Distribution, Population Size, and Habitat Characteristics of the Endangered European Ground Squirrel (Spermophilus citellus, Rodentia, Mammalia) in Its Southernmost Range

The European ground squirrel (Spermophilus citellus) is an endangered species, endemic to Central and Southeastern Europe, inhabiting burrow colonies in grassland and agricultural ecosystems. In recent years, agricultural land-use changes and increased urbanization have largely contributed to a severe population decline across its range, particularly in its southernmost edge. Assessing the population and habitat status of this species is essential for prioritizing appropriate conservation actions. The present study aims to track population size changes and identify habitat characteristics of the species in Greece via a literature search, questionnaires, and fieldwork for assessing trends in population size as well as spatial K-means analysis for estimating its relation to specific habitat attributes. We found that both distribution size (grid number) and colony numbers of the species decreased in the last decades (by 62.4% and 74.6%, respectively). The remaining colonies are isolated and characterized by low density (mean = 7.4 ± 8.6 ind/ha) and low number of animals (mean = 13 ± 16 individuals). Most of the colonies are situated in lowlands and did not relate to specific habitat attributes. Habitat aspect and system productivity (NDVI) were the main factors contributing mostly to the clustering of the existing colonies. These results demonstrate that the species is confined to small, isolated anthropogenic habitats. Specific conservation actions such as population reinforcement, habitat improvement, and specific common agricultural policy measures could effectively improve agroecological zones that are suitable for the maintenance and protection of existing and potential habitats for populations of the species.

Impact of management measures on the European ground squirrel population development

In the past, the European ground squirrel represented a common part of Slovakian fauna. During the 20th century, there was a substantial decrease in its number, mainly due to the intensification of agriculture. Currently, several programs focused on the recovery and preservation of ground squirrel colonies have been implemented. The aim in supporting the population of the European ground squirrel is to increase the number of birds of prey and to ensure a food base for them. In this paper, we focus on evaluating the success rate of European ground squirrel (Spermophilus citellus) management measures. The research was realized at two localities in the Protected Bird Area Slovenský kras (Hrhov and Gemerská Hôrka) in the years 2015–2018. Activities were focused on the management of grassland and supplemental feeding during the breeding period. As a result of the management measures and the supplemental feeding, we managed to maintain a positive trend in the populations’ development, as there was an increase observed in all the monitored seasons.

Energy metabolism in the pancreas of ground squirrels (Spermophilus citellus) during prolonged cold exposure and in hibernation

Mammalian hibernators undergo a host of biochemical adaptations that allow them to survive the harsh cold environment and food restriction. Since the energy metabolism of the pancreas during hibernation remains unknown, we investigated the molecular basis of mitochondrial energy-producing pathways in line with their regulating mechanisms, as well as the (re)organization of antioxidative defence in the pancreas during the prehibernation period and in the hibernating state. To this end, male ground squirrels (Spermophilus citellus) were divided into two groups, the control group kept at room temperature (22±1 °C) and the group exposed to low temperature (4±1 °C). Active animals from the cold exposed group were sacrificed after 1, 3, 7, 12, and 21 days; animals that entered hibernation were sacrificed after 2-5 days of torpor. Our results showed that the protein levels of respiratory complexes I, II, IV and cytochrome c were increased in response to prolonged cold exposure (from day 12) and that such expression profiles were maintained during hibernation. In parallel, AMP-activated protein kinase a (AMPKa) and nuclear respiratory factor 1 (NRF-1) were shown to be upregulated. Moreover, prolonged cold exposure and hibernation induced an increase in the protein expression of antioxidative defence enzymes copper-zinc superoxide dismutase (CuZnSOD) and glutathione peroxidase (GSH-Px). In conclusion, these results point to a controlled metabolic remodeling in the pancreas of ground squirrels during prolonged cold exposure and in hibernation, which includes an improvement of mitochondrial oxidative capacity along with a proportional upregulation of antioxidative defence.

Distribution of Spermophilus citellus in the Komárom-Esztergom County, Hungary, in 1950–2019 (Rodentia: Sciuridae)

The study describes changes in the Hungarian population of the European ground squirrel (Spermophilus citellus) that occurred between 1950 and 2019. Data before 1990 were collected from local communities who were familiar with this mammal (an example of citizen science). The comparison was based on the area occupied by the animals. The studied region was in the Komárom-Esztergom County, north-western Hungary, where the species was widespread in the middle of the 20th century. It was common in the lowlands, low hilly country and even in suitable habitats in uplands. By 1990 the population had drastically declined, to about 1.5% of the previous levels, and today 99.7% of the population has disappeared with only small, vulnerable populations surviving.

Diet of the European ground squirrel (Spermophilus citellus) in the southern Pannonian plain

Overwinter survival of hibernators is directly influenced by the fat reserves accumulated during the active season. The European ground squirrel, Spermophilus citellus, an endangered flagship species of the open grasslands of central and southeastern Europe, is no exception. Considering anthropogenic changes affecting its habitats in northern Serbia, we studied the species? feeding habits by subjecting its feces to microhistological examination. In addition to identifying plant remains in the feces, we examined the vegetation of the four study sites located inside a local mosaic of steppe and saline pastures. Our findings indicate that these remaining European ground-squirrel sites are diverse and stable grasslands covered by native flora that represents a complete dietary base for the species. The diet is dominated by a small number of plant species, specifically Achillea millefolium, legumes and grasses, with sporadic contributions from a number of other species. The diet of S. citellus also differs by location and season in that grasses dominate during the early season, while A. millefolium takes precedence later in the year. This dietary information is essential for the development of future species and habitat management strategies. In light of the predicted impact of climate change on grasslands in northern Serbia, our findings will be instrumental for translocations and conservation actions in the future.

Contribution to the Study of the European Ground Squirrel’s Population (Spermophilus citellus Linnaeus, 1766) in Rila National Park, Bulgaria

Although there are still some large and stable populations of the European Ground Squirrel, there has been a serious decline in the number and density of most of the species populations throughout its range, including in Bulgaria. The aim of the study is to supplement the scientific data about the population of the European Ground Squirrel and its habitat in Rila National Park, Southwestern Bulgaria. The research was carried out in 2017-2019 in two study areas, each divided into 20 (21) transects (every 100 m long and 5 m wide). The results have shown that the relative population density based on the number of holes tends to decrease in the period of study. The most likely reason for this, and the most significant identified threat to the population of the species in the research area in general, is the observed deterioration of the habitat status.

Geographic variability in the alarm calls of the European ground squirrel

Geographic variability in vocalizations has been documented in many mammalian species. We examined to what extent it applies to the alarm calls of the European ground squirrel Spermophilus citellus. We recorded the calls of 82 adult individuals from 5 natural colonies in the Czech Republic and 24 adult individuals from an artificial seminatural colony located in a Czech zoo. The founders of this colony originated from 4 different natural colonies in the Czech Republic. Our results showed that there are hardly any differences in the acoustic structure of the alarm calls between male and female European ground squirrels. Discriminant function analysis showed the highest degree of discriminability for the most isolated sites (54–74% of individuals classified correctly), whereas the lowest degree of discriminability was found for 2 interconnected colonies (38–40% individuals classified correctly). Individuals from the artificial seminatural colony were often classified correctly to this colony (58% classified correctly); however, the precision of the classification was comparatively relatively low, that is, many individuals from other colonies were incorrectly classified into this seminatural colony. This likely corresponds to the different origins of its founders. These findings indicate that there is a rather substantial geographic variability in the alarm calls of the European ground squirrel, and our study highlights its possible impact on conservation measures such as establishing artificial colonies or reintroductions.

The role of ant nests in European ground squirrel’s (Spermophilus citellus) post-reintroduction adaptation in two Bulgarian mountains

The European ground squirrel (Spermophilus citellus) is a vulnerable species, whose populations are declining throughout its entire range in Central and South-Eastern Europe. To a great extent, its conservation depends on habitat restoration, maintenance and protection. In order to improve the conservation status of the species, reintroductions are increasingly applied. Therefore, researchers focus their attention on factors that facilitate these activities and contribute to their success. In addition to the well-known factors like grass height and exposition, others, related to the underground characteristics, are more difficult to evaluate. The presence of other digging species could help this evaluation. Here, we present two reintroduced ground squirrel colonies, where the vast majority of the burrows are located in the base of anthills, mainly of yellow meadow ant (Lasius flavus). This interspecies relationship offers numerous advantages for the ground squirrel and is mostly neutral for the ants. The benefits for the ground squirrel, including reduced energy demand for digging, as well as additional surveillance and hiding places available, could greatly enhance the post-reintroduction adaptation process.

Spatial and temporal estimation of habitat suitability of the Spermophilus citellus(Rodentia: Sciuridae) in the area of Sredna Gora Mountain (Central Bulgaria)

The spatial and temporal aspects of the habitat suitability of the European Souslik (Spermophilus citellus L.) in an area in Sredna Gora Mountain (Bulgaria) was investigated. Data from Landsat satellite imagery were used for modelling changes in the habitat suitability of the species from 1985 till 2018. Linear Regression Analysis showed that spectral bands represent not only the spatial heterogeneity of the landcover, but also the temporal changes of two climatic parameters – monthly temperature and rainfall amount. The obtained results show that the habitat suitability of the European Souslik increased during the studied period. The methodology used here based on statistical modelingis applicable to long-term monitoring and evaluation of the role of land cover change as a result of the human activity and the climate change on the habitat suitability of the European Souslik.