Suppression of Cortisol Levels in Subordinate
Female Marmosets: Reproductive
and Social Contributions
Wendy Saltzman,*
,1
Nancy J. Schultz-Darken,
Frederick H. Wegner, Daniel J. Wittwer, and David H. Abbott*
,
²
Wisconsin Regional Primate Research Center, *Endocrinology-Reproductive Physiology
Program, and †Department of Obstetrics and Gynecology, University of Wisconsin,
Madison, Wisconsin 53715-1299
Received August 26, 1997; revised November 21, 1997; accepted January 7, 1998
Socially subordinate female common marmosets ( Cal-
lithrix jacchus) have markedly lower plasma cortisol levels
than dominant females. Subordinate females also undergo
hypoestrogenemic anovulation, and estrogen can elevate
glucocorticoid levels. Therefore, we previously hypothe-
sized that this cortisol difference is mediated by rank-
related differences in reproductive hormones, probably es-
tradiol. To test this possibility, we characterized the effects
of the ovarian cycle and ovariectomy on plasma cortisol
concentrations. Beginning in the early follicular phase,
basal blood samples were collected from seven cycling
female marmosets daily for 16 days and at 2- to 3-day
intervals for another 16 days. Samples were collected iden-
tically from seven anovulatory subordinate females and
seven long-term ovariectomized females. Cortisol levels
changed reliably across the ovarian cycle, with levels in the
mid- to late follicular, peri-ovulatory, and early luteal
phases higher than those in the remainder of the cycle.
Cortisol levels of cycling females were significantly higher
than those of subordinates at all parts of the cycle, but
were significantly higher than those of ovariectomized fe-
males only during the midcycle elevation. Unexpectedly,
subordinates had significantly lower cortisol levels than
ovariectomized females, as well as higher estradiol and
estrone levels and lower progesterone and luteinizing hor-
mone (LH) levels. These results confirm that circulating
cortisol concentrations are modulated by reproductive
function in female marmosets but also indicate that low
cortisol levels in subordinate females cannot be attributed
simply to hypoestrogenemia. Instead, other factors, such
as direct effects of social subordination or suppression of
LH levels, contribute to suppression of cortisol in subordi-
nates. © 1998 Academic Press
Measures of hypothalamo–pituitary–adrenal (HPA)
activity have been found to correlate with social status in
numerous species, with subordinate animals frequently
evincing higher adrenal weights, basal glucocorticoid
levels, or adrenal responses to stressors than their dom-
inant counterparts (see reviews by Henry, Stephens, and
Ely, 1986; Sapolsky, 1995). These findings have led to the
widely held view that social subordination is inherently
stressful and that the psychosocial stress generated by
subordination directly elevates HPA activity. It is be-
coming clear, however, that this simple socioendocrine
model may not adequately explain the diversity of find-
ings on endocrine function and social status. For exam-
ple, an increasing number of investigations in a growing
number of species have failed to demonstrate the ex-
pected association of high chronic HPA activity with low
social status. Instead, HPA activity may not be system-
atically correlated with social status (e.g., Mays, Vleck,
and Dawson, 1991; Bercovitch and Clarke, 1995; Ziegler,
Scheffler, and Snowdon, 1995; Smith and French, 1997)
or, in a few cases, may be lower in subordinate animals
than in their dominant counterparts (Coe, Mendoza, and
Levine, 1979; Schoech, Mumme, and Moore, 1991; Wing-
field, Hegner, and Lewis, 1991; Saltzman, Schultz-
Darken, Scheffler, Wegner, and Abbott, 1994; Creel,
Creel, and Monfort, 1996).
One reason for the absence of a consistent relationship
between HPA activity and social status may be that HPA
function is modulated by numerous behavioral and
physiological variables in addition to psychosocial
stress. Moreover, many of these variables may them-
selves be influenced by social status. For example, phys-
ical activity (Coleman, Garland, Marler, Newton, Swal-
low, and Carter, 1998; Mallick, Stoddart, Jones, and
Bradley, 1994), immune function (Hermus and Sweep,
1
To whom correspondence should be addressed at Wisconsin
Regional Primate Research Center, University of Wisconsin, 1220
Capitol Court, Madison, WI 53715-1299. Fax: (608) 265-4729. E-mail:
saltzman@primate.wisc.edu.
Hormones and Behavior 33, 58–74 (1998)
Article No. HB981436
0018-506X/98 $25.00
Copyright © 1998 by Academic Press
All rights of reproduction in any form reserved. 58