Advertisement

Mammal Research

, Volume 64, Issue 1, pp 133–145 | Cite as

How to spot a black-footed cat? Successful application of cross-species markers to identify captive-bred individuals from non-invasive genetic sampling

  • Federica Mattucci
  • Marco Galaverni
  • Cino Pertoldi
  • Elena Fabbri
  • Alexander Sliwa
  • Romolo CanigliaEmail author
Methods Paper

Abstract

The black-footed cat (Felis nigripes) is the smallest felid of Southern Africa, endemic to the arid steppe and savannah habitats. However, though threatened and characterized by decreasing sizes of its populations, a number of ecological, demographic, sanitary, and genetic aspects, essential for the long-term conservation of the species, still remain poorly known. Non-invasive genetic sampling may represent an appropriate and cost-effective tool to fill this lack of information. Thus, for the first time so far, we developed a protocol for species and individual identification of black-footed cats, starting from markers originally designed for the domestic cat and from 23 non-invasively collected samples of captive-bred individuals. We then tested its genotyping efficiency and reliability for future applications in non-invasive genetic monitoring programs of the wild populations. Most of the samples (65%), corresponding to 15 individuals, were successfully genotyped at 316 bp of the mtDNA ND5 and at nine autosomal microsatellites. We detected two black-footed cat mtDNA ND5 haplotypes that were clearly distinguishable from all the other wild and domestic felids. All microsatellites were polymorphic and showed low error rates, probabilities of identity < 0.001 and a mean observed heterozygosity HO = 0.68. Subsequent approximate Bayesian computation simulations confirmed that black-footed cats and African and European wildcats likely experienced sequential population splittings that started during the Late Pliocene and continued through the Early Pleistocene. Our study provided the first reliable and cost-effective molecular multilocus characterization of non-invasively collected samples of black-footed cats. Though solely tested on captive-bred individuals, our method could be applied to design and implement effective long-term monitoring and conservation plans of poorly investigated black-footed cat wild populations.

Keywords

Black-footed cats Conservation genetics Felids Phylogenetics Genetic variability Microsatellites mtDNA Non-invasive genetic sampling 

Notes

Acknowledgments

We are grateful to Sofie Nielsen, the Hoedspruit Endangered Species Centre and the Cat Conservation Trust, for the sample collection and to Stefano Anile, Ettore Randi (University of Bologna), and Nadia Mucci (ISPRA) for their useful suggestions on the manuscript.

Funding information

The study was supported by the Danish Natural Science Research Council grant number: 21-01-0526, 21-03-0125, and 95095995 by the Aalborg Zoo Conservation Foundation (AZCF) for CP and by the Italian Institute for Environmental Protection and Research (ISPRA, Istituto Superiore per la Protezione e la Ricerca Ambientale).

Supplementary material

13364_2018_407_MOESM1_ESM.xlsx (20 kb)
ESM 1 (XLSX 19.7 kb)
13364_2018_407_MOESM2_ESM.pdf (52 kb)
ESM 2 Identification of the optimal number of genetic clusters. Rates of increase in the posterior probability LnP(K) between consecutive K used to estimate the most likely number of genetic groups K in the data. (PDF 52.1 kb)
13364_2018_407_MOESM3_ESM.pdf (188 kb)
ESM 3 Model checking. Pre-evaluation of scenario-prior combinations; direct and logistic regression comparison methods of the estimated posterior probabilities among the tree scenarios (Scenario 1 in light blue, Scenario 2 in red and Scenario 3 in green); and fit of the selected best scenario (Scenario 1 in light blue) with the observed data. PCA I and II were plotted using 10.000 data points. (PDF 188 kb)

References

  1. Adrados B, Zanin M, Silveira L et al (2018) Non-invasive genetic identification of two sympatric sister-species: ocelot (Leopardus pardalis) and margay (L. wiedii) in different biomes. Conserv Genet Resour.  https://doi.org/10.1007/s12686-018-0992-5
  2. Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709CrossRefGoogle Scholar
  3. Allendorf FW, Luikart G, Aitken SN (2013) Conservation and the genetics of populations Chichester (UK). John Wiley & Sons, Ltd, HobokenGoogle Scholar
  4. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefGoogle Scholar
  5. Anile S, Arrabito C, Mazzamuto MV, Scornavacca D, Ragni B (2012) A non-invasive monitoring on European wildcat (Felis silvestris silvestris Schreber, 1777) in Sicily using hair trapping and camera trapping: does it work? Hystrix It J Mamm 23:45–50Google Scholar
  6. Arandjelovic M, Vigilant L (2018) Non-invasive genetic censusing and monitoring of primate populations. Am J Primatol 80:1–14CrossRefGoogle Scholar
  7. Beaumont MA, Wand WZ, Balding DJ (2002) Approximate Bayesian computation in population genetics. Genetics 162:2025–2035Google Scholar
  8. Beja-Pereira A, Oliveira R, Alves PC et al (2009) Advancing ecological understandings through technological transformations in noninvasive genetics. Mol Ecol Resour 9:1279–1301CrossRefGoogle Scholar
  9. 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
  10. Bhagavatula J, Singh L (2006) Genotyping faecal samples of Bengal tiger Panthera tigris tigris for population estimation: a pilot study. BMC Genet 7:48CrossRefGoogle Scholar
  11. Bonin A, Nicole F, Pompanon F, Miaud C, Taberlet P (2007) Population adaptive index: a new method to help measure intraspecific genetic diversity and prioritize populations for conservation. Conserv Biol 21:697–708CrossRefGoogle Scholar
  12. Borthakur U, Barman RD, Das C, Basumatary A, Talukdar A, Ahmed MF, Talukdar BK Bharali R (2011) Noninvasive genetic monitoring of tiger (Panthera tigris tigris) population of Orang National Park in the Brahmaputra floodplain, Assam, India. Eur J Wildl Res 57:603–613CrossRefGoogle Scholar
  13. Burchell WJ (1824) Travels in the interior of southern Africa Vol 2. Longman, Hurst, Rees, Orme, Brown and Green, LondonGoogle Scholar
  14. Caniglia R, Fabbri E, Galaverni M, Milanesi P, Randi E (2014) Noninvasive sampling and genetic variability, pack structure, and dynamics in an expanding wolf population. J Mammal 95:41–59CrossRefGoogle Scholar
  15. Cornuet JM, Pudlo P, Veyssier J, Dehne-Garcia A, Gautier M, Leblois R, Marin JM, Estoup A (2014) DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics 30:1187–1189CrossRefGoogle Scholar
  16. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772CrossRefGoogle Scholar
  17. De Barba M, Waits LP, Genovesi P, Randi E, Chirichella R, Cetto E (2010) Comparing opportunistic and systematic sampling methods for non-invasive genetic monitoring of a small translocated brown bear population. J Appl Ecol 47:172–181CrossRefGoogle Scholar
  18. Driscoll C, Yamaguchi N, O’Brien SJ, Macdonald DW (2011) A suite of genetic markers useful in assessing wildcat (Felis silvestris ssp.) – domestic cat (Felis silvestris catus) admixture. J Hered 102(Suppl1):S87–S90CrossRefGoogle Scholar
  19. Fabbri E, Velli E, D'Amico F, Galaverni M, Mastrogiuseppe L, Mattucci F, Caniglia R (2018) From predation to management: monitoring wolf distribution and understanding depredation patterns from attacks on livestock. Hystrix.  https://doi.org/10.4404/hystrix-00070-2018
  20. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587Google Scholar
  21. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  22. García-Alaníz N, Naranjo EJ, Mallory FF (2010) Hair snares: a non-invasive method for monitoring felid populations in the Selva Lacandona, Mexico. Trop Conserv Sci 3:403–411CrossRefGoogle Scholar
  23. Granroth-Wilding H, Primmer C, Lindqvist M, Poutanen J, Thalmann O, Aspi J, Harmoinen J, Kojola I, Laaksonen T (2017) Non-invasive genetic monitoring involving citizen science enables reconstruction of current pack dynamics in a re-establishing wolf population. BMC Ecol 17:44CrossRefGoogle Scholar
  24. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  25. Hassanin A (2014) The complete mitochondrial genome of the servaline genet, Genetta servalina, the first representative from the family Viverridae (Mammalia, Carnivora). Mitochondrial DNA Part A 27:906–907CrossRefGoogle Scholar
  26. Hedrick PW, Miller PS (1992) Conservation genetics: techniques and fundamentals. Ecol Appl 2:30–46CrossRefGoogle Scholar
  27. Hubisz M, Falush D, Stephens M, Pritchard J (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Res 9:1322–1332CrossRefGoogle Scholar
  28. Jakobsson M, Rosenberg NA (2007) Clumpp: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806CrossRefGoogle Scholar
  29. Jerosch S, Götza M, Klarb N, Rotha M (2010) Characteristics of diurnal resting sites of the endangered European wildcat (Felis silvestris silvestris): implications for its conservation. J Nat Conserv 18:45–54CrossRefGoogle Scholar
  30. Johnson WE, O’Brien SJ (1997) Phylogenetic reconstruction of the Felidae using 16S rRNA and NADH-5 mitochondrial genes. J Mol Evol 44:98–116CrossRefGoogle Scholar
  31. Johnson WE, Eizirik E, Pecon-Slattery J, Murphy WJ, Antunes A, Teeling E, O’Brien SJ (2006) The late Miocene radiation of modern Felidae: a genetic assessment. Science 311:73–76CrossRefGoogle Scholar
  32. Jombart T, Devillard S, Dufour AB, Pontier D (2008) Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity 101:92–103CrossRefGoogle Scholar
  33. Kraus RHS, vonHoldt B, Cocchiararo B, Harms V, Bayerl H, Kühn R, Förster DW, Fickel J, Roos C, Nowak C (2015) A single-nucleotide polymorphism-based approach for rapid and cost-effective genetic wolf monitoring in Europe based on noninvasively collected samples. Mol Ecol Resour 15:295–305CrossRefGoogle Scholar
  34. Kubasiewicz LM, Quine CP, Summers RW, Coope R, Cottrell JE, A’Hara SW, Park KJ (2017) Non-invasive genotyping and spatial mark-recapture methods to estimate European pine marten density in forested landscapes. Hystrix It J Mamm 28:265–271Google Scholar
  35. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  36. Leyhausen P (1979) Cat behaviour: predatory and social behaviour of domestic and wild cats. Garland STPM Press, New YorkGoogle Scholar
  37. Li G, Davis BW, Eizirik E, Murphy WJ (2016) Phylogenomic evidence for ancient hybridization in the genomes of living cats (Felidae). Genome Res 26:1–11CrossRefGoogle Scholar
  38. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefGoogle Scholar
  39. Lovari S, Boesi R, Minder I, Mucci N, Randi E, Dematteis A, Ale SB (2009) Restoring a keystone predator may endanger a prey species in a human-altered ecosystem: the return of the snow leopard to Sagarmatha National Park. Anim Conserv 12:559–570CrossRefGoogle Scholar
  40. Lukacs PM, Eggert LS, Burnham KP (2007) Estimating population size from multiple detections with non-invasive genetic data. Wildl Biol Pract 3:83–92CrossRefGoogle Scholar
  41. Macdonald DW, Loveridge AJ (2010) Biology and conservation of wild felids. Oxford University Press, New YorkGoogle Scholar
  42. Mattucci F, Oliveira R, Bizzarri L, Vercillo F, Anile S, Ragni B, Lapini L, Sforzi A, Alves PC, Lyons LA, Randi E (2013) Genetic structure of wildcat (Felis silvestris) populations in Italy. Ecol Evol 3:2443–2458CrossRefGoogle Scholar
  43. Mattucci F, Oliveira R, Lyons LA, Alves PC, Randi E (2015) European wildcat populations are subdivided into five main biogeographic groups: consequences of Pleistocene climate changes or recent anthropogenic fragmentation? Ecol Evol 6:3–22CrossRefGoogle Scholar
  44. Meester JA, Rautenbach IL, Dippenaar NJ, Baker CM (1986) Classification of southern African mammals. Transvaal Museum Monographs 5:1–359Google Scholar
  45. Menotti-Raymond M, O’Brien SJ (1995) Evolutionary conservation of ten microsatellite loci in four species of Felidae. J Hered 86:319–322CrossRefGoogle Scholar
  46. Menotti-Raymond M, David VA, Stephens JC, Lyons LA, O’Brien SJ (1997) Genetic individualization of domestic cats using feline STR loci for forensic applications. J Forensic Sci 42:1039–1051CrossRefGoogle Scholar
  47. Menotti-Raymond M, David VA, Lyons LA, Schäffer AA, Tomlin JF, Hutton MK, O’Brien SJ (1999) Agenetic linkage map of microsatellites in the domestic cat (Felis catus). Genomics 57:9–23CrossRefGoogle Scholar
  48. Milanesi P, Holderegger R, Caniglia R, Fabbri E, Randi E (2016) Different habitat suitability models yield different least-costpath distances for landscape genetic analysis. Basic Appl Ecol 17:61–71CrossRefGoogle Scholar
  49. Miller CR, Joyce P, Waits LP (2002) Assessing allelic dropout and genotype reliability using maximum likelihood. Genetics 160:357–366Google Scholar
  50. Mills LS, Citta JJ, Lair KP, Schwartz MK, Tallmon DA (2000) Estimating animal abundance using non-invasive DNA sampling: promise and pitfalls. Ecol Appl 10:283–294CrossRefGoogle Scholar
  51. Montague MJ, Li G, Gandolfi B, Khan R, Aken BL, Searle SMJ, Minx P, Hillier LDW, Koboldt DC, Davis BW, Driscoll CA, Barr CS, Blackistone K, Quilez J, Lorente-Galdos B, Marques-Bonet T, Alkan C, Thomas GWC, Hahn MW, Menotti-Raymond M, O’Brien SJ, Wilson RK, Lyons LA, Murphy WJ, Warren WC (2014) Comparative analysis of the domestic cat genome reveals genetic signatures underlying feline biology and domestication. Proc Natl Acad Sci U S A PNAS 111:17230–17235CrossRefGoogle Scholar
  52. Norman AJ, Spong G (2015) Single nucleotide polymorphism-based dispersal estimates using noninvasive sampling. Ecol Evol 5:3056–3065CrossRefGoogle Scholar
  53. Nowak RM, Walker EP (1999) Mammals of the world. The Johns Hopkins University Press, Baltimore and LondonGoogle Scholar
  54. Nowell K, Jackson P (1996) Wild cats: status survey and conservation action plan. IUCN/SSC Cat Specialist Group, Gland, Switzerland and Cambrigde, UKGoogle Scholar
  55. O’Brien SJ, Johnson WE (2007) The evolution of cats. Sci Am 297:68–75CrossRefGoogle Scholar
  56. Oh A, Pearce JW, Gandolfi B et al (2017) Early-onset progressive retinal atrophy associated with an IQCB1 variant in African black-footed cats (Felis nigripes). Sci Rep 7:43918.  https://doi.org/10.1038/srep43918 CrossRefGoogle Scholar
  57. Olbricht G, Sliwa A (1997) In situ and ex situ observations and management of black-footed cats. Int Zoo Yb 35:81–89CrossRefGoogle Scholar
  58. Oliveira R, Godinho R, Randi E, Ferrand N, Alves PC (2008) Molecular analysis of hybridisation between wild and domestic cats (Felis silvestris) in Portugal: implications for conservation. Conserv Genet 9:1–11CrossRefGoogle Scholar
  59. Oliveira R, Castro D, Godinho R, Luikart G, Alves PC (2010) Species identification using a small nuclear gene fragment: application to sympatric wild carnivores from South-Western Europe. Conserv Genet 11:1023–1032CrossRefGoogle Scholar
  60. Peakall R, Smouse P (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539CrossRefGoogle Scholar
  61. Pierpaoli M, Biró ZS, Herrmann M et al (2003) Genetic distinction of wildcat (Felis silvestris) populations in Europe, and hybridization with domestic cats in Hungary. Mol Ecol 12:2585–2598CrossRefGoogle Scholar
  62. Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes, consequences and solutions. Nat Rev Genet 6:847–859CrossRefGoogle Scholar
  63. Pontius JU, Mullikin JC, Smith DR, Agencourt Sequencing Team, Lindblad-Toh K, Gnerre S, Clamp M, Chang J, Stephens R, Neelam B, Volfovsky N, Schaffer AA, Agarwala R, Narfstrom K, Murphy WJ, Giger U, Roca AL, Antunes A, Menotti-Raymond M, Yuhki N, Pecon-Slattery J, Johnson WE, Bourque G, Tesler G, NISC Comparative Sequencing Program, O'Brien SJ (2007) Initial sequence and comparative analysis of the cat genome. Genome Res 17:1675–1689CrossRefGoogle Scholar
  64. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959Google Scholar
  65. Randi E, Pierpaoli M, Beaumont M, Ragni B, Sforzi A (2001) Genetic identification of wild and domestic cats (Felis silvestris), and their hybrids using Bayesian clustering methods. Mol Biol Evol 18:1679–1693CrossRefGoogle Scholar
  66. Reddy PA, Cushman SA, Srivastava A, Sarkar MS, Shivaji S (2017) Tiger abundance and gene flow in Central India are driven by disparate combinations of topography and land cover. Divers Distrib 23:863–874CrossRefGoogle Scholar
  67. Renard A, Lavoie M, Pitt JA, Larivière S (2015) Felis nigripes (Carnivora: Felidae). Mamm Species 47(925)78–83CrossRefGoogle Scholar
  68. Rice WR (1989) Analysing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  69. Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  70. Rozhnov VV, Sorokin PA, Lukarevskiy VS, Naidenko SV, Hernandes-Blanko JA, Lukarevskiy SV (2013) Individual identification of Amur leopards (Panthera pardus orientalis) using molecular-genetic methods and the population size estimation. Biol Bull 40:124–129CrossRefGoogle Scholar
  71. Ruell EW, Crooks KR (2007) Evaluation of noninvasive genetic sampling methods for felid and canid populations. J Wildl Managem 71:1690–1694CrossRefGoogle Scholar
  72. Ruiz-González A, Jose Madeira M, Randi E, Urra F, Gómez-Moliner BJ (2013) Non-invasive genetic sampling of sympatric marten species (Martes martes and Martes foina): assessing species and individual identification success rates on faecal DNA genotyping. Eur J Wildl Res 59:371–386CrossRefGoogle Scholar
  73. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425Google Scholar
  74. Shortridge GC (1931) Felis (Microfelis) nigripes thomasi subsp. nov. Records of the Albany Museum 4:1Google Scholar
  75. Sliwa A (2004) Home range size and social organisation of black-footed cats (Felis nigripes). Mamm Biol 69:96–107CrossRefGoogle Scholar
  76. Sliwa A (2008) Felis nigripes. In: IUCN 2010. IUCN Red List of Threatened Species. Version 2015.2 www.iucnredlist.org. Accessed 29 June 2015
  77. Sliwa A, Herbst M, Mills M (2010) Black-footed cats (Felis nigripes) and African wild cats (Felis silvestris): a comparison of two small felids from South African arid lands. Pages 537–558Google Scholar
  78. Sliwa A, Wilson B, Küsters M, Tordiffe A (2016) Felis nigripes. The IUCN red list of threatened species 2016: e.T8542A50652196.  https://doi.org/10.2305/IUCN.UK.2016-1.RLTS.T8542A50652196.en
  79. Stansbury CR, Ausband DE, Zager P, Mack CM, Miller CR, Pennell MW, Waits LP (2014) A long-term population monitoring approach for a wide-ranging carnivore: noninvasive genetic sampling of gray wolf rendezvous sites in Idaho, USA. Wildl Manag 78:1040–1049CrossRefGoogle Scholar
  80. Steyer K, Simon O, Kraus RHS, Haase P, Nowak C (2013) Hair trapping with valerian-treated lure sticks as a tool for genetic wildcat monitoring in low-density habitats. Eur J Wildl Res 59:39–46CrossRefGoogle Scholar
  81. Steyer K, Tiesmeyer A, Muñoz Fuentes V, Nowak C (2018) Low rates of hybridization between European wildcats and domestic cats in a human dominated landscape. Ecol Evol 8:2290–2304Google Scholar
  82. Sugimoto T, Nagata J, Aramilev VV, Mccullough DR (2012) Population size estimation of Amur tigers in Russian Far East using noninvasive genetic samples. J Mammal 93:93–101CrossRefGoogle Scholar
  83. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882CrossRefGoogle Scholar
  84. Valière N (2002) Gimlet: a computer program for analysing genetic individual identification data. Mol Ecol Notes 2:377–379Google Scholar
  85. Velli E, Bologna MA, Silvia C, Ragni B, Randi E (2015) Non-invasive monitoring of the European wildcat (Felis silvestris silvestris Schreber, 1777): comparative analysis of three different monitoring techniques and evaluation of their integration. Eur J Wildl Res 61:657–668CrossRefGoogle Scholar
  86. Verkuil YI, van Guldener WEA, Lagendijk DG et al (2018) Molecular identification of temperate Cricetidae and Muridae rodent species using fecal samples collected in a natural habitat. Mamm Res 63:379–385.  https://doi.org/10.1007/s13364-018-0359-z CrossRefGoogle Scholar
  87. Viglino A, Martinoli A, Elena P et al (2016) What can we learn from faeces ? Assessing genotyping success and genetic variability in three mouse-eared bat species from non-invasive genetic sampling. Hystrix It J Mamm 27.  https://doi.org/10.4404/hystrix-27.2-11835
  88. von Thaden A, Cocchiararo B, Jarausch A, Jüngling H, Karamanlidis AA, Tiesmeyer A, Nowak C, Muñoz-Fuentes V (2017) Assessing SNP genotyping of noninvasively collected wildlife samples using microfluidic arrays. Sci Rep 7:10768.  https://doi.org/10.1038/s41598-017-10647-w CrossRefGoogle Scholar
  89. Waits LP, Paetkau D (2005) Non-invasive genetic sampling tools for wildlife biologists: a review of applications and recommendations for accurate data collection. J Wildl Manag 69:1419–1433CrossRefGoogle Scholar
  90. Waits L, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256CrossRefGoogle Scholar
  91. Wells DL, Egli JM (2004) The influence of olfactory enrichment on the behaviour of captive black-footed cats, Felis nigripes. Appl Anim Behav Sci 85:107–119CrossRefGoogle Scholar
  92. Wultsch C, Waits LP, Kelly MJ (2014) Noninvasive individual and species identification of jaguars (Panthera onca), pumas (Puma concolor) and ocelots (Leopardus pardalis) in Belize, Central America using cross-species microsatellites and faecal DNA. Mol Ecol Resour 14:1171–1182CrossRefGoogle Scholar

Copyright information

© Mammal Research Institute, Polish Academy of Sciences, Białowieża, Poland 2018

Authors and Affiliations

  • Federica Mattucci
    • 1
  • Marco Galaverni
    • 2
  • Cino Pertoldi
    • 3
    • 4
  • Elena Fabbri
    • 1
  • Alexander Sliwa
    • 5
  • Romolo Caniglia
    • 1
    Email author
  1. 1.Area per la Genetica della ConservazioneISPRAOzzano dell’EmiliaItaly
  2. 2.Area ConservazioneWWF ItaliaRomeItaly
  3. 3.Department of Chemistry and BioscienceAalborg UniversityAalborg ØstDenmark
  4. 4.Aalborg ZooAalborg ØstDenmark
  5. 5.Kölner ZooKölnGermany

Personalised recommendations