In Current Primatology, Vol. 2: Social Development, Learning and Behaviour, Roeder, J.J., Thierry, B., Anderson, J.R. & Herrenschmidt, N. (eds.), Université Louis Pasteur, Strasbourg, pp. 103-117, 1994

Tonkean behaviour from the perspective of the evolution of

B. THIERRY, J. R. ANDERSON, C. DEMARIA, C. DESPORTES & O. PETIT

Our vision of macaque societies has intensification of research in Barbary long been shaped by the study of rhesus and macaques (M. sylvanus) showed that not Japanese macaques (Macaca mulatta & M. only may females mate with any male at the fuscata). It was a historical accident that time of ovulation (Taub, 1980) but that they knowledge about these species' social do not follow the rules of rank inheritance behaviour developed earlier and more described in rhesus and Japanese macaques extensively than for any other monkey taxa (Paul & Kuester, 1987). The study of (Altmann, 1962, 1965; Rawlins & Kessler, Tonkean macaques (M. tonkeana) produced 1986; Fedigan & Asquith, 1991) and that a set of data which departs from what was both species exhibit very similar social considered as the norm for the genus relations, including weak interindividual Macaca. These data are reviewed in the tolerance, intense aggression and present paper, allowing a broader submission, strong kin preferences, strict perspective on macaque social evolution. rules of rank inheritance among females, and little affiliation between mature males. Origin of Tonkean macaques Such patterns were once believed to be typical of the whole genus Macaca. The and conditions of study finding that tolerance is more developed in Tonkean macaques are large black bonnet macaques (M. radiata)(Rosenblum macaques found in the central region of the & Kaufman, 1967; Sugiyama, 1971) island of Sulawesi, Indonesia. The slightly modified this stance. Subsequent biogeographic situation of the island is studies in other species enriched our peculiar: deep ocean troughs separate it both knowledge of some of the variations from the Indo-Malayan part of the Sunda occurring within the genus, about mating shelf (Wallace's line) and from the patterns and male care of infants for Australo-Papuan part of the Sahul shelf instance; however, they did not question the (Weber's line). A relatively long period of belief that the social life of macaques is isolation during geological time has given ruled by nepotism and dominance, in line rise to a highly endemic flora and fauna, with the main tenets of behavioral ecology including seven highly derived macaque and sociobiology (Kurland, 1977; Dittus, taxa (Groves, 1976, 1980). 1980; Silk, 1984). In the eighties, direct Individuals belonging to the species comparisons revealed marked interspecific Macaca tonkeana were imported into contrasts in patterns of social interactions France and established as a group in 1972 (Thierry, 1985a & b; de Waal & Luttrell, (Herrenschmidt, 1977). The population 1989) as well as in individual grew from a stock of eight reproducers. In responsiveness (Clarke et al., 1988). The 1 1978, it was divided in two groups. The rs=+.98, n=14, p<.001). Additional main study group was established at the parameters were measured with respect to Center of the University of conflicts occurring spontaneously in the Strasbourg in a 1-acre wooded enclosure group. For initiating aggression, the containing an indoor shelter and surrounded resulting rank order was significantly by a fence electrified at the top. From 7 correlated with the supplantation order individuals at the start of the study in 1982, drawn from the competition test (rs=+.97, the group has grown to 21 members in p<.001). Conversely, protest vocalizations 1992. A second group was maintained in a were negatively correlated with rank order 120 m2 indoor-outdoor cage at the (rs=-.91, p<.001). Therefore, dominance Orangerie Zoo of Strasbourg, where relationships are recognizable in Tonkean observations have occasionnally been macaques, and they may be measured more conducted; group-size has fluctuated readily by using such parameters as who between 9 and 14 individuals. (The periodic initiates aggression or which individual removal of maturing individuals from both screeches, than by the outcome of agonistic groups has led to the formation of three interactions. further breeding groups distributed in On the other hand, when looking at a French zoological parks.) parameter such as first avoidance in an agonistic interaction, the resulting order did Characteristic behavioural not significantly correlate with the traits of Tonkean macaques dominance rank order (rs=-.50, ns), first Relaxed dominance and avoidance may be displayed by the aggressor or the aggressee in a conflict. The social tolerance frequent occurrence of retaliation by A striking feature of Tonkean social subordinates and avoidance by higher- relations is the symmetry observed during ranking individuals indicate a low gradient conflicts. In more than half of agonistic of dominance in the group. For instance, interactions, the threatened individual protests against the highest-ranking male of retaliates, so that the interaction becomes the group are frequent in Tonkeans: it is not bidirectional. This is true even between rare to see this individual being chased into unrelated individuals, and for any a tree by one or two screeching females. It combination of individuals, regardless of should be added that dominance age-and-sex class (Thierry, 1985a). Such relationships are nevertheless quite stable; bidirectionality of conflicts matters with the previously mentioned parameters, regard to the evaluation of dominance. measured from year to year, have shown Dominance relationships are usually minimal changes within each dyad of adult determined according to the outcomes of individuals. agonistic interactions, loser and winner An analysis of the distribution of social being distinguished by which individual flees or submits. Such a criterion cannot be grooming among adult females indicated a weak influence of individual status. used in Tonkeans; when not counter- Ranking females according to the ratio of attacking the aggressee often lipsmacks (Thierry, 1985a). Spontaneous displac- grooming received to grooming performed showed no correlation with dominance ements and supplantations are quite rare in Tonkeans, and neither can be used to rank; supplantations during grooming were rare and the level of competition for higher- construct a rank order. To settle the ranking partners quite low (Thierry et al., question, 9 competition tests of 3 hrs each were conducted around a source of fruit 1990). This low gradient of dominance is linked to an overall elevated social juice with the aim of increasing the rate of tolerance, as exemplified by cofeeding supplantation and unidirectional aggression (Desportes et al., 1989). Rates of around fruits (Petit et al., 1992). supplantation and unidirectional aggression In our conditions, the dominant adult led to strongly correlated rank orders male in each group forms close (Spearman-rank correlation coefficient, consortships with females at the time of 2 genital swelling. He maintains close them with impunity, and the latter tolerate proximity with the female for days and their interference in matings (Thierry, performs serial matings. He appears to be 1986a). Interestingly, the meaning of the only individual to mount the female. agonistic vocalizations is also difficult to Paternity exclusion analyses has confirmed identify (Masataka & Thierry, 1993), that during a 4-yr period, while two males Tonkean individuals often switch from of at least 6 yrs-old were present in the agonism to affiliation and, on rare main study group, the highest-ranking one occasions, mild punishment may even had fathered seven offspring out of eight merge with genuine reconciliation. For (Scheffrahn et al., 1990, & pers. comm.). It example, a female may intervene in a is noteworthy that the second male sired conflict where its offspring is the aggressor one offspring even though the female had by hugging and nibbling the youngster: been observed in continuous consort with while this can stop aggression, it is the dominant male around conception time, impossible for the observer to decide and that the second male was never seen to whether the intervention is aggressive or mount her during this period. However, affinitive, it may best be labelled as given the small number of breeding males "affinitive punishment". and females in the group so far, these The high frequency of peaceful results should be considered preliminary. interventions in conflicts is partly responsible for the complicated nature of Conciliation and weak formalization Tonkean agonistic interactions. In peaceful of relations interventions, a third individual approaches One spectacular pattern reflected in one of the opponents, most often the Tonkean social relations is the frequent aggressor, and appeases it using lipsmack, silent bared-teeth display. In contrast to play, mount or clasp (Thierry, 1984). We most other known macaque species, this have found that such interventions stop the facial expression does not show conflict more often that aggressive directionality among dyads according to interventions, and that they are frequently dominance relationships (Thierry et al., followed by social grooming between the 1989). It does not express submission, but intervening individual and its target (Petit & signals peaceful intentions on the part of the Thierry, ms). These peaceful interventions emitter, and serves to initiate affinitive may represent an outcome of the highly interactions. The jaw may be closed or developed conciliatory tendencies of open, in which case it becomes impossible Tonkean macaques. Non-aggressive to distinguish this display from the relaxed contacts are also frequent among previous open-mouth face usually seen in the context opponents (Thierry, 1986b). Comparing of play in monkeys. In fact, no ritualized post-conflict and matched-control periods, signal of submission exists in Tonkeans. Demaria and Thierry (1992) have shown Outside the context of aggression, the main that the conciliatory tendency is 51% in facial expression displayed towards a dyads of unrelated adult individuals (index higher-ranking individual is lipsmack, a of Veenema et al., 1994), which is higher signal which may also be addressed to than in any other group of macaques in subordinates. which reconciliation has been studied (de Waal & Luttrell, 1989; Veenema et al., Biting is rare and affinitive displays 1994). such as lipsmacks, grunts, and clasps of various forms occur at a high frequency (Thierry, 1984, 1985a & b; Demaria & Open relations and group cohesion Thierry, 1992). Lack of formality in social Another characteristic feature of relations is apparent in the lack of inhibition Tonkean macaques is that every individual by individuals about engaging in contact, can freely interact with any other member even with the highest-ranking individuals. of the group, with little obvious regard for For example, juveniles do not avoid adult kinship bonds. Post-conflict conciliatory males when passing by, they may contact tendencies are not significantly greater

3 among maternal kin than non-kin (Demaria and 1988, they found several different ways & Thierry, 1992; index of Veenema et al., to escape from their enclosure. Tonkean in press). Mothers are quite permissive with subgroups entered the enclosures of rhesus their infants, who may interact with any and longtail macaques (M. fascicularis), other group members from an early age, and attacked them on five occasions (4 this allows other females, kin or non-kin, to rhesus adults were wounded and several perform high levels of alloparental care infants and juveniles were killed: 8 rhesus (Thierry, 1985; Thierry & Herrenschmidt, and 4 longtail macaques). It is common to 1985). see Tonkean macaques threatening With respect to the distribution of neighbouring groups at a distance, whereas grooming bouts among adult females, no the latter rarely display aggressive significant differences appear in the amount behaviour towards the Tonkeans. of social grooming by females toward kin and non-kin (Thierry et al., 1990). As for Exploration and manipulative abilities grooming interactions, contacts during rest Tonkean macaques appear especially periods are hardly influenced by kinship: manipulative. The use of objects in play is any individual may huddle with any other. frequent, including wrestling for an object, As a general rule, Tonkean social structure branch-dragging and non-aimed throwing. cannot be easily interpreted in terms of One adult male spontaneously developed a distances separating individuals, or by the form of tool-use, namely repeatedly composition of subgroups. This does not inserting a plant-stem to reach mucus inside mean that nepotism does not play any role the nose (Bayart, 1981). This again in the social organization of Tonkean occurred in an adult female several years macaques. Group structure is truly later, and included tool manufacture: the matrilineal, as in other species of macaques. female woukd pick up a stem, and In coalitions for instance, help is mostly sometimes break or strip it before use; the given to related partners, which results in stem was straightened or shortened several dominance relations between matrilines. times during tool-use, using hands and teeth The point is that kin-preferential behaviour (Thierry, 1991). in Tonkeans is much less marked than in species such as rhesus or Japanese A series of tests was carried out to macaques. assess interest towards novel objects in rhesus, longtail and Tonkean groups. The The Tonkean group is particularly comparison produced significant cohesive and coordinated when moving. differences in particular, the duration of Contact calls are frequent and their acoustic object manipulation was ten to fifteen times features vary according to distances longer in Tonkean than rhesus macaques, in between emitter and receiver (Masataka & different age-and-sex classes. Other Thierry, 1993). It seems that particular findings suggest that Tonkeans are quick to vocalizations aim to inform other learn. In a classic tool-use task involving individuals about ongoing social events: the use of a rod to reach food outside the affiliation calls attract attention to intense cage - in this case honey - two subadult affinitive interactions, twits and cackles are males spontaneously learned to use the rod uttered by individuals witnessing the after about 6 and 8 hours respectively, occasional polyadic conflict, loud calls are which compares well with learning times of emitted by dominant males, mainly in 8 to 14 hours reported for pigtail macaques situations of social tension or towards (M. nemestrina) and (Papio papio) separated individuals. in a similar situation (Anderson, 1985). Tonkean macaques appear highly Finally, although Tonkean macaques do not aggressive toward other macaque groups appear to show self-recognition when tested living in neighbouring enclosures which with a mirror (Bayart & Anderson, 1985), may be related to their social cohesion. some individuals can learn to use the Tonkeans are especially manipulative and information in a reflection to find hidden destructive (cf. below) and, between 1985 food. This visuospatial adaptation occurred

4 more quickly in a Tonkean juvenile than in severe physical aggression are low, and a young longtail macaque who also learned there are high frequencies of appeasement how to use the mirror (Anderson, 1986). patterns such as clasp and lipsmack, marked The combination of manipulative skills social tolerance, prolonged consortships, and social tolerance of Tonkean macaques interference in mating by immatures, and a may lead to some unexpected outcomes. In weak influence of dominance relationships the tool-use study mentioned above, the on social grooming. Although Matsumura second individual to learn to use the rod to (1991) found a correlation between obtain food did so after several instances of dominance rank and ratio of grooming joint manipulation of the tool with the received to grooming performed among original discoverer (Anderson, 1985). In Moor adult females, variation in individual another study, food incentives were placed grooming rates was limited. In one group of under stones which the monkeys had to crested macaques, the distribution of move. It was found that two individuals grooming was biased in favour of acting together were able to move heavy matrilineal relatives (Baker & Estep, 1985); stones more efficiently than subjects acting however, a high proportion of immatures alone (Petit et al., 1992). While there was was included in the analysis and no values no deliberate coordination between partners, were given, limiting the comparability with the simultaneous action of subjects could Tonkean data. It should be noted that there not have occurred without mutual tolerance. was no influence of kinship on the choice of play partners. A recent study, carried out on On the whole, Tonkean macaques the group of crested macaques held at the appear similar to liontail macaques with Jersey Wildlife Preservation Trust (Petit, regard to exploration, sensorimotor abilities, unpubl. data), has shown that peaceful use and manufacture of tools (cf. Wester- interventions in conflicts is frequent, and gaard & Lindquist, 1987; Westergaard, that the conciliatory tendency is 48.4% for 1988; Clarke & Lindburg, 1993). unrelated adults (figure based on 31 post- conflict and matched 10-mn control periods; Knowledge about index from Veneema et al., in press), which other Sulawesi species is similar to that found in Tonkean macaques. The seven allopatric taxa on the island Given the marked differences in the of Sulawesi derive from a single ancestral population; they share many morphological, environment, composition and history of the physiological and molecular similarities groups studied, the behavioural similarities found between Tonkean, Moor and crested (Fooden, 1969; Melnick & Kidd, 1985; Takenaka, 1985; Fooden & Lanyon, 1989). macaques are striking. Furthermore, challenges of higher-ranking individuals by Intergradation occurs in border areas subordinates appear common in Moor between neighbouring taxa, providing evidence of some gene flow between them macaques (Watanabe & Brotoisworo, 1982; Petit & Thierry, 1992), and crested (Groves, 1980; Camperio Ciani et al., 1989; macaques appear to be adept object Watanabe et al., 1991). It may be asked whether the various behavioural manipulators (Bernstein, 1971; Bernstein & Baker, 1988). Although we have few data characteristics described for Tonkean macaques are unique to this species, or on the other four Sulawesi taxa, it seems highly probable that they share the same whether they are typical of other Sulawesi features. In all taxa, a loud call is emitted by macaques too. We have information on the social behaviour of wild Moor macaques adult males (Dixson, 1977; MacKinnon et al., 1979; Watanabe & Brotoisworo, 1982, (M. maurus)(Watanabe & Brotoisworo, Masataka & Thierry, in press), and the 1982; Matsumura, 1991; Matsumura & Watanabe, this volume) and captive crested silent bared-teeth display is frequently observed (cf. Groves, 1980). In the best macaques (M. nigra)(Bernstein, 1971; Dixson, 1977; Bernstein et al., 1985; Baker known species, the latter display carries an affinitive meaning, it does not convey any & Estep, 1985). In both species, rates of information about the dominance status of

5 partners (Dixson, 1977; Thierry et al., 1989; Current ecological models do not Petit & Thierry, 1992). If lessons drawn account for the social organization observed from the study of Tonkean macaques apply in Tonkean, Moor and crested macaques. to other species, this display would indicate According to Caldecott (1986a), high- a relatively egalitarian social organization quality habitats should be associated with where neither dominance asymmetries nor the evolution of high intermale tolerance strong nepotism prevent individuals from coupled with female selectivity of mates: interacting freely with all other individuals the latter pattern involves brief consortships (Thierry, 1990). and single-mount copulations, which does Finally, it has been noted that group not fit the data. Following van Schaik formation in captivity leads to limited (1989), a frugivorous diet associated with aggression in crested macaques (Bernstein low predation risk should lead to increased & Baker, 1988); this was also found in the between-group competition, but this does establishment of a Tonkean all-male group not correspond to what has been observed in (Thierry, pers. obs.). Notwithstanding Sulawesi macaques. Tonkean attacks against strange species, While it is generally taken for granted these data concur with field reports of that all patterns of social organization have remarkable intergroup tolerance and been ecologically selected for (cf. Richard, proximity in crested and Moor macaques 1981), the additional consideration of (MacKinnon et al., 1979; Watanabe & phylogenetic and epigenetic constraints is Brotoisworo, 1982; Sugardjito et al., 1989; necessary for a fuller understanding of their Matsumura, 1991). Group splitting in evolution. The different characters of subgroups also occurs. From such features, macaque social organizations may be we should expect complex grouping connected by structural relations: patterns superimposed on the multimale- conciliatory patterns, socialization multifemale organization generally processes, dominance asymmetries and kin- observed in the wild. bias in relationships appear to covary (Thierry, 1986b, 1990). Macaque species Discussion can be ordered along a spectrum going from strongly nepotistic and dominance-oriented It is fascinating that species so organizations to more egalitarian, mildly differentiated morphologically should be so nepotistic ones. Rhesus and Japanese similar in their behaviour. If this is macaques are located at one extreme while confirmed, we would face the paradox that known Sulawesi species are representative morphological variation and behavioural of the other extreme. The former species use similarity may not be explained together by a submissive silent bared-teeth display either similar or dissimilar ecological formally expressing submission (de Waal & conditions. The seasonality of the climate is Luttrell, 1985), the latter exhibit an less marked in central Sulawesi than in the affiliative bared-teeth display no longer southern parts of the island (Groves, 1980; meaningful in terms of dominance. In Whitten et al., 1987). The crested macaques between, species possess both the may be more arboreal than heavier taxa submissive bared-teeth and the teeth- (MacKinnon et al., 1979). However, short chattering displays - the latter display surveys suggest that the various Sulawesi conveying a message halfway between macaques exist in broadly similar ecological submission and affiliation - with a range of conditions. They are mainly frugivorous, variation among teeth-chattering species (cf. they have no non-human primate Rosenblum & Kaufman, 1967; de Waal & competitors or strong predators, they use all Luttrell, 1989). It is interesting to view such strata in their environment, and populations data from a cladistic perspective. Japanese, may be found at various altitudes within rhesus and longtail macaques belong to the their range, in lowland and lower montane same phyletic lineage, while pigtail, liontail forests (MacKinnon et al., 1979; Bismark, and Sulawesi macaques belong to another 1982a & b; Whitten et al., 1987; clade, close to Barbary macaques (Fooden, Matsumura, 1991; Kohlhaas et al., 1992).

6 1976; Delson, 1980; Takenaka, 1985; We are still waiting for an integration Fooden & Lanyon, 1989). It may not be of how ecological factors and evolutionary mere coincidence that the first three species pathways constrain primate social present similar social organizations, organizations through epigenetic processes. characterized by strong dominance and Further progress in the , nepotism. Conversely, liontails show an evolution, behaviour and ecology of the 15- affiliative form of the bared-teeth display 20 existing macaque species, and the (Johnson, 1985): it would be interesting to Sulawesi macaques in particular, will be know whether this feature is correlated with essential for such a synthesis. relaxed dominance and mild nepotism. Barbary macaques also show affiliative teeth-chattering, and their bared-teeth References display sometimes lacks unidirectionality Altmann, S.A. (1962). A field study of the from lower to higher-ranking individuals sociobiology of rhesus monkeys Macaca mulatta. (Preuschoft, 1992). On the other hand, Ann. N. Y. Acad Sci. 102: 338-435. pigtails only possess the submissive bared- Altmann, S.A., ed. (1965). Japanese monkeys. A teeth display, associated with a strongly collection of translations. Atlanta, published by dominance-oriented and kin-biased social the editor. organization (Rosenblum & Kaufman, Anderson, J.R. (1985). Development of tool-use to 1967; Caldecott, 1986b). Based on such obtain food in a captive group of Macaca parameters, pigtails do not appear to tonkeana. J. Hum. Evol. 14: 637-645. resemble the other members of their Anderson, J.R. (1986). Mirror-mediated finding of lineage, which would support the ecological hidden food by monkeys (Macaca tonkeana and M. fascicularis). J. Comp. Psychol. 100: argument. 237-242. The data available at present do not Baker, S.C. & Estep, D.Q. (1985). Kinship and allow to speculate further. Knowledge about affiliative behavior patterns in a captive group social relations remains limited for a of Celebes black apes (Macaca nigra). J. number of species. We have no knowledge Comp. Psychol. 99: 356-360. about the speed of evolutionary changes Bayart, F. (1982). Un cas d'utilisation d'outil chez un affecting behavioural characters. It may be macaque (Macaca tonkeana) élevé en semi- liberté. Mammalia 46: 541-544. asked whether behavioural characters Bayart, F. & Anderson, J.R. (1985). Mirror-image represent shared derived characters or reactions in a tool-using, adult male Macaca species-specific variants, liable to appear or tonkeana. Behav. Proc. 10: 219-227. disappear according to environmental Bernstein, I.S. (1971). Activity profiles of primate pressures. It is known that patterns of social groups. In Schrier, A.M. & Stollnitz, F. (eds.), organization are related to individual Behavior of non-human , vol. 3. constitution, either directly (e.g., Dixson, Academic Press, New York, pp. 69-106. 1987) or indirectly through communication Bernstein, I.S. & Baker, S.C. (1988). Activity signals and behavioural propensities (Clarke patterns in a captive group of Celebes black et al., 1988). The protruded lips display of apes (Macaca nigra). Folia Primatol. 51: 61- pigtail, liontail and Sulawesi macaques for 75. instance (Dixson, 1977; Thierry, 1984; Bernstein, I.S., Williams, L. & Ramsay, M. (1983). The expression of aggression in Old World Johnson, 1985; Caldecott, 1986b), is a monkeys. Int. J. Primatol. 4: 113-125. shared derived character in this clade. On Bismark, M. (1982a). Ekologi dan tingkahlaku the other hand, many vocalizations correlate Macaca nigrescens di Suaka Margasatwa weakly with phyletic data within the genus; Dumoga, Sulawesi Utara. Balai Penilitian even the acoustic features of the loud calls Hutan, Rep. 392. emitted by adult males in these species are Bismark, M. (1982b). Habitat dan populasi Macaca very different among taxa (Watanabe & ochreata di Suaka Margasatwa Tanjung Brotoisworo, 1982; Hohmann & Herzog, Peropa, Sulawesi Tenggara. Balai Penilitian 1985; Hohmann, 1989; Masataka & Hutan, Rep. 408. Thierry, 1993). Caldecott, J.O. (1986a). Mating patterns, societies and the ecogeography of macaques. Anim. Behav. 34: 208-220.

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