Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-10T09:34:15.429Z Has data issue: false hasContentIssue false
  • English
  • Français

Can non-invasive glucocorticoid measures be used as reliable indicators of stress in animals?

Published online by Cambridge University Press:  11 January 2023

J Lane
J Lane*
Affiliation:
Animal Welfare Team, Central Science Laboratory, Sand Hutton, York YO41 1LZ, UK
*
email: j.lane@csl.gov.uk
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Refinement techniques are being increasingly employed in all fields of animal research to try to ensure that the highest standards of welfare are upheld. This review concerns one of the main emerging techniques for the assessment of welfare itself, namely the non-invasive measurement of glucocorticoids (GCs) as indicators of stress. The paper is divided into three sections. The first discusses the relationship between GCs and stress. The second section considers whether factors other than stress are linked to rises in GCs, eg exercise, oestrus cycle and diet. The final part examines the reliability of the non-invasive techniques that measure GCs from samples of saliva and faeces. Although it is important to take into account some caveats associated with the methodologies employed, it is concluded, nevertheless, that these techniques can give accurate and reliable information regarding the welfare status of an individual or group of animals without the procedures themselves causing any kind of distress to the subjects.

Keywords

animal welfarecortisolfaecesnon-invasiverefinementstress
Type
Research Article
Information
Animal Welfare , Volume 15 , Issue 4 , November 2006 , pp. 331 - 342
Copyright
© 2006 Universities Federation for Animal Welfare

References

Aardal, E and Holm, A 1995 Cortisol in saliva — reference ranges and relation to cortisol in serum. European Journal of Clinicians 33: 927–932Google ScholarPubMed
Abbott, DH, Keverne, EB, Bercovitch, FB, Shively, CA, Medoza, SP, Saltzman, W, Snowdon, CT, Ziegler, TE, Banjevic, M, Garland, T and Sapolsky, RM 2003 Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Hormones and Behavior 43: 67–82CrossRefGoogle ScholarPubMed
Anderson, DA, Shapiro, JR, Lundgren, JD, Spataro, LE and Frye, CA 2002 Self-reported dietary restraint is associated with elevated levels of salivary cortisol. Appetite 38: 13–17CrossRefGoogle ScholarPubMed
Anderson, DE, Silveira, F and Grubb, T 1999 Effects of venipuncture and correlation of plasma, serum and saliva cortisol concentration with transportation stress in Camelids. Journal of Camel Practice and Research 6: 249–254Google Scholar
Armitage, KB 1991 Factors affecting corticosteroid concentrations in yellow-bellied marmots. Comparative Biochemistry and Physiology 98: 47–54CrossRefGoogle ScholarPubMed
Arthington, JD, Corah, LR, Minton, JE, Elsasser, TH and Blecha, F 1997 Supplemental dietary chromium does not influence ACTH, cortisol, or immune responses in young calves inoculated with bovine herpesvirus–1. Journal of Animal Science 75: 217–223CrossRefGoogle ScholarPubMed
Bakke, M, Tuxen, A, Thomen, CE, Barbow, A, Alkjaer, T and Jensen, BR 2004 Salivary cortisol level, salivary flow rate, and masticatory muscle activity in response to acute mental stress: a comparison between aged and young women. Gerontology 5(6): 383–392CrossRefGoogle Scholar
Beck, SG, List, TJ and Choi, KC 1994 Long-term and short-term administration of corticosterone alters CA1 hippocampal neuronal properties. Neuroendocrinology 60(3): 261–272CrossRefGoogle Scholar
Becker, BA, Nienaber, JA, DeShazer, JA and Hahn, GL 1985 Effect of transportation on cortisol concentrations and on circadian rhythm of cortisol in gilts. American Journal of Veterinary Research 46(7): 1457–1459Google ScholarPubMed
Beehner, JC and Whitten, PL 2004 Modifications of a field method of fecal steroid analysis in baboons. Physiology & Behavior 82: 269–277CrossRefGoogle ScholarPubMed
Bercovitch, FB and Clarke, AS 1995 Dominance rank, cortisol concentrations, and reproductive maturation in male rhesus macaques. Physiology & Behavior 58(2): 215–221CrossRefGoogle ScholarPubMed
Bercovitch, FB and Ziegler, TE 2002 Current topics in primate socioendocrinology. Annual Review of Anthropology 31: 45–67CrossRefGoogle Scholar
Bergman, TJ, Beehner, JC, Cheney, DL, Seyfarth, RM and Whitten, PL 2005 Correlates of stress in free-ranging male chacma baboons (Papio hamadryas ursinus) Animal Behaviour 70: 703–713CrossRefGoogle Scholar
Berk, LS, Tan, SA, Nehlsen-Cannarella, SL, Napier, BJ, Lewis, JE, Lee, JW, Eby, WC and Fry, WF 1988 Humor associated laughter decreases cortisol and increases spontaneous lymphocyte blastogenesis. Clinical Research 36(3): A435-A435Google Scholar
Blanchard, RJ, Nikulina, JN, Sakia, RR, McKittrick, C, McEwen, B and Blanchard, DC 1998 Behavioral and endocrine change following chronic predatory stress. Physiology & Behavior 15: 561–569CrossRefGoogle Scholar
Boinski, S, Swing, SP, Gross, TS and Davis, JK 1999 Environmental enrichment of brown capuchins (Cebus apella): behavioral and plasma and fecal cortisol measures of effectiveness. American Journal of Primatology 48: 49–683.0.CO;2-6>CrossRefGoogle ScholarPubMed
Borg, KE, Esbenshade, KL and Johnson, BH 1991 Cortisol, growth hormone and testosterone concentrations during mating behaviour in the bull and boar. Journal of Animal Science 69: 3230–3240CrossRefGoogle ScholarPubMed
Broom, DM and Johnson, KG 2001 Stress and Animal Welfare. Chapman & Hall: Oxford, UKGoogle Scholar
Cavigelli, SA, Dubovick, T, Levash, W, Jolly, A and Pitts, A 2003 Female dominance status and fecal corticoids in a cooperative breeder with low reproductive skew: ringtailed lemurs (Lemur catta). Hormones & Behavior 43(1): 166–179CrossRefGoogle Scholar
Cavigelli, SA, Monfort, SL, Whitney, TK, Mechref, YS, Novotny, M and McClintock, MK 2005 Frequent serial fecal corticoid measures from rats reflect circadian and ovarian corticosterone rhythms. Journal of Endocrinology 184: 153–163CrossRefGoogle ScholarPubMed
Clarke, FM and Faulkes, CG 1998 Hormonal and behavioural correlates of male dominance and reproductive status in captive colonies of the naked mole rat (Heterocephalus glaber). Proceedings of the Royal Society B: Biological Sciences 265: 1391–1399CrossRefGoogle ScholarPubMed
Coe, CL and Levine, S 1995 Diurnal and annual variation of adrenocortical activity in the squirrel monkey. American Journal of Primatology 35: 283–292CrossRefGoogle ScholarPubMed
Coe, CL, Murai, JT, Wiener, SG, Levine, S and Siiteri, PK 1986 Rapid cortisol and corticosteroid-binding globulin responses during pregnancy and after estrogen administration in the squirrel-monkey. Endocrinology 118: 435–440CrossRefGoogle ScholarPubMed
Colborn, DR, Thompson, DL, Roth, TL, Capehart, JS and White, KL 1991 Responses of cortisol and prolactin to sexual excitement and stress in stallions and geldings. Journal of Animal Science 69: 2556–2562CrossRefGoogle ScholarPubMed
Cook, NK, Schaefer, AL, Lepage, P and Morgan Jones, SD 1997 Radioimmunoassay for cortisol in pig saliva and serum. Journal Agricultural Food Chemistry 45: 395–399CrossRefGoogle Scholar
Cooper, TR, Trunkfield, HR, Zanella, AJ and Booth, WD 1989 An enzyme-linked immunosorbent assay for cortisol in the saliva of man domestic farm animals. Journal of Endocrinology 123: R13–R16CrossRefGoogle ScholarPubMed
Cooperman, MD, Reed, JM and Romero, LM 2004 The effects of terrestrial and breeding densities on corticosterone and testosterone levels in spotted salamanders (Ambystoma maculatum). Canadian Journal of Zoology 82: 1794–1803CrossRefGoogle Scholar
Correa, SA, Fernandes, MO, Iseki, KK and Negrao, JA 2003 Effect of the establishment of dominance relationships on cortisol and other metabolic parameters in Nile tilapia (Oreochromis niloticus). Brazilian Journal of Medical and Biological Research 36: 1725–1731CrossRefGoogle ScholarPubMed
Creel, S 2001 Social dominance and stress hormones. Trends in Ecology & Evolution 16: 491–497CrossRefGoogle Scholar
de Kloet, ER 2003 Hormones, brain and stress. Endocrinological Regulation 37: 51–68Google ScholarPubMed
Del Corral, P, Sampedro, R, Hartsell, M, Howley, ET, Younger, MS, Ashraf, M, Eiler, H, Law, B Jr and Thompson, DL 1999 Reduced cortisol potentiates the exercise-induced increase in corticotropin to a greater extent in trained compared with untrained men. Metabolism 48(3): 390–394CrossRefGoogle ScholarPubMed
Dloniak, SM, French, JA, Place, NJ, Weldele, ML, Glickman, SE and Holekamp, KE 2004 Non-invasive monitoring of fecal androgens in spotted hyenas (Crocuta crocuta). General and Comparative Endocrinology 135: 51–61CrossRefGoogle ScholarPubMed
Dorn, LD and Susman, EJ 1993 Serum and salivary cortisol relations in adolescents during pregnancy and the early post-partum period. Biological Psychiatry 34: 226–233CrossRefGoogle Scholar
Duclos, M, Corcuff, JB and Rashedi, M 1997 Trained versus untrained men. Different immediate post-exercise response of the pituitary adrenal axis — preliminary study. European Journal of Applied Physiology 75(4): 343–350CrossRefGoogle ScholarPubMed
Ekkel, ED, Dieleman, SJ, Schouten, WGP, Portela, A, Cornelissen, G, Tielen, MJM and Halberg, F 1996 The circadian rhythm of cortisol in the saliva of young pigs. Physiology & Behavior 60(3): 985–989CrossRefGoogle ScholarPubMed
Erickson, K and Drevets, W 2003 Glucocorticoid regulation of diverse cognitive functions and pathological emotional states. Neuroscience and Biobehavioural Review 27: 233–246CrossRefGoogle ScholarPubMed
Esch, T and Stefano, GB 2004 The neurobiology of pleasure, reward processes, addiction and their health implications. Neuroendocrinology Letters 25: 235–241Google ScholarPubMed
Exton, MS, Bindert, A, Kruger, T, Scheller, F, Hartmann, U and Schedlowski, M 1999 Cardiovascular and endocrine alterations after masturbation-induced orgasm in women. Psychosomatic Medicine 61: 280–289CrossRefGoogle ScholarPubMed
Few, JD 1974 Effect of exercise on secretion and metabolism of cortisol. Journal of Endocrinology 62: 341–353CrossRefGoogle Scholar
Fulkerson, WJ and Tang, BY 1979 Ultradian and circadian rhythms in the plasma concentration of cortisol in sheep. Journal of Endocrinology 81: 135–141CrossRefGoogle ScholarPubMed
Goymann, W 2005 Non-invasive monitoring in bird droppings: physiological validation, sampling, extraction and sex differences and the influence of diet on hormone metabolite levels. Annals of the New York Academy of Sciences 1046: 35–53CrossRefGoogle Scholar
Graham, LH and Brown, JL 1997 Non-invasive assessment of gonadal and adrenocortical function in felid species via fecal steroid analysis. International Journal of Mammalian Biology 62: 78–82Google Scholar
Gregory, NG 2004 Physiology and Behaviour of Animal Suffering. Blackwell Science: Oxford, UKCrossRefGoogle Scholar
Guechot, J, Fiet, J, Passa, P, Villette, JM, Gourmel, B, Tabuteau, F, Cathelineau, G and Dreux, C 1982 Physiological and pathophysiological variations in saliva cortisol. Hormone Research 61: 357–364CrossRefGoogle Scholar
Gusset, M 2005 Faecal glucocorticoid level is not correlated with stereotypic pacing in two captive margays. Animal Welfare 14: 157–159CrossRefGoogle Scholar
Hainer, V, Kunesova, M, Stunkard, AJ, Parikova, J, Stich, V, Mikulova, R and Starka, L 2001 The within-pair resemblance in serum levels of androgens, sex-hormone binding globulin and cortisol in female obese identical twins — effect of negative energy balance induced by very low-calorie diet. Hormone and Metabolic Research 33: 417–422CrossRefGoogle ScholarPubMed
Hawkes, CH 1992 Endorphins — the basis of pleasure. Journal of Neurology, Neurosurgery and Psychiatry 55: 247–250CrossRefGoogle ScholarPubMed
Hennessy, MB, Williams, MT, Miller, DD, Douglas, CW and Voith, VL 1998 Influence of male and female petters on plasma cortisol and behaviour: can human interaction reduce the stress of dogs in a public animal shelter? Applied Animal Behaviour Science 61: 63–77CrossRefGoogle Scholar
Hodges, JK 1998 Endocrinology of the ovarian cycle and pregnancy in the Asian (Elephas maximus) and African (Loxodonta africana) elephant. Animal Reproduction Science 53(1-4): 3–18CrossRefGoogle ScholarPubMed
Howland, BE, Sanford, LM and Palmer, WM 1985 Changes in serum levels of LH, FSH, prolactin, testosterone and cortisol associated with season and mating in male pygmy goats. Journal of Andrology 6: 89–96CrossRefGoogle ScholarPubMed
Huber, S, Palme, R and Arnold, W 2003 Effects of season, sex and sample collection on the concentrations of fecal cortisol metabolites in red deer (Cervus elaphus). General and Comparative Endocrinology 130(1): 48–54CrossRefGoogle ScholarPubMed
Hunt, K and Wasser, SK 2003 Effect of long term preservation methods on fecal glucocorticoid concentrations of grizzly bear and African elephant. Physiological and Biochemical Zoology 76: 918–928CrossRefGoogle ScholarPubMed
Jacks, DE, Sowash, J, Anning, J, McGloughlin, T and Andres, F 2002 Effect of exercise at three exercise intensities on salivary cortisol. Journal of Strength and Conditioning Research 16(2): 286–289Google ScholarPubMed
Jurimae, J, Maestu, J, Purge, P and Jurimae, T 2004 Changes in stress and recovery after heavy training in rowers. Journal of Science and Medicine in Sport 7: 335–339CrossRefGoogle ScholarPubMed
Khan, MZ, Altmann, J, Isani, SS and Yu, J 2002 A matter of time: evaluating the storage of fecal samples for steroid analysis. General and Comparative Endocrinology 128: 57–64CrossRefGoogle ScholarPubMed
Kirschbaum, C, Kudielka, BM, Gaab, J, Schommer, NC and Hellhammer, DH 1999 Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus-pituitary-adrenal axis. Psychosomatic Medicine 61: 154–162CrossRefGoogle ScholarPubMed
Kirschbaum, C, Wust, S and Hellhammer, D 1992 Consistent sex-differences in cortisol responses to psychological stress. Psychosomatic Medicine 54: 648–657CrossRefGoogle ScholarPubMed
Kitay, JI 1963 Pituitary-adrenal function in male and female rats. Endocrinology 72: 947–954CrossRefGoogle ScholarPubMed
Klein, SL 2000 Hormones and mating system affect sex and species differences in immune function among vertebrates. Behavioural Processes 51(1-3): 149–166CrossRefGoogle ScholarPubMed
Klein, LC, Jamner, LD, Alberts, J, Orenstein, MD, Levine, L and Leigh, H 2000 Sex differences in salivary cortisol levels following naltrexone administration. Journal of Applied Biobehavioral Research 5: 144–153CrossRefGoogle Scholar
Kraemer, RR, Blair, S, Kraemer, GR and Castracane, VD 1989 Effects of treadmill running on plasma β-endorphin, corti-cotropin, and cortisol levels in male and female 10k runners. European Journal of Applied Physiology and Occupational Physiology 58: 845–851CrossRefGoogle ScholarPubMed
Lance, VA, Grumbles, JS and Rostal, DC 2001 Sex differences in plasma corticosterone in desert tortoises (Gopherus agassizii) during the reproductive cycle. Journal of Experimental Zoology 289: 285–2893.0.CO;2-B>CrossRefGoogle ScholarPubMed
Lanctot, RB, Hatch, SA, Gill, VA and Eens, M 2003 Are cor-ticosterone levels a good indicator of food availability and reproductive performance in a kittiwake colony? Hormones and Behavior 43: 489–502CrossRefGoogle Scholar
Laugero, KD and Moberg, GP 2000 Energetic response to repeated restraint stress in rapidly growing mice. American Journal of Physiology — Endocrinology and Metabolism 279: E33–E43CrossRefGoogle ScholarPubMed
Leonardi, M, Sandino, AM and Klempau, A 2003 Effect of a nucleotide-enriched diet on the immune system, plasma cortisol levels and resistance to infectious pancreatic necrosis (IPN) in juvenile rainbow trout (Oncorhynchus mykiss). Bulletin of the European Association of Fish Pathologists 23: 52–59Google Scholar
Le Roux, CW, Sivakumaran, S, Alaghband-Zadeh, J, Dhillo, W, Kong, WM and Wheeler, MJ 2002 Free cortisol index as a surrogate marker for serum free cortisol. Annals of Clinical Biochemistry 39: 406–408CrossRefGoogle ScholarPubMed
Levis, DG, Barnett, JL, Hemsworth, H and Jongman, E 1995 The effect of breeding facility and sexual stimulation on plasma cortisol in boars. Journal of Animal Science 73: 3705–3711CrossRefGoogle ScholarPubMed
Lewis, JG, Lewis, MG and Elder, PA 2003 An enzyme-linked immunosorbent assay for corticosteroid-binding globulin using monoclonal and polyclonal antibodies: decline in CBG following synthetic ACTH. Clinical Chemica Acta 328: 121–128CrossRefGoogle Scholar
Lochmann, RT, Davis, KB and Simco, BA 2002 Cortisol response of golden shiners (Notemigonus crysoleucas) fed diets differing in lipid content. Fish Physiology and Biochemistry 27: 29–34CrossRefGoogle Scholar
Luby, JL, Mrakotsky, C, Heffelfinger, A, Brown, K and Spitznagel, E 2004 Characteristics of depressed pre-schoolers with and without anhedonia: evidence for a melancholic depressive subtype in young children. American Journal of Psychiatry 161(11): 1998–2004CrossRefGoogle Scholar
Lynch, JW, Khan, MZ, Altmann, J, Njahira, MN and Rubenstrein, N 2003 Concentrations of four fecal steroids in wild baboons: short-term storage conditions and consequences for data interpretation. General and Comparative Endocrinology 132(2): 264–271CrossRefGoogle Scholar
Maestu, J, Jurimae, J and Jurimae, T 2003 Psychological and biomechanical markers of heavy resistance training stress in highly trained male rowers. Medicina Dello Sport 56: 95–101Google Scholar
Mashburn, KL and Atkinson, S 2004 Evaluation of adrenal function in serum and feces of Steller sea lions (Eumetopias juba-tus): influences of molt, gender, sample storage, and age on glu-cocorticoid metabolism. General and Comparative Endocrinology 136: 371–381CrossRefGoogle Scholar
McCarthy, DA, Macdonald, I, Grant, M, Marbut, M, Watling, M, Nicholson, S, Deeks, JJ, Wade, AJ and Perry, JD 1992 Studies on the immediate and delayed leucocytosis elicited by brief (30 min) strenuous exercise. European Journal of Applied Physiology 64(6): 513–517CrossRefGoogle ScholarPubMed
McCracken, JT and Poland, RE 1989 Saliva and serum cortisol dynamics flowing intravenous dexamethasone in normal volunteers. Life Sciences 45: 1781–1785CrossRefGoogle Scholar
McEwen, BS and Wingfield, JC 2003 The concept of allostasis in biology and biomedicine. Hormones and Behaviour 43: 2–15CrossRefGoogle ScholarPubMed
McLean, M and Smith, R 1999 Corticotropin-releasing hormone in human pregnancy and parturition. Trends in Endocrinology and Metabolism 10: 174–178CrossRefGoogle ScholarPubMed
Medler, KF and Lance, VA 1998 Sex differences in plasma cor-ticosterone levels in alligator (Alligator mississippiensis) embryos. Journal of Experimental Zoology 280: 238–2443.0.CO;2-O>CrossRefGoogle Scholar
Messina, G, Lissoni, R, Bartolacelli, E, Tancini, G, Villa, S, Gardani, GS and Brivio, F 2003 A psychoncological study of lymphocyte subpopulations in relation to pleasure-related neuro-biochemistry and sexual and spiritual profile to Rorschach's test in early or advanced cancer patients. Journal of Biological Regulators and Homeostatic Agents 17: 322–326Google ScholarPubMed
Meyer, JM, Walker, SL, Freeman, EW, Steinetz, BG and Brown, JL 2004 Species and fetal gender effects on the endocrinology of pregnancy in elephants. General and Comparative Endocrinology 138(3): 263–270CrossRefGoogle ScholarPubMed
Millspaugh, JJ and Washburn, BE 2004 Use of fecal glucocor-ticoid metabolite in conservation biology research: considerations for application and interpretation. General and Comparative Endocrinology 138(3): 189–199CrossRefGoogle Scholar
Mohle, U, Heistermann, M, Palme, R and Hodges, JK 2002 Characterization of urinary and fecal metabolites of testosterone and their measurement for assessing gonadal endocrine function in male non-human primates. General and Comparative Endocrinology 129(3): 135–145CrossRefGoogle Scholar
Monnazzi, P, Leri, O, Guizzardi, L, Matiioli, D and Patacchioli, FR 2002 Anti-stress effect of yoga-type breathing: modification of salivary cortisol, heart rate and blood pressure following a step-climbing exercise. Stress and Health 18: 195–200CrossRefGoogle Scholar
Morgan Jones, SD 1996 Salivary vs serum cortisol for the assessment of adrenal activity in swine. Canadian Journal of Animal Science 76: 329–335Google Scholar
Morrow, CJ, Kolver, ES, Verkerk, GA and Matthews, LR 2002 Fecal glucocorticoid metabolites as a measure of adrenal activity in dairy cattle. General and Comparative Endocrinology 126: 229–241CrossRefGoogle ScholarPubMed
Mostl, ES, Rettenbacher, C and Palme, C 2005 Measurement of corticosterone metabolites in birds' droppings: an analytical approach. Annals of the New York Academy of Sciences 1046: 17–34CrossRefGoogle ScholarPubMed
Muller, MN and Wrangham, RW 2004 Dominance, cortisol and stress in wild chimpanzees (Pan troglodytes schweinfurthii). Behavioral Ecology and Sociobiology 55: 332–340CrossRefGoogle Scholar
Munck, A, Guyre, PM and Holbrook, NJ 1984 Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocrine Reviews 5: 25–44CrossRefGoogle ScholarPubMed
O'Reilly, KM and Wingfield, JC 2003 Seasonal age and sex differences in weight, fat reserves and plasma corticosterone in western sandpipers. Condor 105: 13–26CrossRefGoogle Scholar
Orihuela, A, Sanchez-Mejorada, H and Toledo, M 2002 Effect of short transport during di-oestrus and pro-oestrus on cortisol levels and oestrus behavior of sheep. Journal of Agricultural Science 38: 93–96CrossRefGoogle Scholar
Osadchuk, LV 1996 The role of steroid hormones in sexual and agonistic behavior in silver fox males. Zhurnal Vysshei Nervnoi Deyatelnosti Imeni Palova 46: 78–83Google Scholar
Ott, JA, Mendoca, MT, Guyer, C and Michener, WK 2000 Seasonal changes in sex and adrenal steroid hormones of gopher tortoises (Gopherus polyphemus). General and Comparative Endocrinology 117: 299–312CrossRefGoogle ScholarPubMed
Owen, D and Lane, J 2006 High levels of corticosterone in feather-plucking parrots (Psittacus erithacus). Veterinary Record 158: 804–805CrossRefGoogle ScholarPubMed
Palme, R 2005 Measuring fecal steroids: guidelines for the practical application. Annals of the New York Academy of Sciences 1046: 75–80CrossRefGoogle ScholarPubMed
Palme, R, Rettenbacher, C and Tourna, C 2005 Stress hormones in mammals and birds: comparative aspects regarding metabolism, excretion and non-invasive measurement in fecal samples. Annals of the New York Academy of Sciences 1040: 162–171CrossRefGoogle Scholar
Polsky, RH 1994 Electronic shock collars — are they worth the risks? Journal of American Animal Hospital Association 30: 463–468Google Scholar
Rabb, MH, Thompson, DL, Barry, BE, Colborn, DR, Garza, F and Hehnke, KE 1989 Effects of sexual stimulation, with and without ejaculation, on serum concentrations of LH, FSH, testosterone, cortisol and prolactin in stallions. Journal of Animal Science 67: 2724–2729CrossRefGoogle ScholarPubMed
Ratamess, NA, Kraemer, WJ, Volek, JS, Maresh, CM, Van Heest, JL, Sharman, MJ, Rubin, MR, French, DN, Vescovi, JD, Silvestre, R, Hatfield, DL, Fleck, J and Deschenes, MR 2005 Androgen receptor content following heavy resistance in men. Journal of Steroid Biochemistry and Molecular Biology 93: 35–42CrossRefGoogle ScholarPubMed
Raven, PW and Taylor, NF 1996 Sex differences in human metabolism of cortisol. Endocrine Research 22: 751–755CrossRefGoogle ScholarPubMed
Rettenbacher, S, Mostl, E, Hackl, R, Ghareed, K and Palme, R 2004 Measurement of corticosterone metabolites in chicken droppings. British Poultry Science 45: 704–711CrossRefGoogle Scholar
Riad-Fahmy, D, Read, GF, Walker, RF and Griffiths, K 1982 Steroids in saliva for assessing endocrine functions. Endocrinology Review 3: 367–395CrossRefGoogle Scholar
Rivier, C and Vale, W 1984 Influence of CRF on reproductive functions in the rat. Endocrinology 114: 914–921CrossRefGoogle ScholarPubMed
Rivier, C, Rivier, J and Vale, W 1986 Stress-induced inhibition of reproductive functions: role of endogenous CRF. Science 231: 607–610CrossRefGoogle Scholar
Romero, LM 2000 Effects of weather on corticosterone responses in wild free-living passerine birds. General and Comparative Endocrinology 118: 113–122CrossRefGoogle ScholarPubMed
Romero, LM 2002 Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. General and Comparative Endocrinology 128: 1–24CrossRefGoogle ScholarPubMed
Romero, LM 2004 Physiological stress in ecology: lessons from biomedical research. Trends in Ecology & Evolution 19: 249–255CrossRefGoogle ScholarPubMed
Ruis, MAW, Brake, JHAT, Engel, B, Ekkel, ED, Bust, WG, Blokhuis, HJ and Koolhaas, JM 1997 The circadian rhythm of salivary cortisol in growing pigs: effects of age, gender, and stress. Physiology & Behavior 62(3): 623–630CrossRefGoogle ScholarPubMed
Rushen, J, Robert, S and Farmer, C 1999 Effects of an oat-based high-fibre diet on insulin, glucose, cortisol and free fatty acid concentrations in gilts. Animal Science 69: 395–401CrossRefGoogle Scholar
Sahin, K, Cerci, IH, Guler, T, Sahin, N and Erkal, N 1997 Effect of chromium added basal diet on serum glucose, insulin, cortisol, alkaline phosphatase and feedlot performance in rabbits. Turkish Journal of Veterinary and Animal Sciences 21: 147–152CrossRefGoogle Scholar
Sands, J and Creel, S 2004 Social dominance, aggression and faecal glucocorticoid levels in a wild population of wolves (Canis lupus) Animal Behaviour 67: 387–396CrossRefGoogle Scholar
Sanson, G, Brown, JL and Farstad, W 2005 Non-invasive fecal steroid monitoring of ovarian and adrenal activity in the farmed blue fox (Alopex lagopus) females during late pregnancy, parturition and lactation onset. Animal Reproduction Science 87: 309–319CrossRefGoogle ScholarPubMed
Sapolsky, RM 1996 Why stress is bad for your brain. Science 273(5276): 749–750CrossRefGoogle ScholarPubMed
Sapolsky, RM, Romero, LM and Munck, AU 2000 How do glu-cocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory and preparative actions. Endocrine Reviews 21: 55–89Google ScholarPubMed
Schaffner, CM and French, JA 2004 Behavioral and endocrine responses in male marmosets to the establishment of multi-male breeding groups: evidence for non-monopolizing facultative polyandry. International Journal of Primatology 25: 709–732CrossRefGoogle Scholar
Schatz, S and Palme, R 2001 Measurement of faecal cortisol metabolites in cats and dogs: a non-invasive method for evaluating adrenocortical function. Veterinary Research Communications 25(4): 271–287CrossRefGoogle ScholarPubMed
Schilder, MBH and van der Borg, JAM 2004 Training dogs with the help of the shock collar: short and long term behavioral effects. Applied Animal Behavior Science 85: 319–334CrossRefGoogle Scholar
Schiml, PA and Rissman, EF 1999 Cortisol facilitates induction of sexual behaviour in the female musk shrew (Suncus murinus). Behavioral Neuroscience 113: 166–175CrossRefGoogle ScholarPubMed
Seyle, H 1935 A syndrome produced by diverse nocuous agents. Nature 138: 32–33CrossRefGoogle Scholar
Shepherdson, DJ, Carlstead, KC and Wielebnowski, N 2004 Cross-institutional assessment of stress responses in zoo animals using longitudinal monitoring of faecal corticoids. Animal Welfare 13: S105–S115CrossRefGoogle Scholar
Sher, L 2004 Type D personality, stress and cortisol. Journal of Psychosomatic Research 57(2): 117–118CrossRefGoogle Scholar
Shinkai, S, Watanabe, S, Kurokawa, Y and Torii, J 1993 Salivary cortisol for monitoring circadian rhythm variation in adrenal activity during shiftwork. Archives of Occupational and Environmental Health 64: 499–502CrossRefGoogle ScholarPubMed
Silva, C, Ines, LS, Nour, D, Straub, RH and Da Silva, JAP 2002 Differential male and female adrenal cortical steroid hormone and cortisol responses to interleukin–6 in humans. Annals of the New York Academy of Sciences 966: 68–72CrossRefGoogle ScholarPubMed
Steadman, P 1995 Steadman's Medical Dictionary. 26th edition, Williams and Wilkins Publications: Baltimore, USA.Google Scholar
Stavisky, RC, Adams, MR, Watson, SL and Kaplan, JR 2001 Dominance, cortisol, and behavior in small groups of female cynomolgus monkeys (Macaca fascicularis). Hormones and Behavior 39(3): 232–238CrossRefGoogle ScholarPubMed
Strier, KB, Lynch, JW and Ziegler, TE 2003 Hormonal changes during the mating and conception seasons of wild northern muriquis (Brachyteles arachnoides hypoxanthus). American Journal of Primatology 61: 85–99CrossRefGoogle ScholarPubMed
Stroud, LR, Salovey, P and Epel, ES 2002 Sex differences in stress responses: social rejection versus achievement stress. Biological Psychiatry 52: 318–327CrossRefGoogle ScholarPubMed
Stupnicki, R and Obminski, Z 1992 Glucocorticoid response to exercise as measured by serum and salivary cortisol. European Journal of Applied Physiology 65: 546–549CrossRefGoogle ScholarPubMed
Talling, J, Robson, M and Lane, J 2002 Seasonal differences in behaviour and physiology of performing and exhibit macaws kept at a zoo open to the public. Advances in Ethology 37: 174Google Scholar
Tamanini, C, Giordano, N, Chiesa, F and Seren, E 1983 Plasma cortisol variations induced in the stallion by mating. Acta Endocrinologica 102: 447–450Google ScholarPubMed
Tempel, DJ and Gutierrez, RJ 2004 Factors related to fecal corticosterone levels in California spotted owls: implications for assessing chronic stress. Conservation Biology 18: 538–547CrossRefGoogle Scholar
Terio, KA, Brown JL Moreland, R and Munson, L 2002 Comparison of different drying and storage methods on quantifiable concentrations of fecal steroids in the cheetah. Zoo Biology 21: 215–222CrossRefGoogle Scholar
Teskey-Gerstl, A, Bamberg, E, Steineck, T and Palme, R 2000 Excretion of corticosteroids in urine and faeces of hares (Lepus europaeus). Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 170: 163–168CrossRefGoogle ScholarPubMed
Tilbrook, AJ, Turner, AI and Clarke, IJ 2000 Effects of stress on reproduction in non-rodent mammals: the role of glucocorti-coids and sex differences. Reviews of Reproduction 5: 105–113CrossRefGoogle Scholar
Touma, C, Sachser, N, Mostl, E and Palme, R 2003 Effects of sex and time of day on metabolism and excretion of corticos-terone in urine and feces of mice. General and Comparative Endocrinology 130: 267–278CrossRefGoogle ScholarPubMed
Touma, C, Palme, R and Sachser, N 2004 Analyzing corti-costerone metabolites in fecal samples of mice: a non-invasive technique to monitor stress hormones. Hormones and Behavior 45: 10–22CrossRefGoogle Scholar
Touma, C and Palme, R 2005 Measuring fecal glucocorticoid metabolites in mammals and birds: the importance of validation. Annals of the New York Academy of Sciences 1046: 54–74CrossRefGoogle ScholarPubMed
Tse, S 2004 Relationship between baseline cortisol, social functioning and depression: a mediation analysis. Psychiatry Research 126: 197–201CrossRefGoogle Scholar
Turner, JW, Tolson, P and Halmad, N 2002 Remote assessment of stress in white rhinoceros (Ceratotherium simum) and black rhinoceros (Diceros diceros) by measurement of adrenal steroids in feces. Journal of Zoo and Wildlife Medicine 33: 214–221Google Scholar
van Jaarsveld, AS and Skinner, JD 1992 Adrenocortical responsiveness to immobilization stress in spotted hyenas (Crocuta crocuta). Comparative Biochemical Physiology 103: 73–79CrossRefGoogle ScholarPubMed
van Lier, E, Perez-Clariget, R and Forsberg, M 2003 Sex differences in cortisol secretion after administration of an ACTH analogue in sheep during the breeding and non-breeding season. Animal Reproduction Science 79: 81–92CrossRefGoogle ScholarPubMed
van Praag, HM 2004 Can stress cause depression? Process in Neuro-Psychopharmacology & Biological Psychiatry: 28 (5): 891-907CrossRefGoogle Scholar
Venkatraman, JT, Feng, XH and Pendergast, D 2001 Effects of dietary fat and endurance exercise on plasma cortisol, prostaglandin E-2, interferon-gamma and lipid peroxides in runners. Journal of the American College of Nutrition: 20(5): 529–536CrossRefGoogle Scholar
Vincent, JD 1994 Biological aspects of pleasure. Presse Medicale 23: 1871–1876Google Scholar
Vining, RF, McGinley, RA, Maksyvitis, JJ and Ho, KY 1983 Salivary cortisol: a better measure of adrenal function than serum cortisol. Annals of Clinical Biochemistry 20: 329–335CrossRefGoogle ScholarPubMed
Volek, JS, Kraemer, WJ, Bush, JA, Incledon, T and Boetes, M 1997 Testosterone and cortisol in relationship to dietary nutrients and resistance exercise. Journal of Applied Physiology 82: 49–54CrossRefGoogle ScholarPubMed
von der Ohe, CG and Servheen, C 2002 Measuring stress in mammals using fecal glucocorticoids: opportunities and challenges. Wildlife Society Bulletin 30: 1215–1225Google Scholar
von der Ohe, CG, Wasser, SK, Hunt, KE and Servheen, C 2004 Factors associated with fecal glucocorticoids in Alaskan Brown bears (Ursus arctos horribilis). Physiological and Biochemical Zoology 77: 313–320CrossRefGoogle ScholarPubMed
Wasser, SK, Hunt, KE, Brown, JL, Cooper, K, Crockett, CM, Bechert, U, Millspaugh, JJ, Larson, S and Montfort, SL 2000 A generalised fecal glucocorticoid assay for use in a diverse array of non-domestic mammalian and avian species. General and Comparative Endocrinology 120: 260–275CrossRefGoogle Scholar
Weingrill, T, Gray, DA, Barrett, L and Henzi, SP 2004 Fecal cortisol levels in free-ranging female chacma baboons: relationship to dominance, reproductive state and environmental factors. Hormones and Behavior 45: 259–269CrossRefGoogle ScholarPubMed
Westrin, A, Ekman, R and Traskman-Bendz, L 1999 Alterations of corticotropin releasing hormone (CRH) and neu-ropeptide Y (NPY) plasma levels in mood disorder patients with a recent suicide attempt. European Neuropsychopharmacology 9: 205–211CrossRefGoogle ScholarPubMed
Wong, V, Yan, T, Donald, A and McLean, M 2004 Saliva and bloodspot cortisol: novel sampling methods to assess hydrocortisone replacement therapy in hypoadrenal patients. Clinical Endocrinolgy 612: 131–137CrossRefGoogle Scholar
Yehuda, R, Golier, JA and Kaufman, S 2005 Circadian rhythm of salivary cortisol in holocaust survivors with and without PTSD. American Journal of Psychiatry 162(5): 998–1000CrossRefGoogle ScholarPubMed
Young, KM, Walker, SL, Lanthier, C, Waddell, WT, Monfort, SL and Brown, JL 2004 Non-invasive monitoring of adrenocortical activity in carnivores by fecal glucocorticoid analyses. General and Comparative Endocrinology 138(3): 148–165CrossRefGoogle Scholar
Zhou, XQ, Xie, MX, Niu, CJ and Sun, RY 2003 The effects of dietary vitamin C on growth, liver vitamin C and serum cortisol in stressed and unstressed juvenile soft-shelled turtles (Pelodiscus sinensis). Comparative Biochemistry and Physiology — Part A: Molecular & Integrative Physiology 135: 263–270CrossRefGoogle ScholarPubMed
Zimmer, C, Basler, HD, Vedder, H and Lautenbacher, S 2003 Sex differences in cortisol response to noxious stress. Clinical Journal of Pain 19: 233–239CrossRefGoogle Scholar