Herpetology Notes, volume 12: 519-521 (2019) (published online on 25 May 2019)

First report of a possible hybrid between Gloydius brevicaudus Stejneger 1907 and G. intermedius Strauch 1868 (; )

Min Seock Do 1, Kyo Soung Koo 2,*, and Jae Young Song3

Hybridization occurs not only between closely with a unique morphology that featured various related but also distantly related (Schilde characteristics that are typically attributed to either et al., 2004; LeClere et al., 2012; Koo et al., 2014; Gloydius brevicaudus or G. intermedius whereas other Rubtsov, 2015). The genetic transformation and characters were of an intermediate state between the mix due to hybridization are important phenomena two species (Fig. 2, Table 1), and we suspect it to for understanding the speciation and evolution of be a hybrid between these species. Body length of organisms (Mallet et al., 2016). There are examples the was approximately 53 cm and the dorsal for species belonging to the family Viperidae that colour was light brown. The snake had 22 scale rows frequently hybridize in contact zones, and various around mid-body. There were 32 circular patterns with studies have been conducted in Europe focusing on dark brown, typical for G. brevicaudus (Fig. 2A, B). the role of geography and the morphological and Moreover, it had a longitudinal line along the centre of genetical effects of hybridization (Martínez-Freiría et al., 2010; Tarroso et al., 2014; Guiller et al., 2017). The three viper species inhabiting the Korean Peninsula differ from each other in morphology, distribution, and ecology (Lee et al., 2011; Do, 2018). A recent study based on species distribution models predicted that interspecific contact could be expected to occur frequently in the Taebaek Mountains (Do et al., 2016). Herein, we report a possible case of hybridization between two Gloydius species in South . Field work was conducted in Sobaeksan National Park which is located across Chungcheongbuk-do and Gyeongsangbuk-do (37.0167°N, 128.5892°E, 750 m a.s.l.). Species living in the park are protected by the government. Sobaeksan is a representative mountain of the Taebaek Mountains in (Fig. 1). On August 4, 2016, we observed a snake individual

1 Department of Biology, Kyung Hee University, Seoul 02453, South Korea. 2 Research Center of Ecomimetics, Chonnam National University, Gwangju 61186, South Korea. 3 National Park Research Institute, 87-10, Jinmaeul-gil, Figure 1. Location of the observation site (red star) of the Heuksan-myeon, Sinan-Gun, 58863, South Korea. possible hybrid individual between Gloydius brevicaudus and * Corresponding author. E-mail: [email protected] G. intermedius in Sobaeksan National Park, South Korea. 520 Min Seock Do et al.

Figure 2. Body (top row) and head (bottom row) of Gloydius brevicaudus (A, D), G. intermedius (C, F) and a possible hybrid between the two species (B, E).

the back from the head to the tail, which is an important 2B, E). Most of the morphological features of the morphological characteristic of G. brevicaudus (Fig. possible hybrid were similar to G. intermedius, while 2A, B). The tail colour was the same as that of the the clear vertical centre line on the body and the shape body, and the colour of the tongue was black (Fig. of the circular patterns were typical characteristics

Table 1. External body traits of Gloydius brevicaudus, G. intermedius and the suspected hybrid individual. Table 1. External body traits of Gloydius brevicaudus, G. intermedius and the suspected hybrid individual.

G. brevicaudus* G. intermedius* Traits Hybrid individual (n=10) (n=10) Body length (cm) 30–50 53 (approx.) 40–70 No. of dorsal scale row on mid-body 21 or 23 22 22 or 23 No. of circular patterns 32 32 stripes Keeled scales on dorsal scales present present present white background with light brown with dark light brown with dark Body colour black patterns brown patterns brown stripes Tail tip colour yellow same as body colour same as body colour Tongue colour black black black A white line behind eyes present absent absent Line on the two mid-dorsal scales present present absent from head to tail * The data for G. brevicaudus and G. intermedius were taken from Stejneger (1907), Lee et al. (2011), Koo et al (2017).

Possible hybrid between Gloydius brevicaudus and G. intermedius 521 of G. brevicaudus (Table 1). The genetics of the Koo, K.S., Park, S.H., Kim, J.S., Kwon, S., Choi, W.J., Park, snake could not be analysed because the collection I.K., Cho, H.N., Park, J.J., Oh, H.S., Park, D.S. (2017): The and sampling of live organisms are prohibited in the comparison of size and morphology of scales in nine Korean snake species (6 in Colubridae, 3 in Viperidae). Korean Journal Korea National Park. However, the result of analysis of Ecology and Environment 50: 207–215. on the morphological characteristics of the abnormal LeClere, J.B., Hoaglund, E.P., Scharosch, J., Smith, C.E., snake suggests that the observed anomalies were Gamble, T. (2012): Two naturally occurring intergeneric the results of hybridization between G. brevicaudus hybrid (Pituophis catenifer sayi × Pantherophis and G. intermedius. Our observation represents the vulpinus; Lampropeltini, Squamata) from the Midwestern first reported case of a possible hybrid in the United States. Journal of 46: 257–262. Gloydius. Additional sampling and genetic analyses Lee, J.H., Jang, H.J., Suh, J.H. (2011): Ecological guide book of herpetofauna in Korea. National Institute of Environmental are required to confirm that the two species hybridize Research, Incheon, South Korea. in their natural habitats. Mallet, J., Besansky, N., Hahn, M.W. (2016): How reticulated are species?. BioEssays 38: 140–149. Acknowledgement. This study is based on the results of the Martínez-Freiría, F., Lizana, M., do Amaral, J.P., Brito, J.C. “2016 Natural Resources Survey of Sobaeksan National Park” (2010): Spatial and temporal segregation allows coexistence in conducted by Korea National Park Research Institute. a hybrid zone among two Mediterranean vipers (Vipera aspis and V. latastei). Amphibia-Reptilia 31: 195–212. References Rubtsov, A.S. (2015): Reproductive isolation and the notion of species in birds. Biology Bulletin 42: 793–807. Do, M.S. (2018): Ecology of three Korean viper snakes (Gloydius Schilde, M.A.I.K., Barth, D.A.N.A., Fritz, U. (2004): An ussuriensis, G. brevicaudus and G. Ssaxatilis). Unpublished Ocadia sinensis x Cyclemys shanensis hybrid (Testudines: PhD thesis, Kyung Hee University, Seoul, South Korea. Geoemydidae). Asiatic Herpetological Research 10: 120–125. Do, M.S., Lee, J.W., Jang H.J., Kim, D.I., Yoo, J.C. (2016): Stejneger, L. (1907): Herpetology of and adjacent territory. Interspecific competition and spatial ecology of three species Bulletin of the United States National Museum 58: 1–577. of vipers in Korea: an application of ecological niche-based Tarroso, P., Pereira, R.J., Martínez-Freiría, F., Godinho, R., models and GIS. Korean Journal of Environment and Ecology Brito, J.C. (2014): Hybridization at an ecotone: ecological 30: 173–184. and genetic barriers between three Iberian vipers. Molecular Guiller, G., Lourdais, O., Ursenbacher, S. (2017): Hybridization ecology 23: 1108–1123. between a Euro-Siberian (Vipera berus) and a Para- Mediterranean viper (V. aspis) at their contact zone in western France. Journal of Zoology 302: 138–147. Koo, K.S., Han S.H., Oh, H.S. (2014): First report of a hybridization between Caretta caretta and Chelonia mydas from Jeju Island, South Korea. Korean Journal of Environmental Biology 32: 377–381.

Accepted by Maximilian Dehling