Individual heterogeneity as a pitfall in population estimates based on non-invasive genetic sampling: A review and recommendations

Wildlife Biology

Volumn 16, Issue 3, 2010, Pages 225-240

  Ebert, Cornelia ^a   Knauer, Felix ^b,c   Storch, Ilse ^b   Hohmann, Ulf ^a  

^a Research Institute for Forest Ecology and Forestry Rhineland Palatinate   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c Research Institute of Wildlife Ecology   (Austria)

Author keywords

Canis latrans; Canis lupus; capture recapture; faeces; genotyping; hair sampling; individual heterogeneity; Meles meles; population estimate; Rhinolophus hipposideros; Sus scrofa; Ursus americanus; Ursus arctos; wildlife management

Indexed keywords

ANIMALIA; AVES; CANIS FAMILIARIS; CANIS LATRANS; CANIS LUPUS; MAMMALIA; MELES MELES; RHINOLOPHUS HIPPOSIDEROS; SUIDAE; SUS SCROFA; URSUS AMERICANUS; URSUS ARCTOS;

EID: 77958525612     PISSN: 09096396     EISSN: None     Source Type: Journal    
DOI: 10.2981/09-108     Document Type: Article

References (88)

1. Artois, M., Depner, K. R., Guberti, V., Hars, J., Rossi, S. & Rutili, D. 2002: Classical swine fever (hog cholera) in wild boar in Europe. - Revue Scienfique et Technique de l'Office International des Epizooties 21:287-303.
2. Baber, D. W. & Coblentz, B. E. 1986: Density, home range, habitat use, and reproduction in feral pigs on Santa Catalina Island. - Journal of Mammalogy 67:512-525.
3. Banks, S. C., Piggott, M. P., Hansen, B. D., Robinson, N. A. & Taylor, A. C. 2002: Wombat coprogenetics: enumerating a common wombat population by microsatellite analysis of faecal DNA. - Australian Journal of Zoology 59:193-214.
4. Banks, S. C., Hoyle, S. D., Horsup, A., Sunnucks, P. & Taylor, A. C. 2003: Demographic monitoring of an entire species (the northern hairy-nosed wombat, Lasiorhinus kreftii) by genetic analysis of non-invasively collected material. - Animal Conservation 6:101-107.
5. Bates, D. & Maechler, M. 2010: lme4: Linear mixed-effects models using S4 classes. Rpackage version 0.999375-33. - Available at: http://CRAN. R-project.org/package=lme4 (Last accessed on 15 June 2010).
6. Belant, J. L., Van Stappen, J. F. & Paetkau, D. 2005: American black bear population size and genetic diversity at Apostle Islands National Lakeshore. - Ursus 16:85-92.
7. Bellemain, E., Nawaz, M. A., Valentini, A., Swenson, J. E. & Taberlet, P. 2007: Genetic tracking of brown bear in northern Pakistan and implications for conservation. - Biological Conservation 134:537-547.
8. Bellemain, E., Swenson, J. E., Tallmon, D., Brunberg, S. & Taberlet, P. 2005: Estimating population size of elusive animals with DNA from hunter-collected feces: four methods for brown bears. - Conservation Biology 19:150-161.
9. Boersen, M. R., Clark, J. D. & King, T. L. 2003: Estimating black bear population density and genetic diversity at Tensas River, Louisiana using microsatellite DNA markers. - Wildlife Society Bulletin 31:197-207.
10. Borchers, D. L., Buckland, S. T. & Zucchini, W. 2002: Estimating Animal Abundance - Closed Populations. - Statistics for Biology and Health, Springer, London, UK, 314 pp.
11. Boulanger, J., Himmer, S. & Swan, C. 2004a: Monitoring of grizzly bear population trends and demography using DNA capture-recapture methods in the Owikeno Lake area of British Columbia. - Canadian Journal of Zoology 82:1267-1277.
12. Boulanger, J., Kendall, K. C., Stetz, J. C., Roon, D. A., Waits, L. P. & Paetkau, D. 2008: Multiple data sources improve DNA-based capture-recapture estimates of grizzly bears. - Ecological Applications 18:577-589.
13. Boulanger, J. & McLellan, B. 2001: Closure violation in DNA-based capture-recapture estimation of grizzly bear populations. - Canadian Journal of Zoology 79:642-651.
14. Boulanger, J., McLellan, B. N., Woods, J. G., Proctor, M. F. & Strobeck, C. 2004b: Sampling design and bias in DNA-based capture-capture- recapture population and density estimates of grizzly bears. - Journal of Wildlife Management 68:457-469.
15. Boulanger, J., Proctor, M., Himmer, S., Stenhouse, G., Paetkau, D. & Cranston, J. 2006: An empirical test for DNA capture-recapture sampling strategies for grizzly bears. - Ursus 17:149-158.
16. Boulanger, J., Stenhouse, G. & Munro, R. 2004c: Sources of heterogeneity bias when DNA capture-recapture sampling methods are applied to grizzly bear (Ursus arctos) populations. - Journal of Mammalogy 85:618-624.
17. Boulanger, J., White, G. C., McLellan, B., Woods, J., Proctor, M. & Himmer, S. 2002: A meta-analysis of grizzly bear DNA capture-recapture projects in British Columbia, Canada. - Ursus 13:137-152.
18. Broquet, T., Menard, N. & Petit, E. 2007: Non-invasive 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.
19. Broquet, T. & Petit, E. 2004: Quantifying genotyping errors in non-invasive poulation genetics. - Molecular Ecology 13:3601-3608.
20. Burnham, K. P. & Anderson, D. R. 1998: Model selection and multimodel inference - a practical informationtheoretic approach. - Springer Verlag, 488 pp.
21. Chao, A. 1987: Estimating the population size for capturerecapture data with unequal catchability. - Biometrics 43:783-791.
22. Chao, A. L. & Jeng, S. L. 1992: Estimating population size for capture-recapture data when capture probabilities vary by time and individual animal. - Biometrics 48:201-216.
23. Choquet, R., Lebreton, J. - D., Gimenez, O., Reboulet, A. - M. & Pradel, R. 2009: U-CARE: Utilities for performing goodness of fit tests and manipulating CApture-REcapture data. - Ecography 32:1071-1074.
24. Coleman, K. & Wilson, D. S. 1998: Shyness and boldness in pumpkinseed sunfish: individual differences are contextspecific. - Animal Behaviour 56:927-936.
25. Creel, S., Spong, G., Sands, J. L., Rotella, J., Zeigle, J., Joe, L., Murphy, K. M. & Smith, D. 2003: Population size estimation in Yellowstone wolves with error-prone noninvasive microsatellite genotypes. - Molecular Ecology 12:2003-2009.
26. Crespin, L., Choquet, R., Lima, M., Merritt, J. & Pradel, R. 2008: Is heterogeneity of catchability in capture-recapture studies a mere sampling artefact or a biologically relevant feature of the population? - Population Ecology 50:247-256.
27. Cubaynes, S., Pradel, R., Choquet, R., Duchamp, C., Gaillard, J. - M., Lebreton, J. - D., Marboutin, E., Miquel, C., Reboulet, A. - M., Poillot, C., Taberlet, P. & Gimenez, O. 2010: Importance of accounting for detection heterogeneity when estimating abundance: the case of French wolves. - Conservation Biology 24:621-626.
28. Dingemanse, N. J., Both, C., van Noordwijk, A. J., Rutten, A. L. & Drent, P. 2003: Natal dispersal and personalities in great tits (Parus major). - Proceedings of the Royal Society (London) 270:741-747.
29. Dreher, B. P., Winterstein, S. R., Scribner, K. T., Lukacs, P. M., Etter, D. R., Rosa, G. J. M., Lopez, V. A., Libants, S. & Filcek, K. B. 2007: Non-invasive estimation of black bear abundance incorporating genotyping errors and harvested bear. - Journal of Wildlife Management 71:2684-2693.
30. Ebert, C., Huckschlag, D., Schulz, H. K. & Hohmann, U. 2010: Can hair traps sample wild boar (Sus scrofa) randomly for the purpose of non-invasive population estimation? - European Journal of Wildlife Research 56:583-590.
31. Eggert, L. S., Eggert, J. A. & Woodruff, D. S. 2003: Estimating population size for elusive animals: the forest elephants of Kakum National Park, Ghana. - Molecular Ecology 12:1389-1402.
32. Frantz, A. C., Pope, L. C., Carpenter, P. J., Roper, T. J., Wilson, G. J. & Delahay, R. J. 2003: Reliable microsatellite genotyping of the Eurasian badger (Meles meles) using faecal DNA. - Molecular Ecology 12:1649-1661.
33. Frantz, A. C., Schaul, M., Pope, L. C., Fack, F., Schley, L., Muller, C. P. & Roper, T. J. 2004: Estimating population size by genotyping remotely plucked hair: the Eurasian badger. - Journal of Applied Ecology 41:985-995.
34. Gervasi, V., Ciucci, P., Boulanger, J., Posillico, M., Sulli, C., Focardi, S., Randi, E. & Boitani, L. 2008: A preliminary estimate of the Apennine brown bear population size based on hair-snag sampling and multiple data source capture-recapture Huggins models. - Ursus 19:105-121.
35. Guschanski, K., Vigilant, L., McNeilage, A., Gray, M., Kagoda, E. & Robbins, M. M. 2009: Counting elusive animals: Comparing field and genetic census of the entire mountain gorilla population of Bwindi Impenetrable National Park, Uganda. - Animal Conservation 142:290-300.
36. Ihaka, R. & Gentleman, R. 1996: R: A language for data analysis and graphics. - Journal of Computational and Graphical Statistics 5:299-314.
37. Immell, D. & Anthony, R. G. 2006: Estimation of black bear abundance using a discrete DNA sampling device. - Journal of Wildlife Management 72:324-330.
38. Jacob, G., Debrunner, R., Gugerli, F., Schmid, B. & Bollmann, K. 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.
39. Knapp, S. H., Craig, B. A. & Waits, L. P. 2007: Incorporating genotyping error into non-invasive DNA-based capture-recapture population estimates. - Journal of Wildlife Management 73:598-604.
40. Kohn, M. H., York, E. C., Kamradt, D. A., Haught, G., Sauvajot, R. M. & Wayne, R. K. 1999: Estimating population size by genotyping faeces. - Proceedings of the Royal Society (London) 266:657-663.
41. Link, W. A. 2003: Nonidentifiability of population size from capture-recapture data with heterogeneous detection probabilities. - Biometrics 59:1123-1130.
42. Link, W. A. 2004: Individual heterogeneity and identifiability in capture-recapture models. - Animal Biodiversity and Conservation 27:87-91.
43. Long, R. A., Donovan, T. M., Mackay, P., Zielinski, W. J. & Buzas, J. S. 2007: Comparing faeces detection dogs, cameras, and hair snares for surveying carnivores. - Journal of Wildlife Management 71:2018-2025.
44. Lukacs, P. M. & Burnham, K. P. 2005: Review of capturerecapture methods applicable to non-invasive genetic sampling. - Molecular Ecology 14:3909-3919.
45. Marucco, F., Pletscher, D. H., Boitani, L., Schwartz, M. K., Pilgrim, K. L. & Lebreton, J. - D. 2009: Wolf survival and population trend using non-invasive capture-recapture techniques in the Western Alps. - Journal of Applied Ecology 46:1003-1010.
46. Maudet, C., Luikart, G., Dubray, D., von Hardenberg, A. & Taberlet, P. 2004: Low genotyping error rates in wild ungulate faeces sampled in winter. - Molecular Ecology Notes 4:772-775.
47. McKelvey, K. S. & Pearson, D. E. 2001: Population estimation with sparse data: the role of estimators versus indices revisited. - Canadian Journal of Zoology 79:1754-1765.
48. McKelvey, K. S. & Schwartz, M. K. 2004: Genetic errors associated with population estimation using non-invasive molecular tagging: problems and new solutions. - Journal of Wildlife Management 68:439-448.
49. McLoughlin, P. D., Cluff, H. D., Gau, R. J., Mulders, R., Case, R. & Messier, F. 2003: Effect of spatial differences in habitat on home ranges of grizzly bears. - Écoscience 10:11-16.
50. Meijer, T., Norén, K., Hellström, P., Dalén, L. & Angerbjörn, A. 2008: Estimating population parameters in a threatened arctic fox population using molecular tracking and traditional field methods. - Animal Conservation 11:330-338.
51. Menkens, G. E. & Anderson, S. H. 1988: Estimation of small-mammal population size. - Ecology 69:1952-1959.
52. Mettke-Hofmann, C., Ebert, C., Schmidt, T., Steiger, S. & Stieb, S. 2005: Personality traits in resident and migratory warbler species. - Behaviour 142:1357-1375.
53. Miller, C. R., Joyce, P. & Waits, L. P. 2005: A new method for estimating the size of small populations from genetic capture-recapture data. - Molecular Ecology 14:1991-2005.
54. Mills, L. S., Citta, J. J., Lair, K. P., Schwartz, M. K. & Tallmon, D. A. 2000: Estimating animal abundance using non-invasive DNA sampling: promise and pitfalls. - Ecological Applications 10:283-294.
55. Minta, S. & Mangel, M. 1989: Asimple population estimate based on simulation for capture-recapture and captureresight data. - Ecology 70:1738-1751.
56. Miquel, C., Bellemain, E., Poillot, C., Bessiere, J., Durand, A. & Taberlet, P. 2006: Quality indexes to assess the reliability of genotypes in studies using non-invasive sampling and multiple-tube approach. - Molecular Ecology Notes 6:985-988.
57. Mowat, G., Heard, D. C., Seip, D. R., Poole, K. G., Stenhouse, G. & Paetkau, D. W. 2005: Grizzly Ursus arctos and black bear Ursus americanus densities in the interior mountains of North America. - Wildlife Biology 11(1):31-48.
58. Mowat, G. & Paetkau, D. 2002: Estimating marten Martes americana population size using hair capture and genetic tagging. - Wildlife Biolog 8(3):201-209.
59. Mowat, G. & Strobeck, C. 2000: Estimating population size of Grizzly bears using hair capture, DNA profiling, and mark-recapture analysis. - Journal of Wildlife Management 64:183-193.
60. Obbard, M. E., Howe, E. J. & Kyle, C. J. 2010: Empirical comparison of density estimators for large carnivores. - Journal of Applied Ecology 47:76-84.
61. Otis, D. L., Burnham, K. P., White, G. C. & Anderson, D. R. 1978: Statistical inference for capture-recapture experiments. - Wildlife Monographs 62:1-135.
62. Paetkau, D. 2003: An empirical exploration of data quality in DNA-based population inventories. - Molecular Ecology 12:1375-1387.
63. Petit, E. & Valiere, N. 2006: Estimating population size with non-invasive capture-recapture data. - Conservation Biology 20:1062-1073.
64. Piggott, M. P. & Taylor, A. C. 2003: Remote collection of animal DNA and its applications in conservation management and understanding the population biology of rare and cryptic species. - Wildlife Research 30:1-13.
65. Pledger, S. & Efford, M. 1998: Correction of bias due to heterogeneous capture probability in capture-recapture studies in open populations. - Biometrics 54:888-898.
66. Pollock, K. H., Nichols, J. D., Brownie, C. & Hines, J. E. 1990: Statistical inference for capture-recapture experiments. - Wildlife Monographs 107:1-97.
67. Pollock, K. H., Nichols, J. D., Brownie, C. & Hines, J. E. 1982: Statistical inference for capture-recapture experiments. - Wildlife Monographs 107:1-97.
68. Poole, K. G., Mowat, G. & Fear, D. A. 2001: DNA-based population estimate for grizzly bears Ursus arctos in northeastern British Columbia, Canada. - Wildlife Biology 7(2):105-115.
69. Pradel, R. 2005: Multievent, an extension of multistate capture-recapture models to uncertain states. - Biometrics 61:442-447.
70. Prigioni, C., Remonti, L., Balestrieri, A., Sgrosso, S., Priore, G., Mucci, N. & Randi, E. 2006: Estimation of European otter (Lutra lutra) population size by fecal DNA typing in southern Italy. - Journal of Mammalogy 87:855-858.
71. Prugh, L. R., Ritland, C. E., Arthur, S. M. & Krebs, C. J. 2005: Monitoring coyote population dynamics by genotyping faeces. - Molecular Ecology 14:1585-1596.
72. Puechmaille, S. J. & Petit, E. 2007: Empirical evaluation of non-invasive capture-capture-recapture estimation of population size based on a single sampling session. - Journal of Applied Ecology 44:843-852.
73. Roon, D. A., Thomas, M. E., Kendall, K. C. & Waits, L. P. 2005a: Evaluating mixed samples as a source of error in non-invasive genetic studies using microsatellites. - Molecular Ecology 14:195-201.
74. Roon, D. A., Waits, L. P. & Kendall, K. C. 2005b: A simulation test of the effectiveness of several methods for error-checking non-invasive genetic data. - Animal Conservation 8:203-215.
75. Rudnick, J. A., Katzner, T. E., Bragin, E. A. & DeWoody, J. A. 2008: A non-invasive genetic evaluation of population size, natal philopatry, and roosting behaviour of non-breeding eastern imperial eagles (Aquila heliaca) in central Asia. - Conservation Genetics 9:667-676.
76. Ruis, M. A. W., te Brake, J. H. A., van de Burgwal, J. A., de Jong, I. C., Blokhuis, H. J. & Koolhaas, J. 2000: Personalities in female domesticated pigs: behavioural and physiological indications. - Applied Animal Behavioural Sciences 66:31-47.
77. Scheppers, T. L. J., Frantz, A. C., Schaul, M., Engel, E., Breyne, P., Schley, L. & Roper, T. J. 2007: Estimating social group size of Eurasian badgers Meles meles by genotyping remotely plucked single hairs. - Wildlife Biology 13(2):195-207.
78. Settlage, K. E., Van Manen, F. T., Clark, J. D. & King, T. L. 2008: Challenges of DNA-based capture-recapture studies of American black bears. - Journal of Wildlife Management 72:1035-1042.
79. Solberg, K. H., Bellemain, E., Drageset, O. - M., Taberlet, P. & Swenson, J. E. 2006: An evaluation of field and noninvasive genetic methods to estimate brown bear (Ursus arctos) population size. - Biological Conservation 128:158-168.
80. Sweitzer, R., van Vuren, D., Gardner, I. A., Boyce, W. & Waithman, J. D. 2000: Estimating sizes of wild pig populations in the north and central coast regions of California. - Journal of Wildlife Management 64:531-543.
81. Taberlet, P., Waits, L. P. & Luikart, G. 1999: Non-invasive genetic sampling: look before you leap. - Trends in Ecology and Evolution 14:323-327. (Pubitemid 29334432)
82. Triant, D. A., Pace, R. M., III. & Stine, M. 2004: Abundance, genetic diversity and conservation of Louisiana black bears (Ursus americanus luteolus) as detected through noninvasive sampling. - Conservation Genetics 5:647-659.
83. Wasser, S. K., Davenport, B., Ramage, E. R., Hunt, K. E., Parker, M., Clarke, C. & Stenhouse, G. 2004: Faeces detection dogs in wildlife research and management: application to grizzly and black bears in the Yellowhead Ecosystem, Alberta, Canada. - Canadian Journal of Zoology 82:475-492.
84. White, G. C., Andersen, D. R., Burnham, K. P. & Otis, D. L. 1982: Capture-recapture and removal methods for sampling closed populations. - Los Alamos National Laboratory Report LA-8787-NERP, Los Alamos, New Mexico, USA, 235 pp.
85. White, G. C. & Burnham, K. P. 1999: Program MARK: survival estimation from populations of marked animals. - Bird Study 46:120-138.
86. Williams, B. K., Nichols, J. D. & Conroy, M. J. 2002: Analysis and management of animal populations. - Academic Press, San Diego, California, USA, 817 pp.
87. Wilson, G. J., Frantz, A. C., Pope, L. C., Roper, T. J., Burke, T. A., Cheeseman, C. L. & Delahay, R. J. 2003: Estimation of badger abundance using faecal DNA typing. - Journal of Applied Ecology 40:658-666.
88. Woods, J. G., Paetkau, D., Lewis, D., McLellan, B. N., Proctor, M. & Strobeck, C. 1999: Genetic tagging of freeranging black and brown bears. - Wildlife Society Bulletin 27:616-627.