Winter activity of the snake-eyed lizard Ophisops elegans (Reptilia: Lacertidae) in the northwesternmost part of its range

: There is a lack of information for potential winter activity of the snake-eyed lizard Ophisops elegans in Europe, where it has a limited distribution. To test the hypothesis that this species can be active during the winter months, two locations in Bulgaria were chosen. The visits were conducted in January, February and December 2022 near the village of Meden Buk and in December 2022 above the village of Mezek. A total of 19 individuals of O. elegans were recorded. In addition, we confirmed foraging behaviour based on faecal sample collection. To our knowledge, this is the northernmost record of winter activity in the snake-eyed lizard and the first consecutive observation of year-round activity for this species in Europe

Winter activity in lacertid lizards in temperate zones across Europe is rarely observed. In this area lizards normally are induced to hibernate during winter and show great ability to survive low temperatures (Grenot et al., 2022). In lowlands (up to 500 m a.s.l.) lizards usually hibernate between mid-October to early April, while at higher altitude this period may be prolonged from September to May (Stojanov et al., 2011;Zamora-Camacho et al., 2013) and some species may be active in hot days during this period or can escape earlier from hibernacula (Rugiero, 1995;Vongrej et al., 2008;Piccoli & De Lorenzis, 2018). These assumptions are general for all lacertids in Europe, but indeed there is lack of information for some species, like the snake-eyed lizard Ophisops elegans Ménétries, 1832.
The genus Ophisops Ménétries, 1832 includes at least eleven species, distributed across Southeast Europe, North Africa, the Middle East, and the Indian subcontinent including Sri Lanka (Bozkurt et al., 2022;Uetz et al., 2022). Ophisops elegans is the only European representative of the genus. It occurs from Algeria across North Africa, Asia Minor and Iran to West Pakistan, as well as in Southeast Europe (northeastern Greece, south-eastern Bulgaria, the islands along the Aegean coast, European Turkey and partially in the Caucasus region) (Ananjeva et al., 2006;Stojanov et al., 2011). In Bulgaria, the species has very limited distribution assigned to the easternmost part of the Rhodopes Mts up to 650 m a.s.l. (Tzankov, 2004(Tzankov, , 2015. This area also represents the most north-western part of the species range in general. Here, O. elegans inhabits extremely dry and warm habitats with bare ground, stones and scarce xerophytic vegetation, rare shrubs (Juniperus sp.) and scattered wood (Beshkov & Nanev, 2006;Stojanov et al., 2011).
For the purpose of this study (testing the hypothesis that Ophisops elegans exhibits activity during the winter months) we choose two sites in Bulgaria where the presence of the species was previously known:   January, 11 in February and 7 in December (Table 1; Fig. 3). The body temperature of the captured lizards varied between 20.6 and 34.3°C, and the temperature of the air and substrate (at the place and time of registration of each individual) -between 15.4 and 24.6°C and 16.2 and 26.3°C, respectively. All individuals were registered in the afternoon, between 11:30 and 16:00 h. No other reptile species were observed, with the exception of one juvenile Lacerta viridis (Laurenti, 1768), spotted on January 3 at the site of Meden Buk. The analysis of the contents of the collected fecal samples (from 5 individuals from February and 1 from December) showed the presence of remains from the following invertebrate groups: order Araneae (in 5 individuals), order Opiliones (in 1 The first site was visited three times (January, February and December 2022), and the second -only in December 2022. Individual visits lasted two days, taking into account the following factors: body, air and substrate temperatures (using a digital thermometer with probe -Multi Thermometer, Möller-Therm, with 1.0°C precision) and snout-vent length (SVL) of caught individuals; in several cases, faecal samples were also collected (preserved in ethanol and examined later under a stereomicroscope; for a more detailed description of the methodology see Vacheva & Naumov, 2020).
As a result of the conducted research, a total of 19 Ophisops elegans (8 males, 6 females, 1 indeterminate adult and 4 subadults) were recorded, respectively 1 in Table 1. Data and time of the observation of winter activity in Ophisops elegans in the two sites. Age, sex and snout-vent length (SVL) for each specimen were recorded, as well as temperatures and weather (TB, TA, and TS refer respectively to body, air, and substrate temperature in ºC). n/a n/a n/a n/a Sunny December 29 13:26 Meden Buk ad. M n/a n/a n/a n/a Sunny Our results provide strong evidence of regular activity in all winter months, as well as for foraging during winter. At least half of the captured specimens in February were fed, as well as one captured in December. This finding shows that the Snake-eyed lizards not incidentally emerge from hibernation during hot and sunny winter days, but they continue with their activities such as feeding. A similar type of activity seems to have been proven only for the İzmir Region (the Aegean Coast of Asia Minor, ca. 350 km south of Bulgarian localities), where according to Öktem (1963) it is possible to find O. elegans all the year round, except on rainy or cold days when the temperature is generally below 5ºC. For other parts of the range however (e.g., Central Anatolia and Armenia), the species is known to hibernate from November to March (Darewskĳ & Beutler, 1981 and references therein). There are a number of occasional observations on the winter activity of O. elegans in the more southern parts of its range (e.g. Franzen, 1986 for the southern coast of Asia Minor). Among them, the data given by Özgül et al. (2022)  For some other lacertid species in the temperate zone, winter activity was also documented, e.g.: Podarcis muralis (Laurenti, 1768) (Italy: Rugiero, 1995, Piccoli & De Lorenzis, 2018; Bulgaria: authors' personal data), Darevskia spp. (Turkey: Franzen, 2000), Lacerta viridis (Slovakia: Vongrej et al., 2008), Anatololacerta danfordi (Günther, 1876) (Turkey: Özkan & Bülbül, 2021), etc. Most of these data represent observations only of individuals going outside during warm and sunny days (i.e., basking), while other types of behaviour, such as feeding or breeding, have been observed rarely (e.g., Sahin, 2021). It should be noted that despite the relatively large number of lacertid species that are generally found in the sites we studied (Meden Buk: 4 species according to personal observations; Mezek: 6 species according to Tzankov, 2004), during the winter months of 2022, apart from O. elegans, it was only one specimen of another species observed (a juvenile L. viridis). In all probability, this is due to a significant difference in the temperature requirements of O. elegans compared to the other lacertids in Bulgaria.
In conclusion, it can be stated that in the temperate zone (in the sense of geographical region defined by latitude), Ophisops elegans seems to be active all year round, even in the northernmost parts of its range, as long as they are at low altitude. It is possible that this is only a consequence of more intensive and targeted research (as it is for the Eastern Rhodopes Mts), but in our opinion, it is also possible that the manifestation of year-round activity is a relatively recent phenomenon, reflecting the impact of global warming on O. elegans. Further research with a larger geographic scope is needed to clarify this question.