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 Assessment of Gastrointestinal Parasites in Two Wild Groups of Endangered Moor Macaques (Macaca maura) from Sulawesi

International Journal of Primatology - Information on parasite biodiversity and abundance can improve our understanding of parasitic infections on endangered wildlife, as parasites can affect host...     

Effect of Anthropogenic Activities on the Population of Moor Macaques (Macaca maura) in South Sulawesi,Indonesia

International Journal of Primatology - Forest loss due to anthropogenic activities is one of the main causes of plant and animal species decline. Studying the species’ population status...     

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.     

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.     

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.     

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.     

野生雌性黄山短尾猴产后摄食胎盘新发现

摄食胎盘行为是哺乳动物分娩过程的组成部分之一,具有重要的生态学和生物学意义。野生哺乳动物的分娩大多发生在夜间,受光线和视线等观察条件的限制,很难直接观察到野生动物的分娩行为。2015年4月9日8点59分,我们在安徽黄山观察野生短尾猴 (Macaca thibetana) 鱼鳞坑A1群时,发现初次生产的雌性个体“头华玉 (THY)”分娩后摄食胎盘的行为,随即采用目标动物取样法记录了该个体摄食胎盘的行为过程。THY摄食胎盘包括舔舐、撕成片状、刮食和吞咽等过程,历时2小时29分钟,其中摄食胎盘有效时间长于63min,进程缓慢。与其他相关研究比较,初次生产的雌性短尾猴头华玉 (THY) 摄食胎盘具有花费时间长、社会交往多、警惕性高的特点。本研究是本课题组在安徽黄山研究短尾猴30年首次直接观察到产后摄食胎盘行为,为了解短尾猴的繁殖行为和非人灵长类的繁殖特性提供了难得基础资料。     

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.     

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.     

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.     

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.     

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.     

Extraintestinal Campylobacteriosis in Rhesus Macaques (Macaca mulatta)

Two cases of clinical disease associated with extraintestinal Campylobacter infection were recently encountered in rhesus macaques (Macaca mulatta). The first case was that of a 3-y-old, male, rhesus macaque experimentally infected with SIV, who presented with abdominal pain and a midabdominal mass and was euthanized. Pathology findings included an abscess within the median liver lobe, fibrinopurulent peritonitis, and intestinal serositis with isolation of Campylobacter fetus from the blood, liver, and the hepatic abscess. The second case was that of a 1-mo-old, female, rhesus macaque who died with no apparent history of illness. Gross pathology findings included thin body condition and diarrheic staining of the perineum; histologically, acute multifocal hepatitis with intralesional bacteria was noted. Campylobacter coli was isolated from the liver and colon. Extraintestinal Campylobacter infection is uncommon in humans, usually occurring in immunocompromised subjects and most commonly manifesting as bacteremia. Extraintestinal Campylobacter infections in animals are rare but have been associated with bacteremia and cholecystitis. The macaques presented here were either immunocompromised due to SIV infection (case 1) or more vulnerable due to young age (case 2). These factors likely contributed to the extraintestinal spread of Campylobacter.Campylobacter spp. are curved or spiral, gram-negative, microaerobic, typically motile bacteria with a single flagellum at one or both ends of the cell.²⁵ Campylobacter is one of the most common bacterial causes of gastroenteritis in humans worldwide.³ The Centers for Disease Control and Prevention estimate it to affect more than 1.3 million people in the United States each year.¹¹ Campylobacter spp. colonize the intestinal tract of primates, other mammals, birds, reptiles, and shellfish, but infection is not always associated with clinical signs of disease.^2,23 Contaminated or undercooked poultry represents the largest potential source of human infection.²² Campylobacteriosis is a zoonosis, and other significant sources of human infection include livestock, wildlife, pets, and contaminated water.²² The species most commonly isolated from humans and nonhuman primates are C. jejuni and C. coli; other species like C. fetus are less commonly found.^2,4,9,23 Extraintestinal campylobacteriosis in humans usually occurs in immunocompromised or elderly persons with underlying medical problems and most commonly manifests as bacteremia.²³ There have been a few reports of extraintestinal Campylobacter infections in animals, including bacteremia and cholecystitis in 2 dogs.^17,30     

Maternal Anxiety in Rhesus Macaques (Macaca mulatta)

Visual monitoring and scratching were used as behavioral indicators of maternal and social anxiety in small captive groups of rhesus macaques. Young infants were especially at risk from other group members during the first weeks of locomotion away from their mothers. Mothers received aggression from other individuals irrespective of their infants' presence or absence. The rate at which mothers scratched themselves increased significantly when their infants moved away from them and when the infants approached or were approached by individuals who frequently harassed them. The rate of maternal scratching and the rate of glancing at the infant and at other individuals when the infant was away decreased as infants grew older and became less vulnerable to harassment. In contrast, the rate of maternal scratching and visual monitoring of other individuals when the infant was in contact remained stable across the first 12 wk of lactation. The rate of maternal scratching increased when the mother-infant pair was in spatial proximity to the adult male or higher ranking adult females. Although visual monitoring and scratching showed a similar sensitivity to social variables, it is speculated that they might reflect different components of anxiety, namely, anticipation of danger and uncertainty due to motivational conflict. The results of this investigation indicate that a macaque mother's emotional reactivity to a perceived danger for herself and her infant can be measured quite accurately using the rates of visual monitoring and scratching and that the latter represent reliable tools to investigate the emotional correlates of maternal behavior in nonhuman primates.     

Representation of Faces in Longtailed Macaques (Macaca fascicularis)

The experiments described in this study were intended to increase our knowledge about social cognition in primates. Longtailed macaques (Macaca fascicularis) had to discriminate facial drawings of different emotional expressions. A new experimental approach was used. During the experimental sessions social interactions within the group were permitted, but the learning behaviour of individual monkeys was analysed. The procedure consisted of a simultaneous discrimination between four visual patterns under continuous reinforcement. It has implications not only for simple tasks of stimulus discrimination but also for complex problems of internal representations and visual communication. The monkeys learned quickly to discriminate faces of different emotional expressions. This discrimination ability was completely invariant with variations of colour, brightness, size, and rotation. Rotated and inverted faces were recognized perfectly. A preference test for particular features resulted in a graded estimation of particular facial components. Most important for face recognition was the outline, followed by the eye region and the mouth. An asymmetry in recognition of the left and right halves of the face was found. Further tests involving jumbled faces indicated that not only the presence of distinct facial cues but the specific relation of facial features is essential in recognizing faces. The experiment generally confirms that causal mechanisms of social cognition in non-human primates can be studied experimentally. The behavioural results are highly consistent with findings from neurophysiology and research with human subjects.     

Tail-Length Evolution in Fascicularis-Group Macaques (Cercopithecidae: Macaca)

In the four species of macaques that constitute the fascicularis-group, relative tail length generally decreases with increasing latitude, in accord with Allen's Rule. Although this generalization applies to Macaca mulatta in the northern part of its range—north of ca. 26°N, it does not apply south of ca. 26°N, where the tail is anomalously short in Macaca mulatta. This suggests that the anomalously short-tailed population of Macaca mulatta did not originate within its present latitudinal range, but instead dispersed there from farther north. The anomalously short-tailed population apparently replaced a now-extinct longer-tailed population, from which founders of insular Macaca cyclopis previously had been derived. Southward dispersal of the anomalously short-tailed population of Macaca mulatta, and correlated extinction of the longer-tailed population that it apparently replaced, may have been induced by a major glacial advance.     

Sexual Behaviour of Sumatran Long-tailed Macaques (Macaca fascicularis)

The sexual behaviour of wild long-tailed macaques (Macaca fascicularis) was studied in the Gunung Leuser National Park, Sumatra, Indonesia. All females showed some swelling of the sexual skin, but the frequency and maximum size of the swelling decreased with age. The frequency of copulations and consortships for a given female increased with increasing degree of swelling or coloration. No regular cycles could be found in the occurrence of swellings, copulations and consortships. Periods for which a female had consortships tended to be long (up to 5–6 weeks on end). These two results suggest that in the wild the predictability of the moment of ovulation is very low. The consortships were not exclusive: both the male and the female occasionally copulated with others. All females had many different male partners and, as ovulation signalling was not clear, none of these males could have any certainty about paternity of a female's offspring. Yet, the highest-ranking males probably had the best chances to father children because they were more often involved in sexual interaction (both copulations and consortships), especially around the estimated date of conception. This does not hold for the nulliparous females who were virtually ignored by the higher-ranking males. Consortships were occasionally actively maintained by the female, for whom a direct advantage of consorting might be an increased safety against conspecifics and predators. One advantage of mating with many different males might be a reduced risk of infanticide.