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Hair snaring and molecular genetic identification for reconstructing the spatial structure of Eurasian lynx populations

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Abstract

Non-invasive genetic sampling (NGS) is being increasingly applied in wildlife monitoring and population genetic research. This study was designed to evaluate the use of NGS for reconstructing the spatial structure of populations of large felids. We developed a procedure for reliably genotyping individuals of Eurasian lynx (Lynx lynx) from samples obtained through a hair-trapping scheme based on a network of lynx scent-marking sites. The spatial locations of the identified genotypes were matched with the home ranges distribution of radio-tracked individuals, thus cross-checking the accuracy of the two methods. We analyzed DNA extracted from 170 hair samples and 11 blood samples from live-trapped lynx collected in 2004–2009 in the Białowieża Primeval Forest, Poland. We obtained PCR products in 96 (67%) hair samples; 82 (85%) of them were reliably genotyped at 12 autosomal microsatellite loci following a multiple-tubes protocol and stringent quality-controls of the data set. The sample included 29 distinct genotypes; 18 were found only in hair samples, five were determined only in live-trapped animals, and six in both hair and blood samples. Based on linkage disequilibrium we estimated an effective population size Ne = 20.3 (90% CI = 15–28). The total population size estimated with Capwire was Nc =32 (95% CI = 25–37) in close agreement with the observed number of genotypes. The genotypes obtained from hair samples were re-sampled on average 3.9 times and 50% of them were recorded for more than one year. The spatial distribution of six hair-genotypes was consistent with their home ranges obtained by radio-tracking in the same period. The distribution ranges of hair-trapped genotypes overlapped on average in 86.4% (mode 100%) with home ranges of the corresponding individuals. Hair-trapping and molecular identification is a reliable method for reconstructing the spatial organization of lynx population. It is likely to be also efficiently used in other rare and endangered species of felids in combination with data from other monitoring techniques, such as radio- and snow-tracking and photo-trapping.

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References

  • 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 (in French).

  • Boulanger, J., Himmer, S., Swan, C., 2004. Monitoring of grizzly bear population trends and demography using DNA mark-recapture methods in the Owikeno Lake area of British Columbia. Can. J. Zool. 82, 1267–1277.

    Article  CAS  Google Scholar 

  • Boulanger, J., Proctor, M., Himmer, S., Stenhouse, G., Paetkau, D., Cranston, J., 2006. An empirical test of DNA mark-recapture sampling strategies for grizzly bear. Ursus 17, 149–158.

    Article  Google Scholar 

  • Breitenmoser, U., 1989. A footsnare for medium-sized Carnivores. Cat News 11, 20.

    Google Scholar 

  • Breitenmoser, U., Breitenmoser-Würsten, C., Okarma, H., Kaphegyi, T., Kaphegyi-Wallmann, U., Müller, U.M., 2000. Action Plan for the Conservation of the Eurasian Lynx in Europe (Lynx lynx). Nature and Environment 112. Council of Europe, Strasbourg Cedex, France.

    Google Scholar 

  • Breitenmoser-Würsten, C., Vandel, J.M., Zimmermann, F., Breitenmoser, U., 2007. Demography of lynx Lynx lynx in the Jura Mountains. Wildl. Biol. 13, 381–392.

    Article  Google Scholar 

  • Broquet, T., Petit, E., 2004. Quantifying genotyping errors in noninvasive population genetics. Mol. Ecol. 13, 3601–3608.

    Article  CAS  PubMed  Google Scholar 

  • Castro-Arellano, I., Madrid-Luna, C., Lacher Jr., T.E., Leon-Paniagua, L., 2008. Hair-trap efficacy for detecting mammalian carnivoresin the tropics. J. Wildl. Manage. 72, 1405–1412.

    Article  Google Scholar 

  • Crow, J.F., Kimura, M., 1970. An Introduction to Population Genetics Theory. Harper & Row, New York, NY, USA.

    Google Scholar 

  • Davison, A., Birks, J.D.S., Brookes, R.C., Braithwaite, T.C., Messanger, J.E., 2002. On the origin of faeces: morphological versus molecular methods for surveying rare carnivores from their scats. J. Zool. (Lond.) 257, 141–143.

    Article  Google Scholar 

  • De Barba, M., Waits, L.P., Garton, E.O., Genovesi, P., Randi, E., Mustoni, A., Groff, C., 2010. The power of genetic monitoring for studying demography, ecology and genetics of a reintroduced brown bear population. Mol. Ecol. 19, 3938–3951.

    Article  PubMed  Google Scholar 

  • Delibes, M., Rodríguez, A., Ferreras, P., 2000. Action Plan for the conservation of the Iberian lynx (Lynx pardinus) in Europe. Council of Europe, Strasbourg, France.

    Google Scholar 

  • Downey, P.J., Hellgren, E.C., Caso, A., Carvajal, S., Frangioso, K., 2007. Hair snares for noninvasive sampling of felids in North America: do gray foxes affect success. J. Wildl. Manage. 71, 2090–2094.

    Article  Google Scholar 

  • Eizirik, E., Kim, J.H., Menotti-Raymond, M., Crawshaw, P.G., O’Brien, S.J., Johnson, W.E., 2001. Phylogeography, population history and conservation genetics of jaguars (Panthera onca, Mammalia, Felidae). Mol. Ecol. 10, 65–79.

    Article  CAS  PubMed  Google Scholar 

  • Fabbri, E., Miquel, C., Lucchini, V., Santini, A., Caniglia, R., Duchamp, C., Weber, J.M., Lequette, B., Marucco, F., Boitani, L., Fumagalli, L., Taberlet, P., Randi, E., 2007. From the Appennines to the Alps: colonization genetics of the naturally expanding Italian wolfs (Canis lupus) population. Mol. Ecol. 16, 1661–1671.

    Article  CAS  PubMed  Google Scholar 

  • Faliński, J.B., 1986. Vegetation Dynamics in Temperate Lowland Primeval Forest. Dr. W. Junk Publishers, Dordrecht, Germany.

    Book  Google Scholar 

  • Gerloff, U., Schlötterer, C., Rassmann, K., Rambold, I., Hohmann, G., Fruth, B., Tautz, D., 1995. Amplification of hypervariable simple sequence repeats (microsatellites) from excremental DNA of wild living bonobos (Pan paniscus). Mol. Ecol. 4, 515–518.

    Article  CAS  Google Scholar 

  • Gervasi, V., Ciucci, P., Davoli, F., Boulanger, J., Boitani, L., Randi, E., 2010. Addressing challenges in non invasive capture–recapture based estimates of small populations: a pilot study on the Apennine brown bear. Conserv.Genet. 11, 2299–2310.

    Article  Google Scholar 

  • Haag, T., Santos, A.S., De Angelo, C., Srbek-Araujo, A.C., Sana, D.A., Morato, R.G., Salzano, F.M., Eizirik, E., 2009. Development and testingofanoptimized method for DNA-based identification of jaguar (Panthera onca) and puma (Puma concolor) faecal samples for use in ecological and genetic studies. Genetics 136, 505–512.

    CAS  Google Scholar 

  • Janečka, J.E., Blankenship, T.L., Hirth, D.H., Tewes, M.E., Kilpatrick, C.W., Grassman Jr., L.I., 2006. Kinship and social structure of bobcats (Lynx rufus) inferred from microsatellite and radio-telemetry data. J. Zool. 269, 494–501.

    Article  Google Scholar 

  • Jędrzejewski, W., Jędrzejewska, B., Okarma, H., Schmidt, K., Bunevich, A.N., Miłkowski, L., 1996. Population dynamics (1869–1994), demography and home ranges of the lynx in Białowieża Primeval Forest (Poland and Belaruss). Ecography 19, 122–138.

    Article  Google Scholar 

  • Kalinowski, S.T., Wagner, A.P., Taper, M.L., 2006a. ML-Relate: a computer program for maximum likelihood estimation of relatedness and relationship. Mol. Ecol. Notes 6, 576–579.

    Article  CAS  Google Scholar 

  • Kalinowski, S.T., Sawaya, M., Taper, M.L., 2006b. Individual identification and distributions of genotypic differences. J. Wildl. Manage. 70, 148–150.

    Article  Google Scholar 

  • Kolbe, J.A., Squires, J.R., Parker, T.W., 2003. An effective box trap for capturing lynx. Wildl. Soc. Bull. 31, 980–985.

    Google Scholar 

  • McDaniel, G.W., McKelvey, K.S., Squires, J.R., Ruggiero, L.F., 2000. Efficacy of lures and hair snares to detect lynx. Wildl. Soc. Bull. 28, 119–123.

    Google Scholar 

  • McKelvey, K.S., Von Kienast, J., Aubry, K.B., Koehler, G.M., Maletzke, B.T., Squires, J.R., Lindquist, E.L., Loch, S., Schwartz, M.K., 2006. DNA analysis of hair and scat collected along snow tracks to document the presence of Canada lynx. Wildl. Soc. Bull. 34, 451–455.

    Article  Google Scholar 

  • Mellen, J.D., 1993. A comparative analysis of scent-marking, social and reproductive behavior in 20 species of small cats (Felis). Am. Zool. 33, 151–166.

    Article  Google Scholar 

  • Menotti-Raymond, M., David, V.A., Lyons, L.A., Schafer, A.A., Tomlin, J.F., Hutton, M.K., O’Brien, S.J., 1999. A genetic linkage map of microsatellites in the domestic cat (Felis catus). Genomics 57, 9–23.

    Article  CAS  PubMed  Google Scholar 

  • Miller, C.R., Joyce, P., Waits, L.P., 2002. Assessing allelic dropout and genotyping reliability using maximum likelihood. Genetics 160, 357–366.

    PubMed  PubMed Central  Google Scholar 

  • Miller, C.R., Joyce, P., Waits, L.P., 2005. A new method for estimating the size of small populations from genetic mark—recapture data. Mol. Ecol. 14, 1991–2005.

    Article  CAS  PubMed  Google Scholar 

  • Mills, L.S., Citta, J.J., Lair, K.P., Schwartz, M.K., Tallmon, D.A., 2000. Estimating animal abundance using noninvasive DNA sampling: promise and pitfalls. Ecol. Appl. 10, 283–294.

    Article  Google Scholar 

  • Mowat, G., Paetkau, D., 2002. Estimating marten Martes americana population size using hair capture and genetic tagging. Wildl. Biol. 8 (3), 201–209.

    Article  Google Scholar 

  • Nichols, J.D., Williams, B.K., 2006. Monitoring for conservation. Trends Ecol. Evol. 21, 668–673.

    Article  PubMed  Google Scholar 

  • Nikolov, I.S., Gum, B., Markov, G., Kuehn, R., 2009. Population genetic structure of wild boar Sus scrofa in Bulgaria as revealed by microsatellite analysis. Acta Theriol. 54 (3), 193–205.

    Article  Google Scholar 

  • Paetkau, D., 2003. Anempirical exploration of data qualityin DNA-based population inventories. Mol. Ecol. 12, 1375–1387.

    Article  CAS  PubMed  Google Scholar 

  • Palomares, F., Godoy, J.A., Piriz, A., O’Brien, S.J., Johnson, W.E., 2002. Faecal genetic analysis to determine the presence and distribution of elusive carnivores: design and feasibility for the Iberian lynx. Mol. Ecol. 11, 2171–2182.

    Article  CAS  PubMed  Google Scholar 

  • Peakall, R., Smouse, P.E., 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6, 288–295.

    Article  Google Scholar 

  • Pilgrim, K.L., McKelvey, K.S., Riddle, A.E., Schwartz, M.K., 2005. Felid sex identification based on noninvasive genetic samples. Mol. Ecol. Notes 5, 60–61.

    Article  CAS  Google Scholar 

  • Pilot, M., Jędrzejewski, W., Branicki, W., Sidorovich, V.E., Jedrzejewska, B., Stachura, K., Funk, S.M., 2006. Ecological factors influence population genetic structure of European grey wolves. Mol. Ecol. 15, 4533–4553.

    Article  CAS  PubMed  Google Scholar 

  • Pompanon, F., Bonin, A., Bellemain, E., Taberlet, P., 2005. Genotyping errors: causes, consequences and solutions. Nat. Rev. Genet. 6, 847–859.

    Article  CAS  PubMed  Google Scholar 

  • Roon, D.A., Thomas, M.E., Kendall, K.C., Waits, L.P., 2005. Evaluating mixed samples as a source of error in non-invasive genetic studies using microsatellites. Mol. Ecol. 14, 195–201.

    Article  CAS  PubMed  Google Scholar 

  • Rowcliffe, J.M., Carbone, C., 2008. Surveys using camera traps: are we looking to a brighter future? Anim. Conserv. 11, 185–186.

    Google Scholar 

  • Ruell, E.W., Crooks, K.R., 2007. Evaluation of non-invasive genetic sampling methods for felid and canid populations. J. Wildl. Manage. 71, 1690–1694.

    Article  Google Scholar 

  • Rueness, E.K., Jorde, P.E., Hellborg, L., Stenseth, N.C., Ellegren, H., Jakobsen, K.S., 2003. Cryptic population structure in a large, mobile mammalian predator: the Scandinavian lynx. Mol. Ecol. 12, 2623–2633.

    Article  CAS  PubMed  Google Scholar 

  • Sawaya, M.A., Ruth, T.K., Creel, S., Rotella, J.J., Stetz, J.B., Quigley, H.B., Kalinowski, S.T., 2011. Evaluating noninvasive genetic sampling methods for cougars in Yellowstone National Park. J. Wildl. Manage. 75, 612–622.

    Article  Google Scholar 

  • Schmidt, K., 2008. Behavioural and spatial adaptation of the Eurasian lynx to a decline in prey availability. Acta Theriol. 53, 1–16.

    Article  Google Scholar 

  • Schmidt, K., Je˛drzejewski, W., Okarma, H., 1997. Spatial organization and social relations in the Eurasian lynx population in Białowieża Primeval Forest. Poland. Acta Theriol. 42, 289–312.

    Article  Google Scholar 

  • Schmidt, K., Kowalczyk, R., 2006. Using scent-marking stations to collect hair samples to monitor Eurasian lynx populations. Wildl. Soc. Bull. 34, 462–466.

    Article  Google Scholar 

  • Schmidt, K., Kowalczyk, R., Ozolins, J., Männil, P., Fickel, J., 2009. Genetic structure of the Eurasian lynx population in north-eastern Poland and the Baltic states. Conserv. Genet. 10, 497–501.

    Article  Google Scholar 

  • Schwartz, M.K., Mills, L.S., Ortega, Y., Ruggiero, L.F., Allendorf, F.W., 2003. Landscape location affects genetic variation of Canada lynx (Lynx canadensis). Mol. Ecol. 12, 1807–1816.

    Article  CAS  PubMed  Google Scholar 

  • Schwartz, M.K., Luikart, G., Waples, R.S., 2007. Genetic monitoring as a promising tool for conservation and management. Trends Ecol. Evol. 22, 25–33.

    Article  PubMed  Google Scholar 

  • Sutherland, W.J., 1996. Ecological Census Techniques: AHandbook. Cambridge University Press, Cambridge, United Kingdom.

    Google Scholar 

  • Taberlet, P., Griffin, S., Goossens, B., Questiau, S., Manceau, V., Escaravage, N., Waits, L.P., Bouvet, J., 1996. Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res. 26, 3189–3194.

    Article  Google Scholar 

  • Taberlet, P., Waits, L.P., Luikart, G., 1999. Non-invasive genetic sampling: look before you leap. Trends Ecol. Evol. 14, 323–327.

    Article  CAS  PubMed  Google Scholar 

  • Valière, N., 2002. GIMLET: a computer program for analysing genetic individual identification data. Mol. Ecol. Notes 2, 377–379.

    Google Scholar 

  • Waits, L.P., Paetkau, D., 2005. Non-invasive genetic sampling tools for wildlife biologists: a review of applications and recommendations for accurate data collection. J. Wildl. Manage. 69 (4), 1419–1433.

    Article  Google Scholar 

  • Waples, R.S., 2006. A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conserv. Genet. 7, 167–184.

    Article  Google Scholar 

  • Wasser, S.K., Houston, C.S., Koehler, G.M., Cadd, G.G., Fain, S.R., 1997. Techinques for the application of faecal DNA methods to field studies of Ursids. Mol. Ecol. 6, 1091–1097.

    Article  CAS  PubMed  Google Scholar 

  • Weaver, J.L., Wood, P., Paetkau, D., Laack, L.L., 2005. Use of scented hair snares to detect ocelots. Wildl. Soc. Bull. 33 (4), 1384–1391.

    Article  Google Scholar 

  • Weir, B.S., Cockerham, C.C., 1984. Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.

    CAS  PubMed  Google Scholar 

  • Woods, J.G., Paetkau, D., Lewis, D., McLellan, B.N., Proctor, M., Strobeck, C., 1999. Genetic tagging of free-ranging black and brown bears. Wildl. Soc. Bull. 27 (3), 616–627.

    Google Scholar 

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Davoli, F., Schmidt, K., Kowalczyk, R. et al. Hair snaring and molecular genetic identification for reconstructing the spatial structure of Eurasian lynx populations. Mamm Biol 78, 118–126 (2013). https://doi.org/10.1016/j.mambio.2012.06.003

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  • DOI: https://doi.org/10.1016/j.mambio.2012.06.003

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