Male Social Behavior and Dominance Hierarchy in the ... - Springer Link

International Journal of Primatology, Vol. 18, No. 2, 1997h

Male Social Behavior and Dominance Hierarchy in the Sulawesi Crested Black Macaque (Macaca nigra) Caitlin Reed,1,2 Timothy G. O'Brien,3,4 and Margaret F. Kinnaird3

In a 6-week study of the social behavior of wild Sulawesi crested black macaques (Macaca nigra), we found a linear and transitive dominance hierarchy among the six adult males in one social group. Dominance rank, as determined by the direction of supplantations, correlated strongly with percentage of time near more than four neighbors, frequency of grooming received from adult females, and percentage of time with an adult female as nearest neighbor. These results suggest that high-ranking males are socially attractive. Adult females sexually solicited high-ranking males more often than low-ranking males, but frequency of copulation was not correlated with dominance rank. Frequency and intensity of aggression between males are strongly correlated with rank distance, but aggression toward females was greatest for mid-ranking males. Males of all rank displayed significantly more aggression toward sexually receptive females than toward females in other estrous states. These data indicate that male Sulawesi crested black macaques display a social organization similar to that reported for multimale groups in other macaque species rather than the egalitarian social organization described for female Sulawesi macaques. KEY WORDS: Sulawesi crested black macaque; male dominance hierarchy; social organization; Macaca nigra.

'Department of Biology, University of North Carolina, Chapel Hill, North Carolina 27514. 2Present address: Department of Zoology, Cambridge University, Downing Street, Cambridge CB2 3EJ, England. 3 Wildlife Conservation Society, Indonesia Program, P.O. Box 311, Jl. Ciremei No. 8, Bogor 16003, Indonesia. 4To whom correspondence should be addressed, e-mail: [email protected].

247 0164-0291/97/0400-0247$12.50/0 6 1997 Plenum Publishing Corporation

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INTRODUCTION

Dominance is a stable asymmetry in agonistic behavior of two or more individuals (Dewsbury, 1982; Drews, 1993). It is usually measured by observing the direction of agonistic signals, supplantations and avoidance in dyadic interactions. Consistent and predictable asymmetries in the interactions of two individuals indicate a stable dominance relationship between them. Transitive dominance relationships in a group of individuals result in a linear dominance hierarchy. Dominance hierarchies have been identified in many primate species, particularly cercopithecines (Melnick and Pearl, 1987). High dominance rank confers benefits to males and females, particularly when access to resources is contested. Because females can be a contested resource among primates (Altmann, 1962; Wrangham, 1980), dominance rank is expected to correlate with female-male social interactions: grooming, proximity, and copulation. Based on studies of reconciliation behavior and female dominance hierarchies in captivity, Thierry (1990) and co-workers (Thierry et al., 1994) argued that female Sulawesi macaques have relaxed dominance hierarchies, with more egalitarian social relationships, than those of other macaque species, such as Japanese macaques (Macaca fuscata) and rhesus macaques (M. mulatta) (Das and Hooff, 1993). However, they did not explore the role of dominance hierarchies in male social organization. The egalitarian model of dominance predicts that male dominance hierarchy would not correlate with social interactions. Of 19 macaque species, 7 are endemic to the island of Sulawesi, Indonesia (Fooden, 1969; Albrecht, 1978). Although there are several studies of time budget (Bernstein and Baker, 1988) and sexual behavior (Dixon, 1977; Bernstein et al., 1982) of crested black macaques in captivity, social behavior of free-ranging or wild groups had not been reported for any of the seven taxa of Sulawesi macaques. The crested black macaques (Macaco nigra) are primarily frugivorous, semiterrestrial primates that live in large, female-bonded social groups (Kinnaird and O'Brien, 1995; O'Brien and Kinnaird, 1996). They are restricted to the northern peninsula of Sulawesi and are highly endangered due to loss of habitat and hunting (Sugardjito et al., 1989; O'Brien and Kinnaird, 1996). We examined the effect of dominance hierarchies on social interactions of adult male Sulawesi crested black macaques. Specifically, we evaluated the relationship between dominance rank and grooming, aggression, spatial association, and reproductive behavior.

Social Behavior of Male Black Macaques

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METHOD

We studied crested black macaques in the Tangkoko-DuaSudara Nature Reserve (TDS) in North Sulawesi, Indonesia (125°14r E, 1°34'N). The 8867-ha reserve ranges from sea level to 1300 m and is classified as lowland tropical rain forest, although habitats range from beach forest to elfin cloud forest. We established a 461 ha study area in primary and secondary forest, as well as regenerating 30-year old gardens. We divided the study area into 1-ha blocks by a trail system spaced at 100-m intervals. Crested black macaques occur at relatively high densities (380 animals in nine groups) in the study area (Kinnaird and O'Brien, 1995). We studied adult males (n = 6) in one large social group. A seventh male was associated with the group at the beginning of the study, but he disappeared before the end of the study and is not included in the analysis. The group consisted of 97 individuals, including 30 adult females, 5 subadult males, 38 juveniles, and 18 infants. The adult males were individually recognizable by size, scars, gait, facial structure, ischial callosities and broken fingers. The group was habituated to human observers for 2 years before our study and all individuals were approachable to within 2 m. Observation conditions were excellent because the forest understory is relatively open below 3 m and the macaques spent 78% of the time on the ground. Between 5 June and 14 July 1994, we observed the study group 4-5 days/week. We sampled subjects from 0600 until the completion of 40-min focal samples on each adult male. If an animal was absent during a follow, we sampled him twice on the following day to achieve four samples per male per week. We randomized the order of sampling on the first day of the week and reversed the order on alternate days. During each focal sample, we noted all instances of social behavior (Table I), recorded duration to the nearest minute, and identified interacting animals by age, sex and identity, if known. At 5-min intervals during each focal sample, we noted the focal subject's behavior, nearest neighbor, and number of neighbors within 5 m. We categorized aggressive interactions by intensity as supplantation, threat, and chase/contact. We classified adult females as sexually receptive or not based on the presence of perineal swellings. Within the receptive category, swellings were inflating, swollen, or deflating.

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Table I. Social Behaviors of Adult Male Sulawesi Crested Black Macaques: Presentation Is a Female Behavior Directed Toward an Adult Male Behavior Contact Chase Copulate Follow Grimace Groom Lipsmack Loud call Mount Penis grab Play Presentation Supplant Threat Yawn

Description Hits, grapples with, or bites target animal Charges at target animal and pursues as target animal flees Mounts female with intromission of penis, thrusts repeatedly, may or may not ejaculate Walks behind target animal as it moves Open lips to expose teeth and gums, teeth remain clenched Manipulate target animal's fur with hands and teeth to remove ectoparasites and dirt Rapidly open and close mouth to make an popping noise A loud 2- to 3-sec staccato vocalization Stands erect behind animal, both hands clasping hips of target animal; directed at both males and females and does not involve intromission Holding the penis of target animal, often mutual and usually accompanied by lipsmacking Affiliative chase and contact accompanied by wide, open-mouthed expression Sit or stand as female approaches and turns her bottom toward male; usually female stands in front of male for a short time Causing target animal to move from original position by approaching or starting Flatten ears against head, stare at target animal, perhaps accompanied by a bark-like vocalization Opens mouth slightly, tilts head back, and opens mouth widely to expose canines and gums

RESULTS Interactions Among Males During 6 weeks we conducted 1307 instantaneous samples during 128 focal samples on six males. We determined the dominance hierarchy among six adult males by the direction of supplantations (n = 79) within each dyad (Table II). The hierarchy was linear, with no triangle (nontransitive relationship) or reversal. Appleby's test of linearity (1983) showed that the linearity of this hierarchy is significant (n = 6; no reversals; P = 0.022). Relationships among males were characteristically by aggressive and lacked affiliative interaction. We saw grooming between males only twice, and both grooming sessions were < 1 min in duration. The distribution of male nearest neighbors is not significantly different from a random distribution of associations among males (X2 = 8.70, df = 5, n = 78, P > 0.05). Penis grabbing behavior did not correlate with rank (Spearman rank correlation, n = 24, P > 0.05) and was often reciprocated or mutual (8 of 24 instances).


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Table II. Adult Male Dominance Hierarchy Determined by Direction of Supplantations (n = 79) Loser

Winner BB BP JP PK B M

BB

BP

JP

PK

B

M

X

11 X

3 7 X

6 7 3 X

2 0 8 9 X

2 5 6 7 1 X

Aggressive interactions between males involved closely ranked opponents significantly more often than males with large rank distances as defined by de Waal [(1991); *RD = t = 8.8, ^0 = 2 = 7.2, *RD>2 = 0.833; F = 13.01, df = 2,12, P < 0.001]). Intensity of aggression (threats versus chase/contact) also is significantly associated with rank distance; closely ranked dyads had higher levels of chase and contact than expected and pairs with rank distances >2 (A-RD = ! = 4.8, *RD = 2 = 3.8, *RD>2 = 0.17; F = 12.03, df = 2,12, P < 0.001). Interactions Between Males and Other Group Members Analysis of the number of neighbor < 5 m of adult males revealed strong correlations with dominance rank. As male rank decreased, the percentage of time with no neighbors increased (rs = 0.943, n = 6, P = 0.008; Fig. 1). High-ranking males spent more time not only with neighbors, but also with more than four neighbors than low-ranking males did (rs = -0.943, n = 6, P = 0.002; Fig. 1). As rank increased, males spent less time with subadult males as nearest neighbors (rs = 0.771, n = 6, P = 0.033). There is significant heterogeneity in the pattern of male association with adult females (& = 97.94, n = 6, P < 0.001; Fig. 2). The highest ranking and lowest ranking males contributed most to the statistic, interacting more and less than expected by chance, respectively. Percentage of time with sexually receptive females as nearest neighbors also correlated with male dominance rank (rs = -0.886, n = 6, P = 0.0028; Fig. 2). Finally, adult females groomed high ranking males significantly more than low ranking males (rs = -0.782, n = 6, P = 0.0378). Males received grooming from females four times as often as they groomed females (110:25). When males reciprocated grooming, however, grooming sessions lasted twice as

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Fig. 1. Proportion of time spent with no neighbor within 5 m (open circle), and with more than 4 neighbors (closed circle) within 5 m during scan samples. Lines indicate linear trends.

long (mean = 7.1 min) as did sessions in which males did not reciprocate (mean = 3.5 min). Although the duration of grooming was not significantly correlated with male rank, the two lowest ranking males received the shortest average grooming sessions. The frequency of male aggression (supplantations, threats, chases/contacts) toward all adult females varies significantly with male rank (two-way ANOVA: F = 8.91, df = 5,10, P < 0.002). The relationship is not linear: the lowest; and highest-ranked males were least frequently involved in aggression, and the third-ranked male was the most aggressive toward females. Intensity of aggression toward females varied; males threatened females significantly more often than they supplanted females, and chases or contact occurred at an intermediate frequency (two-way ANOVA: F = 24.23, df = 2,10, P < 0.001). Females were supplanted more often by males that also threatened or chased them, but overall there was a low rate of supplantation compared to other aggressive behaviors. Estrous states of females had significant effects on the frequency of grooming and aggression by adult males. Adult males had more aggressive interactions with swollen adult females than with detumescent females; inflating females received intermediate levels of aggressions (one-way ANOVA: F = 3.94, df = 2,15, P = 0.042). Similarly, adult males had more grooming sessions with swollen females than with detumescent females; in-


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Fig. 2. Proportion of time spent with (a) adult females as nearest neighbors (closed circle) and receptive females (open females), and (b) sub-adult males as nearest neighbors. Lines indicate trends.

flating females were intermediate (one-way ANOVA: F = 4.1, df = 2,15, P = 0.038). Frequency of female presentations was strongly correlated with male dominance rank (rs = -0.865, n = 6, P = 0.012 Fig. 3); frequency of copulation, however, is not significantly correlated with rank (rs = -0.760, n = 6, P = 0.076; Fig. 3). Female estrous state significantly affected the frequency of male copulation: males copulated with swollen females at twice the rate that they copulated with females in other estrous states (F - 4.50, df = 2,15, P = 0.03).


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Fig. 3. Frequency of presentation (closed circle) by females and copulation with receptive females (open circle). Lines indicate trends.

DISCUSSION Interactions Among Males Social relationships among adult male macaques usually are described as antagonistic (Lindburg, 1971; Grewal, 1980; Takahata, 1982; Caldecott, 1986). However, Hill, (1994) suggests that affiliative relationships among male macaques are more common than is generally recognized, particularly when groups are small and have sex ratios close to parity. For example, adult male bonnet macaques (M. radiata), frequently groom, greet, and sit with each other (Silk, 1994). Hill (1994) proposed that males in small groups with more equal sex ratios have less competition for mates and a shortage of potential female grooming partners. These two factors increase the probability of affiliative relationships among males and could account for grooming, clasping, and other friendly behaviors seen among adult macaques in other studies (Sugiyama, 1971; Furuichi, 1983; Thierry, 1984; Deng and Zhao, 1987). In our study, grooming between males occurred only twice and the distribution of males as nearest neighbors with other males is not different from that expected by chance alone, a more typical pattern in male macaques (Melnick and Pearl, 1987), indicating a lack of affiliative relationships among crested black macaque males. The group was


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large and had a highly skewed sex ratio (1 M:5 F). As Hill (1994) suggested, when many females are present as potential grooming partners, males may not resort to grooming one another. Frequency and severity of male-male aggression correlate with the ranks distance of contestants (de Waal, 1991). Several studies report that the primary purpose of aggressive interactions appears to be the reassertion of rank over another animal (Rowell, 1974; Walters, 1980; de Waal, 1991). In multimale groups with female-skewed sex ratios, there often is strong competition for females. Male-male-aggression increases when more estrous females are present (Vandenbergh and Vessey, 1968; Bercovitch, 1983; Janson, 1984), and the large number of females in our study increased the probability that more females were in estrous simultaneously. The difficulty in monopolizing females when so many females and potential competitors are present could provoke antagonistic relationships among males. Because rank changes usually occur between individuals of adjacent rank (Johnson 1989) and access to resources usually depends on the outcome of aggressive contests, we expect intense fights to occur most frequently between animals of adjacent rank since the contestant that ranks immediately below an individual has the greatest chance of all subordinate animals to win an agonistic interaction and thus gain access to contested resources. Exceptions to the aggressive interactions typical of crested black macaques are male-male mounting and penis-grabbing behavior. There is no consistent rank-related pattern in mounting; animals of all rank initiated mounts. Penis-grabbing may be an example of the stereotyped greeting behavior observed in baboons (Papio anubis) and bonnet macaues (Sugiyama, 1971; Strum, 1982). Possibly the behaviors serve to reduce tension among males in close proximity, but the role of these affiliative behaviors in malemale social relationships of crested black macaques requires more study. Rank-Based Attractiveness High-ranking male crested black macaques had more neighbors more often than low-ranking males did, a result reported for other macaque species (Fairbanks, 1980; Silk, 1982; Chapais, 1983b). These neighbors tended to be adult females and juveniles rather than adult and subadult males. Seyfarth (1977) proposed that, among female cercopithecine primates, high ranking individuals are attractive because proximity to dominant animals confers special benefits, such as support during agonistic interactions (Smuts, 1985). Among our subjects, the high-ranking males received more grooming from adult females, which indicates that high-ranking males are attractive social partners for females (Kaufman, 1965; Sugiyama, 1971;

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Smuts, 1985; Hill, 1987; O'Brien, 1991). Kinship is probably unimportant as an explanation for attractiveness because males have immigrated into the group and are probably unrelated to adult females (Smuts, 1985). Highranking male crested black macaques may offer several benefits to females. First, the proximity of a high-ranking male may deter low-ranking adult and subadult males from harassing them. Such protection may be important because low-ranking crested black macaque males are more aggressive toward females than high-ranking males are. Second, females foraging in the vicinity of high-ranking adult males may suffer less feeding competition from other adult and subadult males (Janson, 1985). Finally, the high-ranking males usually are preferred sexual partners (O'Brien, 1991; Janson, 1984) and presumably confer superior genes to the female's offspring. The data on grooming, spatial association, and sexual presentations (Bernstein and Baker, 1988; Bulger, 1993) suggest that female crested black macaques prefer high-ranking adult males as partners. The preference of females for high-ranking males and the priority of access to females based on dominance rank suggest that male dominance in Sulawesi macaques should skew male reproductive success (Altmann, 1962; Hausfater, 1975; Seyfarth, 1978; Rasmussen, 1983). Many students of social behavior and reproduction have found a correlation between dominance rank and mating success (Kaufmann, 1965; Packer, 1979; Smith, 1981; Berenstain and Wade, 1983; Chapais, 1983a,b; Hill, 1987; Cowlishaw and Dunbar, 1991; Bulger, 1993), but the result is not universal (Loy, 1971; Smuts, 1985; Bercovitch, 1986, 1987; McMillan, 1989; Berard et al., 1990). For example, among species with infanticidal males, females may mate with many males in order to confuse paternity and to prevent male aggression toward their infants in the future (Hrdy, 1974; Taub, 1980; Wrangham, 1980). Genetic paternity testing in captive groups for the relationship between rank and reproductive success has yielded ambiguous results: some studies show that dominance rank and reproductive success are correlated (Paul et al., 1993; de Ruiter and van Hooff, 1993; Smith, 1993), while others exhibit no such correlation (Duvall et al., 1976; Bercovitch, 1991; Berard et al., 1993). Although we found a high correlation between rank and frequency of copulation (the two highest-ranking males had more than twice as many copulations than the four lower ranking males), the sample size is small and the trend is not statistically significant (0.05 < P < 0.10). In particular, the highest ranking male had fewer copulations than the second ranking male did. Copulation rate per se may not be an appropriate measure of mating success. Because female primates often mate at times when they are not ovulating, males that mate more frequently, but at the wrong times, will not necessarily sire more offspring. Several studies that show either weak or no correlation between rank and rate of mating also evi-


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dence that high ranking-males often mate more on days when the female is most likely ovulate (Carpenter, 1942; Packer, 1979; Chapais, 1983b). In our subject, the frequency of copulation for all males was twice as high with swollen (sexually receptive) females as with females in the early or late stages of the estrous cycle which indicates that all males attempt to time copulations when females are likely to conceive. Since accurate data on the timing of ovulation during estrous are unavailable for our subjects, we cannot assess whether high-ranking males were especially selective in mating during ovulation. Male Dominance Hierarchies

Thierry (1994) reported only a weak influence of dominance relationships on social grooming for tonkean macaques, and Bernstein and Baker (1988) found no correlation between dominance hierarchy and mounting or grooming relationships in captive crested black macaques. Contrarily found that dominance, defined in terms of aggressive interactions among males, strongly correlates with other forms of social behavior. High-ranking males received grooming more frequently, had receptive females as their nearest neighbors more often, and may copulate more frequently with receptive females than low ranking males do. These data do not support the view that adult male crested black macaques have an egalitarian pattern of dominance interactions. Male dominance in crested black macaques appears to be an important factor in access to desirable resources and social organization; this pattern is more representative of that described for free ranging populations of macaques (Hill, 1994). Captive housing conditions under which Sualwesi macques typically have been studied—single male groups or confined space—may inhibit expression of the full range of behavior and obscure the overall nature of dominance relationships in Sulawesi macaques. ACKNOWLEDGMENTS

This study was conducted under the auspices of the Indonesian Institute of Science (LIPI) and the Indonesian Ministry of Forestry (PHPA). Financial support was provided by the Wildlife Conservation Society, the Wenner-Gren Anthropological Foundation, and the John Motley Morehead Foundation. We thank Romon Palete (PHPA, North Sulawesi) for his support of WCS research in North Sulawesi and Haven Wiley for extensive comments on early drafts of the manuscript. We also thank Felix Manderos, Sakar Tunungki, and Uri Ganta for their assistance in data collection.


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