Elsevier

Physiology & Behavior

Volume 62, Issue 2, August 1997, Pages 225-232
Physiology & Behavior

Psychosocial Stress and Urinary Cortisol Excretion in Marmoset Monkeys

https://doi.org/10.1016/S0031-9384(97)00103-0Get rights and content

Abstract

Smith, T. E. and J. A. French. Psychosocial stress and urinary cortisol excretion in marmosets (Callithrix kuhli). Physiol Behav 62(2) 225–232, 1997.—Activation of the hypothalamic-pituitary-adrenal (HPA) axis is one of the hallmarks of the physiological responses to psychosocial stressors. The most common method of assessing HPA function is via the measurement of plasma cortisol levels. However, venipuncture involves capture and restraint, which can modify HPA function. We validated a noninvasive procedure for monitoring HPA responses to stressors by measuring excretion of free urinary cortisol. Samples collected throughout the day displayed marked circadian variation, with low cortisol values in first-void samples, followed by a mid-morning peak in cortisol excretion. Concentrations of excreted cortisol declined throughout the day. Exposing marmosets to mild and moderate stressors (11 h isolation in a small cage and manual restraint) increased excreted cortisol concentrations in a dose-dependent fashion: isolation in a small cage led to elevated cortisol in afternoon samples, while manual restraint and isolation produced elevated cortisol in both morning and afternoon samples. The marmoset HPA is differentially sensitive to rather subtle variations in stressors, and these results show that urinary cortisol excretion is a valid and sensitive index of the HPA response to these stressors.

Section snippets

Subjects

Subjects were seven male and nine female Wied's black tufted-ear marmosets aged 1.2 to 10.2 years, housed in social groups at the University of Nebraska at Omaha Callitrichid Research Facility (see Table 1). Marmosets were housed in either family groups or breeding pairs or trios that had been established for at least six months. Six of the females used in the study were breeding females in the first or second trimester of pregnancy. The remaining three females were the eldest daughter in the

Urine Samples

We attempted to collect 12 samples (i.e. hourly samples 0700–1800 h) from each animal under each condition. For each condition, the following percent of the possible samples were collected: Control = 79%, SC = 91%, SC + H = 90%.

Circadian Pattern

All subjects exhibited a circadian pattern of hormone excretion under stress-free conditions (see Fig. 1). Analysis of the data by ANOVA revealed a significant main effect of time and sex on the diurnal pattern of cortisol excretion (Time, F(9,84) = 3.29, p < 0.01; sex, F

Discussion

The study has established that urinary cortisol can be used as a valid indicator of stress in marmosets. The circadian variation evident in plasma cortisol was also reflected in urinary cortisol values (e.g., 7, 49, 64). In addition, the adrenocortical response to SC+H, a relatively major stressor for animals in our colony, was discerned by elevations in urinary cortisol within a couple of hours of the stressor. Cortisol concentrations rose more rapidly, and remained elevated for significantly

Acknowledgements

The authors thank Dr. A. Pissinatti and A. Coimbra-Filho from the Centro de Primatologia do Rio de Janeiro for their help in establishing the colony of Callithrix kuhli at UNO. We also thank Denise Hightower-Merritt and Danny Revers for their care and management of the animals. Reagents for the cortisol EIA were provided by Bill Lasley and Coralie Munro of the University of California, Davis, and the latter provided assistance in establishing the assay in our laboratory. The authors are

References (74)

  • D.H Abbott

    Behavioral and physiological suppression of fertility in subordinate marmoset monkeys

    Am. J. Primatol.

    (1984)
  • F.B Bercovitch et al.

    Dominance rank, cortisol concentrations, and reproductive maturation in male rhesus macaques

    Physiol. Behav.

    (1995)
  • M Bradbury et al.

    Stress-induced ACTH secretion: Diurnal responses and decreases during stress in the evening are not dependent on corticosterone

    Endocrinology

    (1991)
  • N.G Caine

    Flexibility and co-operation as unifying themes in Saguinus social organization and behaviour: the role of predation pressures

  • Clarke, A. S. ACTH and glucocorticoid responses under two conditions of stress in macaques. Am. J. Primatol....
  • C.L Coe

    Psychosocial factors and immunity in nonhuman primates: A review

    Psychosom. Med.

    (1993)
  • C.L Coe et al.

    Diurnal and annual variation of adrenocortical activity in the squirrel monkey

    Am. J. Primatol.

    (1995)
  • C.L Coe et al.

    Hormonal response to stress in the squirrel monkey (Saimiri sciureus)

    Neuroendo.

    (1978)
  • C.L Coe et al.

    Rapid cortisol and corticosteroid-binding globulin responses during pregnancy and after estrogen administration in the squirrel monkey

    Endocrinology

    (1986)
  • C.L Coe et al.

    Phylogentic influences on hormone levels across the Primate order

    Am. J. Primatol.

    (1992)
  • S Cohen et al.

    Stress, social support, and the buffering hypothesis

    Psychol. Bull.

    (1985)
  • C.M Crockett et al.

    Appetite suppression and urinary cortsiol responses to different cage sizes and tethering procedures in longtailed macaques

    Am. J. Primatol.

    (1990)
  • C.M Crockett et al.

    Urinary cortisol responses of longtailed macaques to five cage sizes, tethering, sedation, and room change

    Am. J. Primatol.

    (1993)
  • C.M Crockett et al.

    Behavioral responses to four sizes of home cage by adult pigtailed macaques

    Am. J. Primatol.

    (1994)
  • C.M Crockett et al.

    Behavioral responses of longtailed macaques to different cage sizes and common laboratory experiences

    J. Comp. Psychol.

    (1995)
  • D.D Cubicciotti et al.

    Differences between Saimiri sciureus and Callicebus moloch in physiological responsiveness: implications for behavior

    J. Comp. Psychol.

    (1986)
  • S.E Cummins et al.

    The relationship between daily stress and urinary cortisol in a normal population: An emphasis on individual differences

    Behav. Med.

    (1993)
  • N.M Czekala et al.

    Diurnal urinary cortocoid excretion in the human and gorilla

    Am. J. Primatol.

    (1994)
  • M.F Dallman et al.

    Regulation of ACTH secretion: Variations on a theme of B

    Recent Prog. Horm. Res.

    (1987)
  • D Darlington et al.

    Responses of ACTH, epinephrine, norepinephrine, and cardiovascular system to hemorrhage

    Am. J. Physiol.

    (1986)
  • J.M Dietz et al.

    Polygyny and female reproductive success in golden lion tamarins, Leontopithecus rosalia

    Anim. Behav.

    (1993)
  • A.K Dubey et al.

    A suppression of gonadotropin secretion by cortisol in castrated male rhesus monkeys (Macaca mulatta) mediated by the interruption of hypothalamic gonadotropin-releasing hormone release

    Biol. Reprod.

    (1985)
  • J Eberhart et al.

    Social influences on circulating levels of cortisol and prolactin in male talapoin monkeys

    Physiol. Behav.

    (1983)
  • J.A French

    Proximate regulation of singular breeding in Callitrichid primates

  • B Friedmann et al.

    Energy metabolism and regulatory hormones in women and men during endurance exercise

    Eur. J. Appl. Physiol.

    (1989)
  • P.A Garber

    Feeding ecology and behaviour of the genus Saguinus

  • D.A Gust et al.

    Effect of a preferred companion in modulating stress in adult female rhesus monkeys

    Physiol. Behav.

    (1994)
  • D.A Gust et al.

    Behavioral and physiological response of juvenile Sooty Mangabeys to reunion with their mothers following a year's absence

    Develop. Psychobiol.

    (1992)
  • J.W Hennessy et al.

    Stress, Arousal, and the pituitary adrenal system: A psychoendocrine hypothesis

  • M.B Hennessy et al.

    Endocrine sensitivity to novelty in squirrel monkeys and titi monkeys: species differences in characteristic modes of responding to the environment

    Physiol. Behav.

    (1995)
  • B .J Inglett et al.

    Dynamics of intrafamily aggression and social reintegration in lion tamarins

    Zoo Biol.

    (1989)
  • M.N Jurke et al.

    An investigation into the socioendocrinology of infant care and postpartum fertility in Goeldi's monkey (Callimico goeldii)

    Int. J. Primatol.

    (1995)
  • G Kant et al.

    Diurnal variation in neuroendocrine responses to stress in rats: plasma ACTH, beta-LPH, corticosterone, prolactin, and pitiutary cyclic AMP responses

    Neuroendocrinol.

    (1986)
  • G Keppel

    A Researcher's Handbook

    (1991)
  • E.B Keverne et al.

    Dominance and subordination: Concepts or physiological states

  • C Kirschbaum et al.

    Sex-specific effects of social support on cortisol and subjective responses to acute psychological stress

    Psychosom. Med.

    (1995)
  • J.I Kitay

    Sex differences in adrenal cortical secretion in the rat

    Endocrinol.

    (1961)
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