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Mammalian Biology

, Volume 76, Issue 5, pp 615–621 | Cite as

Genetic diversity of Dinaric brown bears (Ursus arctos) in Croatia with implications for bear conservation in Europe

  • Ivna KocijanEmail author
  • Ana Galov
  • Helena Ćetković
  • Josip Kusak
  • Tomislav Gomerčić
  • Đuro Huber
Original Investigation

Abstract

Brown bears have lost most of their range on the European continent. The remaining western populations are small, isolated and highly endangered. The Dinaric-Pindos brown bear population is the western-most stable population and the fourth largest in Europe. It has been recognized as a potential source for recolonization of populations whose survival is at risk. Indeed, several translocations of Dinaric bears to Italy, Austria and France have recently been made. Despite the importance of the Dinaric bear population, its genetic status remains poorly understood. Using tissue samples from 156 hunted or accidentally killed Dinaric bears in Croatia, this study analysed genetic diversity at 12 microsatellite loci, as well as population structure and past reductions in size. In addition, a subset of 59 samples was used to assess diversity of the mitochondrial DNA control region. The results indicate that Dinaric bears have high nuclear genetic diversity, as compared to other extant brown bear populations, despite genetic evidence of a bottleneck caused by past persecutions. However, haplotype diversity was low, probably as a result of male-biased dispersal and female philopatry. Not surprisingly, no evidence of population sub-structure was found using nuclear markers, as the bear habitat has remained continuous and the highway network has been built only recently. Management should focus on maintaining habitat connectivity and keeping the effective population size as large as possible. In addition, when removing individuals, care should be taken not to further deplete the population of rare haplotypes. A coordinated transboundary management of the entire Dinaric-Pindos brown bear population should be a priority for its long-term conservation.

Keywords

Ursus arctos Dinaric brown bears Genetic diversity Management Conservation 

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References

  1. Belkhir, K., Borsa, P., Chikhi, L., Raufaste, N., Bonhomme, F., 1996–2004. GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier, France.Google Scholar
  2. Bellemain, E., Nawaz, M.A., Valentini, A., Swenson, J.E., Taberlet, P., 2007. Genetic tracking of the brown bear in northern Pakistan and implications for conservation. Biol. Conserv. 134, 537–547.CrossRefGoogle Scholar
  3. Bellemain, E., Taberlet, P., 2004. Improved noninvasive genotyping method: application to brown bear (Ursus arctos) faeces. Mol. Ecol. Notes 4, 519–522.CrossRefGoogle Scholar
  4. Chapron, G., Quenette, P.-Y., Legendre, S., Clobert, J., 2003. Which future for the French Pyrenean brown bear (Ursus arctos) population? An approach using stage-structured deterministic and stochastic models. C. R. Biol. 326 (Suppl. 1), 174–182.CrossRefGoogle Scholar
  5. Clark, J.D., Huber, D., Servheen, C., 2002. Bear reintroductions: lessons and challenges. Ursus 13, 335–346.Google Scholar
  6. Cornuet, J.M., Luikart, G., 1996. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144, 2001–2014.PubMedPubMedCentralGoogle Scholar
  7. Di Rienzo, A., Peterson, A.C., Garza, J.C., Valdes, A.M., Slatkin, M., Freimer, N.B., 1994. Mutational processes of simple-sequence repeat loci in human populations. Proc. Natl. Acad. Sci. U.S.A. 91, 3166–3170.PubMedPubMedCentralCrossRefGoogle Scholar
  8. Evanno, G., Regnaut, S., Goudet, J., 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14, 2611–2620.CrossRefGoogle Scholar
  9. Excoffier, L., Laval, G., Schneider, S., 2005. ARLEQUIN ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinform. Online 1, 47–50.Google Scholar
  10. Ferreira, E., Suoto, L., Soares, A.M.V.M., Fonseca, C., 2009. Genetic structure of the wild boar population in Portugal: evidence of a recent bottleneck. Mamm. Biol. 74, 274–285.CrossRefGoogle Scholar
  11. Fischer, J., Lindenmayer, D.B., 2000. An assessment of the published results on animal relocations. Biol. Conserv. 96, 1–11.CrossRefGoogle Scholar
  12. Frankham, R., Ballou, J.D., Briscoe, D.A., 2002. Genetic management for reintroduction. In: Frankham, R., Ballou, J.D., Briscoe, D.A. (Eds.), Introduction to Conservation Genetics. Cambridge University Press, Cambridge, UK, pp. 448–470.CrossRefGoogle Scholar
  13. Frkovic, A., Ruff, R.L., Cicnjak, L., Huber, D., 1987. Brown bear mortality during 1946-85 in Gorski kotar, Yugoslavia. Int. Conf. Bear Res. Manage. 7, 87–92.Google Scholar
  14. Garza, J.C., Williamson, E.G., 2001. Detection of reduction in population size using data from microsatellite loci. Mol. Ecol. 10, 305–318.PubMedPubMedCentralGoogle Scholar
  15. Hall, T.A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/97/NT. Nucleic Acids Symp. Ser. 41, 95–98.Google Scholar
  16. Hartl, G.B., Hell, P., 1994. Maintenance of high levels of allelic variation in spite of a severe bottleneck in population size — the brown bear (Ursus arctos) in the Western Carpathians. Biodivers. Conserv. 3, 546–554.CrossRefGoogle Scholar
  17. Huber, D., Frković, A., 1993. Brown bear management in Croatia. International Union of Game Biologist Congress 21, 287–292.Google Scholar
  18. Huber, Đ., Jakšić, Z., Frković, A., Štahan, Ž., Kusak, J., Majnarić, D., Grubešić, M., Kulić, B., Sindičić, M., Majić-Skrbinšek, A., Lay, V., Ljuština, M., Zec, D., Laginja, R., Francetić, I., 2008a. Brown Bear Management Plan for the Republic of Croatia. Ministry of Regional Development, Forestry and Water Management, Zagreb, Croatia (accessed 19.07.10) http://www.mrrsvg.hr/UserDocslmages/Plan%20gospodarenja%20smedim%20medvjedima%20eng.pdf.Google Scholar
  19. Huber, D., Kusak, J., Majić-Skrbinšek, A., Majnarić, D., Sindičić, M., 2008b. A multidimensional approach to managing the European brown bear in Croatia. Ursus 19, 22–32.CrossRefGoogle Scholar
  20. Huber, D., Roth, H.U., 1993. Movements of European brown bears in Croatia. Acta Theriol. 38, 151–159.CrossRefGoogle Scholar
  21. Jarne, P., Lagoda, P.J.L., 1996. Microsatellites, from molecules to populations and back. Trends Ecol. Evol. 11, 424–429.CrossRefGoogle Scholar
  22. Karamanlidis, A.A., Drosopoulou, E., de Gabriel Hernando, M., Georgiadis, L., Krambokoukis, L., Pllaha, S., Zedrosser, A., Scouras, Z., 2010. Noninvasive genetic studies of brown bears using power poles. Eur. J. Wildl. Res., doi: https://doi.org/10.1007/s10344-010-0363-3.CrossRefGoogle Scholar
  23. Kohn, M., Knauer, F., Stoffella, A., Schroder, W., Paabo, S., 1995. Conservation genetics of the European brown bear — a study using excremental PCR of nuclear and mitochondrial sequences. Mol. Ecol. 4, 95–103.PubMedCrossRefPubMedCentralGoogle Scholar
  24. Kojola, I., Heikkinen, S., 2006. The structure of the expanded brown bear population at the edge of the Finnish range. Ann. Zool. Fenn. 43, 258–262.Google Scholar
  25. Kruckenhauser, L., Rauer, G., Däubl, B., Haring, E., 2009. Genetic monitoring of a founder population of brown bears (Ursus arctos) in central Austria. Conserv. Genet. 10, 1223–1233.CrossRefGoogle Scholar
  26. Kusak, J., Huber, D., Gomerčić, T., Schwaderer, G., Gužvica, G., 2009. The permeability of highway in Gorski kotar (Croatia) for large mammals. Eur. J. Wildl. Res. 55, 7–21.CrossRefGoogle Scholar
  27. Linnell, J., Salvatori, V., Boitani, L., 2007. Guidelines for population level management plans for large carnivores in Europe. A Large Carnivore lnitiative for Europe, Report Prepared for the European Commission. http://www.lcie.org/.
  28. Lorenzini, R., Posillico, M., Lovari, S., Petrella, A., 2004. Non-invasive genotyping of the endangered Apennine brown bear: a case study not to let one’s hair down. Anim. Conserv. 7, 199–209.CrossRefGoogle Scholar
  29. Mills, L.S., Allendorf, F.W., 1996. The one-migrant-per-generation rule in conservation and management. Conserv. Biol. 10, 1509–1518.CrossRefGoogle Scholar
  30. Paetkau, D., Calvert, W., Stirling, I., Strobeck, C., 1995. Microsatellite analysis of population structure in Canadian polar bears. Mol. Ecol. 4, 347–354.PubMedPubMedCentralCrossRefGoogle Scholar
  31. Paetkau, D., Shields, G.F., Strobeck, C., 1998a. Gene flow between insular, coastal and interior populations of brown bear in Alaska. Mol. Ecol. 7, 1283–1292.PubMedCrossRefPubMedCentralGoogle Scholar
  32. Paetkau, D., Strobeck, C., 1994. Microsatellite analysis of genetic variation in black bear populations. Mol. Ecol. 3, 459–489.CrossRefGoogle Scholar
  33. Paetkau, D., Waits, L.P., Clarkson, P.L., Craighead, L., Vyse, E., Ward, R., Strobeck, C., 1998b. Variation in genetic diversity across the range of north American brown bears. Conserv. Biol. 12, 418–429.CrossRefGoogle Scholar
  34. Pérez, T., Vázquez, F., Naves, J., Fernández, A., Corao, A., Albornoz, J., Domínguez, A., 2009. Non-invasive genetic study of the endangered Cantabrian brown bear (Ursus arctos). Conserv. Genet. 10, 291–301.CrossRefGoogle Scholar
  35. Piry, S., Luikart, G., Cornuet, J.M., 1999. BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J. Hered. 90, 502–503.CrossRefGoogle Scholar
  36. Pritchard, J.K., Stephens, M., Donnelly, P., 2000. Inference of population structure using multilocus genotype data. Genetics 155, 945–959.PubMedPubMedCentralGoogle Scholar
  37. Quenette, P.Y., Alonso, M., Chayron, L., Cluzel, P., Dubarry, E., Dubreuil, D., Palazon, S., Pomarol, M., 2001. Preliminary results of the first transplantation of brown bears in the French Pyrenees. Ursus 12, 115–120.Google Scholar
  38. Randi, E., Gentile, L., Boscagli, G., Huber, D., Roth, H.U., 1994. Mitochondrial DNA sequence divergence among some west European brown bear (Ursus arctos L.) populations. Lessons for conservation. Heredity 73, 480–489.PubMedCrossRefGoogle Scholar
  39. Rauer, G., 1997. First experiences with the release of 2 female brown bears in the Alps of Eastern Austria. Int. Conf. Bear Res. Manage. 9 (2), 91–95.Google Scholar
  40. Raymond, M., Rousset, F., 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86, 248–249.CrossRefGoogle Scholar
  41. Rice, W.R., 1989. Analyzing tables of statistical tests. Evolution 43, 223–225.PubMedPubMedCentralCrossRefGoogle Scholar
  42. Rousset, F., 2008. Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol. Ecol. Resour. 8, 103–106.PubMedCrossRefPubMedCentralGoogle Scholar
  43. Saarma, U., Kojola, I., 2007. Matrilineal genetic structure of the brown bear population in Finland. Ursus 18, 30–37.CrossRefGoogle Scholar
  44. Skrbinšek, T., Jelenčič, M., Waits, L., Kos, I., Trontelj, P., 2010. Highly efficient multiplex PCR of noninvasive DNA does not require pre-amplification. Mol. Ecol. Resour. 10, 495–501.PubMedCrossRefPubMedCentralGoogle Scholar
  45. Støen, O.-G., Bellemain, E., Sæbø, S., Swenson, J.E., 2005. Kin-related spatial structure in brown bears Ursus arctos. Behav. Ecol. Sociobiol. 59, 191–197.CrossRefGoogle Scholar
  46. Taberlet, P., Bouvet, J., 1994. Mitochondrial DNA polymorphism, phylogeography, and conservation genetics of the brown bear Ursus arctos in Europe. Proc. R. Soc. B 255, 195–200.PubMedCrossRefPubMedCentralGoogle Scholar
  47. Taberlet, P., Camarra, J.J., Griffin, S., Uhres, E., Hanotte, O., Waits, L.P., Dubois-Paganon, C., Burke, T., Bouvet, J., 1997. Noninvasive genetic tracking of the endangered Pyrenean brown bear population. Mol. Ecol. 6, 869–876.PubMedCrossRefPubMedCentralGoogle Scholar
  48. Taberlet, P., Mattock, H., Dubois-Pagnon, C., Bouvet, J., 1993. Sexing free-ranging brown bears Ursus arctos using hairs found in the field. Mol. Ecol. 2, 399–403.PubMedCrossRefPubMedCentralGoogle Scholar
  49. Thompson, J.D., Higgins, D.G., Gibson, T.J., 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680.PubMedPubMedCentralCrossRefGoogle Scholar
  50. Valière, N., 2002. GIMLET: a computer program for analysing genetic individual identification data. Mol. Ecol. Notes 2, 377–379.Google Scholar
  51. Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M., Shipley, P., 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4, 535–538.CrossRefGoogle Scholar
  52. Vernesi, C., Crestanello, B., Pecchioli, E., Tartari, D., Caramelli, D., Hauffe, H., Bertorelle, G., 2003. The genetic impact of demographic decline and reintroduction in the wild boar (Sus scrofa): a microsatellite analysis. Mol. Ecol. 12, 585–595.CrossRefGoogle Scholar
  53. Waits, L.P., Luikart, G., Taberlet, P., 2001. Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol. Ecol. 10, 249–256.PubMedCrossRefPubMedCentralGoogle Scholar
  54. Waits, L.P., Taberlet, P., Swenson, J.E., Sandgren, F., Franzen, R., 2000. Nuclear DNA microsatellite analysis of genetic diversity and gene flow in the Scandinavian brown bear (Ursus arctos). Mol. Ecol. 9, 421–431.CrossRefGoogle Scholar
  55. Waits, L.P., Talbot, S.L., Ward, R.H., Shields, G.F., 1998. Mitochondrial DNA phylogeography of the North American Brown Bear and Implications for Conservation. Conserv. Biol. 12, 408–417.CrossRefGoogle Scholar
  56. Williamson-Natesan, E.G., 2005. Comparison of methods for detecting bottlenecks from microsatellite loci. Conserv. Genet. 6, 551–562.CrossRefGoogle Scholar
  57. Wilson, A.C., Cann, R.L., Carr, S.M., George, M., Gyllensten, U.B., Helm-Bychowski, K.M., Higuchi, R.G., Palumbi, S.R., Prager, E.M., Sage, R.D., Stoneking, M., 1985. Mitochondrial DNA and two perspectives on evolutionary genetics. Biol. J. Linn. Soc. 26, 375–400.CrossRefGoogle Scholar
  58. Zachos, F.E., Otto, M., Unici, R., Lorenzini, R., Hartl, G.B., 2008. Evidence of a phylogeographic break in the Romanian brown bear (Ursus arctos) population from the Carpathians. Mamm. Biol. 73, 93–101.CrossRefGoogle Scholar
  59. Zedrosser, A., Dahle, B., Swenson, J.E., Gerstl, N., 2001. Status and management of the brown bear in Europe. Ursus 12, 9–20.Google Scholar
  60. Zedrosser, A., Støen, O.-G., Sæbø, S., Swenson, J.E., 2007. Should I stay or should I go? Natal dispersal in the brown bear. Anim. Behav. 74, 369–376.CrossRefGoogle Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2010

Authors and Affiliations

  • Ivna Kocijan
    • 1
    Email author
  • Ana Galov
    • 1
  • Helena Ćetković
    • 2
  • Josip Kusak
    • 3
  • Tomislav Gomerčić
    • 3
  • Đuro Huber
    • 3
  1. 1.Division of Biology, Faculty of ScienceUniversity of ZagrebZagrebCroatia
  2. 2.Laboratory of Molecular Genetics, Division of Molecular BiologyRuđer Bošković InstituteZagrebCroatia
  3. 3.Department of Biology, Faculty of Veterinary MedicineUniversity of ZagrebZagrebCroatia

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