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.     

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.     

Lack of Evidence for Energetic Costs of Mate-Guarding in Wild Male Assamese Macaques (Macaca assamensis)

Mate-guarding is a widespread and efficient male strategy for increasing paternity success. The inability to guard entire female receptive phases or complete lack of mate-guarding has been explained by energetic constraints posed on males. The energetic costs per unit time a male can afford to suffer are thought to be lowest in year-round breeding species in marginal habitats and highest in seasonally breeding species in rich habitats. Here we test the prediction that mate-guarding is energetically costly in seasonal breeders in marginal habitats. We observed all males in one group of wild Assamese macaques (Macaca assamensis) for two 4-mo mating seasons and recorded activity and travel paths via focal animal sampling, physical condition via visual inspection, and collected feces for analysis of glucocorticoid levels. Generalized linear mixed model (GLMM) analyses did not reveal an effect of mate-guarding on time spent feeding or moving or on distance traveled, travel speed, directedness of travel, or glucocorticoid levels. This lack of mate-guarding costs was consistent with the lack of a relationship between individual time spent mate-guarding and change in physical condition over the mating season. Within the limitations of our study the results do not support the idea that seasonally breeding males in marginal habitats face energetic costs of mate-guarding. With others we suggest instead that though these costs may be found in species where strength, size, and mass predict rank, mating, and reproductive success, males may not engage in costly mate-guarding in species such as Assamese macaques where also smaller, weaker males may attain high social status via political coalitions or other routes alternative to direct contest over guarded females.     

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 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.     

Brief communication: Fecal androgen excretion and fetal sex effects during gestation in wild Assamese macaques (Macaca assamensis)

In placental mammals, pregnancy usually is associated with an increase in maternal androgens, which may significantly impact fetal growth and differentiation, and affect postnatal development and behavior. Owing to their slow life histories and challenging social conditions, determination of maternal androgens and potential interference effects of fetal androgen production are of particular interest in wild primates. However, androgen production has been rarely investigated in wild female primates, and studies on maternal androgens during gestation in particular often do not span the entire pregnancy. Here, we characterize fecal androgen production throughout gestation in wild Assamese macaques (Macaca assamensis) using noninvasive hormone analysis and, furthermore, examine fetal sex effects on maternal androgen excretion. A total of 207 fecal samples were analyzed from seven females for concentrations of immunoreactive epiandrosterone (iEA). Fecal iEA concentrations, as predicted based on cercopithecine blood-serum patterns, increased during early gestation and were significantly higher during the first trimester compared with preconception concentrations and those recorded during later stages of gestation. Further, during the third trimester, male-carrying mothers showed significantly higher iEA concentrations compared with female-carrying mothers. This first characterization of fecal androgen excretion during gestation in Assamese macaques indicates both a maternal and fetal effect on androgen production. Although our sample size is small, our results, nevertheless, provide the basis for assessing potential influences of maternal androgens on postnatal offspring development and behavior.     

Social bonds enhance reproductive success in male macaques

For animals living in mixed-sex social groups, females who form strong social bonds with other females live longer and have higher offspring survival [1-3]. These bonds are highly nepotistic, but sometimes strong bonds may also occur between unrelated females if kin are rare [2, 3] and even among postdispersal unrelated females in chimpanzees and horses [4, 5]. Because of fundamental differences between the resources that limit reproductive success in females (food and safety) and males (fertilizations), it has been predicted that bonding among males should be rare and found only for kin and among philopatric males [6] like chimpanzees [7-9]. We studied social bonds among dispersing male Assamese macaques (Macaca assamensis) to see whether males in multimale groups form differentiated social bonds and whether and how males derive fitness benefits from close bonds. We found that strong bonds were linked to coalition formation, which in turn predicted future social dominance, which influenced paternity success. The strength of males' social bonds was directly linked to the number of offspring they sired. Our results show that differentiated social relationships exert an important influence on the breeding success of both sexes that transcends contrasts in relatedness.     

What Hanuman langur males know about female reproductive status

In species with a high risk of infanticide, a conflict of interest exists between the sexes over the amount of paternity information that is available to males. While females are expected to keep males unaware of their reproductive status in order to confuse paternity, selection should favor those male traits that enhance the males' assessment of female status and consequently of paternity probability. In Hanuman langurs (Semnopithecus entellus), a species that is extremely vulnerable to infanticide, females have been shown to successfully conceal the exact timing of ovulation from males--perhaps because they exhibit no sexual swelling and mate during all reproductive phases, including gestation. Nevertheless, it remains unclear whether males have hitherto unrecognized information about females' reproductive condition on a broader level that could still enhance male reproductive success. We investigated male assessment of female reproductive states in a population of wild Hanuman langurs as indicated by changes in male behavior, such as rates of copulations, anogenital inspections, and consortships, in relation to different female receptive periods (pregnant, fertile-nonconceptional, and conceptional). Our data indicate that males were able to discern qualitatively distinct reproductive states. Males were more interested in fertile than pregnant females, as indicated by higher copulation rates. Based on consortships, males distinguished fertile from nonfertile phases, as well as fertile, nonconceptional receptive periods from conceptional ones. Hanuman langur males are thus not as unaware of female reproductive condition as previously thought, supporting the idea of an ongoing battle of the sexes over paternity information. However, granting some knowledge while at the same time concealing the exact day of ovulation may also reflect a pure female strategy of balancing paternity concentration with paternity confusion, which is the most likely strategy in this system with high infanticide risk and male defense of infants.     

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.