Impact of conservation and hunting on big game species: comparison of the genetic diversity of the red deer population groups from a national park and neighboring hunting areas in northern Poland

References

• Apollonio M, Belkin VV, Borkowski J, Borodin OI, Borowik T, Cagnacci F, Yanuta G. 2017. Challenges and science-based implications for modern management and conservation of European ungulate populations. Mammal Research 62(3):209–217. DOI:10.1007/s13364-017-0321-5.
   Web of Science ®Google Scholar
• Bana NA, Nyiri A, Nagy J, Frank K, Nagy T, Steger V, Orosz L. 2018. The red deer Cervus elaphus genome CerEla1.0: Sequencing, annotating, genes, and chromosomes. Molecular Genetics and Genomics 293(3):665–684. DOI:10.1007/s00438-017-1412-3.
   Web of Science ®Google Scholar
• Barendse W, Armitage SM, Kossarek LM, Shalom A, Kirkpatrick BW, Ryan AM, Hetzel DJS. 1994. A genetic linkage map of the bovine genome. Nature Genetics 6(3):227–235. DOI:10.1038/ng0394-227.
   Web of Science ®Google Scholar
• Barton NH, Slatkin M. 1986. A quasi-equilibrium theory of the distribution of rare alleles in a subdivided population. Heredity 56(3):409–415. DOI:10.1038/hdy.1986.63.
   PubMedGoogle Scholar
• Bishop MD, Kappes SM, Keele. JW, Stone RT, Sunden SLF, Hawkins GA, Toldo SS, Fries R, Grosz MD, Yoo J, Beattie CW. 1994. A genetic linkage map for cattle. Genetics 136:619–639.
   PubMed Web of Science ®Google Scholar
• Borkowski J. 2004. Distribution and habitat use by red and roe deer following a large forest fire in south-western Poland. Forest Ecology and Management 201(2–3):287–293. DOI:10.1016/j.foreco.2004.07.011.
   Web of Science ®Google Scholar
• Borkowski J, Banul R, Jurkiewicz J, Hołdyński C, Świeczkowska J, Nasiadko M, Załuski D. 2019. High density of keystone herbivore vs. conservation of natural resources: Factors affecting red deer distribution and impact on vegetation in Słowiński National Park, Poland. Forest Ecology and Management 450:117503. DOI:10.1016/j.foreco.2019.117503.
   Web of Science ®Google Scholar
• Buchanan FC, Crawford AM. 1993. Ovine microsatellites at the OARFCB11, OARFCB128, OARFCB193, OARFCB266 and OARFCB304 loci. Animal Genetics 24(2):145. DOI:10.1111/j.1365-2052.1993.tb00269.x.
   Google Scholar
• Carranza J. 1999. Red deer females collect on male clumps at mating areas. Behavioral Ecology 10(5):525–532. DOI:10.1093/beheco/10.5.525.
   Web of Science ®Google Scholar
• Chape S, Harrison J, Spalding M, Lysenko I. 2005. Measuring the extent and effectiveness of protected areas as an indicator for meeting global biodiversity targets. Philosophical Transactions of the Royal Society B: Biological Sciences 360(1454):443–455. DOI:10.1098/rstb.2004.1592.
   PubMed Web of Science ®Google Scholar
• Clutton-Brock TH, Wilson K, Stevenson IR. 1997. Density-dependent selection on horn phenotype in Soay sheep. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 352(1355):839–850. DOI:10.1098/rstb.1997.0064.
   Web of Science ®Google Scholar
• Côté SD, Rooney TP, Tremblay J-P, Dussault C, Waller DM. 2004. Ecological impacts of deer overabundance. Annual Review of Ecology, Evolution, and Systematics 35(1):113–147. DOI:10.1146/annurev.ecolsys.35.021103.105725.
   Google Scholar
• Coulon A, Cosson JF, Angibault JM, Cargnelutti B, Galan M, Morellet N, Hewison AJM. 2004. Landscape connectivity influences gene flow in a roe deer population inhabiting a fragmented landscape: An individual-based approach. Molecular Ecology 13(9):2841–2850. DOI:10.1111/j.1365-294X.2004.02253.x.
   PubMed Web of Science ®Google Scholar
• Depczyk K, Łogin M, Pielowski Z, Przybylski A, Weksej K, Wędziński A. 1997. Jeleń na Pomorzu, 1st edition, p. 1–64, SGGW, Warsaw, ISBN:83-906854-0-X. [In Polish].
   Google Scholar
• Dzięgielewski S. 1970. Jeleń. In: Monografia przyrodniczo-łowiecka. Warszawa: Państwowe Wydawnictwo Rolnicze i Leśne (PWRiL), Warszawa. [In Polish].
   Google Scholar
• Emst M, Putnova L, Pokoradi J, Matouskova J, Zidek R, Marsalkova L, Lamka J. 2012. Microsatellite analysis DNA for controlled breeding of Cervidae and genetic breeding of white coloured Cervus elaphus in the Czech Republic. Iranian Journal of Applied Animal Science 2(3):233–237.
   Google Scholar
• Excoffier L, Lischer HEL. 2010. Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10(3):564–567. DOI:10.1111/j.1755-0998.2010.02847.x.
   PubMed Web of Science ®Google Scholar
• Excoffier L, Smouse PE, Quattro JM. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 131(2):479–491.
   PubMed Web of Science ®Google Scholar
• Fernandez‐Garcia JL, Carranza J, Martinez JG, Randi E. 2014. Mitochondrial D-loop phylogeny signals two native Iberian red deer (Cervus elaphus) Lineages genetically different to Western and Eastern European red deer and infers human-mediated translocations. Biodiversity and Conservation 23(3):537–554. DOI:10.1007/s10531-013-0585-2.
   Web of Science ®Google Scholar
• Festa-Bianchet M. 2016. When does selective hunting select, how can we tell, and what should we do about it? Mammal Review 47(1):76–81. DOI:10.1111/mam.12078.
   Web of Science ®Google Scholar
• Fløjgaard C, De Barba M, Taberlet P, Ejrnæs R. 2017. Body condition, diet and ecosystem function of red deer (Cervus elaphus) in a fenced nature reserve. Global Ecology and Conservation 11:312–323. DOI:10.1016/j.gecco.2017.07.003.
   Web of Science ®Google Scholar
• Frantz AC, Pourtois JT, Heuertz M, Schley L, Flamand MC, Krier A, Burke T. 2006. Genetic structure and assignment tests demonstrate illegal translocation of red deer (Cervus elaphus) into a continuous population. Molecular Ecology 15(11):3191–3203. DOI:10.1111/j.1365-294X.2006.03022.x.
   Web of Science ®Google Scholar
• Frantz AC, Zachos FE, Bertouille S, Eloy M-C, Colyn M, Flamand MC. 2017. Using genetic tools to estimate the prevalence of non-native red deer (Cervus elaphus) in a Western European population. Ecology and Evolution 7(19):7650–7660. DOI:10.1002/ece3.3282.
   Web of Science ®Google Scholar
• Galarza JA, Sanchez-Fernandez B, Fandos P, Soriguer R. 2015. The genetic landscape of the Iberian red deer (Cervus elaphus hispanicus) after 30 years of big-game hunting in southern Spain. The Journal of Wildlife Management 79(3):500–504. DOI:10.1002/jwmg.854.
   Web of Science ®Google Scholar
• Galarza JA, Sanchez-Fernandez B, Fandos P, Soriguer R. 2017. Intensive management and natural genetic variation in red deer (Cervus elaphus). Journal of Heredity 108(5):496–504. DOI:10.1093/jhered/esx052.
   Web of Science ®Google Scholar
• Georges M, Massey JM. 1992. Polymorphic DNA markers in Bovidae. Patent WO, 092/13102. Geneva: World Intellectual Property Organization.
   Google Scholar
• Goudet J, 2001. FSTAT, a program to estimate and test gene diversities and fixation indices. Available http://www2.unil.ch/popgen/softwares/fstat.htm
   Google Scholar
• Grignolio S, Merli E, Bongi P, Ciuti S, Apollonio M. 2011. Effects of hunting with hounds on a non-target species living on the edge of a protected area. Biological Conservation 144(1):641–649. DOI:10.1016/j.biocon.2010.10.022.
   Web of Science ®Google Scholar
• Haanes H, Roed KH, Perez-Espona S, Rosef O. 2011. Low genetic variation support bottlenecks in Scandinavian red deer. European Journal of Wildlife Research 57(6):1137–1150. DOI:10.1007/s10344-011-0527-9.
   Web of Science ®Google Scholar
• Hartl G, Willing R, Lang G, Klein F, Köller J. 1990. Genetic variability and differentiation in red deer (Cervus elaphus L.) of Central Europe. Genetics Selection Evolution 22(3):289. DOI:10.1186/1297-9686-22-3-289.
   Web of Science ®Google Scholar
• Hartl GB, Zachos F, and Nadlinger K. 2003. Genetic diversity in European red deer (Cervus elaphus L.): anthropogenic influences on natural populations. C.R. Biol. 326: 37–42. DOI: 10.1016/s1631-0691(03)00025-8
   Google Scholar
• Hartl GB, Zachos FE, Nadlinger K, Ratkiewicz M, Klein F, Lang G. 2005. Allozyme and mitochondrial DNA analysis of French red deer (Cervus elaphus) populations: Genetic structure and its implications for management and conservation. Mammalian Biology - Zeitschrift Für Säugetierkunde 70(1):24–34. DOI:10.1078/1616-5047-00173.
   Web of Science ®Google Scholar
• Hoffmann GS, Johannesen J, Griebeler EM. 2016. Population dynamics of a natural red deer population over 200 years detected via substantial changes of genetic variation. Ecology and Evolution 6(10):3146–3153. DOI:10.1002/ece3.2063.
   Web of Science ®Google Scholar
• Imperio S, Ferrante M, Grignetti A, Santini G, Focardi S. 2010. Investigating population dynamics in ungulates: Do hunting statistics make up a good index of population abundance? Wildlife Biology 16(2):205–214. DOI:10.2981/08-051.
   Web of Science ®Google Scholar
• Krojerová-Prokesová J, Baranceková M, Koubek P. 2015. Admixture of eastern and western European red deer lineages as a result of postglacial recolonization of the Czech Republic (Central Europe). Journal of Heredity 106(4):375–385. DOI:10.1093/jhered/esv018.
   Web of Science ®Google Scholar
• Kropil R, Smolko P, Garaj P. 2015. Home range and migration patterns of male red deer Cervus elaphus in Western Carpathians. Europ. Journal of Wildlife Research 61(1):63–72. DOI:10.1007/s10344-014-0874-4.
   Web of Science ®Google Scholar
• Krzysiak MK, Larska M. 2014. Pharmacological immobilization of European bison. Medycyna Weterynaryjna 70(3):172–175. [In Polish].
   Web of Science ®Google Scholar
• Kuehn R. 2004. Genetic roots of the red deer (Cervus elaphus) population in eastern Switzerland. Journal of Heredity 95(2):136–143. DOI:10.1093/jhered/esh019.
   Web of Science ®Google Scholar
• Kuehn R, Schroeder W, Pirchner F, Rottmann O. 2003. Genetic diversity, gene flow and drift in Bavarian red deer populations (Cervus elaphus). Conservation Genetics 4(2):157–166. DOI:10.1023/A:1023394707884.
   Web of Science ®Google Scholar
• Linnell JDC, Zachos FE. 2011. Status and distribution patterns of European ungulates: Genetics, population history and conservation. In: Putman R, Apollonio M, Andersen R, editors. Ungulate management in Europe: Problems and practices. Cambridge (UK): Cambridge University Press. pp. 12–53.
   Google Scholar
• Maruyama T, Fuerst PA. 1985. Population bottlenecks and non-equilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics 111(3):675–689.
   Web of Science ®Google Scholar
• Mysterud A. 2011. Selective harvesting of large mammals: How often does it result in directional selection? Journal of Applied Ecology 48(4):827–834. DOI:10.1111/j.1365-2664.2011.02006.x.
   Web of Science ®Google Scholar
• Nei. 1987. Molecular evolutionary genetics. New York: Columbia University Press. DOI:10.7312/nei-92038.
   Google Scholar
• Nei M, Maruyama T, Chakraborty R. 1975. The bottleneck effect and genetic variability in populations. Evolution 29(1):1–10. DOI:10.1111/j.1558-5646.1975.tb00807.x.
   PubMed Web of Science ®Google Scholar
• Nei M, Roychoudhury AK. 1974. Sampling variances of heterozygosity and genetic distance. Genetics 76(2):379–390.
   PubMed Web of Science ®Google Scholar
• Niedziałkowska M, Fontaine MC, Jędrzejewska B. 2012a. Factors shaping gene flow in red deer (Cervus elaphus) in seminatural landscapes of central Europe. Canadian Journal of Zoology 90(2):150–162. DOI:10.1139/z11-122.
   Google Scholar
• Niedziałkowska M, Jędrzejewska B, Wójcik JM, Goodman SJ. 2012b. Genetic structure of red deer population in northeastern Poland in relation to the history of human interventions. The Journal of Wildlife Management 76(6):1264–1276.
   Web of Science ®Google Scholar
• Nielsen EK, Olesen CR, Pertoldi C, Gravlund P, Barker JSF, Mucci N, Loeschcke V. 2008. Genetic structure of the Danish red deer (Cervus elaphus). Biological Journal of the Linnean Society 95(4):688–701. DOI:10.1111/j.1095-8312.2008.01115.x.
   Web of Science ®Google Scholar
• Nussey DH, Pemberton J, Donald A, Kruuk LE. 2006. Genetic consequences of human management in an introduced island population of red deer (Cervus elaphus). Heredity 97(Edinb):56–65. DOI:10.1038/sj.hdy.6800838.
   Google Scholar
• Peakall R, Smouse PE. 2012. GenAlEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research–an update. Bioinformatics 28(19):2537–2539. DOI:10.1093/bioinformatics/bts460.
   PubMed Web of Science ®Google Scholar
• Pérez-González J, Frantz AC, Torres-Porras J, Castillo L, Carranza J. 2012. Population structure, habitat features and genetic structure of managed red deer populations. European Journal of Wildlife Research 58(6):933–943. DOI:10.1007/s10344-012-0636-0.
   Web of Science ®Google Scholar
• Pérez-González J, Mateos C, Carranza J. 2009. Polygyny can increase rather than decrease genetic diversity contributed by males relative to females: Evidence from red deer. Molecular Ecology 18(8):1591–1600. DOI:10.1111/j.1365-294X.2009.04150.x.
   Web of Science ®Google Scholar
• Piry S, Luikart G, Cornuet JM. 1999. Bottleneck: A computer program for detecting recent reductions in the effective population size using allele frequency data. Journal of Heredity 90(4):502–503. DOI:10.1093/jhered/90.4.502.
   Web of Science ®Google Scholar
• Pritchard JK, Stephens M, Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics 155:945–959.
   PubMed Web of Science ®Google Scholar
• Queiros J, Vicente J, Boadella M, Gortázar C, Alves PC. 2013. The impact of management practices and past demographic history on the genetic diversity of red deer (Cervus elaphus): An assessment of population and individual fitness. Biological Journal of the Linnean Society 111(1):209–223. DOI:10.1111/bij.12183.
   Web of Science ®Google Scholar
• Roed KH, Midthjell L. 1998. Microsatellites in reindeer (Rangifer tarandus) and their use in other Cervids. Molecular Ecology 7(12):1773–1776. DOI:10.1046/j.1365-294x.1998.00514.x.
   Web of Science ®Google Scholar
• Rousset F. 2008. Genepop’007: A complete reimplementation of the Genepop software for Windows and Linux. Molecular Ecology Resources 8(1):103–106. DOI:10.1111/j.1471-8286.2007.01931.x
   Web of Science ®Google Scholar
• Schnitzler A, Granado JA, Putelat O, Arbogast R-M, Drucker D, Eberhard A, Schmutz A, Klaefiger Y, Lang G, Salzburger W, Schibler J, Schlumbaum A, Bocherens H. 2018. Genetic diversity, genetic structure and diet of ancient and contemporary red deer (Cervus elaphus L.) from north-eastern France. PLoS One 13(1):e0189278. DOI:10.1371/journal.pone.0189278.
   Web of Science ®Google Scholar
• Schwartz M, Luikart G, Waples R. 2007. Genetic monitoring as a promising tool for conservation and management. Trends in Ecology & Evolution 22(1):25–33. DOI:10.1016/j.tree.2006.08.009.
   PubMed Web of Science ®Google Scholar
• Skog A, Zachos FE, Rueness EK, Feulner PGD, Mysterud A, Langvatn R, Jakobsen KS. 2009. Phylogeography of red deer (Cervus elaphus) in Europe. Journal of Biogeography 36(1):66–77. DOI:10.1111/j.1365-2699.2008.01986.x.
   Web of Science ®Google Scholar
• Van Oosterhout CV, Hutchinson WF, Wills DPM, Shipley P. 2004. MICRO-CHECKER: Software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology 4(3):535–538. DOI:10.1111/j.1471-8286.2004.00684.x.
   Web of Science ®Google Scholar
• Vetter SG, Arnold W. 2018. Effects of population structure and density on calf sex ratio in red deer (Cervus elaphus) - implications for management. European Journal of Wildlife Research 64(3). DOI:10.1007/s10344-018-1190-1.
   Web of Science ®Google Scholar
• Weir BS, Cockerham CC. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38(N Y):1358–1370.
   Google Scholar
• Wilson GA, Strobeck C, Wu L, Coffin JW. 1997. Characterization of microsatellite loci in caribou (Rangifer tarandus) and their use in other artiodactyls. Molecular Ecology 6(7):697–699. DOI:10.1046/j.1365-294X.1997.00237.x.
   Web of Science ®Google Scholar
• Zachos FE, Althoff C, Steynitz Y, Eckert I, Hartl G.B. 2006. Genetic analysis of an isolated red deer (Cervus elaphus) population showing signs of inbreeding depression. European Journal of Wildlife Research, 53(1), 61–67. DOI:10.1007/s10344-006-0065-z
   Google Scholar
• Zachos FE, Althoff C, V Steynitz Y, Eckert I, Hartl GB. 2007. Genetic analysis of an isolated red deer (Cervus elaphus) population showing signs of inbreeding depression. European Journal of Wildlife Research 53(1):61–67. DOI:10.1007/s10344-006-0065-z.
   Web of Science ®Google Scholar
• Zachos FE, Frantz AC, Kuehn R, Bertouille S, Colyn M, Niedziałkowska M, Flamand M-C. 2016. Genetic structure and effective population sizes in European red deer (Cervus elaphus) at a continental scale: Insights from microsatellite DNA. Journal of Heredity 107(4):318–326. DOI:10.1093/jhered/esw011.
   Web of Science ®Google Scholar