Contribution to the knowledge of distribution of Colubrid snakes in Serbia

Detailed distribution pattern of colubrid snakes in Serbia is still inadequately described, despite the long historical study. In this paper, we provide accurate distribution of seven species, with previously published and newly accumulated faunistic records compiled. Comparative analysis of faunas among all Balkan countries showed that Serbian colubrid fauna is among the most distinct (together with faunas of Slovenia and Romania), due to small number of species. Zoogeographic analysis showed high chorotype diversity of Serbian colubrids: seven species belong to six chorotypes. South-eastern Serbia (Pčinja River valley) is characterized by the presence of all colubrid species inhabiting our country, and deserves the highest conservation status at the national level. This study should provide the basis for further, more comprehensive faunistic research, as the data on distribution of colubrid species in our country are far from complete, with large distribution “gaps”, especially in northern and central parts of Serbia.


Introduction
A growing body of evidence suggests that many reptile species are endangered worldwide (Böhm et al. 2013), and that many populations are declining (reviews in Gibbons et al. 2000;Reading et al. 2010;Sinervo et al. 2010;Ihlow et al. 2012).Given the fact that the first step, preceding the studies of e.g.systematics, ecology and biogeography, is the comprehensive knowledge of biodiversity of the certain region, faunistic studies are of growing importance, especially in the regions or countries with incomplete species distribution data (Margules et al. 2002;Jelić et al. 2013;Vukov et al. 2013;Sterijovski et al. 2014;Tomović et al. 2014).Concerning conservation biology, detailed faunistic studies provide essential data for identification of biodiversity "hotspots" i.e. areas with exceptional species assemblages, high levels of endemicity and/or areas under significant threats (Gaston et al. 2002).

Research Article
Concerning the reptile fauna, the Balkan Peninsula is recognized as one of the richest biodiversity hotspots in Europe (Gaston & David 1994;Džukić 1995;Médail & Quézel 1999;Džukić & Kalezić 2004).This partly results from its role as an important Pleistocene glacial refugium and a source for subsequent recolonisations of Europe (e.g.Džukić & Kalezić 2004;Ursenbacher et al. 2008;Gvoždík et al. 2010).Being situated in the central part of the Balkans, Serbia is a very important territory for diversity of reptiles, due to the occurrence of various biogeographical phenomena: presence of the Balkan endemic species and relicts, different faunal elements, marginality of certain species' ranges and presence of peripheral populations, as well as range fragmentation (Matvejev 1961;Džukić 1974Džukić , 1980Džukić , 1995;;Džukić & Kalezić 2004;Vukov et al. 2013).
The most recent comprehensive faunistic study of Tomović et al. (2014) is the first publication which presents general distribution and diversity patterns of reptiles in Serbia.However, this study provided only approximative maps of real and potential distributions, without exact locality data or UTM coordinates.
Unpublished distributional data on colubrid species collected in the past decades substantially exceed those from literature sources.Complete presentation of both new records and literature data will enable more comprehensive analyses of distribution pattern, faunal diversity and conservation priorities of the colubrid species in Serbia.Thus, the aims of this study were: 1) to publish a complete dataset of distribution records of all colubrid species in Serbia, with published and new distribution data compiled, 2) provide standardized 10 x 10 UTM maps of all existing distribution data, 3) to analyse patterns of chorotype diversity of colubrids in Serbia, and 4) to compare species diversity of Serbia with regional faunas.

Study group
The snake family Colubridae comprises more than 1,800 species (Pough et al. 2004).It is the most widespread (occurs on all continents except the Antarctica), diverse, and species-rich family within the Ophidia suborder.Members of the colubrid family are relatively large, diurnal and heliothermic snakes (at least in the temperate zone); thus they are usually easily visible.In regions with moderate climate, colubrids hibernate through the cold period of the year.The Balkan Peninsula is inhabited by 17 species of colubrids (Gasc et al. 1997;Sillero et al. 2014).

Study area
Territory of Serbia includes three distinct altitudinal regions -(1) parts of the Pannonian plain in the north (0 -200 m a.s.l.), (2) the Peripannonian lowlands and hills parallel with southern banks of the Sava and Danube rivers, and those along the Velika Morava River valley (200 -600 m a.s.l.), and (3) the Mountain-valley region (600 -2,650 m a.s.l.) (Marković 1970).The Pannonian parts of Serbia are under the continental climate with cold winters and very hot and dry summers.The Peripannonian region is characterized by moderate continental climate.Alpine climate is dominant in mountainous regions above 800 m a.s.l.Sub-Mediterranean climate is present in southern and south-eastern regions, as well as in Kosovo and Metohija; canyons and gorges often have certain climatic peculiarities which make them important refugial habitats (Radovanović & Mijović 2005).

Methods
The species were identified according to standard herpetological literature, by visual inspection of the diagnostic characters on specimens from scientific collections, voucher photos, or directly in the field (Arnold & Ovenden 2002).Regarding taxonomy and current nomenclature, we referred to the work of Speybroeck et al. (2010).
This study was based on the species' occurrence records from different sources: (1) Natural History Museum in Vienna, (2) Hungarian Natural History Museum in Budapest, (3) Students' research organization "Josif Pančić" in Belgrade, (4) Research center "Petnica", (5) authors' field observations, and (6) field data which were kindly donated by our colleagues (see Acknowledgements).We also used data from field herpetology websites (www.bioras.petnica.rsand http://en.balcanica.info)collected by amateur herpetologists and confirmed by experts.When using data from Internet, we complied with terms and conditions of websites, and asked site administrators and contributors for permissions to cite entries.All available records were mapped in the 10 x 10 km UTM (Universal Transverse Mercator) geographic coordinate grid system.Since there have never been systematic efforts to cover the entire territory of Serbia by faunistic investigations, our dataset is still rather patchy hence the lack of data from certain areas does not necessarily imply the absence of species.

Distribution of colubrid species in Serbia
The list of colubrids which inhabit the territory of Serbia includes seven species.Three of the Serbian species are within marginal zones of their overall distributional ranges, and one exhibits range fragmentation (Table 1).Four species are distributed throughout the country -N.natrix, N. tessellata, C. austriaca and Z. longissimus (Fig. 2).One relatively rare species, D. caspius, is related to steppe and forest-steppe habitats, and occupies less than 50% of the Serbian territory (Fig. 3).There are few records for this species in the south-western part; these are, however, doubtful, due to unsuitable climate and habitats in this part of the country; these should be checked for confirmation.Extremely rare species occupy less than 5% of Serbian territory: few locations in the extreme south-east, with sub-Mediterranean climate (P.najadum and E. quatuorlineata) (Fig. 3).For every species, new records in Serbia (with region, broad location, exact locality, UTM coordinates and name of the person who provided data) are given in Appendix I. Data from the literature and Internet sources (with region, broad location, exact locality (when available), UTM coordinates and reference) are presented in Appendix II.

Patterns of colubrid chorology and faunal similarity
Chorotype diversity of Serbian colubrids is very high.Seven species are classified into six chorotypes, with only two being together in the Eastern-Mediterranean type (D. caspius and E. quatuorlineata) (Table 1).
Concerning regional similarity of colubrid fauna in Serbia, majority of regions are identical regarding the composition of species.Exceptions are north-western and western parts where D. caspius does not exist, as well as south-eastern part of our country, where P. najadum and E. quatuorlineata occur exclusively (Table 2).
According to the Bray-Curtis dissimilarity index, Serbian colubrid fauna belongs to group of faunas with the smallest number of colubrid species in the Balkans, together with the Slovenian and Romanian.Faunas of Montenegro, Macedonia, Albania, Croatia and Bosnia and Herzegovina form the most closely related cluster.Colubrids of Bulgaria and especially of Greece seem to be more distinct, owing to large number of species and/or due to the presence of particular species (Fig. 4).

Discussion
Two species widely distributed in Serbia, N. natrix and N. tessellata, show uniform occurrence, determined by the presence of various aquatic habitats, from lowlands to high mountains.The new faunistic data of these species largely expand their known distribution in our country (see Fig. 2).Presence of gaps in distribution reflects rather the lack of faunistic research in particular regions, than the actual absence of the species.The other two wide-ranging species (C.austriaca and Z. longissimus) are also present in all three altitudinal regions (Pannonian, Peripannonian and Mountain-valley), but with considerably smaller numbers of records in the Pannonian part (see Fig. 2).Their distribution north of the Sava and Danube rivers appears more concentrated around the Fruška gora and Vršački breg mountains, as well as along the valleys of large lowland rivers (Danube, Sava, Tisa).This pattern could be related to insufficient faunistic research, but could also result from the inexistence of suitable habitats, due to intensive anthropogenic influences (intensive agriculture and deforestation) in the largest part of the Vojvodina province.Distribution gaps in the Peripannonian and Mountain-valley regions most probably result from the lack of systematic faunistic research, as suitable habitats for these two species are wide-spread in these parts of our country.Dolichophis caspius has a very fragmented and relatively limited range in our country (Fig. 3).According to general herpetological literature (Szczerbak 1997;Arnold & Ovenden 2002), distribution of this species consists of relatively "compact" part which reaches its north-western limits in the central part of Serbia, with few isolated populations in Croatia and Hungary, and in northern parts of Serbia.Similarly to two wide-ranging species (C.austriaca and Z. longissimus), in the Pannonian part of Serbia D. caspius is concentrated around the Fruška gora Mt., Deliblatska peščara Sands, as well as along the valleys of large lowland rivers (Danube, Sava, Tisa).There is also a substantial number of new locality records for this species in the Peripannonian and Mountain-valley parts of our country, which considerably extend the previously known range of D. caspius and spread its known distribution limit further to the west (see Fig. 3).The Caspian whip snake is associated with open steppe and forest-steppe habitats (Arnold & Ovenden 2002).The most probable reason for its current distribution pattern is the lack of suitable habitats caused by alterations of original steppes and forest-steppes into agricultural fields.The new data imply that more populations of this species could be discovered in the remaining suitable steppe fragments in Serbia.This snake should be of special conservation interest because its range is highly fragmented, and the protection of its remaining known habitats in our country should be of high priority.Bearing in mind specific features of these habitats, we assume that numerous other wildlife species could benefit from their protection.
Two colubrid species (P.najadum and E. quatuorlineata) have extremely restricted distribution, in the south-eastern part of the country (Fig. 3).In addition, both species reach their northern range limits in this part of Serbia (Crnobrnja-Isailović & Aleksić 1999;Ristić et al. 2006;Tomović et al. 2014).The prerequisite for the occurrence of these highly thermophilous species in the given region is the influence of the sub-Mediterranean climate in the Pčinja River valley, where two other Mediterranean reptile species were also recorded: Testudo graeca (Tomović et al. 2004) and Podarcis erhardii (Džukić 1980;Crnobrnja-Isailović & Aleksić 1999).Therefore, the Pčinja River valley should be considered as the colubrid hotspot in Serbia, and must be of the highest conservation priority in our country.
In addition to seven colubrid species recorded in Serbia until now, some other taxa can be expected in the south-eastern and southern regions, as well as in Kosovo and Metohija.Malpolon insignitus, Telescopus fallax and Zamenis situla reach their distribution limits in Macedonia, very close to Serbian border (Sterijovski et al. 2014).East-Mediterranean reptile species are present in the Pčinja River valley, and many of these were only recently discovered (Džukić 1980;Crnobrnja-Isailović & Aleksić 1999;Tomović et al. 2004;Ristić et al. 2006).Thus, we suppose that it is only a matter of time until the official, expert confirmation of the presence of the abovementioned species in the south-eastern or southern parts of Serbia.Hierophis gemonensis reaches its distribution borders in north-eastern Albania, very close to Serbian border (Haxhiu 1998).Since East-Mediterranean reptiles, such as Algyroides nigropunctatus and Mediodactylus kotschyi, are present in the Metohija region (along the Drim River valley and close to the border with Albania - Džukić & Pasuljević 1979;Ajtić & Tomović 2001), we suppose that H. gemonensis could also be found in this region.
Compared to other Balkan countries, Serbian colubrid fauna is among the poorest in number of species (together with Romanian and Slovenian) in the region (Gasc et al. 1997;Sillero et al. 2014).However, this does not make Serbia insignificant concerning colubrid diversity in the Balkans, due to the presence of phenomena of biogeographical and evolutionary significance -chorotype diversity, peripheral populations and range fragmentation (Džukić 1995;Džukić & Kalezić 2004).Occurrence of six different chorotypes highlights the adaptability of the listed species, which is very important for the local biodiversity (Džukić 1995;Džukić et al. 2001;Džukić & Kalezić 2004;Tomović et al. 2014).
Colubrid faunas of Montenegro, Albania and Macedonia form the cluster, containing identical lists of species, while Croatia is characterized by the presence of Hierophis viridiflavus (Gasc et al. 1997).Bulgaria and Greece are distinct from the previous group due to large number of species and the presence of unique Turano-Mediterranean taxa (Dolichophis jugularis, Eirenis modestus, Elaphe sauromates, Hemorrhois nummifer, Platyceps collaris) (Petrov 2007;Valakos et al. 2008).Faunas of Slovenia, Serbia and Romania are the most distant in this comparison, due to smallest numbers of species (Gasc et al. 1997;Krofel et al. 2009).
Bearing in mind that this is the first comprehensive study of the distribution of colubrids in Serbia, the faunistic data presented herein are far from complete.Many parts of Serbia (especially in the north) are still inadequately studied (Tomović et al. 2014).New records of up to four species are to be expected in the southern and south-eastern parts of Serbia, but the general distribution pattern is unlikely to be changed considerably.

Figure 4 .
Figure 4. Cluster diagram of Bray-Curtis similarity Index of colubrid fauna for the Balkan countries.

Table 1 .
Species list of Serbian colubrids with marginality, range fragmentation and chorotype classification.