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Analysis of rhesus monkey vocalizations Maturation-related sex differences in clear-call frequency.

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Analysis of Rhesus Monkey Vocalizations :
Maturation-related Sex Differences in
Clear-call Frequency ’
Department o f Psychology, Department o f Behavioral Biology, and
California Primate Research Center, Davis, California 9561 6
In the first of two studies six like-sexed pairs of rhesus macaques
early in their third year of life were observed for two days, then separated for
two days, and finally reunited for two days. In the second, about nine months
later, the same animals were paired across sex and were separated in a similar
fashion to that in the previous study. The number of distress-related clear calls
uttered by females remained stable through both studies, but the males showed
a decrease with age in this behavior. The results of these two studies are compared with other research in which maturation-related sex differences have become apparent. These comparisons suggested that decreases in the production of
clear calls accompany the onset of puberty. Since the females which were involved in our research reached puberty shortly before the time of our first study
and the males did so shortly before the second, the decreases in male clear-call
rate which we observed across these two studies appears to have been linked with
peri-pubertal influences.
The dynamics of mother-infant attachment formation and disruption has been a
popular research topic for some time (cf.
Bowlby, ’58; Elliot and Scott, ’61), and
some of the most significant research in
this area has involved the use of nonhuman primates as subjects (DeVore, ’63;
Hinde, Spencer-Booth, and Bruce, ’66; Jay,
’63; Seay, Hansen and Harlow, ’62; Simons, Bobbitt and Jensen, ’67). Macaques,
especially rhesus macaques, have received
the most attention. A common research
strategy which has been used in the testing of the strength of attachment of mother-infant dyads has been observation of
the responses to separation of sociallybonded animals. The most reliable correlate of mother-infant separation has been
a distinctive vocal sound emitted by both
(Scollay, ’ 7 0 ) , which in its simplest form
is tonal and usually of rather long duration
relative to most other macaque vocalizations. These sounds vary in form but generally fit into a class of calls designated
by Rowel1 and Hinde (’62) as “clear calls”
because of their tonal structure. They have
also been referred to in the literature as
AM. J. PHYS.ANTHROP., 38: 4 6 3 4 6 8 .
“coos” (Seay and Harlow, ’65) and “whoo
calling” ( Spencer-Booth and Hinde, ’ 6 6 ) ,
among other names.
While clear calls occur in many contexts
other than separation, few situations seem
to be as closely correlated with these
sounds as are those involving separation.
Consequently, clear calls have come to be
used by many laboratory investigators as
indicators of separation distress and therefore of the strength of social-emotional
bonds. This measure has been included as
part of our continuing examination of social interactions in rhesus macaque dyads
of various ages and both sexes in a series
of studies in which the incidence of various behavioral elements has been monitored. Some interesting age and sex differences have emerged from this research.
1 The research reported here was supported in part
by the following U. S. Public Health Service/NIH
grants: MH19760 and MH17425 to G . Mitchell; HD04335 to the Department of Behavioral Biology, School
of Medicine; RR00169 to California Primate Research
Center (previously The National Center for Primate
Biology); and HD06367 to William Mason.
ZRequests for reprints of this paper should be addressed to J. Erwin, Department of Psychology, University of California, Davis, California 95616.
In this paper, only the results concerning
clear calling are reported from two recent
separation studies and are discussed in the
light of other investigations conducted in
our laboratory and elsewhere. The complete results of these two studies have been
reported elsewhere (Erwin et al., ’71;
Erwin et al., ’72).
Twelve rhesus macaques, six males and
six females, were the subjects for our studies; all were laboratory-born. Each subject
had experienced two brief experimental
separations from its mother in infancy
(Scollay, ’70) and was weaned between
seven and ten months of age. In addition,
each animal had been paired briefly,
shortly after weaning, with strangers of
the same age and of both like and opposite sex (Stevens and Mitchell, ’72),
none of which were also subjects of our
When our 12 subjects were 9 to 12
months old, they were matched within the
group for age and sex and paired; age differences within pairs ranged from one to
ten days. Each pair was housed individually in a l m X l m X l m cage and had no
physical contact with other animals during a period of about 17 months before
the initiation of the separation study described. The six like-sex ( 3 male, 3 female)
pairs of subjects ranged in age from 26 to
29 months when they were separated.
All observations were made in a l m X
Im x 2m test cage with three walls of wire
mesh and the front one of clear Plexiglas.
A sliding translucent Plexiglas partition
made it possible to divide the cage into two
equal segments the size of the home cage.
Observations were recorded by using two
clock-counter recording devices described
in detail elsewhere (Odom, Mitchell and
Lindburg, ’70).
Before data recording began, each pair
of animals was placed in the test cage for
a one-day adaptation period. A six-day
study of each pair following the adaptation
period consisted of two days of presepara-
tion, two days of separation and two days
of reunion. Two observers using clockcounter devices recorded the frequencies
and durations of 20 behaviors; each observer scored the behavior of one member
of each pair. The behaviors recorded were
grouped into classes of five behaviors each;
and two five-minute samples of each behavioral class were recorded on each of the
six data collection days, which were supplemented by the taking of extensive films
and notes. A base rate for comparative
purposes was established during the twoday preseparation phase of the study. On
the third day the partition was slid into
place, dividing the cage and separating the
animals, and was left in place until the
fifth day of the study when it was removed
to allow reunion for two days. After the
two-day reunion period, the subjects were
removed from the test cage and placed in
separate home cages.
The frequency of clear calls increased
dramatically at separation, as expected,
and decreased at reunion to a level below
that of the preseparation phase. During
preseparation, separation and reunion
phases, respectively, the mean number of
“coo”-vocalizations per animal was 11.75,
59.00, and 5.25 ( p < 0.05, ANOVAR).
Most of the animals called much more
frequently on the first day of separation
than on the second day. The intensity of
the “coo”-vocalization seemed to be much
greater immediately following separation
than at any other time. It was common
during the period shortly after separation
for calls to begin as smooth tonal sounds
and to increase in pitch and intensity until
they became loud, harsh screeches. There
were no apparent sex differences in rates
of clear calling in this study.
The same 12 rhesus macaques were
used at ages 34 to 37 months as subjects
for this later study which was conducted
about nine months after the first one. During part of the intervening period, eight
of the animals had been involved in another study in which they were paired for
two months with infants (Brandt and Mit-
chell, ’73) ; however, all subjects had been
again housed alone for a t least three
months before the beginning of this study.
The same test cages and data acquisition devices were used in study two as in
study one.
In this study males and females were
paired in a pre-test phase for one, two,
or three weeks before separation. Observers recorded data in a manner similar to
that described for the first study, except
that 50 behaviors grouped in five classes
were recorded in one five-minute sampling
period per class per day. Again a one-day
test-cage adaptation period was followed
in order by two-day phases of preseparation, separation, and reunion. Data were
also collected in the home cages of the
subject pairs for two days during each
week of the pre-test-cage phase of the
study and for two days per week for two
weeks following the test-cage phase. Films
and notes supplemented clock-counter
Even with the short periods of time allowed in this study for attachment formation, the rate of “coo”-vocalizations increased significantly during the separation
phase for all except three animals. The
mean number of clear calls per animal
during preseparation, separation, and reunion phases was 4.50, 15.58, and 11.67,
respectively ( p < 0.05 ANOVAR). It
should be noted that two ( a male and a
female) of the three animals showing no
increase in vocalization at separation were
both members of dyads paired for only one
week; the female, however, vocalized frequently during the reunion phase. The
high reunion mean is therefore a reflection
of the behavior of one animal that accounted for more than 80% of the calls
occurring during this phase.
During this study males vocalized much
less often than did females. The mean
number of clear calls during the test-cage
period of the study was 5.42 for males and
17.50 for females ( p < 0.05 Mann-Whitney U ) . Few clear calls occurred during
the other parts of the study. A comparison
of the overall rates of clear calling in study
one, when the animals were a little more
than two years old, with the rates i n study
two, when the subjects were about three
years old, presents a n interesting contrast.
Since a n accurate comparison of the results of our two studies required a n adjustment for the different time-periods
monitored, the clear-call rates are expressed in figures 1 and 2 as the mean
number of vocalizations per animal per
minute. The adjusted mean values for twoand three-year-old males were 1.20 and
0.36, respectively, and the respective
means for two- and three-year-old females
were 1.33 and 1.17 (see fig. 1 ) .
The relative rarity of clear calling by
adult male rhesus macaques has been
rather well established (Rowel1 and Hinde,
’62) although clear calling is common
among juvenile males. The data support
our guess that there is a decrease in clear
call rate among males around the time of
the onset of puberty. It is interesting that
the two males that vocalized least at three
years were also the only ones that succeeded in impregnating their female partners.
Although adult females emit clear calls
more,often than do adult males, the fullyadult female clear-call rate is much less
than that of juveniles. This statement is
Fig. 1 Clear-call rates of male a n d female
rhesus macaques during the third year of life.
borne out by a recent study of attachment
in rhesus consort pairs (Maple, Risse and
Mitchell, unpublished) and by a later experiment using ten of our 12 subjects at
ages between 42 and 48 months (Erwin,
unpublished data). A decrease in male rate
of clear-calling conforming to their average age at onset of puberty ( 3 years) was
demonstrated in the previously.mentioned
experiment which intervened between our
two studies (Brandt and Mitchell, in press)
involving the pairing with infants of eight
of our subjects at ages of approximately
34 to 37 months. The decreases observed
in female clear-calling rates were less
Fig. 2 Clear-call rates of male and female
closely related to pubertal changes, which rhesus macaques during the first three years of
occur in females a year earlier than in life.
males. The fact that the females were just
entering puberty at the time of our first the change of rate of clear-calling with age,
study, however, may explain the absence as shown in figures 1 and 2, were approxiin our data of significant sex differences, mately parallel except during most of the
since previous studies that included the third year of life, the level of vocalizations
same subjects showed definite sex differ- in the study two two-year-old post-pubertal
ences in clear-calling rates even at the very females must have already been reduced
earliest ages tested ( 2 , 3. 5, or 5 months; to approximately the same level as that of
Scollay, ’ 7 0 ) , as well as a n increase with the still pre-pubertal males.4 When correage for both sexes (Stevens and Mitchell, lated with maturation stage, therefore, the
’72). The Stevens and Mitchell study (’72) changes of rate would be consistently pardescribed previously, where the subjects allel for the two sexes. The females, howwere still less than a year old, showed a n ever, seemed to undergo further decrease
even stronger sex difference than for Scol- during the fourth year of life, as indicated
lay’s young infants, as well as a rate of by their responses during a second separaclear-calling for both sexes higher than at tion from like-aged males. Other evidence
supports the point of view that females
any other age studied.
This result is not surprising since juve- may continue gradually to decrease their
nile macaques, both in the field (cf. Lind- emission of calls during early adulthood.
burg, ’71) and in the laboratory (Grimm, For example, it has been repeatedly dern’67), have also been shown to clear-call onstrated that primiparous mothers “coo”more frequently than either young infants vocalize more than do multiparous mothers
or adults.? The early-age overall increase (Seay, ’66; Mitchell and Brandt, ’70; Scolwith age in infants’ “coo”-calling rates lay, ’70). The age of the mothers was not
found by Scollay (’70) corroborated the re- controlled, but primiparous mothers are
sults of another study (Mitchell, ’68) in usually younger than their multiparous
which the behavior of 32 mother-infant counterparts. This difference may be due
dyads during the infants’ first six months primarily to emotional factors directly rewas monitored. No significant sex differ- lated to the amount of maternal experience
ences in the infants’ coos were observed in of primiparous mothers relative to multithe latter, however, perhaps because the parous mothers.
Clearly there are many other factors
pairs were not separated as were Scollay’s.
In general, these comparisons show other than sex and chronological age/
sharp increases in clear-call frequency dur- maturation stage associated with clear-call
ing the first year of life and sharp de3 Nishimura (’72) reported similar age-related difin rates of clear calling among Japanese macreases during the second year for both ferences
caques (Macaca fuscata).
sexes. with the decrease for males continu4 Nishimura (personal communication) also found
rate. of clear calling among female Japanese maing during their third year (fig. 2). Since that
caques decreased at an earlier age than among males.
production in rhesus macaques and related
species. However, it seems obvious that
some of the most influential factors are
those that are operative in many situations.
Sex and stage of maturation seem to be
two of these factors influencing even such
capricious behaviors as rhesus macaque
clear calls.
Through our studies and comparisons
with similar research, we have demonstrated that, at least under conditions of
separation, females consistently clear call
more frequently than do males, except
during the time-period when females have
already reached puberty and males have
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sex, vocalizations, monkey, differences, rhesus, maturation, call, frequency, analysis, related, cleary
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