The Role of the Endocrine System in Baboon Maternal Behavior

M. Bardi et al BIOL PSYCHIATRY 2004;55:724–732 725
(Bardi et al 2003a). Elevated prolactin and cortisol levels have
been related to male parental care (Ziegler et al 2000).
Both the direction and the extent of these associations have
generated problematic interpretations, however, because a number
of studies have failed to confirm those findings, often within
the same species and when conducted by the same research
groups. Although Bahr and colleagues originally found an association
between progesterone, cortisol, and a maternal competence
score in gorillas (Bahr 1995; Bahr et al 1998), later
expansion of their studies did not support a relation between
hormonal levels and maternal behavior (Bahr et al 2001). Moreover,
despite several studies pointing toward a role for ovarian
steroid hormones in shaping maternal behavior, Maestripieri and
Megna (2000) failed to find a relation between peripheral ovarian
steroid hormonal levels during early lactation and individual
differences in the maternal style of abusive and controlling
mothers. Finally, whereas most studies revealed a positive association
between elevated estrogen and maternal behavior, Fite
and French (2000) found that estradiol levels were higher in
mothers of infants who did not survive.
Contradictory results exist in humans as well. Fleming and
colleagues reported that changes in maternal feeling during
pregnancy were unrelated to the levels of pregnancy hormones
or cortisol (Corter and Fleming 1995) and that cortisol was not
associated with attitudinal measures of maternal responsiveness
(Fleming et al 1997b). The same research group also found that
the pattern of change in the ratio of plasma E 2 to progesterone
from early to late pregnancy was related to postpartum attachment
feelings (Fleming et al 1997a) and that mothers with higher
cortisol levels were more attracted to their own infant’s body
odor (Fleming et al 1997b).
A large body of human research on changes in hypothalamopituitary-adrenal
(HPA) and hypothalamic-pituitary-gonadal
(HPG) axes functioning during pregnancy and the postpartum
period has assessed their relation with mood, anxiety, and stress
response, linking these two systems, albeit indirectly, with
parenting behavior and infant outcome. Susceptibility to psychosocial
stressors during lactation has been found in several
studies, pointing toward a central mechanism that influences
both reproduction and the hypothalamo-pituitary-adrenal HPA
axis for mediating the effects of environmental challenges (Carter
et al 2001). Others found that the degree of change in circulating
hormones in response to happy and sad emotions was small and
possibly not functionally significant (Turner et al 2002). Finally,
effects of the postpartum maternal endocrine status have been
significantly associated with the child’s temperament (Susman et
al 2001).
The baboon provides an excellent model for the study of the
endocrinology of human pregnancy because the characteristics
of the menstrual cycle in baboons are very similar to those of
women, and the pattern of estrogens and progesterone secretion
are virtually identical (Stevens 1997). In addition, the baboon has
a visually identifiable menstrual cycle and pregnancy status. The
goal of this study was to assess the relation between the overall
endocrine steroid changes during the peripartum period and
maternal behavior. Because adrenocortical activity is likewise
affected by the changes in physiologic status that occur during
the peripartum period, we also evaluated the synergistic functioning
of the HPA and HPG axes across parturition for its effect
on the quality of maternal care in baboons. In particular, we
tested the hypotheses that maternal behavior is positively correlated
with high values of the estrogen–progesterone balance, and
that physiologic peripartum stress, as measured by cortisol levels,
is negatively correlated with later mother–infant levels of interaction.
This project was designed to account for multiple sources
of variation and for the great physiologic and behavioral individual
phenotypic plasticity using a large, extensively monitored
subject pool. Because our aim was to compare two sets of
variables divided naturally in two groups, the endocrine and the
behavioral sets, we used canonical correlation analysis to take
into account the complexity of the relations within and between
the two sets, thus considering for the first time in any primate
species the overall association between hormonal levels and
maternal behavior during the late pregnancy–early lactation
period.
Methods and Materials
Study Sample
The subjects include 89 pregnant female savannah baboons
(Papio hamadryas sp.) and their newborn offspring. Females
were of known lineage and were between the ages of 5 and 20
years (mean age 11.4 3.6 SD). All females were housed in
similar outdoor enclosures (47 m 2 ), including a heated sheltered
area for the winter, at the Southwest Foundation for Biomedical
Research, San Antonio, Texas. The enclosures had perches,
swings, and standard toys available at all times. Subjects lived in
social groups including one adult male and 8–20 adult females.
Subjects were never transferred from a group to another during
the course of the study, and they were all born in captivity. The
subjects were part of a planned breeding program and were not
used for other research during the course of the study. Offspring
remained within the home cage until they were weaned at the
age of 12–15 months. Animals were fed commercially available
diet daily. Grain was scattered in the cage daily, and water was
supplied ad libitum.
Dominance matrices were constructed using the prepartum
data by considering the directionality of affiliative, submissive,
and aggressive behaviors given and received by the subject and
with all other adult individuals within the social group. Social
rank was further determined by the subject’s priority of access to
a preferred food source (fruit), which was placed at the front of
the cage by the observer who then recorded the order of
approaching females. Each individual in each social group was
then ranked on a scale of high, medium, and low rank by
evaluating the dominance matrices and food access.
Gender distribution among the 89 newborns was homoge-
neous (43 males, 46 females). Maternal rank and age were also
homogeneously distributed in the sample ( 2
[4] 2.1, ns), with
no significant interaction between these two factors (r .1, n
89, ns). Maternal experience, as represented by the number of
previous offspring delivered, was also homogeneously distributed
in the sample: the number of previous offspring ranged
between 1 and 9 (mean number of offspring 4.8 2.1 SD). As
expected, we found a significant association between age and
number of previous offspring (r .7, n 89, p .05).
Data Collection
Each subject was monitored for pregnancy by recording
changes in the gender skin size and color. The scoring of the
gender skin swelling (on a scale of 1–4 plus menstruation) was
used to indicate the menstrual cyclicity (Hendrickx 1965). Pregnancy
was then determined starting when the normal cycling
was interrupted and choosing the estimated date of parturition as
185 days after the last day of fully swollen gender skin. The
average estimated data of parturition was within 5 days of the
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