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. 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