Turkish Journal of Zoology Turk J Zool (2016) 40: 917-924 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Research Article doi:10.3906/zoo-1505-28

Site selection of European ground ( citellus) in Eastern and how they are influenced by climate, relief, and vegetation

1 2 2, Gheorghe ZAHARIA , Laurențiu PETRENCU , Emanuel Ștefan BALTAG * 1 “Anastasie Fătu” Botanical Garden, “Alexandru Ioan Cuza” University of Iasi, Iasi, Romania 2 Department of Zoology, Faculty of Biology, “Alexandru Ioan Cuza” University of Iasi, Iasi, Romania

Received: 17.05.2015 Accepted/Published Online: 08.05.2016 Final Version: 06.12.2016

Abstract: Climatic and relief factors could limit the distribution of nonmigratory , and especially those that inhabit temperate areas. The limitations are stronger for habitat specialist species and a good understanding of these influences can contribute significantly to the development of conservation measures to protect them. The European ground (Spermophilus citellus) is a small inhabiting pastures and areas of short herbaceous vegetation from Central and Southeastern Europe with limited data about their colony site selectivity. During the first wide survey of the European ground squirrel in Eastern Romania we identified a strong influence of annual precipitation, aspect, slope, vegetation height, and tree/bush coverage on the species’ distribution and density. Lower precipitation values were associated with higher densities of European ground squirrel as well as slope. The same relationship was found with vegetation height and the amount of tree and bush coverage. The European ground squirrel uses areas with a southern and eastern aspect and slopes with a higher gradient. The elevation and the summer-winter temperatures do not have a significant influence on European ground squirrel colonies. Our results will contribute to the species’ conservation across its distribution range and will help to determine the most appropriate sites for future relocation and repopulation programs.

Key words: Small mammal, habitat selection, pasture management, conservation

1. Introduction artificial habitats, such as lawns, sports fields, and golf Habitat selection influences an organism’s subsequent courses, which have light, well-drained soils where it can choice concerning food availability, nest, risk of predation, excavate its burrows (Váczi and Altbäcker, 1999; Özkurt et and mating opportunities (Orians and Wittenberger, al., 2005; Janderková et al., 2011). The natural conditions 1991). It will choose the habitat first and then make of its prime habitats are lost when grassland is converted successive decisions about the use of different sections or into arable land and sometimes forest. Another important microhabitats within it (Prevedello et al., 2010). Depending limiting factor is when grazing ceases, leading to the on environmental factors and the species’ adaptations, the growth of tall-grassy areas and scrubland. In western resulting individuals use specific habitat features and avoid parts of the European ground squirrel’s distribution range others. more and more colonies are occupying artificial habitats The European ground squirrel (Spermophilus citellus) (Hoffmann et al., 2003, Baltag et al., 2015), but in eastern is a small mammal inhabiting pastures and short grassy areas the species is still keeping to its natural habitat due areas from Central and Eastern Europe (Baltag et al., 2015). to its availability and also the presence of the migrating Dating back to the Middle Pleistocene, the European corridors (Baltag et al., 2015). ground squirrel shows three highly divergent phylogenetic The European ground squirrel population is in lineages that are all under conservation concerns due to continuous decline across its geographical range. The their declining trends (Kryštufek et al., 2009). Depending species decline is suspected to be more than 30% over on the local environmental conditions, the European the last 10 years (Coroiu et al., 2008). For this reason ground squirrel distribution could be influenced by specific the species is assessed as Vulnerable (A2bc) by the limiting factors in different parts of its range (Koshev and International Union for Conservation of Nature and Kocheva, 2007). The European ground squirrel is restricted Natural Resources (Botnariuc et al., 2005; Coroiu et al., to short-grass steppe and pastures, or even completely 2008). The European ground squirrel is a poorly studied * Correspondence: [email protected] 917 ZAHARIA et al. / Turk J Zool species in Romania. However, in recent years, a few 5–10 cm; 3) 10–15 cm, and 4) over 15 cm. For tree and surveys have been conducted in the Pannonian Plain shrub coverage we defined three categories: 1) 0%–5%; revealing a much steeper decline in its population than has 2) 5%–10%, and 3) over 10%. For the data for relief been recorded in the western parts of its European range variables (altitude, slope gradient, and aspect) we used the (Hegyeli et al., 2012). Shuttle Radar Topography Mission (SRTM) 90 m Digital In order to be able to quantify the European ground Elevation Model Dataset (Jarvis et al., 2008). The climatic squirrel’s decline and to build a conservation strategy to variables and precipitation and temperature data were counteract this negative trend we need to understand accessed using the WorldClim database (Hijmans et al., the species’ requirements for building up its colonies. It 2005), which gives climatic data as the average of multiple is important to know why a species prefers a particular years’ records. The data regarding geographic and climatic area in order to explain the existence of colonies and features were extracted for each surveyed square using their dynamics, but also to understand why many are spatial analysis tools from Arc GIS v9.3 software. disappearing. This study analyzes the habitats and A generalized linear model (GLM) approach was used to geographic and climatic features that allow European determine the influence of altitude, slope gradient, aspect, ground squirrels to occupy an area, such as vegetation vegetation height, tree and shrub cover, temperature, and height, tree and shrub cover, altitude, slope gradient, precipitation on European ground squirrel colonies in aspect, temperature, and precipitation, in order to clarify Eastern Romania. Calculations were made in R statistical the species selection of colony sites. software, v3.1 (R Development Core Team, 2012)

2. Materials and methods 3. Results The study area is located in Eastern Romania (46°48′N, The European ground squirrel’s density and distribution 26°57′E), at the northeastern border of the species’ are strongly influenced by annual precipitation, but also geographical range. This area, covering 27,173 km2, is by aspect, slope, vegetation height, and tree and bush a mix of artificial and natural habitats where the land coverage (Table). The elevation, mean temperature of July, management still uses traditional practices (Baltag, 2013) and mean winter temperature do not have a significant and the species is present in high densities (Baltag et al., influence on European ground squirrel colonies. 2014). Most of the pasture and herbaceous vegetation We analyzed the precipitation quantity in relation to from this area is grazed by livestock. The agricultural land the European ground squirrel’s distribution because it is is mainly cultivated with grains, vegetables, and fodder the basic factor of the humidity value, which influences the plants. Forests are fragmented and distributed mostly soil consistency and also the vegetation. By analyzing the in the central and northern part of our study area. The data collected in 2013 we succeeded in establishing a range rivers create long valleys, which represent ideal dispersal of annual precipitation quantity in areas where ground corridors for small . squirrel has been identified. Therefore, in the Moldova The study was conducted during 1 year (2013), when region, the colonies are found in areas with precipitation 872 survey plots were inventoried (Figure 1). The survey of 474–636 mm per year. Lower precipitation values were squares (250 × 250 m) were randomly chosen using associated with higher densities of European ground Hawth’s Tools for Arc GIS v.9.3. In the survey selection squirrel. process, only pastures or other herbaceous vegetation Other climate factors that were tested for their influence associations were included, according to CORINE Land on European ground squirrel density were the mean Cover (Bossard et al., 2000). During the survey we counted temperature of July and the winter mean temperature. the vertical burrow entrances on transects (3 × 150 m, According to the GLM analysis these two factors do not with 50 m between transects) within a distance of 2.5 m on have a significant influence on the distribution of our target every side of the counted European ground squirrel holes species (Table). However, the European ground squirrel (Katona et al., 2002; Koshev, 2008). Active burrows were colonies occupy areas where the mean temperature in differentiated from old and inactive ones by the presence July ranges from 18 °C to 22 °C. Regarding the winter of fresh soil deposits, runways, and lack of vegetation into temperature, the colonies from Eastern Romanian are the hole. Only active burrows were included in the analysis located in areas where they range between –3.8 °C and to indicate the presence of European ground squirrels. –0.5 °C (with an average of –2.1 °C). During the survey we collected data on two habitat The European ground squirrel density is influenced related variables (vegetation height and tree and shrub by slope gradient and aspect and not by altitude (Table). coverage) in order to analyze the European ground Population density increases with slope from 10.3 squirrel selectivity for these type of factors. The vegetation individuals/ha at a gradient of 0°–4° to 19.4 individuals/ha heights were divided into four categories: 1) 0–5 cm; 2) in areas with slope greater than 12.1°, up to 17°. The density

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Figure 1. The study area location (in the small map marked with black) and the distribution of the surveyed squares (250 × 250 m grids) conducted during the 2013 season in Eastern Romania. also varies according to aspect (Fr = 75.12, P < 0.0001), m). The high elevation survey squares had not only low from 10.7 individuals/ha on southwestern slopes to 15.2 density but also a high proportion of zero observations. individuals/ha on eastern slopes. During the surveys we Above 300 m we surveyed 62% of squares without finding conducted observations at elevations between 5 and 469 any European ground squirrels (Figure 2). However, the m. The density varies with altitude (Fr = 14.18, P < 0.001); elevation does not have a significant influence on European the highest density was recorded at low altitudes (0–150 ground squirrel colonies from Eastern Romania (Table).

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Table. General linear model (GLM, R v.3.1.2) for the density of For our study area, the European ground squirrel density European ground squirrel individuals. Model factors consist of decreases from areas with less than 5% tree and shrub climatic and habitat-related variables according to AIC selection. cover, where the mean density is 15.2 individuals/ha, to Significant P-values (P < 0.05) are in bold. areas with more than 10% tree and shrub cover, for which we recorded a mean density of 10.2 individuals/ha. The Variable No. of individuals P influence of vegetation height and tree and bush coverage Elevation –0.037 0.970 is significant, outlining two important habitat criteria for the existence of European ground squirrel colonies. Slope 2.446 0.014 Aspect –2.517 0.012 4. Discussion Mean temperature (July) 0.434 0.664 This large study area is characterized by a heterogeneity Mean winter temperature 1.724 0.085 of habitat and geographical conditions, which may Precipitations –3.896 0.0001 influence the distribution and density of European Vegetation height –2.097 0.036 ground squirrels. Environmental factors are important for the annual trend in ground squirrels (Schwanz, 2006). Tree and bush cover –2.166 0.030 Climatic variables could influence, directly or indirectly, a sedentary species such as the European ground squirrel. According to our analyses, a higher density of European In Eastern Romania, European ground squirrels prefer ground squirrels is associated with a lower precipitation natural or seminatural habitats, especially pastures with quantity. Approximately the same range, 500–700 mm, very short vegetation (Figure 2). The highest densities was recorded in localities with European ground squirrels were recorded in areas with vegetation up to 10 cm tall. colonies from , the , and , Occasionally, the species was also found in hayfields, but for the last two countries precipitation can reach up to where the vegetation height frequently exceeds 20 cm. 1000 mm per year (Koshev and Kocheva, 2007; Janák et Most of these areas were used for pasture in past years, al., 2013). The annual precipitation quantity differs across but due to recently reduced grazing or the absence of the species range, from 550–650 mm per year in grazing altogether the vegetation has started to develop. to 600–800 mm per year in (Straschil, 1972; Janák The population density of European ground squirrels et al., 2013). In eastern parts of Romania the highest decreases with an increase in trees and shrub coverage. densities (26.4 individuals/ha) are found in areas with

Figure 2. The European ground squirrel density (individuals/ha) variation against vegetation height measured in 872 surveyed squares (250 × 250 m grids) conducted during the 2013 season in Eastern Romania.

920 ZAHARIA et al. / Turk J Zool low precipitation quantity (450–500 mm/year), while the 19 °C and 22 °C for July mean temperature, depending lowest density (4.1 individuals/ha) were recorded in areas on the latitude and altitude (Călinescu, 1956). The mean with 601–650 mm of precipitation. These data confirm the July temperature values recorded in Eastern Romania are European ground squirrel’s selection of those areas with almost the same; the lower limit is just one degree less, low rainfall. However, arid years can alter the vegetation at 18 °C. The mean July temperature range is similar to structure, causing some plant species to disappear or those of other colonies from the same latitude. However, even see the degradation of the projective vegetation we did not find a significant influence of this variable on cover. These habitat modifications could cause behavioral European ground squirrel density and distribution. This changes or fluctuations in a colony’s density. For instance, lack of influence is probably caused by small differences in dry years lead the yellow ground squirrel (Spermophilus temperature across the study area. fulvus), an Asiatic species, to enter its burrow earlier for European ground squirrels construct and hibernate (Neronov and Shilova, 2012). The influence in burrows. The species’ survival success depends on of precipitation was also detected for North American the hibernaculum temperature and winter length. For species. The body size of the California ground squirrel this reason we integrate the winter temperature in our (Spermophilus beecheyi) declines during years with heavy analyses. European ground squirrel colonies are found rainfall (Blois et al., 2007). particularly in those areas with mild winters (–1 °C to –3 Extreme environmental events such as heavy rainfall °C; Koshev and Kocheva, 2007). In Eastern Romania, the can kill high numbers of European ground squirrels or European ground squirrel colonies are distributed in areas even destroy whole colonies. Flooding is becoming a more with winter mean temperature over –3.8 °C, even if in our common occurrence in recent years and this hydrological study area the temperature at ground level drops down to phenomenon sometimes covers large valleys in the –8 °C (Ion et al., 2011). A high temperature during winter southern parts of our study area. During the autumn of influences the number of ground squirrels surviving their hibernation (Csongor et al., 2010). Therefore, the highest 2013 we found large colonies in these flooded valleys that density (25 individuals/ha) was recorded in areas with were partially destroyed. The vulnerability of the European winter temperatures between –0.5 °C and –1 °C. However, ground squirrel to flooding has also been recorded due to a low variation in winter mean temperature across in Bulgaria (Koshev, 2008) and Austria (Hoffmann et the study area, this factor does not have a significant al., 2003). Additionally, the high amount of snow and influence on European ground squirrel distribution. mild temperatures during the beginning of spring can Most of the identified colonies from Eastern Romania be dangerous because it raises the ground water level, are situated along river valleys, which are the most potentially flooding their hibernation chambers (Janák et important dispersal corridors for this species (Koshev, al., 2013). 2008). In these areas they use high slope gradients to build High temperatures and a dry climate are well tolerated burrows and flat areas for feeding. High slope gradients by European ground squirrels and if the temperature are associated with higher European ground squirrel goes to extremes they can avoid it by retreating into densities. When the colonies are on flat areas, near rivers their burrows (Váczi, 2005; Váczi et al., 2006). Higher or lakes, the burrows are built on higher structures (dykes, than average summer temperatures may cause periods embankments, mounds) in order to avoid flooding of lethargy (Koshev and Kocheva, 2007). Due to their vulnerability. This microtopography selection is influenced selectivity for hot and dry continental summers the overall not only by flooding risk but also by a better view of distribution of ground squirrels in Europe is limited by July predators. The same result was obtained by Barker and mean temperatures, which should be higher than 19 °C Derocher (2010) for Artic ground squirrels (Spermophilus (Werth, 1932). The European ground squirrels can occupy parryii), proving selection for well-drained habitats and areas with lower July mean temperatures, especially in the sloped or convex terrain. western geographical range. At the northwestern limit of the Slopes that have a western, southwestern, northern, species’ distribution (Slovakia and the Czech Republic), it and northwestern orientation are characterized by a can be found in areas with mean July temperatures starting higher atmospheric and edaphic humidity, which favors from 17 °C (Janak et al., 2013). Also, in Austria and former landslides (Ion et al., 2011), representing unsuitable areas Poland distributions, European ground squirrel colonies to establish colonies. A southern and eastern facing slope were found in areas with July mean temperatures of more (more open to sunlight and warm winds) will be warmer than 18 °C (Janak et al., 2013). Even if it can be found in and dryer due to higher levels of evapotranspiration than areas with mean July temperatures lower than 19 °C, the a north-facing slope (Bennie et al., 2006). Because of highest densities occupy warmer areas from the Czech this microclimate, southern and eastern slopes positively Republic, Slovakia, Poland, and Austria (Grulich, 1960; influence the density of the European ground squirrel Straschil, 1972). In Romania the colonies spread between colonies from Eastern Romania.

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European ground squirrels use low-lying areas of land of tree and shrub coverage provides many perches for birds (below 300 m a.s.l.) to settle their colonies in Eastern of prey, becoming a limiting factor for the European ground Romania. While we made surveys at higher altitudes, we squirrels. This specific habitat requirement was also seen only found our target species in 38% of the squares. The with the long-tailed ground squirrel, which tolerates only same result was obtained by Călinescu (1956) in his studies a small density of trees and bush vegetation (Ricankova et on the Romanian population of European ground squirrels. al., 2006). Furthermore, the majority of colonies (82.5%) from Bulgaria In the Czech Republic, the species does not depend on a are located at altitudes below 500 m a.s.l., and in the Czech specific plant or vegetation assemblage (Matějů et al., 2011), Republic the average altitude is 317 m a.s.l. (Koshev and nor does it require a particular soil type (Janderková et al., Kocheva, 2007; Matějů et al., 2008). However, according to 2011), but a reduction in grazing intensity together with the our study, the elevation does not have a significant influence effect of high slope inclination and northern aspect change on species density and distribution, the same result being the plant community structure, leading to increases in how obtained by Ricankova et al. (2006) for long-tailed ground long they have to forage and decreases of the nutritional squirrels (Spermophilus undulatus). The highest altitude at value of their food (Amezaga et al., 2004). Grazing, mowing, which the species was identified in Bulgaria is 2592 m a.s.l., and limiting succession of trees and shrubs are measures in the Rila Mountains (Janak et al., 2013), but in Bulgaria apt to maintain the species’ habitat. The species’ most the climate is softer compared to our study area. However, suitable habitats (pastures, steppe areas) across Central and European ground squirrel colonies at higher altitudes Southeastern Europe are in decline due to their conversion are not common, unlike the Asia Minor ground squirrel to agricultural and built-up areas (Janák et al., 2013; Baltag (Spermophilus xanthoprymnus), which prefers elevations et al., 2015). from 800 to 2900 m a.s.l. (Gür and Gür, 2010). Our results are limited by the scope of the studied area, Being a species characteristic of open habitats, European which may reduce the influence of some variables such ground squirrels depend on short vegetation, which makes as altitude. For example, because we selected the Extra- them able to easily detect the predators (Baltag et al., 2015). Carpathian Region for surveys, it led to a low representation A higher vegetation cover can obstruct the ground squirrel’s of high elevations in our analysis. However, overall, view of its surroundings. Being a small mammal and an this study is able to improve the species’ conservation important prey for a large variety of meat-eaters (Baltag strategy through a better understanding of the ecology et al., 2015), detecting predators is an essential condition of the European ground squirrel, especially climatic, for its survival. The European ground squirrel selects areas relief, and habitat selection. These data could be used for with low vegetation height and its numbers decrease as broadening the important areas for species conservation vegetation height increases. Short vegetation selectivity was and increasing the success of forthcoming relocations also recorded in Macedonia (Kryštufek, 1993) and the Czech or introduction programs. Given the present situation Republic (Matějů et al., 2011). In Macedonia, the European of the European ground squirrel trend in Romania and ground squirrel is linked to heavily grazed mountain in Europe, conservation measures are urgently required pastures and it is being affected by the decline in livestock to be implemented in order to stop the species’ decline. grazing (Kryštufek et al., 2012). The Artic ground squirrel, Otherwise, the conservation status could be changed to a which inhabits tundra, alpine meadows, and clearings more dramatic category. within boreal forests (Woods, 1991), also uses areas with low vegetation, together with sloped terrain that offers more Acknowledgments effective vigilance behavior (Barker and Derocher, 2010). We wish to thank Lucian Eugen Bolboacă, Lucian Fasolă, The same habitat (low vegetation) and slope gradient is used Sergiu Pleșcan, and Constantin Ion for their help during the by long-tailed ground squirrels, whose optimal vegetation is survey program and also Zsolt Hegyeli for his suggestions in up to 10 cm in height (Ricankova et al., 2006). Pastures with data analysis. We also thank the editor and two anonymous tall grasses are also likely to be detrimental to Richardson’s reviewers for their constructive comments, which helped ground squirrel ( richardsonii; Downey et al., to improve the manuscript. This work was supported by 2006), a North American species. Because of their habitat the Conservation Leadership Programme, Idea Wild, and selection, regular grazing in order to keep a short vegetation the strategic grant POSDRU/159/1.5/S/133391, Project− cover should be an important conservation activity in those Doctoral and Post-Doctoral Programs of Excellence for areas with European ground squirrel colonies. Highly Qualified Human Resources Training for Research Population density of European ground squirrels in the Field of Life Sciences, Environment and Earth Science, decreased with an increase in tree and shrub coverage. For cofinanced by the European Social Fund within the Sectorial our study area, the highest density (15.2 individuals/ha) Operational Program Human Resources Development was in areas with less than 5% cover. A higher percentage 2007–2013. The study complied with Romanian laws.

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