Glucocorticosteroid concentrations in feces and hair of captive caribou and reindeer following adrenocorticotropic hormone challenge

General and Comparative Endocrinology

Volumn 172, Issue 3, 2011, Pages 382-391

  Ashley, N T ^a   Barboza, P S ^b   Macbeth, B J ^c   Janz, D M ^c   Cattet, M R L ^c   Booth, R K ^d   Wasser, S K ^d  

^a UNIVERSITY OF ALASKA ANCHORAGE   (United States)

^b UNIVERSITY OF ALASKA FAIRBANKS   (United States)

^c UNIVERSITY OF SASKATCHEWAN   (Canada)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Caribou; Fecal glucocorticosteroids; Hair cortisol; Rangifer tarandus; Reindeer; Stress

Indexed keywords

CORTICOTROPIN; GLUCOCORTICOID; HYDROCORTISONE;

ADRENAL GLAND; ANIMAL EXPERIMENT; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DOSE RESPONSE; FECES ANALYSIS; FEMALE; HAIR ANALYSIS; HORMONAL THERAPY; HORMONE ACTION; HORMONE DETERMINATION; HORMONE RELEASE; MALE; NONHUMAN; PRIORITY JOURNAL; REINDEER; SEX DIFFERENCE;

EID: 79957856189     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2011.03.029     Document Type: Article

References (94)

1. Accorsi P.A., Carloni E., Valsecchi P., Viggiani R., Gamberoni M., Tamanini C., Seren E. Cortisol determination in hair and faeces from domestic cats and dogs. Gen. Comp. Endocrinol. 2008, 155:398-402.
2. Albert F.W., Shchepina O., Winter C., Römpler H., Teupser D., Palme R., Ceglarek U., Kratzsch J., Sohr R., Trut L.N., Thiery J., Morgentstern R., Plyusnina I.Z., Schöneberg T., Pääbo S. Phenotypic differences in behavior, physiology and neurochemistry between rats selected for tameness and for defensive aggression towards humans. Horm. Behav. 2008, 53:413-421.
3. Anisimov O.A., Vaughan D.G., Callaghan T.V., et al. Polar regions (Arctic and Antarctic). Climate Change 2007: Impacts, Adaptation and Vulnerability. Fourth Assessment Report of the Intergovernmental Panel on Climate Change 2007, 653-685. Cambridge University Press, New York. M.L. Parry (Ed.).
4. Arlettaz R., Patthey P., Baltic M., Leu T., Schaub M., Palme R., Jenni-Eiermann S. Spreading free-riding snow sports represent a novel serious threat for wildlife. Proc. R. Soc. Lond. B 2007, 274:1219-1224.
5. Baden H.P., Kubilus J., Baden L. A stain for plucked anagen hairs. J. Am. Acad. Dermatol. 1979, 1:121-122.
6. Barboza P.S., Hartbauer D.W., Hauer W.E., Blake J.E. Polygynous mating impairs body condition and homeostasis in male reindeer (Rangifer tarandus tarandus). J Comp. Physiol. B 2004, 174:309-317.
7. Barboza P.S., Parker K.L. Allocating protein to reproduction in Arctic reindeer and caribou. Physiol. Biochem. Zool. 2008, 81:835-855.
8. Barboza P.S., Parker K.L. Body protein stores and isotopic indicators of N balance in female reindeer (Rangifer tarandus) during winter. Physiol. Biochem. Zool. 2006, 79:628-644.
9. Bårdsen B., Fauchald P., Tveraa T., Langeland K., Nieminen M. Experimental evidence of costs of lactation in a low risk environment for a long-lived mammal. Oikos 2009, 118:837-852.
10. Barry T.P., Malison J.A., Held J.A., Parrish J.J. Ontogeny of the cortisol stress response in larval rainbow trout. Gen. Comp. Endocrinol. 1995, 97:57-65.
11. Bechshøft T.Ø., Sonne C., Dietz R., Born E.W., Novak M.A., Henchey E., Meyer J.S. Cortisol levels in hair of East Greenland polar bears. Sci. Total Environ. 2011, 409:831-834.
12. Bennett A., Hayssen V. Measuring cortisol in hair and saliva from dogs: coat color and pigment differences. Domest. Anim. Endocrinol. 2010, 39:171-180.
13. Bókony V., Lendvai A.Z., Liker A., Angelier F., Wingfield J.C., Chastel O. Stress response and the value of reproduction: are birds prudent parents?. Am. Nat. 2009, 173:589-598.
14. Boonstra R., Hik D., Singleton G.R., Tinnikov A. The impact of predator-induced stress on the snowshoe hare cycle. Ecol. Monogr. 1998, 79:371-394.
15. Boonstra R., Singleton G.R. Population declines in the snowshoe hare and the role of stress. Gen. Comp. Endocrinol. 1993, 91:126-143.
16. Breuner C.W., Orchinik M. Plasma binding proteins as mediators of corticosteroid action in vertebrates. J. Endocrinol. 2002, 175:99-112.
17. Brownie A.C. The metabolism of adrenal cortical steroids. The Adrenal Gland 1992, 20-224. Raven Press, New York. V.H.T. James (Ed.).
18. Brunton P.J., Russell J.A., Douglas A.J. Adaptive responses of the maternal hypothalamic-pituitary-adrenal axis during pregnancy and lactation. J. Neuroendocrinol. 2008, 20:764-776.
19. Bubenik G.A., Schams D., White R.G., Rowell J., Blake J., Bartos L. Seasonal levels of metabolic hormones and substrates in male and female reindeer (Rangifer tarandus). Comp. Biochem. Physiol. 1998, 120C:307-315.
20. Cameron R.D., Smith W.T., White R.G., Griffith B. Central arctic caribou and petroleum development: distributional, nutritional, and reproductive implications. Arctic 2005, 58:1-9.
21. Cebrian M.R., Kielland K., Finstad G. Forage quality and reindeer productivity: multiplier effects amplified by climate change. Arc. Ant. Alp. Res. 2008, 40:48-54.
22. Charbonnel N., Chaval Y., Bertheir K., Deter J., Morand S., Palme R., Cosson J. Stress and demographic decline: a potential effect mediated by impairment of reproduction and immune function in cyclic vole populations. Physiol. Biochem. Zool. 2008, 81:63-73.
23. Chinnadurai S.K., Millspaugh J.J., Matthews W.S., Canter K., Slotow R., Washburn B.E., Woods R.J. Validation of fecal glucocorticoid metabolite assays for South African herbivores. J. Wildl. Manag. 2009, 73:1014-1020.
24. Cone E.J., Joseph R.E.J. The potential for bias in hair testing for drugs of abuse. Drug Testing in Hair 1996, 69-93. CRC Press, Boca Raton. P. Kintz (Ed.).
25. Cote T.E., Yasumura S. Effect of ACTH and histamine stress on serum corticosterone and adrenal cyclic AMP levels in immature rats. Endocrinology 1975, 92:1775-1779.
26. Creel S., Fox J.E., Hardy A., Sands J., Garrott B., Peterson R.O. Snowmobile activity and glucocorticosteroid stress responses in wolves and elk. Conserv. Biol. 2002, 16:809-814.
27. Cronin M.A., MacNeil M.D., Patton J.C. Mitochondrial DNA and microsatellite DNA variation in domestic reindeer (Rangifer tarandus tarandus) and relationships with wild caribou (Rangifer tarandus granti, Rangifer tarandus groenlandicus, and Rangifer tarandus caribou). J. Hered. 2006, 97:525-530.
28. Davenport M.D., Tiefenbacher S., Lutz C.K., Novak M.A., Meyer J.S. Analysis of endogenous cortisol concentrations in the hair of rhesus macaques. Gen. Comp. Endocrinol. 2006, 147:255-261.
29. Dehnhard M., Clauss M., Lechner-Doll M., Meyer H.H.D., Palme R. Noninvasive monitoring of adrenocortical activity in roe deer (Capreolus capreolus) by measurement of fecal cortisol metabolites. Gen. Comp. Endocrinol. 2001, 123:111-120.
30. Diaz S.F., Torres S.M.F., Dunstan R.W., Jessen C.R. The effect of body region on the canine hair cycle as defined by unit area trichogram. Vet. Dermatol. 2004, 15:225-229.
31. Fauchald P., Rødven R., Bårdsen B., Langeland K., Tveraa T., Yoccoz N.G., Ims R.A. Escaping parasitism in the selfish herd: age, size and density-dependent warble fly infestation in reindeer. Oikos 2007, 116:491-499.
32. Ferin M. Stress and the reproductive system. Knobil and Neill's Physiology of Reproduction 2006, vol. 2:2627-2698. Elsevier, St. Louis.
33. G. Finstad, Applied range ecology of reindeer (Rangifer tarandus tarandus) on the Seward Pennisula, Alaska. Ph.D. Dissertation, University of Alaska, Fairbanks, 2008, p. 255.
34. Finstad G.L., Prichard A.K. Growth and body weight of free-range reindeer in Western Alaska. Rangifer 2000, 20:221-227.
35. N.L. Freeman, Motorized backcountry recreation and stress response in mountain caribou (Rangifer tarandus caribou). M.S. Thesis, The University of British Columbia, Vancouver, 2008, p. 83.
36. Goymann W. Noninvasive monitoring of hormones in bird droppings: physiological validation, sampling, extraction, sex differences, and the influence of diet on hormone metabolite levels. Ann. NY Acad. Sci. 2006, 1046:35-53.
37. Hagemoen R.I., Reimers E. Reindeer summer activity pattern in relation to weather and insect harassment. J. Anim. Ecol. 2002, 71:883-892.
38. Handa R.J., Burgess L.H., Kerr J.E., O'Keefe J.A. Gonadal steroid hormone receptors and sex differences in the hypothalamo-pituitary-adrenal axis. Horm. Behav. 1994, 28:464-476.
39. Harper J.M., Austad S.N. Fecal glucocorticoids: a noninvasive method of measuring adrenal activity in wild and captive rodents. Physiol. Biochem. Zool. 2000, 73:12-22.
40. Helle T., Kojola I. Demographics in an alpine reindeer herd: effects of density and winter weather. Ecography 2008, 31:221-230.
41. Huber S., Palme R., Zenker W., Möstl E. Non-invasive adrenocortical monitoring in red deer. J. Wildl. Manag. 2003, 67:258-266.
42. Keay J.M., Singh J., Gaunt M.C., Kaur T. Fecal glucocorticoids and their metabolites as indicators of stress in various mammalian species: a literature review. J. Zoo. Wildl. Med. 2006, 37:234-244.
43. D.A. Kidwell, D.L. Blank, Environmental exposure: the stumbling block of hair testing, in: P. Kintz (Ed.), Drug testing in hair, Boca Raton, 1996, pp. 17-64.
44. Koren L., Mokady O., Karaskov T., Klein J., Koren G., Geffen E. A novel method using hair for determining hormonal levels in wildlife. Anim. Behav. 2002, 63:403-406.
45. Künzl C., Sachser N. The behavioral endocrinology of domestication: a comparison between the domestic guinea pig (Cavia aperea f. porcellus) and its wild ancestor, the cavy (Cavis aperea). Horm. Behav. 1999, 35:28-37.
46. Love O.P., Bird D.M., Shutt L.J. Corticosterone levels during post-natal development in captive American kestrels (Falco sparverius). Gen. Comp. Endocrinol. 2003, 130:135-141.
47. Macbeth B.J., Cattet M.R.L., Stenhouse G.B., Gibeau M.L., Janz D.M. Hair cortisol concentration as a noninvasive measure of long-term stress in free-ranging grizzly bears (Ursus arctos): considerations with implications for other wildlife. Can. J. Zool. 2010, 88:935-949.
48. McMaster M.E., Munkittrick K.R., Van Der Kraak G.J. Protocol for measuring circulating levels of gonadal sex steroids in fish. Can. Tech. Rep. Fish. Aquat. Sci. 1992, 1836:29.
49. Meaney M.J., Sapolsky R.M., McEwen B.S. The development of the glucocorticoid receptor system in the rat limbic system. I. Ontogeny and autoregulation. Dev. Brain Res. 1985, 18:159-164.
50. Miller F.L., Gunn A. Catastrophic die-off of Peary caribou on the Western Queen Elizabeth Islands, Canadian High Arctic. Arctic 2003, 56:381-390.
51. Millspaugh J.J., Washburn B.E. Use of fecal glucocorticoid metabolite measures in conservation biology research: considerations for application and interpretation. Gen. Comp. Endocrinol. 2004, 138:189-199.
52. Millspaugh J.J., Washburn B.E., Milanick M.A., Beringer J., Hansen L.P., Meyer T.M. Non-invasive techniques for stress assessment in white-tailed deer. Wildl. Soc. Bull. 2002, 30:899-907.
53. National Research Council, Cumulative Environmental Effects of Oil and Gas Activities on Alaska's North Slope, The National Academies Press, Washington, DC, 2003. p. 288.
54. Neumann I.D., Bosch O.J., Toschi N., Torner L., Douglas A.J. No stress response of the hypothalamo-pituitary-adrenal axis in parturient rats: lack of involvement of brain oxytocin. Endocrinology 2003, 144:2473-2479.
55. Palme R. Measuring fecal steroids: guidelines for practical application. Ann. NY Acad. Sci. 2005, 1046:75-80.
56. Pettorelli N., Weladji R.B., Holand Ø., Mysterud A., Breie H., Stenseth N.C. The relative role of winter and spring conditions: linking climate and landscape-scale plant phenology to alpine reindeer body mass. Biol. Lett. 2005, 1:24-26.
57. Post E., Forchhammer M.C. Climate change reduces reproductive success of an Arctic herbivore through trophic mismatch. Phil. Trans. R. Soc. B 2008, 363:2369-2375.
58. Pragst F., Balikova M.A. State of the art in hair analysis for detection of drug and alcohol abuse. Clin. Chim. Acta 2006, 370:17-49.
59. Pride E.R. High faecal glucocorticoid levels predict mortality in ring-tailed lemurs (Lemur catta). Biol. Lett. 2004, 1:60-63.
60. Rödl T., Berger S., Romero L.M., Wikelski M. Tameness and stress physiology in a predator-naive island species confronted with novel predation threat. Proc. R. Soc. Lond. B 2007, 274:577-582.
61. Romero L.M. Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen. Comp. Endocrinol. 2002, 128:1-24.
62. Romero L.M., Ramenofsky M., Wingfield J.C. Season and migration alters the corticosterone response to capture and handling in an arctic migrant, the White-crowned Sparrow (Zonotrichia leucophrys gambelii). Comp. Biochem. Physiol. C 1997, 116:171-177.
63. Romero L.M., Soma K.K., Wingfield J.C. Hypothalamic-pituitary-adrenal axis changes allow seasonal modulation of corticosterone in a bird. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1998, 274:R1338-R1344.
64. Romero L.M., Wikelski M. Corticosterone levels predict survival probabilities of Galápagos marine iguanas during El Niño events. Proc. Natl. Acad. Sci. USA 2001, 98:7366-7370.
65. Romero L.M., Wingfield J.C. Alterations in hypothalamic-pituitary-adrenal function associated with captivity in Gambel's white-crowned sparrows (Zonotrichia leucophrys gambelii). Comp. Biochem. Physiol. B 1999, 122:13-20.
66. Romero L.M., Wingfield J.C. Seasonal changes in adrenal sensitivity alter corticosterone levels in Gambel's white-crowned sparrows (Zonotrichia leucophrys gambelii). Comp. Biochem. Physiol. C 1998, 119:31-36.
67. Russell D.E., Martell A.M., Nixon W.A.C. Range ecology of the Porcupine caribou herd in Canada. Rangifer 1993, 13:1-168.
68. Säkkinen H., Tornberg J., Goddard P.J., Eloranta E., Dahl E., Ropstad E., Saarela S. Adrenal responsiveness of reindeer (Rangifer tarandus tarandus) to intravenously administered ACTH. Anim. Sci. 2005, 81:399-402.
69. Sapolsky R.M., Meaney M.J. Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Res. Rev. 1986, 11:65-76.
70. Sapolsky R.M., Romero L.M., Munck A.U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 2000, 21:55-89.
71. Sauvé B., Koren G., Walsh G., Tokmakejian S., Van Uum S.H. Measurement of cortisol in human hair as a biomarker of systemic exposure. Clin. Invest. Med. 2007, 30:E183-E191.
72. Schoenfield N.M., Leathem J.H., Rabbi J. Maturation of adrenal stress response in the rat. Neuroendocrinology 1980, 31:101-105.
73. Skoogland T. Comparative social organization of wild reindeer in relation to food, mates and predator avoidance. Adv. Ethol. 1989, 29:1-74.
74. Sokal R.R., Rohlf F.J. Biometry: The Principles and Practice of Statistics in Biological Research 1995, W.H. Freeman and Company, New York, p. 880.
75. Stearns S.C. The Evolution of Life Histories 1992, Oxford University Press, New York, p. 264.
76. Teskey-Gerstl A., Bamberg W., Steineck T., Palme R. Excretion of corticosteroids in urine and faeces of hares (Lepus europaeus). J. Comp. Physiol. B 2000, 170:163-168.
77. Touma C., Möstl E., Sachser N., Palme R. Effect of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice. Gen. Comp. Endocrinol. 2003, 130:267-278.
78. Touma C., Palme R. Measuring fecal glucocorticoid metabolites in mammals and birds: the importance of validation. Ann. NY Acad. Sci. 2005, 1046:54-74.
79. Trut L.N., Naumenko E.V., Belyaev D.K. Changes in pituitary-adrenal axis during postnatal development of domesticated silver foxes (Vulpes vulpes). Genetika 1972, 8:35-43. In Russian.
80. Tyler N.J.C., Forchhammer M.C. Nonlinear effects of climate and density in the dynamics of a fluctuating population of reindeer. Ecology 2008, 89:1675-1686.
81. Vistnes I., Nelleman C. The matter of spatial and temporal scales: a review of reindeer and caribou response to human activity. Polar Biol. 2008, 31:399-407.
82. Vors L.S., Boyce M.S. Global declines of caribou and reindeer. Glob. Change Biol. 2009, 15:2626-2633.
83. Vors L.S., Schaefer J.A., Pond B.A., Rodgers A.R., Patterson B.R. Woodland caribou extirpation and anthropogenic landscape disturbance in Ontario. J. Wild. Manag. 2007, 71:1249-1256.
84. Wada H., Hahn T.P., Breuner C.W. Development of stress reactivity in white-crowned sparrow nestlings: total corticosterone response increases with age, while free corticosterone response remains low. Gen. Comp. Endocrinol. 2007, 150:405-413.
85. Wasser S.K., Bevis K., King G., Hanson E. Noninvasive physiological measures of disturbance in the northern spotted owl (Strix occidentalis caurina). Conserv. Biol. 1997, 11:1019-1022.
86. Wasser S.K., Hunt K.E., Brown J.L., Cooper K., Crockett C.M., Bechert U., Millspaugh J.J., Larson S., Monfort S.L. A generalized fecal glucocorticosteroid assay for use in a diverse array of nondomestic mammalian and avian species. Gen. Comp. Endocrinol. 2000, 120:260-275.
87. Weiler U., Claus R., Schnoebelen-Combes S., Louveau I. Influence of age and genotype on endocrine parameters and growth performance: a comparative study in Wild boars, Meishan and Large White boars. Livest. Prod. Sci. 1998, 54:21-31.
88. Weladji R.B., Holand Ø., Almøy T. Use of climatic data to assess the effect of insect harassment on the autumn weight of reindeer (Rangifer tarandus) calves. J. Zool. Lond. 2003, 260:79-85.
89. Wikelski M., Cooke S.J. Conservation physiology. Trends Ecol. Evol. 2006, 21:38-46.
90. Wingfield J.C. Avian migration: regulation of facultative-type movements. Avian Migration 2003, 113-126. Springer-Verlag, Berlin. P. Berthold, E. Gwinner, E. Sonnenschein (Eds.).
91. Wingfield J.C., Maney D.L., Breuner C.W., Jacobs J.D., Lynn S., Ramenofsky M., Richardson R.D. Ecological bases of hormone-behavior interactions: the " emergency life history stage" Am. Zool. 1998, 38:191-206.
92. Wingfield J.C., Romero L.M. Adrenocortical responses to stress and their modulation in free-living vertebrates. Handbook of Physiology, Section 7: The Endocrine System 2001, vol. 4:211-236. Oxford University Press, Oxford.
93. Wingfield J.C., Sapolsky R.M. Reproduction and resistance to stress: when and how. J. Neuroendocrinol. 2003, 15:711-724.
94. Wingfield J.C., Vleck C.M., Moore M.C. Seasonal changes of the adrenocortical response to stress in birds of the Sonoran Desert. J. Exp. Zool. 1992, 264:419-428.