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

Authors

DOI:

https://doi.org/10.2298/ABS201231007A

Keywords:

grasslands, dietary preferences, hibernators, microhistology, habitat management

Abstract

Paper description:

 

Abst

  • Overwinter survival of hibernators is influenced by the amount and quality of food consumed during the active season.
  • Microhistological analysis of feces was used to establish the feeding habits of the European ground squirrel (Spermophilus citellus) in northern Serbia, a region that has experienced human-induced environmental changes during the last 7 decades.
  • Whereas a number of different species appear in the diet, there is clear preference for a small number of food categories.
  • Considering the predicted impact of climate change on food availability for this species, its feeding habits should be taken into account when developing habitat management plans.

ract: 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.

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References

Mátrai K, Altbäcker V, Hahn I. Seasonal diet of rabbits and their browsing effect on juniper in Bugac Juniper Forest (Hungary). Acta Theriol. 1998;43(1):107-12.

Győri-Koósz B, Katona K, Altbäcker V. Az ürge (Spermophilus citellus) étrendjének vizsgálata legelt és kaszált gyepterületeken [Diet composition of European Ground Squirrel in grazed or mowed grasslands]. Magyar Apróvad Közlemények. 2013;11:215-25. Hungarian.

Lodé T. Polecat predation on frogs and toads at breeding sites in western France. Ethol Ecol Evol. 1996;8(2):115-24.

Steenhof K, Yensen E, Kochert MN, Gage KL. Populations and habitat relationships of Piute ground squirrels in southwestern Idaho. West N Am Nat. 2006;66(4):482-91.

Reichlin T, Klansek E, Hackländer K. Diet selection by hares (Lepus europaeus) in arable land and its implications for habitat management. Eur J Wildl Res. 2006;52(2):109-18.

Demment MW, Van Soest PJ. A nutritional explanation for body size patterns of ruminant and non-ruminant herbivores. Am Nat. 1985;125(5):641-72.

Váczi O. The effects of abiotic environmental factors on spatio-temporal activity pattern of the European ground squirrel (Spermophilus citellus) [dissertation]. Budapest: Eötvös Loránd University. 2005. 131p. Hungarian.

Yensen E, Shock B, Tarifa T, Evans Mack D. Forbs Dominate Diets of the Threatened Endemic Northern Idaho Ground Squirrel (Urocitellus brunneus). Northwest Sci, 2018;92(4):290-310.

Smith GW, Johnson DR. Demography of a Townsend ground squirrel population in southwestern Idaho. Ecology. 1985;66(1):171-8.

Dobson FS, Risch TS, Murie JO. Increasing returns in the life history of Columbian ground squirrels. J Anim Ecol. 1999;68:73-86.

Risch TS, Michener GR, Dobson FS. Variation in litter size: a test of hypotheses in Richardson’s ground squirrels. Ecology. 2007;88(2):306-314.

Sherman PW, Runge MC. Demography of a population collapse: the northern Idaho ground squirrel (Spermophilus brunneus brunneus). Ecology. 2002;83(10):2816-31.

Grulich I. Sysel obecný Citellus citellus L. v ČSSR. Práce Brněnské základny ČSAV. 1960;32(11): 473-563. Czech.

Strauss A, Hoffmann IE, Millesi E. Effects of nutritional factors on juvenile development in male European ground squirrels (Spermophilus citellus). Mamm Biol. 2007;72(6):354-63.

Janák M, Marhoul P, Matějů J. Action Plan for the Conservation of the European Ground Squirrel Spermophilus citellus in the European Union [Internet]. European Commission. 2013. [cited 2021 Feb 6]. Available from: https://ec.europa.eu/environment/nature/conservation/species/action_plans/pdf/EUSAP_EuropeanGround%20Squirrel_Final.pdf

Carpaneto GM, Mazziotta A, Pittino R, Luiselli L. Exploring co-extinction correlates: the effects of habitat, biogeography and anthropogenic factors on ground squirrels-dung beetles associations. Biodivers Conserv. 2011;20(13):3059-76.

Ramos-Lara N, Koprowski JL, Kryštufek B, Hoffmann IE. Spermophilus citellus (Rodentia: Sciuridae). Mamm Species. 2014;46(913):71-87.

Lindtner P, Ujházy K, Svitok M, Kubovčík V. The European ground squirrel increases diversity and structural complexity of grasslands in the Western Carpathians. Mammal Res. 2018;63:223-9.

Lindtner P, Svitok M, Ujházy K, Kubovčík V. Disturbances by the European ground squirrel enhance diversity and spatial heterogeneity of plant communities in temperate grassland. Biodivers Conserv. 2020;29:853-67.

Hegyeli, Z. Spermophilus citellus. The IUCN Red List of Threatened Species [Internet]. International Union for the conservation of nature. 2020. [updated 2019 Sep 8; cited 2021 Feb 6]. Available from: https://dx.doi.org/10.2305/IUCN.UK.2020-2.RLTS.T20472A91282380.en.

Ćosić N, Říčanová Š, Bryja J, Penezić A, Ćirović D. Do rivers and human-induced habitat fragmentation affect genetic diversity and population structure of the European ground squirrel at the edge of its Pannonian range? Conserv Genet. 2013;14(2):345-54.

Ćosić N. Vijabilnost populacija tekunice Spermophilus citellus (L., 1766) na području Srbije [dissertation]. Belgrade; University of Belgrade; 2015. 111p.

Nikolić T, Radišić D, Ćosić N, Díaz-Delgado R, Milić D, Vujić A, Ćirović D. Landscape heterogeneity effects on keystone rodent species: agro-ecological zoning for conservation of open grasslands. Biodivers Conserv. 2019;28(12):3139-58.

Nikolić T, Arok M, Radišić D, Mirč M, Velaja L, Milić D, Ćirović D. Endangered species’ trait responses to environmental variability in agricultural settings. Arch Biol Sci. 2020;72(1):13-21.

Ružić A. Prilog poznavanju ekologije tekunice Citellus citellus L. Zbor Rad Instit Ekol Biogeog SANU. 1950;97(1):97-140. Serbian.

Matějů J, Hulová Š, Nová P, Cepáková E, Marhoul P, Uhlíková J. Action plan for the European Ground Squirrel (Spermophilus citellus) in the Czech Republic. Charles University and Agency for Nature and Landscape Protection of the Czech Republic; 2010. 80 p.

Herzig-Straschil B. Nahrung und Nahrungserwerb des Ziesels. Acta Theriol. 1976;21:131-9. German.

Puzović S, Panjković B, Tucakov M, Stojnić N, Sabadoš K, Stojanović T, Vig L, Marić B, Tešić O, Kiš A, Galamboš L, Pil N, Kicošev V, Stojšić V, Timotić D, Perić R, Bošnjak T, Delić J, Dobretić V, Stanišić J. Upravljanje prirodnom baštinom u Vojvodini. Novi Sad: Sekretarijat za urbanizam, graditeljstvo i zaštitu životne sredine, Pokrajinski zavod za zaštitu prirode; 2015. 156p. Serbian.

Uredba o ekološkoj mreži. Služb Glasn Rep Srb. 2010;102. Serbian.

Ružić A. Der order das Europäische Ziesel (Citellus citellus). In: Niethammer J, Krapp F, editors. Handbuch der Säugetiere Europas. Wiesbaden: Akademische Verlagsges; 1978. p. 122-44. German.

Maia MJ, Rego F, Machado FS. Determining optimal sampling schemes to study red deer diets by fecal analysis. Silva Lusit. 2003;11(1):91-9.

Paupério J, Alves PC. Diet of the Iberian hare (Lepus granatensis) in a mountain ecosystem. Eur J Wildl Res. 2008;54(4):571-9.

Van Horne B, Schooley RL, Sharpe PB. Influence of habitat, sex, age, and drought on the diet of Townsend’s ground squirrels. J Mammal. 1998;79(2):521-37.

Leitner BM, Leitner P. Diet of the Mohave ground squirrel (Xerospermophilus mohavensis) in relation to season and rainfall. West N Am Nat. 2017;77(1):1-13.

Harestad AS. Food habits of Columbian ground squirrels: a comparison of stomach and fecal samples. Murrelet. 1986;67:75-8.

Tischler, W. Grundzüge der terrestrischen Tierökologie. Braunschweig: Friedrich Vieweg und Sohn; 1949. 219 p. German.

Krebs, CJ. Ecological methodology. New York: Harper & Row; 1989.

Yensen E, Quinney DL. Can Townsend’s ground squirrels survive on a diet of exotic annuals? Great Basin Naturalist. 1992;52:269-77.

Spitzenberger F, Bauer K. Ziesel Spermophilus citellus (Linnaeus, 1766). In: Spitzenberger F, editor. Die Saugetierfauna Österreichs. Wien: Grune Reihe des Bundesministeriums fur Land- und Forstwirtschaft, Umwelt und Wasserwirtschaft; 2002. p. 356-65. German.

Dyni EJ, Yensen E. Dietary similarity in sympatric Idaho and Columbian ground squirrels (Spermophilus brunneus and S. columbianus). Northwest Sci. 1996;70(2):99-108.

Tarifa T, Yensen E. Analysis of diets of remnant populations of southern Idaho ground squirrels: the importance of native vs. exotic flora [Annual Report 2003.] Boise: Idaho Department of Fish and Game; 2004.

Tarifa T, Yensen E. Washington ground squirrel diets in relation to habitat condition and population status [Annual report 2003.] Spokane: Bureau of Land Management, Spokane District Office; 2004.

Giorgi A, Bombelli R, Luini A, Speranza G, Cosentino M, Lecchini S, Cocucci M. Antioxidant and cytoprotective properties of infusions from leaves and inflorescences of Achillea collina Becker ex Rchb. Phytother Res. 2009;23(4):540-5.

Goli S, Rahimmalek M, Tabatabaei B. Physicochemical characteristics and fatty acid profile of yarrow (Achillea tenuifolia) seed oil. Int J Agric Biol. 2008;10(3):355-7.

Frank CL. 1992. The influence of dietary fatty acids on hibernation by golden-mantled ground squirrels (Spermophilus lateralis). Physiol Zool. 1992;65(5):906-20.

Florant GL, Hester L, Ameenuddin S, Rintoul AD. The effect of a low essential fatty acid diet on hibernation in marmots. Am J Physiol. 1993;264(4):747-53.

Geiser F, Kenagy GJ. 1993. Dietary fats and torpor patterns in hibernating ground squirrels. Can J Zool. 1993;71(6):1182-5.

Rogers LE, Gano KA. Townsend ground squirrel diets in the shrub-steppe of southcentral Washington. J Range Manag. 1980;33(6):463-65.

Holechek JL. Comparative contribution of grasses, forbs, and shrubs to the nutrition of range ungulates. Rangelands. 1984;6(6):261-3.

Carey HV. Nutritional ecology of yellow-bellied marmots in the White Mountains of California. Holarctic Ecol. 1985;8:259-64.

Stallman EL, Holmes WG. Selective foraging and food distribution of high-elevation yellow-bellied marmots (Marmota flaviventris). J Mammal. 2002;83(2):576-84.

Bennett RP. Effects of food quality on growth and survival of juvenile Columbian ground squirrels (Spermophilus columbianus). Can J Zool. 1999;77(10):1555-61.

Győri-Koósz B. Diet preference of the European ground squirrel [Spermophilus citellus (Linnaeus, 1766)] in Hungarian natural and seminatural grassland habitats investigation by floristic composition and microhistological faeces analysis [dissertation]. Sopron: University of West Hungary; 2015. 16 p.

Haufler JB, Nagy JG. Summer food habits of a small mammal community in the pinyon-juniper ecosystem. Great Basin Nat. 1984;31:145-50.

Hisaw FL, Emery FE. Food selection of ground squirrels, Citellus tridecemlineatus. J Mammal. 1927;8(1):41-4.

Gillis EA, Hik DS, Boonstra R, Karels TJ, Krebs CJ. Being high is better: effects of elevation and habitat on arctic ground squirrel demography. Oikos. 2005;108:231-40.

Řičánková V, Fric Z, Chlachula J, Stastna P, Faltynkova A, Zemek F. Habitat requirements of the long-tailed ground squirrel (Spermophilus undulatus) in the southern Altai. J Zool. 2006;270(1):1-8.

Gedeon CI, Váczi O, Koósz B, Altbäcker V. Morning release into artificial burrows with retention caps facilitates success of European ground squirrel (Spermophilus citellus) translocations. Eur J Wildl Res. 2011;57(5):1101-5.

Thuiller W, Lavorel S, Araújo MB, Sykes MT, Prentice IC. Climate change threats to plant diversity in Europe. Proc Natl Acad Sci. 2005;102(23):8245-50.

Čavlović D, Beloica J, Obratov-Petković D, Đurdević V, Košanin O. Simulation of long-term changes in environmental factors and grassland composition in three protected areas of Serbia. Tuexenia. 2017:431-46.

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Published

2021-03-19

How to Cite

1.
Arok M, Nikolić T, Győri-Koósz B, Milinski L, Ćirović D. Diet of the European ground squirrel (Spermophilus citellus) in the southern Pannonian plain. Arch Biol Sci [Internet]. 2021Mar.19 [cited 2024Nov.24];73(1):111-22. Available from: https://serbiosoc.org.rs/arch/index.php/abs/article/view/6110

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