition in azhdarchids, as it clearly Cambridge Greensand reflect different positions in the shows, “ hanging “ within the hollow centrum, the bony tube, or tuba vertebralis, which enclosed the spinal cord, a very peculiar feature first reported in Arambourgiania philadelphiae by Martill et al. [1998] and also visible in the azhdarchid vertebra from Cruzy [Buffetaut, 2001] and in at least one specimen from Alberta [TMP 89.36.254, Godfrey and Currie, 2005]. However, the presence of a tuba vertebralis is not characteristic of azhdarchids, as it also oc- curs in other pterosaurs, notably dsungaripterids [Buffetaut and Kuang, 2010].

A NOTE ON CAMBRIDGE GREENSAND SPECIMENS

Elongate pterosaur cervical vertebrae have been reported from the Cambridge Greensand of England, which is only slightly younger than the Sables verts of the Paris basin. The vertebrate fossils of the Cambridge Greensand are con- sidered to originate from late Albian sediments, reworked into the basal Cenomanian [see review in Unwin, 2001]. Owen [1859a, b] and Seeley [1870, pl. 10] figured elongate pterosaur vertebrae, which they misidentified as caudals, whereas they clearly are cervical vertebrae. According to Unwin [2001], these vertebrae can be referred to the family Lonchodectidae, also represented in the Cambridge Greensand by jaw fragments. However, it cannot be demon- strated that the vertebrae and the jaw elements belong to- gether, all the more so that the vertebrae of lonchodectids are very poorly known. Lonchodectes itself was erected by FIG. 2. – Cervical vertebra of an azhdarchid pterosaur from the Albian Sa- Hooley [1914] on the basis of material from the Turonian bles verts of Grandpré (Ardennes, northeastern France). Palaeontological Chalk of Kent, which does not include vertebrae. Very few collection of University Paris 6, Toucas collection, UPMC-080. A, B: phos- articulated specimens of lonchodectids have been de- phate-filled cross sections at the level of the break (A: caudal; B: cranial), showing the tuba vertebralis (tv), a very thin-walled bony tube that housed scribed. In the type skeleton of the putative lonchodectid the spinal cord. Scale bar: 10 mm. Yixianopterus jingangshanensis, from the Early Cretaceous FIG.2.–Vertèbre cervicale d’un ptérosaure azhdarchidé des Sables verts Yixian Formation of northeastern China, the cervical verte- albiens de Grandpré (Ardennes, Nord-Est de la France). Collection paléon- brae are not preserved [Lü et al., 2006]. The reasons for re- tologique de l’Université Paris 6, collection Toucas, UPMC-080. A, B : sections emplies de phosphate au niveau de la cassure (A : caudale ; B : ferring the elongate vertebrae from the Cambridge craniale), montrant le tuba vertebralis (tv), un tube osseux aux parois très Greensand to the Lonchodectidae are thus unclear. Direct minces qui contenait la moelle épinière. Barre d’échelle : 10 mm.

Bull. Soc. géol. Fr., 2012, no 6 528 BUFFETAUT E. vertebral column or the occurrence of several taxa. In view Albian. Some specimens from the late Albian Cambridge of the similarities between some of the Cambridge Greensand are probably referable to azhdarchids as well. Greensand vertebrae and that from Grandpré, which itself is The identification of an azhdarchid vertebra, which is nearly identical with Late Cretaceous azhdarchid vertebrae, quite different from the ornithocheirid-like pterosaur verte- it seems that azhdarchids may be present in the pterosaur bra previously reported from the Sables verts [Barrois, assemblage from the Cambridge Greensand. A detailed 1875; Sauvage, 1882], indicates that the pterosaur assem- redescription of the elongated vertebrae from that formation blage from this formation is more diverse than previously is necessary in order to confirm this, and is beyond the realised. The slightly younger Cambridge Greensand, scope of this paper. which shows a high diversity of pterosaurs [Unwin, 2001], suggests that the real diversity of these animals in the Sa- bles verts is probably higher than what is indicated by the very few available specimens. As collecting additional ma- CONCLUSION terial from the Sables verts has now become difficult be- cause of the lack of outcrops, a search in old collections The elongate pterosaur vertebra from the Albian Sables may be the best way to obtain a better knowledge of their verts of Grandpré shows a number of distinctive characters pterosaur assemblage. which allow assignment to the family Azhdarchidae. Al- though the existence of azhdarchids before the Late Creta- Acknowledgements. – Thanks to Isabelle Rouget (Université Paris 6) for ceous had been postulated for phylogenetic reasons the loan of the specimen and to Attila Ôsi (Budapest), David Norman and Mathew Riley (Cambridge) and Don Brinkman and Brandon Stilisky [Unwin, 2006], Early Cretaceous records were ambiguous. (Drumheller) for access to pterosaur material in their care. Useful com- The specimen from Grandpré thus constitutes tangible evi- ments were provided by Lorna Steel (London) and Eberhard Frey (Karl- dence of their occurrence at least as far back as the early sruhe).

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