Use of fecal glucocorticoid metabolite measures in conservation biology research: Considerations for application and interpretation

General and Comparative Endocrinology

Volumn 138, Issue 3, 2004, Pages 189-199

  Millspaugh, Joshua J ^a   Washburn, Brian E ^b  

^a UNIVERSITY OF MISSOURI   (United States)

^b U S DEPARTMENT OF AGRICULTURE   (United States)

Author keywords

ACTH challenge; Conservation biology; Corticosterone; Cortisol; Fecal glucocorticoids; Feces; Noninvasive; Physiology; Stress; Stress response; Wildlife

Indexed keywords

GLUCOCORTICOID; STEROID HORMONE;

ARTICLE; CONSERVATION BIOLOGY; COST; DATA BASE; DIET; FECES ANALYSIS; IMMUNOASSAY; LITERATURE; MEASUREMENT; METABOLITE; NONHUMAN; PRIORITY JOURNAL; REPRODUCTION; RESEARCH; SAMPLING; STEROID METABOLISM; WILDLIFE;

EID: 4444346055     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2004.07.002     Document Type: Review

References (104)

1. H. Aldercreutz, F. Martin, M. Pulkkinen, H. Dencker, U. Rimér, N.-O. Sjöberg, and M.J. Tikkanen Intestinal metabolism of estrogens Journal of Clinical Endocrinology and Metabolism 43 1976 497 505
2. L.B. Astheimer, W.A. Buttemer, and J.C. Wingfield Interactions of corticosterone with feeding, activity and metabolism in passerine birds Ornis Scandinavia 23 1992 355 365
3. N. Bahr, R. Palme, U. Möhle, K. Hodges, and M. Heistermann Comparative aspects of the metabolism and excretion of cortisol in three individual nonhuman primates General and Comparative Endocrinology 117 2000 427 438
4. J.L. Barnett, P.H. Hemsworth, G.M. Cronin, E.A. Newman, and T.H. McCallum Effects of design of individual cage-stalls on the behavior and physiological responses related to the welfare of pregnant pigs Applied Animal Behavior Science 32 1991 23 34
5. A.B. Bercovitz, N.M. Czekala, and B.L. Lasley A new method of sex determination in monomorphic birds Journal of Zoo and Animal Medicine 9 1978 114 124
6. E.V. Berkeley, J.F. Kirkpatrick, N.E. Schaffer, W.M. Bryant, and W.R. Threlfall Serum and fecal steroid analysis of ovulation, pregnancy, and parturition in the black rhinocerus (Diceros bicornis) Zoo Biology 16 1997 121 132
7. V.D. Bokkenheuser, and J. Winter Biotransformation of steroid hormones by gut bacteria American Journal of Clinical Nutrition 33 1980 2502 2506
8. C.W. Breuner, J.C. Wingfield, and L.M. Romero Diel rhythms of basal and stress-induced corticosterone in a wild, seasonal vertebrate, Gambel's white-crowned sparrow Journal of Experimental Zoology 284 1999 334 342
9. J.L. Brown, S.K. Wasser, D.E. Wildt, and L.H. Graham Comparative aspects of steroid hormone metabolism and ovarian activity in felids, measured noninvasively in feces Biology of Reproduction 51 1994 776 786
10. C.J. Cook, D.J. Mellor, P.J. Harris, J.R. Ingram, and L.R. Matthews Hands-on and hands-off measurement of stress G.P. Moberg J.A. Mench The Biology of Animal Stress 2000 CABI Publishing, New York New York, USA 123 146
11. J.V. Craig, and J.A. Craig Corticosteroid levels in white leghorn hens as affected by handling, laying house environment, and genetic stock Poultry Science 64 1985 809 816
12. S. Creel, J.E. Fox, A. Hardy, J. Sands, B. Garrott, and R.O. Peterson Snowmobile activity and glucocorticoid stress responses in wolves and elk Conservation Biology 16 2002 809 814
13. A. Dawson, and P.D. Howe Plasma corticosterone in wild starlings (Sturnus vulgaris) immediately following capture and in relation to body weight during the annual cycle General and Comparative Endocrinology 51 1983 303 308
14. M. Dehnhard, A. Schreer, O. Krone, K. Jewgenow, M. Krause, and R. Grossmann Measurement of plasma corticosterone and fecal glucocorticoid metabolites in the chicken (Gallus domesticus), the great cormorant (Phalacrocorax carbo), and the goshawk (Accipiter gentiles) General and Comparative Endocrinology 131 2003 345 352
15. M. Dehnhard, M. Clauss, M. Lechner-Doll, H.H.D. Meyer, and R. Palme Noninvasive monitoring of adrenocortical activity in roe deer (Capreolus capreolus) by measurement of fecal cortisol metabolites General and Comparative Endocrinology 123 2001 111 120
16. A.M. Dufty Jr., and J.R. Belthoff Corticosterone and the stress response in young western screech-owls: effects of captivity, gender, and activity period Physiological Zoology 70 1997 143 149
17. Ewing, S.A., Lay Jr., D.C., von Borell, E., 1999. Farm Animal Well-being, Prentice Hall, Upper Saddle River, New Jersey, USA
18. C.A.H. Foley, S. Papageorge, and S.K. Wasser Noninvasive stress and reproductive measures of social and ecological pressures in free-ranging African elephants Conservation Biology 15 2001 1134 1142
19. A. Ganswindt, R. Palme, M. Heistermann, S. Borragan, and J.K. Hodges Non-invasive assessment of adrenocortical function in the male African elephant (Loxodonta africana) and its relation to musth General and Comparative Endocrinology 134 2003 156 166
20. B.R. Goldin, H. Adlercreutz, S.L. Gorbach, J.H. Warram, J.T. Dwyer, L. Swenson, and M.N. Woods Effect of diet on excretion of estrogen and pre- and post-menopausal woman Cancer Research 41 1981 3771 3773
21. B.R. Goldin, H. Adlercreutz, S.L. Gorbach, J.H. Warram, J.T. Dwyer, L. Swenson, and M.N. Woods Estrogen excretion patterns and plasma levels in vegetarian and omnivorous women New England Journal of Medicine 307 1982 1542 1547
22. T. Good, M.Z. Khan, and J.W. Lynch Biochemical and physiological validation of a corticosteroid radioimmunoassay for plasma and fecal samples in oldfield mice (Peromyscus polionotus) Physiology and Behavior 80 2003 405 411
23. W. Goymann, E. Möstl, T. Van't Hof, M.L. East, and H. Hofer Noninvasive fecal monitoring of glucocorticoids in spotted hyenas (Crocuta crocuta) General and Comparative Endocrinology 114 1999 340 348
24. W. Goymann, E. Möstl, and E. Gwinner Corticosterone metabolites can be measured noninvasively in excreta of European stonechats (Saxicola torquata rubicola) Auk 119 2002 1167 1173
25. L.H. Graham, and J.L. Brown Cortisol metabolism in the domestic cat and implications for non-invasive monitoring of adrenocortical function in endangered felids Zoo Biology 15 1996 71 82
26. L.F. Gregory, and J.R. Schmid Stress responses and sexing of wild Kemp's Ridley Sea Turtles (Lepidochelys kempii) in the Northeastern Gulf of Mexico General and Comparative Endocrinology 124 2001 66 74
27. M.E. Hadley Endocrinology 1996 Prentice-Hall, Upper Saddle River New Jersey, USA
28. G.D. Hamilton, and H.P. Weeks Jr. Cortisol and aldosterone comparisons of cottontail rabbits collected by shooting, trapping, falconry Journal of Wildlife Diseases 31 1985 40 42
29. H.J. Harlow, T.D.I. Beck, L.M. Walters, and S.S. Greenhouse Seasonal serum glucose, progesterone, and cortisol levels of black bears (Ursus americanus) Canadian Journal of Zoology 68 1990 183 187
30. J.M. Harper, and S.N. Austad Fecal glucocorticoids: a noninvasive method of measuring adrenal activity in wild and captive rodents Physiological and Biochemical Zoology 73 2000 12 22
31. J.M. Harper, and S.N. Austad Effect of capture and season on fecal glucocorticoid levels in deer mice (Peromyscus maniculatus) and red-backed voles (Clethrionomys gapperi) General and Comparative Endocrinology 123 2001 337 344
32. V. Hayssen, J.M. Harper, and R. DeFina Fecal corticosteroids in agouti and non-agouti deer mice (Peromyscus maniculatus) Comparative Biochemistry and Physiology A - Molecular and Integrative Physiology 132 2002 439 446
33. J.A. Heath, and A.M. Dufty Jr. Body condition and the adrenal stress response in captive American kestrel juveniles Physiological Zoology 71 1998 67 73
34. R.L. Holberton Changes in patterns of corticosterone secretion concurrent with migratory fattening in a neotropical migratory bird General and Comparative Endocrinology 116 1999 49 58
35. L.C. Hood, P.D. Boersma, and J.C. Wingfield The adrenocortical response to stress in incubating magellanic penguins (Spheniscus magellanicus) Auk 115 1998 76 84
36. S. Huber, R. Palme, and W. Arnold Effects of season, sex, and sample collection on concentrations of fecal cortisol metabolites in red deer (Cervus elaphus) General and Comparative Endocrinology 130 2003 48 54
37. K.E. Hunt, A.W. Trites, and S.K. Wasser Validation of a fecal glucocorticoid assay for Stellar sea lions (Eumetopias jubatus) Physiology and Behavior 80 2004 595 601
38. M.M. Joseph, and A.H. Meier Daily rhythms of plasma corticosterone in the Common Pigeon, Columba livia General and Comparative Endocrinology 20 1973 326 330
39. M.H. Jurke, N.M. Czekala, D.G. Lindburg, and S.E. Millard Fecal corticoid metabolite measurement in the cheetah (Acinonyx jabatus) Zoo Biology 16 1997 133 147
40. G.J. Kenagy, and N.J. Place Seasonal changes in plasma glucocorticosteroids of free-living yellow pine chipmunks: effects of reproduction and capture and handling General and Comparative Endocrinology 117 2000 189 199
41. M.Z. Khan, J. Altmann, S.S. Isani, and J. Yu A matter of time: evaluating the storage of fecal samples for steroid analysis General and Comparative Endocrinology 128 2002 57 64
42. J.F. Kirkpatrick, J.C. McCarthy, D.F. Gudermuth, S.E. Shideler, and B.L. Lasley An assessment of the reproductive biology of Yellowstone bison (Bison bison) subpopulations using noncapture methods Canadian Journal of Zoology 74 1996 8 14
43. Y. Le Maho, H. Karmann, D. Briot, Y. Handrich, J.-P. Robin, E. Mioskowski, Y. Cherel, and J. Farni Stress in birds due to routine handling and how to avoid it American Journal of Physiology 263 1992 R775 R781
44. J.W. Ludders, J.A. Langenberg, N.M. Czekala, and H.N. Erb Fecal corticosterone reflects serum corticosterone in Florida sandhill cranes Journal of Wildlife Diseases 37 2001 646 652
45. J.W. Lynch, M.Z. Khan, J. Altmann, M.N. Njahira, and N. Rubenstein Concentrations of four fecal steroids in wild baboons: short-term storage conditions and consequences for data interpretation General and Comparative Endocrinology 132 2003 264 271
46. P.P. Marra, K.T. Lampe, and B.L. Tedford Plasma corticosterone levels in two species of Zonotrichia sparrows under captive and free-living conditions Wilson Bulletin 107 1995 296 305
47. T. Mathies, T.A. Felix, and V.A. Lance Effects of trapping and subsequent short-term confinement stress on plasma corticosterone in the brown treesnake (Boiga irregularis) on Guam General and Comparative Endocrinology 124 2001 106 114
48. B. Matkovics In vitro transformation of steroids as a substitute of microbial transformation Steroids Lipids Research 3 1972 1 7
49. S. Merl, S. Scherzer, R. Palme, and E. Möstl Pain causes increased concentrations of glucocorticoid metabolites in horse feces Journal of Equine Veterinary Science 20 2000 586 590
50. M.W. Miller, N.T. Hobbs, and M.C. Sousa Detecting stress responses in Rocky Mountain bighorn sheep (Ovis canadensis canadensis): reliability of cortisol concentrations in urine and feces Canadian Journal of Zoology 69 1991 15 24
51. J.J. Millspaugh, R.J. Woods, K.E. Hunt, K.J. Raedeke, G.C. Brundige, B.E. Washburn, and S.K. Wasser Using fecal glucocorticoid assays to study the physiological stress response of elk Wildlife Society Bulletin 29 2001 899 907
52. J.J. Millspaugh, B.E. Washburn, M.A. Milanick, J. Beringer, L.P. Hansen, and T.M. Meyer Noninvasive techniques for stress assessment in white-tailed deer Wildlife Society Bulletin 30 2002 899 907
53. J.J. Millspaugh, B.E. Washburn, M.A. Milanick, R. Slotow, and G. van Dyk Effects of heat and chemical treatments on fecal glucocorticoid measurements: implications for sample transport Wildlife Society Bulletin 31 2003 399 406
54. J.J. Millspaugh, and B.E. Washburn Within-sample variation of fecal glucocorticoid measurements General and Comparative Endocrinology 132 2003 21 26
55. G.P. Moberg Biological response to stress: implication for animal welfare G.P. Moberg J.A. Mench The Biology of Animal Stress 2000 CABI Publishing, New York New York, USA 1 21
56. S.L. Monfort, C.S. Schwartz, and S.K. Wasser Monitoring reproduction in captive moose using urinary and fecal steroid metabolites Journal of Wildlife Management 57 1993 400 407
57. I.T. Moore, M.J. Greene, and R.T. Mason Environmental and seasonal adaptations of the adrenocortical and gonadal responses to capture stress in two populations of the male garter snake, Thamnophis sirtalis Journal of Experimental Zoology 289 2001 99 108
58. C.J. Morrow, E.S. Kolver, G.A. Verkerk, and L.R. Matthews Fecal glucocorticoid metabolites as a measure of adrenal activity in dairy cattle General and Comparative Endocrinology 126 2002 229 241
59. E. Möstl, S. Messmann, E. Bagu, C. Robia, and R. Palme Measurement of glucocorticoid metabolite concentrations in faeces of domestic livestock Journal of Veterinary Medicine A 46 1999 621 631
60. A. Munck, P.M. Guyre, and N.J. Holbrook Physiological functions of glucocorticoids in stress and their relation to pharmacological actions Endocrine Reviews 5 1984 25 44
61. E. Möstl, J.L. Maggs, G. Schrotter, U. Besenfelder, and R. Palme Measurement of cortisol metabolites in faeces of ruminants Veterinary Research Communications 26 2002 127 139
62. E. Möstl, and R. Palme Hormones as indicators of stress Domestic Animal Endocrinology 23 2002 67 74 (Special Issue)
63. R. Palme, C. Robia, W. Baumgartner, and E. Möstl Transport stress in cattle as reflected by an increase in faecal cortisol metabolite concentrations Veterinary Record 146 2000 108 109
64. R. Palme, and E. Möstl Measurement of cortisol metabolites in faeces of sheep as a parameter of cortisol concentration in blood International Journal of Mammalian Biology 62 1997 192 197 (Suppl. 2)
65. T. Piersma, and M. Ramenofsky Long-term decreases of corticosterone in captive migrant shorebirds that maintain seasonal mass and moult cycles Journal of Avian Biology 29 1998 97 104
66. J.L.F. Raminelli, M.B.C. de Sousa, M.S. Cunha, and M.F.V. Barbosa Morning and afternoon patters of fecal cortisol excretion among reproductive and non-reproductive male and female common marmosets, Callithrix jacchus Biological Rhythm Research 32 2001 159 167
67. J. Rushen Some issues in the interpretation of behavioural responses to stress G.P. Moberg J.A. Mench The Biology of Animal Stress 2000 CABI Publishing, New York New York, USA 23 42
68. L.M. Romero Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates General and Comparative Endocrinology 128 2002 1 24
69. L.M. Romero Physiological stress in ecology: lessons from biomedical research Trends in Ecology and Evolution 19 2004 249 255
70. L.M. Romero, M. Ramenofsky, and J.C. Wingfield Season and migration alters the corticosterone response to capture and handling in an arctic migrant, the white-crowned sparrow (Zonotrichia leucophrys gambelli) Comparative Biochemistry and Physiology C 116 1997 171 177
71. L.M. Romero, and L. Remage-Healey Daily and seasonal variation in response to stress in captive starlings (Sturnus vulgaris): corticosterone General and Comparative Endocrinology 119 2000 52 59
72. L.M. Romero, K.K. Soma, and J.C. Wingfield Changes in pituitary and adrenal sensitivities allow the snow bunting (Plectrophenax nivalis), an arctic-breeding song bird, to modulate corticosterone release seasonally Journal of Comparative Physiology B 168 1998 353 358
73. L.M. Romero, K.K. Soma, and J.C. Wingfield Hypothalamic-pituitary-adrenal axis changes allow seasonal modulation of corticosterone in a bird American Journal of Physiology 274 1998 R1338 R1344
74. L.M. Romero, K.K. Soma, and J.C. Wingfield The hypothalamus and adrenal regulate modulation of corticosterone release in redpolls (Carduelis flammea, an arctic-breeding song bird) General and Comparative Endocrinology 109 1998 347 355
75. L.M. Romero, and J.C. Wingfield Seasonal changes in adrenal sensitivity alter corticosterone levels in Gambel's white-crowned sparrows (Zonotrichia leucophrys gambelii) Comparative Biochemistry and Physiology C 119 1998 31 36
76. L.M. Romero, and J.C Wingfield Alterations in hypothalamic†"pituitary-adrenal function associated with captivity in Gambel's white-crowned sparrows (Zonotrichia leucophrys gambelii) Comparative Biochemistry and Physiology B 122 1999 13 20
77. R.M. Sapolsky, L.M. Romero, and A.U. Munck How do glucocorticoids influence stress-responses? Integrating permissive, suppressive, stimulatory, and adaptive actions Endocrine Reviews 21 2000 55 89
78. G.T. Smith, J.C. Wingfield, and R.R. Veit Adrenocortical response to stress in the common diving petrel, Pelecanoides urinatrix Physiological Zoology 67 1994 526 537
79. K.M. Suedkamp Wells, B.E. Washburn, J.J. Millspaugh, M.R. Ryan, and M. Hubbard Effects of radiotransmitters on fecal glucocorticoid levels in captive dickcissels Condor 105 2003 805 810
80. D.J. Tempel, and R.J. Gutiérrez Fecal corticosterone levels in California Spotted Owls exposed to low-intensity chainsaw sound Wildlife Society Bulletin 31 2003 698 702
81. D.J. Tempel, and R.J. Gutiérrez Factors related to fecal corticosterone levels in California Spotted Owls: implications for assessing chronic stress Conservation Biology 18 2004 538 547
82. K.A. Terio, J.L. Brown, R. Moreland, and L. Munson Comparison of different drying and storage methods on quantifiable concentrations of fecal steroids in the Cheetah Zoo Biology 21 2002 215 222
83. A. Teskey-Gerstl, E. Bamberg, T. Steineck, and R. Palme Excretion of corticosteroids in urine and faeces of hares Journal of Comparative Physiology B 170 2000 163 168
84. C. Touma, N. Sachser, E. Möstl, and R. Palme Effects of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice General and Comparative Endocrinology 130 2003 267 278
85. C. Touma, R. Palme, and N. Sachser Analyzing corticosterone metabolites in fecal samples of mice: a noninvasive technique to monitor stress hormones Hormones and Behavior 45 2004 10 22
86. J.W. Turner Jr., R. Nemeth, and C. Rogers Measurement of fecal glucocorticoids in parrotfishes to assess stress General and Comparative Endocrinology 133 2003 341 352
87. C.G. von der Ohe, and C. Servheen Measuring stress in mammals using fecal glucocorticoids: opportunities and challenges Wildlife Society Bulletin 30 2002 1215 1225
88. B.E. Washburn, and J.J. Millspaugh Effects of simulated environmental conditions on glucocorticoid metabolite measurements in white-tailed deer feces General and Comparative Endocrinology 127 2002 217 222
89. B.E. Washburn, D.L. Morris, J.J. Millspaugh, J. Faaborg, and J.H. Schulz Using a commercially available radioimmunoassay to quantify corticosterone in avian plasma Condor 104 2002 558 563
90. B.E. Washburn, J.J. Millspaugh, J.H. Schulz, S.B. Jones, and T.W. Mong Using fecal glucocorticoids for stress assessment in mourning doves Condor 105 2003 696 706
91. B.E. Washburn, D.J. Tempel, J.J. Millspaugh, R.J. Gutiérrez, and M.E. Seamans Factors related to fecal estrogens and fecal testosterone in California spotted owls Condor 106 2004 567 579
92. S.K. Wasser, R. Thomas, P.P. Lair, C. Guidry, J. Southers, J. Lucas, D.E. Wildt, and S.L. Monfort Effects of dietary fibre on faecal steroid measurements in baboons (Papio cynocephalus cynocephalus) Journal of Reproduction and Fertility 97 1993 569 574
93. S.K. Wasser, S. Papageorge, C. Foley, and J.L. Brown Excretory fate of estradiol and progesterone in the African elephant (Loxodonta africana) and patterns of fecal steroid concentrations throughout the estrous cycle General and Comparative Endocrinology 102 1996 255 262
94. S. Wasser, K. Bevis, G. King, and E. Hanson Non-invasive physiological measures of disturbance in the northern spotted owl Conservation Biology 11 1997 1019 1022
95. S.K. Wasser, K.E. Hunt, J.L. Brown, K. Cooper, C.M. Crockett, U. Bechert, J.J. Millspaugh, S. Larson, and S.L. Monfort A generalized fecal glucocorticoid assay for use in a diverse array of non-domestic mammalian and avian species General and Comparative Endocrinology 120 2000 260 275
96. P.L. Whitten, D.K. Brockman, and R.C. Stavisky Recent advances in noninvasive techniques to monitor hormone-behavior interactions Yearbook of Physical Anthropology 41 1998 1 23
97. J.M. Whittier, F. Corrie, and C. Limpus Plasma steroid profiles in nesting loggerhead turtles (Caretta caretta) in Queensland, Australia: relationship to nesting episode and season General and Comparative Endocrinology 106 1997 39 47
98. E.P. Widmaier, T.L. Harmer, A.M. Sulak, and T.H. Kunz Further characterization of the pituitary-adrenocortical responses to stress in chiroptera The Journal of Experimental Zoology 269 1994 442 449
99. N.C. Wielebnowski, N. Fletchall, K. Carlstead, J.M. Busso, and J.L. Brown Noninvasive assessment of adrenal activity associated with husbandry and behavioral factors in the North American clouded leopard population Zoo Biology 21 2002 77 98
100. R.J. Windle, S.A. Wood, S.L. Lightman, and C.D. Ingram The pulsatile characteristics of hypothalamo-pituitary-adrenal activity in female Lewis and Fischer 344 rats and its relationship to differential stress responses Endocrinology 139 1998 4044 4052
101. J.C. Wingfield, J.P. Smith, and D.S. Farner Endocrine responses of white-crowned sparrows to environmental stress Condor 84 1982 399 409
102. Wingfield, J.C., 1994. Modulation of the adrenocortical response to stress in birds. in: K.G. Davey, R.E. Peter, S.S. Tobe, (Eds.), Perspectives in Comparative Endocrinology National Research Council of Canada, Ottawa, Canada, pp. 520-528
103. J.C. Wingfield, R. Suydam, and K. Hunt The adrenocortical responses in snow buntings (Plectrophenax nivalis) and Lapland longspurs (Calcarius lapponicus) at Barrow, Alaska Comparative Biochemistry and Physiology B 108 1994 299 306
104. G.F. Woods Chemical and microbiological transformation of steroids E.H.D. Cameron S.G. Hillier K. Griffiths Steroid Immunoassay 1975 Alpha Omega Cardiff 5 10