Evaluation of non-invasive genetic sampling methods for estimating tiger population size

Biological Conservation

Volumn 142, Issue 10, 2009, Pages 2350-2360

  Mondol, Samrat ^a   Ullas Karanth, K ^b,c   Samba Kumar, N ^b,c   Gopalaswamy, Arjun M ^b,c   Andheria, Anish ^a   Ramakrishnan, Uma ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^b WILDLIFE CONSERVATION SOCIETY   (India)

^c Centre for Wildlife Studies   (India)

Author keywords

Carnivore conservation; Elusive carnivores; Fecal DNA; Genetic capture recapture sampling; Individual identification; Panthera tigris; Population estimation; Scats

Indexed keywords

ABUNDANCE; CAPTIVE POPULATION; CARNIVORE; DNA; FECES; FELID; FIELD SURVEY; GENETIC ANALYSIS; GENETIC MARKER; MARK-RECAPTURE METHOD; PHOTOGRAPHY; POPULATION ESTIMATION; POPULATION SIZE; SAMPLING; SPECIES CONSERVATION; TAGGING;

ANIMALIA; PANTHERA; PANTHERA TIGRIS;

EID: 68549133161     PISSN: 00063207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocon.2009.05.014     Document Type: Article

References (78)

1. Amstrup S.C., McDonald T.L., and Manly B.F.J. Handbook of Capture-Recapture Analysis (2005), Princeton University Press, Princeton, NJ
2. Andheria, A.P., 2006. Assessment of diet and abundance of large carnivores from field surveys of scats. M.Sc. Thesis, Manipal University.
3. Banks S.C., Piggott M.P., Hansen B.D., Robinson N.A., and Taylor A.C. Wombat coprogenetics: enumerating a common wombat population by microsatellite analysis of faecal DNA. Australian Journal of Zoology 50 (2002) 193-204
4. Bhagavatula J., and Singh L. Genotyping faecal samples of Bengal tiger (Panthera tigris tigris) for population estimation: a pilot study. BMC Genetics 7 (2006) 48
5. Boersen M.R., Clark J.D., and King T.L. Estimating black bear population density and genetic diversity at Tensas River, Louisiana using microsatellite DNA markers. Wildlife Society Bulletin 31 (2003) 197-207
6. Borchers D.L., and Efford M.G. Spatially explicit maximum likelihood methods for capture-recapture studies. Biometrics 64 (2008) 377-385
7. Broquet T., Menard N., and Petit E. Noninvasive population genetics: a review of sample source, diet, fragment length and microsatellite motif effects on amplification success and genotyping error rates. Conservation Genetics 8 (2007) 249-260
8. Burnham K.P., and Overton W.S. Estimation of the size of a closed population when capture probabilities vary among animals. Biometrika 65 (1978) 625-633
9. Creel S., Spong G., Sands J.L., Rotella J., Zeigle J., Joe J., Murphy K.M., and Smith D. Population size estimation in Yellowstone wolves with error-prone noninvasive microsatellite genotypes. Molecular Ecology 12 (2003) 2003-2009
10. Davison A., Birks J.D.S., Brookes R.C., Braithwaithe T.C., and Messenger J.E. On the origin of faeces: morphological versus molecular methods for surveying rare carnivores from their scats. Journal of Zoology 257 (2002) 141-143
11. Dreher B.P., Winterstein S.R., Scribner K.T., Lukacs P.M., Etter D.R., Rosa G.J.M., Lopez V.A., Libants S., and Filcek K.B. Noninvasive estimation of black bear abundance incorporating genotyping errors and harvested bear. Journal of Wildlife Management 71 (2007) 2684-2693
12. Eggert L.S., Eggert J.A., and Woodruff D.S. Estimating population sizes for elusive animals: the forest elephants of Kakum National Park, Ghana. Molecular Ecology 12 (2003) 1389-1402
13. Fickel J., and Hohmann U. A methodological approach for non-invasive sampling for population size estimates in wild boars (Sus scrofa). European Journal of Wildlife Research 52 (2006) 28-33
14. Flagstad Ø., Hedmark E., Landa A., Broseth H., Persson J., Andersen R., Segeratrom P., and Ellegren H. Colonization history and non-invasive monitoring of a re-established wolverine population. Conservation Biology 18 (2004) 676-688
15. Frantz A.C., Pope L.C., Carpenter P.J., Roper T.J., Wilson G.J., Delahay R.J., and Burke T. Reliable microsatellite genotyping of the Eurasian badger (Meles meles) using faecal DNA. Molecular Ecology 12 (2003) 1649-1661
16. Frantz A.C., Schaul M., Pope L.C., Fack F., Schley L., Muller C.P., and Roper T.J. Estimating population size by genotyping remotely plucked hair: the Eurasian badger. Journal of Applied Ecology 41 (2004) 985-995
17. Henschel, P., Ray, J., 2003. Leopards in African Rainforests: Survey and Monitoring Techniques, Global Carnivore Program, Wildlife Conservation Society. ().
18. Karanth K.U., and Nichols J.D. Estimating tiger densities in India from camera trap data using photographic captures and recaptures. Ecology 79 (1998) 2852-2862
19. Karanth K.U., and Sunquist M.E. Behavioral correlates of predation by tiger, leopard and dhole in Nagarahole, India. Journal of Zoology 250 (2000) 255-265
20. Karanth, K.U., Nichols, J.D., 2002. Monitoring Tigers and their Prey: A Manual for Researchers, Managers and Conservationists in Tropical Asia. Centre for Wildlife Studies, Bangalore.
21. Karanth, K.U., Nichols, J.D., Kumar, N.S., 2004a. Photographic sampling of elusive mammals in tropical forests. In: Thompson, W.L. (Ed.), Sampling Rare or Elusive Species. Island Press, Washington, DC, pp. 229-247.
22. Karanth K.U., Nichols J.D., Kumar N.S., Link W.A., and Hines J.E. Tigers and their prey: predicting carnivore densities from prey abundance. Proceedings of National Academy of Sciences of USA 101 (2004) 4854-4858
23. Karanth K.U. Estimating tiger Panthera tigris populations from camera-trap data using capture recapture models. Biological Conservation 71 (1995) 333-338
24. Karanth K.U., Nichols J.D., Kumar N.S., and Hines J.E. Assessing tiger population dynamics using photographic capture-recapture sampling. Ecology 87 (2006) 2925-2937
25. Karanth, K. U., Kumar, N. S., Gopalaswamy, A., Srinivas, V., 2008. Distribution and Dynamics of Tiger and Prey Populations in Karnataka. Centre for Wildlife Studies (Unpublished report).
26. Kawanishi K., and Sunquist M.E. Conservation status of tigers in a primary rainforest of Peninsular Malaysia. Biological Conservation 120 (2004) 329-344
27. Kerley L.L., and Salkina G.P. Using scent-matching dogs to identify individual Amur tigers from scats. Journal of Wildlife Management 71 (2006) 1349-1356
28. Kishore R., Hardy W.R., Anderson V.J., Sanchez B.S., and Buoncristiani M.R. Optimization of DNA extraction from low-yield and degraded samples using the Biorobot EZ1 and Biorobot M48. Journal of Forensic Science 51 (2006) 1055-1061
29. Kohn M.H., York E.C., Kamradt D.A., Haught G., Sauvajot R.M., and Wayne R.K. Estimating population size by genotyping faeces. Proceedings of Royal Society B 266 (1999) 657-663
30. Lukacs P.M., and Burnham K.P. Review of capture-recapture methods applicable to noninvasive genetic sampling. Molecular Ecology 14 (2005) 3909-3919
31. Luo S.-J., Kim J.-H., Johnson W.E., et al. Phylogeography and genetic ancestry of tigers (Panthera tigris). PLoS Biology 2 (2004) 2275-2293
32. Marshall T.C., Slate J., Kruuk L.E.B., and Pemberton J.M. Statistical confidence for likelihood-based paternity inference in natural populations. Molecular Ecology 7 (1998) 639-655
33. McKelvey K.S., and Schwartz M.K. Providing reliable and accurate capture mark-recapture estimates in a cost-effective way. Journal of Wildlife Management 68 (2004) 453-456
34. Menotti-Raymond M., David V.A., Lyons L.A., Schaffer A.A., Tomlin J.L., Hutton M.K., and O'Brien S.J. A genetic linkage map of microsatellites of the domestic cat (Felis catus). Genomics 57 (1999) 9-23
35. Miller C.R., Joyce P., and Waits L.P. A new method for estimating the size of small populations from genetic mark-recapture data. Molecular Ecology 14 (2005) 1991-2005
36. Mills L.S., Citta J.J., Lair K., Schwartz M., and Tallmon D. Estimating animal abundance using non-invasive DNA sampling: promise and pitfalls. Ecological Applications 10 (2000) 283-294
37. Miquel C., Bellemain E., Poillot C., Bessiere J., Durand A., and Taberlet P. Quality indexes to assess the reliability of genotypes in studies using noninvasive sampling and multiple-tube approach. Molecular Ecology Notes 6 (2006) 985-988
38. Morell V. Can the wild tiger survive?. Science 317 (2007) 1312-1314
39. Mowat G., and Paetkau D. Estimating marten Martes americana population size using hair capture and genetic tagging. Wildlife Biology 8 (2002) 201-209
40. Mukherjee N., Mondol S., Andheria A., and Ramakrishnan U. Rapid multiplex PCR based species identification of wild tigers using non-invasive samples. Conservation genetics 8 (2007) 1465-1470
41. Murphy M.A., Waits L.P., Kendall K.C., Wasser S.K., Higbee J.A., and Bogden R. An evaluation of long-term preservation methods for brown bear (Ursus arctos) faecal DNA samples. Conservation Genetics 3 (2002) 435-440
42. Nagata J., Aramilev V.V., Belozor A.B., Sugimoto T., and McCullough D.R. Fecal genetic analysis using PCR-RFLP of cytochrome b to identify sympatric carnivores, the tiger Panthera tigris and the leopard Panthera pardus, in far eastern Russia. Conservation Genetics 6 (2005) 863-866
43. Otis D.L., Burnham K.P., White G.C., and Anderson D.R. Statistical inference from capture data on closed animal populations. Wildlife Monographs 62 (1978) 1-135
44. Petit E., and Valiere N. Estimating population size with noninvasive capture-mark-recapture data. Conservation Biology 20 (2006) 1062-1073
45. Piggott M.P., Banks S.C., Stone N., Banffy C., and Taylor A.C. Estimating population size of endangered brush-tailed rock-wallaby (Petrogale penicillata) colonies using faecal DNA. Molecular Ecology 15 (2006) 81-91
46. Pledger S. Unified maximum likelihood estimates for closed capture-recapture models using mixtures. Biometrics 56 (2000) 434-442
47. Prugh L.R., Ritland C.E., Arthur S.M., and Crebs C.J. Monitoring coyote population dynamics by genotyping faeces. Molecular Ecology 14 (2005) 1585-1596
48. Puechmaille S.J., and Petit E.J. Empirical evaluation of non-invasive capture-mark-recapture estimation of population size based on a single sampling session. Journal of Applied Ecology 44 (2007) 843-852
49. Ranganathan J., Chan K.M.A., Karanth K.U., and Smith J.L.D. Where can tigers persist in the future? A landscape-scale, density-based population model for the India subcontinent. Biological Conservation 141 (2008) 67-77
50. Rexstad, E., Burnham, K.P., 1993. Users' guide for interactive program CAPTURE. Abundance estimation of closed animal populations. Colorado State University, Fort Collins, CO, USA.
51. Royle A.J., and Young K.V. A hierarchical model for spatial capture-recapture data. Ecology 89 (2008) 2281-2289
52. Royle A.J., Nichols J.D., Karanth K.U., and Gopalaswamy A.M. A hierarchical model for estimating density in camera trap studies. Journal of Applied Ecology 46 (2009) 118-127
53. Rudnick J.A., Katzner T.E., Bragin E.A., and DeWoody J.A. A non-invasive genetic evaluation of population size, natal philopatry, and roosting behavior of non-breeding eastern imperial eagles (Aquila heliaca) in central Asia. Conservation Genetics 9 (2008) 667-676
54. Sanderson, E., Forrest, J., Loucks, C., et al. (2006) Setting Priorities for the Conservation and Recovery of Wild Tigers: 2005-2015, The Technical Assessment. WCS, WWF, Smithsonian and NFWF-STF, New York, Washington DC, USA.
55. Schipper J., et al. The status of the world's land and marine mammals: diversity, threat, and knowledge. Science 141 (2008) 67-77
56. Simchareon S., Pattanavibool A., Karanth K.U., Nichols J.D., and Kumar N.S. How many tigers (Panthera tigris) are there in Huai Kha Khaeng wildlife sanctuary, Thailand? An estimate using photographic capture-recapture sampling. Oryx 41 (2007) 1-7
57. Silver S.C., Ostro L.E.T., Marsh L.K., Maffei L., Noss A.J., Kelly M.J., Wallece R.B., Gomez H., and Ayala G. The use of camera traps for estimating jaguar (Panthera onca) abundance and density using capture/recapture analysis. Oryx 38 (2004) 1-7
58. Sloane M.A., Sunnucks P., Alpers D., Beheregaray L.B., and Taylor A.C. Highly reliable genetic identification of individual northern hairy-nosed wombats from single remotely collected hairs: a feasible censusing method. Molecular Ecology 9 (2000) 1233-1240
59. Smith J.L.D., McDougal C., and Miquelle M. Scent marking in free-ranging tigers, Panthera tigris. Animal Behaviour 37 (1989) 1-10
60. Solberg K.H., Bellemain E., Drageset O.M., Taberlet P., and Swenson J.E. An evaluation of field and non-invasive genetic methods to estimate brown bear (Ursus arctos) population size. Biological Conservation 128 (2006) 158-168
61. Stanley T.R., and Burnham K.P. A closure test for time-specific capture-recapture data. Environmental and Ecological Statistics 6 (1999) 197-209
62. Taberlet P., and Luikart G. Non-invasive genetic sampling and individual identification. Biological Journal of Linnean Society 68 (1999) 41-55
63. Triant D.A., Pace R.M., and Stine M. Abundance, genetic diversity and conservation of Louisiana black bears (Ursus americanus luteolus) as detected through noninvasive sampling. Conservation Genetics 5 (2004) 647-659
64. Trolle M., and Kery M. Estimation of ocelot density in the Pantanal using capture-recapture analysis of camera trapping data. Journal of Mammalogy 84 (2003) 607-614
65. Valière N. GIMLET, a computer program for analyzing genetic identification data. Molecular Ecology Notes 2 (2002) 377-379
66. Waits L.P., Luikart G., and Taberlet P. Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Molecular Ecology 10 (2001) 249-256
67. Waits, L.P., 2004. Using noninvasive genetic sampling to detect and estimate abundance of rare wildlife species. In: Thompson, W.L. (Ed.), Sampling Rare or Elusive Species: Concepts, designs, and techniques for estimating population parameters. Island press, pp. 211-228. .
68. Waits L.P., and Paetkau D. Noninvasive genetic sampling tools for wildlife biologists: a review of applications and recommendations for accurate data collection. Journal of Wildlife Management 69 (2005) 1419-1433
69. Wasser S.K., Davenport B., Ramage E.R., Hunt K.E., Parker M., Clarke C., and Stenhouse G. Scat detection dogs in wildlife research and management: application to grizzly and black bears in the Yellowhead Ecosystem, Alberta, Canada. Canadian Journal of Zoology 82 (2004) 475-492
70. Wegge P., Pokheral C.P., and Jnawali S.R. Effects of trapping effort and trap shyness on estimates of tiger abundance from camera trap studies. Animal Conservation 7 (2004) 251-256
71. White G.C., and Burnham K.P. Program MARK: survival rate estimation from both live and dead encounters. Bird Study 46 (1999) 120-139
72. White, G.C., Anderson, D.R., Burnham, K.P., Otis, D.L., 1982. Capture-Recapture Removal Methods for Sampling Closed Populations. Los Alamos National Laboratory publication no. LA-8787-NERP. Los Alamos, USA.
73. Williams B.K., Nichols J.D., and Conroy M.J. Analysis and Management of Animal Populations (2002), Academic Press, San Diego
74. Williamson J.E., Heubinger RM., Sommer J.A., Louis E.E., and Barber R.C. Development and cross-species amplification of 18 microsatellite markers in the Sumatran tiger (Panthera tigris sumatrae). Molecular Ecology Notes 2 (2002) 110-112
75. Wilson G.J., Franz A.C., Pope L.C., Roper T.J., Cheeseman C.L., and Delahay R.J. Estimation of badger abundance using faecal DNA typing. Journal of Applied Ecology 40 (2003) 658-666
76. Xu Y.C., Li B., Li W.S., Bai S.Y., Jin Y., Li X.P., Gu M.B., Jing S.Y., and Zhang W. Individualization of tiger by using microsatellites. Forensic Science International 151 (2005) 45-51
77. Zhan X., Li M., Zhang Z., Goossens B., Chen Y., Wang H., Bruford M., and Wei F. Molecular censusing doubles giant panda population estimate in a key nature reserve. Current Biology 16 (2006) R451-R452
78. Zhang Z.H., Zhang W.P., Yue B.S., Shen F.J., Zhang L., Hou R., and Zhu M.Y. Twelve polymorphic microsatellite loci for the South China tiger Panthera tigris amoyensis. Molecular Ecology Notes 6 (2005) 24-26