How to overcome genotyping errors in non-invasive genetic mark-recapture population size estimation - A review of available methods illustrated by a case study

Journal of Wildlife Management

Volumn 77, Issue 8, 2013, Pages 1490-1511

  Lampa, Simone ^a,b   Henle, Klaus ^a   Klenke, Reinhard ^a   Hoehn, Marion ^a,d   Gruber, Bernd ^c  

^a HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^c UNIVERSITY OF CANBERRA   (Australia)

^d CSIRO   (Australia)

Author keywords

capture mark recapture (CMR); consensus genotypes; Eurasian otter (Lutra lutra); fecal DNA; microsatellites; screening approach

Indexed keywords

CONSERVATION GENETICS; DNA; ERROR ANALYSIS; FECES; GENETIC MARKER; GENOTYPE; MARK-RECAPTURE METHOD; MUSTELID; POPULATION SIZE;

EID: 84886806893     PISSN: 0022541X     EISSN: 19372817     Source Type: Journal    
DOI: 10.1002/jwmg.604     Document Type: Review

References (145)

1. Adams, J. R., B. T. Kelly, and, L. P. Waits,. 2003. Using faecal DNA sampling and GIS to monitor hybridization between red wolves (Canis rufus) and coyotes (Canis latrans). Molecular Ecology 12: 2175-2186.
2. Adams, J. R., and, L. P. Waits,. 2007. An efficient method for screening faecal DNA genotypes and detecting new individuals and hybrids in the red wolf (Canis rufus) experimental population area. Conservation Genetics 8: 123-131.
3. Arandjelovic, M., K. Guschanski, G. Schubert, T. R. Harris, O. Thalmann, H. Siedel, and, L. Vigilant,. 2009. Two-step multiplex polymerase chain reaction improves the speed and accuracy of genotyping using DNA from noninvasive and museum samples. Molecular Ecology Resources 9: 28-36.
4. Arandjelovic, M., J. Head, L. I. Rabanal, G. Schubert, E. Mettke, C. Boesch, M. M. Robbins, and, L. Vigilant,. 2011. Non-invasive genetic monitoring of wild central chimpanzees. PLoS ONE 6 (3): e14761.
5. Arrendal, J., C. Vila, and, M. Bjorklund,. 2007. Reliability of noninvasive genetic census of otters compared to field censuses. Conservation Genetics 8: 1097-1107.
6. Banks, S. C., M. P. Piggott, B. D. Hansen, N. A. Robinson, and, A. C. Taylor,. 2002. Wombat coprogenetics: enumerating a common wombat population by microsatellite analysis of faecal DNA. Australian Journal of Zoology 50: 193-204.
7. Bayes, M. K., K. L. Smith, S. C. Alberts, J. Altmann, and, M. W. Bruford,. 2000. Testing the reliability of microsatellite typing from faecel DNA in the savannah baboon. Conservation Genetics 1: 173-176.
8. Beja-Pereira, A., R. Oliveira, P. C. Alves, M. K. Schwartz, and, G. Luikart,. 2009. Advancing ecological understandings through technological transformations in noninvasive genetics. Molecular Ecology Resources 9: 1279-1301.
9. Bellemain, E., J. E. Swenson, O. Tallmon, S. Brunberg, and, P. Taberlet,. 2005. Estimating population size of elusive animals with DNA from hunter-collected feces: four methods for brown bears. Conservation Biology 19: 150-161.
10. Bellemain, E., and, P. Taberlet,. 2004. Improved noninvasive genotyping method: application to brown bear (Ursus Arctos) faeces. Molecular Ecology 4: 519-522.
11. Bhagavatula, J., and, L. Singh,. 2006. Genotyping faecal samples of Bengal tiger (Panthera tigris tigris) for population estimation: a pilot study. BioMed Central Genetics 7: 48. http://www.biomedcentral.com/1471-2156/7/48
12. Bjorklund, M., 2005. A method for adjusting allele frequencies in the case of microsatellite allele drop-out. Mol Ecol Notes 5: 676-679.
13. Blejwas, K. M., C. L. Williams, G. T. Shin, D. R. McCullough, and, M. M. Jaeger,. 2006. Salivary DNA evidence convicts breeding male coyotes of killing sheep. Journal of Wildlife Management 70: 1087-1093.
14. Bonin, A., E. Bellemain, P. B. Eidesen, F. Pompanon, C. Brochmann, and, P. Taberlet,. 2004. How to track and assess genotyping errors in population genetics studies. Molecular Ecology 13: 3261-3273.
15. Boulanger, J., M. Proctor, S. Himmer, G. Stenhouse, D. Paetkau, and, J. Cranston,. 2006. An empirical test of DNA mark-recapture sampling strategies for grizzly bears. Ursus 17: 149-158.
16. Boulanger, J., G. C. White, B. N. McLellan, J. Woods, M. Proctor, and, S. Himmer,. 2002. A meta-analysis of grizzly bear DNA mark-recapture projects in British Columbia, Canada. Ursus 13: 137-152.
17. Brinkman, T. J., D. K. Person, F. S. Chapin, W. Smith, and, K. J. Hundertmark,. 2011. Estimating abundance of Sitka black-tailed deer using DNA from fecal pellets. Journal of Wildlife Management 75: 232-242.
18. Brinkman, T. J., D. K. Person, M. K. Schwartz, K. L. Pilgrim, K. E. Colson, and, K. J. Hundertmark,. 2010a. Individual identification of Sitka black-tailed deer (Odocoileus hemionus sitkensis) using DNA from fecal pellets. Conservation Genetics Resources 2: 115-118.
19. Brinkman, T. J., M. K. Schwartz, D. K. Person, K. L. Pilgrim, and, K. J. Hundertmark,. 2010b. Effects of time and rainfall on PCR success using DNA extracted from deer fecal pellets. Conservation Genetics 11: 1547-1552.
20. Broquet, T., N. Ménard, and, E. Petit,. 2007. 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: 249-260.
21. Broquet, T., and, E. Petit,. 2004. Quantifying genotyping errors in noninvasive population genetics. Molecular Ecology 13: 3601-3608.
22. Buchan, J. C., E. A. Archie, R. C. Van Horn, C. J. Moss, and, S. C. Alberts,. 2005. Locus effects and sources of error in noninvasive genotyping. Molecular Ecology Notes 5: 680-683.
23. Burnham, K. P., and, D. R. Anderson,. 1998. Model selection and inference: a practical information theoretic approach. Springer-Verlag, New York, New York, USA.
24. Chang, Z. F., Z. J. Liu, J. Y. Yang, M. Li, and, L. Vigilant,. 2012. Noninvasive genetic assessment of the population trend and sex ratio of the Shennongjia population of Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Chinese Science Bulletin 57: 1135-1141.
25. Chao, A., and, R. M. Huggins,. 2005. Modern closed-population capture-recapture models. Pages 58-87 in, S. C. Amstrup, T. L. McDonald, and, B. F. J. Manly, editors. Handbook of capture-recapture analysis. Princeton University Press, Princeton, New Jersey, USA.
26. Chao, A., and, H.-C. Yang,. 2003. Program Care-2 (for capture-recapture part 2). Program and user's guide. . Accessed 08 May 2013.
27. Chao, A., P. S. F. Yip, S. M. Lee, and, W. T. Chu,. 2001. Population size estimation based on estimating functions for closed capture-recapture models. Journal of Statistical Planning and Inference 92: 213-232.
28. Creel, S., G. Spong, J. L. Sands, J. Rotella, J. Zeigle, L. Joe, K. M. Murphy, and, D. Smith,. 2003. Population size estimation in Yellowstone wolves with error-prone noninvasive microsatellite genotypes. Molecular Ecology 12: 2003-2009.
29. Cullingham, C. I., M. Curteanu, M. C. Ball, and, M. Manseau,. 2010. Feasibility and recommendations for swift fox fecal DNA profiling. Journal of Wildlife Management 74: 849-859.
30. Dallas, J. F., D. N. Carss, F. Marshall, K.-P. Koepfli, H. Kruuk, S. B. Piertney, and, P. J. Bacon,. 2000. Sex identification of the Eurasian otter (Lutra lutra) by PCR typing of spraints. Conservation Genetics 1: 181-183.
31. Dallas, J. F., F. Marshall, S. B. Piertney, P. J. Bacon, and, P. A. Racey,. 2002. Spatially restricted gene flow and reduced microsatellite polymorphism in the Eurasion otter (Lutra lutra) in Britain. Conservation Genetics 3: 15-29.
32. Dallas, J. F., and, S. B. Piertney,. 1998. Microsatellite primers for the Eurasian otter. Molecular Ecology-Primer Notes 7: 1247-1263.
33. DeWoody, J., J. D. Nason, and, V. D. Hipkins,. 2006. Mitigating scoring errors in microsatellite data from wild populations. Molecular Ecology Notes 6: 951-957.
34. Dreher, B. P., S. R. Winterstein, K. T. Scribner, P. M. Lukacs, D. R. Etter, G. J. M. Rosa, V. A. Lopez, S. Libants, and, K. B. Filcek,. 2007. Noninvasive estimation of black bear abundance incorporating genotyping errors and harvested bear. Journal of Wildlife Management 71: 2684-2693.
35. Ebert, C., F. Knauer, B. Spielberger, B. Thiele, and, U. Hohmann,. 2012. Estimating wild boar (Sus scrofa) population size using faecal DNA and capture-recapture modelling. Wildlife Biology 18: 142-152.
36. Eggert, L. S., J. A. Eggert, and, D. S. Woodruff,. 2003. Estimating population sizes for elusive animals: the forest elephants of Kakum National Park, Ghana. Molecular Ecology 12: 1389-1402.
37. Ernest, H. B., M. C. T. Penedo, B. P. May, M. Syvanen, and, W. M. Boyce,. 2000. Molecular tracking of mountain lions in the Yosemite Valley region in California: genetic analysis using microsatellites and faecal DNA. Molecular Ecology 9: 433-441.
38. Ferrando, A., R. Lecis, X. Domingo-Roura, and, M. Ponsa,. 2008. Genetic diversity and individual identification of reintroduced otters (Lutra lutra) in north-eastern Spain by DNA genotyping of spraints. Conservation Genetics 9: 129-139.
39. Flagstad, O., E. Hedmark, A. Landa, H. Broseth, J. Persson, R. Andersen, P. Segerstrom, and, H. Ellegren,. 2004. Colonization history and noninvasive monitoring of a reestablished wolverine population. Conservation Biology 18: 676-688.
40. Flagstad, O., K. Roed, J. E. Stacy, and, K. S. Jakobsen,. 1999. Reliable noninvasive genotyping based on excremental PCR of nuclear DNA purified with a magnetic bead protocol. Molecular Ecology 8: 879-883.
41. Frantz, A. C., L. C. Pope, P. J. Carpenter, T. J. Roper, G. J. Wilson, R. J. Delahay, and, T. Burke,. 2003. Reliable microsatellite genotyping of the Eurasian badger (Meles meles) using faecal DNA. Molecular Ecology 12: 1649-1661.
42. Frantzen, M. A. J., J. B. Silk, J. W. H. Fergusen, R. K. Wayne, and, M. H. Kohn,. 1998. Empirical evaluation of preservation methods for faecal DNA. Molecular Ecology 7: 1423-1428.
43. Garton, E. O., J. S. Horne, J. L. Aycrigg, and, J. T. Ratti,. 2012. Research and experimental design. Pages 1-40 in, N. J. Silvy, editor. The wildlife techniques manual. Johns Hopkins University Press, Baltimore, Maryland, USA.
44. Gazey, W. J., and, M. J. Staley,. 1986. Population estimation from mark-recapture experiments using a sequential Bayes algorithm. Ecology 67: 941-951.
45. Guertin, D. A., M. Ben-David, A. S. Harestad, and, J. E. Elliott,. 2012. Fecal genotyping reveals demographic variation in river otters inhabiting a contaminated environment. Journal of Wildlife Management 76: 1540-1550.
46. Guichoux, E., L. Lagache, S. Wagner, P. Chaumeil, P. Léger, O Lepais, C. Lepoittevin, T. Malausa, E. Revardel, F. Salin, and, R. J. Petit,. 2011. Current trends in microsatellite genotyping. Molecular Ecology Resources 11: 591-611.
47. Hajkova, P., B. Zemanova, J. Bryja, B. Hajek, K. Roche, E. Tkadlec, and, J. Zima,. 2006. Factors affecting success of PCR amplification of microsatellite loci from otter faeces. Molecular Ecology Notes 6: 559-562.
48. Hajkova, P., B. Zemanova, K. Roche, and, B. Hajek,. 2009. An evaluation of field and noninvasive genetic methods for estimating Eurasian otter population size. Conservation Genetics 10: 1667-1681.
49. Hansen, H., M. Ben-David, and, D. B. McDonald,. 2008. Effects of genotyping protocols on success and errors in identifying individual river otters (Lontra canadensis) from their faeces. Molecular Ecology Resources 8: 282-289.
50. Harris, R. B., J. Winnie, S. J. Amish, A. Beja-Pereira, R. Godinho, V. Costa, and, G. Luikart,. 2010. Argali abundance in the Afghan Pamir using capture-recapture modeling from fecal DNA. Journal of Wildlife Management 74: 668-677.
51. Hauer, S., H. Ansorge, and, O. Zinke,. 2002a. Mortality patterns of otters (Lutra lutra) from Eastern Germany. Journal of Zoology 256: 361-368.
52. Hauer, S., H. Ansorge, and, O. Zinke,. 2002b. Reproductive performance of otters (Lutra lutra, Linnaeus, 1758) in Eastern Germany: low reproduction in a long-term strategy. Biological Journal of the Linnean Society 77: 329-340.
53. Hausknecht, R., R. Gula, B. Pirga, and, R. Kuehn,. 2007. Urine-a source for noninvasive genetic monitoring in wildlife. Molecular Ecology Notes 7: 208-212.
54. Hayakawa, S., and, O. Takenaka,. 1999. Urine as another potential source for template DNA in polymerase chain reaction (PCR). American Journal of Primatology 48: 299-304.
55. Hoffman, J. I., and, W. Amos,. 2005. Microsatellite genotyping errors: detection approaches, common sources and consequences for paternal exclusion. Molecular Ecology 14: 599-612.
56. Huggins, R. M., 1989. On the statistical analysis of capture experiments. Biometrika 76: 133-140.
57. Idaghdour, Y., D. Broderick, and, A. Korrida,. 2003. Faeces as a source of DNA for molecular studies in a threatened population of great bustards. Conservation Genetics 4: 789-792.
58. Inoue, E., M. Inoue-Murayama, O. Takenaka, and, T. Nishida,. 2007. Wild chimpanzee infant urine and saliva sampled noninvasively usable for DNA analyses. Primates 48: 156-159.
59. Jacob, G., R. Debrunner, F. Gugerli, B. Schmid, and, K. Bollmann,. 2010. Field surveys of capercaillie (Tetrao urogallus) in the Swiss Alps underestimated local abundance of the species as revealed by genetic analyses of non-invasive samples. Conservation Genetics 11: 33-44.
60. Johansson, M. P., B. J. McMahon, J. Hoglund, and, G. Segelbacher,. 2012. Amplification success of multilocus genotypes from feathers found in the field compared with feathers obtained from shot birds. Ibis 154: 15-20.
61. Johnson, P. C. D., and, D. T. Haydon,. 2007. Maximum-likelihood estimation of allelic dropout and false allele error rates from microsatellite genotypes in the absence of reference data. Genetics 175: 827-842.
62. Knapp, S. M., B. A. Craig, and, L. P. Waits,. 2009. Incorporating genotyping error into non-invasive DNA-based mark-recapture population estimates. Journal of Wildlife Management 73: 598-604.
63. Kohn, M., F. Knauer, A. Stoffella, W. Schröder, and, S. Pääbo,. 1995. Conservation genetics of the European brown bear-a study using excremental PCR of nuclear and mitochondrial sequences. Molecular Ecology 4: 95-103.
64. Kohn, M. H., E. C. York, D. A. Kamradt, G. Haught, R. M. Sauvajot, and, R. K. Wayne,. 1999. Estimating population size by genotyping faeces. Royal Society 266: 657-663.
65. Kruuk, H., 2006. Otters-ecology, behaviour and conservation. Oxford University Press, Oxford, United Kingdom.
66. Lampa, S., B. Gruber, K. Henle, and, M. Hoehn,. 2008. An optimisation approach to increase DNA amplification success of otter faeces. Conservation Genetics 9: 201-210.
67. Lanszki, J., A. Hidas, K. Szentes, T. Revay, I. Lehoczky, and, S. Weiss,. 2008. Relative spraint density and genetic structure of otter (Lutra lutra) along the Drava river in Hungary. Mammalian Biology 73: 40-47.
68. Lee, S. M., and, A. Chao,. 1994. Estimating population-size via sample coverage for closed capture-recapture models. Biometrics 50: 88-97.
69. Li, R., W. Fan, G. Tian, H. Zhu, L. He, J. Cai, Q. Huang, Q. Cai, B. Li, Y. Bai, Z. Zhang, Y. Zhang, W. Wang, J. Li, F. Wei, H. Li, M. Jian, J. Li, Z. Zhang, R. Nielsen, D. Li, W. Gu, Z. Yang, Z. Xuan, O. A. Ryder, F. C.-C. Leung, Y. Zhou, J. Cao, X. Sun, Y. Fu, X. Fang, X Guo, B. Wang, R. Hou, F. Shen, B. Mu, P. Ni, R. Lin, W. Qian, G. Wang, C. Yu, W. Nie, J Wang, Z. Wu, H. Liang, J. Min, Q. Wu, S. Cheng, J. Ruan, M. Wang, Z. Shi, M. Wen, B. Liu, X. Ren, H. Zheng, D. Dong, K. Cook, G. Shan, H. Zhang, C. Kosiol, X. Xie, Z. Lu, H Zheng, Y. Li, C. C. Steiner, T.T.-Y. Lam, S. Lin, Q. Zhang, G. Li, J. Tian, T. Gong, H. Liu, D. Zhang, L. Fang, C. Ye, J. Zhang, W. Hu, A. Xu, Y. Ren, G. Zhang, M. W. Bruford, Q. Li, L. Ma, Y. Guo, N. An, Y. Hu, Y. Zheng, Y. Shi, Z. Li, Q. Liu, Y. Chen, J. Zhao, N. Qu, S. Zhao, F. Tian, X. Wang, H. Wang, L. Xu, X. Liu, T. Vinar, Y. Wang, T. -W. Lam, S.-M. Yiu, S. Liu, H Zhang, D. Li, Y. Huang, X. Wang, G. Yang, Z. Jiang, J. Wang, N. Qin, L. Li, J. Li, L. Bolund, K. Kristiansen, G. K. -S. Wong, M. Olson, X. Zhang, S. Li, H. Yang, J. Wang, and, J. Wang,. 2010. The sequence and de novo assembly of the giant panda genome. Nature 463: 311-317.
70. Link, W. A., J. Yoshizaki, L. L. Bailey, and, K. H. Pollock,. 2010. Uncovering a latent multinomial: analysis of mark-recapture data with misidentification. Biometrics 66: 178-185.
71. Luikart, G., N. Ryman, D. A. Tallmon, M. K. Schwartz, and, F. W. Allendorf,. 2010. Estimation of census and effective population sizes: the increasing usefulness of DNA-based approaches. Conservation Genetics 11: 355-373.
72. Lukacs, P. M., 2010. Closed population capture-recapture models. Page 509 in, E. Cooch, and, G. C. White, editors. Program MARK-a gentle introduction. http://www.phidot.org/software/mark/docs/book/. Accessed 25 Apr 2013.
73. Lukacs, P. M., and, K. P. Burnham,. 2005a. Review of capture-recapture methods applicable to noninvasive genetic sampling. Molecular Ecology 14: 3909-3919.
74. Lukacs, P. M., and, K. P. Burnham,. 2005b. Estimating population size from DNA-based closed capture-recapture data incorporating genotyping error. Journal of Wildlife Management 69: 396-403.
75. Manly, B. F. J., S. C. Amstrup, and, T. L. McDonald,. 2005. Capture-recapture methods in practice. Princeton University Press, Princeton, New Jersey, USA.
76. Martín-Gálvez, D., J. M. Peralta-Sanchez, D. A. Dawson, A. M. Martín-Platero, M. Martínez-Bueno, T. Burke, and, J. J. Soler,. 2011. DNA sampling from eggshell swabbing is widely applicable in wild bird populations as demonstrated in 23 species. Molecular Ecology Resources 11: 481-493.
77. Marucco, F., L. Boitani, D. H. Pletscher, and, M. K. Schwartz,. 2011. Bridging the gaps between non-invasive genetic sampling and population parameter estimation. European Journal of Wildlife Research 57: 1-13.
78. McKelvey, K. S., and, M. K. Schwartz,. 2004. Genetic errors associated with population estimation using non-invasive molecular tagging: problems and new solutions. Journal of Wildlife Management 68: 439-448.
79. McKelvey, K. S., and, M. K. Schwartz,. 2005. Dropout: a program to identify problem loci and samples for noninvasive genetic samples in a capture-mark-recapture framework. Molecular Ecology Notes 5: 716-718.
80. Miller, C. R., P. Joyce, and, L. P. Waits,. 2002. Assessing allelic dropout and genotype reliability using maximum likelihood. Genetics 160: 357-366.
81. Miller, C. R., P. Joyce, and, L. P. Waits,. 2005. A new method for estimating the size of small populations from genetic mark-recapture data. Molecular Ecology 14: 1991-2005.
82. Mills, L. S., J. J. Citta, K. P. Lair, M. K. Schwartz, and, D. A. Tallmon,. 2000. Estimating animal abundance using noninvasive DNA sampling: promise and pitfalls. Ecological Applications 10: 283-294.
83. Miquel, C., E. Bellemain, C. Poillot, J. Bessière, A. Durand, and, P. Taberlet,. 2006. Quality indexes to assess the reliability of genotypes in studies using noninvasive sampling and multiple-tube approach. Molecular Ecology Notes 6: 985-988.
84. Mondol, S., K. U. Karanth, N. S. Kumar, A. M. Gopalaswamy, A. Andheria, and, U. Ramakrishnan,. 2009. Evaluation of non-invasive genetic sampling methods for estimating tiger population size. Biological Conservation 142: 2350-2360.
85. Morin, P. A., K. E. Chambers, C. Boesch, and, L. Vigilant,. 2001. Quantitative polymerase chain reaction analysis of DNA from noninvasive samples for accurate microsatellite genotyping of wild chimpanzees (Pan troglodytes versus). Molecular Ecology 10: 1835-1844.
86. Mowat, G., and, D. Paetkau,. 2002. Estimating marten (Martes americana) population size using hair capture and genetic tagging. Wildlife Biology 8: 201-209.
87. Mowat, G., and, C. Strobeck,. 2000. Estimating population size of grizzly bears using hair capture, DNA profiling, and mark-recapture analysis. Journal of Wildlife Management 64: 183-193.
88. Murphy, M. A., K. C. Kendall, A. Robinson, and, L. P. Waits,. 2007. The impact of time and field conditions on brown bear (Ursus arctos) faecal DNA amplification. Conservation Genetics 8: 1219-1224.
89. Murphy, M. A., L. P. Waits, K. C. Kendall, S. K. Wasser, J. A. Higbee, and, R. Bogden,. 2002. An evaluation of long-term preservation methods for brown bear (Ursus Arctos) faecal DNA samples. Conservation Genetics 3: 435-440.
90. Nsubuga, A. M., M. M. Robbins, A. D. Roeder, P. A. Morin, C. Boesch, and, L. Vigilant,. 2004. Factors affecting the amount of genomic DNA extracted from ape faeces and the identification of an improved sample storage method. Molecular Ecology 13: 2089-2094.
91. Otis, D. L., K. P. Burnham, G. C. White, and, D. R. Anderson,. 1978. Statistical-inference from capture data on closed animal populations. Wildlife Monographs 62: 7-135.
92. Paetkau, D., 2003. An empirical exploration of data quality in DNA-based population inventories. Molecular Ecology 12: 1375-1387.
93. Palomares, F., A. Godoy, A. Piriz, J. O'Brien, and, W. E. Johnson,. 2002. Faecal genetic analysis to determine the presence and distribution of elusive carnivores: design and feasibility for the Iberian lynx. Molecular Ecology 11: 2171-2182.
94. Palsboll, P. J., J. Allen, M. Berube, P. J. Clapham, T. P. Feddersen, P. S. Hammond, R. R. Hudson, H. Jorgensen, S. Katona, A. H. Larsen, F. Larsen, J. Lien, D. K. Mattila, J. Sigurjonsson, R. Sears, T. Smith, R. Sponer, P. Stevick, and, N. Oien,. 1997. Genetic tagging of humpback whales. Nature 388: 767-769.
95. Pennell, M. W., C. R. Stansbury, L. P. Waits, and, C. R. Miller,. 2013. Capwire: a R package for estimating population census size from non-invasive genetic sampling. Molecular Ecology Resources 13: 154-157.
96. Petit, E., and, N. Valière,. 2006. Estimating population size with noninvasive capture-mark-recapture data. Conservation Biology 20: 1062-1073.
97. Piggott, M. P., S. C. Banks, N. Stone, C. Banffy, and, A. C. Taylor,. 2006. Estimating population size of endangered brush-tailed rock-wallaby (Petrogale penicillata) colonies using faecal DNA. Molecular Ecology 15: 81-91.
98. Piggott, M. P., E. Bellemain, P. Taberlet, and, A. C. Taylor,. 2004. A multiplex pre-amplification method that significantly improves microsatellite amplification and error rates for faecal DNA in limiting conditions. Conservation Genetics 5: 417-420.
99. Piggott, M. P., and, A. C. Taylor, 2003. Extensive evaluation of faecel preservation and DNA extraction methods in Australian native and introduced species. Australian Journal of Zoology 51: 341-355.
100. Pledger, S., 2000. Unified maximum likelihood estimates for closed capture-recapture models using mixtures. Biometrics 56: 434-442.
101. Pollock, K. H., J. D. Nichols, C. Brownie, and, J. E. Hines,. 1990. Statistical inference for capture-recapture experiments. Wildlife Monographs 107: 1-97.
102. Pompanon, F., A. Bonin, E. Bellemain, and, P. Taberlet,. 2005. Genotyping errors: causes, consequences and solutions. Nature Reviews Genetics 6: 847-859.
103. Poole, K. G., D. M. Reynolds, G. Mowat, and, D. Paetkau,. 2011. Estimating mountain goat abundance using DNA from fecal pellets. Journal of Wildlife Management 75: 1527-1534.
104. Pradel, R., 1996. Utilization of capture-mark-recapture for the study of recruitment and population growth rate. Biometrics 52: 703-709.
105. Prigioni, C., L. Remonti, A. Balestrieri, S. Sgrosso, G. Priore, N. Mucci, and, E. Randi,. 2006. Estimation of European otter (Lutra lutra) population size by fecal DNA typing in southern Italy. Journal of Mammalogy 87: 855-858.
106. Puechmaille, S. J., and, E. J. Petit,. 2007. Empirical evaluation of non-invasive capture-mark-recapture estimation of population size based on a single sampling session. Journal of Applied Ecology 44: 843-852.
107. Reed, J. Z., D. J. Tollit, P. M. Thompson, and, W. Amos,. 1997. Molecular scatology: the use of molecular genetic analysis to assign species, sex and individual identity to seal faeces. Molecular Ecology 6: 225-234.
108. Rew, M. B., J. Robbins, D. Mattila, P. J. Palsboll, and, M. Berube,. 2011. How many genetic markers to tag an individual? An empirical assessment of false matching rates among close relatives. Ecological Applications 21: 877-887.
109. Robinson, S. J., L. P. Waits, and, I. D. Martin,. 2009. Estimating abundance of American black bears using DNA-based capture-mark-recapture models. Ursus 20: 1-11.
110. Roon, D. A., L. P. Waits, and, K. C. Kendall,. 2005. A simulation test of the effectiveness of several methods for error-checking non-invasive genetic data. Animal Conservation 8: 203-215.
111. Ruell, E. W., S. P. D. Riley, M. R. Douglas, J. P. Pollinger, and, K. R. Crooks,. 2009. Estimating bobcat population sizes and densities in a fragmented urban landscape using noninvasive capture-recapture sampling. Journal of Mammalogy 90: 129-135.
112. Ruibal, M., R. Peakall, A. Claridge, and, K. Firestone,. 2009. Field-based evaluation of scat DNA methods to estimate population abundance of the spotted-tailed quoll (Dasyurus maculatus), a rare Australian marsupial. Wildlife Research 36: 721-736.
113. Santini, A., V. Lucchini, E. Fabbri, and, E. Randi,. 2007. Ageing and environmental factors affect PCR success in wolf (Canis lupus) excremental DNA samples. Molecular Ecology Notes 7: 955-961.
114. Sastre, N., O. Francino, G. Lampreave, V. V. Bologov, J. M. Lopez-Martin, A. Sanchez, and, O. Ramirez,. 2009. Sex identification of wolf (Canis lupus) using non-invasive samples. Conservation Genetics 10: 555-558.
115. Scheppers, T. L. J., A. C. Frantz, M. Schaul, E. Engel, P. Breyne, L. Schley, and, T. J. Roper,. 2007. Estimating social group size of Eurasian badgers (Meles meles) by genotyping remotely plucked single hairs. Wildlife Biology 13: 195-207.
116. Schwartz, M. K., S. A. Cushman, K. S. McKelvey, J. Hayden, and, C. Engkjer,. 2006. Detecting genotyping errors and describing American black bear movement in northern Idaho. Ursus 17: 138-148.
117. Schwartz, M. K., G. Luikart, and, R. S. Waples,. 2007. Genetic monitoring as a promising tool for conservation and management. Trends in Ecology & Evolution 22: 25-33.
118. Smith, D. A., K. Ralls, A. Hurt, B. Adams, M. Parker, and, J. E. Maldonado,. 2006. Assessing reliability of microsatellite genotypes from kit fox faecal samples using genetic and GIS analyses. Molecular Ecology 15: 387-406.
119. Smith, P. J., 1991. Bayesian analyses for a multiple capture-recapture model. Biometrika 78: 399-407.
120. Solberg, K. H., E. Bellemain, O. M. Drageset, P. Taberlet, and, J. E. Swenson,. 2006. An evaluation of field and non-invasive genetic methods to estimate brown bear (Ursus arctos) population size. Biological Conservation 128: 158-168.
121. Stanley, T. R., and, J. D. Richard,. 2005. Software review: a program for testing capture-recapture data for closure. Wildlife Society Bulletin 33: 782-785.
122. Stenglein, J. L., L. P. Waits, D. E. Ausband, P. Zager, and, C. M. Mack,. 2010. Efficient, noninvasive genetic sampling for monitoring reintroduced wolves. Journal of Wildlife Management 74: 1050-1058.
123. Stevick, P. T., P. J. Palsboll, T. D. Smith, M. V. Bravington, and, P. S. Hammond,. 2001. Errors in identification using natural markings: rates, sources, and effects on capture-recapture estimates of abundance. Canadian Journal of Fisheries and Aquatic Sciences 58: 1861-1870.
124. Sundqvist, A.-K., H. Ellegren, and, C. Vilà,. 2008. Wolf or dog? Genetic identification of predators from saliva collected around bite wounds on prey. Conservation Genetics 9: 1275-1279.
125. Taberlet, P., S. Griffin, B. Goossens, S. Questiau, V. Manceau, N. Escaravage, L. P. Waits, and, J. Bouvet,. 1996. Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Research 24: 3189-3194.
126. Tredick, C. A., M. R. Vaughan, D. F. Stauffer, S. L. Simek, and, T. Eason,. 2007. Sub-sampling genetic data to estimate black bear population size: a case study. Ursus 18: 179-188.
127. Uno, R., M. Kondo, T. Yuasa, K. Yamauchi, H. Tsuruga, H. B. Tamate, and, M. Yoneda,. 2012. Assessment of genotyping accuracy in a non-invasive DNA-based population survey of Asiatic black bears (Ursus thibetanus): lessons from a large-scale pilot study in Iwate Prefecture, northern Japan. Population Ecology 54: 509-519.
128. Valière, N., 2002. Gimlet: a computer program for analysing genetic individual identification data. Molecular Ecology Notes 2: 377-379.
129. Valière, N., P. Berthier, D. Mouchiroud, and, D. Pontier,. 2002. Gemini: software for testing the effects of genotyping errors and multitubes approach for individual identification. Molecular Ecology Notes 2: 83-86.
130. Van Manen, F. T., M. F. McCollister, J. M. Nicholson, L. M. Thompson, J. L. Kindall, and, M. D. Jones,. 2012. Short-term impacts of a 4-lane highway on American black bears in eastern North Carolina. Wildlife Monographs 181: 1-35.
131. Van Oosterhout, C., W. F. Hutchinson, D. P. M. Wills, and, P. Shipley,. 2004. Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535-538.
132. Vigilant, L., and, K. Guschanski,. 2009. Using genetics to understand the dynamics of wild primate populations. Primates 50: 105-120.
133. Waits, J. L., and, P. L. Leberg,. 2000. Biases associated with population estimation using molecular tagging. Animal Conservation 3: 191-199.
134. Waits, L. P., G. Luikart, and, P. Taberlet,. 2001. Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Molecular Ecology 10: 249-256.
135. Waits, L. P., and, D. Paetkau,. 2005. Noninvasive genetic sampling tools for wildlife biologists: a review of applications and recommendations for accurate data collection. Journal of Wildlife Management 69: 1419-1433.
136. White, G. C., D. R. Anderson, K. P. Burnham, and, D. L. Otis,. 1982. Capture-recapture and removal methods for sampling closed populations. Los Alamos National Laboratory Rep. LA-8787-NERP, Los Alamos, New Mexico, USA.
137. White, G. C., and, K. P. Burnham,. 1999. Program Mark: survival estimation from populations of marked animals. Bird Study 46: 120-139.
138. Williams B. K., J. D. Nichols, and, M. J. Conroy, editors. 2002. Analysis and management of animal populations. Academic Press, San Diego, California, USA.
139. Williams, B. W., D. R. Etter, D. W. Linden, K. F. Millenbah, S. R. Winterstein, and, K. T. Scribner,. 2009. Noninvasive hair sampling and genetic tagging of co-distributed fishers and American martens. Journal of Wildlife Management 73: 26-34.
140. Wilson, G. J., A. C. Frantz, L. C. Pope, T. J. Roper, T. A. Burke, C. L. Cheeseman, and, R. J. Delahay,. 2003. Estimation of badger abundance using faecal DNA typing. Journal of Applied Ecology 40: 658-666.
141. Wright, J. A., R. J. Barker, M. R. Schofield, A. C. Frantz, A. E. Byrom, and, D. M. Gleeson,. 2009. Incorporating genotype uncertainty into mark-recapture-type models for estimating abundance using DNA samples. Biometrics 65: 833-840.
142. Wright, J. A., M. R. Schofield, and, R. J. Barker,. 2012. Closed population genetic mark-recapture with genotyping error and heterogeneity. Proceedings of the International Statistical Ecology Conference (ISEC), 3-6 July 2012, Krokkleiva, Norway.
143. Yoshizaki, J., C. Brownie, K. H. Pollock, and, W. A. Link,. 2011. Modeling misidentification errors that result from use of genetic tags in capture-recapture studies. Environmental and Ecological Statistics 18: 27-55.
144. Zhan, X. J., M. Li, Z. J. Zhang, B. Goossens, Y. P. Chen, H. J. Wang, M. W. Bruford, and, F. W. Wei,. 2006. Molecular censusing doubles giant panda population estimate in a key nature reserve. Current Biology 16: R451-R452.
145. Zhan, X. J., Y. Tao, M. Li, Z. J. Zhang, B. Goossens, Y. P. Chen, H. J. Wang, M. Bruford, and, F. W. Wei,. 2009. Accurate population size estimates are vital parameters for conserving the giant panda. Ursus 20: 56-62.