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.     

Male competition and its hormonal correlates in Assamese macaques (Macaca assamensis)

In polygynous mammals, where males compete over access to females, the potential of males to monopolize reproductive females largely depends on the spatio-temporal distribution of reproductive females. We investigated mechanisms of male reproductive competition and its hormonal basis in a cercopithecine species with reduced contest potential owing to female reproductive synchrony and concealed ovulation. Over 16 months including two mating seasons we collected 1218 h of observational focal animal data and 1254 fecal samples of 11-12 adult and large subadult male Assamese macaques (Macaca assamensis) living in their natural habitat in Thailand. Androgen output along with aggressive behavior showed a seasonal pattern, with highest values being obtained by all males during the mating season and by those males experiencing acute social challenges, e.g. rank change and dispersal. Individual androgen levels and rates of attacks were linked across the study period, suggesting a promoting function of androgens for aggressive behavior. Dominance rank predicted neither mating success nor androgen levels consistently, indicating a reduced selective advantage of high social status for general mating access. However, high ranking males engaged in extended consortships with reproductive females. Distribution of consortships across males followed a priority of access distribution, with the two top ranking males accounting for 75% of consort activity, suggesting that high social status also carries fitness benefits in a species characterized by low contest potential.     

Personality of Wild Male Crested Macaques (Macaca nigra)

Animal personalities, i.e. consistent differences in behavior across time and/or context, have received increased attention of behavioral biologists over the last years. Recent research shows that personalities represent traits on which natural and sexual selection work and which can have substantial fitness consequences. The aim of this study is to establish the personality structure of crested macaque (Macaca nigra) males as foundation for future studies on its adaptive value. We collected behavioral data through focal animal sampling and additionally conducted two sets of playback experiments. Results of a factor analysis on the behavioral data revealed a four factor structure with components we labeled Anxiety, Sociability, Connectedness and Aggressiveness. Results from the experiments revealed an additional and independent Boldness factor but the absence of Neophilia. Overall, this structure resembles other macaque and animal species with the exception of Connectedness, which might be a consequence of the species'' tolerant social style. Our results thus not only form the basis for future studies on the adaptive value of personality in crested macaques but also contribute an important data point for investigating the evolution of personality structure from a comparative perspective by refining, for example, which personality factors characterized the last common ancestor of hominids and macaques.     

Dominance, aggression and physiological stress in wild male Assamese macaques (Macaca assamensis)

In group-living animals relative rank positions are often associated with differences in glucocorticoid output. During phases of social stability, when dominance positions are clear and unchallenged, subordinates often face higher costs in terms of social stress than dominant individuals. In this study we test this prediction and examine additional potential correlates of stress, such as reproductive season, age and amount of aggression received in wild, seasonally breeding Assamese macaques (Macaca assamensis). During a mating and a non-mating season we collected 394 h of focal observational data and 440 fecal samples of six adult and six large subadult males living in a multimale–multifemale group in their natural habitat in northeastern Thailand. The mating season was characterized by a general increase in aggressive behavior and glucocorticoid excretion across all males compared to the non-mating season. Among adult males, mating season glucocorticoid levels were significantly negatively related with dominance rank and positively with the amount of aggression received. Both relationships were non-significant among large subadult males. Thus, our results suggest that in adult Assamese macaques a high dominance position is not associated with high costs. Low costs of dominance might be induced by strong social bonds among top-ranking males, which exchange frequent affiliative interactions and serve as allies in coalitionary aggression against potentially rank-challenging subordinate males.     

The Costs of Reproductive Success in Male Rhesus Macaques (Macaca mulatta) on Cayo Santiago

Sexual selection acts to increase the success of males possessing advantageous traits in competition over females. In primates, interspecific variability in social and mating systems creates highly variable selective pressures on males, changing the relative strength of both intra- and intersexual selection, and the relative degree of direct vs. indirect male–male competition. Rhesus macaques are an interesting species for studying intrasexual selection and male–male competition, because they exhibit relatively low (for Papionini) body and canine size dimorphism, and exhibit large testes, suggesting reduced direct competition and strong indirect competition. We have undertaken several studies of male rhesus macaques on Cayo Santiago, from analyses of long-term life-history data to shorter term projects that combined noninvasive measures of physiological markers such as concentrations of urinary C-peptide of insulin and androgen and glucocorticoid (GC) concentrations, with measures of behavior and of sexually selected signals (male red facial coloration). We here review these studies, combining data from short-term studies with long-term mortality data to present an integrated picture of both the short- and long-term gross costs of male mating competition. We find that males exhibit many signs of the costs of indirect competition, such as energetic consequences of reduced feeding and high copulation rates. During periods of more direct contest, such as during dominance instability, males are also characterized by high androgen and GC concentrations among high-ranking individuals. Consistent with relatively weak direct male–male competition, male red skin coloration appears to be more related to female choice (intersexual selection) than the signaling of dominance status (intrasexual selection). Forty-five years of life-history data show that male mortality is higher during the mating than the birth season, a pattern we hypothesize to be linked to the costs associated with mating activity. We finish by discussing unresolved issues, such as the costs of sperm competition and the data that are needed to address them.     

Distribution of Assamese macaques (Macaca assamensis) in the Inner Himalayan region of Bhutan and their mtDNA diversity

The distributions of Assamese macaques (Macaca assamensis) and rhesus macaques (M. mulatta) in Bhutan have been only partially documented. In order to investigate the distribution patterns of these species, we conducted field observation and genetic assessment with mitochondrial DNA (mtDNA) typing of macaques in the Inner Himalayas of Bhutan. There were 24 sightings of macaque groups, and all were visually identified as Assamese macaques. No groups of rhesus macaques were sighted in this survey area, in contrast with the survey results in the Nepalese Himalayas. Molecular phylogenetic analysis revealed that the Bhutan macaques are closer in proximity to their counterparts in the Indo-Chinese region (Thailand and Laos) than to rhesus macaques in China, Laos and India. However, clustering results suggested the marked differentiation of the macaques in Bhutan from the Assamese macaques in Indo-China. We tentatively conclude that the macaques of the Inner Himalayan regions in Bhutan are Assamese macaques and that they appear to be of a lineage distinct from Assamese macaques in the Indo-Chinese region (subspecies M. a. assamensis). The degree of mtDNA diversity suggests that the Assamese macaques in Bhutan are of a more ancient ancestry than M. a. assamensis, thereby supporting the speciation hypothesis of the expansion of a sinica-group of macaques from South Asia to Southeast and then to East Asia (Fooden; Fieldiana Zool 45:1–44, 1988). Assignment of Assamese macaques in Bhutan to M. a. pelops is premature due to the lack of molecular data and recent taxonomic controversy. The mtDNA diversity of Assamese macaques was greater than that of rhesus macaques, suggesting the earlier speciation of Assamese macaques. The significance of the ecogeographic segregation model of macaque distribution is discussed in relation to the evolutionary range expansion into the Himalayan regions in South Asia.     

Reaction to Snakes in Wild Moor Macaques (Macaca maura)

International Journal of Primatology - Snake predation is considered an important evolutionary force for primates. Yet, very few studies have documented encounters between primates and snakes in...     

Preliminary study of the genetic diversity of eastern Assamese macaques (Macaca assamensis assamensis) in Thailand based on mitochondrial DNA and microsatellite markers

Human overpopulation, deforestation, invasion of agricultural areas, and livestock are the primary causes for population fragmentation of wildlife. The distribution range of species of the genus Macaca is constantly decreasing and becoming increasingly fragmented due to forest deterioration. Assamese macaques (M. assamensis) are classified as near threatened in the International Union for Conservation of Nature (IUCN) Red List of Threatened Animals (2008) and have been declared a protected wildlife animal according to Wildlife Preservation and Protection Act, B.E.2535 (1992) of Thailand. As studies of the population history and genetic diversity of Assamese macaques in Thailand are currently lacking, we aimed at a first investigation of their genetic diversity based on mitochondrial DNA [hypervariable regions 1 and 2 (HV1, HV2) and cytochrome B (CYTB) regions], as well as 15 microsatellite markers of five sampling sites distributed across Thailand. Our results indicate that Assamese macaques in Thailand are diverse, with eight maternal haplotypes and a low inbreeding coefficient in the Phu Khieo Wildlife Sanctuary (PKWS) population. Moreover, our phylogenetic and median-joining network analysis based on mitochondrial (mt)DNA suggests a population distribution in accordance with the evolutionary scenario proposed for M. sinica. Today, the population of Assamese macaques is fragmented, and conservation strategies are needed to ensure the maintenance of genetic diversity of this primate species.     

Snake Species Discrimination by Wild Bonnet Macaques (Macaca radiata)

Wild bonnet macaques (Macaca radiata) were studied in southern India to assess their ability to discriminate non‐venomous, venomous and predatory snakes. Realistic snake models were presented to eight troops of bonnet macaques at feeding stations and their behavior was video‐recorded 3 min before and 3 min after snake exposure. Snakes presented were: (1) venomous Indian cobra (Naja naja) displaying an open hood with ‘eyespots’; (2) venomous common Indian krait (Bungarus caeruleus); (3) non‐venomous green keelback (Macropisthodan plumbicolor); (4) non‐venomous rat snake (Ptyas mucosus); and (5) Indian python (Python molurus) which preys on macaques. Latencies to detect and react to the snakes were evaluated to determine initial responsiveness. Longer‐term assessment was measured as the percentage of time individuals looked at the snakes and monitored the activity of nearby individuals before and after snake detection. All snake models engendered caution and maintenance of a safe distance. Alarm calling occurred only during python presentations. The cobra engendered a startle response or running in the largest percentage of individuals after its detection, whereas the rat snake and python elicited bipedal standing or ambulating to monitor the snakes. We also examined the influence of age on snake recognition. Juveniles and subadults looked at the cobra, krait, and python for a larger percentage of time than adults did; albeit, adults looked at the python substantially longer than at the other snakes. Age differences in behavior suggest that, with the exception of the python, repeated experience with snakes in the wild moderates excitability, consistent with the likely threat of envenomation.     

Birth Patterns in Wild and Captive Lion-Tailed Macaques (Macaca silenus)

During a 5-yr study of lion-tailed macaques in their natural habitat, we found that: 1) most births occurred from January to April (70%) and from September to December (19%), showing a bimodal pattern with a major and a minor birth peak; 2) the period of peaks remained the same over 5 yr; and 3) a similar pattern of birth peaks occurred both in groups in large forest complexes that had overlapping home ranges with other groups and in single groups that were isolated in forest fragments in the same region but with similar ecological conditions. The results suggest more of a birth seasonality than mere breeding synchronization in the wild lion-tailed macaques. We also analyzed data on births in captivity in European Zoos for 10 yr. We observed no seasonality or peaks in births, and the pattern was the same over the years. Data on rainfall suggest that resource availability in the wild habitat may not be uniform throughout the year; hence, ecological factors may play an important role in determination of birth patterns in the natural habitats of lion-tailed macaques.     

Male Migration in Barbary Macaques (Macaca sylvanus) at Affenberg Salem

We analyzed male migration during a 20-year period in the free-ranging Barbary macaque population of Affenberg Salem. Most natal migrations occurred around puberty, but only one third of all males left the natal group. Secondary group transfers were rare. All males immediately transferred to other bisexual groups. Migration rates were highest during periods with high adult female/male ratios within social groups. Immigrants highly preferred groups with fewer males of their own age than in the natal group, and many males immigrated into groups that had no male their own age. These groups originated from a skewed distribution of resident males during group fissions. A comparison of emigrants with their natal peers supports the inbreeding avoidance hypothesis as cause of emigration rather than the male competition avoidance hypothesis. Emigrants had no lower individual rank position and did not come from lower-ranking matrilines. Emigrants had more female maternal relatives, especially sisters. Males without female relatives almost never emigrated. Conversely, there is virtually no indication that emigrants were evicted from the natal group. Emigrants had no increased mortality. Paternity data revealed that the reproductive success of emigrants and natal males is similar, indicating that emigration had no reproductive cost. Many similarities between emigrants and natal males that separated from female maternal kin during group fissions suggest that inner migration during fissions is an alternative way to avoid maternal inbreeding. The mating system resulted in a genetic structure within social groups that largely diminished the chances for paternal inbreeding even without recognizing paternal kin.     

Correlates of Male Consortship Rate in Free-Ranging Rhesus Macaques (Macaca mulatta)

Male–male competition for access to receptive females can take the form of nonrecurring fights and/or a sustained contest over mating opportunities. Male physical condition has been linked to dominance rank and reproductive success in species characterized by intrasexual fights for dominance and access to females. In group-living species characterized by endurance rivalry, however, factors contributing to male reproductive success are less well understood. In such species, particularly seasonally breeding ones with low sexual dimorphism and seniority-based rank, age and social factors other than rank may prove important. In the absence of genetic data, male mate guarding or consortship can serve as an indicator of male reproductive success. To evaluate the contribution of age and intragroup sociality to male consortship rate, I collected behavioral data during one nonmating and one mating season in two social groups of free-ranging rhesus macaques that experience no predation or food scarcity. Higher-ranking males, younger males, or males that exhibited lower rate of intrasexual aggression had higher consortship rates. Male–female dyads that groomed outside consortship did not form consortships as often as dyads that did not engage in nonconsort grooming. This is the first study to identify the significance of male–male aggression and male–female affiliation to male consortship rate in a species characterized by endurance rivalry, high male rank stability, and strong female mate choice. Social behaviors and male age may be particularly important in determining male reproductive success in populations experiencing high food availability and a lack of predation, which are typical of an increasing number of vertebrates in areas densely populated by humans.     

The Habituation Process in Two Groups of Wild Moor Macaques (Macaca maura)

International Journal of Primatology - When studying animal behavior in the wild, some behaviors may require observation from a relatively short distance. In these cases, habituation is commonly...     

Anxiety Level Predicts Post-Conflict Behaviour in Wild Japanese Macaques (Macaca fuscata yakui)

Reconciliation (i.e. the post-conflict exchange of friendly behaviour between former opponents) functions to control for the detrimental effects that aggression may have on social relationships. Studies conducted so far have investigated intra-individual sources of variation in post-conflict behaviour, showing that animals have a stronger increase in anxiety and are more likely to reconcile after conflicts with valuable partners, such as kin. Much less attention has been given to how differences between individuals in emotional profiles affect post-conflict behaviour. Our aim was to analyse whether inter-individual differences in baseline anxiety levels predicted the magnitude of the increase in anxiety following a conflict and the occurrence of reconciliation. We collected data on two groups of wild Japanese macaques ( Macaca fuscata yakui ). Animals having a higher baseline level of anxiety had a more dramatic anxious response following a conflict while controlling for a series of factors (e.g. relationship quality between opponents). These more anxious animals were also less likely to reconcile than more relaxed individuals. Therefore, more anxious animals face some social costs by being less able to cope with the post-conflict condition. We propose that differences in anxiety levels may be interpreted as tradeoffs between benefits and costs across conditions. For example, more anxious animals, who are less able to reconcile conflicts, might also be less exploratory and thus face a lower risk to eat unknown, poisonous food.     

Socioecological Context of Parturition in Wild Japanese Macaques (Macaca fuscata) on Yakushima Island

Female primates may adopt special feeding, foraging, and social strategies around the time of giving birth. We observed 8 females during the prepartum period, the day of birth, and the postpartum period in a wild troop of Japanese macaques (Macaca fuscata yakui) on Yakushima Island, Japan. We collected data on their activity budgets, quantitative feeding and foraging behavior, and on female-male interactions. On the day of birth, females spent less time moving and feeding, and more time resting relative to other periods. Overall dietary diversity as well as arthropod foraging also decreased on the day of birth. Females fed mostly on mature leaves, new leaves and shoots during prepartum periods but mostly on fruit during postpartum periods. Decreased feeding on leaves and increased feeding on fruit probably changed as a result of seasonal availability, independently of parturition. Feeding on flowers, fungi and other items remained constant over all periparturitional periods. On the day of birth, new mothers had fewer social interactions with males and spent more time out of proximity with other adults than in other periods. Females rejected grooming presentations from males, groomed less with males, spent less time 3 m of males, and received less aggression from males on the day of birth. In the postpartum period, interactions with males returned to prepartum values. Grooming with females did not differ across the three periods. These results suggest that interactions with males may be costly for females on the day of birth.     

弄岗熊猴的活动节律和活动时间分配

2005年9月至2006年9月,采用瞬时扫描取样法,在弄岗国家级自然保护区对野生熊猴(Macaca assamensis)进行了连续跟踪观察,收集相关的活动节律和活动时间分配的数据,通过分析其与气候及食物组成的关系,从中探讨影响熊猴活动节律及活动时间分配的因素。研究结果发现:在熊猴的日活动节律中,觅食活动表现为逐渐增强的趋势,最高峰值出现在下午15:00,休息活动在中午出现一个小的高峰;其日活动节律表现出明显的季节性差异,主要表现为旱季大部分时间段的觅食强度均高于雨季,且早上7:00-10:00出现一段长时间的休息,而雨季里长时间的休息则发生在中午12:00-14:00;在活动时间分配上,熊猴平均花费39.6%时间用于休息,33.2%用于移动,18.3%用于摄食,5.1%用于理毛,2.4%用于玩耍,1.4%用于其他行为,其活动时间分配也表现出明显的季节性差异;与雨季相比,在旱季熊猴明显增加用于觅食的时间,而相应地减少用于休息的时间,活动时间分配的季节性变化明显与食物组成的变化有关;在不同年龄组个体间,青少年猴花费更多的时间用于玩耍,而用于休息和理毛的时间明显少于成年猴。     

Post-conflict Behaviour in Long-tailed Macaques (Macaca fascicularis)

After being the victim of an agonistic conflict, long-tailed macaques increased the rate of tension-related activities such as scratching, body-shake and selfgrooming. This increase indicates that they experienced physiological changes preparing them to cope with the uncertainty of the post-conflict situation. Indeed, victims of agonistic conflict experienced a higher risk of renewed attacks. However, victims were also involved in social interactions characteristic of post-conflict situations, namely reconciliation and redirection. These two post-conflict social events reduced the rate of scratching, body-shake and selfgrooming. This suggests a faster termination of the stress response. Indeed, the two social events also decreased the likelihood of renewed attacks, one of the causes of the state of uncertainty. Reconciliation is more effective than redirection in this process probably because the restoration of the relationship with the former aggressor allows the victim to resume control of the situation.     

Group Fission in Moor Macaques (Macaca maurus)

This is the first report of group fission in a wild group of Moor macaques (Macaca maurus) in South Sulawesi, Indonesia. The subject group, which has been observed on the basis of individual identification since 1988, showed no sign of fission in April 1999. In August 1999, the group had split in two, with the same number of mature females in each new group. For the most part, mothers and their offspring joined the same groups. Dominance relations and association patterns established during the previous year among adult females did not strongly affect new group membership. The difference in female reproductive state between the two branch groups was a prominent characteristic. The -male of the original group visited both groups at the first stage of group fission, even though otherwise the compositions of the new groups were stable. After the division, six adult males from outside the original group immigrated exclusively into the group that did not contain the -male of the original group. Severe intergroup encounters occurred between the two groups. We discuss the process of the fission and the resultant pattern in relation to the egalitarian dominance style among females, lack of seasonality in reproduction, and resemblance to one-male type social organization.     

The Organization of Collective Group Movements in Wild Barbary Macaques (Macaca sylvanus): Social Structure Drives Processes of Group Coordination in Macaques

Social animals have to coordinate activities and collective movements to benefit from the advantages of group living. Animals in large groups maintain cohesion by self-organization processes whereas in smaller groups consensus decisions can be reached. Where consensus decisions are relevant leadership may emerge. Variation in the organization of collective movements has been linked to variation in female social tolerance among macaque species ranging from despotic to egalitarian. Here we investigated the processes underlying group movements in a wild macaque species characterized by a degree of social tolerance intermediate to previously studied congeneric species. We focused on processes before, during and after the departure of the first individual. To this end, we observed one group of wild Barbary macaques (Macaca sylvanus) in the Middle Atlas, Morocco using all-occurrence behaviour sampling of 199 collective movements. We found that initiators of a collective movement usually chose the direction in which more individuals displayed pre-departure behavior. Dominant individuals contributed to group movements more than subordinates, especially juveniles, measured as frequencies of successful initiations and pre-departure behaviour. Joining was determined by affiliative relationships and the number of individuals that already joined the movement (mimetism). Thus, in our study group partially shared consensus decisions mediated by selective mimetism seemed to be prevalent, overall supporting the suggestion that a species’ social style affects the organization of group movements. As only the most tolerant species show equally shared consensus decisions whereas in others the decision is partially shared with a bias to dominant individuals the type of consensus decisions seems to follow a stepwise relation. Joining order may also follow a stepwise, however opposite, relationship, because dominance only determined joining in highly despotic, but not in intermediate and tolerant species.