The European pond turtle (Emys orbicularis) is the only native freshwater turtle species in Slovakia. Due to watercourse regulations in the middle of the 20^th century, its range became fragmented and, currently, there are only two isolated populations. From a total of 1,236 historical records in Slovakia, most observations (782 records) came from the area of the Tajba National Nature Reserve (NNR). Three of the population viability analysis models (‘baseline’, ‘catastrophe’, ‘nest protection during a catastrophe’) indicated the extinction of the population in Tajba, with the highest probability of extinction occurring during a catastrophic event (probability of extinction 1.00). We also evaluated information about the activity patterns of seven radio-tracked individuals and about the number of destroyed nests from the area. During the period 2017–2021, we recorded only two turtles leaving the aquatic habitat of Tajba. An alarming fact is the massive number of destroyed nests found in the area during the study period (Tajba 524; Poľany 56). Our results indicate that the population in the Tajba NNR require immediate application of management steps to ensure its long-term survival.

Central Europe, freshwater turtle, management, threats, Vortex

Despite widespread conservation efforts, turtles are facing serious survival issues worldwide. The most significant threats to turtle biodiversity are caused by anthropogenic disturbances (habitat loss, habitat fragmentation, pollution and unsustainable harvesting) and by climate change (Böhm et al. 2013; Stanford et al. 2020). Given the life-history traits of turtles, which include delayed sexual maturity, low fecundity, low survival of eggs, hatchlings and juveniles and long-life span, they are vulnerable to human pressure and their ability to compensate for environmental stochasticity (including catastrophic events) is also limited (Enneson and Litzgus 2008; Spencer et al. 2017).

The European pond turtle (Emys orbicularis (Linnaeus, 1758)) is a freshwater turtle species inhabiting ponds, slow-flowing rivers and swamps, with a wide distribution range, extending from northern Africa through most of Europe up to the Aral Sea (Fritz 2001, 2003; Rogner 2009). In Europe, the present distribution of E. orbicularis is discontinuous and the species is listed as endangered in many countries (Fritz 2012). Similarly to other European freshwater turtles, the species is also experiencing demographic declines throughout its geographic distribution which are attributed to a variety of factors, such as habitat fragmentation, drying of wetlands, loss of landscape connectivity, population isolation and nest depredation (Rogner 2009). Furthermore, the co-occurrence of the invasive non-native pond sliders (Trachemys scripta (Thunberg in Schoepff, 1792)) within the natural ranges of E. orbicularis, with several countries reporting its successful reproduction, represents a serious threat to their persistence (Cadi et al. 2004; Perez-Santigosa et al. 2008; Standfuss et al. 2016; Liuzzo et al. 2020). Pond sliders can impact indigenous species through various competitions and parasite transmission (Cadi and Joly 2003; Iglesias et al. 2015; Héritier et al. 2017). The European pond turtle is also facing most of these threats at its northern range margin in Slovakia (Randík et al. 1971; Kminiak 1992; Havaš and Danko 2009).

In Slovakia, the species has been historically noted since the end of the 18^th century (Korabinsky 1791), with several sites situated in the south-eastern part of the country (Stollmann 1957). The first comprehensive review of the species distribution covered the period 1862–1963 (Lác and Lechovič 1964) and was supplemented by a subsequent attempt to recognise the species’ distribution, based on a questionnaire survey (Randík et al. 1971). Currently, despite of the past existence of multiple occurrences, mostly in the south-eastern part of the country, there are only two known reproducing populations in Slovakia and it is the only reptile species locally evaluated as critically endangered (Urban and Kautman 2014; Jablonski et al. 2015). Extensive alterations of the lowland agricultural landscape in the middle of the 20^th century caused a radical decrease in suitable habitats for the species, which was reflected in a decline of E. orbicularis populations in the area (Lác and Lechovič 1964; Lác 1968; Kunaková and Terek 2016). An autochthonous population inhabiting the Tajba National Nature Reserve (NNR) has been a subject of long-term study (e.g. Novotný et al. 2004, 2008; Havaš and Danko 2009; Horváth et al. 2017) and, currently, seems to be experiencing a demographic bottleneck (Horváth et al. 2021).

Extreme environmental stochasticity, such as wetland drying, is known to have deleterious ecological and demographic effects, especially on small, isolated populations, leading to the disruption of the population structure of species and their recovery requires long periods of time (Anthonysamy et al. 2013; Keevil et al. 2018; Mullin et al. 2020). Drought conditions could force freshwater turtle species either to immigrate to other nearby water bodies or to aestivate until the next rainfall (Serrano et al. 2020). The desiccation of a marsh, where the mating of E. orbicularis takes place, has a direct impact on and also indirectly influences the nesting activity of females. Due to the absence of a suitable nesting habitat close to water, migrating females are imperilled by increased predation or exhaustion (Baguette and Van Dyck 2007). Today, the two main threats jeopardising the existence of this isolated population in the Tajba NNR are high rates of nest depredation and the alteration of both their aquatic (drainage) and terrestrial habitats (overgrown by the invasive trees Robinia pseudoacacia and Ailanthus altissima, as well as agricultural activities). After watercourse regulation in the region, the water level of the Tajba Marsh depends only on the amount of rainfall. Such problems indicate that this population is threatened on a multi-stage level. However, despite all the described threats, there is currently no ongoing conservation programme for the species in Slovakia. In contrast, several successful management programmes have been implemented throughout Europe, focusing mainly on nest protection, re-introduction and habitat restoration of the species (Canessa et al. 2016; Mascort and Budó 2017; Schindler et al. 2017).

Thus, for a better understanding of the current status of E. orbicularis in Slovakia and for the implementation of effective conservation programmes in the future, we set the following goals. First, based on the collection of all available presence data, we evaluated changes in the E. orbicularis distribution range in Slovakia. We further aimed to analyse the population viability of the turtle population from the Tajba NNR based on an assessment of the local demographic situation and examined the effect of a potential catastrophic event and the benefits of nest protection. For better implication of future conservation steps, the viability of this threatened population is also evaluated using information about activity patterns collected by the radio-tracking of selected individuals and about the number of destroyed nests from this area.

Literature sources dealing with the distribution of E. orbicularis in Slovakia allowed us to make an assumption about its accurate distribution range only in the middle of the 20^th century. Comparing recent distribution data to the available fossil findings ranging from the Pliocene to the Holocene, the range of the species today is likely more reduced and fragmented. The more northern historical distribution of E. orbicularis in Europe was the result of the favourable early Holocene climate, when the species reached its maximum range extension (Sommer et al. 2007). Its recent range is limited by climatic factors and by the species habitat preference for the lowlands of mainly eastern Slovakia, with just two or three confirmed reproducing populations (Jablonski et al. 2015). As most of the findings (with the exception of the Tajba NNR and Marcelová, in eastern and western Slovakia, respectively) are sporadic or accidental observations of single individuals and no further nesting sites have yet been discovered, it is almost impossible to determine the origin of the recorded turtles. Even the population in Marcelová needs further genetic studies for the verification of its autochthony. Other recent observations reported from western Slovakia are listed and discussed in detail in Jablonski et al. (2015). Another noteworthy region in south-western Slovakia, from where regular reliable observations of single individuals are made, is located at the floodplains of the River Ipeľ. The close location of the population in Danube-Ipoly National Park, Hungary, suggests possible migration of the species to this area (S. Bérces, pers. comm.). Fragmentation of the species’ distribution range due to habitat deterioration is further supported by the fact that the population discovered in Poľany diminished within four years. Destroyed clutches were discovered again in 2017 and 2018, but in the last two years, the adjacent wetland has dried out and no turtle activity has been observed in the area. The fate of the population remains unknown, as no turtle observation has been reported from the vicinity of Poľany since 2017. Observations of single turtle individuals are relatively common in the Východoslovenská Nížina Lowland, especially from the Medzibodrožie Region. These individuals are probably the still surviving remnants of past existing populations, although no comprehensive monitoring activities are being carried out in the Region. For this reason, the implementation of such species monitoring should be a priority in the future.

Despite this decreasing and fragmented distribution and the fact that the mostly known and still reproducing E. orbicularis population in the Tajba NNR is in decline, the last conservation activity was carried out in 2002–2006, with most of the turtle observations made during that time (BureŠová et al. 2001). Although even small populations can persist for long periods of time, the existence of high-quality habitat conditions are inevitable (Folt et al. 2021). The results of our population viability analysis support the importance of suitable habitats. We found that the population projected during a ‘catastrophic’ event had slightly higher probability of extinction than our ‘baseline’ model. Although, the populations became extinct in both of the simulated models, during a ‘catastrophic’ event, it happened 24 years earlier. The only PVA for E. orbicularis was conducted on a population from north-western Spain, in which a ‘catastrophic’ event decreased their survival probability in 100 years to 8%. Simulations were employed on a population with a lower initial population size than in our simulation, but it was also male-biased (Cordero Rivera and Ayres Fernández 2004). Similar results were obtained by Famelli et al. (2012); a ‘catastrophic’ event led to a 99% extinction probability for the Maximilian’s snake-necked turtle (Hydromedusa maximiliani (Mikan, 1825)) population in Brazil. Unfortunately, the negative impacts of habitat drying are already visible on our studied population. In the last decade, the water surface of the Tajba Marsh has been drastically reduced, losing more than half of its initial area. Due to these unfavourable conditions, aestivating individuals have been regularly observed since 2009 and more frequently in the last few unusually dry years. One tagged individual buried in the mud for more than five months was exposed to very low winter temperatures (-10 °C) during its hibernation period; however, the critical minimum temperature for adult turtles is known to be – 2 °C (Hutchison 1979). While long-distance migration of E. orbicularis individuals to overwintering sites was detected in France (Thienpont et al. 2004), we did not observe this strategy in any of our tagged individuals. In addition, E. orbicularis populations inhabiting the Tordera River system in north-eastern Spain showed high fidelity to their capture sites with low dispersal movements between neighbouring water habitats (Escoriza et al. 2020). An unusually long migration of a female E. orbicularis individual was recorded by Bona et al. (2012); the turtle migrated about 5 km distance from the Tajba NNR and then returned. During our radio-tracking survey, we were unable to detect the final destination of the only possible migration attempt to a more suitable water habitat, as we only found the detached transmitter. We speculate that the female was heading to the nearby Somotorský Canal, in which regular E. orbicularis observations are made.

Both of these strategies (aestivation or migration) could influence the adult survival of the population, which is especially important for the population persistence of long-lived species (Howell and Seigel 2019); high adult survival is essential to compensate for low hatchling survival (Enneson and Litzgus 2008). Studies have shown that turtle populations are unable to sustain more than 2–3% annual adult additive mortality (Gibbs and Shriver 2002), which is also, based on our long-term observations, a realistic scenario for the population in the Tajba NNR. Due to shallow water levels, the turtles could be exposed to increased adult predation (Hall and Cuthbert 2000). These habitat conditions are suitable for wild boars (Sus scrofa Linnaeus, 1758), whose impact is already detectable on the turtle population in the Tajba NNR. However, predation by wild boars is recognised especially on nests and young individuals (Zuffi 2000; Ibáñez et al. 2018). In 2020, three adult turtles (2 females, 1 male) were observed with multiple injuries caused presumably by this predator. Female turtles are at even higher risk, because due to the desiccation, they have to reach distant nesting sites mainly on land, which we were able to prove by radio-tracking. According to this observation in 2020, the turtle moved ~1.5 km in a week, mainly on land, in an effort to reach the nesting site. While the upper limit of terrestrial movement for E. orbicularis is recognised to be less than 2 km (Ficetola et al. 2004; Pereira et al. 2011), terrestrial movements for nesting were also detected in other parts of their range, however, to shorter distances (Rovero and Chelazzi 1996; Kotenko 2000; Cadi et al. 2004). We also observed a great decrease in the total number of nesting females. While in 2017, more than 20 females were nesting, in 2020, just five females were found. Most studies on the nesting ecology of the European pond turtle are focused on other aspects of nesting (Meeske 1997; Mitrus 2006; Najbar and Szuszkiewicz 2007). The number of depredated nests is also massive in the area: during the period 1999–2020, more than 520 destroyed nests were found, causing very high rates of hatchling mortality. According to our PVA model, a reduction in hatchling mortality by about 30% (from 98% to 70%) would mean the survival of the population, with none of the simulated populations becoming extinct. Even during the simulated catastrophic event, protection of the nests postponed the time of the first extinction (Table 2). For the long-term viability of the olive ridley turtle population (Lepidochelys olivacea (Eschscholtz, 1829)), securing high emergence success of hatchlings was shown to be essential (Maulany et al. 2017). In the Tajba NNR, square metal grids were used for predation exclusion, but with low efficiency due to the extensive area of the nesting sites (~ 5 ha). Therefore, we recommend testing the suitability of chemical deterrents to reduce hatchling mortality. On the other hand, the implementation of nest protection grids enabled a population increase in the Donau-Auen National Park, Austria (Schindler et al. 2017). The high mortality rate of hatchlings is already reflected in the demographic structure of the population. Our observations showed a general shift towards a presumably old population. During the last sampling occasions and observations in 2020, no 1 to 4-year-old individuals were discovered; furthermore, in the years 2018–2020, we found only one hatchling per year. An adult dominated E. orbicularis population was described in Algeria (Fediras et al. 2017), in contrast to two populations in the Tordero River, where juveniles accounted for more than 20% and 10% of the captured specimens, respectively (Escoriza et al. 2020).

All of these alarming threats to the population in the Tajba NNR require immediate application of management steps to ensure the long-term survival of this unique population. Therefore, we recommend the application of the following conservation measures in the near future.

The preparation of this contribution was supported by the Scientific Grant Agency of the Slovak Republic (Vega 2/0077/17 and 1/0298/19). We thank the members of Fauna Carpatica NGO, namely Adriana Burešová and Milan Novotný, for their dedicated work in the field. Fieldwork within this study was conducted under a licence from the Ministry of Environment of the Slovak Republic (4347/2016–2.3 and 6598/2020–6.3).