ANIMAL BEHAVIOUR, 2008, 75, 1441e1453 doi:10.1016/j.anbehav.2007.09.018

Available online at www.sciencedirect.com

Do meerkats engage in conflict management following aggression? Reconciliation, submission and avoidance N O BU Y U KI K U T S UK AK E*† & TI M H . CLUTT ON- B ROCK *

*Large Animal Research Group, Department of Zoology, University of Cambridge yDepartment of Biological Sciences, Graduate School of Sciences, The University of Tokyo (Received 12 January 2007; initial acceptance 2 March 2007; final acceptance 27 September 2007; published online 21 February 2008; MS. number: 9232R)

Group-living primates and other animals use postaggression (PA) behavioural strategies to reduce the social costs of aggression. However, the relative frequency with which individuals use these conflict management strategies is unclear in many species, and functional analyses of these behaviours are rare. We observed aggression by dominant individuals against group members in cooperatively breeding meerkats, Suricata suricatta, and examined the incidents and effects of PA affiliation between the opponents (reconciliation), avoidance and submission. Aggression had a negative effect on the social relationship between opponents because of an elevated probability of aggression occurrence and an increased time interval until the first nonagonistic PA encounter compared to nonagonistic (control) encounters. The probability of aggression reoccurrence did not decrease with increasing time interval until the first PA encounter, indicating that aggression had long-lasting negative effects on social relationships. Evidence of reconciliation following aggression was not confirmed in this species. Avoidance and submission by the victim characterized the social behaviour following aggression. Although avoidance by victims in the first PA encounter reduced the probability of aggression reoccurrence, submission during aggression neither reduced the probability of aggression reoccurrence nor shortened the time interval until the first PA encounter. These results suggest that avoidance is the only behavioural option for victims of aggression to deal with PA hostility. Reconciliation and other forms of conflict management may be more important in species with low reproductive skew and with opportunities for negotiating relationships between group members than in despotic singular cooperative breeders. Ó 2007 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Keywords: aggression; avoidance; conflict management; meerkats; reconciliation; submission; Suricata suricatta

Group-living animals often experience interindividual conflicts that occasionally develop into aggressive interactions that can have various costs, including the use of time and energy, the risk of injury and damage to dyadic social relationships. The simplest option to reduce the occurrence or escalation of aggression may be to avoid the potential aggressor. In addition, animals may be able to reduce the probability of aggression by submission, appeasement and greeting behaviours that convey the

Correspondence and present address: N. Kutsukake, Laboratory for Biolinguistics, RIKEN Brain Science Institute, 2-1 Hirosawa, Wako-shi, Saitama, 351-0198, Japan (email: [email protected] or kutsu@ darwin.c.u-tokyo.ac.jp). T. H. Clutton-Brock is at Large Animal Research Group, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, U.K. 0003e 3472/08/$34.00/0

nonagonistic intentions of the actor to the opponent (East et al. 1993; Maestripieri 1996; Colmenares et al. 2000; Kutsukake & Castles 2004; Kutsukake et al. 2006), although the empirical effects of these behaviours have seldom been investigated. Friendly reunions of the opponents soon after an aggressive interaction (reconciliation) can also reduce the probability of further aggression and decrease the stress caused by aggression (de Waal & van Roosmalen 1979; Kutsukake & Castles 2001; Aureli et al. 2002). Although mechanisms reducing the costs of aggression (conflict management; Aureli & de Waal 2000) have been intensively studied in primates, the relative frequency with which opponents use these different strategies in other group-living species is unclear (Cords 1997; Schino 2000). Studies of primates have shown that the three strategies are commonly used (avoidance: long-tailed

1441 Ó 2007 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

1442

ANIMAL BEHAVIOUR, 75, 4

macaques, Macaca fascicularis, Aureli 1992; gorilla, Gorilla gorilla, Watts 1995; submission: Maestripieri 1996; Preuschoft & van Schaik 2000; reconciliation: Aureli & de Waal 2000; Aureli et al. 2002). Both avoidance and submission are common in various mammals that live in social groups (e.g. spotted hyenas, Crocuta crocuta, East et al. 1993; Smuts & Smuts 1993). Relatively few studies have investigated the occurrence of reconciliation in nonprimate species, and reconciliation has been reported quantitatively in only a few group-living animals (domestic goats, Capra hircus, Schino 1998; spotted hyenas, Wahaj et al. 2001; bottlenose dolphins, Tursiops truncatus, Samuels & Flaherty 2000; Weaver 2003; Tamaki et al. 2006; absence of reconciliation in domestic cats, Felis catus, van den Bos 1998; rooks, Corvus frugilegus, Seed et al. 2007). Aureli et al. (2002) predicted that reconciliation should be common among species that live in stable social groups, have individualized relationships and experience hostility after aggression, particularly among species in which aggressive interactions disturb valuable social relationships. Given that most previous studies of reconciliation examined primates, this framework needs to be further tested, in particular in nonprimate social animals. Additionally, most conflict management studies have observed captive animals. With regard to reconciliation, it has been argued that there are no differences in its form or frequency in wild and captive primates (reviewed in Colmenares 2006). Still, whether animals living in the wild rely on other behavioural mechanisms, such as avoiding opponents, to reduce the risk of further attacks remains unclear (Sommer et al. 2002). Therefore, data from wild animals is indispensable for complete elucidation of the diversity and evolution of conflict management strategies in group-living animals. We examined these behavioural strategies in a cooperatively breeding carnivore, the meerkat, Suricata suricatta. Meerkats live in multimale, multifemale groups of up to 40 individuals. A dominant pair produces over 80% of the litters (Griffin et al. 2004), whereas subordinate individuals reproduce less frequently and help to rear the offspring of the dominant pair. During a breeding season that lasts approximately 8 months, dominant pairs breed approximately three times. Aggression by dominant individuals against subordinates is frequently observed in meerkats (mean  SE: 2.03  0.33 times per focal observation hour; Kutsukake & Clutton-Brock 2006a, in press), but subordinates attack dominant individuals only when an opportunity for a dominance challenge occurs. Aggression by the dominant individuals reflects the reproductive conflict between same-sex group members (Clutton-Brock et al. 1998; Kutsukake & Clutton-Brock 2006a). For example, aggression by the dominant female manifests during pregnancy; subordinate females over 9 months old are often expelled from the group, whereas subordinate males disperse voluntarily (Doolan & MacDonald 1996, 1997a, b; Clutton-Brock et al. 1998, 2001). Aggression also occurs over food items; dominant individuals attack other group members and steal food from its owner. In meerkats, dominant individuals maintain special affiliative relationships characterized by stable reproductive partnerships with frequent and long-duration grooming and a high probability

of reciprocation that are distinct from those between dominant and subordinate individuals (Clutton-Brock et al. 2006; Kutsukake & Clutton-Brock 2006b), suggesting that the social relationships between dominants are valuable. Additionally, subordinates help rear the offspring of dominant pairs; the growth, survival and successful dispersal of the dominants’ offspring depend on these helping behaviours (Clutton-Brock 2002; Russell et al. 2002, 2003). Therefore, subordinates can be regarded important social resources for dominant individuals, despite the fact that these relationships are asymmetrical and cannot be considered valuable. Because meerkats meet the prerequisite conditions for the evolution of reconciliation as proposed by Aureli et al. (2002), we expected reconciliation to occur in this species. We investigated several questions. Does aggression disturb the social relationship between opponents? How commonly do the victims of aggression show reconciliation, avoidance and submission? Are the strategies used by the victims of aggression effective in reducing the cost of aggression, for example, by reducing the probability of renewed aggression by the dominant individual? Do these behaviours facilitate nonagonistic interactions between opponents following aggression?

METHODS

Study Animals and Field Site This study was conducted in the Kalahari, South Africa, close to Vanzylsrus (26 580 S, 21 490 E), from September to December 2003 and from October to November 2005, as a part of research projects investigating the effects of reproductive conflict on social interactions by dominant individuals (Kutsukake & Clutton-Brock 2006a, b, in press). The study periods corresponded to the beginning of the breeding season, during which 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 198 individuals living in 13 social groups in 2003 and 257 individuals in 12 social groups in 2005. 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 The first author conducted continuous focal observations (Altmann 1974) of the dominant female in nine groups (in 2003) and of the dominant male in six groups

KUTSUKAKE & CLUTTON-BROCK: CONFLICT MANAGEMENT IN MEERKATS

(in 2005). In one study group, the same female was dominant in both 2003 and 2005 but, in the other study groups, the dominant females were different individuals in 2003 and 2005. All of the dominant males were different individuals in 2003 and 2005. The group size varied from nine to 36 individuals in 2003 (median ¼ 19) and from eight to 38 individuals in 2005 (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 3 h 33 min for dominant females (in 2003) and 2 h 50 min for dominant males (in 2005); sessions lasting <1 h were excluded because there was insufficient information about the context of the social behaviours (e.g. the influence of a predator). On average, focal observations were conducted 22 times for dominant females and 18 times for dominant males in each group (2003: range 7e33 times, total observation time 608 h; 2005: range 11e24 times, total observation time 312 h). During observations, we recorded all social interactions involving the focal dominant individual (i.e. all individuals that came within a 1-m radius of the dominant individual; hereafter referred to as ‘encounters’), the type of individual (i.e. focal individual or opponent) that approached and left during an encounter, all aggression received and performed, all submission received and the identity of the interacting partners. Aggressive behaviour was classified as follows: ‘charge’ (running directly at the subordinate), ‘hip-slam’ (slamming the hip against the side of a subordinate), ‘chin mark’ (rubbing the chin on a subordinate), ‘hit’ (swatting a subordinate with one paw), ‘chase’ and physical contact by ‘biting’ (Kutsukake & Clutton-Brock 2006a). Submissive behaviour included high-pitched vocalizations that typically lasted more than a few seconds and grovelling movements or assuming a crouching posture in the presence of the dominant individual (Kutsukake & Clutton-Brock 2006a). Affiliative behaviour included social grooming (manipulation of the fur of other individuals with the mouth), huddling (gathering involving mutual bodily contact between two or more animals), playing (wrestling, clasping and grappling), sniffing (sniffing of anogenital region) and mounting.

Data sets and Comparison between Behaviour after Aggression and Behaviour in Nonagonistic Situations We observed 1874 cases (for dominant females) and 452 cases (for dominant males) of aggression by a dominant individual towards other group members. These data did not include aggression between subordinates. To avoid pseudoreplication caused by the same aggressorevictim dyad within a single observation day and possible influences of previous aggression on the ensuing interactions,

we chose only cases of aggression against a group member that was first observed during one focal observation session and excluded other cases of aggression from the analysis. Acts of aggression by dominant females that resulted in the eviction of subordinate females were excluded from this data set because this aggression was quantitatively different from other types of aggression and no opportunities for social interactions existed after eviction. We classified the context of the aggression into three categories: competition for food (nonforaging individual approached an owner of food or a digging site and attacked the owner, who usually showed defensive action), aggression for no apparent reason (hereafter termed ‘dominance assertion’ because this type of aggression seemed to function in asserting the status of the dominant individual relative to that of the target) and aggression in other contexts (e.g. interruption of grooming, encounters between subgroups following group fission, and severe play that developed into aggression). We excluded aggression that occurred in other contexts because of the low sample size. To examine postaggression (PA) interactions, we focused on the first PA encounter. Traditionally, previous studies have compared PA interactions between opponents to interactions under nonagonistic conditions, which are usually evaluated on the day after the agonistic encounter (the so-called ‘postconflict matched-control’ (PCMC) method; de Waal & Yoshihara 1983). Although the PCMC method is useful for clarifying the characteristics of PA behaviour by comparing it to behaviour during a control situation, several studies have used a relaxed protocol of the PCMC method to analyse PA behaviour in species in which the standard PCMC method cannot be used (e.g. Wahaj et al. 2001; Wittig & Boesch 2003; Kutsukake & Castles 2004). We did not use the traditional PCMC method because the regular observation of nine groups (in 2003) and six groups (in 2005) made it impossible to collect control data systematically on the day following aggression. We therefore used a relaxed protocol and collected control data from the focal observation data on the nearest observation day after aggression was observed (mean interval between aggression date and control date ¼ 5.32 days) and during group activities (foraging or resting) similar to the situation in which the aggression had occurred. These control data were regarded as nonagonistic encounters between opponents. We also collected data from the first encounter that occurred after the control data were collected (the postcontrol encounter), comparing these results to the first PA encounter. Thus, one set of data is composed of aggression, the first PA encounter, a control encounter, and a postcontrol encounter. In meerkats, the dominant female becomes more aggressive during late pregnancy (Kutsukake & Clutton-Brock 2006a), but the dominant male does not (unpublished data). Therefore, we chose control data for dominant females from the observation data after the day on which aggression was observed; thus, this analysis is conservative because the increased aggressive tendency in the control data compared to the aggression data should hamper the detection of avoidance, submission and aggression occurrence during the PA period. We also calculated the time interval between the control encounter and the next

1443

1444

ANIMAL BEHAVIOUR, 75, 4

If aggression disturbs the social relationship between opponents, the opponents will be separated for a long time following aggression relative to their separation during a control situation. We tested this idea by comparing the time interval in minutes between an agonistic encounter and the first PA encounter to the interval between the two encounters during the control conditions. In this analysis, we excluded data for which aggression reoccurrence was observed in the first PA encounter. Because the time interval between two encounters was a positive integer, we used this as a dependent variable with a Poisson error structure in a GLMM (Crawley 2002).

encounter between the opponents and regarded this as the time interval between encounters during the nonagonistic control situation. We analysed 501 cases for dominant females and 138 cases for dominant males (Table 1).

Statistical Analyses Does aggression disturb the social relationship between opponents? If aggression disturbs the social relationship between opponents, the risk of aggression occurrence between former opponents will be higher following aggression than during nonagonistic situations. We evaluated this idea using generalized linear mixed models (GLMMs; Schall 1991). GLMMs allow both fixed and random terms to be fitted to a model. Random terms take into consideration repeated sampling. When the random terms did not have a statistical effect, we excluded them and used a generalized linear mixed model. As random terms, we included the group (i.e. to account for the identity of the focal dominant individual), the identity of the subordinate’s litter (i.e. to account for any similarities in behaviour among subordinates from the same litter) and the identity of each subordinate individual (i.e. to account for pseudoreplication caused by including the same aggressorevictim dyad). The dependent variable was a binary term (binomial error structure) of whether the focal dominant individual attacked the opponent (i.e. attacked ¼ 1; not attacked ¼ 0). The probability of aggression occurrence was compared between the first PA encounter and the postcontrol encounter.

How commonly do meerkats reconcile after aggression? We investigated whether meerkats reconcile soon after aggression (i.e. within 10 min) by simply counting the number of aggressive acts that were followed by reconciliation. We also counted the frequency of affiliation between opponents during the 10 min after the corresponding nonagonistic (i.e. control) encounter and compared the frequencies of reconciliation and affiliation during nonagonistic conditions using a Wilcoxon signedranks test. For each dominant individual, we calculated the corrected conciliatory tendency (Veenema et al. 1994) as follows: [(the observed number of affiliations during the PA period)  (the observed number of affiliations during the control period)]/(the total number of aggression events); individual means are reported. Because individuals that form special bonds likely reconcile more frequently than other dyads (the ‘relationship value’ hypothesis; de Waal & Yoshihara 1983; Cords & Aureli 2000; Aureli et al. 2002), reconciliation may be common

Table 1. Aggressive encounters and the frequency of affiliation between opponents during 10-min periods following aggression (reconciliation) and nonagonistic encounters (postcontrol) Group size Aggressor Dominant female

Victim

Age

4e10

11e20

21e30

>31

Total

Subordinate female (N¼289)

0e1 1e2 2e3 3< 0e1 1e2 2e3 3< Total

6 [0,0] 2 [0,0] d 1 [0,0] 8 [0,0] 1 [0,0] 1 [0,0] 5 [0,0] 24 [0,0]

76 [1,1] 80 [1,3] 4 [1,0] d 45 [1,1] 39 [1,0] 14 [0,0] 14 [0,0] 272 [5,5]

28 [0,2] 37 [0,1] 10 [1,0] 5 [0,1] 16 [0,0] 11 [0,0] 7 [0,0] 4 [0,0] 118 [1,4]

5 [0,0] 21 [0,0] 11 [0,0] 3 [0,0] 5 [0,0] 2 [0,0] d 3 [0,0] 50 [0,0]

115 [1,3] 140 [1,4] 25 [2,0] 9 [0,1] 74 [1,1] 53 [1,0] 22 [0,0] 26 [0,0] 464 [6,9]

0e1 1e2 2e3 3< 0e1 1e2 2e3 3< Total

1 4 7 9 3

[0,0] [0,0] [0,0] [0,0] [0,0] d d 8 [1,0] 32 [1,0]

d 2 [0,0] 1 [0,0] 2 [0,0] d 9 [1,0] 1 [0,0] 19 [0,0] 34 [1,0]

d d 1 [0,0] d d d d 7 [0,0] 8 [0,0]

d d 1 [0,0] 1 [0,0] d 2 [0,0] 1 [0,0] 16 [0,0] 21 [0,0]

1 [0,0] 6 [0,0] 10 [0,0] 12 [0,0] 3 [0,0] 11 [1,0] 2 [0,0] 50 [1,0] 95 [2,0]

5 [1,0] 14 [1,0] 19 [2,0]

23 [0,1] 21 [0,2] 44 [0,3]

8 [0,0] 1 [0,0] 9 [0,0]

1 [0,0] 7 [0,0] 8 [0,0]

37 [1,1] 43 [1,2] 80 [2,3]

Subordinate male (N¼175)

Dominant male

Subordinate female (N¼29)

Subordinate male (N¼66)

Dominant female Dominant male

Dominant male Dominant female Total

The number of affiliations during the PA period and during the control period is shown in brackets.

KUTSUKAKE & CLUTTON-BROCK: CONFLICT MANAGEMENT IN MEERKATS

only between dominant individuals and not between dominant and subordinate individuals. In meerkat societies, dominant individuals maintain special relationships, characterized by frequent grooming, which are distinct from the relationships between the dominant individual and the subordinates (Kutsukake & Clutton-Brock 2006b). Therefore, we separately analysed PA behaviour between the dominant individuals and PA behaviour between a dominant individual and the subordinates. To test whether dominant individuals reconcile more frequently than dominantesubordinate pairs, we compared the corrected conciliatory tendency between dominants and between a dominant and a subordinate using a Wilcoxon signed-ranks test. With regard to aggression against subordinates, we investigated whether the occurrence of reconciliation was affected by other social factors, such as group size and the opponent’s sex and age.

How commonly do meerkats avoid the aggressor after aggression? Avoidance was defined as an encounter in which the aggressor approached the victim and the victim left the approaching aggressor. Other victim reactions (e.g. approaching the aggressor or not leaving the approaching aggressor) were considered encounters in which the victim did not avoid the aggressor. To compare the proportion of avoidance encounters between the first nonagonistic PA encounter and the nonagonistic postcontrol encounter, encounters showing avoidance by the victim were assigned a value of 1 and all other encounters were assigned a value of 0; this was used as a dependent variable with binomial error structure in a GLMM (Crawley 2002). The probability that the victim of aggression avoided the aggressor was compared between the first nonagonistic PA encounters and the nonagonistic postcontrol encounters. We excluded encounters in which individuals simultaneously approached or left each other.

How commonly do meerkats submit to the aggressor? Meerkats occasionally submit to the aggressor during or immediately after receiving aggression. If the submission occurs in response to the risk of aggression, the victim of aggression will increase its submission to the dominant individual not only in agonistic encounters but also in the first PA encounter relative to nonagonistic encounters. To test this prediction, whether the opponent submitted was set as a dependent variable with binomial error structure in a GLMM, and its rate was compared among three conditions: during agonistic encounters, during the first PA encounter and during control encounters. We predicted that the submission rate in agonistic encounters and the first PA encounter would be higher than that in the nonagonistic control.

What predicts aggression reoccurrence between opponents and is PA behaviour effective in reducing the costs of aggression? After investigating the occurrence of reconciliation, submission and avoidance, we investigated the effects of submission behaviours. We did not investigate the effect

of reconciliation because reconciliation rarely occurred (see Results). Therefore, we focused on avoidance and submission in subsequent analyses. We investigated factors affecting aggression reoccurrence between the opponents to examine the long-term effects of aggression on PA behaviour between opponents and the function of avoidance and submission on subsequent interactions with the dominant individual. If negative effects of aggression on the PA social interactions between opponents are long lasting, the agonistic tendency by the dominant individual (i.e. the probability of aggression reoccurrence) will not decrease with increasing time. If avoidance or submission reduces the aggressive tendencies of the dominant individual, the probability of renewed aggression from the dominant individual should decrease when the opponent shows these behaviours. To test these ideas, we used the dependent variable of whether the dominant individual attacked the opponent in the first PA encounter (i.e. attacked ¼ 1, not attacked ¼ 0; binomial error structure) in a GLMM. The independent variables were the time interval between the aggressive act and the first PA encounter, whether the opponent showed avoidance during the first PA encounter and whether the opponent showed submission during the agonistic encounter. To examine the function of submission, we conducted three additional analyses. If submission in agonistic encounters moderates hostile relationships between the opponents, the time interval between the agonistic encounter and the first PA encounter should be shorter when the victim submits to the dominant individual relative to when the victim does not. We tested this by setting the time interval between the agonistic encounter and the first PA encounter as a dependent term and whether the victim showed submission as an independent term in a GLMM with Poisson error structure. Then we reran this analysis using only data in which aggression reoccurrence was observed at the first PA encounter to test the possibility that submission by victims functions to delay aggression reoccurrence. Additionally, if submission functions to facilitate future interactions between the opponents, the victim of aggression should not avoid the aggressor in the first nonagonistic PA encounter. We tested this by setting whether the victim avoided the aggressor in the first nonagonistic PA encounter as a dependent term in a GLMM with binomial error structure and investigated the effect of the presence of submission by setting the presence of submission as an independent term. In all statistical analyses, we controlled for the effect of the context of aggression by using it as an additional independent term. Because we observed dominant females in 2003 and dominant males in 2005, we initially analysed data collected in 2003 and in 2005 separately. However, the results did not differ between these two data sets, so we report the results of analyses of the pooled data. In these analyses, we used observation year as an additional independent term. We also included the dominance status of the opponents as an independent term to investigate whether PA behaviour differs for aggression between dominants and aggression between a dominant and

1445

1446

ANIMAL BEHAVIOUR, 75, 4

a subordinate. The results in which this term was not included in the final model suggest that the results did not vary between dominantesubordinate and dominante dominant interactions. Following Crawley (2002), we included all independent terms in the maximal model and then excluded terms sequentially by systematically removing the independent term with the largest Akaike’s information criterion (AIC) increase until the most parsimonious model with the minimum AIC was obtained.

RESULTS

Does Aggression Disturb the Social Relationship between Opponents? Aggression disturbed the social relationship between opponents. The probability of aggression occurrence was higher during the PA encounter than during the nonagonistic encounter (Table 2). This effect was independent of the statistical effect of aggression context; the probability of aggression was lower after aggression over food than after dominance assertion (Table 2). Also, there was a longer time interval between an aggressive encounter and the PA encounter than between nonagonistic encounters (Table 2).

How Commonly Do Meerkats Reconcile after Aggression? Meerkats did not affiliate with their opponents soon after aggression. Of 639 cases of aggression, only 10 cases

(1.6%) of PA affiliation occurred between the opponents within 10 min of the end of the agonistic interaction (Table 1). The proportion of agonistic encounters in which affiliation was observed within 10 min was 2.5% (2/80) in aggression between dominants and 1.4% (8/559) in aggression between a dominant and a subordinate individual (Table 1). In contrast, affiliation was observed in 12 postcontrol encounters. There was no statistical difference between the frequency of affiliation between the opponents in PA ðX  SE ¼ 2:2  1:0%Þ and that in control encounters (1.3  0.4%; Wilcoxon signed-ranks test: W ¼ 109, N ¼ 11, P ¼ 0.90). This result did not change when we separated aggression between dominants from aggression between a dominant and a subordinate individual. The individual mean  SE for corrected conciliatory tendency was 0.9  0.01%). The corrected conciliatory tendency did not differ between dominante dominant (0.0  0.2%) and dominantesubordinate interactions (0.6  1.2%; Wilcoxon signed-ranks test: W ¼ 108, N ¼ 10, P ¼ 0.63). The extremely small number of reconciliations suggests that the occurrence of reconciliation is not related to group size or to the ages or sexes of the opponents (Table 1).

How Commonly Do Meerkats Avoid the Aggressor after Aggression? Victims of aggression avoided the aggressor after aggression. The proportion of cases in which the victim avoided the aggressor was higher in the nonagonistic PA encounters than in postcontrol encounters (Table 3). Also, the victims avoided dominant females more frequently than they avoided dominant males (Table 3).

Table 2. Factors affecting the probability of aggression between opponents and the time interval between encounters Mean [SE] Independent term

Aggression occurrence (%)*

Time interval (min)x

Condition (PA: postaggression; CTR: control)

CTR: 5.15 [0.09]
CTR: 20.15 [1.97]
Context of aggression (FC: foraging competition; DA: dominance assertion)

FC: 7.12 [1.59]
FC: 22.02 [2.18]¼DA: 24.13 [2.56] Exp(b) [Exp(bSE)]¼1.04 [1.150.94], t797¼0.36, P¼0.72

Status of the victim (DOM: dominant individual; SUB: subordinate)

DOM: 8.15 [2.10]¼SUB: 9.89 [1.60]y b [SE]¼0.12 [0.30], t78¼0.38, P¼0.70

DOM: 13.17 [2.42]¼SUB: 25.24 [2.33] Exp(b) [Exp(bSE)]¼0.73 [0.900.59], t74¼1.50, P¼0.14

Sex of the dominant individual (i.e. study year; DF: dominant female, 2003; DM: dominant male, 2005)

DF: 9.84 [0.90]¼DM: 9.07 [2.40] b [SE]¼0.02 [0.25], t13¼0.09, P¼0.93

DF: 26.19 [3.00]¼DM: 21.98þ[3.53] Exp(b) [Exp(bSE)]¼0.76 [0.890.64], t13¼1.73, P¼0.11

Random terms (intercept) Group Litter Individual

Standard deviation dz d d

Standard deviation 0.14 0.18 0.45

For each independent term, the marginal individual mean  SE and results are shown. Results in bold remained in the final model. *Results of a generalized linear mixed model are shown. y‘¼’ Indicates no statistical difference. zThe random term was excluded from the model because it had no statistical effect. xExp(b) indicates an exponent of b, which represents the ratio of the time interval between the two categories compared in the analysis.

KUTSUKAKE & CLUTTON-BROCK: CONFLICT MANAGEMENT IN MEERKATS

Table 3. Factors affecting avoidance by the victim of aggression Avoidance by subordinates (%) Independent term

Mean [SE]

Condition (PA: postaggression; CTR: control)

Agg: 72.32 [5.44]>CTR: 65.75 [2.63] b [SE][0.70 [0.15] t894[4.57, P<0.0001

Context of aggression (FC: foraging competition; DA: dominance assertion)

FC: 64.52 [6.15]¼DA: 70.99 [2.82] b [SE]¼0.21 [0.17], t731¼1.23, P¼0.22

Status of the victim (DOM: dominant individual; SUB: subordinate)

DOM: 70.53 [6.23]¼SUB: 69.69 [2.83] b [SE]¼0.03 [0.25], t71¼0.08, P¼0.91

Sex of the dominant individual (i.e. study year; DF: dominant female, 2003; DM: dominant male, 2005)

DF 75.62 [2.35]>DM 59.17 [4.23] b [SE][0.90 [0.20], t13[4.43, P<0.0001

Random terms (intercept) Group Litter Individual

Standard deviation 0.18 0.26 d

For each independent term, the marginal individual mean  SE and results are shown. Results in bold remained in the final model.

How Commonly Do Meerkats Submit to the Aggressor? Aggression increased the probability that victims submitted to the dominant individual. The submission frequency by victims varied among agonistic encounters, first nonagonistic PA encounters and second nonagonistic control encounters: the victim submitted to the dominant individual in agonistic encounters and during the first nonagonistic PA encounter more frequently than during nonagonistic control encounters (Table 4). Also, victims submitted to the dominants less frequently in aggression caused by food than in aggression for dominance assertion (Table 4). Submission was rarely observed during agonistic encounters between dominants (one case by a dominant female and one case by a dominant male)

and was not observed in PA or control encounters. This resulted in a statistical difference in submission frequency for the dominant and subordinate opponents (Table 4).

What Predicts Aggression Reoccurrence and Are Avoidance and Submission Effective in Reducing the Costs of Aggression? Aggression had long-lasting effects on the PA behaviour between opponents. The probability of renewed aggression did not decrease with increasing time after aggression (Table 5, Fig. 1), suggesting that PA hostility did not vary by time after aggression. Victims that showed avoidance during the PA encounter were less likely to be reattacked by the aggressor than victims that did not avoid the

Table 4. Factors affecting submission by the opponents Submission (%) Independent term

Mean [SE]

Condition (Agg: aggression; PA: postaggression; CTR: control)

Agg: 38.10 [4.22]>CTR: 10.77 [2.35] b [SE][L2.39 [0.17], t1583[L14.59, P<0.0001 Agg: 38.10 [4.22]>PA: 14.16 [2.02] b [SE][L1.89 [0.15], t1583[L12.63, P<0.0001 CTR: 10.77 [2.35]
Context of aggression (FC: foraging competition; DA: dominance assertion)

FC: 9.51 [1.56]
Status of the victim (DOM: dominant individual; SUB: subordinate)

DOM: 1.67 [1.25]
Sex of the dominant individual (i.e. study year; DF: dominant female, 2003; DM: dominant male, 2005)

DF: 23.28 [3.25]¼DM: 17.61 [2.48] b [SE]¼0.07 [0.29], t13¼0.23, P¼0.82

Random terms (intercept) Group Litter Individual

Standard deviation 0.28 0.42 0.75

For each independent term, the marginal individual mean  SE and results are shown. Results in bold remained in the final model.

1447

ANIMAL BEHAVIOUR, 75, 4

Table 5. Factors affecting a probability of aggression reoccurrence following aggressive encounters Aggression reoccurrence (%) Independent term

Mean [SE]

Submission (SUB: submitted, NO SUB: not submitted)

SUB: 16.08 [2.97]>NO SUB: 13.43 [2. 99] b [SE][1.91 [0.25], t651[L12.47, P<0.001

Avoidance by the victim of aggression

avoid: 12.85 [2.02]
Status of the victim (DOM: dominant individual; SUB: subordinate)

DOM: 16.09 [4.45]¼SUB: 15.92 [2.88] b [SE]¼0.35 [0.34], t651¼1.04, P¼0.30

Sex of the dominant individual (i.e. study year; DF: dominant female, 2003; DM: dominant male, 2005)

DF: 16.28 [2.71]¼DM: 15.41 [5.98] b [SE]¼0.53 [0.28], t13¼1.92, P¼0.08

Context of aggression (FC: foraging competition; DA: dominance assertion)

FC: 10.32 [2.53]¼DA: 17.01 [2.91] b [SE]¼0.24 [0.27], t651¼0.88, P¼0.38

Time interval until the first nonagonistic PA encounter

b [SE]¼0 [0], t651¼0.53, P¼0.60

Random terms (intercept) Group Litter Individual

Standard deviation 0.11 d d

For each independent term, the marginal individual mean  SE and results are shown. Results in bold remained in the final model.

aggressor (Table 5). The probability of renewed aggression did not decrease, but rather increased, when the subordinate submitted to the dominant individual during the aggressive interaction (Table 5). Additional analyses indicated that submission did not facilitate nonagonistic interactions between the opponents. The time interval until the first PA encounter was not affected by whether the subordinate submitted to the dominant individual during the aggressive interaction in analyses using all data or using only data with aggression reoccurrence (Table 6). Finally, submission during aggression did not affect which of the opponents (i.e. the focal dominant animal or the victim) avoided the aggressor during the first nonagonistic PA encounter (Table 7). 30

% Aggression

1448

20

10

0

0–15

16–30 31–45 Time after aggression (min)

46+

Figure 1. Relationship between the time interval until the first encounter after aggression and the probability of renewed aggression in the first PA encounter. Individual mean  SE is shown.

DISCUSSION In meerkats, aggression had negative effects on social interactions between the opponents following aggression. This is because, relative to nonagonistic interactions, aggression between opponents was more likely to occur after previous aggressive encounters and because the opponents did not interact after aggression for a long interval. These results suggest that aggression disturbs social relationships in meerkats. Because social relationships between dominant individuals can be regarded as valuable and subordinates are important social resources for dominant individuals, meerkats fit the prerequisite conditions for the occurrence of reconciliation proposed by Aureli et al. (2002). However, PA affiliation between opponents (reconciliation) was quite rare, occurring in only 1.6% of cases following an aggressive act. This frequency did not differ from the affiliation frequency during the control encounters. The corrected conciliatory tendency in meerkats is substantially lower than the corrected conciliatory tendency reported for primates (range 6.4e 77.0%; data from Table 36.1 in Arnold & Aureli 2006). Given that primate studies based on smaller sample sizes than those in our study have found statistical evidence for the occurrence of reconciliation (e.g. about 200 data points in Kutsukake & Castles 2004), it is unlikely that our failure to detect reconciliation was an artefact of our methodology or sample size. One could say that reconciliation occurs in specific dyads or during specific social conditions. For example, group size varied in this study and it was expected that each helper would be of greater value to dominant individuals in small groups, in which only a few helpers were available, than in large groups (Schaffner et al. 2005; Aureli & Schaffner 2006). However, the extremely low rate of reconciliation seems to suggest that the absence of reconciliation did not depend on

KUTSUKAKE & CLUTTON-BROCK: CONFLICT MANAGEMENT IN MEERKATS

Table 6. Factors affecting the time interval until the first PA encounter following aggressive encounters Time interval until the first PA encounter (min) Mean [SE] Independent term

All data

Data with aggression reoccurrence

Submission (SUB: submitted, NO SUB: not submitted)

SUB: 25.93 [4.22]¼NO SUB: 26.98 [3.06] Exp(b) [Exp(bSE)]¼0.91 [1.080.77], t370¼0.52, P¼0.60

SUB: 28.60 [6.00]¼NO SUB: 16.61 [3.22] Exp(b) [Exp(bSE)]¼0.98 [1.230.78], t23¼0.11, P¼0.92

Status of the victim (DOM: dominant individual; SUB: subordinate)

DOM: 15.75 [3.49]
DOM: 10.70 [3.46]¼SUB: 23.72 [4.05] Exp(b) [Exp(bSE)]¼0.50 [0.720.35], t18¼1.88, P¼0.08

Sex of the dominant individual (i.e. study year; DF: dominant female, 2003; DM: dominant male, 2005)

DF: 30.96 [3.31]¼DM: 19.02 [3.07] Exp(b) [Exp(bSE)]¼0.66 [0.790.55], t13¼1.02, P¼0.33

DF: 20.80 [2.21]¼DM: 22.37 [7.64] Exp(b) [Exp(bSE)]¼1.05 [1.380.80], t12¼0.18, P¼0.86

Context of aggression (FC: foraging competition; DA: dominance assertion)

FC: 22.22 [3.78]¼DA: 26.59 [3.23] Exp(b) [Exp(bSE)]¼1.08 [1.210.97], t370¼0.68, P¼0.50

FC: 15.30 [5.32]¼DA: 23.20 [4.42] Exp(b) [Exp(bSE)]¼0.69 [0.840.57], t23¼1.34, P¼0.19

Random terms (intercept) Group Litter Individual

Standard deviation 0.24 d 0.35

Standard deviation d d 0.58

One analysis used all data and the other analysis used data with aggression reoccurrence. For each independent term, the marginal individual mean  SE and results are shown. Results in bold remained in the final model.

group size (Table 1). The failure to detect reconciliation may have been caused by the study design in which we focused on aggression during the breeding season and meerkats might reconcile more frequently during the nonbreeding season. For example, primate studies have shown that reconciliation is unlikely to occur when aggression occurs over a resource such as food (Arnold & Aureli 2006). This study was conducted during the breeding season; therefore most cases of aggression may reflect reproductive conflict. However, reconciliation was not observed even between heterosexual dyads of a dominant and a subordinate individual (Table 1). This suggests that

competition for specific resources cannot explain the absence of reconciliation in meerkats. Similarly, we observed aggression only by dominant individuals; reconciliation may occur following aggression between subordinates, but we did not observe such encounters. Although we have not systematically collected sufficient data during the nonbreeding season or on aggression among subordinates, our personal observations suggest that the behaviour patterns (i.e. the occurrence of reconciliation) after aggression in such situations is not qualitatively different from the results presented here. Although more observations are needed, we believe that the absence of

Table 7. Factors affecting avoidance by victims at the first nonagonistic PA encounter Avoidance by subordinates (%) Independent term

Mean [SE]

Submission (SUB: submitted, NO SUB: not submitted)

SUB: 69.65 [7.10]¼NO SUB: 70.58 [5.82] b [SE]¼0.08 [0.36], t363¼0.23, P¼0.82

Status of the victim (DOM: dominant individual; SUB: subordinate)

DOM: 71.52 [6.82]¼SUB: 71.52 [4.97] b [SE]¼0.03 [0.44], t85¼0.20, P¼0.94

Sex of the dominant individual (i.e. study year; DF: dominant female, 2003; DM: dominant male, 2005)

DF: 84.31 [2.29]>DM: 50.11 [4.19] b [SE][L2.15 [0.29], t13[7.32, P<0.001

Context of aggression (FC: foraging competition; DA: dominance assertion)

FC: 68.08 [7.01]¼DA: 69.37 [6.72] b [SE]¼0.15 [0.23], t363¼0.69, P¼0.49

Time interval until the first nonagonistic PA encounter

b [SE]¼0 [0], t363¼1.18, P¼0.24

Random terms (intercept) Group Litter Individual

Standard deviation 0.20 d 1.02

For each independent term, the marginal individual mean  SE and results are shown. Results in bold remained in the final model.

1449

1450

ANIMAL BEHAVIOUR, 75, 4

reconciliation is not caused by the social or seasonal factors discussed here. Then, why do meerkats not reconcile? In primate studies, the relationship value hypothesis suggests that animals reconcile with an individual whose relationship is biologically valuable (de Waal & Yoshihara 1983; Cords & Aureli 2000). In our study, the absence of reconciliation between dominant and subordinate individuals may be explained by the absence of valuable relationships; however, reconciliation was not observed even in the dominant pairs, which maintained stable relationships (see Introduction). This result does not fit the relationship value hypothesis. Relationship ‘security’, which is a dimension of the quality of a relationship that relates to the perceived probability that the relationship will change, may partly explain the absence of reconciliation (Cords & Aureli 1993, 2000). That is, reconciliation may not be necessary between individuals (e.g. relatives) whose relationship is highly secure even when it is disturbed by aggression. However, it is unlikely that such relationships are secure in meerkat societies because there is intense intrasexual reproductive conflict between these individuals (Clutton-Brock et al. 1998, 2001; Kutsukake & CluttonBrock 2006a, b, in press). Previous studies of PA behaviour in primates have provided three cases for the absence of reconciliation at the species level (Schaffner & Caine 2000; Westlund et al. 2000; Roeder et al. 2002; Schaffner et al. 2005; see also Kappeler 1993; Rolland & Roeder 2000 for ring-tailed lemurs, Lemur catta). For black lemurs, Eulemur macaco, living in small multimaleemultifemale groups with plural female breeding, affiliations between opponents were high shortly after both aggression and control periods, in which reconciliation was not statistically demonstrated (Roeder et al. 2002). In two primate species with high reproductive skew (i.e. cooperative breeders) in which PA behaviour was investigated, diverse results on the occurrence of reconciliation have been reported. A study of common marmosets, Callithrix jacchus jacchus, showed evidence of reconciliation because the frequency of PA affiliation was higher soon after aggression than during nonagonistic (control) conditions (Westlund et al. 2000). However, most PA affiliations in this species included being in proximity or approaching; thus, whether these implicit behaviours can be truly labelled ‘reconciliation’ is still unknown (Aureli & Schaffner 2006). In captive red-bellied tamarins, Saguinus labiatus, aggression was rarely observed within a group, and opponents affiliated soon after aggression and during nonagonistic control conditions, such that the occurrence of the reconciliation was not statistically detected (Schaffner & Caine 2000; Schaffner et al. 2005). From this result, Schaffner & Caine (2000) proposed that cooperative breeders living in peaceful societies do not require reconciliation after aggression. However, the results of our study indicate that a lack of reconciliation is also evident in species such as meerkats that live in societies with frequent aggression (Kutsukake & Clutton-Brock 2006a) and aggression disturbed the social relationship between opponents. These comparisons indicate that the peacefulness of these societies is not the sole factor explaining the absence of reconciliation in cooperatively breeding species.

From these interspecific comparisons, we infer that the combination of cooperative breeding with strong reproductive skew and the despotic characteristics of meerkat society may explain the absence of reconciliation in meerkats and may partly explain similar trends in some primate species. Reproductive skew is stronger in cooperatively breeding species than in group-living primates and other animals (e.g. spotted hyenas) in which the occurrence of reconciliation has been statistically detected. In cooperatively breeding species, subordinates may have little room for ‘compromise’ or ‘negotiation’ in terms of reproductive opportunities (Clutton-Brock et al. 2001; Kutsukake & Clutton-Brock 2006a, b). Therefore, it may be meaningless for subordinates to reconcile after aggression because reconciliation does not modify the behaviour of the dominant individuals or resolve the conflict between individuals. In contrast, subordinates in species with low reproductive skew may be able to modify the behaviour of other individuals to some extent by strategic grooming and coalition formation (Cords 1997), which ultimately increase the fitness of the actors (Silk et al. 2003). Reconciliation may evolve only in species where the possibility of negotiation among group members exists but not in cooperatively breeding or eusocial species. In addition, it should be noted that the absence of reconciliation in meerkats is quantitatively distinct from the lack of reconciliation shown for the above-mentioned primate species. Meerkats seldom affiliated with opponents in both PA and control situations, whereas other species showed increased affiliation during both PA and control conditions. The extremely low rate of PA affiliation in meerkats, relative to that of common marmosets and red-bellied tamarins, may be explained by the despotic characteristics of meerkat society, in which aggression is frequent and relationships between dominants and subordinates are asymmetrical. These considerations highlight the necessity of considering multiple social factors, such as reproductive skew and species-specific societal characteristics, when constructing a comprehensive framework for the evolution of reconciliation. Previous studies of conflict management have focused on explicit behaviours such as reconciliation, but alternative mechanisms such as avoidance and submission have rarely been investigated. In meerkats, victims showed avoidance and submission to the dominant individual. Sommer et al. (2002) reported that wild hanuman langur, Semnopithecus entellus, rarely reconcile after aggression and proposed that avoidance is an important mechanism that modulates the occurrence of aggression, particularly in wild animals that do not have spatial limitations. However, they did not provide quantitative data on avoidance and its effects on PA interactions between opponents. Beyond investigating the occurrence of alternative conflict mechanisms, we empirically examined the functions of PA behaviour. Our analyses showed that victims that avoided the aggressor were less likely to be reattacked than victims that did not avoid the aggressor, suggesting that avoidance functions in conflict management. On the other hand, submission does not decrease the social costs of aggression in meerkats. Aggression had a long-lasting negative effect on the relationship between opponents

KUTSUKAKE & CLUTTON-BROCK: CONFLICT MANAGEMENT IN MEERKATS

because the probability of renewed aggression did not vary with the time interval between the aggressive act and the first PA encounter. Theoretically, submission can convey the relative subordinate status of the actor and may function to prevent the occurrence of aggression. Thus, we hypothesized that submission functions to reduce the possibility of renewed aggression between opponents (Maestripieri 1996; Preuschoft & van Schaik 2000; Matsumura & Hayden 2006). However, submission did not decrease the probability of renewed aggression, did not shorten the time interval between the aggression and the first PA encounter and did not affect the initiator of PA encounters. These results suggest that submission during agonistic situations does not decrease the costs of aggression, which disagrees with the generally assumed function of submission. One explanation for this result is that the function of submission differs according to social context; submission during an agonistic situation may not function in conflict management. For example, Flack & de Waal (2007) reported that submission signals (i.e. display of bared teeth) in pigtailed macaques, Macaca nemestrina, have different social functions during nonagonistic situations and during aggression. Similarly, submission in nonagonistic conditions may decrease the agonistic tendency by dominant individuals in meerkats, but submission in an aggressive context may not have the same effect. Although classifying submission according to context is uncommon, better classification is necessary to empirically test the function of submission in each social context. In summary, meerkats have limited behavioural options to reduce the social costs of aggression. Avoidance appears to be the only behavioural option for victims of aggression when dealing with PA hostility; reconciliation was absent and submission was ineffective in reducing the agonistic tendency of dominant individuals. Negative results are always difficult to interpret, but our results suggest that the conflict management strategy in meerkats is qualitatively different from those in group-living primates and other group-living species in which reconciliation has been detected statistically. Detailed analyses of conflict management are biased towards group-living primates (Aureli et al. 2002; Arnold & Aureli 2006; Colmenares 2006); similar attempts in other species are rare. Our study expanded the framework to a nonprimate group-living carnivore living under natural conditions. Our results also highlight the unresolved question of how widely the behavioural framework proposed from primate studies can be applied to other group-living animals. In addition, most previous studies of conflict management have reported the occurrence of PA behaviour, but few studies have empirically investigated its functions. To our knowledge, this is the first investigation of multiple behaviours and their effects on PA interactions between opponents. Our results highlight the importance of functional analyses of PA behaviours that are regarded as conflict management. These analyses should stimulate further investigation of conflict management in group-living species with various social systems, in particular in nonprimates, and further the elucidation of the mechanisms of relationship regulation and social cognition in social animals (Cords 1997; Schino 2000; de Waal & Tyack 2003).

Acknowledgments We thank S. English, K. Moyes, Z. Fry, F. Ballantyne, M. Baker, A. King, A. Ross-Gillespie, C. Walker, K. Skinner, M. Hill, K. Golabek, H. Johnson, P. Minting, A. Thornton, A. Turbe, G. Spong, M. van der Vyver, M. Scantlebury, M. Ridley, N. Raihani, L. Hollen, 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 support over the course of this study. We especially thank N. Jordan, T. Flower, L. L. Sharpe, A. Russell, S. Hodge, K. K. Fujisawa and K. Okanoya, for supporting this study and discussions. This study was supported by JSPS Research Fellowships, RIKEN Special Postdoctoral Researchers Program and a Grant-in-Aid for Scientific Research (No. 18870025).

References Altmann, J. 1974. Observational study of behavior: sampling methods. Behaviour, 49, 227e265. Arnold, K. & Aureli, F. 2006. Postconflict reconciliation. In: Primates in Perspective (Ed. by C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger & S. K. Bearder), pp. 592e608. New York: Oxford University Press. Aureli, F. 1992. Post-conflict behaviour among wild long-tailed macaques (Macaca fascicularis). Behavioral Ecology and Sociobiology, 31, 329e337. Aureli, F. & Schaffner, C. 2006. Causes, consequences and mechanisms of reconciliation: the role of cooperation. In: Cooperation in Primates and Humans: Mechanisms and Evolutions (Ed. by P. M. Kappeler & C. P. van Schaik), pp. 121e136. New York: Springer. Aureli, F. & de Waal, F. B. M. 2000. Natural Conflict Resolution. Berkeley, California: University of California Press. Aureli, F., Cords, M. & van Schaik, C. P. 2002. Conflict resolution following aggression in gregarious animals: a predictive framework. Animal Behaviour, 64, 325e343. van den Bos, R. 1998. Post-conflict stress-response in confined group-living cats (Felis silvestris catus). Applied Animal Behaviour Science, 59, 323e330. Clutton-Brock, T. H. 2002. Breeding together: kin selection and mutualism in cooperative vertebrates. Science, 296, 69e72. Clutton-Brock, T. H., Brotherton, P. N. M., Smith, R., McIlrath, G. M., Kansky, R., Gaynor, D., O’Riain, J. M. & Skinner, J. D. 1998. Infanticide and expulsion of females in a cooperative mammal. Proceedings of the Royal Society of London, Series B, 265, 2291e2295. Clutton-Brock, T. H., MacColl, A. D. C., Chadwick, P., Gaynor, D., Kansky, R. & Skinner, J. D. 1999a. Reproduction and survival of suricates (Suricata suricatta) in the southern Kalahari. African Journal of Ecology, 77, 69e80. Clutton-Brock, T. H., Gaynor, D., McIlrath, G. M., MacColl, A. D. C., Kansky, R., Chadwick, P., Manser, M., Brotherton, P. N. M. & Skinner, J. D. 1999b. Predation, group size and mortality in a cooperative mongoose, Suricata suricatta. Journal of Animal Ecology, 68, 672e683. Clutton-Brock, T. H., Brotherton, P. N. M., Russell, A. F., O’Riain, M. J., Gaynor, D., Kansky, R., Griffin, A., Manser, M., Sharpe, L., McIlrath, G. M., Small, T., Moss, A. & Monfort, S. 2001. Cooperation, conflict and concession in meerkat groups. Science, 291, 478e481.

1451

1452

ANIMAL BEHAVIOUR, 75, 4

Clutton-Brock, T. H., Hodge, S. J., Spong, G., Russell, A. F., Jordan, N. R., Bennett, N. C., Sharpe, L. L. & Manser, M. B. 2006. Intrasexual competition and sexual selection in cooperative mammals. Nature, 444, 1065e1068. Colmenares, F. 2006. Is postconflict affiliation in captive nonhuman primates an artifact of captivity? International Journal of Primatology, 27, 1311e1336. Colmenares, F., Hofer, H. & East, M. L. 2000. Greeting ceremonies in baboons and hyenas. In: Natural Conflict Resolution (Ed. by F. Aureli & F. B. M. de Waal), pp. 94e96. Berkeley, California: University of California Press. Cords, M. 1997. Friendship, alliances, reciprocity, and repair. In: Machiavellian Intelligence II (Ed. by A. Whiten & R. W. Byrne), pp. 24e 49. Cambridge: Cambridge University Press. Cords, M. & Aureli, F. 1993. Pattern of reconciliation among juvenile long-tailed macaques. In: Juvenile Primates: Life History, Development, and Behavior (Ed. by M. E. Pereira & L. A. Fairbanks), pp. 271e284. Oxford: Oxford University Press. Cords, M. & Aureli, F. 2000. Reconciliation and relationship quality. In: Natural Conflict Resolution (Ed. by F. Aureli & F. B. M. de Waal), pp. 177e198. Berkeley, California: University of California Press. Crawley, M. J. 2002. Statistical Computing: an Introduction to Data Analysis Using S-Plus. New York: J. Wiley. Doolan, S. P. & MacDonald, D. W. 1996. Dispersal and extra-territorial prospecting by slender-tailed meerkats (Suricata suricatta) in the south-western Kalahari. Journal of Zoology, 240, 59e73. Doolan, S. P. & MacDonald, D. W. 1997a. Band structure and failure of reproductive suppression in a cooperative breeding carnivore, the slender-tailed meerkats (Suricata suricatta) in the south-western Kalahari. Behaviour, 134, 827e848. Doolan, S. P. & MacDonald, D. W. 1997b. Breeding and juvenile survival among slender-tailed meerkats (Suricata suricatta) in the south-western Kalahari: ecological and social influences. Journal of Zoology, 242, 309e327. East, M. L., Hofer, H. & Wickler, W. 1993. The erect ‘‘penis’’ is a flag of submission in a female-dominated society: greetings in Serengeti spotted hyenas. Behavioral Ecology and Sociobiology, 33, 355e370. Flack, J. C. & de Waal, F. 2007. Context modulates signal meaning in primate communication. Proceedings of the National Academy of Sciences, U.S.A. 104, 1581e1586. Griffin, A. S., Pemberton, J. M., Brotherton, P. N. M., McIlrath, G. M., Gaynor, D., Kansky, R. & Clutton-Brock, T. H. 2004. A genetic analysis of breeding success in the cooperative meerkat (Suricata suricatta). Behavioral Ecology, 14, 472e480. Kappeler, P. M. 1993. Reconciliation and post-conflict behaviour in ringtailed lemurs, Lemur catta, and redfronted lemurs, Eulemur fulvus rufus. Animal Behaviour, 45, 901e915. Kutsukake, N. & Castles, D. L. 2001. Reconciliation and variation in post-conflict stress in Japanese macaques (Macaca fuscata fuscata): testing the integrated hypothesis. Animal Cognition, 4, 259e268. Kutsukake, N. & Castles, D. L. 2004. Reconciliation and postconflict third-party affiliation among wild chimpanzees at the Mahale Mountains, Tanzania. Primates, 45, 157e165. Kutsukake, N. & Clutton-Brock, T. H. 2006a. Aggression and submission reflect reproductive conflict between females in cooperatively breeding meerkats. Behavioral Ecology and Sociobiology, 59, 541e548. Kutsukake, N. & Clutton-Brock, T. H. 2006b. Social function of allogrooming in cooperatively breeding meerkats. Animal Behaviour, 72, 1059e1068. Kutsukake, N., & Clutton-Brock, T. H. In press. The number of subordinates moderates intra-sexual competition among males in cooperatively breeding meerkats. Proceedings of the Royal Society of London, Series B.

Kutsukake, N., Suetsugu, N. & Hasegawa, T. 2006. Pattern, distribution, and function of greeting behaviour among black-and-white colobus. International Journal of Primatology, 27, 1271e1291. Maestripieri, D. 1996. Primate cognition and the bared-teeth display: a reevaluation of the concept of formal dominance. Journal of Comparative Psychology, 110, 402e405. Matsumura, S. & Hayden, T. J. 2006. When should signals of submission be given?dA game theory model. Journal of Theoretical Biology, 240, 425e433. Preuschoft, S. & van Schaik, C. P. 2000. Dominance and communication: conflict management in various social settings. In: Natural Conflict Resolution (Ed. by F. Aureli & F. B. M. de Waal), pp. 77e105. Berkeley, California: University of California Press. Roeder, J. J., Fornasieri, I. & Gosset, D. 2002. Conflict and postconflict behaviour in two lemur species with different social organizations (Eulemur fulvus and Eulemur macaco): a study on captive groups. Aggressive Behavior, 28, 62e74. Rolland, N. & Roeder, J. J. 2000. Do ringtailed lemurs (Lemur catta) reconcile in the hour post-conflict?: a pilot study. Primates, 41, 223e227. Russell, A. F., Clutton-Brock, T. H., Brotherton, P. N. M., Sharpe, L. L., McIlrath, G. M., Dalerum, F. D., Cameron, E. Z. & Barnard, J. A. 2002. Factors affecting pup growth and survival in cooperatively breeding meerkats Suricata suricatta. Journal of Animal Ecology, 71, 700e709. Russell, A. F., Brotherton, P. N. M., McIlrath, G. M., Sharpe, L. L. & Clutton-Brock, T. H. 2003. Breeding success in cooperative meerkats: effects of helper number and maternal state. Behavioral Ecology, 14, 486e492. Samuels, A. & Flaherty, C. 2000. Peaceful conflict resolution in the sea? In: Natural Conflict Resolution (Ed. by F. Aureli & F. B. M. de Waal), pp. 229 Berkeley, California: University of California Press. Schaffner, C. M. & Caine, N. G. 2000. Peacefulness in cooperatively breeding primates. In: Natural Conflict Resolution (Ed. by F. Aureli & F. B. M. de Waal), pp. 155e169. Berkeley, California: University of California Press. Schaffner, C. M., Aureli, F. & Caine, N. G. 2005. Following the rules: why small groups of tamarins do not reconcile conflicts. Folia Primatologica, 76, 67e76. Schall, R. 1991. Estimation in generalized linear models with random effects. Biometrika, 78, 719e727. Schino, G. 1998. Reconciliation in domestic goats. Behaviour, 135, 343e356. Schino, G. 2000. Beyond the primates: expanding the reconciliation horizon. In: Natural Conflict Resolution (Ed. by F. Aureli & F. B. M. de Waal), pp. 225e242. Berkeley, California: University of California Press. Seed, A. M., Clayton, N. S. & Emery, N. J. 2007. Postconflict thirdparty affiliation in rooks, Corvus frugilegus. Current Biology, 17, 152e158. Sharpe, L. L., Clutton-Brock, T. H., Brotherton, P. N. M., Cameron, E. Z. & Cherry, M. I. 2002. Experimental provisioning increases play in free-ranging meerkats. Animal Behaviour, 64, 113e121. Silk, J. B., Alberts, S. C. & Altmann, J. 2003. Social bonds of female baboons enhance infant survival. Science, 302, 1231e1234. Smuts, B. B. & Smuts, R. W. 1993. Male aggression and sexual coercion of females in nonhuman primates and other mammals: evidence and theoretical implications. Advances in the Study of Behavior, 22, 1e63. Sommer, V., Denham, A. & Little, K. 2002. Postconflict behaviour of wild Indian langur monkeys: avoidance of opponents but rarely affinity. Animal Behaviour, 63, 637e648. Tamaki, N., Morisaka, T. & Taki, M. 2006. Does body contact contribute towards repairing relationships? The association between flipper-rubbing and aggressive behavior in captive bottlenose dolphins. Behavioural Processes, 73, 209e215.

KUTSUKAKE & CLUTTON-BROCK: CONFLICT MANAGEMENT IN MEERKATS

Veenema, H. C., Das, M. & Aureli, F. 1994. Methodological improvements for the study of reconciliation. Behavioural Processes, 31, 29e38. de Waal, F. B. M. & van Roosmalen, A. 1979. Reconciliation and consolation among chimpanzees. Behavioral Ecology and Sociobiology, 5, 55e66. de Waal, F. B. M. & Tyack, P. L. 2003. Animal Social Complexity: Intelligence, Culture, and Individualized Societies. Cambridge, Massachusetts: Harvard University Press. de Waal, F. B. M. & Yoshihara, D. 1983. Reconciliation and redirected affection in rhesus monkeys. Behaviour, 85, 224e241. Wahaj, S. A., Guse, K. R. & Holekamp, K. E. 2001. Reconciliation in spotted hyena (Crocuta crocuta). Ethology, 107, 1057e1074.

Watts, D. P. 1995. Post-conflict social events in wild mountain gorillas (Mammalia, Hominoidea). I. Social interactions between opponents. Ethology, 100, 139e157. Weaver, A. 2003. Conflict and reconciliation in captive bottlenose dolphins, Tursiops Truncatus. Marine Mammal Science, 19, 836e 846. Westlund, K., Ljungberg, T., Borefelt, U. & Abrahamsson, C. 2000. Post-conflict affiliation in common marmosets (Callithrix jacchus jacchus). American Journal of Primatology, 52, 31e46. Wittig, R. M. & Boesch, C. 2003. ‘‘Decision-making’’ in conflicts of wild chimpanzees (Pan troglodytes): an extension of the relational model. Behavioral Ecology and Sociobiology, 54, 491e504.

1453