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Developmental changes in mother-offspring grooming in Japanese macaques.

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American Journal of Primatology 3757-64 (1995)
BRIEF REPORTS
Developmental Changes in Mother-Offspring Grooming
in Japanese Macaques
YASUYUKI MUROYAMA
Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan
A cross-sectional analysis was made of developmental changes in motheroffspring grooming in Japanese macaques, Macaca fuscata. When offspring were immature, time spent grooming by their mothers decreased
with offspring age. Soliciting by offspring increased steadily with age, in
contrast to their successful soliciting, which decreased gradually until
early adolescence. This is in accord with the hypothesis that grooming is
one form of post-weaning maternal investment, which may entail behavioral conflict between mothers and immature offspring. On the other
hand, mothers spent much more time for grooming of their adult female
offspring than for their adolescent male and female offspring. It is argued
that grooming by mothers may shift from a form of maternal investment
in their offspring to a benefit to be exchanged reciprocally with them.
0 1995 Wiley-Liss, Inc.
Key words: grooming, soliciting, developmental changes, behavioral
conflict, post-weaning maternal investment
INTRODUCTION
In most mammalian species, females allocate most of their reproductive effort
to raising their offspring and ensuring their survival through pre-weaning maternal investment, whereas males devote most of their effort to mating [Trivers, 1972,
1985; Kurland & Gaulin, 19841. Extended post-weaning maternal care is also
significant for slowly reproducing mammals such as primates, because the survival of each offspring represents a substantial proportion of a female’s reproductive output [Altmann et al., 1988; Cheney et al., 19881. In these species, it is likely
that mothers invest in post-weaning offspring for considerably prolonged periods
in various forms, e.g., support in agonistic interactions and protection against
predators [Dunbar, 19881.
To examine this hypothesis, I made a cross-sectional analysis of developmental
changes in mother-offspring grooming in Japanese macaques (Macaca fuscata).
Social grooming is the most common affiliative behavior in nonhuman primates,
especially between mothers and offspring [Goosen, 1987; Gouzoules & Gouzoules,
19871. Grooming may serve to remove ectoparasites [Hutchins & Barash, 1976;
Received for publication September 16,1994;revision accepted February 27, 1995
Address reprint requests to Yasuyuki Muroyama, Primate Research Institute, Kyoto University, Inuyama, Aichi, 484 Japan.
0 1995 Wiley-Liss, Inc.
58 I Muroyama
McKenna, 1978; Barton, 1983; Boccia, 1983; Tanaka, 19931 and to reduce tension,
anxiety, and social stress [Terry, 1970; Schino et al., 1988; Boccia et al., 1989;
Maestripieri et al., 19921, which can have detrimental effects on the immune
system [Sapolsky, 1982; Alberts et al., 19921; thus it may be of benefit to the
recipient, in particular, young and vulnerable animals, in terms of hygienic and
psychophysiological functions. Therefore, grooming might be one of the forms that
post-weaning maternal investment could take.
Mothers are expected to groom their offspring most frequently when they are
young, if grooming is a form of post-weaning maternal investment. Indeed, previous studies have reported that grooming given by mothers decreases as offspring
age [Kurland, 1977; Cheney, 1978; Fairbanks & McGuire, 19851. Decreases in
grooming given by mothers, however, may not necessarily correspond to decreases
in grooming demanded by their offspring. Trivers’ theory predicts that disagreement between parents and offspring over the amount of parental investment a t the
genetic level should be expressed at the behavioral level [Trivers, 19741. If the
optimal level of grooming for a mother does not coincide with that of her offspring,
the result may be behavioral conflict in grooming interactions; this may be characterized by soliciting behavior by offspring and rejecting behavior (no responding
with grooming) by mothers, like weaning conflict [Nicolson, 1987; Gomendio,
19911. In the present study, I used these behavioral measures to determine
whether or not behavioral conflict over the the amount of grooming occurs between
mothers and offspring, and to assess until when mothers provide grooming as
maternal investment.
MATERIALS AND METHODS
Subjects
The present study involved one of the two troops of Japanese macaques that
inhabit Koshima, Miyazaki, Japan, over a total of 4 months in 1985-1986. Kin
relationships among the members of the troop, who had been well habituated and
identified, were known. When I started the study the troop consisted of eight adult
males (> 6 years old), 28 adult females, seven adolescent males (4-6 years old),
four adolescent females, nine juvenile males (1-3 years old), six juvenile females,
and four infants (< 1year old). From these individuals, I chose four adult females,
one adolescent male, and one adolescent female as target animals (see Table I).
Two adult females had two offspring and the other two had four. Each of the
adolescent individuals had a mother. Consequently, 14 mother-offspring pairs
were observed during the study period.
For each target animal, I undertook a total of 60 h of observation by the focal
animal sampling method [Altmann, 19743. Focal animal sessions lasted all day
long, when possible. Whenever a focal session was interrupted, I resumed it at
approximately the same time on another day. Thus, I scheduled observation hours
such that they were almost evenly distributed between 0700 and 1700 h.
Behavioral Categories
During focal sampling, I recorded the occurrence and duration of grooming
bouts, together with the identity of the partner. Whenever I observed soliciting
prior to the occurrence of a grooming bout, I also recorded it. A grooming bout was
defined as a continuous act of picking by one animal through the fur of another
without pauses of longer than 1sec. Soliciting was defined as presenting the neck,
face, rump, dorsum, ventrum, or flank, or lying down in front of one animal from
whom another is soliciting grooming [Oki & Maeda, 19131. When an animal who
Adult
Adult
Adult
Adult
Adolescent
Adolescent
URI
KED
GAK
TUT
MBR"
MMJ"
5
1
3
8
18
22
Rankb
4
2
2
4
1
1
No. of
pairs
1F
1F
Adult
(>6 yr)
1F
1M
1F
1M
1F
1M
1F
1F
Juvenile
(2-3 yr)
Adolescent
(4-6 yr)
*M: male; F: female.
"MBR and MMJ had a mother and two siblings, respectively.
bRanks of mothers are given in cases of MBR and MMJ.
Age class
Subject
1F
1M
1F
Yearling
(1yr)
Age and sex of offspring in pairs
1M
Infant
(<1 yr)
14.12
8.91
8.86
8.88
2.16
8.65
5.93
5.52
5.49
3.30
5.17
2.54
90.8
77.7
54.6
91.1
-
-
89.5
86.4
74.5
97.7
-
-
Received
Given
Given
Received
Grooming with
offspring (%)
Time spent grooming
(miru'hr)
TABLE I. Summary of Mother-OffspringPairs and of Grooming Given and Received by Each Focal Animal*
60 I Muroyama
had solicited another was groomed by the second animal within 1 min, it was
concluded that the soliciting was successful.
Data Analysis
In order to examine the occurrence of behavioral conflict between mothers and
offspring, I analyzed the total duration of grooming, the percentage of grooming
bouts preceded by soliciting, and the percentage of successful soliciting during the
total study period as a function of offspring age. In the present study, each focal
adult female was involved in two or four mother-offspring dyads (see Table I), and
thus the results could be affected by “litter effects” [Martin & Bateson, 19861.
However, the small sample size (each female has three immature offspring at
maximum) did not allow to analyze each female’s data separately and pool the
individual P values. Therefore, I used tentatively both the values of each dyad (N
= 14) and the median values for each age (N = 7) for statistical tests, in order to
see overall trends. Data from dyads in which I observed less than six grooming
bouts or soliciting were omitted from the analysis concerning soliciting and successful soliciting.
Kendall rank correlation tests and Wilcoxon Signed Rank Tests were used.
Corrections for ties were made, when necessary. All probabilities reported are
two-tailed.
RESULTS
Time Spent Grooming of Offspring
Among all six focal animals, adult females spent, on average, 17.0%(N = 4,
range: 14.8-23.5%) of their observation time for social grooming given to, and 8.0%
(N = 4, range: 5.5-9.9%) for grooming received from, the members of the group
(Table I). Most of their grooming given and received was likely to be devoted to
their offspring, although the percentages varied with the number and the age-sex
class of their offspring.
Developmental Changes in Grooming Rates
Grooming given by mothers appeared to decrease gradually with offspring age
from 1 year to adolescence (Table 11).With one exception (URI’s case), each mother
groomed her younger immature offspring more often than her older immatures.
However, two adult female offspring were groomed a t the same high rate as infant
and yearling offspring. On the other hand, grooming of mothers by their offspring
appeared to increase until early adolescence, although there was great variance
between individuals (Table 11). Both male and female offspring in late adolescence
were less likely than juvenile and early adolescent offspring to groom their mothers, whereas adult female offspring groomed more frequently than late adolescents.
Soliciting and Response to Soliciting
Infant and yearling offspring received nearly all their grooming without soliciting from their mothers (Table 11). The percentage of solicited grooming increased steadily with offspring age, reaching more than 65% in mother-adult female offspring dyads. With one exception (URI’s case), each mother was likely to
be solicited more frequently by its older offspring than by its younger. In contrast,
while the percentage of soliciting by mothers varied with offspring age, there was
no linear relation (Table 11).
Offspring attempts to be groomed were gradually less successful with offspring
age (Table 11). The decrease in successful soliciting continued until early adoles-
Development of Mother-OffspringGrooming f 61
TABLE 11. Rate of Grooming, Percentage of Solicited Grooming, and Percentage of
Response to Soliciting in Each Mother-OffspringGrooming Dyad
Grooming by mothers
Grooming by offspring
Age and sex Rate of Solicited Successful Rate of Solicited Successful
of offspring grooming grooming soliciting grooming grooming soliciting
(%)
(%)
(min/hr)
(%I
(%)
(vrs:sex)
(minhr)
Subiect
~
URI
TUT
MBR
URI
TUT
GAK
MMJ
KED
URI
TUT
KED
URI
GAK
TUT
28:F
28:F
6:M
6:M
6:F
4:M
4:F
4:F
3:F
2:F
1:M
1:F
1:F
O:M
Kendall's tau for dyads
All (Nmax = 14)
Immature (Nmax = 12)
Kendall's tau for ages
All(Nmax = 7)
Immature (Nmax = 6)
4.66
3.48
0.79
0.94
0.20
1.70
0.44
2.49
3.96
1.46
5.21
3.09
4.90
3.54
69.7
65.1
51.3
33.3
41.4
53.3
57.1
40.4
38.1
14.5
16.4
11.9
1.0
-0.314
-0.685**
-0.143
-0.467
46.8
36.4
65.0
53.8
50.0
64.5
50.0
46.7
-
-a
27.0
23.1
39.6
57.6
54.8
6.7
27.8
-
63.0
30.0
70.7
58.5
63.0
-a
-a
-a
-a
1.91
1.41
0.98
0.38
0.51
2.67
0.89
4.20
2.89
1.09
0.08
0.22
0.33
0.00
0.731**
0.720**
-0.513*
-0.851**
0.408*
0.326
0.250
0.299
-0.062
-0.217
0.905**
0.867*
-0.600
-0.800
0.429
0.467
0.333
0.060
-0.738
-b
-a
71.7
76.7
66.7
71.4
-a
70.7
72.7
59.5
85.2
84.2
100.0
100.0
100.0
"Dyads in which less than 6 grooming bouts or soliciting were observed
bNo statistical test ( N 5 4).
*P < 0.05:**P < 0.01.
cence, followed by a constant response rate by mothers. This tendency was the case
for each mother. In contrast, percentage of successful soliciting by mothers appeared relatively stable with offspring age. In general, mothers were more likely
to respond to soliciting by their offspring than vice versa (Wilcoxon Signed Rank
Tests, T = 2, N = 9, P < 0.01).
Interactions Between Grooming, Soliciting, and Response to Soliciting
One might expect the three variables-grooming, soliciting, and response to
soliciting-to be correlated either positively or negatively, although offspring age
may mediate the relationship. As expected, significant negative correlations were
found between the frequency of soliciting and the response rate to soliciting in
grooming given by mothers (Table 111). Other correlations were also in the expected
direction, although nonsignificant.
In contrast, for grooming given by offspring, correlations between the percentages of solicited grooming and the two other variables were low or even positive,
whereas there were positive correlations between grooming rates and the percentages of response to soliciting (Table 111, tests for dyads). Thus, unlike offspring,
mothers did not appear to increase their soliciting when they were groomed less
often, and were unlikely to suffer decreased response rates to their increasing
soliciting.
62 I Muroyama
TABLE 111. Kendall's Rank Correlation Test on the Three Variables Measured in Each
Grooming Dyadt
Grooming by mother
Immature offspring
N
Time spent
grooming vs. %
of solicited
grooming
Time spent
grooming vs. %
of successful
soliciting by the
partner
% of solicited
grooming vs. %
of successful
soliciting by the
partner
tau
Grooming by offspring
All offspring
Immature offspring
All offspring
N
tau
N
tau
N
tau
-0.110
-0.048)
9
(5
0.333
-0.200)
11
(6
0.236
-0.067)
12
(6
-0.351
-0.333)
14
(7
10
(5
0.460
0.800)
12
(6
0.419
0.600)
7
(4
0.683*
10
(5
-0.667**
-0.600)
12
(6
-0.496*
-0.467)
7
(4
0.000
-9
-9
9
(5
9
(5
0.572*
0.105)
0.000
-0.316)
'N indicates the number of mother-offspring dyads used for statistical tests. Statistics for the median values of
each age are indicated in parentheses. Dyads in which less than 6 grooming bouts or soliciting were observed are
omitted.
aNo statistical test (N 5 4).
*P < 0.05: **P < 0.01.
DISCUSSION
Behavioral conflict between mothers and offspring in nonhuman primates has
been studied mostly in the context of the weaning process [e.g., Gomendio, 19911.
However, this study demonstrates that mothers may groom their offspring as a
form of maternal investment when the latter is immature, and that behavioral
conflict may occur over the amount of grooming given by mothers. The conflict
appears to intensify with offspring age. It remains stable after an immature offspring becomes an early adolescent, while grooming given by mothers continues to
decrease until their offspring reaches late adolescence. This stable phase may be
related to the decreasing need for and importance of grooming as maternal care for
offspring. Independence of offspring from mothers and development of social relationships with group members other than relatives may also lower the demand for
grooming from mothers [Walter, 19871, and thus might prevent the conflict from
intensifying.
It should be noticed that my results by a cross-sectional analysis cannot specify
how and at what offspring age the conflict would settle [see Martin & Bateson,
19861. In addition, small sample size in the present study did not allow to examine
the variations among different mother-offspring dyads of the same age-sex classes.
Indeed, there were substantial differences between mothers (e.g., time spent
grooming, see Tables 1,II), although the overall trends were identical among them.
It is possible that social factors such as social ranks of mothers and the number and
sex of offspring affect the timing and pattern of the conflict over grooming amounts
given by the mother. Further studies with additional subjects and longitudinal
sampling may provide corroborative information.
The results suggest that mothers may no longer groom their offspring as a
form of maternal investment when the latter reaches late adolescence. However,
Development of Mother-Offspring Grooming I 63
mothers groomed their adult female offspring much more often than their adolescent female offspring. Such conspicuous increase of grooming by mothers may
indicate that their grooming shifts from a form of maternal investment in their
offspring t o a benefit t o be exchanged reciprocally with them. Fairbanks and
McGuire [19851 proposed a view for post-weaning mother-offspring relationships
in group-living primates, which emphasizes that the reciprocal exchange of beneficial acts increases both mothers’ and their offspring’s reproductive potential.
Frequent exchanges of beneficial acts between mothers and female offspring may
be also significant for maintaining their social relationships [Dunbar & Sharman
1984; Walter and Seyfarth, 19871, and thereby may benefit both of them in matrilineally organized groups [Gouzoules & Gouzoules, 1987; Pusey & Packer 1987;
Silk 19871. It appears likely that mothers vary the nature of relationship with
their offspring according to the offspring’s age, so as to maximize their reproductive success.
CONCLUSIONS
1. Behavioral measures concerning grooming given by mothers and soliciting
by offspring varied with offspring age, when the offspring were immature. This
indicates that mothers groom their immature offspring as a form of maternal
investment, which may entail behavioral conflict between them.
2. Frequent grooming of adult female offspring by their mothers may indicate
that grooming by mothers shifts from a form of maternal investment in their
offspring to a benefit to be exchanged reciprocally with them.
ACKNOWLEDGMENTS
I thank M. Kawai and Y. Sugiyama for their constant support and encouragement throughout this study. I also thank the staff of the Koshima Field Laboratory
for allowing me to use their facilities and for providing helpful information. I am
grateful to F. Colmenares, L. Fairbanks, B. Thierry, and two referees for their
helpful comments on earlier drafts of the manuscript, and to J. R. Anderson for
correcting my English. This study was supported in part by the Cooperative Research Fund of the Primate Research Institute, Kyoto University, Japan.
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