Effects of orbitofrontal lesions on social behavior in a confined group of stump-tail macaques (Macaca speciosa)

We grouped 14 stump-tail macques, five males and nine females, and observed social behavior before subjecting four of them to resection of orbitofrontal cortex. Four monkeys also received control lesions of superior temporal cortex and the remaining animals served as unoperated controls. Observations of social behavior continued after surgery on the following behavior: Joining, grooming, self-grooming, threat, aggression, and presenting (total hours of observation equaled 154). Monkeys with orbitofrontal lesions showed decreases in threat and aggression but only one such monkey fell in dominance. Control (operated and unoperated) monkeys displayed little change in these behaviors. Monkeys with orbitofrontal lesions also increased joining and self-grooming but showed a decrease in grooming of others. Presenting did not change. The role of orbitofrontal cortex in modulating different aspects of social interaction is emphasized by these results. However, in primates this area of the frontal lobes appears to have its major influence in the emotional loading of such complex behaviors.     

Male Social Behavior and Dominance Hierarchy in the Sulawesi Crested Black Macaque (Macaca nigra)

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.     

Evaluating Dominance Styles in Assamese and Rhesus Macaques

Researchers have suggested that several types of agonistic and affiliative behavior covary as a set of species-specific traits, and have used the term dominance style to describe the covariation. We compared measures of dominance style between a group of Assamese macaques (Macaca assamensis) and a group of rhesus macaques (M. mulatta), though kinship information was unknown. Assamese and rhesus female-female dyads each showed a low proportion of counter aggression and a low conciliatory tendency, suggesting that they have despotic social relationships. They also showed a despotic pattern on several other types of agonistic and affiliative behavior, such as approach outcomes and grooming distributions, which is consistent with the covariation of dominance style traits. Assamese male-male dyads showed relatively high levels of reconciliation and counter aggression versus other macaque males portrayed in the literature, suggesting that Assamese males have a tolerant dominance style. Insofar as macaque dominance style depends on the behavior of females, we suggest that Assamese macaques, like rhesus macaques, have despotic social relationships, which contrasts with evidence of a strong correlation between phylogeny and dominance style in macaques. Further, our results indicate that strong male bonding and tolerant dominance relationships among males are independent of female dominance style. Lastly, some measures of agonistic behavior, such as rate of aggression or proportion of bites, are likely altered in competitive environments and thus are not useful indicators of dominance style.     

Social communication among captive stump-tailed macaques (Macaca arctoides)

I compared the frequency of occurrence, contextual usage, and meaning of some of the most prominent gestural signals in stump-tailed macaques. I recorded the occurrence of 15 visual and tactile behavior patterns in a multimale multifemale captive group of stump-tailed macaques with the behavior sampling method in 100 hr of observation and analyzed the data via factor analysis and analyis of variance. The hindquarter presentation was the most frequent gesture. It was displayed by subordinates to appease dominants even in the absence of impending risk of aggression. Bared-teeth, lip-smack, teeth-chatter, and present-arm are submissive signals as well, but they differ from the presentation and from one another in their contextual usage. Nonthrusting mount, hip-touch, hip-clasp, and genital manipulation are directed down the hierarchy and appear to reflect dominance, reassurance, protection, or bonding. Mock-bite is a ritualized aggressive behavior pattern, often used to resolve uncertain dominance relationships. Ventroventral embrace occurs as a female bonding pattern. Overall, most gestural signals in stump-tailed macaques relate to dominance and submission and, to a lesser extent, social bonding.     

Mating behavior of ring-tailed lemurs (Lemur catta) at Berenty,Madagascar

The mating behavior of ring-tailed lemurs at Berenty, Madagascar, was observed in April 1982. Although Troop A included five adult females, only two were observed to mate. The mating period covered two consecutive days, April 24 and 25. Each female was receptive for about 4 hr. Data from 47 copulations, of which 38 were with ejaculation, suggest that to be the first mating partner is of importance for male ring-tailed lemurs. Previously it has been suggested that male dominance is of little significance in determining mating partners. In this investigation it was observed that the second most dominant male MK was always the first mating partner. Only after several ejaculations and resultant fatigue did he lose possession of the female to lower ranking males, and the first ranking male was not seen to copulate with either female at any time. These results suggest that a male's mating success is partly, but not completely correlated with his dominance rank, and that other factors, including his length of residence in the group and female choice, also determine patterns of mating.     

Behavioural dominance and reproductive success in female Japanese monkeys (Macaca fuscata)

Eight years of reproductive data (including 248 births) from a translocated troop of Japanese monkeys (Macaca fuscata) living in a 42-ha enclosure provided three measures of female reproductive success: fecundity, survival of infants to 1 year of age, and age at first parturition. No significant relationship was found between social dominance and these measures. Social dominance was considered with respect to both matrilineal and individual female rank. Additional data on female dominance ranks over four generations of adult females revealed no significant concordance over time. The finding that ranks may not be stable over the lifetime of a female is a significant one because the variation in reproductive success among the females of a group is likely to be further diminished by any instability. For 34 females that were adults for the 8-year period considered, there was no significant correlation between the average rank of a female and either fecundity or survivorship of infants to 1 year of age. These data considered along with the results of other studies of female dominance and reproduction suggest that any effect of female social dominance on reproductive success is probably dependent upon resource availability, with significant benefits accruing to high-ranking individuals only during subsistence periods. It is suggested that dominance competition among female macaques may be a behavioural strategy with a variable payoff.     

Emergence of complex social networks from spatial structure and rules of thumb: a modelling approach

Individual-based computer models show that simple heuristic governing individuals’ behavior may suffice to generate complex patterns of social behavior at the group level such as those observed in animal societies. ‘GrooFiWorld’ is an example of such kind of computer models. In this model, self-organization and simple behavioral rules generate complex patterns of social behavior like those described in tolerant and intolerant societies of macaques. Social complexity results from the socio-spatial structure of the group, the nature of which is, in turn, a side-effect of intensity of aggression. The model suggests that a similar mechanism may give rise to complex social structures in macaques. It is, however, unknown if the spatial structure of the model and that of macaques are indeed similar. Here we used social networks analysis as a proxy for spatial structure of the group. Our findings show that the social networks of the model share similar qualitative features with those of macaques. As group size increases, the density and the average individual eigenvector centrality decrease and the modularity and centralization of the network increase. In social networks emerging from simulations resembling intolerant societies the density is lower, the modularity and centralization are higher, and the individuals ranking higher in the dominance hierarchy are more central than in the social networks emerging from simulations resembling egalitarian societies. Given the qualitative similarity between the social networks of the model and that of empirical data, our results suggest that the spatial structure of macaques is similar to that of the model. It seems thus plausible that, as in the model, the spatial structure combined with simple behavioral rules plays a role in the emergence of complex social networks and complex social behavior in macaques.     

Counter aggression and reconciliation in Assamese macaques (Macaca assamensis)

Patterns of aggressive and affiliative behavior, such as counter aggression and reconciliation, are said to covary in the genus Macaca; this is referred to as the systematic variation hypothesis. These behavior patterns constitute a species dominance style. Van Schaik's [1989] socioecological model explains dominance style in macaques in terms of within- and between-group contest competition. Dominance style is also said to correlate with phylogeny in macaques. The present study was undertaken to examine phylogenetic and socioecological explanations of dominance style, as well as the systematic variation hypothesis. We collected data on counter aggression and reconciliation from a habituated group of Assamese macaques (Macaca assamensis) at the Tukeswari Temple in Assam, India. The proportion of agonistic episodes that involved counter aggression was relatively low. Counter aggression, however, occurred more often among males than among females, and it was most common when females initiated aggression against males. The conciliatory tendency for this group of Assamese macaques was 11.2%. The frequency of reconciliation was low for fights among males and for fights among females, but reconciliation was particularly rare for opposite-sexed opponents. Female social relationships were consistent with the systematic variation hypothesis, and suggest a despotic dominance style. A despotic dominance style in Assamese macaques weakens the correlation between dominance style and phylogeny in macaques, but it is not inconsistent with the socioecological model. Male-female relationships were not well explained by the despotic-egalitarian framework, and males may well have more tolerant social relationships than do females. Sex differences need to be considered when categorizing species according to dominance style.     

The Absence of Grooming for Rank-Related Benefits in Female Assamese Macaques (Macaca assamensis)

Seyfarth’s model of social grooming proposes that by grooming females higher ranking than themselves, females can gain access to important rank-related benefits, such as agonistic support. This, in turn, produces a distinctive pattern of grooming in which females direct their grooming up the female dominance hierarchy and compete for access to the highest ranking individuals. We aimed to test to what extent the grooming behavior of female Assamese macaques (Macaca assamensis) fits the assumptions and predictions of Seyfarth’s model. During two 1-yr sampling periods (October 2007–September 2008, May 2010–April 2011) we collected >2100 focal hours of data from a single wild group in their natural habitat at Phu Khieo Wildlife Sanctuary, Thailand. Subjects included all adult female group members (N?=?12 in 2007/8; N?=?15 in 2010/11). We collected detailed data on grooming interactions, approaches, and departures as well as all aggressive and submissive behaviors between all subjects. We found no evidence that grooming was exchanged for rank-related benefits. In line with this we found no evidence that the grooming of female Assamese macaques fits the pattern predicted by Seyfarth’s model. These results are surprising given that such deviations from Seyfarth’s model are relatively rare among macaques. We propose that our findings are best explained as a lack of a need for rank-related benefits by females in this group.     

Play behavior in immature moor macaques (Macaca maura) and Japanese macaques (Macaca fuscata)

Play is widespread across mammalian taxa, but species strongly vary in the ways they play. In less despotic primate species (i.e., with less steep dominance hierarchies, less severe conflicts, and more reconciliation), play has been described as being more frequent, cooperative, and freely expressed. To study the link between social play and dominance style, we compared play behavior in free-ranging infants, juveniles and subadults of more despotic Japanese macaques (Macaca fuscata, N = 24) and less despotic moor macaques (Macaca maura, N = 17). We found interspecific differences in play behavior that corresponded with the contrasting dominance styles of the study species, largely confirming our predictions. In particular, moor macaques spent a larger proportion of time in solitary and social play than Japanese macaques, while Japanese macaques spent a larger proportion of time in grooming interactions. In moor macaques, play sessions included more players, a larger variety of play behaviors, greater play face rates, a greater proportion of time in contact play, and a higher rate of reciprocal play-biting than in Japanese macaques. Aggressive escalations were not common, but more frequent in Japanese macaques. Finally, a higher frequency of play faces during play sessions predicted the occurrence of more reciprocal play-bites, but not the proportion of time spent in contact play behaviors. Additional studies on other groups and species will allow a better understanding of the link between dominance style and social play.     

Behavior, color change and time for sexual inversion in the protogynous grouper (Epinephelus adscensionis)

Hermaphroditism, associated with territoriality and dominance behavior, is common in the marine environment. While male sex-specific coloration patterns have been documented in groupers, particularly during the spawning season, few data regarding social structure and the context for these color displays are available. In the present study, we define the social structure and male typical behavior of rock hind (Epinephelus adscensionis) in the wild. In addition, we detail the captive conditions and time period necessary to induce the onset of the sex-specific coloration and sexual change. At six oil production platform locations in the Gulf of Mexico, rock hind social group size and typical male rock hind social behavior were documented. We observed a rapid temporary color display in rock hind that could be turned on and off within three seconds and was used for confronting territory intruders and displays of aggression towards females. The male-specific "tuxedo" pattern consists of a bright yellow tail, a body with alternating dark brown and white patches and a dark bar extending from the upper mandible to the operculum. Identification and size ranges of male, female and intersex fish collected from oil platforms were determined in conjunction with gonadal histology. Rock hind social order is haremic with one dominant male defending a territory and a linear dominance hierarchy among individuals. In five captive experiments, the largest remaining female rock hind displayed the male specific color pattern within 32d after dominant male removal from the social group. To our knowledge, this is the first evidence in a grouper species of color patterning used to display territoriality and dominance outside of spawning aggregations. The behavioral paradigm described here is a key advance that will enable mechanistic studies of this complex sex change process.     

Social Tolerance in Wild Female Crested Macaques (Macaca nigra) in Tangkoko‐Batuangus Nature Reserve,Sulawesi, Indonesia

In primates, females typically drive the evolution of the social system and present a wide diversity of social structures. To understand this diversity, it is necessary to document the consistency and/or flexibility of female social structures across and within species, contexts, and environments. Macaques (Macaca sp.) are an ideal taxon for such comparative study, showing both consistency and variation in their social relations. Their social styles, constituting robust sets of social traits, can be classified in four grades, from despotic to tolerant. However, tolerant species are still understudied, especially in the wild. To foster our understanding of tolerant societies and to assess the validity of the concept of social style, we studied female crested macaques, Macaca nigra, under entirely natural conditions. We assessed their degree of social tolerance by analyzing the frequency, intensity, and distribution of agonistic and affiliative behaviors, their dominance gradient, their bared‐teeth display, and their level of conciliatory tendency. We also analyzed previously undocumented behavioral patterns in grade 4 macaques: reaction upon approach and distribution of affiliative behavior across partners. We compared the observed patterns to data from other populations of grade 4 macaques and from species of other grades. Overall, female crested macaques expressed a tolerant social style, with low intensity, frequently bidirectional, and reconciled conflicts. Dominance asymmetry was moderate, associated with an affiliative bared‐teeth display. Females greatly tolerated one another in close proximity. The observed patterns matched the profile of other tolerant macaques and were outside the range of patterns of more despotic species. This study is the first comprehensive analysis of females’ social behavior in a tolerant macaque species under natural conditions and as such, contributes to a better understanding of macaque societies. It also highlights the relevance of the social style concept in the assessment of the degree of tolerance/despotism in social systems. Am. J. Primatol. 75:361‐375, 2013. © 2013 Wiley Periodicals, Inc.     

Dihydrotestosterone propionate effects on dominance and sexual behaviors in gonadectomized male and female rhesus monkeys.

One triad of male and two triads of female gonadectomized rhesus monkeys were observed as social groups assembled for repeated hour-long sessions. Social relationships were measured in terms of aggressive behavior between the members of each group in order to determine the dominance hierarchical order. Sexual performance was assessed for each male, before and after castration, in tests with an estrogen-stimulated ovariectomized female. Similar measures were made when the same female was periodically introduced to the all-male triad. When dihydrotestosterone propionate (DHTP) was administered for a period of 6 weeks to the middle-ranking member of each group, social status changes occurred in two groups, one male and one female, resulting in the elevation of the treated monkeys to the highest rank in the dominance hierarchy. In the other female group, aggressive behavior was increased with DHTP treatment of the middle-ranking female. Somatic effects, particularly a gain in body weight, occurred in all treated animals. Yawning behavior also increased significantly in those animals receiving DHTP. The latter two effects returned toward pretreatment levels following the cessation of hormone injection; however, changes in dominance hierarchy persisted to the end of the experiment, 6 weeks following the last DHTP treatment.     

Female rank instability in newly formed groups of familiar sooty mangabeys (Cercocebus torquatus atys)

The formation of two new groups of sooty mangabeys (N=6; N=11) comprised of individuals removed from their natal group of 98 animals led to dominance rank challenges with aggression and wounding, though this occurred after an interval of months. Dominance rank challenges were not expected because, unlike rhesus macaques, adult female sooty mangabeys do not affiliate with adult kin significantly more than nonkin and show minimal agonistic aiding even with adult kin, thus rank would seem to be independent of aiding. Moreover, during the last nine years, severe wounding of adults in a large stable group of sooty mangabeys has been virtually absent and agonistic behavior in a stable group of sooty mangabeys is exhibited at a low rate compared to some macaque species. New members in the group of six maintained their relative ranks for 12 weeks after which the beta supplanted the alpha female with no serious wounding. This ranking remained stable for 29 weeks after which the alpha and beta females were supplanted with fatal wounds inflicted to the alpha and less severe wounds to the beta female. The second subgroup also kept their relative ranks initially. However, after 27 weeks the lowest ranking female severely wounded the next to last ranking female and 1 week later attacked and displaced the alpha female with minimal wounding. Fourteen weeks later the beta female (formerly the alpha) attacked and severely wounded the new alpha female and regained the top dominance position. These events suggest that although sooty mangabeys do not exhibit strong kin preferential behavior among adults, they do have defined relationships within the long term, stable group. Removal from those defined relationships allows the possibility of social reorganization that may be mediated by serious aggression.     

Close bonds and social rank similarities favor non-random mating in captive stump-tailed macaques (Macaca arctoides)

Assortative mating is non-random mating by the mutual choice of phenotypes or behavioral types. In polygynandrous species, competition for mating by social rank can lead to assortative mating. However, although not an individual trait, social bonds also influence mating opportunities resembling assortative mating. Stump-tailed macaques form long-term close bonds and organize in a linear dominance–subordination hierarchy. Therefore, we studied whether the strength of the social bond and rank closeness influenced mating decisions and increased mating opportunities, particularly for low- and middle-ranking animals. Firstly, we observed whether females directed proceptive behavior to close-bonded or adjacent rank males. Secondly, we measured whether successful copulations were related to the strength of social bonds and close ranking. Thirdly, to ensure that copulations owed mainly to the aforementioned factors, we also evaluated whether sexual coercion was unrelated to social bonds and rank similarities. Finally, we assessed whether close bonds mediated agonistic support to females. The study subjects were 12 adult female and 11 male captive stump-tailed macaques. We monitored daily females' reproductive status by vaginal cytology. Sexual behavior was recorded by all occurrences sampling and scan sampling to collect the agonistic and affiliative instances required to calculate social ranks, social bond strength, and agonistic support. The results indicated that the probability of females displaying proceptivity increased during the follicular phase toward close-bonded and high-ranking males. Copulation chances increased with male–female social bonds and rank closeness. Forced copulation decreased in close-bonded individuals, while agonistic support increased in close-ranking strong-bonded animals. In conclusion, close social bonds and similar social rank result in non-random mating in stump-tailed macaques.     

The influence of rank on affect perception by pigtailed macaques (Macaca nemestrina)

Previous studies of affect perception in nonhuman primates have involved young animals and/or manipulations of early experience. Based upon data suggesting that middle-ranked monkeys in small social groups show patterns of behavior different from their low- or high-ranked counterparts, the current study examined the role of social rank in affect perception by normally reared, adult female pigtailed macaques. Employing color videotapes as the presentation medium, we observed animals as they watched unfamiliar animals display social (aggressive or submissive) or nonsocial behavior. Virtually all threats were recorded as the subjects watched the submissive presentations, and most submissive signals occurred while watching aggressive behavior tapes. Middle-ranked monkeys were most attentive during all presentations, and levels of disturbance behavior were related to rank of the watcher and type of presentation observed. The results suggest that dominance status is an influence in the process of affect perception.     

The effectiveness of sampling methods in detecting copulatory behavior in Macaca arctoides

The copulatory behavior of a social group of 18 stumptail macaques was observed for 171 hours over a period of 5 months. The occurrence of copulation and several quantitative measures of copulation were compared using sampling periods of 2 hours daily and continuous dawn-to-dusk observation. In this environment copulation was found to occur in brief bouts of relatively short duration. Copulation was detected on 34% of the days observed with 2 hr sampling and 100% of the days with DTD sampling. Thus, brief limited-time samples of behavior are not adequate for reliably detecting copulation in this species under social group-living conditions.     

Male–Male Relationships in Lion-tailed Macaques (<Emphasis Type="Italic">Macaca silenus</Emphasis>) and Bonnet Macaques (<Emphasis Type="Italic">Macaca radiata</Emphasis>)

Socioecology suggests that female distribution in space is determined by the distribution of food resources and the male distribution is influenced by female distribution. Though studies have traditionally focused on females, males have received increasing attention in recent years. We compared male–male relationships in lion-tailed macaques and bonnet macaques. Because bonnet macaques have a high adult male:female sex ratio and are seasonal breeders whereas lion-tailed macaques have a low adult male:female sex ratio and are largely aseasonal breeders, we predicted that bonnet macaque males would be spatially and socially more tolerant of each other and would have less linear dominance relationships than lion-tailed macaques. We recorded male–male and male–female relationships in 1 group of wild macaques of each species via scan sampling and 1–0 sampling. The results revealed that lion-tailed macaque males largely remained at a distance from each other whereas bonnet macaque males remained in close proximity to one another. Lion-tailed macaque males were more agonistic toward each other whereas bonnet macaque males showed more affiliative interactions. The dominance hierarchy among lion-tailed macaque males was more linear than among bonnet macaque males. Our data support the hypothesis that the study of spatial structuring, temporality of interactions, and linearity of social relationships may contribute to a better understanding of macaque social systems.     

成年黄山短尾猴雌性等级结构稳定性

等级结构稳定性是衡量群体凝聚力的重要指标,雌性等级结构稳定对于母系社会群体具有重要的生物学意义。本文采用目标动物取样和全事件记录相结合的方法,研究黄山短尾猴鱼鳞坑A1 群(YA1 群)和鱼鳞坑A2 群(YA2 群)的成年雌性分别在交配季节(2011 年9 ～ 12 月)和非交配季节(2012 年2 ～ 5 月)内的攻击-屈服行为。采用等级结构中雌性间攻击- 屈服频率、社会顺位和等级梯度3 个量化指标,首次定量探讨了短尾猴雌性等级结构及其稳定性。研究期间,YA1 群和YA2 群雌性间攻击- 屈服频率、社会顺位和等级梯度均无季节性变化(P >0. 05)。结果表征短尾猴雌性等级结构趋于稳定,该结果支持了短尾猴雌性等级结构稳定性的定性判断。     

Affiliative relationships and reciprocity among adult male bonnet macaques (Macaca radiata) at Arunachala Hill, India

In captivity, male bonnet macaques (Macaca radiata) frequently express "friendship" toward one another, including affiliative behavior such as huddling, grooming, coalitionary support, and sitting in close proximity. The purpose of this study was to determine whether wild adult male bonnet macaques also express "friendship" by investigating whether or not (1) adult male bonnet macaques have affiliative social relationships with other males, (2) the strength of social relationships varies among dyads, (3) there is time-matched reciprocity in allogrooming among dyads, and if so, whether the level of reciprocity occurs within a bout of grooming, a day, or over 2 months (the limit of this study), and (4) a correlation exists between the strength of social relationships and dominance ranks among adult males. Focal samples totaling 150 hr on all seven adult males in one study group were conducted to record both agonistic and affiliative interactions. Agonistic interactions were used to construct a dominance hierarchy, whereas affiliative interactions (sitting in proximity to within 1 m with and without grooming) were used to quantify the existence and strength of social bonds within dyads. Results show that adult male bonnet macaques had differentiated affiliative relationships with other males in their group. There was little reciprocity of grooming within a bout of grooming or within a day, but greater reciprocity over the study period of 2 months. There was no correlation between dominance ranking distance and the strength of affiliative relationship within dyads; however, within dyads lower-ranking males groomed higher-ranking males more than vice versa. This study suggests that friendships in male bonnet macaques are characterized not by immediate tit-for-tat reciprocal altruism, but by reciprocity over a longer time span, and that affiliative social relationships may be less constrained by agonistic relationships than is the case in more despotic species of macaques.