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Changes in yearling rhesus monkeysТ relationships with their mothers after sibling birth.

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American Journal of Primatology 54:193–210 (2001)
Changes in Yearling Rhesus Monkeys’ Relationships With
Their Mothers After Sibling Birth
B.J. DEVINNEY1*, C.M. BERMAN1,3, AND K.L.R. RASMUSSEN2,3
1
Department of Anthropology, State University of New York at Buffalo, Buffalo, New York
2
Laboratory of Comparative Ethology, National Institute of Child Health and Human
Development, Poolesville, Maryland
3
Caribbean Primate Research Center, Punta Santiago, Puerto Rico
The birth of a new sibling is believed to signify an abrupt and important transition in a young primate’s relationship with its mother—one
that is of potential importance from at least three theoretical perspectives: attachment theory, parent–offspring conflict theory, and dynamic
assessment models. This study examines changes in relationships between free-ranging yearling rhesus monkeys (Macaca mulatta) and their
mothers concomitant with the birth of the mother’s next infant, and
tests predictions derived from each theoretical perspective. We observed
31 yearling rhesus on Cayo Santiago, Puerto Rico, 3 months before and
3 months after their siblings’ births, using focal animal sampling methods. Changes in measures related to mother–yearling interaction and
yearling distress were examined using repeated-measures analysis of
variance. After sibling birth, mothers and yearlings abruptly reduced
amounts of time in contact and increased amounts of time at a distance
and out of sight of one another. Mothers and yearlings played approximately equal roles in bringing about decreases in proximity, and yearlings took the primary roles in bringing about decreases in contact. Rates
of maternal aggression toward yearlings increased immediately and
markedly after birth, possibly providing yearlings with early cues regarding subsequent decreased levels of maternal care. There were no
marked increases in overt signs of yearling distress (e.g., vocalizations
or tantrums) following the births. We conclude that yearlings generally
acquiesced to reduced levels of care, responding behaviorally with increased independence and maturity. In this sense, our study provides
preliminary support for dynamic assessment models over attachment
theory and parent–offspring conflict theory models. Am. J. Primatol.
54:193–210, 2001. © 2001 Wiley-Liss, Inc.
Key words: sibling birth; Macaca mulatta; juveniles; mother–offspring
relationships
Contract grant sponsor: Wenner-Gren Foundation for Anthropological Research.
*Correspondence to: B.J. DeVinney, Laboratory of Comparative Ethology, NICHD, P.O. Box 529,
Poolesville, MD 20837. E-mail: bd99x@nih.gov
Received 12 October 2000; revision accepted 30 April 2001
© 2001 Wiley-Liss, Inc.
194 / DeVinney et al.
INTRODUCTION
The birth of a new sibling is believed to signify an important transition in a
young primate’s relationship with its mother. For many species, it is marked by
an abrupt decrease in direct forms of maternal care and it often coincides with
the complete termination of suckling by the older sibling. As such, it is a transition that is of potential importance from a number of theoretical perspectives,
although none address it specifically or exclusively. Attachment theory [Bowlby,
1969; Ainsworth, 1979] would liken the event to the psychological separation of a
mother from her infant [Berman et al., 1994], or “partial removal” of the mother
[Holman & Goy, 1988]. Hence it might predict similar responses to those seen in
studies of physical separation from mothers [reviewed by Mineka & Suomi, 1978],
such as increases in behavioral distress followed in some cases by signs of depression, particularly among anxiously attached offspring. Parent–offspring conflict theory [Trivers, 1974] potentially views this transition as a shift in the
mother’s distribution of investment from the older immature to the younger. It
would predict the increased occurrence of behavioral conflict between mother
and yearling as the yearling attempts to use deceptive signaling to elicit more
investment from the mother than she is “willing” to give. Alternative “dynamic
assessment” approaches to parent–offspring relations propose that rather than
conflict, cooperation and compromise between parents and offspring over levels
of care may be prevalent [Altmann, 1980; Bateson, 1994]. Bateson’s [1994] approach suggests that during reductions in care, parents provide cues regarding
their ability to provide care, offspring signal honestly regarding their condition
or need for resources [see Grafen, 1990; Godfray, 1991], and both monitor each
other, as well as environmental conditions, and respond dynamically. For example, cat and rat mothers experiencing a restricted diet precociously wean their
offspring, and those offspring exhibit accelerations in behavioral development
during the weaning process [Bateson et al., 1990; Smith, 1991]. In addition, baboon infants’ weaning tantrums seem to function as honest signals of need to
which mothers respond with increased nursing. Tantruming occurs only when
weaning foods are unavailable due to seasonal changes in the environment
[Barrett & Henzi, 2000].
The relevance of each of these perspectives for the sibling birth transition
can not be ascertained, partly because little systematic research has been done
documenting the nature of changes in mother–offspring relationships upon the
birth of new infants. In this work, we begin to fill this gap by describing sibling
birth transitions among free-ranging rhesus monkeys on Cayo Santiago, Puerto
Rico, and by testing a few predictions for each perspective. Our goal is not to
provide definitive support for one theory over the others, but rather to guide
further research into the sibling birth transition. No detailed study of nonhuman
primates’ reactions to the birth of a sibling has been conducted outside of captivity other than Lee’s [1983a] study of wild vervet yearlings, and that study included only three yearlings.
The sibling birth transition has been studied more thoroughly among humans than among nonhuman primates. The findings to date suggest that a number of parallels exist between the behavioral patterns of human and nonhuman
primates in the initial weeks and months after sibling birth. Among humans,
older siblings typically experience reduced levels of maternal care or interaction
and/or increases in confrontation with their mothers [Dunn & Kendrick, 1980;
Dunn et al., 1981]. They also may exhibit signs of increased distress, including
tearfulness, clinginess, and increased demandingness and negativity, and signs
of disturbance such as withdrawal, passivity, or aimless wandering. Paradoxi-
Yearling Rhesus at Sibling Birth / 195
cally, a given child can show both signs of regression (i.e., decreased self-care)
and evidence of increased independence in different behaviors [Taylor & Kogan,
1973; Trause et al., 1981; Dunn & Kendrick, 1982].
A few studies of this transition in cercopithecines have been reported. Among
cercopithecines, one sees decreased maternal time in proximity (vervets [Lee,
1983a] and rhesus macaques [Holman & Goy, 1988]), decreased maternal grooming [Lee, 1983a], decreased maternal approaches (male rhesus [Holman & Goy,
1988]), and increased maternal aggression (pigtail macaques and Papio spp.
[Bolwig, 1980]) to yearling offspring following the birth of a younger sibling. In
addition, at sibling birth, mothers who have not already weaned their older offspring terminate suckling (Japanese macaques [Tanaka, 1992]). A few individual
youngsters among vervets [Lee, 1983a] and captive rhesus [Holman & Goy, 1988]
may briefly become “depressed” (i.e., they may sit in a typically hunched posture
indicative of depression in macaques [Kaufman & Rosenblum, 1967]).
Rhesus older siblings (mean age at sibling birth = 2 yr) show increases in
interaction with their mothers after sibling birth, apparently due to the older
siblings’ interest in the new infant siblings [DiGregorio et al., 1987]. The subjects of DiGregorio et al.’s study were housed with their families in a nuclear
family apparatus in which parents and peers were in separate parts of the housing, thereby forcing subjects to make a choice between interacting with family
vs. peers. After sibling birth, juvenile cotton-top tamarins, members of a cooperatively breeding species, increase time near parents compared to the period
before sibling birth [Achenbach & Snowdon, 1998]. This increase is due to the
juveniles’ greater time spent near their parents when the parents are carrying
new infants, illustrating the juveniles’ great interest in their infant siblings.
Among humans, sex differences in response to sibling birth occur such that
withdrawal is more common among boys, while dependence is typical for girls
[Dunn & Kendrick, 1980; Nadelman & Begun, 1982]. Captive yearling rhesus
males show initial increases in agitation followed by decreases in time spent
near the mother, whereas females stay near their mothers and achieve proximity
to the new infant as much as they did previously by approaching and grooming
their mothers more [Holman & Goy, 1988].
Defining when the age period of infancy ends and when juvenescence begins
among nonhuman primates has been a source of controversy and has been based
on various criteria, such as the period during which the individual is physically
dependent on the mother/caretakers, the age at which the individual can survive
the death of its mother, the age at weaning, or the interbirth interval [Walters,
1987]. Each of these criteria potentially points to a different age at which infancy ends, with the interbirth interval being the upper limit [Pereira & Altmann,
1985]. As rhesus monkeys are seasonal breeders, the interbirth interval is minimally about 1 year. Thus, at sibling birth, yearling rhesus are making the transition from infancy to juvenescence.
In this study, we ask the following specific questions: 1) to what extent do
mothers and yearlings experience abrupt decreases in proximity and contact patterns upon the birth of a sibling; 2) to what extent are these changes due to
changes in maternal vs. yearling behavior; 3) to what extent do yearlings show
increases in overt distress, contact-seeking behavior, or signs of depression; and
4) to what extent do patterns of change differ for males and females?
All three theoretical perspectives predict that mothers and yearlings will
show abrupt decreases in contact and proximity at the time of the sibling’s birth.
Attachment theory assumes in addition that the agent of separation will not be
the yearling itself; hence, it predicts that 1) mothers will be primarily respon-
196 / DeVinney et al.
sible for decreases in proximity and contact; and 2) yearlings will respond with increases in behavior related to distress, disturbance, and the reestablishment of contact. Parent–offspring conflict theory similarly assumes that the mother will be the
agent of separation as she redirects investment into the new sibling. Hence, it also
predicts that 1) mothers will be primarily responsible for decreases in contact and
proximity; 2) yearlings will respond with increases in behavior related to distress
and the reestablishment of contact; and 3) yearlings will display “regressive behavior,” i.e., reversions to more immature behavior patterns. It sees both reversion and
increases in distress and contact-seeking behavior as dishonest attempts to elicit
additional investment from mothers who may resist, ignore, or acquiesce to their
demands, depending on conditions [Trivers, 1974]. Bateson’s [1994] dynamic assessment approach predicts that 1) mothers will provide a prominent cue to yearlings at
the time of the infant’s birth that predicts or accompanies decreases in levels of care.
Yearlings in low-risk (e.g., food-rich and predator-free) environments, such as Cayo
Santiago, are predicted to respond cooperatively to these cues. For this reason, the
dynamic assessment approach predicts that 2) mothers in low-risk environments
may not be primarily or directly responsible for actual decreases in proximity or
contact with yearlings. Rather, mothers and yearlings may equally share this responsibility or yearlings may even assume the primary role. Similarly, yearlings in
low-risk environments are predicted 3) to show few signs of distress, disturbance, or
contact-seeking behavior. On the contrary, they are expected to show signs of acquiescence and increased behavioral maturity.
METHODS
Study Site and Sample
This study was conducted between April 1994 and July 1995 on Cayo Santiago,
a 15.2-ha island located 1 km from Puerto Rico’s southeast coast. C.R. Carpenter
founded the free-ranging rhesus monkey (Macaca mulatta) colony residing there
by introducing 409 animals from India in 1938. Since that time, individuals have
been added to the population only by birth, although some individuals have been
removed in planned culls. The island population during the entire data collection
period averaged 897 individuals (range = 812–960). The monkeys were predatorfree and were provisioned with high-protein chow supplied from hog feeders inside quarter-acre corrals. Water was available ad libitum. The monkeys were
habituated to human presence, and identification of individual monkeys was facilitated for observers by the monkeys’ tattoos and ear-notches. The population
has been censused daily since 1956. Maternal kinship relationships were known
for all monkeys. (For more information on Cayo Santiago’s history and terrain,
see Rawlins and Kessler [1986] and Sade et al. [1985].)
The monkeys organized themselves into species-typical multi-male, multifemale groups [Lee, 1983b]. We studied two social groups: group R, which averaged 237 animals (range = 212–262) and contained three matrilines, and group
S, which averaged 125 animals (range = 113–134) and contained two matrilines.
Groups R and S formed when group I fissioned during 1985 and 1986. Thus, the
oldest females in each group were, at one time, members of the same social group.
During this study, group S was in the process of fissioning, and group S females
again began associating with group R females. Thus, the subjects of this study
associated both with animals considered to be in their social group and with
another fission-product social group.
We observed 31 subjects whose mothers gave birth to viable siblings when
the yearlings were between the ages of 40 to 67 wk (average inter-birth interval
Yearling Rhesus at Sibling Birth / 197
= 54.36 wk or 380.5 days). Focal subjects were born between 24 November 1993
and 19 April 1994; their younger siblings (10 males, 21 females) were born between 17 December 1994 and 16 April 1995. We observed 19 males (12 in group
R, 7 in S) and 12 females (all in group R). All mothers were multiparous. Subjects were balanced as much as possible for mother’s age and dominance rank.
The study began with 36 subjects and we had initially planned to compare changes
in mother–yearling relationships in families with and without new siblings; however, due to the high fecundity of the mothers (and the deaths of one mother and
one infant sibling), only three families without new infant siblings were available for comparison.
Data Collection
We used focal animal sampling methods [Altmann, 1974] to record the frequencies, durations, and sequences of yearlings’ interactions with all other group
members, observing each subject for three 15-min sessions per wk. During the
focal-animal sessions, we also collected point (instantaneous) time samples at 3min intervals, recording 1) the identities of animals in contact, within 60 cm,
and within 5 m of the subject; 2) the yearling’s and mother’s activities; and 3)
the yearling’s activity level and apparent affective state. The behaviors analyzed
are listed along with their definitions in Table I. Interobserver reliability was
high among observers (Kappa coefficient ≥ .90 [Cohen, 1960]). The day was divided into four time periods: 0700–0930, 0930–1200, 1300–1530, and 1530–1800
AST. The collection of samples was distributed evenly across these time periods
within each month of data collection. The sequence of subjects observed within
each time period was determined by a random order. After the birth of a younger
sibling, data collection was increased to two 15-min sessions per day for 2 wk.
We collected the data on hand-held computers (Micropalm 4000/5000), reviewed
them for typing errors soon after data collection, and later tabulated them within
month-long blocks of time. The month-long blocks were based on the date of the
younger sibling’s birth, using that date as the zero point in a time line and counting out by months from that point.
The annual trapping period, during which all yearlings on Cayo Santiago
were tattooed and ear-notched, and during which our subjects were studied for
physiological parameters, occurred between 17 January and 17 February 1995.
Capture of animals occurred Monday through Thursday weekly. To minimize the
effects of trapping on our data, we collected as much data as possible between
Friday and Sunday of each week. In addition, we waited 2 days before resuming
observations after each subject was released.
Data Analysis
The data analysis focused on 6 mo during the yearling life-stage, specifically
the 3 mo before and the 3 mo after the younger sibling’s birth. The average total
amount of data collected per subject for this study was 24.58 hr (±SD = 31.76
min; range = 23.7–26.3 hr).
Repeated-measures ANOVA techniques [SPSS version 10.0, 1999] were used
to identify significant changes over time in measures related to the yearlings’
affective state and nursing, and in proximity, contact, and agonism between mothers and yearlings. In the repeated-measures design, we entered yearling sex,
mother’s rank, and social group as between-subjects factors, yearling age (in days)
as a covariate, and the level of each behavioral measure across each of the 6-
198 / DeVinney et al.
TABLE I. Behaviors Analyzed and Their Definitions
Behavioral measures related to nipple contact
Time on nipple: percentage of point time samples in which the yearling is on mother’s nipple
Nipple attempts: frequency/hour of successful and rejected attempts by the yearling to gain
access to the mother’s nipple
Nipple contacts: frequency/hour of successful attempts to gain access to the nipple initiated
by the yearling or mother
Rejections: rate per hour of attempts to get on the nipple that are prevented by the mother
Behavioral measures related to proximity and contact
Time in contact: percentage of point time samples in which the yearling is in physical contact
with mother
Time < 60cm: percentage of point time samples that the yearling is within 60cm of the
mother
Time > 5m: percentage of point time samples that the yearling is over 5m away from the
mother
Time out of sight: percentage of point time samples in which the mother and yearling are out
of sight of one another
Approaches to mother: frequency per hour of yearling crossing from more than 60cm away
from mother to less than 60cm from mother
Approaches by mother: frequency per hour of mother crossing from more than 60cm away
from yearling to less than 60cm from mother
Yearling contacts mother: frequency per hour with which yearling makes physical contact
with mother
Mother contacts yearling: frequency per hour with which mother makes physical contact
with yearling
Proportion of mother-initiated contacts: ratio of physical contacts initiated by the mother
divided by total physical contacts initiated by both mother and yearling
Behavioral measures related to maternal aggression and infant distress
Mother threatens: rate per hour of any characteristic threat gesture, e.g., open-mouth threat,
head bob, eye-raising, lunging while staying in place
Mother lunges: rate per hour of mother moving at least three feet toward yearling, or
chasing yearling without making contact with it
Gecker: rate per hour of bursts of staccato vocalizations
Scream: rate per hour of screaming or shrieking
Fear grins/cower: rate per hour of bared teeth grimace and/or lateral flexion of the spine
away from mother
Time passive: proportion of point time samples in which the yearling was stationary; could
be just sitting or self-grooming
Time tense/distressed: proportion of point time samples in which the yearling appeared
physically tense (i.e., muscles tensed) or exhibited agitated behaviors, such as distress
vocalizations
Time depressed: proportion of point time samples in which the yearling was sitting in a
hunched posture, with head hanging down, yet animal is awake
Behavioral measures related to grooming
Mother grooms: duration of stereotyped picking through yearling’s fur
Yearling grooms: duration of stereotyped picking through mother’s fur, Table II
month-long blocks of time (three pre-sibling-birth and three post-sibling-birth)
as the within-subject dependent variables. Probability values for F tests were
adjusted using the Greenhouse-Geisser method when necessary [Greenhouse &
Geisser, 1959]. As a post hoc test to examine when changes occurred within the
6-month period for each behavioral measure, we computed paired t-tests, pairing
sequential months. For measures related to suckling, paired comparisons were
Yearling Rhesus at Sibling Birth / 199
not made for the second and third post-sibling-birth months. Critical values for
the paired t-tests were Bonferroni-corrected such that for nursing-related measures the results were considered statistically significant at P < .016 and for all
other measures at P < .01. All statistical tests were two-tailed.
Because the annual trapping season on Cayo Santiago overlapped with the
birth season, it was necessary to account for possible effects of trapping on levels
of mother–yearling interaction. We wanted to compare yearlings who had experienced sibling birth and trapping simultaneously with those who had experienced
the two events separately. We used the following approach to categorize a
yearling’s experience of trapping: if there were 3 or more weeks overlap between
trapping season and the sibling’s first month of life, then these subjects were
considered to have experienced sibling birth “during” trapping (n = 9). Alternatively, if 3 or more weeks of the sibling’s first month of life were either before or
after the trapping season, then these subjects were categorized as having sibling
birth “before/after” trapping (n = 12).
RESULTS
Proximity and Contact
Fifteen of 31 (48%) of the yearlings were observed on their mothers’ nipples
during the month immediately preceding their siblings’ births, up to within 1
day of sibling birth (seen in two subjects). None was seen on the nipple after the
sibling’s birth. Thus, for some subjects, completion of weaning coincided with the
sibling’s birth, and among these yearlings the mean percentage of time on the
nipple decreased by nearly 50%, from 17% of observation time to 9% of observation across the 3 months preceding sibling birth. For all subjects, time on the
nipple (F3,72 = 18.210, P = 0.000; Fig. 1a), nipple attempts (F3,72 = 21.563, P =
0.000), nipple contacts (F3,72 = 21.333, P = 0.000), and maternal rejections per
hour (F3,72 = 10.045, P = 0.000) all declined significantly across the pre-birth
period (Table II).
Yearlings experienced significant reductions in the proportion of time spent
in physical contact with mothers (F5,120 = 23.707, P = 0.000; Fig. 1a) and within
60 cm of mothers (F5,120 = 2.723, P = 0.041) over the 6-month period. Figure 1a
suggests that mean values of time in contact decreased most rapidly between the
first pre-birth month and the first post-birth month, after which they changed
little. Similar patterns of change were seen for time at a distance of more than 5
m (F5,120 = 26.726, P = 0.000) and for time out of sight (F5,120 = 24.742, P = 0.000;
Fig. 1b) of the mother. Mothers significantly reduced their grooming of yearlings
over the 6 months (F5,120 = 8.647, P = 0.000), and yearlings significantly reduced
grooming of mothers as well (F5,120 = 2.569, P = 0.030).
Changes in Maternal Vs. Yearling Behavior
Rates of approaches by yearlings to mothers (F5,120 = 21.079, P = 0.000) and
rates of approaches by mothers to yearlings (F5,120 = 11.924, P = 0.000) also declined significantly over the 6 months and appeared to decline most rapidly between the first pre-birth and first post-birth months (Fig. 1c). The proportionate
changes in rates of approaches from the first pre-birth to the first post-birth
month were similar for mothers and yearlings, suggesting that each contributed
approximately equally to changes in their proximity relationships. Rates of initiations of contact by both mothers (F5,120 = 7.019, P = 0.000) and yearlings (F5,120
= 11.447, P = 0.000) also declined significantly over the 6-month period (Fig. 1d).
200 / DeVinney et al.
Fig. 1. Means and standard errors for: (a) the proportion of time in contact with the mother and the
proportion of time on the nipple, (b) the proportion of time over 5 m from the mother and the proportion of
time out of sight of the mother, (c) the rate per hour of approaches by the yearling to the mother and the
rate per hour of approaches by the mother to the yearling, and (d) the rate per hour of the yearling making
physical contact with the mother and the rate per hour of the mother making physical contact with the
yearling. The dashed line in the center of each graph indicates the time of the younger siblings’ births. The
time blocks represented along the x-axis are in a format such that “3mPRE” stands for the third month presibling-birth, and so forth.
The decrease in mean rates of contact initiation by yearlings was most dramatic (43%) between the first pre-birth month and first post-birth month. On a
descriptive level, rates of contact initiation by mothers increased for daughters
in the first post-birth month and decreased slightly for sons. The proportion of
physical contacts initiated by the mother (calculated as the ratio of mother
contacts yearling over mother contacts yearling plus yearling contacts mother)
actually increased after sibling birth (F5,90 = 2.464, P = 0.039; Fig. 2a), suggesting that yearlings, not mothers, were primarily responsible for decreases in
contact time.
Rates of maternal threats (F5,120 = 3.415, P = 0.006) and lunges (F5,120 = 2.734,
P = 0.022) directed toward yearlings increased significantly and dramatically
over the 6-month period. Like other measures, the largest changes generally coincided with the birth of the sibling (Fig. 2b). Half of the subjects (52%) were
threatened by their mothers during the observations in the first week post-sibling-birth, and 71% were threatened during the first post-birth month. The yearlings who were not threatened in the first month were already spending less
time near their mothers (within 60 cm) than those who were threatened during
that month (Wilcoxon-Mann-Whitney test, W = 94.5, P = 0.029). Yearlings apparently responded to maternal aggression with significantly higher rates of feargrinning at their mothers (F5,120 = 2.783, P = 0.020; Fig. 2c).
TABLE II. Repeated Measures ANOVA F-values and Paired t-tests for Month-to-Month Comparisons
Behavioral measures
related to
Repeated
measures
ANOVA
F-values
2mpPRE
vs. 1mPRE
1mPRE
vs. 1mPOST
1mPOST
vs. 2mPOST
2mPOST
vs. 3mPOST
–2.05
–4.79***
–5.22***
–2.46
–2.25
–0.91
–1.51
–0.10
–3.46**
–4.45***
–3.44***
–3.95***
–0.08
1.15
–0.22
–0.61
0.09
1.94
0.29
0.02
0.64
–2.20
–0.82
2.53
3.15**
–2.07
–1.63
–0.40
–2.12
–1.36
–4.32***
–1.76
4.49***
5.02***
–5.43***
–4.32***
–4.92***
0.38
3.73***
–0.07
–0.21
1.06
0.37
1.71
0.82
0.30
–1.60
–1.73
–0.21
0.03
–0.93
0.63
–0.50
–0.41
–0.16
–2.48
–0.29
–1.21
1.00
1.15
0.92
–3.81***
–0.75
0.39
–1.00
–0.66
0.76
1.31
–0.34
2.24
3.03**
4.21***
0.64
–1.75
–1.26
0.34
–0.68
–1.24
0.75
–0.66
–0.59
0.60
–0.42
0.13
–0.79
–0.60
–1.13
–2.41
0.12
0.76
–2.85*
–1.23
1.03
–1.05
–0.08
1.24
2.17
Note that repeated measures ANOVAs for behavioral measures related to nipple contact for the third, second, and first pre-sibbirth months and the first post-sib-birth month, df=3,75; for all other repeated measures ANOVAs df=5,120, except for proportion
of mother-initiated contacts df=5,90; for paired t-tests, df=30. Critical values for paired t-tests are Bonferroni corrected.
*P < 0.05; **P < 0.01; ***P < 0.001.
Yearling Rhesus at Sibling Birth / 201
Nipple contact
Time on nipple
18.210***
Nipple attempts
21.563***
Nipple contacts
21.333***
Rejections per hour
10.045***
Proximity and contact
Time in contact
23.707***
Time < 60cm
2.723*
Time > 5m
26.726***
Time out of sight
24.742***
Approach to mother
21.079***
Approach by mother
11.924***
Yearling contacts mother
11.447***
Mother contacts yearling
7.019***
Proportion of mother2.464*
initiated contacts
Maternal aggression and infant distress
Mother threatens
3.415*
Mother lunges
2.734*
Time passive
4.765**
Fear grin
2.783*
Gecker
7.820***
Scream
3.467*
Grooming
Mother grooms yearling
8.647***
Yearling grooms mother
2.569*
t-values
3mPRE
vs. 2mPRE
202 / DeVinney et al.
Fig. 2. Means and standard errors for: (a) the proportion of physical contacts that were initiated by the
mother, (b) rate per hour of maternal threats and maternal lunges, (c) the rate per hour of females’ fear
grins and males’ fear grins, and (d) the rate per hour of geckering and screaming. The dashed line in the
center of each graph indicates the time of the younger siblings’ births. The time blocks represented along
the x-axis are in a format such that “3mPRE” stands for the third month pre-sibling-birth, and so forth.
Distress and Disturbance
Contrary to expectations, overt signs of distress (e.g., screaming and
geckering) decreased significantly over the 6 months (screaming: F5,120 = 3.467,
P = 0.006; geckering: F5,120 = 7.820, P = 0.000; Fig. 2d). The mean proportion of
time yearlings were observed in apparently tense or depressed states was ≤1%
and did not change across the study. Two male yearlings were observed in depressed postures at one time-point sample each. For one male, this occurred 2
days after sibling birth, and represented 1.35% of time during the first week
after sibling birth, and, for the other male, the depressed posture was observed
4 days after sibling birth and represented 1.25% of the first week’s observation
time. What distress was shown apparently was ineffective in eliciting additional care from mothers. In fact, there was a significant negative correlation
between rates of yearlings’ geckering and rates of being approached by mother
in the first post-birth month (Table III). Similarly, there was a significant negative correlation between geckering and time within 5 m of the mother and a
nonsignificant trend toward a negative relationship between geckering and time
in contact with the mother. There was no relationship between geckering and
these measures of care during the pre-birth period. Time in a passive state, a
possible indicator of mild distress, significantly increased across these 6 months
(F5,120 = 4.765, P = 0.001), particularly between the first pre-birth month and
the first post-birth month.
Yearling Rhesus at Sibling Birth / 203
TABLE III. Partial Correlations for Geckering vs. Measures of Mother-Yearling
Interaction, Controlling for Age*
Geckering and
Mother approaches
Time < 5m
Time in contact
3mPRE
2mPRE
1mPRE
1m POST
2mPOST
3mPOST
r=
0.09
(P=0.62)
–0.13
(P=0.50)
0.15
(P=0.42)
r=
0.03
(P=0.87)
0.01
(P=0.97)
0.17
(P=0.38)
r=
–0.29
(P=0.12)
0.02
(P=0.90)
0.20
(P=0.16)
r=
–0.40
(P=0.03)
–0.36
(P=0.05)
–0.35
(P=0.06)
r=
–0.08
(P=0.69)
–0.20
(P=0.29)
0.36
(P=0.05)
r=
–0.28
(P=0.22)
–0.45
(P=0.01)
0.33
(P=0.08)
*P values are given in parentheses.
Abruptness of Change
The fact that many measures of behavior seemed to change most rapidly
between the first pre-birth month and the first post-birth month suggests abrupt
change around the time of the sibling’s birth. This notion is supported by the
results of the paired t-tests between sequential months (Table II). Fourteen of 21
measures (66%) showed highly significant changes between the first pre-birth
and the first post-birth month. No significant changes occurred after that time.
In addition to the changes at sibling birth, some measures showed changes earlier. These included: 1) measures related to the dynamics of nipple contacts (nipple
attempts and nipple contacts), which significantly decreased between the third
and second pre-birth months; 2) time out of sight of the mother, which significantly increased between the second and first pre-birth months; and 3) geckering,
which significantly decreased between the third and second pre-birth months.
Sex Differences
Across the 6 months of analysis, male yearlings spent significantly more time
at a distance of over 5 m from mothers than did female yearlings (F1,24 = 7.191, P
= 0.013), while female yearlings spent significantly more time within 60 cm of
their mothers than did male yearlings (F1,24 = 6.320, P = 0.019). Female yearlings
approached their mothers more than males did (F1,24 = 5.034, P = 0.034) and female yearlings groomed their mothers more than males did (F1,24 = 11.912, P =
0.002). Females, but not males, showed a nonsignificant tendency to fear-grin at
their mothers more frequently after the births of their siblings (F1,24 = 0.299, NS).
Fear-grinning to the mother may have functioned as an appeasement gesture,
facilitating the females’ efforts to stay near the mother. There were no significant
two-way interactions between the factor sex and the various behavioral measures,
suggesting that patterns of change over time did not vary significantly by sex.
Rank and Group Differences
Yearlings of low-ranking mothers spent more time in contact with their mothers (F1,24 = 5.010, P = 0.035) and initiated physical contact more frequently with
their mothers (F1,24 = 5.582, P = 0.027) than did yearlings of high-ranking mothers.
Low-ranking mothers themselves made contact with their yearlings more frequently
than did high-ranking mothers (F1,24 = 5.256, P = 0.031). Before sibling birth, highranking mothers groomed their yearlings more than did low-ranking mothers, and
after sibling birth, low-ranking mothers groomed their yearlings more than did highranking mothers (F1,24 = 6.063, P = 0.021). Across all 6 months, yearlings of low-
204 / DeVinney et al.
ranking mothers groomed their mothers more than did yearlings of high-ranking
mothers (F1,24 = 13.584, P = 0.001). Group S yearlings made more nipple attempts
(F1,24 = 6.893, P = 0.015), made more nipple contacts (F1,24 = 8.585, P = 0.007), and
geckered more (F1,24 = 8.390, P = 0.008) than did Group R yearlings.
Trapping Effects
Contrary to expectations, we found no evidence of increased distress when
trapping coincided with sibling birth (i.e., for the “during” monkeys) compared to
when sibling birth occurred outside the trapping period (“before/after”).
Yearlings Without Younger Siblings
Our sample included only three families in which no new sibling was born. As
a method to assess whether measures of mother-infant interaction for the no-sib-
Fig. 3. Means (squares) and 95% confidence intervals of the mean for the with-sibling group and means
(filled circles) and raw data points (open circles) for the three no-sibling yearlings for: (a) proportion of time
on the nipple, (b) proportion of time in contact with mother, (c) proportion of time out of sight of the mother,
and (d) rate of yearlings’ approaches to mother. Asterisks along the top of each panel indicate those months
in which the three data points for the no-sibling group fell outside the 95% confidence interval of the mean
for the with-sibling group.
Yearling Rhesus at Sibling Birth / 205
ling families differed from those for families with new siblings, we plotted the 95%
confidence interval of the mean for measures of proximity and physical and nipple
contact for the with-sibling group, and then examined whether the data points for
the three no-sibling focals fell outside that range. The mean age at sibling birth
(54.4 wk) was used to determine where to divide the data into months for the nosibling yearlings. For the no-sibling focals, 95/117 (81.2%) of the comparisons (3
infants × 3 mo × 13 measures) before sibling birth and 104/117 (88.9%) of the
comparisons after sibling birth were outside the confidence interval. The yearlings
without siblings generally exhibited higher levels of association with their mothers across these 6 months, with the differences between groups being stronger in
the post-sibling-birth period, as illustrated for four behaviors in Fig. 3.
DISCUSSION
Rhesus mother–yearling relationships changed markedly during the 6-month
period surrounding the siblings’ birth. Levels of maternal care decreased across
this period in many ways, including the termination of nursing and the reduction of maternal grooming, contact, and proximity (the latter being “care” in that
proximity to the mother can provide protection from conspecific aggression
[Maestripieri, 1993] and opportunities for observational learning [Pereira &
Altmann, 1985]). Since these are developmental data, at the outset one would
anticipate some behavioral change over time as the subjects became more independent of their mothers across these 6 months. What these data seem to point
to, however, is a discontinuity, or abrupt transition, toward accelerated independence from the mother associated with the birth of a younger sibling. Most measures showed their largest and most consistent changes between the first
pre-sibling-birth month and the first post-sibling-birth month (Table II).
A comparison between yearlings that did and did not experience sibling
birth could provide further suggestive evidence that the changes observed in
yearlings with new siblings represented abrupt transitions associated specifically with the sibling’s birth rather than simple age-related shifts toward independence. Unfortunately, in this well-provisioned and relatively unmanipulated
colony, our sample yielded only three families without new siblings to compare
with the yearlings with siblings, and of course we were unable to control for
possible differences in quality [Clutton-Brock, 1991] or responsiveness [Berman
et al., 1993] between mothers who did and did not give birth again. Nevertheless, in our sample the yearlings without siblings exhibited higher and more
constant levels of association with the mother compared to yearlings with siblings across these 6 months.
Attachment Theory
From the view of attachment theory, the birth of a younger sibling is a
normal yet stressful transition in which older siblings experience a reduction
in maternal care to which they often respond with behavioral distress [Teti et
al., 1996], particularly if they are insecurely attached. Evidence for increases
in yearling distress and/or disturbance was lacking or, at best, equivocal. All
measures of overt distress decreased rather than increased with the birth of
the sibling. Time spent in a passive state increased in the month after sibling
birth, but the extent to which passivity represents mild distress vs. a simple
reorganization of yearlings’ time budgets is unclear. Finally, the two males who
assumed depressed postures [Kaufman & Rosenblum, 1967] did so only fleet-
206 / DeVinney et al.
ingly and only during the first week after the sibling’s birth. Hence, while some
yearlings may have been disturbed briefly, in general yearlings showed only
mild or no disturbance and distress in response to their siblings’ births. Since
we did not attempt to assess the security of the mother–yearling attachment,
we cannot evaluate whether the low levels of distress observed at sibling birth
are related to yearlings being securely attached to their mothers or, alternatively, whether the theory’s prediction of distress at this “partial removal” of
the mother should be considered unsupported. Attachment theory also would
predict that the mother will be the agent of separation, meaning that she would
be responsible for decreases in proximity and contact, and that yearlings should
exhibit behavior related to trying to reestablish contact. Although mothers behaved more aggressively and punitively after the sibling’s birth, they did not
take primary responsibility for decreases in proximity and contact. Indeed, mothers actually increased the proportion of contacts they initiated toward yearlings, and increased the rate of contact initiations with daughters. Thus,
attachment theory predictions regarding the agent of change in proximity and
contact were not supported.
Parent–Offspring Conflict
Parent–offspring conflict theory would view sibling birth as a reallocation
of maternal investment by mothers from the yearling to the new sibling. Even
if we assume that the changes in care provided by mothers to year-old offspring before and after sibling birth represent changes in maternal investment
that could theoretically trigger genetic conflict between mothers and yearlings
[Trivers, 1974], we are unable to provide strong support for this perspective. As
discussed above, two key predictions for this perspective were not confirmed by
the results of this study: 1) mothers did not take primary responsibility for
bringing about decreases in proximity and contact, and 2) yearlings showed
little or no increases in behavior related to distress or contact-seeking. What
distress was shown apparently did not serve to elicit additional care from the
mothers. Indeed, there were negative correlations between both the rates of
yearlings’ geckering and of being approached by their mothers in the first postbirth month and time within 5 m of the mother, suggesting that geckering may
have been a reaction to decreases in maternal care rather than a mechanism
for soliciting it, or that mothers actively resisted attempts to elicit “extra” care.
Finally, we saw no signs of “regression” to an earlier state of development.
Trivers [1974] suggested that youngsters might mimic or imitate earlier stages
of development in order to elicit the higher levels of care typically given to
younger individuals. While there is some support for this interpretation of
children’s regressive behaviors [Stewart et al., 1987], we found no evidence for
this tactic among year-old monkeys.
Dynamic Assessment
Bateson’s alternative parent–offspring dynamic assessment perspective would
predict that transitions in parent–offspring relationships would be determined
by mutual honest signaling regarding the mother’s ability to provide care and
the offspring’s need for care. Offspring in low-risk environments would be expected to respond cooperatively to mother’s signals and to accelerate rates of
development when mothers are unable to continue high levels of care. Although
our data do not provide a definitive test of this perspective, we believe our find-
Yearling Rhesus at Sibling Birth / 207
ings point to its potential usefulness for guiding future research in this area.
Certainly, two key predictions were supported: 1) yearlings played roles equal to
or larger than mothers in bringing about decreases in proximity and contact,
and 2) yearlings showed little distress or disturbance at the sibling’s birth. A
third key prediction was that mothers would provide yearlings with prominent
cues indicating that the period of greatest maternal investment was over [Bateson
et al., 1990]. Although further research is needed, we would like to raise the
hypothesis that the abrupt increases in maternal aggression after the sibling’s
birth may have represented such cues, although other changes, such as the appearance of the new sibling itself, or more subtle cues from the mother may also
be worthy of consideration.
Maternal aggression was almost entirely in the form of mild threats and
lunges rather than contact aggression. Hence, it provided conspicuous stimuli to
yearlings with little potential for actual injury. The increase in this kind of maternal aggression at the time of the sibling’s birth was abrupt and dramatic;
threats in particular increased by a factor of more than 3 and remained elevated
during the first 3 post-birth months. Yearlings apparently responded with increased fear-grinning directed towards mothers and with decreased attempts to
remain near and make contact with them, but not with increased distress, disturbance, or contact-seeking. In this sense, mothers may have instigated the transition in their relationships with their yearlings, but rather than protesting or
attempting to cling, yearlings cooperated with mothers in bringing about changes
in patterns of proximity and contact more typical of juvenile rhesus monkeys.
This is in contrast to reactions by Cayo Santiago rhesus infants when their mothers resume mating, an event that takes place approximately 6–9 months earlier
than sibling birth [Berman et al., 1993, 1994]. At that time, rates of maternal
punishment (defined as hits, bites, slaps, and pushes) increase abruptly, and the
infants’ time in proximity and contact with the mother decrease abruptly. However, changes in the relationship are due primarily to decreases in mothers’ propensities to seek contact, and the infants respond with dramatic increases in
distress and contact-seeking behavior. Thus, compared with youngsters approximately 6–9 months younger, we suggest that the yearlings’ behavior represented
an acquiescence to their mothers’ increased threats and an abrupt increase in
behavioral maturity rather than an attempt to restore contact or elicit more care.
One potential concern with this interpretation is that Holman and Goy’s [1988]
study of captive rhesus reported no increase in maternal aggression with the
birth of a sibling. Further research is needed to determine whether this discrepancy in findings indicates that 1) maternal aggression is not the salient cue, 2) a
dynamic assessment approach is not useful in interpreting the sibling transition,
or 3) different cues or different theoretical perspectives may apply in different
environments.
Barrett and Henzi’s [2000] analysis of weaning tantrums in infants of
nonseasonally-reproducing wild baboons also provides preliminary support for a
dynamic assessment model over parent–offspring conflict theory, in that tantrums
appeared to be honest signals of need to which mothers responded with increased
nursing. However, Barrett and Henzi describe a primarily passive role for mothers in which signaling takes place primarily from infant to mother. Infants are
hypothesized to take the initiative to reduce levels of care before mothers need to
reallocate care to younger siblings. We suggest that this scenario is not likely to
occur in food-rich, seasonally-reproducing species because mothers operate within
a more constrained reproductive schedule. Rich food resources open the possibility of yearly reproduction provided mothers are able to conceive during the mat-
208 / DeVinney et al.
ing season following their current infant’s birth. However, this often requires
initiating reductions in levels of care both when they resume mating [Gomendio,
1989; Berman et al., 1993] and when the new sibling is born. Failure to do so is
likely to be costly in that females will have to delay reproduction for an additional year. Hence, one would expect to find signaling by both infants and mothers in these circumstances. In younger infants, active care reduction also appears
to be necessary.
Sex Differences
The sex differences in behavior we observed were consistent across the 6
months of observation. Males spent more time at a distance greater than 5 m
from their mothers than did females, and females spent more time within 60 cm
of their mothers and approached their mothers more than did males. Holman
and Goy [1988] found sex differences in rhesus mother-yearling proximity, but
only after sibling birth; thus they suggested that the males’ “disengagement”
from their mothers was triggered by sibling birth. Berman et al. [1994] found
that when Cayo Santiago rhesus infants are approximately 6 months old and
their mothers return to estrus, infant sons suddenly spend more time at a distance (>5 m) from their mothers; however, it is unclear whether this pattern
persisted from the time of first estrus until the 3 months preceding sibling birth.
The sex differences in behavior observed in these yearlings foreshadow the pattern of male peripheralization typical of rhesus social organization [Colvin, 1983];
however, it is unknown why this pattern would begin earlier in free-ranging groups
than in captive groups.
In summary, after sibling birth yearling rhesus monkeys experienced marked
reductions in maternal care and increases in maternal aggression, yet exhibited
little distress. We suggest that maternal aggression served as a cue regarding
decreased levels of care, and that yearlings acquiesced to the reduction in care,
exhibiting increased independence. These findings are in concert with the predictions of dynamic assessment approaches to the sibling birth transition, more so
than with the predictions of attachment theory or parent–offspring conflict theory.
Dynamic assessment approaches to parent–offspring relationships have only recently been applied to studies of primates; thus, future work should address
whether this approach has value in addressing the sibling birth transition in other
environments and species, and address the relevance of maternal aggression as a
cue regarding reductions in maternal care among nonhuman primates.
ACKNOWLEDGMENTS
We thank John Berard and Matt Kessler for permission to work on Cayo
Santiago. We thank the Wenner-Gren Foundation for Anthropological Research
(grant to B.J.D.) and the National Institute of Child Health and Human Development through the Laboratory of Comparative Ethology, Division of Intramural
Research. This investigation was supported in part by an Animal Resources
Branch Program Award, RR-03460, from the National Center for Research Resources, National Institutes of Health and the University of Puerto Rico, Medical
Sciences Campus. We are grateful to Kristin Abbott, Jennifer Rodger, and Steve
Ross for assistance with the behavioral observations. Many thanks to those who
wrote the computer programs used in this research: Helen Ball, Michael Hulett,
and Ken Whang. We thank Stephen Suomi and three anonymous reviewers for
their helpful suggestions regarding this manuscript.
Yearling Rhesus at Sibling Birth / 209
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