Hair cortisol concentration as a noninvasive measure of long-term stress in free-ranging grizzly bears (Ursus arctos): Considerations with implications for other wildlife

Canadian Journal of Zoology

Volumn 88, Issue 10, 2010, Pages 935-949

  Macbeth, B J ^a   Cattet, M R L ^a   Stenhouse, G B ^b   Gibeau, M L ^c   Janz, D M ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b Alberta Sustainable Resource Development   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BEAR; BIOMARKER; BIOMONITORING; CAPTURE METHOD; DEVELOPMENTAL BIOLOGY; DOMESTIC SPECIES; ENVIRONMENTAL FACTOR; ENVIRONMENTAL STRESS; FUNCTIONAL MORPHOLOGY; HAIR; LANDSCAPE; NATIVE SPECIES; POPULATION DENSITY; RANGE EXPANSION; SURVIVAL; SUSTAINABILITY; WILD POPULATION; WILDLIFE MANAGEMENT;

ALBERTA; CANADA;

ANIMALIA; URSUS ARCTOS;

EID: 77958530244     PISSN: 00084301     EISSN: 14803283     Source Type: Journal    
DOI: 10.1139/Z10-057     Document Type: Article

References (88)

1. Accorsi, P.A., Carloni, E., Valsecchi, P., Viggiani, R., Gamberoni, M., Tamanini, C., and Seren, E. 2008. Cortisol determination in hair and faeces from domestic cats and dogs. Gen. Comp. Endocrinol. 155(2): 398-402. doi:10.1016/j.ygcen.2007.07.002.PMID:17727851.
2. Al-Bagdadi, F.K., Titkemeyer, C.W., and Lovell, J.E. 1979. Histology of the hair cycle in male beagle dogs. Am. J. Vet. Res. 40(12): 1734-1741. PMID:525892.
3. Alberta Grizzly Bear Recovery Team. 2008. Alberta Grizzly Bear Recovery Plan 2008-2013. Alberta Sustainable Resource Development Fish and Wildlife Division, Alberta Species at Risk Recovery Plan No. 15, Edmonton. Available from http://www.srd.alberta.ca/ManagingPrograms/FishWildlifeManagement/BearManagement/GrizzlyBears/documents/GrizzlyBear-RecoveryPlan2008-13-revJuly23-2008.pdf[accessed4January2010].
4. Arnemo, J.M., Ahlqvist, P., Andersen, R., Berntsen, F., Ericsson, G., Odden, J., Brunberg, S., Segerstrom, P., and Swenson, J.E. 2006. Risks of capture-related mortality in large free-ranging mammals: experiences from Scandinavia. Wildl. Biol. 12(1): 109-113. doi:10.2981/0909-6396(2006)12[109:ROCMIL]2.0.CO;2.
5. Alberta Sustainable Resource Development. 2010. Alberta designates grizzly bears a threatened species. Alberta Sustainable Resource Development press release, 3 June 2010. Available from http://alberta.ca/acn/201006/28501FF40EEF0-D53C-C48F6FF952CC62DDEF7C.html [accessed 15 July 2010].
6. Baden, H.P., Kubilus, J., and Baden, L. 1979. A stain for plucked anagen hairs. J. Am. Acad. Dermatol. 1(2): 121-122. doi:10. 1016/S0190-9622(79)70008-9. PMID:93116.
7. Baumgartner, W.A., and Hill, V.A. 1992. Hair analysis for drugs of abuse: decontamination issues. In Recent developments in therapeutic drug monitoring and clinical toxicology. Edited by I. Sunshine. Marcel Dekker, New York. pp. 577-597.
8. Beerda, B., Schilder, M.B.H., Janssen, N.S.C.R.M., and Mol, J.A. 1996. The use of saliva cortisol, urinary cortisol, and catecholamine measurements for a noninvasive assessment of stress responses in dogs. Horm. Behav. 30(3): 272-279. doi:10.1006/ hbeh.1996.0033. PMID:8918684.
9. Belant, J.L., Seamus, T.W., and Paetkau, D. 2007. Genetic tagging of free-ranging white-tailed deer using hair snags. Ohio J. Sci. 107(4): 50-56.
10. Boonstra, R. 2005. Equipped for life: the adaptive role of the stress axis in male mammals. J. Mammal. 86(2): 236-247. doi:10. 1644/BHE-001.1.
11. Bradley, B.J., Doran-Sheehy, D.M., and Vigilant, L. 2008. Genetic identification of elusive animals: re-evaluating tracking and nesting data for wild western gorillas. J. Zool. (Lond.), 275(4): 333-340. doi:10.1111/j.1469-7998.2008.00431.x.
12. Cattet, M.R.L., Christison, K., Caulkett, N.A., and Stenhouse, G.B. 2003. Physiologic responses of grizzly bears to different methods of capture. J. Wildl. Dis. 39(3): 649-654. PMID:14567227.
13. Cattet, M.R.L., Carlson, R., Hamilton, J., Janz, D., Vijayan, M., and Boulanger, J. 2006. Understanding grizzly bear health in the context of changing landscapes. In Foothills Model Forest Grizzly Bear Research Program Annual Report 2005. Edited by G. Stenhouse and K. Graham. Foothills Model Forest, Hinton, Alta. pp. 80-86. Available from http://foothillsresearchinstitute. ca/pages/ProgramsGrizzly_Bear/default.aspx?publications=1 [accessed 4 January 2010].
14. Cattet, M.R.L., Boulanger, J., Stenhouse, G.B., Powell, R.A., and Reynolds-Hogland, M.J. 2008a. An evaluation of long-term capture effects in ursids: implications for wildlife welfare and research. J. Mammal. 89(4): 973-990. doi:10.1644/08-MAMM-A-095.1.
15. Cattet, M.R.L., Stenhouse, G.B., and Bollinger, T. 2008b. Exertional myopathy in a grizzly bear (Ursus arctos) captured by leghold snare. J. Wildl. Dis. 44(4): 973-978. PMID:18957653.
16. Charmandari, E., Tsigos, C., and Chrousos, G. 2005. Endocrinology of the stress response. Annu. Rev. Physiol. 67(1): 259-284. doi:10.1146/annurev.physiol.67.040403.120816. PMID:15709959.
17. Chown, S.L., and Gaston, K.J. 2008. Macrophysiology for a changing world. Proc. R. Soc. Lond. B Biol. Sci. 275(1642): 1469-1478. doi:10.1098/rspb.2008.0137.
18. Clara, E., Tommasi, L., and Rogers, L.J. 2008. Social mobbing calls in common marmosets (Callithrix jacchus): effects of experience and associated cortisol levels. Anim. Cogn. 11(2): 349-358. doi:10.1007/s10071-007-0125-0. PMID:18066607.
19. Cone, E.J., and Joseph, R.E., Jr. 1996. The potential for bias in hair testing for drugs of abuse. In Drug testing in hair. Edited by P. Kintz. CRC Press, Boca Raton, Fla. pp. 69-93.
20. Constable, S., Parslow, A., Dutton, G., Rogers, T., and Hogg, C. 2006. Urinary cortisol sampling: a non-invasive technique for examining cortisol concentrations in the Weddell seal, Leptonychotes weddellii. Zoo Biol. 25(2): 137-144. doi:10.1002/zoo.20088.
21. Davenport, M.D., Tiefenbacher, S., Lutz, C.K., Novak, M.A., and Meyer, J.S. 2006. Analysis of endogenous cortisol concentrations in the hair of rhesus macaques. Gen. Comp. Endocrinol. 147(3): 255-261. doi:10.1016/j.ygcen.2006.01.005.PMID: 16483573.
22. Dawson, T.J., Blaney, C.E., Munn, A.J., Krockenberger, A., and Maloney, S.K. 2000. Thermoregulation by kangaroos from mesic and arid habitats: influence of temperature on routes of heat loss in eastern grey kangaroos (Macropus giganteus) and red kangaroos (Macropus rufus). Physiol. Biochem. Zool. 73(3): 374-381. doi:10.1086/316751. PMID:10893177.
23. Diaz, S.F., Torres, S.M.F., Dunstan, R.W., and Jessen, C.R. 2004. The effect of body region on the canine hair cycle as defined by unit area trichogram. Vet. Dermatol. 15(4): 225-229. doi:10. 1111/j.1365-3164.2004.00386.x. PMID:15305929.
24. Ecke, F., Christensen, P., Sandstrom, P., and Hornfeldt, B. 2006. Identification of landscape elements related to local declines of a boreal grey-sided vole population. Landsc. Ecol. 21(4): 485-497. doi:10.1007/s10980-005-2376-y.
25. Ekkel, E.D., Dieleman, S.J., Schouten, W.G.P., Portela, A., Cornélissen, G., Tielen, M.J.M., and Halberg, F. 1996. The circadian rhythm of cortisol in the saliva of young pigs. Physiol. Behav. 60(3): 985-989. PMID:8873280.
26. Elgmork, K., and Riiser, H. 1991. Hair structure of brown bears (Ursus arctos) from North America and Scandinavia. Can. J. Zool. 69(9): 2404-2409. doi:10.1139/z91-337.
27. Felicetti, L.A., Schwartz, C.C., Rye, R.O., Haroldson, M.A., Gunther, K.A., Phillips, D.L., and Robbins, C.T. 2003. Use of sulphur and nitrogen stable isotopes to determine the importance of whitebark pine nuts to Yellowstone grizzly bears. Can. J. Zool. 81(5): 763-770. doi:10.1139/z03-054.
28. Festa-Bianchet, M. 2010. Status of the grizzly bear (Ursus arctos) in Alberta: update 2010. Alberta Wildlife Status Rep. No. 37 (Update 2010), Alberta Sustainable Resource Development and Alberta Conservation Association, Edmonton.
29. Garshelis, D.L., Gibeau, M.L., Herrero, S., and Gehrt. 2005. Grizzly bear demographics in and around Banff National Park and Kananaskis Country, Alberta. J. Wildl. Manage. 69(1): 277-297. doi:10.2193/0022-541X(2005)069<0277:GBDIAA>2.0.CO;2.
30. Gibeau, M.L., and Herrero, S. 1998. Roads, rails and grizzly bears in the Bow River Valley, Alberta. In Proceedings of the International Conference on Ecology and Transportation, Fort Meyers, Fla., 10-12 February 1998. Publ. No. FL-ER-69-98, State of Florida Department of Transportation, Environmental Management Office, Tallahassee. pp. 104-108.
31. Gosling, L.M., and McKay, H.V. 1990. Scent-rubbing and status signalling by male mammals. Chemoecology, 1(3-4): 92-95. doi:10.1007/BF01241649.
32. Gow, R., Thomson, S., Rieder, M., Van Uum, S., and Koren, G. 2010. An assessment of cortisol analysis in hair and its clinical applications. Forensic Sci. Int. 196(1-3): 32-37. doi:10.1016/j. forsciint.2009.12.040. PMID:20096513.
33. Habib, K.E., Gold, P.W., and Chrousos, G.P. 2001. Neuroendocrinology of stress. Endocrinol. Metab. Clin. North Am. 30(3): 695-728, vii-viii. doi:10.1016/S0889-8529(05)70208-5. PMID: 11571937.
34. Harkey, M.R. 1993. Anatomy and physiology of hair. Forensic Sci. Int. 63(1-3): 9-18. doi:10.1016/0379-0738(93)90255-9. PMID: 8138238.
35. Harlow, H.J., Beck, T.D.I., Walters, L.M., and Greenhouse, S. 1990. Seasonal serum glucose, progesterone and cortisol levels of black bears (Ursus americanus). Can. J. Zool. 68(1): 183-187. doi:10.1139/z90-025.
36. Hellgren, E.C., Rogers, L.L., and Seal, U.S. 1993. Serum chemistry and haematology of black bears physiological indices of habitat quality or seasonal patterns? J. Mammal. 74(2): 304-315. doi:10.2307/1382385.
37. Herrero, S. (Editor). 2005. Biology, demography, ecology and management of grizzly bears in and around Banff National Park and Kananaskis Country: final report of the Eastern Slopes Grizzly Bear Project. Faculty of Environmental Design, University of Calgary, Calgary, Alta. Available from http://www.canadianrockies.net/wp-content/uploads/2009/03/ Complete_ESGBP_FinalReport2005.pdf [accessed 4 January 2010].
38. Hunt, K.E., and Wasser, S.K. 2003. Effect of long-term preservation methods on fecal glucocorticoid concentrations of grizzly bear and African elephant. Physiol. Biochem. Zool. 76(6): 918-928. doi:10.1086/380209. PMID:14988807.
39. Jones, E.S., Heard, D.C., Gillingham, M.P., and Bowman, J. 2006. Temporal variation in stable carbon and nitrogen isotopes of grizzly bear guard hair and underfur. Wildl. Soc. Bull. 34(5): 1320-1325. doi:10.2193/0091-7648(2006)34[1320:TVISCA]2.0.CO;2.
40. Kalra, S., Einarson, A., Karaskov, T., Van Uum, S., and Koren, G. 2007. The relationship between stress and hair cortisol in healthy pregnant women. Clin. Invest. Med. 30(2): E103-E107. PMID:17716540.
41. Keay, J.M., Singh, J., Gaunt, M.C., and Kaur, T. 2006. Fecal glucocorticoids and their metabolites as indicators of stress in various mammalian species: a literature review. J. Zoo Wildl. Med. 37(3): 234-244. doi:10.1638/05-050.1. PMID:17319120.
42. Kidwell, D.A., and Blank, D.L. 1996. Environmental exposure: the stumbling block of hair testing. In Drug testing in hair. Edited by P. Kintz. CRC Press, Boca Raton, Fla. pp. 17-64.
43. Kidwell, D.A., and Smith, F.P. 2007. Passive exposure, decontamination procedures, cut-offs and bias: pitfalls in the interpretation of hair analysis results for cocaine use. In Analytical and practical aspects of drug testing in hair. Edited by P. Kintz. CRC Press, Boca Raton, Fla. pp. 25-72.
44. Kintz, P. 2004. Value of hair analysis in postmortem toxicology. Forensic Sci. Int. 142(2-3): 127-134. doi:10.1016/j.forsciint. 2004.02.027. PMID:15172076.
45. Kirschbaum, C., Tietze, A., Skoluda, N., and Dettenborn, L. 2009. Hair as a retrospective calendar of cortisol production-increased cortisol incorporation into hair in the third trimester of pregnancy. Psychoneuroendocrinology, 34(1): 32-37. doi:10.1016/j. psyneuen.2008.08.024. PMID:18947933.
46. Koren, L., Mokady, O., Karaskov, T., Klein, J., Koren, G., and Geffen, E. 2002. A novel method using hair for determining hormonal levels in wildlife. Anim. Behav. 63(2): 403-406. doi:10.1006/anbe.2001.1907.
47. Koren, L., Mokady, O., and Geffen, E. 2008. Social status and cortisol levels in singing rock hyraxes. Horm. Behav. 54(1): 212-216. doi:10.1016/j.yhbeh.2008.02.020. PMID:18423638.
48. Lindenmayer, D.B., and Fischer, J. 2006. Habitat fragmentation and landscape change: an ecological and conservation synthesis. Island Press, Washington, D.C.
49. Martin, J.G.A., and Réale, D. 2008. Animal temperament and human disturbance: implications for the response of wildlife to tourism. Behav. Processes, 77(1): 66-72. doi:10.1016/j.beproc. 2007.06.004.PMID:17683881.
50. Mattson, D.J., Herrero, S., Wright, R.G., and Pease, C.M. 1996. Science and management of Rocky Mountain grizzly bears. Conserv. Biol. 10(4): 1013-1025. doi:10.1046/j.1523-1739. 1996.10041013.x.
51. Maurel, D., Coutant, C., Boissin-Agasse, L., and Boissin, J. 1986. Seasonal moulting patterns in three fur bearing mammals: the European badger (Meles meles L.), the red fox (Vulpes vulpes L.), and the mink (Mustela vison). A morphological and histological study. Can. J. Zool. 64(8): 1757-1764. doi:10.1139/z86-265.
52. McDaniel, G.W., McKelvey, K.S., Squires, J.R., and Ruggiero, L.F. 2000. Efficacy of lures and hair snares to detect lynx. Wildl. Soc. Bull. 28(1): 119-123.
53. McEwen, B.S., and Wingfield, J.C. 2003. The concept of allostasis in biology and biomedicine. Horm. Behav. 43(1): 2-15. doi:10. 1016/S0018-506X(02)00024-7. PMID:12614627.
54. McLellan, B.N., Hovey, F.W., Mace, R.D., Woods, J.G., Carney, D.W., Gibeau, M.L., Wakkinen, W.L., and Kasworm, W.F. 1999. Rates and causes of grizzly bear mortality in the interior mountains of British Columbia, Alberta, Montana, Washington and Idaho. J. Wildl. Manage. 63(3): 911-920. doi:10.2307/3802805.
55. Millspaugh, J.J., Washburn, B.E., Milanick, M.A., Beringer, J., Hansen, L.P., and Myer, T.M. 2002. Non-invasive techniques for stress assessment in white-tailed deer. Wildl. Soc. Bull. 30(3): 899-907.
56. Moberg, G.P. 2000. The biology of animal stress. CABI publishing, New York.
57. Mormède, P., Andanson, S., Aupérin, B., Beerda, B., Guémené, D., Malmkvist, J., Manteca, X., Manteuffel, G., Prunet, P., van Reenen, C.G., Richard, S., and Veissier, I. 2007. Exploration of the hypothalamic-pituitary-adrenal function as a tool to evaluate animal welfare. Physiol. Behav. 92(3): 317-339. doi:10.1016/j. physbeh.2006.12.003. PMID:17234221.
58. Mowat, G., and Strobeck, C. 2000. Estimating population size in grizzly bears using hair capture, DNA profiling, and mark-recapture analysis. J. Wildl. Manage. 64(1): 183-193. doi:10.2307/3802989.
59. Noss, R.F., Quigley, H.B., Hornocker, M.G., Merrill, T., and Paquet, P.C. 1996. Conservation biology and carnivore conservation in the Rocky Mountains. Conserv. Biol. 10(4): 949-963. doi:10.1046/j.1523-1739.1996.10040949.x.
60. Owen, M.A., Czekala, N.M., Swaisgood, R.R., Steinman, K., and Lindburg, D.G. 2005. Seasonal and diurnal dynamics of glucocorticoids and behaviour in giant pandas. Ursus, 16(2): 208-211. doi:10.2192/1537-6176(2005)016[0208:SADDOG]2.0.CO;2.
61. Pearson, A.M. 1975. The northern interior grizzly bear Ursus arctos L. Can. Wildl. Serv. Rep. Ser. No. 34.
62. Pragst, F., and Balikova, M.A. 2006. State of the art in hair analysis for detection of drug and alcohol abuse. Clin. Chim. Acta, 370(1-2): 17-49. doi:10.1016/j.cca.2006.02.019. PMID:16624267.
63. Raul, J.S., Cirimele, V., Ludes, B., and Kintz, P. 2004. Detection of physiological concentrations of cortisol and cortisone in human hair. Clin. Biochem. 37(12): 1105-1111. doi:10.1016/j. clinbiochem.2004.02.010. PMID:15589817.
64. Reeder, D.M., and Kramer, K.M. 2005. Stress in free-ranging mammals: integrating physiology, endocrinology and natural history. J. Mammal. 86(2): 225-235. doi:10.1644/BHE-003.1.
65. Rollins, D.E., Wilkins, D.G., Krueger, G.G., Augsburger, M.P., Mizuno, A., O'Neal, C., Borges, C.R., and Slawson, M.H. 2003. The effect of hair color on the incorporation of codeine into human hair. J. Anal. Toxicol. 27(8): 545-551.PMID:14670132.
66. Rothe, M., Pragst, F., Thor, S., and Hunger, J. 1997. Effect of pigmentation on the drug deposition in hair of grey-haired subjects. Forensic Sci. Int. 84(1-3): 53-60. doi:10.1016/S0379-0738(96) 02048-8. PMID:9042710.
67. Sauvé, B., Koren, G., Walsh, G., Tokmakejian, S., and Van Uum, S.H. 2007. Measurement of cortisol in human hair as a biomarker of systemic exposure. Clin. Invest. Med. 30(5): E183-E191. PMID:17892760.
68. Schwartz, C.C., Miller, S.D., and Haroldson, M.A. 2003. Grizzly bear (Ursus arctos). In Wild mammals of North America: biology, management and conservation. 2nd ed. Edited by G.C. Feldhamer, B.C. Thompson, and J.A. Chapman. The Johns Hopkins University Press, Baltimore. pp. 556-586.
69. Stelfox B., Herrero S., and Ryerson D. 2005. Implications of historical, current and likely future transjections of human land uses and population growth to grizzly bears in the Alberta portion of the CRE. In Biology, demography, ecology and management of grizzly bears in and around Banff National Park and Kananaskis Country: final report of the Eastern Slopes Grizzly Bear Project. Edited by S. Herrero. Faculty of Environmental Design, University of Calgary, Calgary, Alta. pp. 202-222.
70. Stenhouse, G.B., and Graham, K. (Editors). 2006. Foothills Model Forest Grizzly Bear Research Program Annual Report 2005. Foothills Model Forest, Hinton, Alta. Available from http://foothillsresearchinstitute.ca/pages/ProgramsGrizzly_Bear/default.aspx?publications=1 [accessed 4 January 2010].
71. Stevens, S., and Gibeau, M. 2005. Research methods regarding capture, handling and telemetry. In Biology, demography, ecology and management of grizzly bears in and around Banff National Park and Kananaskis Country: final report of the Eastern Slopes Grizzly Bear Project. Edited by S. Herrero. Faculty of Environmental Design, University of Calgary, Calgary, Alta. pp. 17-20.
72. Thomson, S., Koren, G., Fraser, L.A., Rieder, M., Friedman, T.C., and Van Uum, S.H. 2010. Hair analysis provides a historical record of cortisol levels in Cushing's syndrome. Exp. Clin. Endocrinol. Diabetes, 118(2): 133-138. doi:10.1055/s-0029-1220771.PMID:19609841.
73. Touma, C., and Palme, R. 2005. Measuring fecal glucocorticoid metabolites in mammals and birds: the importance of validation. Ann. N.Y. Acad. Sci. 1046(1): 54-74. doi:10.1196/annals.1343. 006. PMID:16055843.
74. van der Zee, F.F., Wiertz, J., Ter Braak, C.J.F., van Apeldoorn, R.C., and Vink, J. 1992. Landscape change as a possible cause of the badger Meles meles L. decline in the Netherlands. Biol. Conserv. 61(1): 17-22. doi:10.1016/0006-3207(92)91203-5.
75. Van Uum, S.H.M., Sauvé, B., Fraser, L.A., Morley-Forster, P., Paul, T.L., and Koren, G. 2008. Elevated content of cortisol in hair of patients with severe chronic pain: a novel biomarker for stress. Stress, 11(6): 483-488. doi:10.1080/10253890801887388. PMID:18609301.
76. von der Ohe, C.G., and Servheen, C. 2002. Measuring stress in mammals using fecal glucocorticoids: opportunities and challenges. Wildl. Soc. Bull. 30(4): 1215-1225.
77. von der Ohe, C.G., Wasser, S.K., Hunt, K.E., and Servheen, C. 2004. Factors associated with fecal glucocorticoids in Alaskan brown bears (Ursus arctos horribilis). Physiol. Biochem. Zool. 77(2): 313-320. doi:10.1086/378139. PMID:15095251.
78. Wasser, S.K., Hunt, K.E., Brown, J.L., Cooper, K., Crockett, C.M., Bechert, U., Millspaugh, J.J., Larson, S., and Monfort, S.L. 2000. A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. Gen. Comp. Endocrinol. 120(3): 260-275. doi:10.1006/gcen.2000. 7557. PMID:11121291.
79. Weaver, J.L., Paquet, P.C., and Ruggiero, L.F. 1996. Resilience and conservation of large carnivores in the Rocky Mountains. Conserv. Biol. 10(4): 964-976. doi:10.1046/j.1523-1739.1996. 10040964.x.
80. Webb, E., Thomson, S., Nelson, A., White, C., Koren, G., Rieder, M., and Van Uum, S. 2010. Assessing individual systemic stress through cortisol analysis of archaeological hair. J. Archaeol. Sci. 37(4): 807-812. doi:10.1016/j.jas.2009.11.010.
81. Wennig, R. 2000. Potential problems with the interpretation of hair analysis results. Forensic Sci. Int. 107(1-3): 5-12. doi:10.1016/ S0379-0738(99)00146-2. PMID:10689559.
82. Whittle, C.L., Bowyer, R.T., Clausen, T.P., and Duffy, L.K. 2000. Putative pheromones in urine rolling of rutting male moose (Alces alces): evolution of honest advertisement? J. Chem. Ecol. 26(12): 2747-2762. doi:10.1023/A:1026485725805.
83. Wikelski, M., and Cooke, S.J. 2006. Conservation physiology. Trends Ecol. Evol. 21(1): 38-46. doi:10.1016/j.tree.2005.10.018. PMID:16701468.
84. Williams, B.W., Etter, D.R., Linden, D.W., Millenbah, K.F., Winterstein, S.R., and Scribner, K.T. 2009. Non invasive hair sampling and genetic tagging of co-distributed fisher and American marten. J. Wildl. Manage. 73(1): 26-34. doi:10.2193/2007-429.
85. Wittmer, H.U., McLellan, B.N., Serrouya, R., and Apps, C.D. 2007. Changes in landscape composition influence the decline of a threatened woodland caribou population. J. Anim. Ecol. 76(3): 568-579. doi:10.1111/j.1365-2656.2007.01220.x. PMID: 17439473.
86. Woods, J.G., Paetkau, D., Lewis, D., McLellan, B.N., Proctor, M., and Strobeck, C. 1999. Genetic tagging of free ranging black and brown bears. Wildl. Soc. Bull. 27(3): 616-627
87. Yamada, J., Stevens, B., de Silva, N., Gibbins, S., Beyene, J., Taddio, A., Newman, C., and Koren, G. 2007. Hair cortisol as a potential biologic marker of chronic stress in hospitalized neonates. Neonatology, 92(1): 42-49. doi:10.1159/000100085. PMID:17356304.
88. Young, K.M., Walker, S.L., Lanthier, C., Waddell, W.T., Monfort, S.L., and Brown, J.L. 2004. Noninvasive monitoring of adrenocortical activity in carnivores by fecal glucocorticoid analyses. Gen. Comp. Endocrinol. 137(2): 148-165. doi:10.1016/j.ygcen. 2004.02.016. PMID:15158127.