A New Ctenochasmatid Pterosaur from the Lower Cretaceous, Western Liaoning, China

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Anais da Academia Brasileira de Ciências (2011) 83(4): 1243-1249 (Annals of the Brazilian Academy of Sciences) Printed version ISSN 0001-3765 / Online version ISSN 1678-2690 www.scielo.br/aabc

A new ctenochasmatid pterosaur from the Lower Cretaceous, western Liaoning, China

, SHUNXING JIANG1 2 and XIAOLIN WANG1

1Key Laboratory of Evolutionary Systematics of Vertebrates, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, PO Box 643, Beijing, 100044, China 2Graduate University of the Chinese Academy of Sciences, Beijing, 100049, China

Manuscript received on August 8, 2011; accepted for publication on September 28, 2011

ABSTRACT A nearly complete skull of a new ctenochasmatid pterosaur, Pterofiltus qiui gen. et sp. nov., from the Lower Cretaceous deposits of Liaoning, China, is described here. The specimen (IVPP V12339), was collected from the shale of the lower Yixian Formation (125 Ma) at the Zhangjiagou locality. It has the following combination of characters: about 112 teeth in total (including the upper and lower jaws); the dentition occupies more than 50% of the skull length; the anterior teeth vary in size; the mandibular symphysis is longer than half of the whole mandible length; in ventral view, an apparent symphyseal trough in the median part of the symphysis. Key words: Lower Cretaceous, Yixian Formation, Pterofiltus qiui, Ctenochasmatidae, Liaoning, China.

INTRODUCTION Gegepterus changi Wang et al. 2007)] and Elanodac- tylus prolatus (Andres and Ji 2008). Most of them come The pterosaur record from China has yielded several from the Jianshangou Bed of the lower Yixian Forma- important new taxa due to the collecting activities done tion, except Cathayopterus from the Dawangzhangzi Bed particularly in western Liaoning (e.g., Wang et al. 2009, of the middle Yixian Formation. 2010). The most important deposits are known as Recently, another interesting specimen of a cteno- the Jehol Biota that comprises numerous articulated chasmatid pterosaur was discovered from the Zhang- fossils, from plants and insects to all kinds of verte- jiagou locality near Beipiao City, Liaoning Province brates, making it one of the most amazing terrestrial (Fig. 1). In the same locality, there are many other ver- Cretaceous ecosystems in the world (Chang et al. 2003, tebrate fossils such as Dendrorhynchoides curvidentatus Zhou et al. 2003, Wang et al. 2008, Zhou and Wang (Ji and Ji 1998, Wang and Lü 2001), Protarchaeopteryx 2010). robusta (Ji et al. 1998), Caudipteryx dongi (Zhou and Since the first description of a pterosaur in 1997 Wang 2000), Caudipteryx zoui (Ji et al. 1998), and an (Ji and Ji 1997), many more pterosaur fossils have immature iguanodontian. The specimen V 12339 con- been discovered in the Jehol Biota. Among them, four sists of most part of skull and mandibles and was col- ctenochasmatids play an important role in the pterosaur lected from the Jianshangou Bed of the lower Yixian research: Beipiaopterus chenianus (Lü 2003), Cathay- Formation. It represents a new genus and species, Ptero- opterus grabaui (Wang and Zhou 2006), Gegepterus filtrus qiui, which is described here. Additionally, we changae [nom. correct. Wang and Dong 2008 (pro discuss the relationship between the new taxon and other ctenochasmatid pterosaurs. Correspondence to: Xiaolin Wang E-mail: [email protected]

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Fig. 1 – Sketch of the map of China with the indication of the fossil locality.

SYSTEMATIC PALEONTOLOGY Diagnosis – A Ctenochasmatid pterosaur with the fol- Pterosauria Kaup, 1834 lowing combination of characters that distinguish it from Pterodactyloidea Plieninger, 1901 the other members of this clade (autapomorphies are Archaeopterodactyloidea Kellner, 2003 marked with an asterisk): about 112 teeth in total (in- Ctenochasmatidae Nopcsa, 1928 cluding the upper and lower jaws); the dentition occupies more than 50% of the skull length; the anterior teeth vary Pterofiltrus gen. nov. in size; the mandibular symphysis is longer than half of the whole mandible length*; in ventral view, an apparent Etymology – ptero-, from pteron (Greek), means wing; symphyseal trough in the median part of the symphysis*. filtrus, from filtrum (Medieval Latin), means filter.

Type species – Pterofiltrus qiui gen. et sp. nov. DESCRIPTION Diagnosis – As for the species. IVPP V12339 preserves nearly all elements of the skull, but they are not articulated (Fig. 2A, B). The es- Pterofiltrus qiui sp. nov. timated length of the skull is 208 mm. The rostrum and Etymology – In honor of Prof. Qiu Zhanxiang, who has the posterior part of the skull can be observed in both made great contributions to the Chinese paleontology. right and dorsal sides, respectively. The mandibles are preserved dorsoventrally flattened. Their posterior and Type specimen – IVPP V12339 (Fig. 2), most part of anterior parts are respectively preserved in the dorsal skull and mandible, and first two cervical vertebrae, and ventral sides, as the anterior part was turned over housed in the Institute of Vertebrate Paleontology and (Fig. 2C; showing the relationship of the main elements). Paleoanthropology (IVPP), Chinese Academy of Sci- ences, Beijing, China. PREMAXILLAAND MAXILLA Locality and horizon – Zhangjiagou, Beipiao City, The premaxilla and maxilla are fused, and the suture Liaoning Province, China. Jianshangou Bed, lower between them is unclear (Fig. 2A, B, D). The premaxilla Yixian Formation, Lower Cretaceous, about 125 Ma is very long, and it is estimated to extend to the poster- (Swisher et al. 2001). ior end of the nasoantorbital fenestra. The anterior tip

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Fig. 2 – Pterofiltrus qiui gen. et sp. nov., IVPP V12339; photograph (A); line drawing (B) showing the general position of the elements; their relationship (C), blue, rostrum; green, mandible; red, posterior part of the skull; white, indeterminate; The anterior teeth in the upper jaw, the teeth are numbered based mainly on the presence of the alveoli. The 2nd and 5th teeth are the longest ones (D); photograph (E) and line drawing (F) of the anterior mandibles, the teeth are directed laterally, and the anterior teeth directed anterolaterally, which is an important feature of Ctenochasmatidae. ang, angular; art, articular; at, atlas; ax, axis; d, dentary; f, frontal; hy, hyoid; j, jugal; m, maxilla; naof, nasoantorbital fenestra; p, parietal; pm, premaxilla; por, postorbital; q, quadrate; qj, quadratojugal; sq, squamosal; sym.t, symphyseal trough; t, tooth; utf, upper temporal fenestra; l, left; r, right.

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1246 SHUNXING JIANG and XIAOLIN WANG of the premaxilla is not expanded like in some other rate has an expanded end, which would connect with ctenochasmatids, such as Plataleorhynchus and Gna- the articular. The other end is laid by the premaxilla. thosaurus (Howse and Milner 1995). There is no crest on the maxilla or premaxilla. The maxilla is separated FRONTAL, PARIETAL AND SQUAMOSAL from the jugal, and exceeds the middle of the nasoant- The posterior portions of both frontals are preserved. orbital fenestra, forming the ventral margin of the naso- They are fused together and no suture can be observed. antorbital fenestra. They taper posteriorly and wedge into the middle of the There are 29 teeth on each side. The number of the both parietals. There is no crest on the frontals. The teeth is mainly based on the alveoli on the specimen. right frontal is broken, and the upper temporal fenestra The diameter of the anterior alveoli nearly equals the cannot be recognized. The left frontal is well preserved, distance between two teeth. The density of them is surrounding the upper temporal fenestra with the pari- 3.4 teeth/cm (15 teeth/4.4 cm). The teeth are inclined etal, squamosal, and postorbital. Because of the preser- anteriorly, and the inclination angle becomes smaller vation, the posterior part of the eye socket is overlaid, from the anterior portion to the posterior portion. The and part of the upper temporal fenestra is visible. anterior teeth have a 135◦ angle to the ventral margin Both parietals are fused together, and have a of the premaxilla, but the last few ones are nearly ver- groove in the middle. The parietal is very smooth, and tical. The anterior teeth vary in size. The 2nd and 5th it is easy to distinguish it from the other bones. There is teeth are the longest ones (Fig. 2D). The alveoli be- also no crest on the parietals. The squamosal is not well come shallower posteriorly. The teeth also become preserved. Only the outline can be recognized and the smaller and vary in shape. The anterior and posterior details are lost. teeth are slender and triangular, respectively. The whole tooth row is about 116 mm long, 55.8% of the skull MANDIBLE length, having a 2.5 teeth/cm density on average. Both mandibles are narrow, with about 174 mm length. Both retroarticular processes are developed. The out- JUGAL, QUADRATOJUGAL AND QUADRATE lines of the angular and the surangular cannot be recog- Both jugals are preserved, but not in their original ana- nized. The dentary is the largest bone in the lower jaw. tomic position. The right jugal is complete, and it is a The tip of the dentary is not expanded. The anterior triradiate bone. The anterior process is thin, smooth and portions fuse together, forming a symphysis, which very long, nearly 70% of the jugal length. The right bears an apparent symphyseal trough in the ventral side dorsal process, which is in contact with the lacrimal, (Fig. 2E, F). The symphyseal trough is nearly 5 mm is preserved in a 60◦ angle with the anterior process. depth and fills 26% of the mandible length. The surface Only some broken process remains on the left jugal. of the symphysis is smooth. The symphysis occupies On the ventral side of the left jugal, the posterior pro- 58% of the mandible length. cess is fused with the quadratojugal, forming the an- The mandibles also have slender teeth. Because terior margin of the lower temporal fenestra, which is some teeth are lost and the alveoli are not exposed, the surrounded by the jugal, quadrate, quadratojugal, squa- number of teeth is not certain. Considering the length mosal, and postorbital. of the tooth row, it should nearly subequal that of the The quadratojugal is a V-shaped bone. One end upper jaw, so it may have 27 teeth per side. The mandible fuses with the jugal without any perceptible suture, and is preserved dorsoventrally flattened; the teeth are di- the other one would fuses with the quadrate. However, rected laterally, and only the anterior teeth are directed a small glenoid cavity is found at the bottom of each the anterolaterally (Fig. 2E, F). quadratojugal where it would be in contact with the YOID quadrate. In the specimen, some fragmentary bones are H located between the upper and lower jaws. Two stick-like Although the anterior part of the hyoid is absent, both bones may both be quadrates. The putative right quad- posterior rami are preserved. They are separated.

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VERTEBRAE lar and reach the anterior margin of the nasoantorbital fenestra. The posterior teeth of Gegepterus are still slen- Only the first two cervical vertebrae, atlas and axis are der, and the last tooth has a distance to the anterior margin preserved. They are fused together and their outline is of the nasoantorbital fenestra. not very clear. Huanhepterus has a skull (Dong 1982). Most elements of the postcranial skeleton are absent, but left COMPARISON AND DISCUSSION some three dimensional impression in the sandstone. The Ctenochasmatidae is part of the clade known Although Huanhepterus is not complete, it is obviously as Archaeopterodactyloidea (Kellner 2003). Pterofiltrus larger than Pterofiltus. Huanhepterus has an apparent qiui is assigned to the Ctenochasmatidae based on the crest beginning at the anterior portion of the premax- extremely elongated rostrum, a large number of slen- illa, which is absent in Pterofiltus. Huanhepterus has der teeth, and the upper anterior teeth inclined ventro- about 25 teeth per jaw side, slightly fewer than Ptero- anteriorly. filtus (27-29 teeth per jaw side). The density of teeth in There are five genera and species of ctenochas- Huanhepterus (1.6 teeth/cm) is less than that in Pterofil- matids reported in China (Dong 1982, Lü 2003, Wang tus (2.5 teeth/cm). All teeth in Huanhepterus are similar, and Zhou 2006, Wang et al. 2007, Andres and Ji and they are not as slender as in other ctenochasmatids. 2008). Beipiaopterus and Elanodactylus are known Compared with other ctenochasmatid pterosaurs, only postcranial skeletons, which cannot be compared Pterofiltus is unique. Pterodaustro from the Lagarcito with the holotype of Pterofiltrus, whereas Huanhep- Formation, Lower Createous of Argentina, is very spe- terus, Cathayopterus and Gegepterus have partial or cialized, with nearly a thousand needle-like teeth on nearly complete skulls. the upper jaws (Chiappe et al. 2000), and it is easy to Cathayopterus and Pterofiltus share some import- distinguish it from Pterofiltus. Ctenochasma has three ant features. For example, the amounts of the teeth are species, including C. roemeri, C. elegans and C. taqueti similar, and the ratio of rostrum to skull length is more from the Upper Jurassic Solnhofen Limestone of Ba- than 50% (Wang and Zhou 2006). However, they have varia, Germany, Upper Jurassic Calcaires tachetés of some significant differences. The teeth row of Ptero- eastern France and Lower Cretaceous “Purbeck” Forma- filtus exceeds the anterior margin of the nasoantorbital tion of Deister Hill, Germany. Ctenochasma has more fenestra, while that of Cathayopterus does not reach the than 50 teeth per jaw side (Bennett 2007), and their nasoantorbital fenestra. The teeth shapes are different in density is much greater than in Pterofiltus. Plataleo- both pterosaurs. Cathayopterus lost the last few teeth, rhynchus from the Upper Jurassic or Lower Cretaceous and only the alveoli left. The preserved teeth are slen- Purbeck Limestone of Dorset, England, has only the der, and only vary in size from the anterior to the pos- part of the rostrum preserved, with an estimated skull terior region. In Pterofiltus, the teeth can vary both in length of at least 400 mm, nearly twice of that in size and in shape, from the slender ones in the anterior Pterofiltus (208 mm). Furthermore, Plataleorhynchus portion to the triangular ones in the posterior portion. has an expanded spatulated rostrum (Howse and Milner Gegepterus has more complete and articulated 1995), which differs from Pterofiltrus. Gnathosaurus, skulls than that of Pterofiltus (Wang et al. 2007, Jiang including G. subulatus and G. macrurus from the Soln- and Wang 2011). It has a very low premaxillary crest, hofen Limestone and Purbeck Limestone, respectively, not found in Pterofiltus. Although some authors con- have expanded anterior tips and maxillary crests, which sider the cranial crests in the skull is considered as cannot be found in Pterofiltus. The symphyseal portion sexual dimorphism in some genera (for instance, Lü of the mandible is about 40% and 58% in Gnathosaurus et al. 2011), this difference may not only related to and Pterofiltus, respectively. We observed a symphyseal sexual dimorphism, but also to an interspecific differ- trough on the dorsal side of the mandible in Pterofiltus, ence (Kellner 2010). The teeth of both pterosaurs are while the symphyseal trough is found on the ventral side slender, but the posterior teeth of Pterofiltus are triangu- in Gnathosaurus macrurus (Howse and Milner 1995).

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Boreopterus, from the Yixian Formation, resem- da metade do comprimento da mandíbula; abertura ventral na bles Pterofiltus regarding the very slender teeth of the parte média da sínfise mandibular. rostrum tip (Lü and Ji 2005). The most marked differ- Palavras-chave: Cretáceo Inferior, Formação Yixian, Ptero- ence is the direction of the teeth. In Boreopterus, the filtus qiui, Ctenochasmatidae, Liaoning, China. teeth are inclined anteriorly, while in Pterofiltus, they are inclined not only anteriorly but also ventrally, which REFERENCES is a significant character of the Ctenochasmatidae. ANDRES B AND JI Q. 2008. A new pterosaur from the Liaoning Province of China, the phylogeny of the Ptero- CONCLUSIONS dactyloidea, and convergence in their cervical vertebrae. Based on a series of combination of characters, the Palaeontology 51: 453–469. new genus and species Pterofiltus qiui is established. The BENNETT SC. 2007. A review of the pterosaur Ctenochasma: Jehol Biota comprises many pterosaurs and ctenochas- taxonomy and ontogeny. Neues Jahrb Geol P-A 245(1): matids play a very important role. The amount of clade 23–31. members is not big, but this clade has more taxa than CHANG MM,CHEN PJ,WANG YQ,WANG Y AND MIAO many others. This new member provides further infor- DS. 2003. The Jehol Biota, the Emergence of Feathered Dinosaurs, Beaked Birds and Flowering Plants, Shanghai: mation on the global distribution of the ctenochasmatid, Shanghai Scientific & Technical Publishers, 208 p. in Asia, Europe and America (Rodrigues and Kellner CHIAPPE LM,KELLNER AWA, RIVAROLA D,DAVILA S 2010). AND FOX M. 2000. Cranial morphology of Pterodaustro guinazui (Pterosauria: Pterodactyloidea) from the Lower ACKNOWLEDGMENTS Createous of Argentina. Nat Hist Mus Los Angeles We thank Drs. Alexander W.A. Kellner (Museu Nacio- County, Contrib Sci 483: 1–19. nal/UFRJ, Rio de Janeiro, Brazil), Zhonghe Zhou (In- DONG ZM. 1982. On a new Pterosauria (Huanhepterus quin- stitute of Vertebrate Paleontology and Paleoanthropol- gyangensis gen. et sp. nov.) from Ordos, China. Vert Pal- ogy, Chinese Academy of Sciences, Beijing) and Desui Asit 20(2): 115–121 (in Chinese with English abstract). Miao (Natural History Museum and Biodiversity Re- HOWSE SCB AND MILNER AR. 1995. The pterodactyloids search Center, University of Kansas, Lawrence, USA) from the Purbeck Limestone Formation of Dorset. Bull and two anonymous reviewers for their useful comments Nat Hist Mus, London (Geol) 51(1): 73–88. and English correction on the manuscript. We also thank JI Q,CURRIE PJ,NORELL MA AND JI SA. 1998. Two Yutong Li for preparing the specimen and Jie Zhang feathered dinosaurs from the northeast China. Nature for photographing. This study was supported by the Na- 393: 753–761. tional Science Fund for Distinguished Young Scholars JI SA AND JI Q. 1997. Discovery of a new pterosaur from the (40825005), National Basic Research Program of China Lower Cretaceous of Chaoyang Basin, western Liaoning, (973 Program) (2012CB821903) and National Natural China. Acta Geol Sin 71(1): 1–6 (in Chinese with English abstract). Science Foundation of China (40121202), . JI SA AND JI Q. 1998. A new fossil pterosaur (Rhampho- RESUMO rhynchoidea) from Liaoning. Jiangsu Geol 22(4): 199– 206 (in Chinese with English abstract). Um crânio quase completo de um novo pterossauro ctenochas- JIANG SX AND WANG XL. 2011. Important features of matídeo, Pterofiltus qiui gen. et sp. nov., de depósitos do Cre- Gegepterus changae (Pterosauria: Archaeopterodactyloi- táceo Inferior de Liaoning, China é descrito. O exemplar (IVPP dea, Ctenochasmatidae) from a new specimen. Vert Pal- V12339) foi coletado de um argilito da parte inferior da For- Asit 49(2): 172–184. mação Yixian (125 Ma) na localidade Zhangjiagou. A nova KELLNER AWA. 2003. Pterosaur phylogeny and comments espécie possui a seguinte combinação de caracteres: aproxi- on the evolutionary history of the group. In: BUFFETAUT madamente 112 dentes (incluindo ambas as arcadas); dentição E AND MAZIN JM (Eds), Evolution and Palaeobiology ocupando mais de 50% do comprimento do crânio; dentes an- of Pterosaur, London: Geological Society, Special Publi- teriores de tamanho variado; sínfise mandibular ocupando mais cation, p. 105–137.

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KELLNER AWA. 2010. Comments on the Pteranodontidae WANG XL,KELLNER AWA, JIANG S AND MENG X. 2009. (Pterosauria, Pterodactyloidea) with the description of two An unusual long-tailed pterosaur with elongated neck new species. An Acad Bras Cienc 82(4): 1063–1084. from western Liaoning of China. An Acad Bras Cienc LÜ JC. 2003. A new pterosaur: Beipiaopterus chenianus, 81(4): 793–812. gen. et sp. nov. (Reptilia: Pterosauria) from western Liaon- WANG XL,KELLNER AWA, ZHOU ZH AND CAMPOS DA. ing Province of China. Mem Fukui Pref Dino Mus 2: 2007. A new pterosaur (Ctenochasmatidae, Archaeoptero- 153–160. dactyloidea) from the Lower Cretaceous Yixian Formation LÜ JC AND JI Q. 2005. A new ornithocheirid from the early of China. Cretaceous Res 28(2): 245–260. Cretaceous of Liaoning Province, China. Acta Geol Sin WANG XL AND LÜ JC. 2001. Discovery of a pterodactylid (Engl) 79(2): 157–163. pterosaur from the Yixian Formation of western Liaoning, RODRIGUES T AND KELLNER AWA. 2010. Note on the China. Chin Sci Bull 46(13): 1112–1117. pterosaur material described by Woodward from the Re- WANG XL AND ZHOU ZH. 2006. Pterosaur radiation of côncavo Basin, Lower Cretaceous, Brazil. Rev Bras Pale- Jehol Biota and their paleoenvironment. In: RONG JY ontol 13(2): 159–164. (Eds), Originations, Radiations and Biodiversity Changes- SWISHER IIICC,WANG XL,ZHOU ZH,WANG YQ,JIN Evidences from the Chinese Fossil Record, Beijing: Sci- F,ZHANG JY, XU X,ZHANG FC AND WANG Y. 2001. ence Press, p. 665–689, 937–938 (in Chinese). Further support for a Cretaceous age for the feathered- ZHOU ZH,BARRETT PM AND HILLTON J. 2003. An excep- dinosaur beds of Liaoning, China: New Ar-40/Ar-39 dat- tionally preserved Lower Cretaceous ecosystem. Nature ing of the Yixian and Tuchengzi formations. Chin Sci Bull 421: 807–814. 47(2): 135–138. ZHOU ZH AND WANG XL. 2000. A new species of Caudip- WANG XL,CAMPOS DA,ZHOU ZH AND KELLNER AWA. teryx from the Yixian Formation of Liaoning, Northeast 2008. A primitive istiodactylid pterosaur (Pterodacty- China. Vert PalAsit 38(2): 111–127. loidea) from the Jiufotang Formation (Early Cretaceous), ZHOU ZH AND WANG Y. 2010. Vertebrate diversity of northeast China. Zootaxa 1813: 1–18. the Jehol Biota as compared with other lagerstätten. Sci WANG XL AND DONG ZM. 2008. Order Pterosauria. In: China Earth Sci 53: 1894–1907. doi: 10.1007/s11430- LI JL,WU XC AND ZHANG FC (Eds), Chinese Fossil 010-4094-9 Reptiles and Their Kin, 2nd ed., Beijing: Science Press, p. 215–234. WANG XL,KELLNER AWA, JIANG SX,CHENG X,MENG X AND RODRIGUES T. 2010. New long-tailed pterosaurs (Wukongopteridae) from western Liaoning of China. An Acad Bras Cienc 82(4): 1045–1062.

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