Conservation Genetics

, Volume 9, Issue 3, pp 615–625 | Cite as

Population genetic structure of the European ground squirrel in the Czech Republic

  • Štěpánka HulováEmail author
  • František Sedláček
Research Article


The European ground squirrel (Spermophilus citellus) is considered an endangered species with declining numbers throughout Europe, most pronounced at the western margin of its distribution area. Being extinct in Germany and Poland, the western margin of its distribution is in the Czech Republic. Here, landscape fragmentation has restricted the ground squirrels into few and very isolated localities where local extinctions still occur. In the present study we analysed European ground squirrels from six Czech and one Slovak localities using five microsatellite loci as genetic marker. The results show a strong genetic differentiation among the investigated populations (mean value of F ST = 0.16) and high levels of inbreeding (values of F IS ranged from 0.34 to 0.90). High level of inbreeding is generally considered to affect the viability of each population, which could lead to extinction. One of the most important factors is the lack of migration due to the large distances between the populations and the presence of migration barriers. Based on the results obtained we recommend a few suggestions for a conservation management of this species.


Ground squirrel Habitat fragmentation Inbreeding Microsatellites 



Permission to catch and sample specimens was given by the Ministry of Environment of the Czech Republic (permission no. 11295/02 OOP/2986/02 V1028). We are very thankful to the colleagues at the Laboratory of Fish Genetics, the Institute of Animal Physiology and Genetics, Liběchov, the Academy of Sciences of the Czech Republic, especially to Vendula Šlechtová, Vlastimil Šlechta and Peter Ráb for their support in laboratory work. We would also like to thank Vendula Šlechtová, Jöerg Bohlen, Josef Bryja and the two anonymous referees for useful comments on the manuscript. The authors acknowledge other people who helped during the birth of this study: Michal Berec, David Boukal, Petra Judy Cehláriková, Jan Matějů, František Marec, Peter Mikulíček, Zdeněk Lajbner, Dana Schröffelová and Jan Vondrák. This project was supported by a grant of the Czech Science Foundation (GAČR) no. 206/04/0254.


  1. Ambros M (1995) Projekt záchrany sysl'a obyčajného a súčasné poznatky o jeho rozšíření na Slovensku [Conservation project of the European ground squirrel and its current distribution in Slovakia] Výzkum a ochrana cicavcov na Slovensku 2:99–102 [Mammals Research and Conservation in Slovakia] (in Slovak)Google Scholar
  2. Ambros M (2000) Návrh genofondovej siete lokalít sysľa pasienkového (Spermophilus citellus L.) na Slovensku. [Proposal for genofund network of the European ground squirrel sites in Slovakia] Výzkum a ochrana cicavcov na Slovensku 4:99–105 [Mammals Research and Conservation in Slovakia] (in Slovak, with the abstract in English)Google Scholar
  3. Anděra M (2003) Sysel obecný [European ground squirrel]. Vesmír 82(9):518–521 (in Czech)Google Scholar
  4. Anděra M, Hanzal V (1995) Projekt “Sysel”. Podúkol A: Mapování výskytu sysla obecného (Spermophilus citellus) na území České republiky, Zpráva o řešení I. a II. etapy, 1994–1995, 41 pp. [Project “Ground squirrel”. Subtask A: Mapping of the occurrence of the European ground squirrel (Spermophilus citellus) in the Czech Republic. Interim report on 1st and 2nd phases] (in Czech)Google Scholar
  5. Anděra M, Horáček I (1982) Poznáváme naše savce [Get to know our mammals], Mladá Fronta Praha, 256 pp (in Czech)Google Scholar
  6. Balasz P (2000) Poznámky k príčinám ústupu sysľa pasienkového stredoeurópského (Spermophilus citellus citellus L.). [Notes on the causes of the decline of the European ground squirrel] Výzkum a ochrana cicavcov na Slovensku 4:107–109 [Mammal Research and Conservation in Slovakia] (in Slovak, with the abstract in English)Google Scholar
  7. Bárta Z (1992) Poslední syslové obecní, Spermophilus citellus L., na Mostecku. [Die letzten Zieseln bei Most] Sborn. Severočec. Muz.- Přír. Vědy, Liberec, 18:151–154 [Proc. North-Bohemian Mus. – Nat. Hist.] (in Czech, with the summary in German)Google Scholar
  8. Baruš V, Bauerová Z, Kokeš J, Král B, Lusk S, Pelikán J, Sládek J, Zejda J, Zima J (1988) Červená kniha ohrožených a vzácných druhů rostlin a živočichů ČSSR. Státní zemědělské nakladatelství. 90–91 [Red List of Vertebrates of Czechoslovakia] (in Czech)Google Scholar
  9. Belkhir K, Borsa P, Chicki L, Raufaste N, Bonhomme F (1996) GENETIX 4.02, logiciel sous Windows TM pour la génétique des populations. Montpellier: Laboratoire Génome, Populations, interactions, CNRS UMR 5000, Université de Montpellier IIGoogle Scholar
  10. Budayová J (1995) Skúšenosti z repatriáce sysla obyčajného v Košickej Kotlině. [Experiences with repatriation of the European souslik in Košická Basin]. Výskum a ochrana cicavcov na Slovensku 2:103–107 [Mammal Research and Conservation in Slovakia] (in Slovak, with the summary in English)Google Scholar
  11. Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Evolution 21:550–570CrossRefGoogle Scholar
  12. Cepáková E, Hulová Š (2002) Current distribution of the European souslik (Spermophilus citellus) in the Czech Republic. Lynx 33:89–103Google Scholar
  13. Excoffier L, Slatkin M (1998) Incorporating genotypes of relatives into a test of linkage disequilibrium. Am J Hum Genet Jan 62(1):171–180CrossRefGoogle Scholar
  14. Favre L, Balloux F, Goudet J, Perrin A (1997) Female-biased dispersal in the monogamous mammal (Crocidura russula): evidence from field data and microsatellite patterns. Proce Roy Soc Lond B 264:127–132CrossRefGoogle Scholar
  15. Feiler A (1988) Über das ehemalige Zieselvorkommen in der DDR (Rodentia, Sciuridae, Spermophilus citellus L. 1766). Rudolfstädter naturhistorischen Schriften 1:115–118Google Scholar
  16. Felsenstein J (1993) PHYLIP (Phylogeny Inference Package) version 3.5c. Distributed by the author. Department of Genetics, University of Washington, SeattleGoogle Scholar
  17. Frankel OH, Soulé ME (1981) Conservation and evolution. Cambridge University Press, Cambridge, UKGoogle Scholar
  18. Frankham R, Ballou JD, Briscoe DA (2004) A primer of conservation genetics. Cambridge University Press, Cambridge, UKGoogle Scholar
  19. Garner A, Rachlow JL, Waits LP (2005) Genetic diversity and population divergence in fragmented habitats: Conservation of Idaho ground squirrel. Conserv Gen 6:759–774CrossRefGoogle Scholar
  20. Gavin TA, Sherman PW, Yensen E, May B (1999) Population genetic structure of the northern Idaho ground squirrel (Spermophilus brunneus brunneus). J Mamm 80(1):156–168CrossRefGoogle Scholar
  21. Gilpin ME, Soulé ME (1986) Minimum viable populations. In: Gilpin ME, Soulé ME (eds) Conservation biology, the science of scarcity and diversity. Sinauer Association, Inc., Sunderland, MA, pp 19–34Google Scholar
  22. Goodman D (1987) The demography of chance extinction. In: Soulé ME (ed) Viable populations for conservation. Cambridge University Press, Cambridge, UK, pp 11–34Google Scholar
  23. Goossens B, Chikhi L, Taberlet P, Waits LP, Allainé D (2001) Microsatellite analysis of genetic variation among and within Alpine marmot populations in the French Alps. Mol Ecol 10:41–52PubMedCrossRefGoogle Scholar
  24. Grulich I (1960) Sysel obecný Citellus citellus L. v ČSSR. [European ground squirrel Citellus citellus L. in Czechoslovakia]. Práce brněn. Zákl. ČSAV 32(11):473–563 (in Czech, with the summary in English)Google Scholar
  25. Guo SW, Thompson EA (1992) Performing the exact test of Hardy Weinberg proportion for multiple alleles. Biometrics 48:361–372PubMedCrossRefGoogle Scholar
  26. Hanski I (1999) Metapopulation ecology. Oxford University Press, Oxford, UKGoogle Scholar
  27. Hanslik S, Kruckenhauser L (2000) Microsatellite loci for two European sciurid species (Marmota marmota, Spermophilus citellus). Mol Ecol 9:2163–2165PubMedCrossRefGoogle Scholar
  28. Hartl DL, Clark AG (1997) Principles of population genetics. Sinauer Ass., Sunderland, MassGoogle Scholar
  29. Harris JH, Leitner P (2005) Long-distance movements of juvenile Mohave ground squirrels, Spermophilus mohavensis. Southwestern Nat 50(2):188–196CrossRefGoogle Scholar
  30. Hess G (1996) Disease in metapopulation models: implications for conservation biology. Ecology 77:1617–1632CrossRefGoogle Scholar
  31. Jansová A (1992) Projekt na záchranu sysla v Českém krasu. [Conservation project of the ground squirrel in Český kras- Protected Area], In: Metody a výsledky studia drobných savců [Methods and results of studies of small mammals] Sborník příspěvků z pracovní conference, Nasavrky, pp. 31–34. (in Czech, with the summary in English)Google Scholar
  32. Kosnar J (1979) Biologie rozmnožování, populační dynamika a etologie sysla obecného (Citellus citellus). [The biology of reproduction, population dynamics, and etiology of the European ground squirrel] Master Thesis, Faculty of Science, Charles University in Prague, Department of Zoology, 154 pp (in Czech)Google Scholar
  33. Kratochvíl J (1964) K poznání teritoríí sysla obecného (Citellus citellus) [The knowledge of the territories of the European ground squirrel]. Folia Zoologica 13:99–106 (in Czech)Google Scholar
  34. Kruckenhauser L, Pinsker W (2004) Microsatellite variation in autochthonous and introduced populations of the Alpine marmot (Marmota marmota) along a European west-east transect. J Syst Evol Res 42:19–26CrossRefGoogle Scholar
  35. Lacy RC (1993) Impact of inbreeding in natural and captive populations of vertebrates: implications for conservation. Perspect Biol Med 36:480–496Google Scholar
  36. Lacy RC, Lindenmayer DB (1995) Effectiveness of selection in reducing the genetic load in populations of Peromyscus polionotus during generations of inbreeding. Evolution 52:900–909CrossRefGoogle Scholar
  37. Lomolino MV, Smith GA (2000) Dynamic biogeography of prairie dog (Cynomys ludovicianus) towns near the edge of their range. J Mamm 82:937–945CrossRefGoogle Scholar
  38. Ložek V (1973) Příroda ve čtvrtohorách [Nature in Quaternary]. Academia (in Czech)Google Scholar
  39. Mantel A (1967) The detection of disease clustering and generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  40. May B, Gavin TA, Sherman PW, Korves TM (1997) Characterization of microsatellite loci in the Northern Idaho ground squirrel Spermophilus brunneus brunneus. Mol Ecol 6:399–400PubMedCrossRefGoogle Scholar
  41. McCullough DR (1996) Metapopulations and wildlife conservation. Island Press, Covelo, CaliforniaGoogle Scholar
  42. Meczynski S (1985) Does the European Ground Squirrel, Spermophilus citellus L. 1766, still occur in Poland? Przeglad Zoologiczny 29(4):521–526Google Scholar
  43. Mitchell-Jones AJ, Amori G, Bogdanowicz W, Kryštufek B, Reijnders PJH, Spitzenberger F, Stube M, Thissen JBM, Vohralík V, Zima J (1999) The atlas of European mammals. Academic Press, LondonGoogle Scholar
  44. Neumann K, Jansman H, Kayser A, Maak S, Gattermann R (2004) Multiple bottlenecks in threatened western European populations of the common hamster cricetus cricetus (L.). Conserv Gen 5:181–193CrossRefGoogle Scholar
  45. Nowak RM (1999) Walker’s mammals of the World, 6th edn, vol 2. The John Hopkins University Press, Baltimore, MarylandGoogle Scholar
  46. Page RDM, Holmes EC (1998) Molecular evolution—a phylogenetic approach. Cambridge University, UKGoogle Scholar
  47. Ralls K, Ballou JD, Templeton AR (1988) Estimates of lethal equivalents and the cost of inbreeding in mammals. Cons Biol 2:185–193CrossRefGoogle Scholar
  48. Rejl J (1997) Sysel obecný (Spermophilus citellus)- vyhynulý druh východočeské fauny [European ground squirrel- extinct species of Eastern Bohemia]. Vč. Sb. Přír.- Práce a studie 5:171–174 [EB Proc. Nat. Hist. Works and Studies] (in Czech with the summary in English)Google Scholar
  49. Roach JL, Stapp P, Van Horne B, Antolin M (2001) Genetic structure of a metapopulation of black-tailed prairie dogs. J Mamm 82(4):946–959CrossRefGoogle Scholar
  50. Ružič A (1978) Citellus citellus (Linnaeus, 1726)- Der oder das Europäische Ziesel. In: Niethhammer J, Krapp F (eds) Handbuch der Säugertiere Europas, Bd. 1. Wiesbaden, Akademische Verlasgesellsch, pp 123–144Google Scholar
  51. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbour Laboratory Press, New YorkGoogle Scholar
  52. Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2.000: software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, SwitzerlandGoogle Scholar
  53. Schonewald-Cox CM, Chambers SM, MacBryde B, Thomas L (eds) (1983) Genetics and conservation. Benjamin/Cummings, Menlo Park, CalifGoogle Scholar
  54. Smouse PE, Long JC, Sokal RR (1986) Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Syst Zool 35:627–632CrossRefGoogle Scholar
  55. Soulé ME (ed.) (1987): Viable populations for conservation. Cambridge Univ. Press., Cambridge, UKGoogle Scholar
  56. Swofford DL, Selander RB, Black WC (1997) boisys-2: a computer program for the Analysis of allellic variation in genetics, Ft. Collins, COGoogle Scholar
  57. Van Treuren R, Bijlsma R, Ouborg NJ, Van Delden W (1993) The significance of genetic erosion in the process of extinction. III. Inbreeding depression and heterosis effects due to selfing and outcrossing in Salvia pratensis and Scabiosa. Evolution 47:1669–1680CrossRefGoogle Scholar
  58. Van Treuren R, Bijlsma R, Van Delden W, Ouborg NJ (1991) The significance of the genetic erosion in the process of extinction. I. Genetic differentiation in Salvia pratensis and Scabiosa columbaria in relation to population size. Heredity 66:181–189CrossRefGoogle Scholar
  59. Wilcove DC, McClelland M, Dobson A (1986) Habitat fragmentation in the temperate zone. In: Soulé ME (ed) Conservation Biology: the Science of Scarcity and Diversity. Sinauer, Sunderland, MA, pp 237–256Google Scholar
  60. Wright S (1943) Isolation by distance. Genetics 28:139–156PubMedGoogle Scholar
  61. Wright S (1969) The theory of gene frequencies. Evolution and the genetics of populations, vol 2. University of Chicago Press, ChicagoGoogle Scholar
  62. Wright S (1978) Evolution and the genetics of population, vol 4. Variability among and within natural populations. University of Chicago Press, ChicagoGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.University of South Bohemia, Faculty of Biological SciencesČeské BudějoviceCzech Republic
  2. 2.Institute of Animal Physiology and Genetics, Academy of Sciences of the Czech RepublicLiběchovCzech Republic
  3. 3.Institute of Systems Biology and Ecology AS CRČeské BudějoviceCzech Republic

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