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Grooming and the value of social relationships in cooperatively

breeding meerkats

Nobuyuki Kutsukake

^a^,^b^,^c^,^*

, Tim H. Clutton-Brock

^a^,¹

aLarge Animal Research Group, Department of Zoology, University of Cambridge

bDepartment of Evolutionary Studies of Biosystems, The Graduate University for Advanced Studies

cPRESTO, Japan Science and Technology Agency

a r t i c l e i n f o

Article history:

Received 2 February 2009 Initial acceptance 26 February 2009 Final acceptance 5 October 2009 Available online 4 December 2009 MS. number: 09-00070R

Keywords: cooperative breeding grooming

meerkat social relationship Suricata suricatta

In social mammals, grooming is used not only for hygienic purposes; it also serves social functions. We examined the grooming patterns of dominant males in groups of cooperatively breeding meerkats, Suricata suricatta, to test the hypothesis that the distribution of grooming reﬂects the value of social relationships. Grooming between dominant individuals was the most commonly observed interaction. Grooming by the dominant male was less common when the dominant female was in oestrus. Grooming between dominant males and subordinates was asymmetrical, with dominant males receiving more grooming and providing less grooming to subordinates. Because subordinate males defend the group against extragroup males, the dominant male was predicted to groom subordinate males more often than to groom subordinate females. Although the sex of a subordinate did not affect the probability of grooming occurring, dominant males groomed subordinate males for longer than they groomed subordinate females. The duration of grooming by a dominant male was longer in small groups than large groups, suggesting that grooming activity is constrained by time. In contrast, subordinates groomed dominant males for longer in larger groups, and as a result, the asymmetry of grooming exchanges was exaggerated in larger groups. This result is consistent with the biological market theory, which predicts that the value of subordinates is dependent on group size and that subordinates will alter grooming efforts accordingly. These results suggest that meerkat grooming serves several social functions, such as the maintenance of valuable and/or ﬁtness-enhancing relationships.

Social grooming (allogrooming) is a common feature of many animal societies (reviewed in Spruijt et al. 1992). The primary function of grooming may be hygienic (e.g. removing parasites), providing a benefit to the groomee by reducing its parasite load (Hart et al. 1992; Tanaka & Takefushi 1993). Beyond hygiene, grooming can have several social functions, reflecting the characteristics of the social relationship between groomer and groomee. For example, grooming can be used to gain other social benefits (Barrett & Henzi 2006; Gumert 2007; Schino 2007). Although the structure and function of grooming relationships have been studied in many group-living primates, relatively little is known for other group-living animals. Compared to species living within multimale/ multifemale breeding systems with low reproductive skew, only a few studies have investigated the function of grooming in

cooperatively breeding vertebrates (Lazaro-Perea et al. 2004; Kut- sukake & Clutton-Brock 2006b; Radford & du Plessis 2006). In cooperatively breeding vertebrates, reproduction is usually monopolized by a dominant pair; subordinate individuals rarely reproduce and instead help rear the offspring produced by the dominant pair (Stacey & Koenig 1990; Solomon & French 1997; Koenig & Dickinson 2004). Group members also experience competition or conﬂict for limited resources and reproductive opportunities within the group (Emlen 1997; Clutton-Brock et al. 2006). Therefore, cooperatively breeding societies provide excel- lent opportunities to investigate the effects of both cooperation and competition on grooming, and to test the hypothesis that individuals provide more grooming to individuals with whom they maintain valuable (i.e. ﬁtness-generating) relationships. Such studies will expand our knowledge of social behaviour beyond the results obtained from plural-breeding species.

In this study, we investigated the grooming of dominant males in stable groups of the cooperatively breeding meerkat, Suricata suricatta. In this species, related individuals form a family group. Females are philopatric, but subordinate males voluntarily disperse from their natal groups (Doolan & MacDonald 1996; Young et al.

* Correspondence: N. Kutsukake, Department of Evolutionary Studies of Bio- systems, The Graduate University for Advanced Studies, Hayama, Miura-gun, Kanagawa, 240-0193, Japan.

E-mail address:kutsu@soken.ac.jp(N. Kutsukake).

1 T. H. Clutton-Brock is at the Large Animal Research Group, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, U.K.

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Animal Behaviour

j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m / l o c a t e / a n b e h a v

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2007). Reproductive skew is high among both males and females (Grifﬁn et al. 2003; Spong et al. 2008), but intrasexual conﬂict is more intense in females than in males (Clutton-Brock et al. 2006). Dominant pairs of meerkats breed approximately three times per year, and a dominant female resumes her oestrus soon after the birth of her pups. A dominant female is in oestrus for approximately 1 week. During this time, the dominant male persistently follows and guards the female at the expense of other activities (Kutsukake

& Clutton-Brock 2008a). For dominant individuals, subordinates can be regarded as important social resources because a large number of helpers or a low offspring/helper ratio reduces the per capita work burden of group members and is positively related to the reproductive success of the dominant individuals (Emlen 1997; Cockburn 1998; Hatchwell 1999; Clutton-Brock et al. 2001; Clut- ton-Brock 2002; Russell et al. 2002, 2003). Incest avoidance occurs in meerkats; natal males do not have the opportunity to reproduce within their natal group (O’Riain et al. 2000; Grifﬁn et al. 2003).

We previously reported that grooming of dominant female meerkats has several social functions (Kutsukake & Clutton-Brock 2006b). First, the dominant pair forms the most frequent grooming relationship. Given that dominants form stable sexual bonds, this result suggests that grooming reflects the value of social relationships (see alsoKleiman 1977; Lo¨ttker et al. 2007for other cooperatively breeding species). Second, the grooming exchange between dominant and subordinate individuals was asymmetrical, with subordinate females grooming the dominant female more often than vice versa. This asymmetry was more pronounced between the dominant female and older subordinate females because the dominant female groomed immature subordinates most frequently (possibly for parental care: Kleiman 1977; Goldizen 1989) and mature subordinates less frequently (because of intrasexual conflict:Saltzman et al. 1997; Lazaro-Perea et al. 2000). In addition, older subordinate females, which receive the most aggression from the dominant female, groom the dominant female most frequently. Investigating patterns of grooming in dominant males provides an additional and fine-grained opportunity to test the hypothesis that grooming reflects the value of social relationships in meerkats. Previous studies in this species have shown that in contrast to females, among which intrasexual conflict is intense (Clutton-Brock et al. 2006), males show a more flexible behavioural strategy to moderate intrasexual conflict according to group size (Kutsukake & Clutton-Brock 2008a). Therefore, we expected the more valuable group members for dominant males to be different from those for dominant females. As a result, dominant males and dominant females were expected to have different grooming patterns. We derived several predictions according to our understanding of dominant male strategies, and tested these predictions by investigating the effects of social factors (group size and individual intrinsic factors of the grooming partner, such as dominance status, age and sex) and reproductive factors (the oestrous condition of the dominant female) on the distribution of grooming.

First, we investigated whether, similar to dominant females, dominant males groomed their reproductive partner, the dominant female, more frequently than they groomed other group members (Kutsukake & Clutton-Brock 2006b). Since dominant males and females are the primary breeding pair within meerkat groups (Grifﬁn et al. 2003; Spong et al. 2008), we expected the associated grooming patterns to reﬂect the highly adaptive value of their social relationship. Additionally, we tested a new prediction that the dominant male would groom the dominant female more frequently when she was in oestrus.

Regarding grooming directed towards subordinate individuals, we tested the general hypothesis that grooming is used as a reward for a valuable contribution performed by its recipient. In cooperatively breeding primates, for example, grooming by dominant

breeders is directed towards cooperative subordinate group members and is believed to be an incentive for the subordinates’ cooperation (‘pay-for-help’;Lazaro-Perea et al. 2004; Lo¨ttker et al. 2007). In the case of meerkats, we tested predictions derived from the sex difference in territorial defence. In this species, extragroup males form the critical threat to the reproductive success of dominant males, based on recent results from genetic paternity analysis (Spong et al. 2008). Although all group members partici- pate in intergroup aggression and territorial defence from intruders, it is mainly subordinate males that defend the group against extragroup males (Doolan & MacDonald 1996). In contrast, subordinate females may gain individual beneﬁts of mating and reproductive opportunity by having access to the extragroup males (Clutton-Brock et al. 2001; Grifﬁn et al. 2003). Consistent with this sex difference, the frequency of scent marking at the latrine, which functions to advertise the territory and mate defence, is comparable between dominant and subordinate males, but lower in subordinate females (Jordan 2007). Based on these sex differences, we predicted that the dominant male ‘pays’ subordinate males with grooming more often compared to grooming subordinate females. With respect to grooming of the dominant male by subordinates, we predicted that subordinates at the highest risk of aggression would groom the dominant male most frequently to placate him. This is because grooming functions to relax the groomee or groomer as it stimulates beta-endorphin release (Keverne et al. 1989) and reduces heart rate (Feh & de Mazieres 1993; Aureli et al. 1999; Madden & Clutton-Brock 2009). In this study, we use the term placation as analogous to tension reduction, without making any claims about intent. Since aggression from the dominant individual is more likely to be directed towards same-sex subordinates (Clutton-Brock et al. 2006), we predicted that subordinate males would placate the dominant male by grooming him more often than subordinate females would. Furthermore, subordinates should groom the dominant male more often than the dominant male grooms them. Additionally, we conducted contextual analyses of grooming and aggression to investigate whether a dominant male is less likely to attack a subordinate if that subordinate grooms him, and whether a subordinate is more likely to groom a dominant male when attacked.

Finally, the value of social relationships may vary with group size in cooperatively breeding groups. The biological market theory predicts that the characteristics and partner choices of a social interaction are determined by the ratio of different players and the types of social commodities that each player can offer (Noe¨ et al. 1991; Noe¨ & Hammerstein 1994, 1995; Barrett & Henzi 2006). The application of this theory to cooperatively breeding societies suggests that when few subordinates are in a group, the value of each subordinate to the dominant individual increases as its per capita contribution to cooperation (i.e. helping and group defence) increases. As a result, the dominant individuals in smaller groups are predicted to spend more time and effort serving relationships with subordinates (Reyer 1986; Noe¨ et al. 1991; Lo¨ttker et al. 2007; Kutsukake & Clutton-Brock 2008a). Our previous studies that examined aggression in the same meerkat group support the biological market theory: the number of subordinates within a group is positively correlated with the degree of agonism between male meerkats (Kutsukake & Clutton-Brock 2008a). Thus, the biological market theory predicts a negative relationship between group size and grooming activity. Note, however that this negative relationship is also predicted by a more parsimonious explanation that a dominant male in a large group cannot allocate his grooming efforts equally among group members because of constrained opportunities for grooming in large groups (Dunbar 1992; Henzi et al. 1997; Madden et al. 2009). In meerkats, social network analysis revealed that grooming networks became sparser as group

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size increased suggesting that time budgets imposed constraints on the number of grooming partners (Madden et al. 2009; but see Kutsukake & Clutton-Brock 2006b). This time constraint idea is not mutually exclusive and is indistinguishable a priori from the biological market theory. However, the time constraint explanation and the biological market theory give different predictions regarding the grooming of a dominant male by subordinates. The time constraint hypothesis predicts that the grooming activity of a dominant male by subordinates will be lower in large groups than small groups. Alternatively, the grooming of a dominant male by subordinates may be unaffected by group size if the subordinates maintain their grooming activity as regards the dominant individual but reduce their grooming of other subordinates. In contrast, when the value of a subordinate is low, the biological market theory predicts that subordinates should increase their grooming efforts towards dominants to maintain social relationships. As a result, grooming asymmetry between subordinates and dominants should increase in larger groups (Port et al. 2009).

METHODS

Study Animals and Field Site

This study was conducted in the Kalahari, South Africa, close to Vanzylsrus (2658⁰S, 2149⁰E) from October to November 2005. The study period corresponded to the breeding season, when reproductive conflict is intense. The study site consisted of the dry riverbed of the Kuruman River, herbaceous flats and vegetated dunes. The ecological conditions and climate of this region are described elsewhere (Clutton-Brock et al. 1999a, b; Russell et al. 2002). The study population consisted of 257 individuals in 12 social groups. All individuals were habituated to close observation (i.e. from <1 m) and could be identified by a unique pattern of hair- dye marks on the fur, which were maintained while individuals were resting without disturbing or capturing them (Clutton-Brock et al. 1999b; Sharpe et al. 2002). The ages of most individuals were known to within a few days because they had been observed since birth. Groups were visited at least once every 3 days to collect demographic and behavioural data. The study was permitted by the Northern Cape Conservation Service, South Africa.

Observation Methods

N.K. conducted continuous focal observations of the dominant males in six groups (Altmann 1974). Group size varied from eight to 38 individuals (median ¼ 16) at the beginning of the observation period. Morning focal observations began at approximately 0700 hours, when the group appeared from the sleeping burrow, and continued after the group left the burrow to forage until they became inactive at midday (approximately 1200 hours). Evening focal observations began at approximately 1700 hours, when the group was located, and ended when the dominant individual entered the evening sleeping burrow (approximately 1900 hours). On average, each focal session lasted 2 h 50 min; sessions lasting less than 1 h were excluded because there was insufﬁcient infor- mation about the context of the social behaviours (e.g. the inﬂuence of a predator). On average, focal observations were conducted 18 times for dominant males in each group (range 11–24 times, total observation time 312 h, total observation days 58).

During observations, we recorded all social interactions involving the focal dominant male. These interactions included

‘encounters’ (i.e. all individuals that came within a 1 m radius of the dominant male), all aggression received and performed (for deﬁ- nition, seeKutsukake & Clutton-Brock 2008b) and all grooming interactions (deﬁned as a manipulation of another individual’s fur

with the mouth) involving a single dominant male. Meerkats frequently groom each other during the morning sunning period, which occurs shortly after emergence from the sleeping burrow, or before entering the sleeping burrow in the evening. Grooming was also observed during foraging. A grooming interaction was defined as more than 5 s of grooming. A new grooming interaction was defined as commencing when grooming was separated by intervals of more than 1 min. During each grooming interaction, N.K. identified the grooming initiator, its partner and the duration of grooming for each individual. For polyadic grooming, in which three or more animals groomed together in a huddle, all interactions were recorded as dyads. Grooming was occasionally accom- panied by submission by the subordinate to the dominant male (i.e. high-pitched vocalization and grovelling; Kutsukake & Clutton- Brock 2006a, 2008a); because these events represented submission, they were not included in our analysis. In total, 609 grooming interactions were observed.

Statistical Analysis

We used separate general or generalized linear mixed models (GLMMs;Crawley 2007) to examine predictors of each grooming dependent variable. Mixed models allow both fixed and random terms to be fitted. Random terms take into consideration repeated sampling; we included the group (six groups), the identity of the litter (at maximum, 45 litters) and the identity of each grooming partner (at maximum, 93 individuals) as random terms. We included all likely independent terms and possible interactions in the maximal model and excluded terms sequentially until the model included only the significant terms. The alpha level was set as 0.05. When the estimated variance of a given random term was zero, we excluded that random term from the model. If all random terms were excluded from the model, we used a general or generalized linear model (GLM).

Occurrence and duration of grooming

Dominant males were selective in their grooming partners, resulting in dyad data with no grooming interactions observed. To deal with this biased data distribution (the zero-inﬂated distribution: Martin et al. 2005), we conducted two separate analyses (Cockburn et al. 2008; Garamszegi et al., in press). First, we recorded whether each group member engaged in grooming with the dominant male in each focal observation session (‘occurrence’ of grooming; 0: did not engage; 1: engaged) irrespective of its total duration. In this analysis, we used a GLMM with binomial error structure with a logit link function. Second, we investigated the factors affecting the total duration of grooming in one focal session using data in which grooming occurred at least once. In these analyses, we investigated total grooming duration in each focal observation session as a dependent term. We used a GLMM with a normal distribution and an identity link function for grooming duration (log-transformed to ﬁt a normal distribution).

We conducted the above-mentioned GLMMs on the overall data to investigate the effects of the role of the dominant male in grooming (whether the dominant male groomed or was groomed: categorical), the dominance status of the grooming partner (dominant or subordinate; categorical), the oestrous condition of the dominant female (in oestrus or not in oestrus; categorical) and the size of the group (5–31; continuous). Next, we investigated grooming between the dominant male and each subordinate separately and tested the hypotheses speciﬁc to subordinates. In these analyses, we added the following independent variables, which were speciﬁc to subordinates, in addition to the oestrous condition of the dominant female and the group size: the sex of each subordinate (male or female; categorical) and the age of each

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subordinate (calculated in days, all of which were accurately known, 112–3485 days; continuous). In all analyses, the length of the focal observation session during each observation day was ﬁtted as a covariate (using an offset function:Crawley 2007).

Grooming symmetry

Using GLMMs, we investigated whether grooming exchanges between a dominant male and each grooming partner were positively correlated (balanced) within a dyad, and whether grooming exchanges were symmetrical within a dyad (seeTable 1 for the sample size). Regarding the occurrence of grooming, we investigated whether grooming of the dominant male by a given group member in one focal session predicted whether the dominant male groomed the same group member in the same focal session. We next compared the probability of a grooming occurrence performed and received by the dominant male. In these analyses, we conducted GLMMs with binomial error structure and a logit link function. Similar analyses were conducted on the total amount (duration) of grooming performed and received by dominant males for each grooming partner using a GLMM with a normal distribution and an identity link function.

Contextual analysis of grooming and aggression

To determine whether grooming occurrence was contextually related to aggression performed by a dominant male, we investigated the temporal relationships between grooming and aggression. First, in each focal session we selected the ﬁrst encounter in which grooming of a dominant male by each subordinate occurred, and compared the occurrence of aggression by a dominant male against a subordinate during encounters immediately before and after grooming. Similarly, we selected the ﬁrst encounter in which aggression against each subordinate by a dominant male occurred in each focal session, and compared the occurrence of grooming of the dominant male by subordinates during encounters immediately before and after aggression. Unfortunately, however, aggression rarely occurred during encounters either before or after the grooming (N ¼ 19 dominant– subordinate pair data). Additionally, grooming rarely occurred during encounters either before or after aggression (N ¼ 10 dominant–subordinate pair data). Because of small sample sizes, we did not use GLMMs, but instead conducted Wilcoxon signed- ranks tests based on dominant–subordinate pair data to investigate whether the occurrence of grooming (or aggression) differed between encounters before and after aggression (or grooming). All tests are two tailed.

RESULTS

Factors Affecting the Occurrence of Grooming

Grooming exchanges were a distinctive feature of dominant pairs; dominant males were more likely to groom and be groomed by dominant females rather than by subordinates (GLMMs after controlling for observation time; Table 1, Fig. 1). Oestrous condition also affected the occurrence of grooming. Dominant males were less likely to groom other group members (i.e. dominant females and subordinates) when the dominant females were in oestrus (Fig. 1). Similarly, the probability that a dominant male would receive grooming from a dominant female was higher than was the case for subordinates (Fig. 1). The two-way interaction between oestrous condition and the dominance status of the grooming partner indicates that oestrous condition affected the probability of grooming by subordinates and the probability of grooming by a dominant female (Table 1, Fig. 1). That is, grooming by a dominant female increased while grooming by subordinates decreased during the dominant female’s oestrous period (Fig. 1).

Factors Affecting the Duration of Grooming

Next, we investigated the factors affecting grooming duration using data in which at least one bout of grooming was observed (seeMethods).

The duration of grooming performed by dominant males was affected by the status of the grooming partner and group size (Table 1); dominant males groomed dominant females for longer dura- tions than they groomed subordinates, and the duration of grooming performed by dominant males decreased as group size increased (Fig. 2a).

The duration of grooming received by dominant males was also affected by the status of the grooming partner (Table 1), with dominant females grooming dominant males for longer than subordinates. The two-way interaction between group size and the status of the grooming partner (Table 1) suggests that the effect of group size varies between grooming among dominants and grooming between a dominant male and a subordinate (Fig. 2b). That is, the negative effect of group size on the duration of grooming by a dominant female was stronger than the negative effect of group size on the duration of grooming by subordinates.

Table 1

Effects of factors on the occurrence and duration of grooming between dominant males and other group members

Grooming performed by dominant males Grooming received by dominant males

b (SE) t/z P b (SE) t/z P

Probability of grooming occurrence

Status (dominant>subordinate) L2.378 (0.3668) L6.484 <0.001 L2.813 (0.753) L3.734 <0.001

Group size L0.026 (0.0208) L1.262 0.207 L0.032 (0.017) L1.858 0.063

Oestrous condition (nonoestrous>oestrous) 0.853 (0.387) 2.204 0.028 L0.253 (0.651) L0.389 0.697

Status*oestrous 1.555 (0.750) 2.072 0.038

Grooming duration

Status (dominant>subordinate) L0.438 (0.187)y L2.349 0.021 L1.150 (0.396) L2.905 0.004

Group size L0.042 (0.011)y L3.910 <0.001 L0.006 (0.027) L0.228 0.18

Oestrous condition 0.492 (0.350)y 1.405 0.162 0.364 (0.321) 1.135 0.196

Status*group size 0.063 (0.025) 2.492 0.014

Separate statistics were conducted according to the role of the dominant male. For ‘probability of grooming occurrence’ analyses were conducted on a sample of 1454 dyad- focal-sessions for 93 individuals born in 45 litters of six groups; for ‘grooming duration, performed by dominant males’, 271 dyad-focal-sessions in which at least one grooming interaction was observed for 54 individuals born in 36 litters of six groups; and for ‘grooming duration, received by dominant males’ 378 dyad-focal-sessions in which at least one grooming interaction was observed for 66 individuals born in 38 litters of six groups.

yResults of the generalized linear model (GLM); factors in bold were included in the ﬁnal model.

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Grooming Symmetry

The grooming of each group member by a dominant male was positively related to the amount of grooming that the dominant male received from each group member (grooming occurrence: GLMM: b þ SE ¼ 4.705 þ 2.037, Z ¼ 2.309, P ¼ 0.02; grooming duration: GLMM: b þ SE ¼ 0.468 þ 0.052, t ¼ 8.931, P < 0.001). The asymmetry of grooming was found in both the occurrence of grooming (GLMM: b þ SE ¼ 0.352 þ 0.128, Z ¼ 2.756, P ¼ 0.006) and grooming duration (GLMM: b þ SE ¼ 43.66 þ 10.42, t ¼ 4.190, P < 0.001), with dominant males receiving more grooming than they performed. These results were conﬁrmed for both grooming with dominant females and subordinates (results not shown).

Grooming of Subordinates by the Dominant Male

The probability of the dominant male grooming a subordinate was affected by the oestrous condition of the dominant female, with the dominant male being more likely to engage in grooming with a subordinate when the dominant female was not in oestrus (Table 2,Fig. 1). Other than the oestrous condition of the dominant females, however, the social factors investigated in this study did not affect the occurrence of grooming of a subordinate by a dominant male (Table 2,Fig. 3a).

When grooming was observed to occur at least once between dominant males and subordinates, dominant males groomed subordinate males for longer than they groomed subordinate females (Table 2). An interaction was detected between this effect and group size, thus suggesting that the effect of group size varies with subordinate sex (Fig. 2a). However, the main effect of the group size was not signiﬁcant (Table 2), suggesting that the difference in the effect of group size on grooming subordinate males and subordinate females is biologically less important (Fig. 2a).

Grooming of the Dominant Male by Subordinates

The probability that a subordinate will groom the dominant male was affected by the age of the subordinate and the size of the

group, after controlling for the oestrous condition of the dominant female (Table 2). First, the probability that a dominant male will receive grooming was positively correlated with the age of the subordinate (Fig. 3b). Second, subordinates were more likely to groom dominant males when in small groups than in large groups (Table 2,Fig. 3b).

Regarding grooming performed by subordinates, grooming by subordinate males lasted longer than grooming by subordinate

1

0.5

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(b) 0

1

0.5

0

≤10 11−20 ≥21

Group size

Grooming duration (s/h)

Dominant females Subordinate males Subordinate females

Figure 2. Effects of group size and status/sex of grooming partner on the duration of grooming (a) performed and (b) received by a dominant male. For each dyad between a dominant male and a subordinate, we calculated the duration of grooming for each classiﬁcation of the status/sex of the grooming partner and the group size (classiﬁed into three categories: 10, 11–20, 21). Data were pooled across six groups and are dyadic means SE.

60

50

40

30

20

10

0

Probability of grooming (%)

DM groomed DF

DM groomed Sub Sub groomed DM DF groomed DM

Nonoestrous

Reproductive condition of the dominant female Oestrous

Figure 1. Variation in the probability of grooming occurrence between a dominant male and other group members. Data were classiﬁed according to the oestrous condition of the dominant female, the status of the grooming partner and the role of the dominant male in grooming. DM: dominant male; DF: dominant female; Sub: subordinates. Data were pooled across six groups and are dyadic means SE.

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females (Fig. 2b). Grooming duration increased as group size increased (Table 2,Fig. 2b).

Contextual Analysis of Grooming and Aggression

The grooming of a dominant male by subordinates did not affect the occurrence of aggression (probability of aggression occurrence in the encounter before grooming: mean þ SE ¼ 26.0 þ 6.3%; after grooming: 21.9 þ 6.4%; Wilcoxon signed-ranks test: V ¼ 75.7, N ¼ 19, P ¼ 0.68). Similarly, no statistical difference was seen in the probability of grooming during encounters before and after aggression (probability of grooming in the encounter before aggression: mean þ SE ¼ 19.6 þ 3.6%; after aggression: 6.6 þ 3.0%, Wilcoxon signed-ranks test: V ¼ 38, N ¼ 10, P ¼ 0.08).

DISCUSSION

This study showed that grooming reﬂected the value of social relationships in cooperatively breeding meerkats. First, grooming was most common between dominant individuals (Table 1,Fig. 1), suggesting that the grooming interaction maintained the sexual relationship between the dominant individuals (Kutsukake & Clutton-Brock 2006b; Lo¨ttker et al. 2007). Contrary to our prediction, however, the probability of grooming by dominant males did not increase, but decreased, when the dominant female was in oestrus. This decrease, which was conﬁrmed in the grooming interactions between the dominant male and the subordinates, is probably a result of intensive guarding of the dominant female by the dominant male during her oestrous period, which constrains his general activity (Kutsukake & Clutton-Brock 2008a).

Although the grooming exchanged within a dyad was positively correlated, comparisons of grooming exchanged within a dyad suggest that grooming between dominant males and subordinates was asymmetrical (Fig. 1). Speciﬁcally, dominant males received more grooming from other group members while providing less. Previous studies on cooperatively breeding mammals and birds have shown less despotic grooming distributions (e.g. dominant individuals are more frequent groomers than are subordinates: Gaston 1977; Rasa 1987; Zahavi 1990; Lazaro-Perea et al. 2004). However, similar despotic patterns have been found in some cooperatively breeding vertebrates (meerkats:Kutsukake & Clut- ton-Brock 2006b; green woodhoopoes, Phoeniculus purpureus: Radford & du Plessis 2006) as well as in various group-living animals (primates: Schino 2001). Such despotic grooming

distributions indicate that grooming patterns may be determined by social functions beyond simple reciprocal exchanges (Barrett & Henzi 2006; Schino 2007) and may reﬂect a subordinate’s necessity of ‘paying’ grooming to the dominant individuals to gain social beneﬁts (e.g. tolerance) in a strict dominance hierarchy.

The probability that the dominant male would groom a subordinate was unaffected by the age or sex of the subordinates (Table 2). In a dyad that engaged in at least one bout of grooming, however, the duration of grooming performed by the dominant male towards a subordinate male was longer than the grooming provided towards subordinate females (Table 2,Fig. 2). This result matches our prediction that the dominant male would groom subordinate males that could defend the group from extragroup males, and that grooming serves to maintain valuable relationships. In addition, the grooming by dominant males was unaffected by the age of subordinates (Table 2). This result suggests that parental care is not the primary function of grooming by dominant males. This result is different from patterns found in dominant female meerkats, that is, that dominant females groom younger subordinates more than they groom older ones (Kutsukake & Clutton-Brock 2006b). The differences between dominant males and females are probably driven by sex differences in the intensity of intrasexual conflict in this species. In the case of the dominant female, grooming was rarely observed with mature subordinate females owing to intense intrasexual conflict (Clutton-Brock et al. 2006; Kutsukake & Clutton-Brock 2006b), which might have exaggerated the biased distribution of grooming towards immature subordinates. In contrast, intrasexual conflict was present but relatively moderate among males (Kutsukake & Clutton-Brock 2008a), which may explain why no significant effects of subordinate age on grooming by the dominant male were observed.

Regarding grooming by subordinates, the observed pattern of grooming supports the placation hypothesis for the following reasons. First, subordinates provided more grooming to the dominant male than vice versa (Fig. 1). Second, subordinate males groomed the dominant male more than subordinate females did (Table 2) and older subordinates groomed the dominant male more than younger subordinates did (Table 2). In meerkats, older subordinates are more likely to be attacked by the dominant individual of the same sex (Clutton-Brock et al. 2006; Kutsukake & Clutton-Brock 2006a, 2008a). Given that grooming functions to reduce the tension of the groomee (Feh & de Mazieres 1993; Aureli et al. 1999; Madden & Clutton-Brock 2009), our results suggest that subordinates ‘pay’ grooming to the dominant male to gain Table 2

Effects of factors on the occurrence and duration of grooming between dominant males and subordinates

Grooming performed by dominant males Grooming received by dominant males

b (SE) t/z P b (SE) t/z P

Probability of grooming occurrence

Sex 0.153 (0.290) 0.5297 0.596 0.309 (0.225) 1.373 0.17

Age 0 (0) 1.145 0.252 0.001 (0) 1.987 0.047

Group size 0.030 (0.024) 1.262 0.207 L0.035 (0.017) L2.052 0.04

Oestrous condition (nonoestrous>oestrous) 1.212 (0.539) 2.249 0.025 1.279 (0.389) 3.289 0.001

Grooming duration

Sex (male>female) 0.884 (0.395)y 2.237 0.013 0.705 (0.189) 3.720 <0.001

Age 0.001 (0)y 1.865 0.068 0 (0) 0.077 0.888

Group size L0.017 (0.019)y L0.93 0.470 0.047 (0.018) 2.640 0.018

Oestrous condition 0.763 (0.494)y 1.542 0.127 0.159 (0.387) 0.410 0.583

Sex*group size L0.053 (0.025)^y L2.095 0.040

Separate statistics were conducted according to the role of the dominant male. For ‘probability of grooming occurrence’ analyses were conducted on 1349 data of dyad-focal- sessions for 87 individuals born in 40 litters of six groups; for ‘grooming duration for grooming performed by dominant males’ 199 dyad-focal-sessions in which at least one grooming interaction was observed for 48 individuals born in 31 litters of six groups; and for ‘grooming duration for grooming received by dominant males’ 142 dyad-focal- sessions in which at least one grooming interaction was observed for 60 individuals born in 33 litters of six groups.

yResult of the generalized linear model (GLM); factors in bold were included in the ﬁnal model.

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tolerance or to cope with the risk of aggression. Previous studies on cooperatively breeding societies concluded that helping behaviour by subordinates functions as ‘payment’ to gain other social beneﬁts from a dominant individual (‘pay-to-stay’;Gaston 1978; Bergmu¨ller et al. 2007). Grooming of dominant individuals by subordinates may be another form of payment in cooperatively breeding societies (cf.Port et al. 2009 for noncooperatively breeders; see also Lazaro-Perea et al. 2004and Lo¨ttker et al. 2007for grooming by dominants). Our contextual analysis failed to show temporal links

between aggression and grooming as expected from the tension reduction and placation function. Our analyses, however, are based on a relatively small sample size and conclusions should be drawn from more comprehensive analyses. In the same population of meerkats,Madden & Clutton-Brock (2009)experimentally reduced parasite loads and showed that decreased grooming did not result in an increase in antagonism, and that grooming increased towards individuals that increased their antagonism. These results indicate that grooming is a facultative response to antagonism, but not a preemptive strategy to reduce aggression by an antagonistic individual (Madden & Clutton-Brock 2009).

We found a negative effect of group size on the duration of grooming by dominant males (Table 1) and grooming duration of the dominant male by subordinates (Table 2). This result conforms to predictions from both the time constraint hypothesis (Dunbar 1992; Henzi et al. 1997; Madden et al. 2009) and biological market theory, which suggest that each subordinate individual has decreased value in larger groups (Reyer 1986; Noe¨ et al. 1991; Schaffner & French 1997; Lo¨ttker et al. 2007; Kutsukake & Clutton- Brock 2008a). As explained in the Introduction, negative relationships between grooming and group size do not discriminate between these two explanations. However, the time constraint hypothesis does not explain all patterns observed. Grooming duration by subordinates increased in large groups (Table 2,Fig. 2b) and, as a result, asymmetric grooming relationships between the dominant male and subordinates were exaggerated in large groups. This result ﬁts the biological market theory (Noe¨ et al. 1991; Noe¨ & Hammerstein 1994, 1995; Barrett & Henzi 2006). That is, subordinates in larger groups are less valuable per capita for a dominant male in terms of group defence and helping behaviour, and subordinates are predicted to ‘pay’ more in larger groups according to their own value of cooperation and group defence. A similar exaggeration of grooming asymmetry in large groups was found in a group-living strepsirrhine primate, the redfronted lemur, Eulemur fulvus rufus (Port et al. 2009). Therefore, we conclude that both the time constraint and biological market theory operate in grooming between dominant males and subordinates.

Comparisons of grooming patterns by dominant male and female meerkats reveal several similarities and differences (Table 3). Grooming patterns were similar in several respects: both dominants had stronger grooming relationships with the other dominant than with subordinates, which reflects the highly valuable nature of their relationship; the distribution of grooming was asymmetric, with subordinates grooming dominants of both sexes more than dominants groomed subordinates; and patterns of grooming by subordinates to dominants suggest that grooming serves a placation function for both dominant males and females. At the same time, we found three sex differences (Table 3). First, grooming by dominant females was primarily directed towards younger subordinates, while grooming by dominant males was not affected by the age of subordinates. Second, dominant males were more commonly observed to groom subordinate males, but grooming by dominant females was not affected by the sex of subordinates. Finally, group size affected grooming activity in dominant males, but had no effect on that of dominant females. Overall, these comparisons suggest that grooming in meerkats exhibits sex-specific patterns and that these sex differences reflect the distribution of valuable social relationships for each dominant individual.

In summary, this study provides one of the most detailed analyses of grooming structure in social carnivores. Although the social function of grooming has been intensively investigated in plural-breeding primates (e.g.Schino 2001, 2007; Barrett & Henzi 2006), comparative data are widely lacking in other animals. Our study shows that grooming by the dominant male reﬂects the value

40 (b)

(a)

30

20

2 + years 1−2 years

<1 year

10

Probability of grooming (%)

0 ≤10 11−20 ≥21

40

30

20

10

0 ≤10 11−20 ≥21

Group size

Figure 3. Probability of grooming occurrence between a dominant male and a subordinate in relation to the age of subordinate and the size of the group. (a) Grooming performed and (b) grooming received by a dominant male. Data were pooled across six groups and are dyadic means SE.

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of social relationships within a group and that individuals spend more time servicing social relationships with more valuable partners. This strategic use of grooming is the most important similarity in grooming behaviour between primates and meerkats. At the same time, we found that primate and meerkat grooming patterns were functionally different in the context of mating. Although the use of grooming to achieve mating has been reported in primates (e.g. wild long-tailed macaques, Macaca fascicularis:Gumert 2007), the low grooming activity provided by the dominant male during the oestrous period of the dominant female suggests that a comparable mating function was absent in meerkats. These comparisons illustrate the importance of detailed observations of social interactions for understanding social and reproductive strategies as well as within-group social relationships in group- living animals (Kutsukake 2009).

Acknowledgments

We thank A. Thornton, M. Ridley, N. Raihani, M. Sheehan, R. Snelson, N. Dyer, K. Turner, S. Lanfear, H. Freeman, R. Sutcliffe, H. Hedworth, R. Staff, K. Lederie, M. Rasmussen, A. van Wyk, A. le Roux, N. Tayar, L. Browning, M. Nelson J. Oates, H. Kunc and A. Radford for their support over the course of this study. We especially thank T. Flower, A. Russell, S. Hodge, S. English, S. Sharp, J. Madden, K. Okanoya and K. K. Fujisawa for supporting this study and discussions. We thank Paula Stockley, Peter Henzi and the anonymous referees for valuable comments. This study was ﬁnancially supported by Japan Society for Promotion of Science, RIKEN Special Postdoctoral Researchers Program, PRESTO at JST, Grant-in-Aid for Scientiﬁc Research (no. 18870025), and Hayama Center for Advanced Studies at the Graduate University for Advanced Studies.

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Table 3

Summary of factors inﬂuencing the grooming relationships between dominant and subordinate meerkats: a comparison between this study and our previous study on a dominant female (Kutsukake & Clutton-Brock 2006b)

Dominant males* Dominant femalesy

Given Received Given Received

Grooming between dominants Sexual bonds

(value of social relationships)

Supported Supported Supported Supported

Grooming with subordinates

Asymmetry Given<Received Given<Received

Parental care Not supported (no inﬂuences) d Supported d

Intrasexual conﬂict Not supported (opposite) d Supported d

Time constraint Supported Supportedz Not supported (no inﬂuence) Not supported (no inﬂuence)

Biological market theory (value of social relationships)

Supported d Not supported (no inﬂuence) Not supported (no inﬂuence)

Placation by subordinates _d Supported _d Supported

A dash indicates not tested because the hypothesis made no predictions.

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