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Discovery of new marginal populations Candidate localities were identified using satellite images provided by Google Earth (earth.google.com/web/). We visually examined of a regionally vulnerable , images in a search for woodless and steep slopes of river valleys the Halys (Gloydius halys) with potential rocky outcrops (Fig 1a) which could serve as hibernat- ing sites for the Halys pit viper. We did not rely on GIS tools to re- The Halys pit viper Gloydius halys (Pallas, 1776) is a motely derive vegetation/landscape features of interest, because such identification of rocky outcrops is prone to various biases and of venomous viperid with a range in South might fail (Fitzsimons & Michael 2017). Field surveys of identified (), Northern and Northern . Previous- candidate localities were conducted not only during the season of pit ly, it was believed to have much wider distribution, but at vipers activity (May-September) but also in April and October, by the present, the populations from the Caucasus, Central searching for shed skins near potential hibernating sites. The snake and the Far East are considered separate species (Wagner et sheddings are proven to be a reliable tool for species surveys and al. 2016, Shi et al. 2016). However, new findings greatly ex- identification (e.g. Tsai et al. 2020), and a shed skin of G. halys is easi- panding the known range of the species and in gen- ly distinguishable from the skins of the co-occurring species (Natrix eral are still occurring (Orlov et al. 2018), pointing out the natrix and Vipera berus) by the presence of loreal pits and by scuta- tion features. Because there is no dense vegetation or snow cover in need for further research. The north-western limit of the April and October, it is easier to search for the shed skins. Halys pit viper range is located at the north of Kemerovo Region and the Region (West Siberia, Russia) During the fieldwork in 2016-2020, we visited a number (Kuranova et al. 2010). Here, the populations are sporadic of locations in the valleys of the rivers Berd, Karakan, and isolated from the main range. They are associated with Verkhniy Karakan, Ik, Inya and Izdrevaya. The specimens of steep slopes of river valleys with rocky outcrops and patches G. halys and/or shed skins were found in three new loca- of mountain steppe vegetation, surrounded by forests and tions (Fig 1d). In May 13, 2016 five individuals (2 adults, 1 meadows. The currently known populations occur in the subadult, 2 juveniles) of Halys pit viper were found in Kara- valleys of the rivers Tom (Kemerovo Region) and Berd (No- kan river valley, 3 km north-west of Rozhdestvenka village vosibirsk Region). These populations are considered as rel- (54.3978° N, 82.3914° E, 150 m a.s.l.), 100 km to the west from icts of the Holocene climatic optimum, which was character- the previously known population in Berd river valley. In ized by a warmer climate in comparison to the present. Ap- April 23, 2019 we found a shed skin of G. halys near the parently, during that time G. halys occupied a wider range, rocky outcrops in Verkhniy Karakan river valley, 15 km to which shrank with the subsequent climate cooling and hu- the south from the locality described above (54.2680° N, midification that started about 5 000 years ago (Quante 82.4473° E, 190 m a.s.l.). In October 23, 2019 another shed 2010), leaving small populations in limited habitats with skin was found near the rocky outcrops on steep slopes of preserved appropriate microclimatic conditions. This hy- Inya river valley (Fig 1c), and in May 13, 2020 an adult pit pothesis is supported by population genetics data (Simonov viper was found at the same location (55.3081° N 84.1205° E, & Wink 2012). Similar relict populations are known for a 154 m a.s.l.). This population is located 70 km south-west number of temperate snake species in Europe, Asia and from the nearest known population in Tom river valley (e.g. Joger et al. 2010, Somers et al. 2017). (Kemerovo Region), and 77 km north from the population in In Novosibirsk Region, this species had not been discov- Berd river valley. ered until 2002 (Pestov 2003) in spite of herpetological re- Thus, the distribution of G. halys in the region is much search conducted in the region, due to its very limited areas wider than previously thought. It is quite probable that the of occurrence. The ecology, origin and genetics of this popu- species could be found in other locations with appropriate lation have been extensively studied in the following years habitat conditions. Moreover, the places which we surveyed (e.g. Simonov & Wink 2011, 2012; Simonov & Zinchenko and found no pit vipers should be considered for further 2010). Halys pit viper is redlisted in Novosibirsk Region as a surveys as well, since our searches were not systematic and vulnerable species due to its limited distribution and habitat cannot prove species absence. Our findings are also of medi- availability. However, no special efforts have been conduct- cal importance: according to Shikalova et al. (2019) in 2011- ed to investigate the presence of this species in other parts of 2017 snake bite envenomation were registered in 11±2 pa- the region. tients per year on average in Regional Toxicological Center While examining zoological collections of the Faculty of of Novosibirsk (this most probably does not fully reflect the Natural Sciences of the Novosibirsk State University, we real number of cases). To the best of our knowledge, all these found two specimens of G. halys labelled as “Karakan river cases were treated as an envenomation by the most common valley, 1986”, collector unknown. These specimens were ap- snake species in the region – the common adder V. berus. We parently collected during biology students’ fieldwork. That found the Halys pit viper in the administrative districts year, the fieldwork was held near the village Rozhdestvenka where it was not recorded previously, and importantly, the (Dr. Prof. M.G. Sergeev, pers. comm.). This village is in 100 species occupies some sites attractive to local people as rec- km west from the nearest known location inhabited by G. reation sites, increasing the probability of snake bite acci- halys in the Berd river valley. Apparently, this is the earliest dents with pit vipers. The local clinical toxicologists must be record of G. halys in the Novosibirsk Region. However, at the aware of such possibility and avoid using the V. berus anti- time the importance of the find was not recognized, and it venom (which is available in Novosibirsk Region) in case if has never been published. This finding motivated us to carry there is a probability of pit viper envenomation. out field studies to validate the locality of specimens found The rediscovered locality in Karakan river valley is the in the collection and to explore previously unstudied parts westernmost known population of the species, advancing of the region potentially suitable for G. halys. the known north-western range limits of the Halys pit viper

150 North-Western Journal of Zoology 2021, vol.17 (1) - Correspondence: Notes

Figure 1. A – example of a satellite imagery of G. halys habitat (Inya river valley) (Google, Maxar Technologies), B – G. halys habitat in In- ya river valley (photo by authors), C – adult female G. halys encountered in Karakan river valley (photo by authors), D – occurrence of G. halys in north-western part of its range, new records depicted as red triangles. Major rivers (in blue) and regional borders (in white) are shown.

100 km west, close to the river . It is highly unlikely that Orlov, N.L., Boeskorov, G.G., Protopopov, S.G., Nogovitsyn, P.R., G. halys occurs west of the Ob river since the landscapes to Kolodeznikov, V.E., Shchelchkova, M. V., Kropachev, I. (2018): New records and taxonomic position of snakes of the genus Gloydius Hoge et Romano- the west of the river represent a very flat plain covered by Hoge, 1983 (Crotalinae, , Ophidia, Reptilia) in the Republic of grassland with small forest patches and lack river valleys Sakha (Yakutia), with comments on their distribution in the Eastern Siberia with steep or rocky slopes. Notably, the Ob river in this area and the Far East. Russian Journal of 25(4): 275–282. Pestov, M.V. (2003): [Halys pit viper – the new species of Novosibirsk region fauna.] serves as a biogeographical border for some other rare spe- pp.35-38. In: [Amphibians and in West Siberia]. “Revi-K” Press, cies often co-occurring with G. halys, such as forest-steppe Novosibirsk. [in Russian] marmot Marmota kastschenkoi Stroganov et Yudin, 1956 Quante, M. (2010): The changing climate: past, present, future. pp.9-56. In: Hebel, J.C., Assmann, T. (eds.), Relict Species: Phylogeography and (Brandler 2003). Two out of three populations were first dis- Conservation Biology. Springer-Verlag, Berlin, Heidelberg. covered by shed skins and out of the pit vipers activity sea- Shi J.-S., Yang D.-W., Zhang W.Y., Qi S., Li P.P., Ding L. (2016): [Distribution and son, once again underlining the usefulness of such approach, Infraspecies of Gloydius halys-Gloydius intermedius Complex in China (Serpentes: Crotalinae)]. Chinese Journal of Zoology 51(5): 777–798. [in especially for rare and elusive snake species. Chinese] Shikalova, I.A., Lodyagin, A.N., Barsukova, I.M., Nasibullina, A.R., Kalloyda, Acknowledgement. We thank Dr. Prof. Mikhail Sergeev and Dr. D.Y. (2020): The Analysis of Toxicological Situation According to Three Natalia Baturina for granting access to the zoological collections of Specialized Centers of Russian Federation. Russian Sklifosovsky Journal the Novosibirsk State University. “Emergency Medical Care” 8(4): 373–378. Simonov, E., Wink, M. (2011): Cross-amplification of microsatellite loci reveals multiple paternity in Halys pit viper (Gloydius halys). Acta Herpetologica References 6(2): 289–295. Brandler, O.V. (2003): [On species status of the forest-steppe marmot Marmota Simonov, E., Wink, M. (2012): Population genetics of the Halys pit viper kastschenkoi (Rodentia, Marmotinae)]. Zoologicheskii Zhurnal 82(12): 1498– (Gloydius halys) at the northern distribution limit in Siberia. Amphibia- 1505. [in Russian] Reptilia 33(2): 273–283. Fitzsimons, J.A., Michael, D.R. (2017): Rocky outcrops: A hard road in the Simonov, E., Zinchenko, V. (2010): Intensive infestation of Siberian pit-viper, conservation of critical habitats. Biological Conservation 211: 36–44. Gloydius halys halys by the common snake mite, Ophionyssus natricis. North- Joger, U., Fritz, U., Guicking, D., Kalyabina-Hauf, S., Nagy, T.T., Wink, M. Western Journal of Zoology 6(1): 134–137. (2010): Relict populations and endemic clades in Palaearctic reptiles: Somers, C.M., Graham, C.F., Martino, J.A., Frasier, T.R., Lance, S.L., Gardiner, evolutionary history and implications for conservation. pp.119-143. In: L.E., Poulin, R.G. (2017): Conservation genetics of the eastern yellow-bellied Hebel, J.C., Assmann, T. (eds.), Relict Species: Phylogeography and racer (Coluber constrictor flaviventris) and bullsnake (Pituophis catenifer sayi): Conservation Biology. Springer-Verlag, Berlin, Heidelberg. River valleys are critical features for snakes at northern range limits. PLoS Kuranova, V.N., Simonov, E.P., Yartsev, V.V., Shamgunova, R.R., Starikov, V.P. ONE 12(11): 1–14. (2010): [Diversity, distribution and conservation status of reptiles of West Siberia.] Tsai T.S., Wang S.-H., Mao J.J., Chan Y.Y., Lee Y.J., Fan Z.Y., Hung K.H., Wu pp.116-147. In: Duysebaeva T.N. (ed.), [Herpetological studies in Y.H., Tseng Y., Lin T.E. (2020): Species identification of shed snake skins by and adjacent countries.] АСБК – СОПК, Almaty. [in Russian] scanning electron microscopy, with verification of intraspecific variations North-Western Journal of Zoology 2021, vol.17 (1) - Correspondence: Notes 151

and phylogenetic comparative analyses of microdermatoglyphics. Snake species’ foraging strategy lie along a continuum of Herpetological Monographs 34 (1): 178–207. tactics, but most species are sit-and-wait or actively foraging Wagner, P., Tiutenko, A., Mazepa, G., Borkin, L.J., Simonov, E. (2016): Alai! Alai! – a new species of the Gloydius halys (Pallas, 1776) complex (Viperidae, predators (Huey & Pianka 1981, Cundall & Greene 2000, Crotalinae), including a brief review of the complex. Amphibia-Reptilia Glaudas et al. 2019). Active foraging is more energy- 37(1): 15–31. demanding, but also results in capturing more prey per unit

Key words: Crotalinae, range, Reptilia, Siberia, Viperidae. of time. Many snake species accept dead prey in captivity (e.g., Rossi 1992). Scavenging behaviour, as an opportunistic Article No.: e217501 feeding strategy, has also been observed in several snake Received: 22. January 2021 / Accepted: 02. March 2021 species, however there are few studies on snake scavenging, Available online: 10. March 2021 / Printed: June 2021 making this form of feeding quite neglected (Devault & Evgeniy SIMONOV1,*, Lada LISACHOVA1 Krochmal 2002). and Artem LISACHOV1,2 In this work, we present an observation on scavenging behaviour of the Nose-horned Viper Vipera ammodytes (Lin- 1. Institute of Environmental and Agricultural Biology (X-BIO), University of naeus 1758). Tyumen, Lenina str. 25, 625003 Tyumen, Russia. 2. Institute of Cytology and Genetics SB RAS, Lavrentyeva str. 10, 630090 No- vosibirsk, Russia. We were monitoring the effects of traffic on the populations of am- Corresponding author, E. Simonov, E-mail: [email protected] phibians and reptiles on the road in the canyon of Derventa river in the National park of Tara in Serbia (N 43.956734, E 19.355375). We surveyed the road for roadkills on foot, in July 2019.

On 29 July 2019, around 17:30, we found a freshly roadkilled Scavenging behaviour in the Nose-Horned subadult individual Vipera ammodytes (around 35 cm of total Viper Vipera ammodytes (Linnaeus 1758) body length) (Fig. 1 A). Since we needed to check that side of the road on return, we left it on the site of observation. On Diet plays an important role in all aspects of snake life histo- return, around 20:30, we saw another subadult individual V. ry such as growth rate, survival rate, reproduction and activ- ammodytes (around 45 cm of total body length) eating this ity patterns (Luiselli et al. 1996, Naulleau & Bonnet 1996, roadkilled individual (Fig. 1 B). We observed the viper Shine & Madsen 1997, Madsen & Shine 2000, Lourdais et al. without disturbing it. V. ammodytes swallowed the other half 2002). Examination of diet composition is important for nu- of its prey in about 10 minutes, after that it left the road. merous reasons such as for understanding the flow of matter The prey spectrum of Vipera ammodytes consists of liz- and energy in an ecosystem, as well as for the conservation ards and rodents, and occasionally birds, centipedes, snakes of the species (Maritz et al. 2016). Studies in vivo are one of and frogs (Clark 1967, Beškov 1977, Beshkov & Dushkov the widely used methods for analysing snake diet, both by 1981, Biella 1983, Luiselli 1996, Arsovski et al. 2014, Laing natural observations, or caused defecation or regurgitation 2020). This medium-sized is a sit-and-wait of snake’s food after the snakes are captured. For secretive predator, with a small home range (Kreiner 2007, Plasinger such as snakes, analysis of their diet is a big chal- et al. 2014, Dyugmedzhiev et al. 2020) and scavenging be- lenge, and due to their lifestyle and infrequent feeding, it usually requires many years of field research. Dissection of museum specimens is another common method for as- Figure 1. Roadkilled individual Vipera ammodytes (A) and scavenging sessing dietary preferences of reptiles (Glaudas et al. 2017). behaviour of another individual of the species (B). Both of these methods have drawbacks (Luiselli & Amori haviour in this species has not been previously reported. 2016). By examining the stomach contents from museum According to the theory of optimal foraging (MacArthur specimens, it cannot be verified whether digested material & Pianka 1966), a predator will select prey when the profits comes from freshly killed prey or a carcass (Devault & of eating it exceed the costs (Pyke et al. 1977). Nutrition the- Krochmal 2002). The stomach contents are rarely in good ory predicts that individuals will eat the most abundant prey condition, making it difficult to examine information such as or one that requires less energy to swallow or digest prey size, ingestion and digestion time. Duration of swal- (Schoener 1971, Capizzi et al. 1995). Carcasses are good and lowing and digestion, as well as prey type can greatly affect easily accessible food for many animals, including snakes the behaviour of snakes; e.g. longer duration of swallowing (review in Devault & Krochmal 2002). In this case, the Nose- and large prey size in the abdomen reduce locomotive abili- horned Viper was probably attracted by carcass smell. An- ties and snakes might easily become prey themselves, or be other explanation may be the fact that at this locality Vipera roadkilled (Siers et al. 2018). ammodytes often cross the road (several live or dead individ- It is almost impossible to gather comprehensive infor- uals have been observed), although it is a sit-and-wait preda- mation about the diet and hunting methods of predator spe- tor. It is known that chemical cues are important for scav- cies by only conducting a series of field studies. If the species enging behaviour in snakes, notably in the groups Natrici- is predominantly diurnal, its nocturnal activities are usually nae and Viperidae, which rely heavily on chemical signals in accidentally observed; if the species is sedentary and an am- prey detection (Shivik et al. 2000, Devault & Krochmal 2002). bush predator, its mobility and potential other hunting strat- It is a particularly interesting fact that Nose-horned Viper egies are hard to record. For a comprehensive analysis on scavanges a conspecific individual, although cannibalism feeding behaviour, it is necessary to monitor individuals in has been reported in this species (Beshkov & Dushkov 1981), the wild for 24 hours via video cameras (Clark 2006, Clark et but this viper did not kill its prey. The observed scavenging al. 2012).