Skip to main content
Log in

Behavioral and adrenocortical responses of rhesus macaque mothers to infant separation in an unfamiliar environment

  • Published:
Primates Aims and scope Submit manuscript

Abstract

The behavioral and adrenocortical responses of rhesus macaque mothers to a series of four consecutive 4-day separations from their 5-month old infants in an unfamiliar environment were examined. A biphasic behavioral response to separation was observed, with passive behavior, locomotion, and vocalization highest on Day 1 of separation, and self-directed behaviors and environmental exploration peaking during Days 2–4. Stereotyped locomotion increased, and passive behavior decreased, across successive weeks of separation. The rhesus mothers exhibited substantial cortisol elevations one and two hours postseparation, with cortisol decreasing on the fourth day of separation. The cortisol response was strongest during the first week of separation, but robust elevations occurred in response to repeated separations. No signs of behavioral depression were observed. The results indicate that infant separation combined with removal to a novel environment can be a potent stressor for rhesus macaque mothers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Champoux, M., C. L. Coe, S. M. Schanberg, C. M. Kuhn, &S. J. Suomi, 1989. Hormonal effects of early rearing conditions in the infant rhesus monkey.Amer. J. Primatol., 19: 111–117.

    Article  Google Scholar 

  • Coe, C. L., J. C. Glass, S. G. Wiener, &S. Levine, 1983. Behavioral, but not physiological, adaptation to repeated separation in mother and infant primates.Psychoneuroendocrinol., 8: 401–409.

    CAS  Google Scholar 

  • ————,S. P. Mendoza, W. P. Smotherman, &S. Levine, 1978. Mother-infant attachment in the squirrel monkey: adrenal response to separation.Behav. Biol., 22: 256–263.

    Article  CAS  PubMed  Google Scholar 

  • ————,S. G. Wiener, &S. Levine, 1983. Psychoendocrine responses of mother and infant monkeys to disturbance and separation. In:Symbiosis In Parent-offspring Interactions,L. A. Rosenblum &H. Moltz (eds.), Plenum Press, New York, pp. 189–214.

    Google Scholar 

  • Crockett, C. M., C. L. Bowers, G. P. Sackett, &D. M. Bowden, 1993. Urinary cortisol responses of longtailed macaques to five cage sizes, tethering, sedation, and room change.Amer. J. Primatol., 30: 55–74.

    Google Scholar 

  • Duncan, D. B., 1955. Multiple range and multipleF tests.Biometrics, 11: 1–41.

    Google Scholar 

  • Elvidge, H., J. R. G. Challis, J. S. Robinson, C. Roper, &G. D. Thorburn, 1976. Influence of handling and sedation on plasma cortisol in rhesus monkeys (Macaca mulatta).J. Endocrin., 70: 325–326.

    CAS  Google Scholar 

  • Fuller, G. B., W. C. Hobson, F. I. Reyes, J. S. D. Winter, &C. Faimain, 1984. Influence of restraint and ketamine anesthesia on adrenal steroids, progesterone, and gonadotropins in rhesus monkeys.Proc. Soc. Exp. Biol. Med., 175: 487–490.

    CAS  PubMed  Google Scholar 

  • Gunnar, M. R., C. A. Gonzalez, &S. Levine, 1980. The role of peers in modifying behavioral distress and pituitary-adrenal response to a novel environment in year-old rhesus monkeys.Physiol. Behav., 25: 795–798.

    Article  CAS  PubMed  Google Scholar 

  • Hennessy, M. B., 1986. Multiple, brief maternal separations in the squirrel monkey: changes in hormonal and behavioral responsiveness.Physiol. Behav., 36: 245–250.

    Article  CAS  PubMed  Google Scholar 

  • Hinde, R. A. &L. Davies, 1972. Removing infant rhesus from mother for 13 days compared with removing mother from infant.J. Child Psychol. Psychiat., 13: 227–237.

    CAS  PubMed  Google Scholar 

  • ———— &L. McGinnis, 1977. Some factors influencing the effects of temporary mother-infant separation: some experiments with rhesus monkeys.Psychol. Med., 7: 197–212.

    CAS  PubMed  Google Scholar 

  • ———— &Y. Spencer-Booth, 1971. Effects of brief separation from mother on rhesus monkeys.Science, 173: 111–118.

    CAS  PubMed  Google Scholar 

  • Jensen, G. D., 1968. Reaction of monkey mothers to long-term separation from their infants.Psychonom. Sci., 11: 171–172.

    Google Scholar 

  • ———— &C. W. Tolman, 1962. Mother-infant relationship in the monkey,Macaca nemestrina: the effect of brief separation and mother-infant specificity.J. Comp. Physiol. Psychol., 55: 131–136.

    CAS  PubMed  Google Scholar 

  • Jordan, T. C., M. B. Hennessy, C. A. Gonzalez, &S. Levine, 1985. Social and environmental factors influencing mother-infant separation-reunion in squirrel monkeys.Physiol. Behav., 34: 489–493.

    Article  CAS  PubMed  Google Scholar 

  • Kaplan, J., 1970. The effects of separation and reunion on the behavior of mother and infant squirrel monkeys.Devel. Psychobiol., 3: 43–52.

    CAS  Google Scholar 

  • Leshner, A. I., P. T. K. Toivola, &E. Terasawa, 1978. Circadian variations in cortisol concentrations in the plasma of female rhesus monkeys.J. Endocrin., 78: 155–156.

    CAS  Google Scholar 

  • Levine, S., D. F. Johnson, &C. A. Gonzalez, 1985. Behavioral and hormonal responses to separation in infant rhesus monkeys and mothers.Behav. Neurosci., 99: 399–410.

    Article  CAS  PubMed  Google Scholar 

  • Mendoza, S. P., W. P. Smotherman, M. T. Miner, J. Kaplan, &S. Levine, 1978. Pituitary-adrenal response to separation in mother and infant squirrel monkeys.Develop. Psychobiol., 11: 169–175.

    Article  CAS  Google Scholar 

  • Mineka, S. &S. J. Suomi, 1978. Social separation in monkeys.Psychol. Bull., 85: 1376–1400.

    CAS  PubMed  Google Scholar 

  • ————, ————, &R. Delizio, 1981. Multiple separations in adolescent monkeys: an opponentprocess interpretation.J. Exper. Psychol: General., 110: 56–85.

    CAS  Google Scholar 

  • Mitchell, G. &J. Gomber, 1976. Moving laboratory rhesus monkeys (Macaca mulatta) to unfamiliar home cages.Primates, 17: 543–547.

    Article  Google Scholar 

  • Reinhardt, V., D. Cowley, J. Scheffler, R. Vertein, &F. Wegner, 1990. Cortisol response of female rhesus monkeys to venipuncture in home cage versus venipuncture in restraint apparatus.J. Med. Primatol., 19: 601–606.

    CAS  PubMed  Google Scholar 

  • Reite, M., I. C. Kaufman, J. D. Pauley, &A. J. Stynes, 1974. Depression in infant monkeys: physiological correlates.Psychosom. Med., 36: 363–367.

    CAS  PubMed  Google Scholar 

  • Sackett, G. P., R. E. Bowman, J. S. Meyer, R. L. Tripp, &S. S. Grady, 1973. Adrenocortical and behavioral reactions by differentially raised rhesus monkeys.Physiol. Psychol., 1: 209–212.

    Google Scholar 

  • Seay, B., E. Hansen, &H. F. Harlow, 1962. Mother-infant separation in monkeys.J. Child Psychol. Psychiat., 3: 123–132.

    CAS  PubMed  Google Scholar 

  • Smotherman, W. P., L. E. Hunt, L. M. McGinnis, &S. Levine, 1979. Mother-infant separation in group-living rhesus macaques: a hormonal analysis.Develop. Psychobiol., 12: 211–217.

    Article  CAS  Google Scholar 

  • Socol, M. L., F. A. Manning, Y. Murata, J. Challis, &C. B. Martin, Jr., 1978. Plasma cortisol in the chronic rhesus monkey preparation (Macaca mulatta).Amer. J. Obstet. Gynecol., 132: 421–424.

    CAS  Google Scholar 

  • Suomi, S. J., 1983. Social development in rhesus monkeys: consideration of individual differences. In:The Behavior Of Human Infants,A. Oliverio &M. Zappella (eds.), Plenum Press, New York, pp. 71–92.

    Google Scholar 

  • ———— &H. F. Harlow, 1977. Production and alleviation of depressive behavior in monkeys. In:Psychopathology: Experimental Models,J. Maser &M. E. P. Seligman (eds.), Freeman, San Francisco, pp. 131–173.

    Google Scholar 

  • ————, ————, &C. J. Domek, 1970. Effect of repetitive infant-infant separation of young monkeys.J. Abnorm. Psychol., 76: 161–172.

    CAS  PubMed  Google Scholar 

  • ————,S. Mineka, &R. D. Delizio, 1983. Short-and long-term effects of repetitive motherinfant separations on social development in rhesus monkeys.Devel. Psychol., 19: 770–786.

    Google Scholar 

  • Vogt, J. L. &S. Levine, 1980. Response of mother and infant squirrel monkeys to separation and disturbance.Physiol. Behav., 24: 829–832.

    Article  CAS  PubMed  Google Scholar 

  • Walker, M. I., G. J. Pepe, N. L. Garnett, &E. D. Albrecht, 1987. Effects of anesthetic agents on the adrenocortical system of female baboons.Amer. J. Primatol., 13: 325–332.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

About this article

Cite this article

Champoux, M., Suomi, S.J. Behavioral and adrenocortical responses of rhesus macaque mothers to infant separation in an unfamiliar environment. Primates 35, 191–202 (1994). https://doi.org/10.1007/BF02382054

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02382054

Key Words

Navigation