Volule 37-1-57 64 Japan Macaques

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American Journal of Primatology 3757-64 (1995)

BRIEF REPORTS

Developmental Changes in Mother-Offspring Grooming

in Japanese Macaques

YASUYUKI MUROYAMAPrimate Research Institute, Kyoto Un iversity, Inuy am a, Aich i, Jap an

A cross-sectional analysis was made of developmental changes in mother-

offspring grooming in Japanese macaques, Macaca fuscata. When off-

spring were immature, time spent grooming by their mothers decreased

with offspring age. Soliciting by offspring increased steadily with age, incontrast 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 mate rnal investment, which may entai l behav-

ioral 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 995Wiley-Liss, Inc.

Key words: grooming, soliciting, developmental changes, behavioralconflict, post-weaning maternal investment

INTRODUCTION

In most mammalian species, females allocate most of their reproductive effort

to raising the ir offspring and ensuring their survival through pre-weaning mater-

nal 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 sur-

vival of each offspring represents a substantial proportion of a female’s reproduc-

tive output [Altmann et al., 1988; Cheney et al ., 19881. In these species, it is likelythat 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 fusca ta).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; evision accepted February 27,1995

Address repr int requests t o Yasuyuki Muroyama, Primate Research Institute, Kyoto University, In-

uyama, 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 thatpost-weaning maternal investment could take.

Mothers a re expected t o groom their offspring most frequently when they are

young, if grooming is a form of post-weaning maternal investment. Indeed, previ-

ous 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 disagree-

ment 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 char-

acterized 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 t o 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 thatinhabit 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 t o 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 1 sec. 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



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60 I Muroyama

had solicited another was groomed by the second animal within 1 min, it was

concluded th at 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 groomingbouts 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 o r 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 atmaximum) did not allow to analyze each female’s data separately and pool the

individual P values. Therefore, I used tentat ively 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 suc-

cessful 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 tothe ir 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 var iance

between individuals (Table 11). Both male and female offspring in la te adolescencewere less likely than juvenile and early adolescent offspring to groom their moth-

ers, whereas adult female offspring groomed more frequently than late adoles-

cents.

Soliciting and Response to Soliciting

Infant and yearling offspring received nearly all their grooming without so-

liciting from their mothers (Table 11). The percentage of solicited grooming in-

creased steadily with offspring age, reaching more than 65% in mother-adult fe-

male offspring dyads. With one exception (URI’s case), each mother was likely to

be solicited more frequently by its older offspring than by it s 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

Groom ing by moth ers Groom ing by offspring

Age and sex Ra te of Solicited Successful Ra te of Solicited Successful

of offspring grooming gro om ing solici ting grooming grooming solic it ing

Subiect (vrs :sex) (m in hr ) (%) (%) (min /hr) (%I (%)~

URI 28:F

TUT 28:F

MBR 6:M

U RI 6:M

TUT 6:F

GAK 4:M

MMJ 4:F

K E D 4:F

URI 3:F

TUT 2:F

K ED 1:M

URI 1:F

GAK 1:F

TUT O:M

Kendall's tau for dyads

All (Nmax = 14)

Imm a tu re (Nma x = 12)

Kendall 's tau fo r ages

A l l ( N m a x = 7)

Imm a tu re (Nma x = 6)

4.66 69.7

3.48 65.1

0.79 51.3

0.94 33.30.20 -1.70 41.4

0.44 53.3

2.49 57.1

3.96 40.4

1.46 38.1

5.21 14.5

3.09 16.4

4.90 11.9

3.54 1.0

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0.98

0.38

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2.67

0.89

4.20

2.89

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0.08

0.22

0.33

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0.326

0.429

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"Dyads in which less than 6 grooming bouts o r soliciting were observed

bN o statistical test ( N 5 4) .*P < 0.05: *P < 0.01.

cence, followed by a constant response r ate by mothers. This tendency was the case

for each mother. In contrast, percentage of successful soliciting by mothers ap-

peared relatively s table with offspring age. In general, mothers were more likely

to respond to soliciting by the ir offspring th an vice versa (Wilcoxon Signed Rank

Tests, T = 2, N = 9, P < 0.01).

Interactions Between Grooming, Soliciting, and Response to Soliciting

One might expect th e three variables-grooming, soliciting, and response tosoliciting-to be correlated ei ther 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, al though nonsignificant.

In contrast , for grooming given by offspring, correlations between the percent-

ages of solicited grooming and the two other variables were low or even positive,

whereas there were positive correlations between grooming rates and the percent-

ages 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 Grooming by offspring

Immature offspring All offspring Immature offspring All offspring

N tau N tau N tau N tau

Time spent 12 -0.351 14 -0.110 9 0.333 11 0.236

grooming vs. % (6 -0.333) (7 -0.048) (5 -0.200) (6 -0.067)

of solicited

grooming

Time spent 10 0.460 12 0.419 7 0.683* 9 0.572*

grooming vs. % (5 0.800) (6 0.600) (4 -9 (5 0.105)

of successful

soliciting by th e

partner

% of solicited 10 -0.667** 12 -0.496* 7 0.000 9 0.000

grooming vs. % (5 -0.600) (6 -0.467) (4-9

(5 -0.316)of successful

soliciting by the

partner

'N indicates the number of mother-offspring dyads used fo r statistical tests. Statistics for the median values ofeach 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 off-

spring 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 rela-

tionships with group members other than relatives may also lower the demand forgrooming from mothers [Walter, 19871, and thus might prevent the conflict from

intensifying.

It should be noticed tha t my results by a cross-sectional analysis cannot specify

how and a t 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 adoles-

cent 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 bene-ficial 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 ma-

trilineally 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 reproduc-

tive success.

CONCLUSIONS

1. Behavioral measures concerning grooming given by mothers and solicitingby 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 encourage-

ment 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 amgrateful 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 fo rcorrecting my English. This study was supported in part by the Cooperative Re-

search Fund of the Primate Research Institute, Kyoto University, Japan.

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