Redescription of the First Pterosaur Remains from Japan: the Largest Flying Reptile from Asia

Historical Biology An International Journal of Paleobiology

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Redescription of the first pterosaur remains from Japan: the largest flying reptile from Asia

Alexander W.A. Kellner, Fabiana R. Costa, Xiaolin Wang & Xin Cheng

To cite this article: Alexander W.A. Kellner, Fabiana R. Costa, Xiaolin Wang & Xin Cheng (2016) Redescription of the first pterosaur remains from Japan: the largest flying reptile from Asia, Historical Biology, 28:1-2, 304-309

To link to this article: http://dx.doi.org/10.1080/08912963.2015.1028929

Published online: 01 Oct 2015.

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Redescription of the first pterosaur remains from Japan: the largest flying reptile from Asia Alexander W.A. Kellnera*, Fabiana R. Costab, Xiaolin Wangc and Xin Chenga,c aLaboratory of Systematics and Taphonomy of Fossil Vertebrates, Department of Geology and Paleontology, Museu Nacional/ Universidade Federal do Rio de Janeiro, Quinta da Boa Vista s/n, Saõ Cristo´vaõ CEP 20940-040, Rio de Janeiro, RJ, Brazil; bDepartment of Biological Sciences, Institute of Environmental, Chemical and Pharmaceutical Sciences, Universidade Federal de Saõ Paulo (UNIFESP), Diadema campus, Rua Prof. Artur Riedel 275, Jardim Eldorado CEP 09972-270, Diadema, Saõ Paulo, Brazil; cKey Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, P.O. Box 643, Beijing, 100044, P.R. China (Received 3 February 2015; accepted 10 March 2015)

Pterosaur remains are found in numerous deposits of the world, but most are isolated and fragmentary elements. This is the case of Japan where a small number of specimens from those volant reptiles have been reported. Here, we redescribe the ﬁrst pterosaur remains from Japan (NSM PV15005) that were found in outcrops of the Upper Cretaceous Yezo Group (Santonian–lower Campanian) in the Mikasa area of Hokkaido. Further preparation of this material revealed several pterosaur bones, including the distal end of a left femur, a non-ungual phalanx and a proximal caudal vertebra. Based on the double-condyle articulation of the caudal element and the main features of the femur, this specimen is referred to a pteranodontid-like pterosaur. Its wingspan is estimated to be around 6.8 m, making it the largest pterosaur recorded not only from Japan, but also from Asia so far, indicating that large ﬂying reptiles were widespread worldwide during the Upper Cretaceous. Keywords: Upper Cretaceous; Yezo Group; Japan; Pterosauria; Pterodactyloidea

Introduction other pterosaurian elements. Here, we provide a descrip- Although pterosaur remains are known from a compara- tion and comparison of this material, which comprises, tively large number of deposits (e.g. Barrett et al. 2008), besides the distal fragment of a left femur, a non-ungual only very few have yielded a reasonable amount of partial phalanx of a manual digit and a caudal vertebra. or complete skeletons (e.g. Bennett 1994; Chiappe et al. 1998;Wangetal.2005; Kellner et al. 2013;Manzigetal. 2014;Wangetal.2014) or a large quantity of isolated Institutional abbreviations elements (e.g. Unwin 2001; Rodrigues et al. 2011; HMG, Hobetsu Museum, Hokkaido, Japan; NSM PV, Rodrigues and Kellner 2013). Most occurrences, National Science Museum, Tokyo, Japan; PIN, Paleonto- however, consist of isolated and very fragmentary logical Institute, Russian Academy of Sciences, Moscow, material (e.g. O’Connor et al. 2006;Costaetal.2014). Russia; PU, Museum of Natural History, Princeton This is also the case of the Cretaceous deposits of the University, Princeton, USA; RGM, National Natuurhis- Japanese Archipelago, where only a limited number of risch Museum Leiden, Leiden, Netherlands; YPM, Yale specimens were recovered so far (e.g. Okasaki 1995; Peabody Museum, New Haven, USA; ZIN PH, Zoological Chitoku 1996; Ikegami & Tamura 1996; Okazaki & Institute, Russian Academy of Sciences, Saint Petersburg, Kitamura 1996;Unwinetal.1996; Ikegami 1997; Russia. Downloaded by [University of Nebraska, Lincoln] at 18:48 01 October 2015 Ikegamietal.2000). The first pterosaur record for Japan is a femoral distal end and other associated bones (NSM PV15005, casts at Geological setting the Museu Nacional/Universidade Federal do Rio de NSM PV15005 was recovered from Hokkaido Prefecture, Janeiro – MN 4719-V) from the Upper Cretaceous Yezo Northeast Japan, which is tectonically divided into seven Group (Santonian–lower Campanian) in the Mikasa area belts: Nemuro, Tokoro, Hidaka, Kamuikotan, Ishikari, of Hokkaido. This material was briefly reported by Obata Rebun-Kabato and Oshima Belts (Okada and Mateer, et al. (1972), who identified the femur but not the 2000). The Ishikari Belt comprises the Yezo Supergroup remaining elements and referred this specimen to (Aptian–Maastrichtian) that extends from southern Pteranodon sp. without proper justification. This specimen Hokkaido to the Sakhalin Island (East Russia) (Okada has since been prepared and, besides the femur, revealed 1983; Takashima et al. 2004) and is formed by (in

*Corresponding author. Email: [email protected]

q 2015 Taylor & Francis Historical Biology 305

ascending order) the Lower Yezo (late Barremian–late Albian), Middle Yezo (late Albian–Turonian), Upper Yezo (Conician-Santonian) and Hakobuchi (Campanian– Maastrichtian) Groups (Matsumoto 1951; Okada 1982). This supergroup is a marine Cretaceous succession located at the circum-North Pacific regions and because it has been providing a number of macro- and microfossils at its horizons (particularly in the Upper Cretaceous; Iba and Sano 2006), many studies on biostratigraphy and palaeontology have been made on its sediments (e.g. Matsumoto 1942a, 1942b, 1943; Maeda 1986; Toshimitsu Figure 1. (Colour online) Caudal vertebra of NSM PV15005 in et al. 1995). distal (A), proximal (B), lateral (C), dorsal (D) and ventral (E) views. The specimen here described came from an outcrop of con, condyles; nc, neural canal; ns, neural spine. Scale bar: 10 mm. the Upper Cretaceous Yezo Group, which is 400–1300 m thick with argillaceous facies that marks the Urakawan and posterior spool-shaped condyles that fuse laterally. Transgression (Matsumoto 1967, 1977). This group The articular facets are sub-circular; there is a groove extends through central Hokkaido, northern Japan and running dorsally between these condyles at the midline of Sakhalin Island in the Russian Far East (Takashima et al. the centrum. The right condyle is slightly smaller than the 2004; Yazykova 2004) and is regarded as a sequence of left condyle. The neural canal is small, with its dorsal forearc basin sediments (Okada 1983). Within this group border not exceeding the upper limits of the dorsal borders the shelf-coastal Mikasa area – from where NSM PV15005 of both condyles. The neural arch is low (Figure 1, came from – is a succession across the Cenomanian– Table 1). Turonian boundary mainly formed by marine sandy facies (Mikasa Formation; Kurihara et al. 2012). Below this boundary is the only place where weakly laminated Non-ungual phalanx mudstone is observed (Kurihara et al. 2012). The non-ungual phalanx is quite short, with a length of 16.9 mm and has a sub-rectangular shape in dorsal view. It is slightly flattened dorsoventrally and eroded in many Description points of its surface. The proximal articular facet is a The specimen (NSM PV15005) consists of invertebrates concave and the distal one bears two condyles, which are and a few pterosaur bones that are preserved in a hard typical for such a bone. The phalanx is pierced by a black limestone. Some fossils could be isolated by pneumatic foramen at the ventral surface of the distal end, mechanical preparation, particularly the pterosaur just below the condyles (Figure 2). It is difficult to be sure if material. this element is a manual or pedal phalange, although the Regarding the bones, there are several small fragments latter might be more probable based on its overall that are difficult to identify. Among those are two morphology (e.g. being more flattened dorsoventrally and elongated hollow long elements that lack proximal and short) and on the other elements preserved in this specimen. distal articulations. Both show rounded transverse sections, suggesting that they are likely incomplete metatarsals (not figured), and do not provide any particular anatomical Femur Downloaded by [University of Nebraska, Lincoln] at 18:48 01 October 2015 information. There are three more bones that could be The largest preserved bone of NSM PV15005 is the distal identified: a non-ungual phalanx, the distal articulation of a articulation of a femur (Figure 3) as correctly indicated by left femur and a proximal caudal vertebra. All bones are preserved in three dimensions without marked distortions, Table 1. Measurements of the caudal vertebra characters of a rather unusual condition for pterosaur remains. There are NSM PV15005 (in millimetres). no particular differences in proportion and therefore all Characters Measurements bones are treated as belonging to the same individual. Length of left condyle 14.8 Length of right condyle 15.8 Width of vertebra 17.9 Caudal vertebra Height of vertebra 10.1 Apart from the neural spine, which is partially broken at its Length at the basis of the neural spine 7.9 tip, the caudal vertebra is complete and shows no apparent Height of neural spine (preserved) 8.1 Height of neural canal 3.4 distortion (Figure 1). The centrum is wide (17.9 mm Width of neural canal 3.3 width), low (10.3 mm height) and bears double anterior 306 A.W.A. Kellner et al.

Table 2. Measurements of the femoral characters of NSM PV15005 (in millimetres).

Characters Measurements Width of femur (distal epiphysis) 46.2 Height of medial condyle 34.2 Height of lateral condylea 28.6 Height of lateral condyleb 32.6

a Relative to the parasagittal axis. b From anterior to posterior tip.

Figure 2. (Colour online) Non-ungual phalanx of NSM PV15005 in ventral (A), and dorsal (B) views. co, condyles; fo, foramen. Scale bar: 10 mm. a considerable flexion between femur and tibiotarsus. Proximally placed to the condyles on the posterior part, there is a poorly pronounced popliteal fossa for the Obata et al. (1972). It comes from the left side, showing attachment of the flexor muscle (s) of the tibiotarsus and/or part of the diaphysis and an almost complete distal pes. The medial epicondyle is represented by an almost articulation. The bone cortex is very thin (0.8 mm thick) imperceptible small swelling, confluent with the distal and not well preserved in most parts, likely broken away medial condyle, while the lateral epicondyle is not during the collection process. At the base of the diaphysis perceptible at all. just above the condyles, the shaft’s diameter is mediolaterally larger (37.7 mm) than its anteroposterior diameter (25.1 mm), resulting in an oval transverse Discussion section. From this point on, the diameter cannot be Three-dimensionally preserved post-cranial remains of measured because the upper part of the preserved pterosaurs (complete or fragmentary) are limited to few diaphysis is transversally broken at the medial side. deposits worldwide. Pterosaur femora are not usually The condyles that form the articulation are rounded reported (Veldmeijer 2003), and regarding pterodactyloid protrusions that are slightly convex in lateral view. They pterosaurs, the morphology of their caudal series is poorly are asymmetrical, with the lateral condyle moderately known and restricted to few specimens, such asDsungar- smaller than the medial condyle in distal view (see ipterus weii (Young 1964), Pterodactylus antiquus (Well- Table 2). The lateral condyle bears a bulbous edge that nhofer 1970; Bennett 1987), Pteranodon (Bennett 1987, projects obliquely relative to the parasagittal plane (angle o 2001), Anhanguera piscator (Kellner and Tomida 2000), of 60 ). Because of this marked projection, the anterior Pterodaustro guinazui (Codorniu´ 2005), Zhenyuanopterus edge of the lateral condyle in distal view is lower than the longirostris (Lu¨ 2010) and Dawndraco kanzai (Kellner medial condyle. The latter is just slightly oblique, forming o 2010). Even more scanty is a detailed description of these an angle of 20 to the parasagittal plane. Its medial margin structures, which hampers comparisons. is formed by a marked bony ridge. Both condyles are Overall NSM PV15005 can be allocated in the separated by a shallow intercondylar sulcus for the tendon Pterodactyloidea on the basis of the large size of its M. triceps femoris ¼ Mm. ambiens iliotibialis et of ( , , femur because this clade encompasses the largest flying femorotibialis ). This sulcus extends from the anterior to reptiles (e.g. Andres et al. 2014), the shape, size and the posterior part of the distal articulation, which suggests Downloaded by [University of Nebraska, Lincoln] at 18:48 01 October 2015 morphology of the caudal vertebra whose duplex articulation is exclusive from pterodactyloid forms (e.g. Bennett 2001), and also the pneumaticity of the non- ungual phalanx of the forelimb, which is characteristic of Cretaceous pterodactyloids (Seeley 1901; O’Connor 2006; Benson et al. 2012). The Pterodactyloidea is divided into the Archaeopter- odactyloidea and the Dsungaripteroidea (Kellner, 2003). The double-condyle articulation of the caudal vertebra of NSM PV15005 is a feature not present in any known archaeopterodactyloid pterosaur so far, which thus allows the allocation of this specimen into the dsungaripteroid Figure 3. (Colour online) Distal femoral fragment of NSM group. The latter comprises the basalmost clade Nycto- PV15005 in dorsal (A), ventral (B), lateral (C), and medial (D) views. sauridae, the Pteranodontoidea (sensu Kellner 2003, 2010) lcon, lateral condyle; mcon, medial condyle. Scale bar: 50 mm. and the Tapejaroidea. The tail of Nyctosaurus is not well Historical Biology 307

known and comprises only four preserved vertebrae, which are similar to the anterior ones of Pteranodon according to Bennett (1987), although the presence of the duplex articulation cannot be confirmed. This feature is only reported in the pteranodontid pterosaurs Pteranodon (Bennett, 2001), Dawndraco (Kellner, 2010) and Anhan- guera piscator (Kellner and Tomida 2000). In those taxa, the lateral margins of the anterior articular facet of the centrum in the first three anterior caudal vertebrae surround a deep and long concavity. However, these condyles in Pteranodon (Bennett 2001, figure 51(c)) and Dawndraco (Kellner, 2010, figure 4) are more rounded Figure 4. (Colour online) Distal femoral fragment in distal view than in the ones known of Anhanguera piscator (Kellner of (A) NSM PV15005, and (B) Tupuxuaraleonardii (Iwaki specimen). icfs, intercondylar sulcus; lcon, lateral condyle; and Tomida 2000, figure 19(e)), a feature also observed in mcon, medial condyle. Scale bar: 10 mm. NSM PV15005. It should be noted, however, that in the Brazilian specimen, the caudal series was not articulated with the sacrum and therefore the most anterior caudals were most likely not preserved. closely related to that clade. Given that pteranodontids A well-marked duplex centra is a condition present at have typically small feet, the phalanx here described could the proximal vertebrae of the segment in Pteranodon and be a pedal one. Dawndraco (segments 1–4); from caudal 2, the duplex Despite all these features shared with the Pteranodon- character of the centrum becomes reduced (Bennett 2001), tidae, this specimen presents a gap between both condyles although this reduction in size is not as abrupt in in a way that these structures are not levelled anteriorly in Dawndraco (Kellner, 2010). In any case, the caudal the same plane. This feature is not observed in the vertebra of NSM PV15005 has pronounced double condyles of pteranodontoids, despite these structures are condyles and can be regarded as belonging to the differently projected relative to the parasagittal plane. proximal segment of the tail. According to Bennett (1987), Moreover, in distal view (Figure 4(A)), the medial condyle this kind of articulation of the caudal vertebrae did not is very projected anteriorly, which has not been observed allow lateral motion, but dorsoventral flexion, which in any pteranodontid so far. would reduce the mass of muscle that would be necessary Another interesting aspect of the Japanese specimen is to control the tail. its size. As known, establishing pterosaur wingspan on Regarding the femur, the presence of oblique isolated remains is a difficult task (e.g. Averianov et al. condyles is a feature observed in pteranodontoids. 2005; Kellner et al. 2013). Averianov et al. (2005) made a In tapejaroids such as the Azhdarchidae (e.g. Azhdarcho rough estimate based on ornithocheiroid a regression specimens in the collection ZIN PH; Averianov et al. Equation (Z ¼ 3.036 þ 0.082Y) using the distal femur and 2005) and the Dsungaripteridae (Averianov, 2004), the wingspan of two specimens of ornithocheirids. If this condyles are symmetrical, almost parallel to the sagittal equation is used the wingspan of NSM PV15005 was plane. However, in Tupuxuara leonardii (Iwaki speci- around 6.8 m (Table 3). men), the distal end of the femur is very similar to NSM Because pterosaur remains in Japan are limited to a 15005 (Figure 4). Nonetheless, all specimens to which we number of fragmentary specimens, it is difficult to

Downloaded by [University of Nebraska, Lincoln] at 18:48 01 October 2015 had access and that exhibit proximal caudal elements of estimate the wingspan of specimens as aforementioned. Tapejaridae (most not described), lack a duplex centra. Okazaki and Kitamura (1996) described an incomplete Therefore, it seems unlikely that NSM 15005 represents a wing phalanx of an azhdarchid, and based on its member of this or closely related (i.e. Tapejaroidea) resemblance with Dsungaripterus, the wingspan of this clade. specimen was estimated as ,2 m. Chitoku (1996) reported Within the Pteranodontoidea, NSM PV15005 shares an ornithocheirid ( ¼ Anhangueria) cervical vertebra, and with the Pteranodontidae (e.g. Pteranodon, Dawndraco) by comparing it with a cervical vertebra from Delaware, and the Anhangueridae (e.g. Anhanguera piscator) a distal USA assigned to Pteranodon (Baird and Galton 1981) the end of the femur bearing asymmetrical lateral and medial author suggested a wingspan of about 5.8 m, the same as condyles. Moreover, NSM PV15005 also shares with the estimated for the Delaware pterosaur. Unwin et al. (1996) Pteranodontidae the medial condyle being larger than the described a dsungaripterid wing phalanx and estimated a lateral condyle (Bennett 2001; Kellner 2010), a condition wingspan between 1.5 and 2 m for the specimen. The not observed in Anhanguera piscator (Kellner and Tomida wingspan estimated (ES) for NSM PV15005 is thus much 2000). Therefore, based on these comparisons, NSM larger, making it not only the largest pterosaur from Japan PV15005 might be a pterosaur that represents this or is (Table 4), but also from Asia. 308 A.W.A. Kellner et al.

Table 3. Estimated wingspan (EW) in metres based on femur maximum distal width (FEMDW) in millimetres in some ornithocheiroid pterosaurs (modiﬁed from Averianov et al. 2005).

Taxon, specimen FEMDW EW Reference Anhanguera piscator, NSM PV19892 24.0 5.0 Kellner and Tomida (2000) Anhanguera spielbergi, RGM 401880 35.0 5.9 Veldmeijer (2003) Ornithocheiroidea indet., PIN 5028-1 20.3 4.7 Averianov et al. (2005) NSM PV15005 46.2 6.8 This paper

Table 4. Estimated wingspans (EW) of Japanese pterosaurs (in metres).

Specimen Taxon EW Reference PU 21820 Ornithocheiridae indet. 5.8 Baird and Galton (1981) HMG 94767 Ornithocheiridae indet. 5.8 Chitoku (1996) NSM PV20042 Dsungaripteridae indet. 1.5–2 Unwin et al. (1996) KCM VP000,120 Pterodactyloidea indet. ,2 Okazaki and Kitamura (1996) NSM PV15005 Pteranodontidae 6.8 This paper

Conclusion Desenvolvimento Cientı´fico e Tecnolo´gico [grant number 304780/2013-8 to A.W.A. Kellner; grant number 150053/2014- This paper provides the detailed description of NSM 2 to F.R. Costa] and the National Science Fund for Distinguished PV15005, which was the first reported pterosaur specimen Young Scholars [grant number 40825005], National Basic from Japan. The material represents a pteranodontid-like Research Program of China [grant number 2012CB821900] and pterosaur based on the presence of a double-condyle the Hundred Talents (all to X. Wang). condition of the sole preserved proximal caudal vertebra. Furthermore, the shape of the distal end of the femur showing oblique and asymmetrical lateral and medial References condyles, with the medial condyle larger than the lateral Andres B, Clark J, Xu X. 2014. The earliest pterodactyloid and the origin one, is also consistent with this interpretation. We estimate of the group. Curr Biol. 24(9):1011–1016. doi:10.1016/j.cub.2014. that this specimen had a wingspan of around 6.8 m, making 03.030. Averianov AO. 2004. New data on Cretaceous flying reptiles it the largest flying reptile known not only from Japan, but (Pterosauria) from Russia, Kazakhstan, and Kyrgyzstan. Paleontol from Asia as well. This finding indicates that large-winged J. 38(4):426–436. pterosaurs were widespread around the globe during the Averianov AO, Arkhangelsky MS, Pervushov EM, Ivanov AV. 2005. A new record of an azhdarchid (Pterosauria: Azhdarchidae) from the Upper Cretaceous and shows the potential of the Japanese Upper Cretaceous of the Volga Region. Paleontol J. 39(4):433–439. archipelago in providing more important pterosaur Baird D, Galton PM. 1981. Pterosaur bones from the Upper Cretaceous of material. Delaware. J Vert Paleontol. 1(1):67–71. doi:10.1080/02724634. 1981.10011880. Barrett PM, Butler RJ, Edwards NP, Milner AR. 2008. Pterosaur distribution in time and space: an atlas. Zitteliana. B28:61–107. Bennett SC. 1987. New evidence on the tail of pterosaur Pteranodon Acknowledgements (Archosauria: Pterosauria). In: Currie PM, Koster EH, editors. Fourth

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