Primates (2008) 49:176–185 DOI 10.1007/s10329-008-0089-y

ORIGINAL ARTICLE

The trade balance of grooming and its coordination of reciprocation and tolerance in Indonesian long-tailed macaques (Macaca fascicularis) Michael D. Gumert Æ Moon-Ho R. Ho

Received: 14 June 2007 / Accepted: 24 April 2008 / Published online: 11 June 2008 Ó Japan Monkey Centre and Springer 2008

Abstract We collected data on grooming, proximity, and aggression in long-tailed macaques (Macaca fascicularis) in Kalimantan, Indonesia. We used this data to study how grooming influenced a receiver’s (B) behavior towards the bout’s initiator (A). In our first analysis, post-grooming samples were collected after A groomed B. These were compared to matched-control samples of similar conditions but A had not previously groomed B. This comparison was performed on 26 individuals (16 $, 3 #, 7 immature) and tested whether A’s initial act of grooming increased the pair’s time in proximity and the amount of time B groomed A. We also tested if A’s grooming decreased B’s aggression towards A per time in proximity. Rates of B ? A aggression per time in proximity with A for 39 individuals (18 $, 5 #, 16 immature) were compared between postgrooming and focal sample data. Finally, we studied 248 grooming bouts to test if the first two grooming episodes were time matched. We assessed the influence of age, sex, rank and inferred kinship on time matching, and controlled for individual variation and tendency to groom using a general linear mixed model. Our results showed that A ? B grooming acted to increase B ? A grooming and the pair’s proximity, while lowering B ? A aggression. Despite these effects, episodes in grooming bouts were generally not matched, except weakly among similar partners (i.e., female pairs and immature pairs). Grooming imbalance was greatest across age–sex class (i.e., male–

M. D. Gumert (&)
M.-H. R. Ho Division of Psychology, School of Humanities and Social Sciences, Nanyang Technological University, S3.2-B4-35, Nanyang Avenue, Singapore 639798, Singapore e-mail: [email protected]

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female and adult–immature pairs). In similar pairs, grooming duration was skewed in favor of high-ranking individuals. We conclude grooming established tolerance and increased the likelihood that grooming reciprocation would occur, but grooming durations were not typically matched within bouts. Lack of time matching may be the result of grooming that is performed to coordinate interchanges of other social services. Keywords Long-tailed macaque
Grooming
Tolerance
Time matching
Reciprocity
Interchange

Introduction Research on anthropoid primates has provided evidence that grooming is immediately reciprocated during grooming interactions (Goosen 1987). Studies on the balance of input between sequential grooming episodes have shown that grooming partners tend to give as much grooming as they get. Such time matching of sequential grooming has been discovered in female grooming pairs of chacma baboons (Papio ursinus) (Barrett et al. 1999, 2000), whitefaced capuchins (Cebus capucinus), and bonnet macaques (Macaca radiata) (Manson et al. 2004). However, the phenomenon of immediate time matching is weak, and Manson et al. (2004) reports that time matching is not a strong predictor of grooming reciprocation, except for females of close rank. Other researchers report no time matching at all in sequential grooming, as has been demonstrated in research on captive Japanese macaques (Macaca fuscata) (Schino et al. 2003). These findings suggest that although grooming between closely ranked females may be immediately returned in equal amounts, much grooming is not. It is important to

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understand the role of grooming imbalances in primate cooperation. Unmatched bouts might be interchanged with other acts (Barrett and Henzi 2001), lost due to social imbalance (i.e., the hierarchy) or offered to appease and draw support from high-ranked partners (Seyfarth 1977; Barrett et al. 1999, 2002). In long-tailed macaques (Macaca fascicularis), grooming increases the probability of infant handling (Gumert 2007a), sexual activity (2007b) and coalition support (Hemelrijk 1994). Grooming also increases the response to solicitation calls for agonistic support in vervet monkeys (Cercocebus aethiops) (Seyfarth and Cheney 1984). Moreover, grooming increases the likelihood of food sharing in chimpanzees (Pan troglodytes) (de Waal 1997). These findings give an indication of the role that grooming can play in cooperation. Grooming seems to directly coordinate a pair’s social activity patterns, and can be interchanged with other social activities. Henzi and Barrett (1999) argued that grooming coordinates cooperative social trade through two basic behavioral mechanisms. First, grooming leads to grooming reciprocation, especially among partners of similar age, sex, and rank. Such balanced bi-directional grooming establishes relationships and develops social alliances (Seyfarth 1977; Schino et al. 2007). Second, grooming establishes a level of tolerance, defined as increased proximity with reduced aggression. Tolerance is especially valuable in societies where dominance gradients are steep (Barrett et al. 2002) because there is a demand for subordinates to gain tolerance from their dominant social partners to ease resource acquisition. Tolerance also plays a role in social exchange because it increases the opportunity for social interaction (Barrett and Henzi 2001). Once tolerance is established between a pair, other social interactions that require paired coordination can occur more easily. Therefore, an individual could use grooming to coordinate social interchange through establishing tolerance. In anthropoid primates, we would expect that pairs from differing classes should show greater grooming imbalance. This is because grooming across class is more likely to result in the exchange of differing acts, as different classes have differing social resources to offer to their partners. Some examples include grooming across rank, where lowrank partners might groom high-ranked partners for support (Seyfarth 1977; Hemelrijk 1994) and tolerance (Henzi and Barrett 2002), particularly at feeding sites (Ventura et al. 2006). Males might groom females for sexual access or to maintain proximity during consortship and mate guarding (Barrett and Henzi 2001; Gumert 2007b). Females might groom males for support, protection and to reduce harassment. Females may also groom mothers to gain access to infants (Henzi and Barrett 2002). We investigated recent receivers of grooming and studied how grooming influenced subsequent interaction

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between a pair. This allowed us to test Henzi and Barrett’s (1999) predictions on the two behavioral mechanisms of grooming-based social exchange. We studied grooming behavior in long-tailed macaques living in Kalimantan, Indonesia. Data on social activity was collected from periods immediately following acts of grooming and were used to determine the effect of A ? B grooming on B’s behavior, particularly focusing on grooming, proximity, and aggressive behavior. We further investigated whether sequential grooming episodes were time-matched and how grooming balance varied depending on dyad composition.

Methods Study group and site Two researchers (i.e., P.I. and a field assistant) collected data on grooming, proximity, and aggression between June 2003 and February 2005 from a group of long-tailed macaques in Tanjung Puting National Park (TPNP). During the study, the group’s population varied between 48 and 53 individuals due to births, deaths, emigration, and immigration. Eighteen adult females, 5 adult males, and 18 immature individuals (i.e., 4 $ and 14 # juveniles and adolescents) were investigated. The researchers individually recognized each group member by facial characteristics. The study group resided in a 1.2-km2 home range located along the Sekoyner River near an eco-tourist facility on the northwestern border of the park. The macaques were provisioned from discarded refuse and raided food stocks from the tourist lodge. Data collection The researchers followed the group over a 20-month observation period. There were two 3-week breaks when no observations occurred, one in December 2003 and then again in April–May 2004. The researchers collected 10min focal subject samples (Altmann 1974) on 44 adults, adolescents, and juveniles from the group. During samples, grooming, proximity, and aggression involving the focal subject were recorded. Proximity was defined as being within 1 m of a partner. Aggression was defined as threats, charges, chases, physical contacts (e.g., hitting, slapping or grabbing), and bites. Acts of aggression were scored per episode of aggression. If more than one component occurred in the same act, only one act of aggression was scored. The researchers randomized data collection to avoid time biases in sampling. Only a small proportion of time in the forest was suitable for focal sample collection. Therefore, at the end of the 20-month observation period, 303 h

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30 min of focal sample data had been collected from 44 individuals for an average of 7.06 h per individual. Each individual had a proportional amount of samples in each time period during the day. Additionally, half of the focal data was collected in forest areas and half of the data was collected on the premises of the eco-tourist facility. The researchers also collected post-grooming (PG) samples. These were 10-min focal samples collected on a grooming recipient immediately following the end of a grooming act. Grooming was considered finished and a PG sample was started if any of the following conditions were met: (1) a 30-s interval with no grooming activity occurred, (2) the direction of the grooming changed, (3) the actor shifted its grooming to a third party, or (4) another social act occurred. Proximity, grooming, and aggression that involved the PG subject were scored. PG samples were collected during designated time periods. During PG collection periods, the first A ? B grooming act observed was followed by a PG sample on B. When the 10-min sample was finished, the researchers continued to score any remaining grooming between A and B. After the grooming bout was complete, the researchers began scanning for other grooming activity in the group. The amount of PG data collected was 73 h 18 min for 42 individuals, for an average of 1 h 45 min per individual. Matched-control test for effect of A ? B grooming on B We used a matched-control comparison to investigate whether A ? B grooming directly influenced subsequent B ? A grooming and A–B proximity. The matched-control procedure controlled for confounding proximate factors that might influence B’s behavior. We controlled for context, proximity, motivation to groom, and availability to groom. We selected matched-control (MC) samples from the focal sample database with the following five parameters: the MC must have (1) occurred in a social context, (2) had both A and B present, (3) had A and B come in proximity to each other, (4) had B express grooming to any partner, and (5) had B in proximity to A when they were both available to groom. The last criterion was satisfied if both A and B were freed from grooming others at some point during their proximity or if A and B were grooming the same partner and thus B could easily switch to grooming A. We matched as many MC samples with PG samples for which we could find appropriate matches, generating a data set with 71 paired PG–MC samples from 26 individuals in the grooming recipient role. There were 1–8 paired MC– PG samples per individual that were on average 77 days apart (range:\1–320 days). When there was more than one paired sample per individual, we took the PG and MC

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mean to use in a pair-wise comparison. We compared the difference between PG and MC grooming time, PG and MC proximity time, and also the difference between the ratio of grooming performed per time in proximity. This latter comparison accounted for any differences in grooming time that may have been the result of pairs staying in proximity longer during PG samples than in MC samples. In addition, we compared rank differences to determine if reciprocated grooming varied depending on whether B was reciprocating up- or down-rank. Test for grooming-tolerance interchange Tolerance is defined in this study as a combination of increased proximity and reduced aggression. We tested 39 individuals to determine if receiving grooming increased their time in proximity and lowered aggression towards their grooming partners. In focal samples and PG samples, we calculated A–B proximity times and B’s rate of aggression towards each partner (A) in acts per second in proximity. We matched both average proximity times and rates of B ? A aggression in PG and focal samples for each of the 39 individuals. We then compared the two conditions. Next, a general rate of B aggression not specific to time in proximity was calculated in acts per hour for both PG and focal samples. In PG samples, this rate was separated into B ? A and B ? third party (i.e., other than A) rates of aggression. We used this data to compare the rate of B ? A and B ? third party aggression. We also compared overall rates of B’s aggression between PG and focal samples to see if grooming generally lowered a grooming receiver’s level of aggression. Testing for grooming time matching There were 248 PG samples from 40 different individuals in which the duration of the initial episode of A ? B grooming and any subsequent episode of B ? A grooming was fully recorded. These bouts were analyzed to assess the relationship between the first two episodes of grooming and to determine how time-matched they were. An episode is defined as all grooming that occurs until the direction changes or the pair disperses. Only the first two episodes of any grooming bout were used because only 10%, or 26 samples, developed into third episodes. This method was also chosen because the focus of this study was the testing of the immediate contingency between a single episode of grooming on immediately subsequent grooming and tolerance from the partner. We counted how many grooming bouts were actually reciprocated from the 248 samples. We then averaged the amount of A ? B grooming received and B ? A grooming given for each individual (B) and used that data

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to test the balance of A ? B and B ? A grooming. We ran a Pearson correlation to test if A and B input were related, and also ran a pair-wise comparison to assess whether the input of A and B were significantly different. These same analyses were performed on data from 97 bouts where reciprocation occurred to determine the timebalance of just the reciprocated bouts. We then ran comparisons on the 248 bouts from 40 individuals to test how age and sex influenced patterns of immediate grooming reciprocation. We compared adults to immature individuals and we compared males to females. In these comparisons, we tested for differences in the amount of A ? B grooming, the amount of B ? A grooming and the difference between A ? B and B ? A grooming. Statistics for comparisons For all data sets used for paired or independent sample comparisons, the data were tested for normalcy using Kolmogorov–Smirnoff tests. Normally distributed data sets were compared using paired or independent t tests, and data sets significantly different from normal were compared using Wilcoxon-matched pair tests. All tests were evaluated at a \ 0.05 and the P value represents the twotailed probability. Testing for influences on grooming time-balance A general linear mixed model (GLMM) approach (Verbeke and Molenberghs 1997) was taken to test the 248 PG samples studied for factors that might influence time matching in the first two episodes of a grooming bout. Three fixed factors represented the characteristics of each grooming dyad: (1) age–sex combination, (2) rank direction, and (3) inferred kin relationship. A regression between A and B grooming was tested in the model. Also, the relationship between A and B’s tendency to groom and A and B’s time grooming were tested. Finally, the identity of both A and B were input as random factors to account for any sample dependence resulting from subjects being represented multiple times. Three models were used, each testing a different dependent variable: A ? B grooming time (episode 1), B ? A grooming time (episode 2) and the difference between A ? B and B ? A grooming time. The age–sex combination factor was broken into three conditions: similar pairs, adult male–female pairs, and adult–immature pairs. Similar pairs consisted of pairs of adult females or immature individuals, but not adult males because there were no adult male pairs in the sample. Inferred kin relationships were broken into kin and non-kin conditions, and were defined through association with juveniles and roosting patterns. Females that associated frequently and stably over the entire study with the same

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juveniles and roosted reliably in the same groups were considered a matriline and thus kin. This method was used as a best estimate in the absence of long-term genealogical data or genetic data from this group of macaques. Rank direction was broken into conditions of A higher ranked than B and B higher ranked than A. Grooming tendency was measured in minutes of grooming per hour that each individual performed in focal samples. Tukey’s post hoc tests were used to identify where differences occurred within the age–sex combination factor. After running the GLMMs on the complete data set of 248 samples, we sub-divided the data to model time matching in grooming bouts within each age–sex combination. A GLMM for similar dyads was run using rank direction and inferred kinship as fixed factors and testing the same three dependent variables: A grooming, B grooming, and the difference between A and B grooming. We also tested for a correlation between grooming tendency and grooming given for both A and B, as well as the relationship between A and B grooming. For adult– immature dyads, the same modeling procedure was used, but rank direction was replaced by age direction (i.e., younger-to-older, or older-to-younger), as most adults outranked all immature individuals. For male–female dyads, inferred kinship was not factored into the model because male–female kin relationships could not be assessed and were most likely not related, since male long-tailed macaques are known to disperse between groups. Also, rank direction was replaced by sex direction (i.e., male-tofemale, or female-to-male) because all males out-ranked all females. Only models that yielded significant results (P \ 0.05, two-tailed) are reported.

Results Influence of A ? B grooming on B Grooming reciprocation: MC–PG comparison The long-tailed macaques we studied performed significantly more B ? A grooming in post-grooming (PG) than matched-control (MC) samples (paired t test: t = 3.031, df = 25, P = 0.006) (Fig. 1). In addition, B groomed A significantly more than third parties in PG than in MC samples (paired t test: t = 7.138, df = 25, P \ 0.001) and B groomed third parties significantly more in MC than PG samples (paired t test: t = -4.597, df = 25, P \ 0.001) (Fig. 1). Pairs spent significantly more time in proximity in PG than MC samples (paired t test: t = 3.964, df = 25, P = 0.001) (Fig. 2). Moreover, the ratio of B ? A grooming per time in proximity was significantly greater in PG than MC samples (paired t test: t = 6.877, df = 25,

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Primates (2008) 49:176–185

Mean Grooming Duration (min)

5.00

Post Groom Match Control

4.00

3.00

2.00

P \ 0.001) (Fig. 2). These results indicate that A ? B grooming coordinated B ? A grooming. Rank was also found to influence reciprocation. In a paired data set of 9 individuals in the B role under conditions of being both lower and higher ranked than A, it was found that when B was higher ranked than A the mean grooming reciprocation time was 2.08 min (SD = 2.27) and 3.89 min (SD = 1.00) when B was lower in rank. B reciprocated significantly more grooming when A was higher in rank than B (paired t test: t = -2.495, df = 8, P = 0.037). Grooming-tolerance interchange

1.00

0.00 Partner

Third Party

Fig. 1 Bars represent the mean time that recent long-tailed macaque (Macaca fascicularis) receivers of grooming (B) reciprocally groomed their partner, the grooming initiator (A), or groomed third parties. Here, we compare the mean grooming time between 10-min post-grooming (PG) samples, where A had groomed B immediately before, and matched-control (MC) samples, where A had not groomed B immediately before. Whiskers represent 1SE of the mean

Minutes grooming/ minutes in proximity

Time in Proximity Time Grooming

6.00

Following grooming, our criteria for tolerance was met. Partner-specific aggression decreased and proximity increased. A and B spent a greater proportion of time in proximity after A ? B grooming than they did in focal samples (paired t test: t = -14.089; df = 38, P \ 0.001) (Fig. 3a). This indicates that there was greater opportunity for interaction between the pair following grooming. Despite this increase in proximity, the rate in which B aggressed A while in proximity was significantly less frequent in PG than focal samples (Wilcoxon matched-pair test: T = 4, n = 22, P \ 0.001) (Fig. 3b). Tolerance appeared partner-specific because B aggressed third parties significantly more often than A during PG samples (Wilcoxon matched-pair test: T = 0, n = 19, P \ 0.001). Overall, B may have expressed less aggression in PG than in focal samples, but this difference did not quite reach significance (Wilcoxon matched-pair test: T = 226, n = 37, P = 0.058), supporting that tolerance was more partner-specific than generalized. Time matching of grooming

4.00

2.00

0.00 Post Groom

Match Control

Fig. 2 The amount of time spent in proximity by grooming pairs and the time an initial grooming recipient (B) groomed the bout initiator (A) during 10-min post-grooming (PG) and matched-control (MC) samples. This shows the difference in proportion of time that B ? A grooming occurred while A and B were in proximity between the two conditions

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We found no correlation between the average amount of grooming received (A ? B) and reciprocated (B ? A) (r = -0.069, n = 40, P = 0.672). Rather, we found that A grooming was 5.04 (SD = 3.54) min longer compared to how much B groomed (paired t test: t = 8.997, df = 39, P \ 0.001), indicating that initiators groomed significantly more than receivers (Fig. 4). Ninety-seven, or 39.1%, of all grooming bouts resulted in reciprocation. When only reciprocated bouts were analyzed, a positive correlation between A and B grooming was found, but it was not significant (r = 0.171, n = 31, P = 0.357). In addition, the difference between the amount of A and B grooming was only marginally different (paired t test: t = 1.839, df = 30, P = 0.076). In reciprocated bouts, A grooming was 1.24 min (SD = 3.74) longer than B grooming (Fig. 4). We found that grooming tendency influenced how much individuals reciprocated because the average amount

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0.50

181

A

Percent Time in Proximity

0.40

0.30

0.20

0.10

0.00 Focal samples

PG samples

Reciprocated bouts 0.0006

B

Fig. 4 The average amount of grooming received (A grooming) and reciprocated (B grooming) for 40 individuals over 248 grooming bouts in the first two episodes in a grooming bout. The average of all bouts is compared to a subset of 97 reciprocated bouts indicating that even reciprocated bouts were imbalanced. Whiskers represent 1SE of the mean

0.0005

Mean Rate of B→A Aggression

All bouts

0.0004

0.0003

0.0002

0.0001

0.0000 Focal samples

PG samples

Fig. 3 The percentage of time during post-grooming (PG) samples that a recent receiver of grooming (B) was in proximity to the grooming initiator (A) compared to the percentage of time the pair was in proximity during focal samples (a), and B’s rate of aggression to A per second of time in proximity (b). Whiskers represent 1SE of the mean

of B grooming was correlated with the amount of grooming B performed in focal samples (Pearson correlation: r = 0.404, n = 40, P = 0.011). We found that age and sex influenced the amount of grooming that individuals received (A ? B) and reciprocated (B ? A). The difference between A and B grooming was greater for immature than adult individuals (independent t test: t = 2.864, df = 38, P = 0.007). A ? B grooming was not significantly different between adults

and immature individuals (independent t test: t = -1.385, df = 38, P = 0.174), but immature individuals reciprocated significantly less grooming than adults (independent t test: t = 3.046, df = 38, P = 0.004) (Fig. 5a). The difference between A and B grooming was greater for males than females (independent t test: t = 2.705, df = 38, P = 0.010). Males and females were not found to reciprocate significantly different amounts (independent t test: t = 1.633, df = 38, P = 0.111), but males did receive significantly more A grooming (independent t test: t = -2.132, df = 38, P = 0.040) (Fig. 5b). Influences on time-balance in grooming interactions Our general linear mixed models (GLMM) identified how dyad combination can influence time matching of grooming. Age–sex combination, inferred kin relation, and rank direction were used as fixed factors in the models, and a regression was tested between A and B grooming. To account for confounds, A and B’s grooming tendency was regressed to A and B grooming, and individual identity was entered into the model to account for dependency of samples caused by replication of subjects. The entire data set of 248 grooming bouts was input in the GLMM. Age–sex combinations were significantly different for A grooming and the difference between A and B grooming, but no significant difference was found for B

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Primates (2008) 49:176–185 Table 1 A GLMM was used to assess factors that may influence time matching during the first two episodes of 248 grooming bouts between long-tailed macaques (Macaca fascicularis)

A

Parameter

Numerator df

Denominator df

F

P

A: Difference between A and B grooming Age–sex

2

155.649

6.938

0.007*

Kin

1

180.226

0.769

0.382

Rank

1

169.487

0.390

0.533

A tendency

1

146.376

0.157

0.693

B tendency

1

153.276

0.007

0.933

B: A ? B grooming

immature

adult

age

B

Age–sex

2

154.292

8.005

0.000*

Kin

1

184.334

0.655

0.419

Rank

1

160.091

0.564

0.454

B ? A input

1

240.605

0.140

0.708

A tendency

1

144.596

0.002

0.962

C: B ? A grooming Age–sex Kin

2 1

138.922 165.773

0.226 0.153

0.798 0.697

Rank

1

148.833

0.035

0.852

A ? B input

1

238.463

0.077

0.782

B tendency

1

129.552

2.109

0.149

Age–sex composition, inferred kin relationship and rank direction were entered as fixed factors in the model. An individual’s grooming tendency was entered into the model as a covariate, and the correlation between initial actor (A) and initial receiver’s (B) grooming time was assessed. Individual identities were added into the model as random factors to control for individuals appearing in the data set more than once. The dependent variables tested were the difference between A and B grooming, A grooming, and B grooming. * Significant results

female

sex

male

Fig. 5 A comparison of the average amount of grooming received (A grooming) and reciprocated (B grooming) for adults and immature individuals (a), and males and females (b) in the first two episodes in a grooming bout

grooming (Table 1). Tukey post hoc tests showed that the difference between A and B grooming in similar pairs was significantly smaller than in male–female pairs (P = 0.001) and adult–immature pairs (P = 0.001) (Fig. 6). In addition, A grooming in similar pairs was significantly shorter than adult male–female pairs (P = 0.001) and adult–immature pairs (P = 0.004) (Fig. 6). Grooming time was more imbalanced when age

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and sex differed, and the difference between these factors was largely due to a greater amount of grooming by A. A GLMM run on only grooming bouts between similar pairs showed that rank influenced both A grooming and the difference between A and B grooming (Table 2, panels A, B). In addition, there was a significant correlation between A and B grooming (Table 2, panels B, C), indicating the amount of grooming A performed was related to how much B reciprocated in similar pairs. When A was higher ranked, the difference between A and B grooming was less compared to grooming interactions when A was lower ranked than B (Fig. 7). We found no clear relationships with inferred kinship. All three age–sex class conditions showed significantly different relationships for time matching in the first two grooming episodes (Chisquare test: X2 = 7.209, df = 2, P = 0.028). Grooming between similar pairs was more time-matched, and grooming between male–female pairs was more imbalanced (Fig. 8).

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Fig. 6 The mean time that the grooming initiator (A) and the initial grooming recipient (B) groomed each other during the first two episodes in a grooming bout across three age–sex pair combinations; similar pairs, male–female pairs and adult–immature pairs. We show the absolute difference between A and B grooming to compare the imbalance in grooming between the three conditions

Fig. 7 The mean time that the grooming initiator (A) and the initial grooming recipient (B) groomed each other during the first two episodes in a grooming bout. Here, we compare these mean times between rank relationships: A outranks B and B outranks A. We also show the absolute difference between A and B to compare the imbalance of grooming in the two conditions

Discussion Table 2 A GLMM was used to assess factors that influenced time matching within similar pairs (i.e., female pairs and immature pairs) Parameter

Numerator df

Denominator df

A: Difference between A and B grooming Kin 1 61.727

F

P

0.254

0.616

Rank

1

64.129

6.553

0.013*

A tendency

1

59.009

0.108

0.743

B tendency

1

57.906

1.180

0.282

B: A ? B grooming Kin

1

74.080

0.290

0.592

Rank

1

75.049

4.838

0.031*

B ? A input

1

108.983

4.937

0.028*

A tendency

1

70.182

0.377

0.541

76.683

0.008

0.929 0.146

C: B ? A grooming Kin

1

Rank

1

80.779

2.158

A ? B input

1

108.340

5.111

0.026*

B tendency

1

70.972

3.574

0.063

Inferred kin relationship and rank direction were entered as fixed factors. The grooming tendencies of A and B were entered as covariates. Also, the relationship between A and B grooming was tested. Individual identities were entered as random factors. The dependent variables tested were the difference between A and B grooming, A grooming, and B grooming. * Significant results

Single acts of grooming appear to influence the receiver of grooming (B) and lead to reciprocating subsequent grooming, increasing proximity and reducing aggression towards the initiator (A). We have defined this coupling of increased proximity with decreased aggression as tolerance of A by B. Although A ? B grooming increased the amount of B ? A grooming relative to time periods of similar conditions but A had not groomed B, grooming episodes were not typically time-matched. Most of the long-tailed macaques in this study that initiated grooming received less grooming from their partner than they gave in the initial episode. We found clear influences on the level of time matching, and the best predictor of grooming balance appeared to be age–sex composition. Grooming times were most imbalanced in male–female and adult–immature pairs. In contrast, grooming times were most balanced in female–female and immature– immature pairs. The results of this study are consistent with past work. Immediate grooming reciprocation has been reported in many primate species (review: Goosen 1987; Macaca fuscata: Muroyama 1991; Cercopithecus mitis stuhlmanni: Rowell et al. 1991; Cebus olivaceus: O’Brien 1993; Papio hamadryas ursinus: Henzi and Barrett 1999), but these studies did not go into the detail of investigating the direct

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A

B

C

Fig. 8 The relationship between initiator (A) grooming duration and initial recipient (B) grooming duration in the first two episodes of reciprocated grooming bouts. Similar pairs showed a positive relationship (a), adult-male female pairs showed a negative relationship (b), and adult–immature pairs showed no clear relationship (c)

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influence that grooming has on the receiver. Our results also concur with other work on time matching because, as in baboons (Barrett et al. 1999), macaques and capuchins (Manson et al. 2004), grooming was time balanced among female pairs of similar rank. Lastly, our results demonstrate the long-standing idea that grooming inhibits aggression and allows proximity (i.e., tolerance) (Old World monkeys: Sparks 1967; Schino et al. 1988; Presbytis entellus: McKenna 1978; Macaca radiata: Silk 1982; Cebus olivaceus: O’Brien 1993). Grooming coordinated subsequent partner-specific activity in long-tailed macaques. Such coordination was partner-specific because B focused their grooming effort much more on A than on third parties. Tolerance was also coordinated by initial episodes of grooming and was partner-specific, as tolerance was more apparent toward the initial groomer than towards third parties. The increase in partner-specific tolerance is particularly important to social cooperation because other forms of social activity can more easily occur once tolerance is established (Barrett and Henzi 2001). Grooming-induced tolerance may allow the initial groomer to access social resources or services that B can offer because the pair can stay in proximity for longer without conflict, increasing the likelihood of cooperation. Even though grooming increased B ? A grooming relative to comparative time periods where A ? B grooming did not occur, grooming durations were not necessarily balanced in a grooming bout. In general, the grooming initiator A groomed more than was reciprocated from B. Pair combination seemed to be the best predictor of the extent of time matching in grooming pairs. Immature animals reciprocated less grooming and males received more initial A ? B grooming. A and B grooming episodes were more time balanced within female pairs and immature pairs than in male–female or adult–immature pairs. Within similar pairs, dominance rank influenced grooming balance in a manner consistent with Seyfarth’s (1977) model on female grooming. The basic pattern of A grooming exceeding B grooming remained, but episodes that were directed up-rank tended to be longer when compared to down-rank. A ? B grooming was clearly longer when up-rank and there was evidence that B provided more grooming to higher ranked partners when they were reciprocating grooming. Also, there was a greater time loss when A was lower ranked than B compared to the reverse condition, indicating that B was less likely to reciprocate when groomed by a lower-ranked partner. In contrast, the rank difference for male–female and adult– immature pairs, which also corresponded with age difference or sex difference, was not a significant predictor of time imbalance because a similar level of imbalance occurred regardless of grooming direction.

Primates (2008) 49:176–185

We have shown that receiving grooming can influence the receiver’s behavior by increasing their level of grooming and tolerance towards their partner. These results are consistent with the hypothesized behavioral mechanisms of grooming-based social exchange proposed by Henzi and Barrett (1999). It seems that similar pairs trade balanced grooming and differing pairs have more imbalanced grooming, and this may be because they are interchanging grooming with other social acts (Barrett and Henzi 2001, 2006). Similar partners are likely exchanging grooming to maintain alliances (Seyfarth 1977), as shown by the balance in grooming trade coupled with the skewing towards grooming higher-ranked partners for longer. In dissimilar pairs, the grooming initiator may be utilizing grooming to obtain tolerance and/or other social resources. The imbalance of grooming trade was most pronounced in male–female pairs and this is likely related to interchange because male-to-female grooming in this species is strongly linked to interchanges of sex and mating opportunity (Gumert 2007b). Females, too, are likely to be grooming males for interchange trades, such as tolerance, avoiding harassment and protection. We conclude that grooming exchange may be more related to interchange in differing pairs and more to alliance building in similar pairs. Acknowledgments We would like to express thanks to Dr. Alexander H. Harcourt for his useful comments and help in developing this report. This research was made possible by funding from the American–Indonesian Exchange Foundation (AMINEF), Jakarta, Indonesia, through a Fulbright Graduate Research Fellowship. The Indonesian Institute of Sciences (LIPI) provided a research permit (Permit #: 3044/SU/KS/2003), and the Indonesian Department of Forestry granted permission for the PI to enter and reside in Tanjung Puting National Park (Permit #: 1765/IV-SEK/HO/2003). The Institutional Animal Care and Use Committee of the United States approved the research methods (Animal Research Protocol #: A200510167-0). Dr. Noviar Andayani from the Faculty of Mathematics and Natural Sciences at the University of Indonesia sponsored this work. We give special thanks to our field assistant, Peltanadanson, and to the Rimba Orangutan Ecolodge for supporting and housing the field researchers during the study.

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