Contribution to the knowledge of distribution and diversity of lacertid lizards in Serbia

In this study, we present updated distributional data for all Serbian lacertids, having taken into account the available previously published information, and the so far unpublished authors’ field records and evidence from other sources. According to our current knowledge, eight lacertid species inhabit Serbia. Analysis of lacertid diversity within the country showed that biogeographic regions with highest species diversity are Metohija (eight species) and Kosovo (seven species). Regions in Serbia are mutually similar concerning lacertid faunas (average Bray-Curtis dissimilarity index is 0.82). Comparative analysis of lacertid faunas among all Balkan countries showed that Serbian lacertid fauna is the most similar to those of Albania and the FYR of Macedonia, and then to faunas of Romania and Bulgaria. Zoogeographic analysis showed that Serbian lacertids belong to three distinct chorotypes, with the East-Mediterranean being the richest (four species). Generally, diversity of lacertids in Serbia is most strongly determined by topographic diversity, habitat heterogeneity, and climatic peculiarities, with the inflow of the sub-Mediterranean climate along several river valleys in the south being especially important. This paper is intended to serve as a basis for further research, since data on distribution of lacertid species in Serbia are far from complete, with large distributional gaps of recorded species and with unconfirmed presence of two species.


Introduction
Gathering data on species distribution in the given region is the primary prequisite for subsequent studies of ecology, biogeography, evolution and systematics. It is also crucial for the assessing conservation priorities Cogălniceanu et al. 2013;Jelić et al. 2013;Vukov et al. 2013;Sterijovski et al. 2014;Tomović et al. 2014). Detailed faunistic studies can help researchers identify biodiversity "hotspots" -areas with exceptional species concentrations, high levels of endemism and/or areas under significant threats (Myers 1988;Gaston et al. 2002). Also, studies of diversity at different taxonomic (hierarchical) levels can provide valuable insights into faunal taxonomic distinctness (Warwick & Clarke 1995;Clarke & Warwick 1999).
The recent study of Tomović et al. (2014) was a breakthrough in Serbian faunistics, since it was the first publication in decades to provide comprehensive distribution and diversity patterns of all Serbian reptile species. However, this study presented only approximative, contour maps of actual and potential species distributions, without exact locality data or geographic positions.
Data concerning Serbian lacertid fauna, which were being collected during the last 50 years but have never been published greatly outnumber those which have been publicized. Their joint presentation and analysis gave us an opportunity for more precise insight in diversity and distribution patterns of Serbian lacertids.
Therefore, the aims of this study were to: (1) publish detailed distribution information concerning lacertids in Serbia, (2) provide standardized, 10 × 10 km UTM grid maps of all available distribution data, and (3) analyse patterns of lacertid diversity in Serbia.

Study group
The lizard family Lacertidae (Oppel 1811) consists of about 280 species and is widely distributed in the Palearctic and Afrotropics (Arnold et al. 2007). The Balkan Peninsula is inhabited by 23 lacertid species (25 if Crete and the nearby islands are considered: Gasc et al. 1997;Arnold et al. 2007;Sillero et al. 2014).
Lacertids are relatively small, diurnal and heliothermic lizards. Their daily pattern of activity varies according to locality and season. It can be unimodal during cold periods of the year or in areas with harsh climate, with a peak at midday. Activity is bimodal in the summer or in places with warm climate, with peaks in the morning and in late afternoon. In areas under temperate climates, lacertids undergo a period of brumation (Arnold 1987).

Study area
The territory of Serbia encompasses three altitudinal regions: (1) parts of the Great Pannonian plain in the Vojvodina province in the north (0-200 m a.s.l.), (2) the Peripannonian lowlands and hills along southern banks of the Sava and Danube rivers and in 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) (Fig. 1). The Mountain-valley region includes the Dinaric mountain chain in the west and south-west, Scardo-Pindic mountains in the south, and the Balkan-Rhodopes mountains in central, eastern and south-eastern parts (Stevanović 1996). The climate of Pannonian parts of Serbia is continental, with cold winters and very hot summers; steppe climate elements are present, with dry summers, in some parts in the north and east. Peripannonian region and low mountains are under temperate continental climate. Alpine climate is dominant in mountainous regions above 800 m a.s.l. Sub-Mediterranean climate is present in the extreme south and south-east. Detailed regional climate analysis indicated that parts of Kosovo, Metohija, southern and south-eastern Serbia are under strong influence of the Mediterranean climate, that frequent alterations of hot and cold air masses were documented in Vojvodina province , and that canyons and gorges are known for climatic peculiarities which makes them important refugial habitats (Radovanović & Mijović 2005).

Methods
All species considered in the present study were identified according to standard herpetological literature, by visual inspection of diagnostic characters on preserved specimens, in voucher photos or in the field (Arnold & Ovenden 2002). In the cases of species with specific habitat requirements (e.g. D. praticola, P. erhardii, P. tauricus, Z. vivipara, etc.) choice of adequate habitats or their fragments was essential for finding and identifying these species (Radovanović 1951;Arnold 1987). Regarding taxonomy and current nomenclature, we followed the work of Arnold et al. (2007).
This study was based on species' occurrence records from several sources. We used about 120 published literature records and more than 2,000 unpublished records, which came from: (1) Naturhistorisches Museum Wien (NMW), (2) authors' field observations, (3) the late prof. Gojko Pasuljević's field data, and (4) field data kindly donated by our colleagues (see Acknowledgements). We also used, to a lesser extent, data from field herpetology websites (www.euroherp.com; http://en.balcanica.info; www.teraristika.org), collected by amateur herpetologists and confirmed by experts, and from the portal dedicated to mapping and monitoring of biological diversity of Serbia (www.bioras.petnica.rs). When using data from the Internet, we complied with terms and conditions of websites, and asked site administrators and contributors for permissions to cite their entries. All the records we obtained were mapped in the 10 × 10 km UTM (Universal Transverse Mercator) geographic coordinate grid system. Since there have never been systematic efforts to survey the entire territory of Serbia, our dataset is still incomplete, but the lack of records of certain species from some areas does not necessarily imply their physical absence. For correct interpretation of our distributional maps, and to avoid sampling bias, we took into consideration other factors, such as relief, climate, and presence/absence of suitable habitats.

Results
The list of lacertids that inhabit the territory of Serbia includes eight species. Ranges of 50% of them are within marginal zones of their overall distributional ranges, while 50% of species show range fragmentation. Although A. nigropunctatus is subendemic, since its distribution reaches north-eastern Italy around Udine and Trieste (Gasc et al. 1997), we considered it as the Balkan endemic, because only a small part of its distribution range lies outside of the Balkan Peninsula. Thus, two species (A. nigropunctatus and P. erhardii) are endemic for the Balkans (Table 1).
The most widely distributed species of lacertids (L. agilis, L. viridis and P. muralis) occupy more than 50% of territory of Serbia each. Rare are the species related to steppe and forest-steppe habitats (D. praticola and P. tauricus), which occupy between 10% and 50% of territory of Serbia. Extremely rare species are those which occupy less than 5% of Serbia -areas with sub-Mediterranean climate in the extreme south and south-east (A. nigropunctatus and P. erhardii), or alpine habitats (Z. vivipara) (Figs. 2 and 3).
Regarding regional diversity of Serbia, the highest numbers of species were found in Metohija (8) and Kosovo (7). The lowest number of species was found in north-western Serbia and in Pomoravlje (3). Other regions were somewhat inbetween: Bačka, Srem and Šumadija have only four lacertid species, Banat, eastern and north-eastern Serbia had five species, and western, south-western, central, southern and southeastern Serbia had six species each.
For every species, new records in Serbia (with region, broad location and exact locality) are given in the Appendix I. Data from the literature and Internet sources (with region, broad location, exact locality (when available) and reference) are presented in the Appendix II. Table 1. Species list of Serbian lacertids with marginality, endemicity status for Balkans and range fragmentation.

Marginal zone Endemic for the Balkans Fragmented range
Algyroides nigropunctatus + +

Patterns of lacertid diversity -faunal similarity, chorology
The Bray-Curtis dissimilarity index showed that some regions in Serbia have identical composition of lacertid species, and these form four clusters -(1) Bačka and Srem; (2) Banat and north-eastern Serbia; (3) western, south-western and central Serbia, and (4) north-western Serbia and Pomoravlje. Apart from these clusters, Kosovo and Metohija are the most similar mutally and group together with the central-westernsouthwestern cluster and southern Serbia. North-western Serbia and Pomoravlje regions are the most distinct, owing to scarcity in lacertid species (Fig. 4). In general, different regions in Serbia have fairly similar lacertid faunas; the average Bray-Curtis index value is 0.82. Apparently, differences in species richness are the main cause of dissimilarity of certain regions.    (Table 2).

Discussion
Small number of recorded lacertid species puts Serbia among the countries with the lowest number of lacertids in the Balkans, along with Romania and FYR of Macedonia (Gasc et al. 1997;Sterijovski et al. 2014). However, this does not make Serbia insignificant concerning lacertid diversity in the Balkans, due to the presence of phenomena of biogeographical and evolutionary significance: peripheral populations, range fragmentation and Balkan endemics (Džukić 1995;Džukić & Kalezić 2004;Tomović et al. 2014Tomović et al. , 2015. Analysis of the information we obtained revealed that three lacertid species are present in all biogeographic regions of Serbia: Lacerta viridis, L. agilis and Podarcis muralis. Lacerta viridis seems to be present in all parts of Serbia, but larger distribution gaps exist in northern Banat and the most of Bačka. This species is typically found in dense but sunlit bushy vegetation, such as open woods, field and wood edges, hedgerows, bramble and overgrown embankments (Arnold 1987;Arnold & Ovenden 2002). It the Pannonian part of Serbia, such habitats are present in the remaining steppes and forest-steppes of the Deliblatska peščara and Subotička peščara sands, loess deposits on the Sava and Danube river banks and in open forests of the Fruška gora and Vršački breg mountains, where most findings of L. viridis were concentrated.
Lacerta agilis exhibits somewhat disjunct distribution. It is abundant in the Vojvodina province: Banat, Bačka and Srem regions. Conversely, south of the Sava and Danube, it is mostly restricted to mountains above 600 m a.s.l. This disjunct distribution in Serbia corresponds with intraspecific differentiation: Pannonian part of the range is inhabited by L. agilis argus (Laurenti, 1768), while southern mountainous habitats are occupied by the Balkan subspecies, L. agilis bosnica (Schreiber, 1912) (Kalyabina et al. 2001;Andres et al. 2014). This disjunction was most likely determined by climate and glaciation events (Andres et al. 2014). Belonging to the Euro-Siberian chorotype (according to Vigna Taglianti et al. 1999), L. agilis prefers temperate climate and is found in lowlands of the northern and central Europe, but is restricted to mountainous habitats in southern Europe (Arnold 1987;Arnold & Ovenden 2002). Serbian distribution of this species reflects its general distribution pattern in Europe: it inhabits areas with continental and alpine climates, and avoids warmer moderate-continental and sub-Mediterranean climates.
Podarcis muralis is also abundant in Serbia, but its distribution north of the Sava and Danube rivers is dispersed, i.e. concentrated around the Fruška gora and Vršački breg mountains, and in anthropogenic habitats (habitations and modified natural habitats) in the lowlands. The flat, moist lowlands of the Pannonian plain usually lack sunny, rocky habitats preferred by this species (Arnold 1987). Having in mind that P. muralis was initially described as hemerophilous, i.e. synanthropic, "kulturfolger" (Gruschwitz & Böhme 1986), and it was proven capable of expanding its range along anthropogenic corridors (Covaciu-Marcov et al. 2006;Gherghel et al. 2009), we assume that distribution of this species in some parts of the Pannonian plain could be a result of human activity during the historic times . A detailed phylogeographic study is needed to confirm these assumptions.
Two species which reach their north-western range limits in Serbia are Darevskia praticola and Podarcis tauricus (Džukić 1970(Džukić , 1974Ljubisavljević et al. 2006Ljubisavljević et al. , 2010b. The new, previously unpublished, findings of D. praticola populations expand the known distribution of this species in Serbia. Updated distribution map suggests that there could be even more populations of D. praticola still not recorded in suitable habitats in our country. Darevskia praticola is globally regarded with special concern, because its range is highly fragmented, and it is considered as Near Threatened by the IUCN (Agasyan et al. 2009). Marginal populations from Serbia are also distinct in certain life-history characteristics (Ljubisavljević et al. 2008). It should be noted that, based on morphological evidence, populations of D. praticola pontica (Lantz & Cyren, 1919), including those from the Balkans, have recently been raised to species level (D. pontica), while their genetic distinctiveness is yet to be confirmed (Tuniyev et al. 2011;Kosushkin & Grechko 2013). However, this nomenclatural question is out of the scope of the present study and does not make a difference to the total number of lacertid species recorded in Serbia.
Podarcis tauricus has a disjunct distribution range in general. It is a lowland species, associated with open steppe habitats, often sandy and with low herbaceous vegetation (Arnold & Ovenden 2002). According to general herpetological literature (Gasc et al. 1997;Arnold & Ovenden 2002), distribution range of P. tauricus consists of the "compact" part which reaches its western limits in eastern and southern parts of Serbia, and a smaller isolated range in southern Hungary and northern parts of Serbia. Field surveys and literature data reveal existence of some isolated populations in the Vojvodina province between these two parts of the species range. These populations imply that P. tauricus once had broader range, and that its current distribution is probably a consequence of spreading of arable areas, which lead to serious alterations of suitable open habitats ). On the other hand, there are implications that anthropogenic alterations of natural habitats (building of river embankments, floodplains regulation, etc.) could, in some cases, help this species spread into locations it previously had not inhabited . The data collected by now suggest that more populations of this species could be discovered in the remaining steppe fragments in Serbia; these populations could provide better understanding of its distribution. There are also numerous new findings of P. tauricus in south-western, western and central Serbia, which expand its known distribution boundaries in southern parts of Serbia further to the west. A finding of this species in Mali Zvornik in NW Serbia, near the Drina river, mentioned in G. Pasuljević's collection entry, is unexpected and presents an outlier in the known distribution pattern of this species. We treated this finding as doubtful and did not include it in the analyses of lacertid diversity.
To our knowledge, in Serbia high mountains are exclusive habitats for Z. vivipara, which is considered a glacial relict in the central Balkans (Guillaume et al. 1997;Džukić & Kalezić 2004). This species and its preferred habitats in Serbia are very scarce: high mountains (above 1,500 m a.s.l.) in eastern, central, south-western and south-eastern Serbia, Kosovo and Metohija (Stara planina, Čemernik, Vardenik, Kopaonik, Šar planina, Prokletije, and Mokra gora mountains), and mountainous habitats (900-1,000 m a.s.l.) in western Serbia (Tara Mt.). There are some old findings of this species which, despite significant efforts, have never been confirmed by subsequent faunistic research. We treated a finding of this species in the Duga Poljana village at the Pešter plateau, south-western Serbia (Karaman 1921) as doubtful. On the other hand, the record from the Suva planina mountain, mentioned by Karaman (1939) and Radovanović (1951), was given without precise locality data, and it was, most likely, a secondary citation from an uncertain source. Therefore, in the current analysis this particular locality was not included in the distribution map. Fragmented range and morphological differentiation between the studied populations from highaltitude habitats (Šar planina, Stara planina and Kopaonik mountains), and from lower-altitude relict habitats on the Tara mountain (Ljubisavljević et al. 2010a) also highlight Z. vivipara as a top-concern species for Serbian herpetofauna.
Marginal populations of A. nigropunctatus and P. erhardii are found exclusively in the areas under the influence of the sub-Mediterranean climate (Džukić 1970;Džukić 1980;.
Algyroides nigropunctatus is the rarest lacertid in Serbia, known only from a few localities in the Metohija region along the Beli Drim river valley (Džukić 1970;. It inhabits the stony karst habitats in gorges of Beli Drim and Prizrenska Bistrica rivers, on elevations from 270 to 590m a.s.l., surrounded by degraded thermophilous forests . Most new data are reconfirmations of the old published records, or are situated close to them. More populations of this species could be expected in the suitable habitats along the Beli Drim river and its tributaries. Podarcis erhardii reaches its northern range boundaries in southern and south-eastern Serbia, Kosovo and Metohija. Published records included Pčinja river valley (Prohor Pčinjski monastery and Trgovište town), surroundings of Priština and Vranje (Radovanović 1964;Džukić 1980;. The previously unpublished records of his species in Prizren (Metohija) and southern and south-eastern Serbia (in the valleys of Moravica, Južna Morava and Pčinja rivers) expanded the known distribution of this species in Serbia. Podarcis erhardii can generally be found on suitable stony and rocky habitats with low, dense and bushy vegetation (Arnold 1987;Arnold & Ovenden 2002). In Serbia, it is found in open, thermophilous forests on rocky substrate, on elevations from 400 to 780m a.s.l. . More populations of this species could be expected in suitable habitats under the influence of the sub-Mediterranean climate, but the existing northern boundary is unlikely to be changed.
In general, the major predictor of species richness is environmental heterogeneity -habitat diversity, topographic diversity and climatic peculiarities (Maes et al. 2005;Radovanović & Mijović 2005;Schouten et al. 2009;Buse & Griebeler 2012;Vukov et al. 2013;Tomović et al. 2014). Biogeographic regions of Serbia contain similar herpetofaunas, which differ mostly in overall numbers of species. Presence of three chorotypes points out the versatility of zoogeographical links, also important for local biodiversity (Džukić 1995;Džukić et al. 2001;Džukić & Kalezić 2004;Tomović et al. 2014). Another factor which influences our perception of the differences in species diversity is the sampling bias: for the Pomoravlje region, where only three lacertid species have been registered, conspicuously little distributional data are available. Sampling bias is also obvious for Šumadija, parts of north-western Serbia, Banat and Bačka.
The largest numbers of lacertid species can be found in southern Mountain-valley region, owing to long altitudinal gradient and elements of the sub-Mediterranean climate in the valleys of the Beli Drim (Kosovo and Metohija), Južna Morava and Pčinja rivers (southern and south-eastern Serbia). In recent faunistic investigations, several more Mediterranean reptile species were recorded in the Pčinja River valley (south-eastern Serbia): Platyceps najadum (Eichwald, 1831) , Testudo graeca (Linnaeus, 1758) (Tomović et al. 2004), and Elaphe quatuorlineata (Lacepède, 1789) , and also in Prizren (Metohija) -Mediodactylus kotschyi (Steindachner, 1870) (Ajtić & Tomović 2001). These findings highlighted the importance of Mediterranean climate influences along the valleys of the rivers listed above on herpetofaunal diversity . It makes these areas crucial for conservation at the national level. Parts of Kosovo and Metohija are already proposed as national herpetofaunal hotspots .
Compared to other Balkan countries, Serbian lacertid fauna is most similar to those of Albania and the FYR of Macedonia, and then to Romanian and Bulgarian faunas, due to high number of East-Mediterranean taxa. The western Balkan countries (Slovenia, Croatia, Montenegro and Bosnia and Herzegovina) form a distinct cluster, mostly owing to the presence of Dinaric endemics Dalmatolacerta oxycephala (Duméril & Bibron, 1839) and Dinarolacerta spp. (Gasc et al. 1997;Arnold et al. 2007;Ljubisavljević et al. 2007), and of taxa characteristic for central and western Europe and the Apennine Peninsula: Lacerta bilineata (Daudin, 1802), Iberolacerta horvathi (Méhely, 1904), and Podarcis siculus (Rafinesque, 1810) (Gasc et al. 1997;Tvrtković et al. 1998;Krofel et al. 2009). Greece diverges from both clusters of countries, owing to large number of species and to high level of endemicity on the Peloponnesus and Aegean islands (Gasc et al. 1997;Arnold et al. 2007).
When the pattern of diversity of lacertids is compared to the diversity pattern of all reptiles , the distinction between eastern and western Balkan countries is more pronounced, and Slovenia groups together with the western Balkan cluster, while Greece still remains the most distinct. This indicates that, concerning lacertids, there are three distinct diversity areas in the Balkans, which correspond to the six Balkan diversity centres proposed by Džukić & Kalezić (2004): Peripannonia and Dobrogea in the eastern Balkans, SW Croatia and Adriatic Triangle in the western Balkans and Evros and Peloponnesus in Greece. Considering lacertids, southern and south-eastern Serbia, and Metohija (valleys of the Beli Drim, Južna Morava and Pčinja rivers) should be treated as important diversity centres. This is due to the range overlapping of widely distributed species with East-Mediterranean species and with Balkan endemics that reach their northern and north-western range borders in Serbia.
There are still some lacertid species which are supposed to occur in Serbia, but their presence has not yet been confirmed by experts. Lacerta trilineata (Bedriaga, 1886), for instance, reaches its distribution boundary in the FYR of Macedonia, very close to border with Serbia . Several East-Mediterranean reptile species are present in the Pčinja River valley, and many of those were only recently recorded (Džukić 1980;Tomović et al. 2004;Ristić et al. 2006). Since there are already unconfirmed sightings of L. trilineata in this area, we can assume that it is only a matter of time until the official expert confirmation of this species' presence in south-eastern Serbia.