UPDATED DISTRIBUTION OF THE EUROPEAN POND TURTLE EMYS ORBICULARIS ( LINNAEUS , 1758 ) AND ITS CONSERVATION ISSUES IN SERBIA

Although the European pond turtle (Emys orbicularis) has been included in studies for several decades, the information about its distribution and the state of populations in Serbia is still incomplete. The data collected from the available literature sources, and those based on the authors’ own field investigations, indicate that E. orbicularis occupies a large part of the territory of the Republic of Serbia, preferring aquatic biotopes at lower altitudes. We compiled a list of 287 localities where the presence of the pond turtle has been recorded. Of those, 14% (40 localities) were known only from literature sources, localities added during our field investigations represent 82% (235 sites), 4% (12 localities) confirming literature data. We also gathered information on the main negative threats to the endurance of the pond turtle in Serbia. These are habitat pollution, degradation and destruction, and the spread of allochthonous invasive turtle species. Some protective and conservation measures are suggested in the conclusion.


INTRODUCTION
According to Fritz et al. (2007), the only autochthonous representative of freshwater turtles in Serbia, the European pond turtle, belongs to the nominotypical subspecies Emys orbicularis orbicularis (Linnaeus 1758).Its distribution area ranges from Denmark, parts of the Netherlands, Belgium, France, Spain and Portugal in the west, to Kazakhstan, the Aral Sea and the Ural Mountains in the east, and from the northern parts of Germany and Russia to southern Italy, Sicily and North Africa at the far south.To the southeast, it extends through Turkey and the Middle East, to eastern Caucasus, the southern shores of the Caspian Sea and Turkmenistan, i.e. to Iran and Syria (Podloucky, 1997;Fritz, 2001;Arnold and Ovenden, 2002;Stuckas et al., 2014).As a semiaquatic freshwater species (Ficetola and De Bernardi, 2006), the pond turtle can be found in most inland waters.It prefers sunlit, stagnant or slowly flowing waters surrounded by dense vegetation, at altitudes ranging the sea level to 1700 m a.s.l.(Podloucky, 1997).
Despite the relatively long period of herpetological research in Serbia (Džukić, 1977), understanding the distribution and vulnerability of this species has so far been incomplete and fragmentary.The earliest accounts of the presence of E. orbicularis in Serbia date back to the second half of the 19 th and beginning of 20 th century (Pančić, 1869;Đorđević, 1900a, b).In the subsequent decades, and only sporadically, data on the distribution of this species were compiled, but only at the level of zoogeographical and faunistic studies of amphibians and reptiles on the territory of the former Yugoslavia (Karaman, 1939(Karaman, , 1948;;Radovanović, 1951Radovanović, , 1964)).The majority of literature data is concentrated in papers presenting the fauna of amphibians and reptiles on regional or local scales, e.g.mountain ranges, important aquatic ecosystems and areas significant in terms of nature conservation (Pasuljević, 1968;Crnobrnja and Rohalj, 1988;Džukić, 1972Džukić, , 1998;;Krizmanić, 1996Krizmanić, , 1998Krizmanić, , 2000aKrizmanić, , b, 2002;;Panjković et al., 2000;Dobretić, 2011a, b).The first comprehensive and analytical review of the diversity of herpetofauna to mention this species was done for the former Yugoslavia (Džukić, 1995).The first general presence assessment of E. orbicularis on the territory of Serbia (Tomović et al., 2014) provided only a contour map, without precise locality data.
At the international level, E. orbicularis is treated as Near Threatened (Cox and Temple, 2009).However, this assessment was published in 1996 and needs updating.The pond turtle is also listed in the Annexes II  The purpose of this paper was to present the current knowledge of the distribution of E. orbicularis in Serbia based on precise locality information, and to indicate the major factors threatening its survival.

MATERIALS AND METHODS
The information on the distribution of E. orbicularis in Serbia was obtained from literature sources, the authors' field observations, and field data donated by other colleagues (see Acknowledgments).Some data originated from the collection of the Museum of Natural History in Vienna.We also included some information from field herpetology websites (www.euroherp.com, http://en.balcanica.info,www.teraristika.org)and from the portal dedicated to mapping and monitoring the biological diversity of Serbia (http://www.bioras.petnica.rs).For the usage of these data, we followed the terms and conditions of the websites and, where necessary, asked the authors for permissions.During recent field investigations, other than visually observing and catching the animals with nets and/or by hand, we used funnel traps (150 cm and 200 cm long, 50 cm in diameter).A total of 287 records were compiled, over 70% of which (235) were the authors' previously unpublished data.We adopted the altitudinal classification of the territory of Serbia into the Pannonian, Peripannonian and mountain-valley regions of Marković (1980).All available records were mapped on 10 x 10 km and 50 x 50 km UTM (Universal Transverse Mercator) geographic coordinate grid systems.

Distribution
In Serbia, E. orbicularis inhabits a large part of the territory.Being dependent on the presence of aquatic habitats, its distribution is not uniform, but populations can be locally abundant.In general, E. orbicularis was detected in 287 localities.These comprise 168 out of the 1004 (16.7%) 10x10 km UTM squares covering Serbia (Fig. 1).The presence and, in particular, abundance of the pond turtle in Serbia is determined by geographical and other abiotic conditions in its habitats, mainly by altitude and the presence of adequate aquatic biotopes (Radovanović, 1951).Considering that the territory of Serbia can be tentatively divided into two parts strongly differing in topography and hydrology (Marković, 1980), there is a marked difference in the abundance of pond turtles in lowland areas compared to mountainous regions.The majority of localities (195, app.68%) were located in the territory of the Vojvodina prov-ince (altitudes ranging from 65 m to 300 m − Fruška Gora Mountain, DR00).Only 2 localities (Vranje, Sv.Ilija Hill -EN61 and Priština, Grmija Hill -EN12, EN22) inhabited by this species lie above 1 000 m.We concluded that E. orbicularis in Serbia inhabits areas with (sub-)Mediterranean and temperate-continental climates, which is in accordance with the division proposed by Stevanović and Stevanović (1995).
In Serbia, E. orbicularis can be found in almost all types of aquatic biotopes with stagnant and slowly flowing waters.Its populations are particularly numerous in aquatic biotopes with abundant vegetation: mainly backwaters, stagnant tributaries and floodplains of the rivers Danube, Sava, Tisa, Begej, etc.Large populations were also recorded in artificial aquatic habitats such as canals, fishponds, various types of pits and artificial lakes in the parks of larger cities.Turtles rarely venture far from water; however, during the reproductive season, as well as before and after hibernation, several individuals were recorded at large distances from their aquatic habitats.The maximum distance from water recorded was 2.4 km: we found a pond turtle killed by a vehicle on the road between the villages of Hajdukovo and Male Pijace (DS 10).

Legislation, threats and protection
Despite the existence of legal protection of turtles in Serbia from 2009 and2010(a), there is no information concerning the status of the pond turtle populations.In addition, objectives and tasks in their monitoring are not established.Therefore, apart from the basic protective regulations no specific and practical measures have been prescribed and undertaken with regard to pond turtle protection.In many European countries, the rapid degradation of natural pond turtle habitats has led to the implementation of monitoring, protection, captive breeding and reintroduction projects for this species (Ayaz et al., 2013;Ayres et al., 2013;Farkas et al., 2013;Ficetola et al., 2013;Melita et al., 2013;Mollov et al., 2013;Raemy et al., 2013;Schneeweiß and Breu, 2013;Sos, 2013;Šalamon et al., 2013;Teixeira et al., 2013;Thienpont et al., 2013).In Serbia, there has been only one project concerning E. orbicularis (Crnobrnja-Isailović and Mesaroš, 2013).For the time being, there is no discernible progress in the elimination of shortcomings in the protection of this species.In other ex-Yugoslav countries, the pond turtle has various distribution patterns and protection status: it is protected in Slovenia (Vamberger et al., 2012;Vamberger et al., 2013) and Montenegro (Republički zavod za zaštitu prirode, 2006) and strictly protected in Croatia (Jelić et al., 2012).In the FYR of Macedonia, this species has a highly restricted distribution (Sterijovski et al., 2014).In Bosnia and Herzegovina it is considered vulnerable (Ministarstvo okoliša i turizma, 2013).According to the results presented herein, in comparison to some other countries (Bona et al., 2013;Gent, 2013;Schneeweiß and Breu, 2013), the status of populations of pond turtles in Serbia is still not alarming.Recent analysis (Crnobrnja-Isailović and Mesaroš, 2013) showed that the survival of E. orbicularis is not seriously jeopardized by natural causes.Nevertheless, its survival depends on understanding the major non-natural endangering factors.

Endangering factors
The principal cause of the decline and extinction of pond turtle populations throughout their distribution area is the fragmentation and physical destruction of aquatic habitats, accompanied by the strong rise in the level of pollution (Fritz and Chiari, 2013;Crnobrnja-Isailović and Mesaroš, 2013).These factors lead to the direct mortality of individuals, and their migrations and communication between populations become difficult or impossible.
In certain areas of their range, deaths on roads during seasonal or daily migrations are quite frequent, and represent a realistic threat to the stability of some turtle populations (Puky et al., 2004, Trakimas andSidaravičius, 2008).Urbanization in the proximity of the turtles' natural breeding sites, even if it does not cause the destruction (draining) of their habitats, can lead to a decrease in the abundance, and/ or disappearance of populations.
Hydromeliorative interventions over large areas can lead to dramatic changes in aquatic habitats.The regulation of river courses and creation of embankments, which prevent water from reaching the inshore water basins (backwaters, marshes, ponds, canals) (Pavić et al., 2012), in conjunction with climate change and the reduction in atmospheric precipitation (Veljković et al., 2012) may lead to a distortion of the basic conditions necessary for the survival of pond turtle populations.
In the southern part of the Pannonian Plain (present day Vojvodina province, an area of over 2 million hectares), huge hydrological interventions were conducted almost 300 years ago (Dragović et al., 2005;Džukić et al., 2008).These resulted in the draining and destruction of numerous small aquatic habitats in which pond turtles were probably present.The level of this destruction cannot be adequately evaluated, but it is possible to specify some of the consequences of land alterations that could be avoided in future.Hydromeliorative interventions in this area typically involved the digging of a dense network of irrigation/ drainage canals: its overall length today is approximately 1000 km (Likić, 2002;Andrejev, 2004).Massive draining operations have surely caused a serious decline in pond turtle populations in the Vojvodina province.On the other hand, the construction of the huge canal network acted as a complex of corridors through which the turtles and other aquatic wildlife were able to migrate and establish contact with previously separated populations.
Unfortunately, some methods that are being implemented (as well as some that are not) question these positive side effects of anthropogenic landscape alterations.Namely, other than usually being used as dumping sites, these canals are often lined by plastic foil, which has negative impacts on almost all living forms (Draginčić et al., 2011;Draginčić and Marković, 2013).In such canals the macrophyte vegetation, a basic prerequisite for the survival of pond turtles in disturbed habitats, cannot develop.In addition, the very nature of these foils prevents the animals' movements, and they can cause the turtles to drown.Because there is no control and prevention of discharges of various chemicals into the waters of the canal network, thry are highly contaminated (Berge and Medbø, 2005;Dalmacija et al., 2006;Josimov-Dunđerski et al., 2008;Kaisarević et al., 2009) and unsuitable for wildlife.
Lowland aquatic habitats are usually tightly encircled by fields and arable land.These pose a threat to the survival of turtles and the biotope itself.Not only are all agricultural chemicals being washed directly into the canal water, but the ever-increasing plowing of the land leads to the destruction of appropriate egg-laying places.The largest portion of the species distribution range in Serbia lies in the areas under strong influences of agricultural engineering (Pannonian Plain and Peripannonian areas); however, the adverse impacts of agricultural chemicals have never been analyzed (see Bishop et al., 1998;Stewart et al., 2011).
Another gravely understudied threat to native pond turtles is the presence and fast spreading of the highly invasive allochthonous turtle, Trachemys scripta elegans (red-eared slider).This species is already present throughout the world (Cadi and Joly, 2004;Bringsøe, 2006) and in numerous countries has already established viable populations (Ficetola et al., 2002;Cadi and Joly, 2004;Vamberger et al., 2013) it is on the list of the world's 100 worst invasive species (Scalera, 2006).Based on current findings (Ficetola et al., 2012;Lazarević et al., 2012;Urošević et al., 2015, in press), the negative impact of this invader in Serbia is relatively low, since introductions are concentrated in urban and suburban localities.However, this conclusion might be due to the lack of knowledge of the ecology and interactions of the two species.Detailed studies are necessary.There is sound evidence that red-eared sliders can reproduce in Serbia (Đorđević and Anđelković, 2015, in press); therefore, the establishment of naturalized populations can be expected in near future.Recent findings of the Chinese softshell turtles (Pelodiscus spp.) in the Balkans, including Serbia (Urošević et al., 2015, in press) should also be a reason for concern.These medium-sized carnivorous turtles can easily produce viable populations and are therefore potentially invasive (Somma, 2013).
In northern parts of the distribution area of the pond turtle, the high pressure of introduced predatory species, Nyctereutes procyonoides (raccoon dog) and Procyon lotor (raccoon) was noticed (Fritz and Chiari, 2013).These invasive species (Ćirović and Milenković, 2003;Kauhala and Kowalczyk, 2011) may have extremely negative impacts on the abundance and distribution of pond turtle in Serbia as well.A serious threat to numerous species, including E. orbicularis, is the illegal collection and trade of specimens originating in the wild.A recent example is the confiscation of a shipment of 1327 individuals at the border between the FYR of Macedonia and Serbia in December 2012 (CITES Serbia).The tortoises were intended to be smuggled into/ through Serbia.They were sent to the zoo in Belgrade until their status is resolved.To the time of preparation of this manuscript, these turtles are still in Belgrade Zoo, under seriously inadequate conditions.

Proposed conservation measures
There is still no information on the demographic parameters of the pond turtle in Serbia.Therefore, it is necessary to conduct countrywide research in order to assess the current condition and perspectives of the populations of this species.After comprehensive analyses, species-specific monitoring protocols and protection procedures must be prescribed, firmly implemented and strictly controlled.
Nevertheless, even before extensive population ecology investigations, the basic protection measures should be implemented.This is important because realistic threats exist that can seriously jeopardize the survival of E. orbicularis in certain areas.(Vlada Republike Srbije, 2010b;Skupština Autonomne Pokrajine Vojvodine, 2009).Basic measures focused on preventing/mitigating the negative consequences of various "natural" and anthropogenic pressures can be grouped according to the threats they pose.Procedures previously recommended for the protection of the pond turtle in Serbia mostly aim at preserving and/or revitalizing the disturbed or devastated aquatic habitats.However, harmonized procedures at the national level do not exist, and the legislation prescribing the conditions of protecting pond turtles (and other protected species) is inconsistent and unsatisfactory.
Regarding threats to the habitats of E. orbicularis in Serbia, it is necessary to adopt a national plan for the protection of marshes and wetland habitats (which are considered globally threatened areas) (Ramsar Convention Secretariat, 2010).It is essential to prevent the dumping of waste into and near aquatic biotopes.It is especially important to prevent the spilling of toxic substances used in agriculture.
Mitigation of the harmful consequences caused by the introduction of invasive and predatory species, as well as the illegal trade in threatened native turtle species, is possible only through a strict implementation of national and international legislation.The lining of canals with plastic/concrete must be stopped.Proper maintenance of the canal network (necessary for agriculture and flood prevention) can maintain the functioning of the canal system and the stability of E. orbicularis populations at the same time.In particular segments of roads along aquatic habitats, where high turtle mortality has been observed or is infered, it is necessary to set mobile (seasonal) or fixed (permanent) protective fences, or to construct underpasses, which would facilitate the safe seasonal migrations of turtles.In addition, traffic signs should be placed along such roads.These measures should also be accompanied by the education of local inhabitants, some of who intentionally run over animals on the roadConsidering the above, the basic measure we propose is the modification of legislative regulations, and, even more, the strict implementation of the existent regulations.It is necessary to change and amend all legislation regulating agriculture, water management, fishing, hunting, trade and tourism, which may have negative impacts on nature.Habitat conservation is one of the fundamental and most important direct protection measures.It is often in conflict with and hence strongly opposed by the people living in close proximity to areas in need of conservation.Therefore, in addition to system solutions in nature protection, it is necessary to raise public awareness of the status of national natural values and of the need for the expansion of territories under protection.One of the necessary processes is education of the local inhabitants and managers about the necessity of nature protection, the importance of autochthonous species and the dangers of introducing invaders such as Trachemys.
In the future, we must strive towards the establishment and long-term sustainability of national/regional reception centers where confiscated chelonians or unwanted reptilian pets could be properly housed and analyzed before they are returned to nature or given to zoos/private keepers.In addition, the constant education of law practitioners and enforcers is necessary.
and IV of the European Commission Council Directive (Council of the European Communities, 1992 a,b), and Appendix II of the Bern Convention on the Conservation of European Wildlife and Natural Habitats (Council of Europe, 1979).The pond turtle in Serbia is strictly protected under the Law on Nature Protection from 2009, and the Ordinance to Designate and Protect the Strictly Protected and Protected Species of Wild Plants, Animals and Fungi, Appendix 1 from 2010(a).

Fig. 1 .
Fig. 1.Records of E. orbicularis from Serbia (National grid UTM 10 × 10 km).Black squares previously published records; gray squares new records; gray + black literature data confirmed in recent field surveys.