A new azhdarchoid pterosaur from the Lower Cretaceous of China and its implications for pterosaur phylogeny and evolution
- 420 Downloads
Toothless pterosaurs played a key role in broadening the taxonomic, morphological and ecological diversity of Cretaceous pterosaurs. Here we report a complete, articulated skeleton of a 1.4-m-wingspan pterosaur from the Lower Cretaceous Jiufotang Formation of Liaoning Province, China which is identified as a new genus and species, Shenzhoupterus chaoyangensis gen. et sp. nov. The new taxon is edentulous, with a relatively large skull and a remarkably large, tall nasoantorbital fenestra that extends well above the main part of the braincase. Phylogenetic analysis shows that Shenzhoupterus gen. nov. belongs in a distinct clade of azhdarchoid pterosaurs, formally recognised here as a new family, Chaoyangopteridae, that also includes Chaoyangopterus, Jidapterus and Eoazhdarcho from the Jiufotang Formation and Eopteranodon from the Yixian Formation. These new data clarify recent confusion surrounding the systematics of these Lower Cretaceous taxa and provide new insights into the evolutionary history of pterosaurs.
KeywordsAzhdarchoidea Shenzhoupterus Phylogeny Pterosaur Lower Cretaceous China
The pterosaur fossil record is widely perceived as relatively poor compared to that of other vertebrate groups (e.g. Carroll 1987), but recent years have seen a dramatic improvement in its quality thanks in part to a series of important discoveries in Asia and South America (summarised in Unwin 2005). This, coupled with a series of comprehensive phylogenetic analyses (Kellner 2003, 2004; Unwin 2003; Lü and Ji 2006), has led to some dramatic improvements in our understanding of the evolutionary history of the group (cf. Wellnhofer 1978; Unwin 2003, 2005).
Recent accounts (e.g. Unwin 2005; Wang et al. 2005; Unwin and Martill 2007) suggest that pterosaurs reached their highest levels of taxonomic and morphological diversity during the Early Cretaceous, with toothed forms (anurognathids, ctenochasmatids, ornithocheiroids, dsungaripterids) being particularly diverse and widespread during this interval. Until recently, edentulous pterosaurs, which almost completely dominate the Upper Cretaceous record, were practically unknown from the Lower Cretaceous, but have now been reported in some numbers from the Crato and Santana formations of Brazil (e.g. Kellner and Tomida 2000; Unwin and Martill 2007) and the Jehol Group of China (e.g. Lü et al. 2006a; Wang and Zhou 2006). Initially, the two principal edentulous clades, Tapejaridae and Tupuxuaridae, seemed to be confined to the Lower Cretaceous, although fragmentary finds from Africa (Wellnhofer and Buffetaut 1998) and North America (Kellner 2004; Martill and Naish 2006) suggest that, although rare, they persisted into the Upper Cretaceous.
Recently, several edentulous forms from the Lower Cretaceous of China have been assigned to clades previously only certainly known from the Upper Cretaceous. Eoazhdarcho Lü and Ji 2005, was assigned to the Azhdarchidae and Eopteranodon Lü and Zhang 2005, to the Pteranodontidae, while Chaoyangopterus Wang and Zhou 2003, was initially identified as a nyctosaurid, but is now thought by some to be a pteranodontid (Lü 2003; Wang et al. 2005; Wang and Zhou 2006), as is Jidapterus Dong et al. 2003. However, these assignments have been challenged (Lü and Ji 2006, Lü et al. 2006a, Martill and Naish 2006), as has the generic distinctness of these taxa (Wang and Zhou 2006) and there is much uncertainty regarding the identity of these pterosaurs, largely because of the incompleteness of the remains, especially the skulls, upon which they are based. Concomitantly, our understanding of the relationships, diversity and evolutionary history of Lower Cretaceous edentulous pterosaurs has become mired in debate and confusion.
Here, we report on the complete skeleton of a new edentulous pterosaur from the Lower Cretaceous Jiufotang Formation of north-eastern China, a sequence that has yielded many pterosaurs in recent years (Wang et al. 2005, Lü et al. 2006a, Wang and Zhou 2006). The relatively complete skull of this new genus helped identify enigmatic and unusual morphological features present in other Lower Cretaceous edentulous forms such as Chaoyangopterus, Jidapterus and Eopteranodon which, in turn, facilitated a more comprehensive phylogenetic analysis of pterodactyloid pterosaurs than previously attempted. This resolved the disputed systematic relationships of several edentulous taxa, identified a new and highly distinct family of pterosaurs and threw some much needed light on the evolutionary history of the clade during this interval.
The family name is derived from Chaoyangopterus Wang and Zhou 2003, the first named genus of this family.
Chaoyangopterus, Shenzhoupterus, their most recent common ancestor and all taxa more closely related to this clade than to Tapejara, Tupuxuara or Quetzalcoatlus.
Members of Chaoyangopteridae are distinguished from all other pterosaurs by an unusually slender premaxillary bar bounding the nasoantorbital opening and extension of the nasoantorbital opening posterior to the jaw joint.
Chaoyangopterus, Jidapterus, Eoazhdarcho, Eopteranodon, Shenzhoupterus gen. nov. and possibly an undescribed pterosaur from the Crato Formation of Brazil (Witton 2008).
Shenzhoupterus gen. nov.
Shenzhoupterus chaoyangensis sp. nov.
Shenzhoupterus: Shenzhou, an old name for China and ‘pterus’ (Gk.) wing; chaoyangensis refers to the Chinese administrative unit Chaoyang, where the holotype was found.
Type locality and horizon
Chaoyang, Liaoning Province, north-eastern China. Jiufotang Formation, Lower Cretaceous, early Aptian (approximately 120 mya; see He et al. 2004).
Chaoyangopterid pterosaur with slightly concave upper jaw margin and convex lower jaw margin. This is reversed in Chaoyangopterus (Wang and Zhou 2003), while the jaw margins are straight in Jidapterus (Dong et al. 2003), Eopteranodon (Lü and Zhang 2005) and Eoazhdarcho (Lü and Ji 2005). Rostral index (RI; length of prenarial rostrum compared to maximum depth: Martill and Naish 2006) of Shenzhoupterus is 3.7, compared to 5.7 in Chaoyangopterus and 5.0 in Jidapterus. Limb bone proportions also distinguish Shenzhoupterus from other chaoyangopterids (see “Electronic supplementary material-S1a, for comparative morphometric data of chaoyangopterids”).
The skeleton is almost complete and largely articulated. The pectoral girdles are displaced and the limbs no longer lie in a natural position (Fig. 1A,B). The skull lies on its right side and is heavily compressed especially the cranium, some elements of which are indistinct and not well preserved, although the orbit and nasoantorbital opening can be identified. Bone preservation is variable and some regions such as the spinal column are poorly preserved and indistinct.
The skull is relatively large (Fig. 1C), its long dimension almost equivalent to the length of the entire vertebral column, and dominated by the enormous development of the nasoantorbital fenestra and the bones that surround it. The dorsal margin of this opening is bounded by thin, spar-like dorsal rami of the premaxillae that curve upward and backward, extending over the frontals, but do not unite with them as is typical of azhdarchoids (Kellner 2004). The posterior margin of the nasoantorbital opening extends behind the jaw joint. A short, flange-like frontoparietal crest, with an incised posterior edge and a posterodorsally directed triangular apex arises from the rear margin of the skull and is quite unlike that seen in any other pterosaur. The orbit matches that of azhdarchoids: relatively small, pear-shaped and situated well below the dorsal margin of the nasoantorbital fenestra (Unwin 2003). The upper and lower jaws are toothless and taper to sharp points anteriorly. The prenarial rostrum is relatively short and deep, with an RI of 3.7, typical of derived azhdarchoids (Martill and Naish 2006). The position of the jaw joint is under the anterior third of the orbit. The occlusal margin of the rostrum has a slightly concave profile, mirroring the convex dorsal profile of the mandibles. The mandibular symphysis reaches almost 50% of total jaw length and deepens posteriorly achieving a depth almost twice that of the mandibular rami: a common, but not universal feature of azhdarchoids.
The cervical series is long, exceeding the combined length of the dorsals + sacrals. The mid-series cervicals seemingly lack ribs and are elongate, with a depressed neural arch and a low neural spine. Early dorsals and their associated ribs do not appear to be fused hence there is no notarium. The scapula is longer and more slender than the coracoid, which is short, relatively stout and bears a large brachial flange. The head of the humerus is flexed posteriorly and the deltopectoral crest is markedly elongate, with a rounded distal termination. The proximal ends of metacarpals i–iii are reduced and do not appear to contact the carpus.
The length of the wing-metacarpal exceeds that of all other forelimb elements except for wing-phalanx one. Manus digits i–iii exhibit the standard phalangeal formula, 2,3,4 and have stout, well-developed, recurved unguals. As in other azhdarchoids, the wing-finger is relatively short, only 53% total forelimb length, wing-phalanx one forms more than 40% of total wing-finger length, and each phalanx is markedly shorter than the preceding phalanx.
The hind limb is relatively long, robust, and well over 40% the length of the forelimb. The femur is curved anteriorly. The tibia is straight and, at 1.36 times the length of the femur, relatively short compared to other pterodactyloids. Metatarsals i–iv are closely appressed, while the fifth metatarsal is short and spur-like, but well ossified. Metatarsal iii is 28% the length of the tibia. The pes appears to exhibit the standard pterodactyloid phalangeal formula: 2,3,4,5,0, and the pedal claws are relatively small, slender and only slightly recurved.
This individual has a skull length of 0.225 m, an estimated wingspan of 1.4 m and a total hindlimb length of 0.32 m (see “Electronic supplementary material-S1b, for measurements of Shenzhoupterus chaoyangensis”). The extensor tendon process is not fused to the proximal end of the wing-phalanx one, hinting at immaturity (Frey and Martill 1998), but several composite elements, including syncarpals, appear to be coossified, suggesting that this individual was nearing osteological maturity and the end of the main growth spurt (Bennett 1993).
Thin bone walls and unique features such as a pteroid and wing-finger demonstrate that Shenzhoupterus is a pterosaur. Moreover, it undoubtedly belongs within Pterodactyloidea as the absence of a fifth pedal digit and presence of a nasoantorbital opening, elongate wing-metacarpal and several other features of the skull and neck show.
An important outcome of this study was the discovery of strong support for the inclusion in the Azhdarchoidea of several other Lower Cretaceous edentulous pterodactyloids, namely Chaoyangopterus, Jidapterus, Eopteranodon and Eoazhdarcho, a relationship that has also been postulated by Lü and Ji (2006), Lü et al. (2006a) and Martill and Naish (2006). These genera exhibit several azharchoid apomorphies including a relatively large nasoantorbital opening, a relatively short wing-finger, an elongate wing-phalanx one and a relatively long hind limb. Most recently, all four genera had been assigned to the Pteranodontidae by Wang and Zhou (2006), but the only feature they share in common with this clade is a superficial similarity in the shape of the jaws. Otherwise, they lack a large suite of clear cut apomorphies found in the Pteranodontidae and the more inclusive clade Ornithocheiroidea (Bennett 1989; Kellner 2003; Unwin 2003; Lü and Ji 2006).
Relationships within the Azhdarchoidea are controversial. We found good support for the recognition of four distinct clades: Tapejaridae, characterised by the presence of a ventrally flexed rostrum (Lü et al. 2006b); Tupuxuaridae, consisting solely of Tupuxuara and Thalassodromeus; Azhdarchidae, a non-controversial clade of long-necked Late Cretaceous forms; and a new clade, Chaoyangopteridae, uniting Shenzhoupterus with Chaoyangopterus, Jidapterus, Eopteranodon and Eoazhdarcho (Fig. 2B). This family, which may also include an as yet undescribed large edentulous pterosaur from the Crato Formation of Brazil (Witton 2008), is distinguished by the presence of an unusually slender premaxillary bar bounding the nasoantorbital opening and extension of the nasoantorbital opening posterior to the jaw joint. In the strict consensus tree (Fig. 2B), chaoyangopterids form an unresolved polytomy with other azhdarchoid clades. We note, however, that, apart from the absence of a premaxillary crest, the chaoyangopterid skull is similar to that of tupuxuarids (Kellner and Campos 2003; Kellner 2004). Chaoyangopterids also have some limb bone proportions (relatively elongate wing-phalanx one and low forelimb/hindlimb ratio) that are restricted to tupuxuarids and azhdarchids, raising the possibility that chaoyangopterids belong within the Neoazhdarchia (Fig. 2C).
This study was supported by grants from the National Key Basic Research and Development Program (Grant 2006CB701405) and the China Geological Survey (Grant 200413000024). David Unwin thanks Jason Dunlop, the Museum für Naturkunde, Berlin and the University of Leicester for logistical support. We are very grateful to David Martill, Darren Naish, Mark Witton and three referees who provided many helpful comments that greatly improved the quality of this manuscript. We also thank Brian Andres, Chris Bennett, David Martill, Darren Naish, Mark Witton and Alex Kellner for useful discussions regarding pterosaur phylogeny and taxonomy and Mark Witton for generously providing access to his unpublished work.
- Bennett SC (1989) A pteranodontid pterosaur from the Early Cretaceous of Peru, with comments on the relationships of Cretaceous pterosaurs. J Paleontol 63:669–677Google Scholar
- Bennett SC (1993) The ontogeny of Pteranodon and other pterosaurs. Paleobiology 19:92–106Google Scholar
- Carroll RL (1987) Vertebrate paleontology and evolution. W. H. Freeman, New YorkGoogle Scholar
- Dong ZM, Sun YW, Wu SY (2003) On a new pterosaur from the Lower Cretaceous of Chaoyang Basin, Western Liaoning, China. Global Geol 22:1–7Google Scholar
- Frey E, Martill DM (1998) Late ontogenetic fusion of the processus tendinis extensoris in Cretaceous pterosaurs from Brazil. N Jb Geol Paläontol Mh 1998:587–594Google Scholar
- Gradstein FM, Ogg JG, Smith AG (2005) A geological timescale 2004. Cambridge University Press, CambridgeGoogle Scholar
- Kaup JJ (1834) Versuch einer Eintheilung der Säugethiere in 6 Stämme und der Amphibien in 6 Ordnungen. Isis, Jena:1–315Google Scholar
- Kellner AWA (2003) Pterosaur phylogeny and comments on the evolutionary history of the group. In: Buffetaut E, Mazin J-M (eds) Evolution and palaeobiology of pterosaurs. Geological Society, London, pp 105–137 Special Publications 217Google Scholar
- Kellner AWA (2004) New information on the Tapejaridae (Pterosauria, Pterodactyloidea) and discussion of the relationships of this clade. Ameghiniana 41:521–534Google Scholar
- Kellner AWA, Tomida Y (2000) Description of a new species of Anhangueridae (Pterodactyloidea) with comments on the pterosaur fauna from the Santana Formation (Aptian-Albian), northeastern Brazil. National Science Museum Monographs Tokyo 17:1–135Google Scholar
- Lü JC (2003) A new pterosaur: Beipiaopterus chenianus, gen. et sp. nov. (Reptilia: Pterosauria) from Western Liaoning Province of China. Mem Fukui Prefectural Dinosaur Museum 2:153–160Google Scholar
- Lü JC, Ji Q (2005) New azhdarchid pterosaur from the Early Cretaceous of western Liaoning. Acta Geol Sin 79:301–307Google Scholar
- Lü JC, Ji Q (2006) Preliminary results of a phylogenetic analysis of the pterosaurs from western Liaoning and surrounding areas. J Pal Soc Korea 22:239–261Google Scholar
- Lü JC, Ji S, Yuan C, Ji Q (2006a) Pterosaurs from China. Geological Publishing House, BeijingGoogle Scholar
- Lü JC, Zhang BK (2005) New pterodactyloid pterosaur from the Yixian Formation of Western Liaoning. Geol Rev 51:458–462Google Scholar
- Nesov LA (1984) Pterozavryi i ptitsyi pozdnyevo myela sryednyei Azii. Paleonto Z 1984:47–57Google Scholar
- Plieninger F (1901) Beiträge zur Kenntnis der Flugsaurier. Paläontographica 48:65–90Google Scholar
- Swofford DL (2000) PAUP*. Phylogenetic Analysis Using Parsimony (* and other methods). Version 4, Beta 10. Sinauer, Sunderland, MassachusettsGoogle Scholar
- Unwin DM (1995) Preliminary results of a phylogenetic analysis of the Pterosauria (Diapsida: Archosauria). In: Sun AL, Wang YQ (eds) Sixth Symposium on Mesozoic Terrestrial Ecosystems and Biota, Short Papers. China Ocean, Beijing, pp 69–72Google Scholar
- Unwin DM (2003) On the phylogeny and evolutionary history of pterosaurs: In: Buffetaut E, Mazin JM (eds), Evolution and Palaeobiology of Pterosaurs, Geological Society, London, 217:139–190Google Scholar
- Unwin DM (2005) The Pterosaurs from Deep Time. Pi, New YorkGoogle Scholar
- Unwin DM, Martill DM (2007) Pterosaurs from the Lower Cretaceous Crato Formation of the Chapada do Araripe, North East Brazil. In: Martill DM (ed) The fossils of the Crato Formation: window on an ancient world. Cambridge University Press, NY, USA, pp. 475–524Google Scholar
- Wang XL, Zhou ZZ (2003) Two new pterodactyloid pterosaurs from the Early Cretaceous Jiufotang Formation of western Liaoning, China. Vertebrata PalAsiatica 41:34–41Google Scholar
- Wellnhofer P (1978) Pterosauria. In: Wellnhofer P (ed) Handbuch der Paläoherpetologie, Teil 19. Gustav Fischer, Stuttgart, pp 1–82Google Scholar
- Wellnhofer P, Buffetaut E (1998) Pterosaur remains from the Cretaceous of Morocco. Pal Zeitschrift 73:133–42Google Scholar
- Witton M (2008) A new azhdarchoid pterosaur from the Crato Formation (Early Cretaceous, Aptian?) of Brazil. Palaeontology (in press)Google Scholar