Measuring fecal glucocorticoid metabolites in mammals and birds: The importance of validation

Annals of the New York Academy of Sciences

Volumn 1046, Issue , 2005, Pages 54-74

  Touma, Chadi ^a   Palme, Rupert ^b  

^a MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^b UNIVERSITY OF VETERINARY MEDICINE   (Austria)

Author keywords

ACTH challenge test; Corticosterone; Cortisol; Dexamethasone suppression test; Diurnal variation; Feces faeces; Glucocorticoids; HPA axis; Life history stages; Noninvasive monitoring; Review; Seasonal variation; Sex differences; Stress hormones; Validation

Indexed keywords

CORTICOTROPIN; DEXAMETHASONE; GLUCOCORTICOID;

ANALYTIC METHOD; BIRD; CONFERENCE PAPER; CORTICOSTEROID METABOLISM; DEXAMETHASONE SUPPRESSION TEST; EXTRACTION; FECES; FECES ANALYSIS; HORMONE ACTION; HYPOTHALAMUS HYPOPHYSIS SYSTEM; IMMUNOASSAY; LABORATORY TEST; MAMMAL; NON INVASIVE MEASUREMENT; NONHUMAN; PHYSIOLOGY; PROVOCATION TEST; SEASONAL VARIATION; SEX DIFFERENCE; SPECIES DIFFERENCE; STEROID ANALYSIS; STORAGE; STRESS; VALIDATION PROCESS;

ANIMALIA; AVES; MAMMALIA;

EID: 23744506897     PISSN: 00778923     EISSN: None     Source Type: Book Series    
DOI: 10.1196/annals.1343.006     Document Type: Conference Paper

References (123)

1. AXELROD, J. & T.D. REISINE. 1984. Stress hormones: their interaction and regulation. Science 224: 452-459.
2. MUNCK, A., P.M. GUYRE & N.J. HOLBROOK. 1984. Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocr. Rev. 5: 25-44.
3. DE KLOET, E.R., E. VREUGDENHIL, M.S. OITZL & M. JOELS. 1998. Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 19: 269-301.
4. VON HOLST, D. 1998. The concept of stress and its relevance for animal behavior. Adv. Study Behav. 27: 1-131.
5. SAPOLSKY, R.M., L.M. ROMERO & A.D. MUNCK. 2000. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Rev. 21: 55-89.
6. ENGELMANN, M., R. LANDGRAF & C.T. WOTJAK. 2004. The hypothalamic-neurohypophysial system regulates the hypothalamic-pituitary- adrenal axis under stress: an old concept revisited. Front. Neuroendocrinol. 25: 132-149.
7. LANDGRAF, R. & I. NEUMANN. 2004. Vasopressin and oxytocin release within the brain: a dynamic concept of multiple and variable modes of neuropeptide communication. Front. Neuroendocrinol. 25: 150-176.
8. ROMERO, L.M. 2004. Physiological stress in ecology: lessons from biomedical research. Trends Ecol. Evol. 19: 249-255.
9. KORTE, S.M. et al. 2005. The Darwinian concept of stress: benefits of allostasis and costs of allostatic load and the trade-off in health and disease. Neurosci. Behav. Physiol. 29: 3-38.
10. RILEY, V. 1981. Psychoneuroendocrine influences on immunocompetence and neoplasia. Science 212: 1100-1109.
11. MCEWEN, B.S. & R.M. SAPOLSKY 1995. Stress and cognitive function. Curr. Opin. Neurobiol. 5: 205-216.
12. WINGFIELD, J.C. & R.M. SAPOLSKY. 2003. Reproduction and resistance to stress: when and how. J. Neuroendocrinol. 15: 711-724.
13. HOLSBOER, F. 2000. The corticosteroid receptor hypothesis of depression. Neuropsychopharmacology 23: 477-501.
14. KORTE, S.M. 2001. Corticosteroids in relation to fear, anxiety and psychopathology. Neurosci. Biobehav. Rev. 25: 117-142.
15. MÖSTL, E., S. RETTENBACHER & R. PALME. 2005. Measurement of corticosterone metabolites in birds' droppings: an analytical approach. Ann. N.Y. Acad. Sci. 1046: 17-34.
16. PALME, R. et al. 2005. Stress hormones in mammals and birds: comparative aspects regarding metabolism, excretion and noninvasive measurement in fecal samples. Ann. N.Y. Acad. Sci. 1040:.
17. PALME, R. 2005. Measuring fecal steroids: guidelines for practical application. Ann. N.Y. Acad. Sci. 1046: 75-80.
18. HERMAN, J. P. & W.E. CULLINAN. 1997. Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci. 20: 78-84.
19. WINGFIELD, J.C., C.M. VLECK & M.C. MOORE. 1992. Seasonal changes of the adrenocortical response to stress in birds of the Sonora Desert. J. Exp. Zool. 264: 419-428
20. ROMERO, L.M. 2002. Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen. Comp. Endocrinol. 128: 1-24.
21. HENNESSY, M.B. & S. LEVINE. 1978. Sensitive pituitary-adrenal responsiveness to varying intensities of psychological stimulation. Physiol. Behav. 21: 295-297.
22. TAYLOR, W. 1971. The excretion of steroid hormone metabolites in bile and feces. Vitam. Horm. 29: 201-285.
23. 14C-steroid hormones via faeces and urine in domestic livestock. Anim. Reprod. Sci. 43: 43-63.
24. SCHWARZENBERGER, F. et al. 1996. Faecal steroid analysis for non-invasive monitoring of reproductive status in farm, wild and zoo animals. Anim. Reprod. Sci. 42: 515-526.
25. WHITTEN, P.L., D.K. BROCKMAN & R. STAVISKY. 1998. Recent advances in noninvasive techniques to monitor hormone-behavior interactions. Yrbk. Phys. Anthropol. 41: 1-23.
26. MÖSTL, E. & R. PALME. 2002. Hormones as indicators of stress. Dom. Anim. Endocrinol. 23: 67-74.
27. LINDNER, H.R. 1972. Enterohepatic circulation and patterns of urinary excretion of cortisol metabolites in the ewe. J. Endocrinol. 52: xix-xx.
28. MACDONALD, I.A., et al. 1983. Degradation of steroids in the human gut. J. Lipid Res. 24: 675-700.
29. MILLSPAUGH, J.J. & B.E. WASHBURN. 2004. Use of fecal glucocorticoid metabolite measures in conservation biology research: considerations for application and interpretation. Gen. Comp. Endocrinol. 138: 189-199.
30. GOYMANN, W. 2005. Noninvasive monitoring of hormones in bird droppings: physiological validations, sampling, extraction, sex differences, and the influence of diet on hormone metabolite levels. Ann. N.Y. Acad. Sci. 1046: 35-53.
31. KLASING, K.C. 2005. Potential impact of nutritional strategy on noninvasive measurements of hormones in birds. Ann. N.Y. Acad. Sci. 1046: 5-16.
32. WASSER, S.K. et al. 2000. A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. Gen. Comp. Endocrinol. 120: 260-275.
33. WHITTEN, P.L., R. STAVISKY, F. AURELI & E. RUSSELL. 1998. Response of fecal cortisol to stress in captive chimpanzees (Pan troglodytes). Am. J. Primatol. 44: 57-69.
34. CAVIGELLI, S.A. 1999. Behavioural patterns associated with faecal cortisol levels in free-ranging female ring-tailed femurs, Lemur catta. Anim. Behav. 57: 935-944.
35. TOUMA, C., R. PALME & N. SACHSER. 2004. Analyzing corticosterone metabolites in fecal samples of mice: a noninvasive technique to monitor stress hormones. Horm. Behav. 45: 10-22.
36. BAMBERG, E., R. PALME & J.G. MEINGASSNER. 2001. Excretion of corticosteroid metabolites in urine and faeces of rats. Lab. Anim. 35: 307-314.
37. CAVIGELLI, S.A. et al. 2005. Frequent serial fecal corticoid measures from rats reflect circadian and ovarian corticosterone rhythms. J. Endocrinol. 184: 153-163.
38. HARPER, J.M. & S.N. AUSTAD. 2000. Fecal glucocorticoids. A noninvasive method of measuring adrenal activity in wild and captive rodents. Physiol. Biochem. Zool. 73: 12-22.
39. HARPER, J.M. & S.N. AUSTAD. 2001. Effect of capture and season on fecal glucocorticoid levels in deer mice (Peromyscus maniculatus) and red-backed voles (Clethrionomys gapperi). Gen. Comp. Endocrinol. 123: 337-344.
40. TESKEY-GERSTL, A., E. BAMBERG, T. STEINECK & R. PALME. 2000. Excretion of corticosteroids in urine and faeces of hares (Lepus europaeus). J. Comp. Physiol. [B] 170: 163-168.
41. GOYMANN, W. et al. 1999. Noninvasive fecal monitoring of glucocorticoids in spotted hyenas, Crocuta crocuta. Gen. Comp. Endocrinol. 114: 340-348.
42. HUNT, K. & S.K. WASSER. 2003. Effect of long-term preservation methods on fecal glucocorticoid concentrations of grizzly bear and African elephant. Physiol. Biochem. Zool. 76: 918-928.
43. YOUNG, K.M. et al. 2004. Noninvasive monitoring of adrenocortical activity in carnivores by fecal glucocorticoid analyses. Gen. Comp. Endocrinol. 137: 148-165.
44. SCHATZ, S. & R. PALME. 2001. Measurement of faecal cortisol metabolites in cats and dogs: a noninvasive method for evaluating adrenocortical function. Vet. Res. Commun. 25: 271-287.
45. SANDS, J. & S. CREEL. 2004. Social dominance, aggression and faecal glucocorticoid levels in a wild population of wolves, Canis lupus. Anim. Behav. 67: 387-396.
46. MONFORT, S.L., K.L. MASHBURN, B.A. BREWER & S.R. CREEL. 1998. Evaluating adrenal activity in African wild dogs (Lycaon pictus) by fecal corticosteroid analysis. J. Zoo Wildl. Med. 29: 129-133.
47. CREEL, S., N.M. CREEL & S.L. MONFORT. 1997. Radiocollaring and stress hormones in African wild dogs. Conserv. Biol. 11: 544-548.
48. TERIO, K.A., S.B. CITIN & J.L. BROWN. 1999. Fecal cortisol metabolite analysis for noninvasive monitoring of adrenocortical function in the cheetah (Acinonyx jubatus). J. Zoo Wildl. Med. 30: 484-491.
49. WIELEBNOWSKI, N.C. et al. 2002. Noninvasive assessment of adrenal activity associated with husbandry and behavioral factors in the North American clouded leopard population. Zoo Biol. 21: 77-98.
50. YOUNG, K.M., J.L. BROWN & K.L. GOODROWE. 2001. Characterization of reproductive cycles and adrenal activity in the black-footed ferret (Mustela nigripes) by fecal hormone analysis. Zoo Biol. 20: 517-536.
51. MASHBURN, K.L. & S. ATKINSON. 2004. Evaluation of adrenal function in serum and feces of Steller sea lions (Eumetopias jubatus): influences of molt, gender, sample storage, and age on glucocorticoid metabolism. Gen. Comp. Endocrinol. 136: 371-381.
52. GANSWINDT, A. et al. 2003. Noninvasive assessment of adrenocortical function in the male African elephant (Loxodonta africana) and its relation to musth. Gen. Comp. Endocrinol. 134: 156-166.
53. STEAD, S.K., D.G. MELTZER & R. PALME. 2000. The measurement of glucocorticoid concentrations in the serum and faeces of captive African elephants (Loxodonta africana) after ACTH stimulation. J. South Afr. Vet. Assoc. 71: 192-196.
54. MÖSTL, E. et al. 1999. Measurement of glucocorticoid metabolite concentrations in faeces of domestic livestock. Zentralbl. Veterinarmed. A 46: 621-632.
55. MERL, S. et al. 2000. Pain causes increased concentrations of glucocorticoid metabolites in equine faeces. J. Equine Vet. Sci. 20: 586-590.
56. BROWN, J.L. et al. 2001. Comparative analysis of gonadal and adrenal activity in the black and white rhinoceros in North America by noninvasive endocrine monitoring. Zoo Biol. 20: 463-486.
57. PALME, R. et al. 1999. Measurement of faecal cortisol metabolites in ruminants: a non-invasive parameter of adrenocortical function. Wien. Tierärztl. Mschr. 86: 237-241.
58. PALME, R., C. ROBIA, W. BAUMGARTNER & E. MÖSTL. 2000. Transport stress in cattle as reflected by an increase in faecal cortisol metabolites. Vet. Rec. 146: 108-109.
59. MORROW, C.J., E.S. KOLVER, G.A. VERKERK & L.R. MATTHEWS. 2002. Fecal glucocorticoid metabolites as a measure of adrenal activity in dairy cattle. Gen. Comp. Endocrinol. 126: 229-241.
60. HUBER, S. et al. 2003. Non-invasive monitoring of adrenocortical response in red deer. J. Wildl. Manag. 67: 258-266.
61. DEHNHARD, M. et al. 2001. Non-invasive monitoring of adrenocortical activity in the roe deer (Capreolus capreolus) by measuring faecal cortisol metabolites. Gen. Comp. Endocrinol. 123: 111-120.
62. KOTRSCHAL, K. et al. 2000. Effects of physiological and social challenges in different seasons on fecal testosterone and corticosterone in male domestic geese (Anser domesticus). Acta Ethol. 2: 115-122.
63. KOTRSCHAL, K., K. HIRSCHENHAUSER & E. MÖSTL. 1998. The relationship between social stress and dominance is seasonal in greylag geese. Anim. Behav. 55: 171-176.
64. HIRSCHENHAUSER, K. et al. 2000. Endocrine and behavioural responses of male greylag geese (Anser anser) to pairbond challenges during the reproductive season. Ethology 106: 63-77.
65. RETTENBACHER, S. et al. 2004. Measurement of corticosterone metabolites in chicken droppings. Br. Poult. Sci. 45: 704-711.
66. DEHNHARD, M. et al. 2003. Measurement of plasma corticosterone and fecal glucocorticoid metabolites in the chicken (Gallus domesticus), the great cormorant (Phalacrocorax carbo), and the goshawk (Accipiter gentilis). Gen. Comp. Endocrinol. 131: 345-352.
67. THIEL, D., S. JENNI-EIERMANN & R. PALME. 2005. Measuring corticosterone metabolites in droppings of capercaillies (Tetrao urogallus). Ann N.Y. Acad. Sci. 1046: 96-108.
68. BALTIC, M. et al. 2005. A noninvasive technique to evaluate human-generated stress in the black grouse. Ann. N.Y. Acad. Sci. 1046: 81-95.
69. WASSER, S.K. et al. 1997. Noninvasive physiological measures in the northern spotted owl. Conserv. Biol. 11: 1019-1022.
70. CARERE, C. et al. 2003. Fecal corticosteroids in a territorial bird selected for different personalities: daily rhythm and the response to social stress. Horm. Behav. 43: 540-548.
71. GOYMANN, W., E. MÖSTL & E. GWINNER. 2002. Corticosterone metabolites can be measured non-invasively in excreta of European stonechats, Saxicola torquata rubicola. Auk 119: 1167-1173.
72. WELLS, K.M. et al. 2003. Effects of radio-transmitters on fecal glucocorticoid levels in captive Dickcissels. Condor 105: 805-810.
73. WASHBURN, B.E. et al. 2003. Using fecal glucocorticoids for stress assessment in mourning doves. Condor 105: 696-706.
74. NAKAGAWA, S., E. MÖSTL & J.R. WAAS. 2003. Validation of an enzyme immunoassay to measure faecal glucocorticoid metabolites from Adélie penguins (Pygoscelis adeliae): a noninvasive tool for the measurement of stress? Polar Biol. 26: 491-493.
75. PALME, R. & E. MÖSTL. 1997. Measurement of cortisol metabolites in faeces of sheep as a parameter of cortisol concentration in blood. Int. J. Mammal. Biol. 62(Suppl. II): 192-197.
76. KHAN, M.Z., J. ALTMANN, S.S. ISANI & J. YU. 2002. A matter of time: evaluating the storage of fecal samples for steroid analysis. Gen. Comp. Endocrinol. 128: 57-64.
77. TERIO, K.A. et al. 2002. Comparison of different drying and storage methods on quantifiable concentrations of fecal steroids in the cheetah. Zoo Biol. 21: 215-222.
78. WASHBURN, B.E. & J.J. MILLSPAUGH. 2002. Effects of simulated environmental conditions on glucocorticoid metabolite measurements in white-tailed deer feces. Gen. Comp. Endocrinol. 127: 217-222.
79. BEEHNER, J.C. & P.L. WHITTEN. 2004. Modifications of a field method for fecal steroid analysis in baboons. Physiol. Behav. 82: 269-277.
80. LYNCH, J.W. et al. 2003. Concentrations of four fecal steroids in wild baboons: short-term storage conditions and consequences for data interpretation. Gen. Comp. Endocrinol. 132: 264-271.
81. MILLSPAUGH, J.J. et al. 2003. Effects of heat and chemical treatments on fecal glucocorticoid measurements: implications for sample transport. Wildl. Soc. Bull. 31: 399-406.
82. GRAHAM, L.H. & J.L. BROWN. 1996. Cortisol metabolism in the domestic cat and implications for noninvasive monitoring of adrenocortical function in endangered felids. Zoo Biol. 15: 71-82.
83. PALME, R., F. WETSCHER & C. WINCKLER. 2003. Measuring faecal cortisol metabolites: a noninvasive tool to assess animal welfare in cattle? In Proc. of the IVth Central European Buiatric Congress in Lovran, April 23-27, 2003. Josip Kos, Ed.: 145-150. Faculty of Veterinary Medicine, Zagreb and Croation Veterinary Chamber.
84. CREEL, S. et al. 2002. Snowmobile activity and glucocorticoid stress responses in wolves and elk. Conserv. Biol. 16: 809-814.
85. GOYMANN, W. et al. 2001. Social, state-dependent and environmental modulation of faecal corticosteroid levels in free-ranging female spotted hyenas. Proc. R. Soc. London B: Biol. Sci. 268: 2453-2459.
86. WIELEBNOWSKI, N.C. et al. 2002. Impact of social management on reproductive, adrenal and behavioural activity in the cheetah (Acinonyx jubatus). Anim. Conserv. 5: 291-301.
87. MÖSTL, E. et al. 2002. Measurement of cortisol metabolites in faeces of ruminants. Vet. Res. Commun. 26: 127-139.
88. JONES, B.C. et al. 1998. Contribution of sex and genetics to neuroendocrine adaptation to stress in mice. Psychoneuroendocrinology 23: 505-517.
89. HANDA, R.J., L.H. BURGESS, J.E. KERR & J.A. O'KEEFE. 1994. Gonadal steroid hormone receptors and sex differences in the hypothalamo-pituitary- adrenal axis. Horm. Behav. 28: 464-476.
90. BOONSTRA, R. et al. 2001. Seasonal changes in glucocorticoid and testosterone concentrations in free-living arctic ground squirrels from the boreal forest of the Yukon. Can. J. Zool. 79: 49-58.
91. KAISER, S., M. KIRTZECK, G. HORNSCHUH & N. SACHSER. 2003. Sex-specific difference in social support-a study in female Guinea pigs. Physiol. Behav. 79: 297-303.
92. TURNER, A.I. et al. 2002. Influence of sex and gonadal status of sheep on cortisol secretion in response to ACTH and on cortisol and LH secretion in response to stress: importance of different stressors. J. Endocrinol. 173: 113-122.
93. ROMERO, L.M. & L. REMAGE-HEALEY. 2000. Daily and seasonal variation in response to stress in captive starlings (Sturnus vulgaris): corticosterone. Gen. Comp. Endocrinol. 119: 52-59.
94. RAMINELLI, J.L. et al. 2001. Morning and afternoon patterns of fecal cortisol excretion among reproductive and non-reproductive male and female common marmosets, Callitrix jacchus. Biol. Rhythm Res. 32: 159-167.
95. STRIER, K.B., J.W. LYNCH & T.E. ZIEGLER. 2003. Hormonal changes during the mating and conception seasons of wild northern muriquis (Brachyteles arachnoides hypoxanthus). Am. J. Primatol. 61: 85-99.
96. HUNT, K.E., A.W. TRITES & S.K. WASSER. 2004. Validation of fecal glucocorticoid assay for Steller sea lions (Eumetopias jubatus). Physiol. Behav. 80: 595-601.
97. HUBER, S., R. PALME & W. ARNOLD. 2003. Effects of season, sex, and sample collection on concentrations of fecal cortisol metabolites in red deer (Cervus elaphus). Gen. Comp. Endocrinol. 130: 48-54.
98. BREUNER, C.W. & M. ORCHINIK. 2002. Plasma binding proteins as mediators of corticosteroid action in vertebrates. J. Endocrinol. 175: 99-112.
99. TOUMA, C., N. SACHSER, E. MÖSTL & R. PALME. 2003. Effects of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice. Gen. Comp. Endocrinol. 130: 267-278.
100. GANSWINDT, A., H.B. RASMUSSEN, M. HEISTERMANN & J.K. HODGES. 2005. The sexually active states of free-ranging male African elephants (Loxodonta africana): defining musth and non-musth using endocrinology, physical signals, and behavior. Horm. Behav. 47: 83-91.
101. HALBERG, F., P.G. ALBRECHT & J.J. BITTNER. 1959. Corticosterone rhythm of mouse adrenal in relation to serum corticosterone and sampling. Am. J. Physiol. 197: 1083-1085.
102. ATKINSON, H.C. & B.J. WADDELL. 1997. Circadian variation in basal plasma corticosterone and adrenocorticotropin in the rat: sexual dimorphism and changes across the estrous cycle. Endocrinology 138: 3842-3848.
103. COE, C.L. & S. LEVINE. 1995. Diurnal and annual variation of adrenocortical activity in the squirrel monkey. Am. J. Primatol. 35: 283-292.
104. DE JONG, I.C. et al. 2001. Determination of the circadian rhythm in plasma corticosterone and catecholamine concentrations in growing broiler breeders using intravenous cannulation. Physiol. Behav. 74: 299-304.
105. BREUNER, C.W., J.C. WINGFIELD & L.M. ROMERO. 1999. Diel rhythms of basal and stress-induced corticosterone in a wild, seasonal vertebrate, Gambel's white-crowned sparrow. J. Exp. Zool. 284: 334-342.
106. RICH, E.L. & L.M. ROMERO. 2001. Daily and photoperiod variation of basal and stress-induced corticosterone concentrations in house sparrows (Passer domesticus). J. Comp. Physiol. B 171: 543-547.
107. PIHL, L. & J. HAU. 2003. Faecal corticosterone and immunoglobulin A in young adult rats. Lab. Anim. 37: 166-171.
108. STAVISKY, R.C., P.L. WHITTEN, D.H. HAMMETT & J.R. KAPLAN. 2001. Lake pigments facilitate analysis of fecal cortisol and behavior in group-housed macaques. Am. J. Phys. Anthropol. 116: 51-58.
109. TOUMA, C. et al. 2004. Age- and sex-dependent development of adrenocortical hyperactivity in a transgenic mouse model of Alzheimer's disease. Neurobiol. Aging 25: 893-904.
110. MAGRI, F. et al. 1997. Changes in endocrine circadian rhythms as markers of physiological and pathological brain aging. Chronobiol. Int. 14: 385-396.
111. SWAAB, D.F. 1999. Biological rhythms in health and disease: the suprachiasmatic nucleus and the autonomic nervous system. In Handbook of Clinical Neurology, The Autonomic Nervous System-Part I. Normal Functions. P.J. Vinken & G.W. Bruyn, Eds.: Vol. 74: 467-521. Elsevier, Amsterdam.
112. HARTMANN, A. et al. 1997. Twenty-four hour cortisol release profiles in patients with Alzheimer's and Parkinson's disease compared to normal controls: ultradian secretory pulsatility and diurnal variation. Neurobiol. Aging 18: 285-289.
113. KENAGY, G.J. & N.J. PLACE. 2000. Seasonal changes in plasma glucocorticosteroids of free-living female yellow-pine chipmunks: effects of reproduction and capture and handling. Gen. Comp. Endocrinol. 117: 189-199.
114. PRAVOSUDOV, V.V. et al. 2002. The effect of photoperiod on adrenocortical stress response in mountain chickadees (Poecile gambeli). Gen. Comp. Endocrinol. 126: 242-248.
115. ROMERO, L.M., K.K. SOMA & J.C. WINGFIELD. 1998. Changes in pituitary and adrenal sensitivities allow the snow bunting (Plectrophenax nivalis), an arctic-breeding song bird, to modulate corticosterone release seasonally. J. Comp. Physiol. [B] 168: 353-358.
116. ROMERO, L.M., J.M. REED & J.C. WINGFIELD. 2000. Effects of weather on corticosterone responses in wild free-living passerine birds. Gen. Comp. Endocrinol. 118: 113-122.
117. WEINGRILL, T., D.A. GRAY, L. BARRETT & S.P. HENZI. 2004. Fecal cortisol levels in free-ranging female Chacma baboons: relationship to dominance, reproductive state and environmental factors. Horm. Behav. 45: 259-269.
118. STRIER, K.B., T.E. ZIEGLER & D.J. WITTWER. 1999. Seasonal and social correlates of fecal testosterone and cortisol levels in wild male muriquis (Brachyteles arachnoides). Horm. Behav. 35: 125-134.
119. VON DER OHE, C.G., S.K. WASSER, K.E. HUNT & C. SERVHEEN. 2004. Factors associated with fecal glucocorticoids in Alaskan brown bears (Ursus arctos horribilis). Physiol. Biochem. Zool. 77: 313-320.
120. FOLEY, C.A., S. PAPAGEORGE & S.K. WASSER. 2001. Noninvasive stress and reproductive measures of social and ecological pressures in free ranging African elephants. Conserv. Biol. 15: 1134-1142.
121. MILLSPAUGH, J.J. et al. 2001. Fecal glucocorticoid assays and the physiological stress response in elk. Wildl. Soc. Bull. 29: 899-907.
122. FRIGERIO, D., J. DITTAMI, E. MÖSTL & K. KOTRSCHAL. 2004. Excreted corticosterone metabolites co-vary with air temperature and air pressure in male greylag geese (Anser anser). Gen. Comp. Endocrinol. 137: 29-36.
123. LYNCH, J.W., T.E. ZIEGLER & K.B. STRIER. 2002. Individual and seasonal variation in fecal testosterone and cortisol levels of wild male tufted capuchin monkeys, Cebus apella nigritus. Horm. Behav. 41: 275-287.