Historical Biology An International Journal of Paleobiology

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Pleistocene fossil snakes (Squamata, Reptilia) from Shanyangzhai Cave, Hebei, China

Yu Chen, Yong-Xiang Li, Jing-Song Shi, Yun-Xiang Zhang & Kun Xie

To cite this article: Yu Chen, Yong-Xiang Li, Jing-Song Shi, Yun-Xiang Zhang & Kun Xie (2019): Pleistocene fossil snakes (Squamata, Reptilia) from Shanyangzhai Cave, Hebei, China, Historical Biology, DOI: 10.1080/08912963.2019.1658094 To link to this article: https://doi.org/10.1080/08912963.2019.1658094

Published online: 02 Sep 2019.

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ARTICLE Pleistocene fossil snakes (Squamata, Reptilia) from Shanyangzhai Cave, Hebei, China Yu Chena, Yong-Xiang Lia, Jing-Song Shib, Yun-Xiang Zhanga and Kun Xiea aState Key Laboratory of Continental Dynamics, Department of Geology, National Demonstration Center for Experimental Geology Education (Northwest University), Xi’an, China; bChinese Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Beijing, China

ABSTRACT ARTICLE HISTORY Shanyangzhai Cave, located in Hebei Province, North China, has yielded a large number of snake bones Received 21 April 2019 dated back to the late middle Pleistocene and late Pleistocene. These snakes are represented by at least Accepted 17 August 2019 six taxa: three colubrids (Elaphe cf. schrenckii, Elaphe cf. dione, Lycodon sp.), one natricid (Rhabdophis KEYWORDS fi tigrinus), and two viperids (Gloydius sp1. and Gloydius sp2.). Most of the identi ed taxa still occur on the China; Pleistocene; Elaphe; research area, except for Elaphe schrenckii. The snake fauna of Shanyangzhai Cave represents the first Lycodon; Rhabdophis; Pleistocene snake remains described in any detail from a cave locality in North China. The bones in Gloydius Shanyangzhai Cave also represent the first fossil record of pit vipers in China.

Introduction fauna in Shanyangzhai Cave, discussing the age and environ- ment of these fauna (Niu et al. 1999, 2003). However, none of In Eurasia, fossil snakes from the Pleistocene are well docu- these studies mentioned snake fossils. The snake remains mented in western and central Europe, but they are very studied here come from numerous excavations of Northwest poorly known in East Asia. To date, only four localities (or University since 2005 (Wang 2009; Zhang et al. 2010;Li2012; complexes of localities) have yielded fossils of Pleistocene Xie 2017). The purpose of this paper is to provide a detailed snakes: Zhoukoudian location 1 and 3 (Bien 1934), Haimao description of these snake fossils and discuss the paleoenvir- Cave (Sun 1992), Okinawajima Island (Otsuka 2002; Ikeda onment and snake distribution changes since the Pleistocene et al. 2016) and Renzidong Cave (Mead et al. 2016). This may in this region. be due to the lack of an adequate comprehensive skeletal collection of living snake species. Furthermore, snake fossil materials are usually disjointed when they are discovered, Material and methods consisting of fragmentary vertebrae and ribs, which makes it The Shanyangzhai fossil site has been subdivided into four difficult to collect these small fossils. However, snakes are locations by the latest research: SYZ 1 (discovered in 2005 useful in the reconstruction of terrestrial paleoenvironments (Xie 2017)), SYZ 2(discovered in 2000, named as location 2 of the Quaternary, since they are poikilothermal animals with by Niu et al. (2003)), SYZ 3 (discovered in 2000, named as relatively reduced mobility (Bailon 1991). Moreover, their location 1 by Niu et al. (2003)), and SYZ 4(discovered in 2015 fossil record promotes a better understanding of paleofaunis- (Xie 2017)). The snake remains described in this paper come tic and paleobiogeographic events during the Pleistocene from SYZ 2 and SYZ 4. (Venczel 2000), and an implicit understanding of the origin By comparing it with other Pleistocene fauna in North of the modern East Asia snake fauna. China (Niu et al. 2003; Zhang et al. 2010), the fauna of SYZ This paper reports on a snake fauna from the Pleistocene 2 indicates a middle to late Pleistocene age. Work by Xie in Shanyangzhai Cave. This cave is located at 119°31ʹ50″E, (2017) has also assigned SYZ 2 to the top of the middle 40°5ʹ13″N (165 m elevation) (Figure 1), near the village of Pleistocene, with an age of 270–330 ka estimated by Shanyangzhai, approximately 20 km north of Qinhuangdao, Electron Spin Resonance (ESR) dating. Considering that the Hebei Province, North China (Zhang et al. 2010). Since the test sample was collected from a lower layer than the fossil 1980s, the diverse fauna from this location have been site, the age of SYZ 2 should be slightly later than 270 ka. The described in several studies. The first mention of fossil bones of mammals from SYZ 4 were dated by the Accelerator remains a presence in Shanyangzhai Cave dates from Kong Mass Spectrometry (AMS) method, and the age obtained for (2009) who made the first excavation. Then, in the early these specimens was 22,287–22,753a B.P. (δ13C = 20.95). 1980s, a team from the Institute of Vertebrate Paleontology The collected sample included 905 fragments. Among and Paleoanthropology (IVPP), Chinese Academy of Sciences them, 472 fragments were from SYZ 2, and 433 fragments (Beijing) joined the excavation (Huang 1989). In approxi- were from SYZ 4. All of the abovementioned fossil specimens mately 2000, another team described some of the mammalian

CONTACT Yong-Xiang Li [email protected] State Key Laboratory of Continental Dynamics, Department of Geology, National Demonstration Center for Experimental Geology Education (Northwest University), Xi’an China © 2019 Informa UK Limited, trading as Taylor & Francis Group

Published online 02 Sep 2019 2 Y. CHEN ET AL.

Figure 1. Location of Shanyangzhai Cave. are preserved in the Vertebrate Palaeontology Collection, have epizygapophyseal spines on the posterior tips of the Geology Department of Northwest University (NWUV). postzygapophyses (Holman 2000). The identifications of fossils described here were mainly based on the taxa presently inhabiting in the Palearctic Subfamily Colubrinae OPPEL, 1811 Realm of China (3 families, 11 genera, and 19 species), but the extant species only living in the Oriental Realm of China (3 families, 18 genera, and 26 species) were also Diagnosis considered. Skeletons of all 45 species (each species is Hypapophyses lack trunk vertebrae; the haemal keels are well represented by one specimen) were housed in the specimen projected from the centrum; subcentral ridges and grooves room of IVPP (the number of all 45 specimens are listed in are usually distinct; prezygapophyseal processes prominent Appendix 1 and Appendix 2). Furthermore, we also and well projected (Holman 2000). referred to the descriptions in some studies (Szyndlar 1984, 1991a, 1991b; Ratnikov 2004; Ikeda 2007). The dis- Genus Elaphe FITZINGER, 1833 tribution and the habitat of present species were mainly derived from Zhao et al. (1999)andZhao(2006). The Elaphe cf. schrenckii BOULENGER, 1916 vertebrae of snakes were measured according to (Figures 2 & 3) Auffenberg (1963)’s methods. All measurements and photo- graphy were performed with an Automated Digital Material Microscope ZEISS Smartzoom5 to the nearest 0.01 mm. Nineteen specimens from SYZ 4, including 14 mid-trunk The morphological characters and abbreviations used to vertebrae (NWUV 1492-1506) and 5 posterior-trunk verteb- describe the vertebrae follow Auffenberg (1963), Szyndlar rae(NWUV 1507-1510); most are complete or slightly (1984), LaDuke (1991) and Holman (2000). All terminology damaged. Specimens NWUV 1492 (Figure 2) and NWUV follows Holman (2000). The classification of taxa mostly 1507 (Figure 3) are the primary basis for our morphological follows Holman (2000). The regional subdivision of the descriptions. whole snake vertebral column follows LaDuke (1991). Description NWUV 1492 is a mid-trunk vertebra; CL = 7.93 mm; NAW = Systematic palaeontology 5.71 mm; CL/NAW = 1.39. In dorsal view, the anterior edge Family Colubridae OPPEL, 1811 of the zygosphene is concave; the prezygapophyseal articular facet oval; prezygapophyseal accessory process projects 1.33 mm beyond the facet and is directed laterally; the distal Diagnosis tip of the prezygapophyseal accessory process is pointed; Trunk vertebrae are usually lightly built and longer than wide; epizygapophyseal spines are absent. In ventral view, the hae- the centrum usually has prominent subcentral ridges; the mal keel is prominent, spatulate, extending from cotyle to prezygapophyseal processes are prominent; some species condyle, and gradually narrowed anteriorly; the HISTORICAL BIOLOGY 3

Figure 2. Middle-trunk vertebra of Elaphe cf. schrenckii (NWUV 1492). (a) – lateral view, (b) – anterior view, (c) – posterior view, (d) – dorsal view, (e) – ventral view. Scale bar = 2 mm.

Figure 3. Posterior-trunk vertebra of Elaphe cf. schrenckii (NWUV 1507). (a) – lateral view, (b) – anterior view, (c) – posterior view, (d) – dorsal view, (e) – ventral view. Scale bar = 2 mm. postzygapophyseal articular facet is oval; subcentral ridges are slightly narrower than the zygosphene; the prezygapophyseal well developed and straight, with adjacent small subcentral accessory process is developed. In the posterior view, the foramina. In lateral view, the neural spine is 5.83 mm long neural arch is vaulted; the condyle is oval and larger than with a height of 3.08 mm; the anterior end of the neural spine the neural canal. NWUV 1493-1506 have the same morphol- is approximately vertical, and the posterior part of the neural ogy and are similar-sized vertebrae. spine overhangs posteriorly; the parapophyseal process is NWUV 1507 is a slightly damaged trunk vertebra that is undeveloped. In the anterior view, the cotyle is oval and quite similar to NWUV 1492, except for a distinct subcentral 4 Y. CHEN ET AL. paramedian lymphatic fossae between the haemal keel and -InE. anomala, the shape of the anterior edge of the zygosphene parapophyseal. In addition, the haemal keel of NWUV 1507 is in dorsal view is almost straight, not concave, and the neural arch more narrow than that of NWUV 1492. These characteristics and neural spine are lower than those in the fossils; are consistent with trunk vertebrae that are more posteriorly - the vertebrae of E. bimaculata, as a small-sized colubrine (total positioned than NWUV 1492 (LaDuke 1991). NWUV length less than 100 cm) (Zhao et al. 1999; Zhao 2006), seldom 1508–1510 have the same morphology and are vertebrae of reach a length of 5 mm (Szyndlar 1991a); approximately the same size. -inE. carinata, the shape of the anterior edge of the zygosphene in dorsal view is crenate, not concave, and the neural spine is higher than that in the fossils (Ikeda 2007); Remarks The assignment of these specimens to the subfamily -inE. dione, the shape of the anterior edge of the zygosphene in Colubrinae was based on the lack of hypapophyses and devel- dorsal view is crenate, not concave (Ratnikov 2004); oped haemal keel (Holman 2000). There are six genera of -inE. taeniura, the anterior edge of the zygosphene in dorsal Colubrinae currently living in the Palaearctic Realm of China: view is crenate, and the prezygapophyseal process projects at Elaphe, Euprepiophis, Lycodon, Oocatochus, Orientocoluber a slight anterior angle with a longer accessory process (Ratnikov and Ptyas (Zhao et al. 1999; Zhao 2006). 2004; Ikeda 2007). The moderately robust vertebrae described above do not Therefore, the combinations of characters exhibited by these belong to Oocatochus (Ratnikov 2004), Orientocoluber and fossil specimens are shared only with the characters of Elaphe Ptyas, which have slender vertebrae. The above-described speci- schrenckii vertebrae (Figure 4). Even so, these fossils differ, mens are also distinct from Lycodon, which have a foliated more or less, from the vertebrae of Elaphe schrenckii in the prezygapophyseal accessory process and moderately crenated shape of the anterior edge of the zygosphene and articular zygosphene (Ikeda 2007). Only one species of Euprepiophis facet. Furthermore, the vertebral morphology of Elaphe davidi currently lives in the Palaearctic Realm of China: Euprepiophis is still unknown. Thus, we simply identified these fossil ver- mandarina (Zhao et al. 1999;Zhao2006), and the vertebrae of tebrae as belonging to Elaphe cf. schrenckii. this species are more robust than those of these fossils. After excluding all of these genera above, Elaphe is the only remaining genus. However, Elaphe species, which are Elaphe cf. dione PALLAS, 1773 widely distributed in East Asia, vary greatly in their vertebral (Figures 5 & 6) morphology; thus, a one-by-one examination of the seven species of Elaphe that currently live in the Palaearctic Realm Material of China (E. anomala, E. bimaculata, E. carinata, E. davidi, Four specimens from SYZ 4, including a single mid-trunk E. taeniura, E. dione and E. schrenckii (Zhao et al. 1999; Zhao vertebra (NWUV 1511) and 3 posterior-trunk vertebrae ff 2006)) is needed. Most of these species di er from the fossils (NWUV 1512–1514); all of these specimens are complete or as follows: nearly complete. Specimen NWUV 1511 (Figure 5) and

Figure 4. Middle-trunk vertebra of modern Elaphe schrenckii (OV 2499). (a) – lateral view, (b) – anterior view, (c) – posterior view, (d) – dorsal view, (e) – ventral view. Scale bar = 2 mm. HISTORICAL BIOLOGY 5

Figure 5. Middle-trunk vertebra of Elaphe cf. dione (NWUV 1511). (a) – lateral view, (b) – anterior view, (c) – posterior view, (d) – dorsal view, (e) – ventral view. Scale bar = 2 mm.

Figure 6. Posterior-trunk vertebra of Elaphe cf. dione (NWUV 1514). (a) – lateral view, (b) – anterior view, (c) – posterior view, (d) – dorsal view, (e) – ventral view. Scale bar = 2 mm.

NWUV 1514 (Figure 6) are the primary basis for our mor- NAW = 3.82 mm; CL/NAW = 1.23. In the dorsal view, the phological descriptions. anterior edge of zygosphene is crenate; the prezygapophyseal articular facet is ovoid; the prezygapophyseal accessory pro- Description cess projects 0.80 mm beyond the facet and is directed later- NWUV 1511 is a slightly damaged mid-trunk vertebra that ally; the distal tip of the prezygapophyseal accessory process is lost part of the neural arch and neural spine; CL = 4.71 mm; pointed; epizygapophyseal spines are absent. In the ventral 6 Y. CHEN ET AL. view, the haemal keel is prominent, spatulate, extending from -inE. schrenckii, the shape of the anterior edge of the zygosphene cotyle to condyle, and gradually narrowed anteriorly; the in dorsal view is concave, not crenate, and the neural arch and postzygapophyseal articular facet is oval. In the lateral view, neural spine are higher than those in the fossils; the neural spine is approximately 3.53 mm long with a height -inE. taeniura, the neural arch and neural spine are higher than of 1.76 mm; the anterior end of the neural spine overhangs those in the fossils (Ratnikov 2004; Ikeda 2007). slightly, and the posterior part of the neural spine overhangs Therefore, the combinations of characters exhibited by these posteriorly; the parapophyseal process is undeveloped. In the fossil specimens are shared only with the characters of Elaphe anterior view, the cotyle is oval and slightly narrower than the dione vertebrae (Figure 7). Even so, these fossils differ, more zygosphene; the prezygapophyseal accessory process is devel- or less, from the vertebrae of Elaphe dione in the shape of the oped. In the posterior view, the neural arch is arched; the neural spine and haemal keel. Furthermore, the vertebral condyle is oval and approximately equal in size to the neural morphology of Elaphe davidi is still unknown. Thus, we canal. simply identified the fossil vertebrae as belonging to Elaphe NWUV 1514 is a trunk vertebra with most of the same cf. dione. characteristics as NWUV 1511, except for a distinct subcen- tral paramedian lymphatic fossae and a gladiate shaped hae- mal keel. These characteristics indicate that this is a posterior- Genus Lycodon FITZINGER, 1826 trunk vertebra. NWUV 1512-1513 have the same morphology Lycodon sp. CANTOR, 1842 and are similar-sized vertebrae. (Figure 8) Remarks The robustness of the centrum and characteristics of the Material prezygapophyseal accessory process described above do not Four middle-trunk vertebrae from SYZ 4 (NWUV 1515- occur in Euprepiophis, Lycodon, Oocatochus, Orientocoluber 1518). All vertebrae are complete or nearly complete. and Ptyas. Specimen NWUV 1515 (Figure 8) is the primary basis for Most of the remaining seven species of Elaphe currently our morphological descriptions. living in the Palaearctic Realm of China differ from the fossils as follows: Description -inE. anomala, the neural arch is higher than that in the fossils; NWUV 1515 is a slightly damaged mid-trunk vertebra that lost part of the neural spine; CL = 4.77 mm; NAW = -inE. bimaculata, the tip of the prezygapophyseal accessory 3.44 mm; CL/NAW = 1.39. In dorsal view, the anterior edge process is truncated (Ikeda 2007); of the zygosphene is concave or concave with median tuber- -inE. carinata, the neural arch and neural spine are higher than cle; the prezygapophyseal articular facet is ovoid; the prezy- those in the fossils (Ikeda 2007); gapophyseal accessory process projects 1.09 mm beyond the

Figure 7. Middle-trunk vertebra of modern Elaphe dione (OV 2302). (a) – lateral view, (b) – anterior view, (c) – posterior view, (d) – dorsal view, (e) – ventral view. Scale bar = 2 mm. HISTORICAL BIOLOGY 7

Figure 8. Middle-trunk vertebra of Lycodon sp. (NWUV 1515). (a) – lateral view, (b) – anterior view, (c) – posterior view, (d) – dorsal view, (e) – ventral view. Scale bar = 2 mm. facet at a slight anterior angle; the distal tip of the prezyga- L. subcinctus, L. fasciatus, L. laoensis and L. aulicus,currently pophyseal accessory process is foliated; epizygapophyseal only live in the Oriental Realm (Zhao et al. 1999;Zhao2006). spines are absent. In the ventral view, the haemal keel is Until now, the vertebrae of only two of these snakes, prominent, cuneate, extending from cotyle to condyle, and L. flavozonatus and L. ruhstrati,havebeenexamined,andthese gradually narrowed anteriorly; the postzygapophyseal articu- vertebrae are no more similar to the fossils than the specimens of lar facet is auriculiform. In the lateral view, the neural spine is L. rufozonatum. Furthermore, the vertebrae of two other species obviously broken and largely lost; the parapophyseal process of Lycodon that live in the Palaearctic Realm of Japan: L. orientale is undeveloped. In the anterior view, the cotyle is oval and and L. semicarinatus, have been described by Ikeda (2007). slightly narrower than the zygosphene; the prezygapophyseal However, the pictures of these vertebrae are not shown in that accessory process is well developed. In the posterior view, the paper. In lieu of more materials for comparison, we simply neural arch is arched; the condyle is oval and approximately identified these fossil vertebrae as belonging to Lycodon sp. equal in size to the neural canal. NWUV 1516-1518 have the same morphology and are similar-sized vertebrae. Subfamily Natricinae BONAPARTE, 1838 Remarks The assignment of these specimens to the subfamily Colubrinae Diagnosis was based on the lack of hypapophyses and developed haemal The vertebrae of Natricinae have well developed, backwardly keel (Holman 2000). The moderately robust vertebrae described directed, usually somewhat pointed hypapophyses on all of the above do not belong to Oocatochus, Orientocoluber and Ptyas, trunk vertebrae (Holman 2000). These vertebrae differ from which have very slender vertebrae. One character of the fossil – the Viperidae vertebtae, which usually have sigmoid (and not the foliated prezygapophyseal accessory process – does not exist straight) hypapohyses, posteriorly vaulted (and not depressed) on the vertebrae of Euprepiophis and Elaphe currently lives in neural arches, shorter parapophyseal processes, usually much the Palaearctic Realm of China. longer centra and strong subcentral ridges (Szyndlar 1984). The combinations of characters mentioned above are shared only with the vertebrae of some Lycodon snakes. Three species of Lycodon currently live in the Palaearctic Realm of China: Genus Rhabdophis FITZINGER, 1843 L. rufozonatum, L. ruhstrati and L. liuchengchaoi.Among Rhabdophis tigrinus BOIE, 1826 these species, L. ruhstrati (Zhao et al. 1999; Zhao 2006)and (Figure 9) L. liuchengchaoi (Zhang et al. 2011) are excluded due to their small body size. The only species left is L. rufozonatum. However, these fossils differ from L. rufozonatum in many Material ways, such as the shape of the haemal keel and the robustness of One precloacal vertebra from SYZ 2 (NWUV 1530) and 11 the centrum. Other Lycodon snakes in China, such as precloacal vertebrae from SYZ 4 (NWUV 1519-1529). In the L. flavozonatum,L.rosozonatum,L.septentrionalis,subfamily Natricinae, the hypapophysis is present on all 8 Y. CHEN ET AL.

Figure 9. Trunk vertebra of Rhabdophis tigrinus (NWUV 1531). (a) – lateral view, (b) – anterior view, (c) – posterior view, (d) – dorsal view, (e) – ventral view. Scale bar = 2 mm.

precloacal vertebrae, and the division of the precloacal ver- canal. NWUV 1520-1530 have the same morphology and are tebrae into cervical and trunk regions is somewhat arbitrary. similar-sized vertebrae. Thus, we identified these fossil specimens only as precloacal vertebrae. All vertebrae are complete or nearly complete. Remarks Specimen NWUV 1519 (Figure 9) is the primary basis for The assignment of NWUV 1519 to the subfamily Natricinae our morphological descriptions. was based on the combination of the sigmoid-shaped hypa- pophyses, the convex neural arch and the well-developed Description prezygapophyseal accessory process. NWUV 1519 is an almost complete mid-trunk vertebra; CL = Three genera and four species of natricids currently live in 5.20 mm; NAW = 2.75 mm. A CL/NAW ratio of 1.89 indi- the Palaearctic Realm of China: Hebius vibakari, Natrix cates that the vertebra has a slender appearance. The left natrix, N. tessellata and Rhabdophis tigrinus (Zhao et al. prezygapophyseal accessory process, frontal tip of the neural 1999; Zhao 2006). The fairly slender fossil vertebrae do not spine and part of the left synapophyses are absent. belong to N. tessellata, which has relatively robust vertebrae In the dorsal view, the anterior edge of the zygosphene is (Szyndlar 1991b). Furthermore, the size of the fossils pre- convex; the prezygapophyseal articular facet is subtriangular; cludes them from belonging to Hebius vibakari, which is the prezygapophyseal accessory process projects 1.05 mm a small-sized colubrine (Zhao et al. 1999; Zhao 2006). beyond the facet at a slight anterior angle or is directed The combinations of characters exhibited by these fossil laterally; the distal tip of the prezygapophyseal accessory specimens are shared only with the vertebrae of Natrix natrix process is foliated; epizygapophyseal spines are barely devel- (Szyndlar 1991b) and Rhabdophis tigrinus (Figure 10), and oped. In the ventral view, the hypapophysis tip is broken but their morphologies are very similar. As the Shanyangzhai did project well beyond the edge of the condyle; the post- Cave is located in the distribution area of Rhabdophis tigrinus zygapophyseal articular facet is tetragonal. In lateral view, the and the distribution area of Natrix natrix in China is limited fi neural spine is 3.52 mm in length and 1.52 mm in height; the to the northwest, we identi ed these fossils as belonging to anterior end of the neural spine slightly overhangs, and the Rhabdophis tigrinus. posterior part of the neural spine overhangs posteriorly; the parapophyseal process is barely developed and projects for- Family Viperidae OPPEL, 1811 ward; the shape of the hypapophysis is sigmoid. In the ante- rior view, the cotyle is oval and slightly narrower than the zygosphene; the prezygapophyseal accessory process is well Diagnosis developed. In posterior view, the neural arch is arched; the Viperid vertebrae have short accessory processes. Throughout condyle is oval and approximately equal in size to the neural the column, these vertebrae have hypapophyses that are thick HISTORICAL BIOLOGY 9

Figure 10. Trunk vertebra of modern Rhabdophis tigrinus (OV 2310). (a) – lateral view, (b) – anterior view, (c) – posterior view, (d) – dorsal view, (e) – ventral view. Scale bar = 2 mm. but narrow in lateral view. They are usually long and tend to Description point ventrally in the anterior portion of the column. In the NWUV 1532 is a well-preserved trunk vertebra. CL = rear portion of the column, they point more posteriorly 3.80 mm; NAW = 2.39 mm. A CL/NAW ratio of 1.59 (Meylan 1982). Viperids differ from natricines in having dis- indicates that the vertebra has a slender appearance. In tinctly longer parapophyseal processes and posteriorly dorsal view, the anterior edge of the zygosphene is moder- depressed neural arches (Szyndlar 1988). ately convex; the prezygapophyseal articular facet is ovoid; the prezygapophyseal accessory process is at a slight ante- rior angle; the distal tip of the prezygapophyseal accessory Subfamily Crotalinae OPPEL, 1811 process is pointed; epizygapophyseal spines are absent. In ventral view, the hypapophysis projects beyond the edge of the condyle; the postzygapophyseal articular facet is tetra- Diagnosis gonal. In lateral view, the neural spine is 2.51 mm long with The vertebrae of Crotalinae are readily separated from those a height of 1.37 mm; the anterior end of the neural spine of elapids and colubrids based on their short, wide vertebral slightly overhangs, and the posterior part of the neural shape; long, thick hypapophyses that originate near the con- spine overhangs posteriorly; the parapophyseal process is dyles and are greater than or equal to one third the width of developed and projects obliquely downwards; the hypapo- the condyles; and large condylar size (Holman 2000). physis is long and straight, and the distal tip of the hypa- pophysis is pointed. In the anterior view, the cotyle is oval and slightly narrower than the zygosphene; the prezygapo- Genus Gloydius HOGE&HOGE, 1981 physeal accessory process is barely developed. In posterior Gloydius sp1. view, the neural arch is relatively depressed; the condyle (Figure 11) oval is much larger than the neural canal.

Remarks Material The assignment of NWUV 1532 to the family Viperidae was One precloacal vertebra from SYZ 4 (NWUV 1532). In the based on the long and straight hypapophyses, the depressed family Viperidae, the hypapophysis is present on all precloa- neural arch and the barely developed prezygapophyseal acces- cal vertebrae, and the division of the precloacal vertebrae into sory process. cervical and trunk regions is somewhat arbitrary. Thus, we There are two genera and 11 species of viperids currently fi identi ed this fossil specimen only as precloacal vertebra. living in the Palaearctic Realm of China: Gloydius brevicau- This vertebra are nearly complete. Specimen NWUV 1532 dus, G. changdaoensis, G. cognatus, G. halys, G. intermedius, (Figure 11) is the primary basis for our morphological G. lijianlii, G. shedaoensis, G. stejnegeri, G. ussuriensis, Vipera descriptions. berus and V. ursinii (Zhao et al. 1999; Zhao 2006; Shi et al. 10 Y. CHEN ET AL.

Figure 11. Trunk vertebra of Gloydius sp1. (NWUV 1532). (a) – lateral view, (b) – anterior view, (c) – posterior view, (d) – dorsal view, (e) – ventral view. Scale bar = 2 mm.

2016). Among these species, the trunk vertebrae of = 4.33 mm; NAW = 4.05 mm. A CL/NAW ratio of 1.07 G. brevicaudus, G. cognatus, G. intermedius, G. shedaoensis, indicates that the vertebra has a fairly robust appearance. In G. ussuriensis and Vipera berus have been examined. the dorsal view, the anterior edge of the zygosphene is con- The relatively slender fossil vertebra do not belong to cave; the prezygapophyseal articular facet is subtriangular; the G. intermedius and G. shedaoensis, which have robust verteb- prezygapophyseal accessory process is at a slight anterior rae. Furthermore, the moderately convexed anterior edge of angle; the distal tip of the prezygapophyseal accessory process the zygosphene of this fossil precludes it from belonging to is pointed; the epizygapophyseal spines are absent. In the G. ussuriensis or Vipera berus, which have a fairly convexed ventral view, the hypapophysis projects beyond the edge of anterior zygosphene edge. Of the two remaining species, the the condyle; the postzygapophyseal articular facet is tetrago- vertebrae of G. brevicaudus more closely resemble the present nal. In the lateral view, part of the neural spine is lost; the fossil vertebra in having a relatively high neural spine and preserved anterior and posterior edges of the spine are direc- straight hypapophyses. ted caudally, indicating its actual further development; the However, in lieu of more materials for comparison, we parapophyseal process is developed and projects obliquely simply identified this fossil vertebra as belonging to downwards; the hypapophysis is long and straight, and the Gloydius sp1. distal tip of the hypapophysis is pointed. In the anterior view, the cotyle is oval and approximately equal in width to the zygosphene; the prezygapophyseal accessory process is barely Gloydius sp2. developed. In the posterior view, the neural arch is relatively (Figure 12) depressed; the condyle oval is much larger than the neural canal. NWUV 1534-1540 have the same morphology and are similar-sized vertebrae. Material Eight precloacal vertebrae from SYZ 2 (NWUV 1533-1540). Remarks All the vertebrae are complete or nearly complete. Specimen NWUV 1533 (Figure 12) is the primary basis for our mor- The fairly robust fossil vertebrae do not belong to phological descriptions. G. brevicaudus, G. ussuriensis and Vipera berus,which have relatively slender vertebrae. Furthermore, the con- caved anterior edge of the zygosphene of this fossil pre- Description cludes it from belonging to G. cognatus,whichhas NWUV 1533 is an almost complete mid-trunk vertebra. The a convexed anterior zygosphene edge. Of the two remain- prezygapophyseal accessory process is lost on both sides, and ing species, the vertebrae of G. intermedius more closely most of the neural spine, part of the left postzygapophyseal resemble the present fossil in having a robust centrum and articular facet and the left synapophyses are absent as well. CL long and straight hypapophyses. HISTORICAL BIOLOGY 11

Figure 12. Trunk vertebra of Gloydius sp2. (NWUV 1533). (a) – lateral view, (b) – anterior view, (c) – posterior view, (d) – dorsal view, (e) – ventral view. Scale bar = 2 mm.

In lieu of more materials for comparison, we simply iden- late Pleistocene are likely to have been contemporaneous tified these fossil vertebrae as belonging to Gloydius sp2. with slightly cooler climatic conditions than those occurring at present in the area. In future studies, we need to create a more comprehensive Discussion and conclusion skeletal collection of snake species living today to further The site of Shanyangzhai Cave, dating from approximately identify fossil specimens. At the same time, more findings 270 ka to 22 ka, furnished the following snakes: Elaphe cf. in other fossil localities of North China are needed to give schrenckii, Elaphe cf. dione, Lycodon sp., Rhabdophis tigrinus, a more precise picture of the paleoecological and paleobio- Gloydius sp1. and Gloydius sp2. These taxa represent the first geographical changes that occurred during the Pleistocene. snake fauna described in any detail in North China, as well as the first fossil record for Viperidae snakes in China. Hence, Acknowledgments the snakes of Shanyangzhai Cave provide a good opportunity to improve our understanding of Pleistocene fossil snakes in This study was aided by the permission to observe modern comparative the region. Because of the limited number of species that have skeletons under the care of Liu Jun, Yi Hong-yu, Shi Jing-song and Li been identified and the lack of comparative fauna from the Dong-sheng of the Institute of Vertebrate Palaeontology and vicinity, a detailed paleoecological and paleobiogeographical Paleoanthropology. Gong Hu-jun, Wang Wei, Zhao Hong-wei and Ben Gui-yun coordinated and implemented the fieldwork. analysis based on the snake fauna of SYZ 2 is not possible yet, but in SYZ 4, preliminary results could be drawn by compar- ison with recent fauna. Disclosure statement Of the six snake taxa that we report here, two still occur No potential conflict of interest was reported by the authors. in the study area: Elaphe dione and Rhabdophis tigrinus. Another taxon, Elaphe schrenckii, now has a northern and eastern distribution. Elaphe dione today ranges from Funding UkrainetothePacific Ocean, including a large part of the temperate region on the Asia continent. The relatively National Natural Science Foundation of China [41372020,41472013]. broad ecological niches of these snakes making it difficult to use their fossils to reflect the paleoenvironment. The References continuous area of Rhabdophis tigrinus today covers most ff of East Asia (except the western part), and these snakes Au enberg W. 1963. The fossil snakes of Florida. Tulane Stud Zool. 10 (3):131–216. inhabit fairly moist biotopes. In China, Elaphe schrenckii is Bailon S. 1991. Amphibiens et reptiles du Pliocène et du Quaternaire de currently only distributed in Heilongjiang Province, Jilin France et d’Espagne: mise en place et évolution des faunes [Pliocene Province and the eastern part of Liaoning Province. and quaternary amphibians and reptiles from France and Spain: Today,theseareashaveacoolerandmoisterenvironment establishment and evolution of faunas] [dissertation]. Paris: Univ. than the research region. Therefore, the snake fauna in the Paris VII, Paris. French. 12 Y. CHEN ET AL.

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Natricinae 堆积的时代与环境 [Formation period and environment of spe- Hebius vibakari: OV2319 leothem in the Liujiang Basin inferred from the Shanyangzhai mam- Rhabdophis tigrinus: OV2310 – mal fossils]. Mar Geol Quat Geol. 23(2): 117 122. Chinese. Elapidae Otsuka H. 2002. [Paleovertebrate fauna of the Ryukyu Archipelago and Hydrophiinae its origin]. The Formation of the Ryukyu Arc and Migration of Biota Hydrophis cyanocinctus: OV2343 – to the Arc. Okinawa Times (Naha): Japanese. 111 127 Laticauda semifasciata: OV2335 fi Ratnikov VY. 2004. Identi cation of some Eurasian species of Elaphe Viperidae (Colubridae, Serpentes) on the basis of vertebrae. Russ J Herpetol. 11 Crotalinae – (2):91 98. 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Part I: Scolecophidia, Boidae, Colubridae – – Colubrinae. Estud Geol. 47(1 2):103 126. Colubrinae Szyndlar Z. 1991b. A review of Neogene and Quaternary snakes of Boiga kraepelini: OV2692 central and eastern Europe. Part II: Natricinae, Elapidae, Viperidae. Boiga dendrophila: OV2306 – – Estud Geol. 47(3 4):237 266. Elaphe moellendorffi: OV2686 Venczel M. 2000. Quaternary snakes from Bihor (Romania). Oradea: Gonyosoma boulengeri: OV2322 Ţă ş Editura Muzeului rii Cri urilor. Gonyosoma frenata: OV2301 河北秦皇岛山羊寨哺乳动物群中的兔科动物化石 Wang W. 2009. Lycodon flavozonatus: OV2682 [Leporidae fossils from Shangyangzhai mammal fauna Lycodon ruhstrati: OV2323 ’ ’ (Qinhuangdao, Hebei Province)] [master s thesis]. Xi an, Northwest Oreocryptophis: OV2299 University. Chinese. Ptyas mucosa: OV2291 秦皇岛山羊寨第 地点中更新世动物群中的仓鼠化石 Xie K. 2017. 2 Ptyas major: OV2500 [Middle Plesitocene hamster fossils from Locality 2 of Shanyangzhai Natricinae ’ ’ in Qinhuangdao area, China] [master s thesis]. Xi an: Northwest Enhydris plumbea: OV2313 University. Chinese. Macropisthodon rudis: OV2689 HISTORICAL BIOLOGY 13

Rhabdophis subminiatus: OV2684 Crotalinae Sinonatrix annularis: OV2320 Deinagkistrodon acutus: OV2346 Elapidae Ovophis zayuensis: OV2677 Elapinae Protobothrops jerdonii: OV2349 Bungaurs fasciantus: OV2325 Protobothrops mucrosquamatus: OV2347 Bungaurs multicinctus: OV2326 Protobothrops mangshanensis: OV2348 Naja atra: OV2330 Trimeresurus stejnegeri: OV2351 Naja kaouthia: OV2332 Viperinae Ophiophagus hannah: OV2334 Daboia siamensis: OV2364 Viperidae