Herpetology Notes, volume 13: 495-496 (2020) (published online on 25 June 2020)

Notes on the diet of the Tiger Keelback (Rhabdophis tigrinus lateralis), an alleged anuran specialist

Bartosz Borczyk1,* and Iwona Gottfried2

The tiger keelback (Rhabdophis tigrinus [Boie, 1826]) part was in good condition. We determined that the prey is a natricine snake that is widely distributed in the was probably a Wood Lemming (Myopus schisticolor; Japanese islands, eastern Russia, China, North Korea, Rodentia: Arvicolinae) based on the fur colouration South Korea, Taiwan, and Vietnam (Das, 2010). This (adults have a rusty brown patch extending from the species has attracted the attention of scientists because shoulders to the base of the tail), foot size (12.6 mm), of its peculiar defensive adaptations, i.e. the presence hair present only behind the heels and pads, foot shape of nuchal glands with toxic secretions (Hutchinson et with a diagnostic pad pattern (Figure 1), a short and al., 2007). Rhabdophis tigrinus is considered a feeding moderately haired tailed (tail length: 18 mm) (Ognev, specialist that preys on amphibians (Mori and Moriguchi, 1948; Krivoseev, 1984; Wilson et al., 2017). A second 1988; Kadowaki, 1992; Tanaka, 2002; Tanaka and Ota, specimen, a gravid female (SVL 62 cm), contained a 2002; Hirai, 2004; Mori and Vincent, 2008; Mori and freshly ingested stickleback fish (Gasterosteus sp.; total Nagata, 2016) and is often used in studies of snake length: 7.3 cm; body height: 1.6 cm; Figure 1). feeding behaviour as a model frog eater (Mori and Although the feeding habits of tiger keelbacks seem Vincent, 2008); fishes are reported only sporadically to be well studied, all published data come from as an unusual prey (e.g. Hiura, 1976). Here, we report Japanese island populations (Mori and Moriguchi, the first case of R. tigrinus feeding on a mammal and 1988; Kadowaki, 1992; Tanaka and Ota, 2002; Hirai, another case of predation of a fish. 2004; Mori and Vincent, 2008; Mori and Nagata, 2016). Four tiger keelbacks (unnumbered specimens) from The mainland populations have not been seriously the Zoological Institute of the Russian Academy of studied in this respect. Only very general accounts are Sciences were dissected to skeletonise the specimens published in field guides, and they usually contain no for another study. These snakes were collected in literature references (e.g. Das, 2010). Our observations 1978 near the Komarovka River, approximately 60–70 may indicate geographic variation in the feeding habits km north of Vladivostok, eastern Russia. Because of different R. tigrinus populations and point toward the snakes were preserved by drying, they were first the distinctiveness of the mainland form from Japanese rehydrated, and later all soft tissues were removed. populations of this species (Takeuchi et al., 2014). During this process, one of the authors (BB) found Another interesting observation is that the gravid partially digested mammal remains in the stomach of a female had well-developed eggs inside the oviducts and male (snout-vent length [SVL] 43 cm). The rodent had was actively feeding as suggested by the presence of the been ingested head-first. Although the head and anterior stickleback in her stomach. Many female snakes cease part of the prey had already been digested, the posterior feeding when gravid, especially when close to laying eggs. The snakes species has well-developed nuchal glands in their dorsal neck skin, and a highly toxic secretion is released when the snake is attacked. These toxins are ultimately sequestered from toads (Bufo sp.), which are common prey of the snakes in Japan 1 Department of Evolutionary Biology and Conservation of (Hutchinson et al., 2007). Because the sequestered toad Vertebrates, University of Wrocław, ul. Sienkiewicza 21, 50- toxins are provided to the eggs to produce offspring 335 Wrocław, Poland. 2 Department of Behavioral Ecology, University of Wroclaw, ul. with better equipped chemical defences, gravid females Sienkiewicza 21, 50-335 Wrocław. have been reported to pursue toxic toad prey during * Corresponding author. E-mail: [email protected] gestation (Kojima and Mori, 2015). However, based 496 Bartosz Borczyk & Iwona Gottfried

References

Das, I. (2010): A field guide to reptiles of South-East Asia. City, New Holland Publishers, 376 pp. Hirai, T. (2004): Dietary shifts of frog eating snakes in response to seasonal changes in prey availability. Journal of Herpetology 38: 455–460. Hiura I. (1976): A Japanese grass snake (Rhabdophis tigrinus) eating a loach. Nature Study 22: 110 [in Japanese] Hutchinson, D.A., Mori, A., Savitzky, A.H., Burghardt, G.M., Wu, X., Meinwald, J., Schroeder, F.C. (2007): Dietary sequestration of defensive steroids in nuchal glands of the Asian snake Rhabdophis tigrinus. Proceedings of National Academy of Sciences, USA 104: 2265–2270. Kadowaki, S. (1992): Food resource overlap between two sympatric Japanese snakes (Elaphe quadrivirgata and Rhabdophis tigrinus) in the paddy fields. Japanese Journal of Ecology 42: 1–7 [in Japanese, English abstract] Kojima, Y., Mori, A. (2015): Active foraging for toxic prey during gestation in a snake with maternal provisioning of sequestered chemical defences. Proceedings of the Royal Society, Series B 282: 2014–2137. Krivoseev, W.G. (1984): Terrestrial mammals of the Far East of the USSR: A key to the identification. Nauka, Moscow. Mori A. and Moriguchi H. (1988): Food habits of the snakes in Japan: A critical review. The Snake 20: 98–113. Mori, A., Vincent, S.E. (2008): An integrative approach to specialisation: relationships among feeding morphology, mechanics, behaviour, performance and diet in two syntopic snakes. Journal of Zoology 275: 47–56. Figure 1. (Top) Remains of a tickelback (Gasterosteus sp.) Mori, A., Nagata, E. (2016): Relying on a single anuran species: found in the stomach of a gravid female Tiger Keelback feeding ecology of a snake community on Kinkasan Island, (Rhabdophis tigrinus lateralis) (SVL 62 cm). (Bottom) Miyagi Prefecture, Japan. Current Herpetology 35: 106–114. Remains of a wood lemming (Myopus schisticolor) found in Ognev, S.I. (1948): Animals of USSR and adjacent regions. Volume the stomach of a male Tiger Keelback (Rhabdophis tigrinus 7, Animals of eastern Europe and southern Asia. Soviet Academy lateralis) (SVL 43 cm). of Sciences, Leningrad-Moscow, 510–522. (in Russian) Takeuchi, H., Zhu, G.-X., Ding, L., Tang, Y., Ota, H., Mori A., Oh, H.-S., Hikida, T. (2014): Taxonomic validity and phylogeography of the East Eurasian natricine snake, Rhabdophis lateralis on the present example, gravid females appear to not (Berthold, 1859) (Serpentes: Colubridae), as inferred from necessarily distinguish between toxic and non-toxic mitochondrial DNA sequence data. Current Herpetology 33: 148–153. prey when feeding during gestation. Tanaka K. (2002): Foraging behavior of Rhabdophis tigrinus (Serpentes: Colubridae) in a gutter with dense aggregation of Acknowledgements. We thank Konstantin Mil’to and Natalia tadpoles. Current Herpetology 21: 1–8. Ananyeva (ZIN) for making the specimens available for Tanaka, K., Ota, H. (2002): Natural history of two colubrid snakes, dissection and providing a kind reception during a stay (BB) in St. Elaphe quadrivirgata and Rhabdophis tigrinus, on Yakushima Petersburg. Tomasz Gottfried and Stanisław Bury (Jagiellonian Island, southwestern Japan. Amphibia-Reptilia 23: 323–331. University) made valuable comments on an earlier version of the Wilson, D.E., Lacher, T.E., Jr., Mittermeier R.A. (eds) (2017). manuscript. Handbook of the mammals of the world. Volume 7, Rodents II. Lynx Edicions, Barcelona, 1008 pp.

Accepted by Maximilian Dehling