Group Composition and Monandry in Grizzled Langurs, Presbytis comata, on Java.

Grizzled langurs, Presbytis comata, a largely sexually monomorphic species, are reported to occur in populations where either the majority of groups comprise 1 adult male with 1 adult female, or where groups comprise 1 adult male with multiple females. As such, they may have a monandrous mating system. I investigated whether 1-male/1-female groups indeed form a significant part of the species' social system, and whether habitat variation (forest fragment size, distance to the forest edge, altitude) affects social organization. I found the species from sea level to 2,565 m above sea level in groups from 1 to 13 individuals. I recorded mostly 1-male/multifemale groups with offspring or, alternatively, all-male groups. Two out of 55 groups comprised 1-male/1-female groups with offspring. Group size was negatively correlated with altitude and forest fragment size, and positively correlated with increasing distance from the forest edge. Altitudinal variation in group sizes was driven mainly by fewer adult females being present in groups at higher elevations; the number of adult males (almost invariably 1), subadults, juveniles, and infants, as well as the infant/adult female ratio, showed little altitudinal variation. One-male/1-female groups have been recorded repeatedly over a 25-year period in a high-altitude population on Mt. Patuha, West Java, but even here, on average, three fifths of the groups comprise 1 adult male with multiple females. At high-altitude sites, P. comata may indeed have a monandrous mating system, but at lower elevations it seems similar to that of other Presbytis langurs.

Daytime behavior of Pteropus vampyrus in a natural habitat: the driver of viral transmission.

Flying foxes, the genus Pteropus, are considered viral reservoirs. Their colonial nature and long flight capability enhance their ability to spread viruses quickly. To understand how the viral transmission occurs between flying foxes and other animals, we investigated daytime behavior of the large flying fox (Pteropus vampyrus) in the Leuweung Sancang conservation area, Indonesia, by using instantaneous scan sampling and all-occurrence focal sampling. The data were obtained from 0700 to 1700 hr, during May 11-25, 2016. Almost half of the flying foxes (46.9 ± 10.6% of all recorded bats) were awake and showed various levels of activity during daytime. The potential behaviors driving disease transmission, such as self-grooming, mating/courtship and aggression, peaked in the early morning. Males were more active and spent more time on sexual activities than females. There was no significant difference in time spent for negative social behaviors between sexes. Positive social behaviors, especially maternal cares, were performed only by females. Sexual activities and negative/positive social behaviors enable fluid exchange between bats and thus facilitate intraspecies transmission. Conflicts for living space between the flying foxes and the ebony leaf monkey (Trachypithecus auratus) were observed, and this caused daily roosting shifts of flying foxes. The ecological interactions between bats and other wildlife increase the risk of interspecies infection. This study provides the details of the flying fox's behavior and its interaction with other wildlife in South-East Asia that may help explain how pathogen spillover occurs in the wild.

Social organization of Shortridge's capped langur (Trachypithecus shortridgei) at the Dulongjiang Valley in Yunnan, China.

Non-human primates often live in socially stable groups characterized by bonded relationships among individuals. Social organization can be used to evaluate living conditions and expansion potential. Bisexual group size, ratio of males to females and group composition are essential elements determining the type of social organization. Although the first report on Shortridge's capped langurs (Trachypithecus shortridgei) was in the 1970s, until now, the species only inhabits forests of the Dulongjiang valley in northwest Yunnan, China, with c. 250-370 individuals in 19 populations. To understand its social organization, we collected data from five groups of Shortridge's langurs at Silaluo in the Dulongjiang valley during August 2012-October 2013. Family groups consist of one adult male, 2-3 adult females and up to five young. Group size averaged 8 (7-9) individuals. The ratio of adult males to females (M/F) was 1:2.9, infants to adult females was (I/F) 1:2.2; and ratio of adults to immatures was 1:1.2, indicating the potential of a population increasing. Birth season was during March-July and the inter-birth interval was two years.

Maternal kin bias in affiliative behavior among wild adult female blue monkeys.

Kin-biased cooperative and affiliative behavior is widespread in social mammals and is expected to increase fitness. However, despite evolutionary benefits of cooperating with relatives, demographic circumstances may influence the strength of kin bias. We studied the relationship between maternal kinship and affiliative behavior among 78 wild adult female blue monkeys (Cercopithecus mitis) from 8 groups monitored for 1-5 years. We compared behavior and kinship matrices, controlling for rank differences. Using multivariate models, we examined effects of demographic variables on the extent to which females groomed disproportionately with close adult female kin. Female blue monkeys, like other cercopithecine primates, generally preferred closer maternal kin for grooming and spatial association, although there was also substantial variation. Kin bias was weakest for association (at 7 m) while feeding, intermediate for closer (1 m) association while resting, and most intense for grooming. Grooming kin bias was stronger when a female had more very close relatives (either her mother or daughters), when her group contained more adult females, when she groomed with a lower percentage of group-mates, and when she had fewer total kin. Dominance rank did not predict variation in kin bias. Females generally groomed with all kin, but in larger groups they increased the number of unrelated grooming partners and total grooming time. The increased kin bias intensity in larger groups resulted from the addition of unrelated partners with whom grooming occurred less often than with kin, rather than from time constraints that drove females to select kin more strongly. In natural-sized groups, it may be common that females groom with all their adult female kin, which are present in limited numbers. The addition of grooming partners in larger groups may benefit female blue monkeys who rely on collective action in territorial defense; group-wide cooperation may thus influence grooming decisions in this species.

Social behavior, foraging strategies, and fecal glucocorticoids in female blue monkeys (Cercopithecus mitis): potential fitness benefits of high rank in a forest guenon.

Socioecological theory predicts that aggressive feeding competition is associated with linear dominance hierarchies and reproductive advantages for high-ranking females. Female blue monkeys contest fruits and have a linear dominance hierarchy, yet previous research has shown no evidence that high-ranking females benefit from greater feeding success or fertility. Here, we assess whether individuals differ in fecal glucocorticoid (fGC) excretion and examine proximate determinants of such differences to infer potential fitness correlates of rank, using data collected from two study groups in the Kakamega Forest, Kenya. We found that higher ranking females had preferential access to fruits in both groups, although the behavioral mechanisms leading to this effect varied between groups. Despite a consistent rank difference in feeding on fruits, an overall rank effect on fGCs emerged in only one group; females of this group spent comparatively more time feeding on fruits, fruits accounted for a greater proportion of the diet, and females engaged in more frequent food-related agonism. In addition, more females in this group were lactating during a period of low fruit availability, when rank effects on fGCs were particularly strong. Regardless of fruit availability, among lactating females of both groups higher rank was associated with lower fGC levels, indicating lower energetic stress in higher ranking females when energy demands were particularly high. Individual rates of agonism, a potential psychological stressor, were unrelated to fGCs at all times. After we accounted for rates of agonism and feeding on fruits, females of one group who groomed others more had lower fGCs, suggesting that variable social coping behavior can contribute to fGC variation in some groups. This study provides the first empirical evidence that high-ranking female blue monkeys may obtain fitness benefits from their social status, by gaining priority of access to fruits during critical times in the reproductive cycle.

Optimal foraging on the roof of the world: Himalayan langurs and the classical prey model.

Optimal foraging theory has only been sporadically applied to nonhuman primates. The classical prey model, modified for patch choice, predicts a sliding "profitability threshold" for dropping patch types from the diet, preference for profitable foods, dietary niche breadth reduction as encounter rates increase, and that exploitation of a patch type is unrelated to its own abundance. We present results from a 1-year study testing these predictions with Himalayan langurs (Semnopithecus entellus) at Langtang National Park, Nepal. Behavioral data included continuous recording of feeding bouts and between-patch travel times. Encounter rates were estimated for 55 food types, which were analyzed for crude protein, lipid, free simple sugar, and fibers. Patch types were entered into the prey model algorithm for eight seasonal time periods and differing age-sex classes and nutritional currencies. Although the model consistently underestimated diet breadth, the majority of nonpredicted patch types represented rare foods. Profitability was positively related to annual/seasonal dietary contribution by organic matter estimates, whereas time estimates provided weaker relationships. Patch types utilized did not decrease with increasing encounter rates involving profitable foods, although low-ranking foods available year-round were taken predominantly when high-ranking foods were scarce. High-ranking foods were taken in close relation to encounter rates, while low-ranking foods were not. The utilization of an energetic currency generally resulted in closest conformation to model predictions, and it performed best when assumptions were most closely approximated. These results suggest that even simple models from foraging theory can provide a useful framework for the study of primate feeding behavior.

Revisiting play elements and self-handicapping in play: a comparative ethogram of five Old World monkey species.

Play behavior has been viewed as a mixture of elements drawn from "serious" behavior, interspersed by ritualized play signals. Two other types of play behaviors have been overlooked: patterns that are dissimilar from any serious behavior and patterns with self-handicapping character, that is, those that put the animal into unnecessary disadvantageous positions or situations. Here the authors show that these 2 types of patterns can constitute a major part of play repertoire. From our own videorecordings and observations, we constructed play ethograms of 5 monkey species (Semnopithecus entellus, Erythrocebus patas, Chlorocebus pygerythrus, Cercopithecus neglectus, and Cercopithecus diana). The authors evaluated the self-handicapping character of each pattern and in Hanuman langurs also the (dis)similarity to serious behavior. Of the 74 patterns in the 5 species, 33 (45%) were judged to have a self-handicapping character. Of 48 patterns observed in langurs, 16 (33%) were totally dissimilar to any serious langur behavior known to us. The authors discuss the possibility that the different types of play elements may have different functions in play.

Personality in free-ranging Hanuman langur (Semnopithecus entellus) males: subjective ratings and recorded behavior.

The authors obtained behavioral observations and personality ratings for 27 free-ranging Hanuman langur males. Subjects were rated using a questionnaire based on the human Five-Factor Model (FFM). Behavioral observations were taken over 5 months using an ethogram that included 50 behaviors. Principal Component Analysis (PCA) of ratings revealed Agreeableness_(R), Confidence_(R), and Extraversion_(R) components. Each personality dimension was associated with a unique set of observed behaviors. PCA of 36 behavioral indices revealed Dominance_(B), Involvement_(B), and Activity_(B) components. Bivariate correlations showed that Agreeableness_(R) was negatively correlated with Dominance_(B); Confidence_(R) was positively correlated with Dominance_(B) and Involvement_(B) but negatively correlated with Activity_(B); and Extraversion_(R) was positively correlated with Activity_(B). Dominance rank was positively correlated with Confidence_(R) and Dominance_(B) but negatively correlated with Agreeableness_(R) and Activity_(B). These results highlight the comparability of behavioral coding and personality ratings and suggest that some aspects of personality structure were present in the common ancestor of Old World monkeys.

Reproductive and behavioral characteristics of aging in female Asian colobines.

Data from four Asian colobine populations, wild (Ramnagar) and provisioned (Jodhpur) Hanuman langurs, wild Phayre's leaf monkeys (Phu Khieo Wildlife Sanctuary), and captive silvered langurs (Wildlife Conservation Society's Bronx Zoo) were analyzed with respect to reproductive and behavioral trends of aging. All but one female (from a total of seven) became menopausal 1.8 to 5+ years prior to death with a lag time between last parturition and death ranging from 3.0 to 9.0 years (n=8). Hormonal analysis revealed constantly low and acyclic levels of immunoreactive pregnanediol-3-glucuronide (iPdG) in one old, wild female supporting the notion of true menopause. Nonsexual behavior was analyzed based on quantitative data collected for 6 old and 26 younger, adult females simultaneously (1,378.5 h). No support was found for social disengagement, but old females were more inactive and spent less time feeding. Altogether the data support earlier claims of menopause and extended postreproductive life spans in colobine monkeys. Future behavioral studies should aim at longitudinal assessments of behavioral changes and incorporate energetic data as well as testing of social continuity and selectivity.

Ranging behavior of the François' langur (Trachypithecus francoisi) in the Fusui Nature Reserve, China.

Data on activity budgets and ranging patterns were collected from March to December 2001 for one group of François' langurs (Trachypithecus francoisi) inhabiting a forested part of the Fusui Nature Reserve, Guangxi province, China. Our results indicate that the total size of the home range of the study group during the study period was 19 ha. The majority of their activities (52%) occurred within a small area, 22%, of their home range, and was concentrated in or near quadrats containing their sleeping sites, which may reduce the time and energetic cost of travel. The extent of the ranging behavior varied between months, with the smallest, 7 ha, recorded in July and the largest, 13.5 ha, in November. There was no significant difference between seasons. The monthly mean daily path lengths varied from 341 to 577 m. The daily path lengths showed significant seasonal changes: the path lengths were longer during the dry season than in the rainy season, which may be related to the scarcity of preferred food resources during the dry season.

Considerations in the selection and conditioning of Old World monkeys for laboratory research: animals from domestic sources.

Nonhuman primates from domestic sources constitute an important resource for the research community. The life history of the Old World monkey species that comprise the bulk of this resource is described, and issues that colony managers and researchers alike should consider regarding animal selection (e.g., species, age, sex, rearing history, temperament, genotype, viral status, geographic origin) are discussed. Preparation of domestically bred animals for research usually involves some combination of social separation, relocation, resocialization, alterations in physical space, photoperiod, and diet, as well as exposure to novel environments. The research literature that has focused on these issues is reviewed, and authors suggest that once animals have been assigned to their project housing situation, a period ranging up to 3 mo (depending on the magnitude of the change in housing) might be warranted before an experimental protocol should begin. Attention to issues of animal selection and conditioning by both researchers and colony managers can lead to the shared goal of high-quality research that utilizes the minimal number of animals.

Male monkeys remember which group members have given alarm calls.

Primates give alarm calls in response to the presence of predators. In some species, such as the Thomas langur (Presbytis thomasi), males only emit alarm calls if there is an audience. An unanswered question is whether the audience's behaviour influences how long the male will continue his alarm calling. We tested three hypotheses that might explain the alarm calling duration of male Thomas langurs: the fatigue, group size and group member behaviour hypotheses. Fatigue and group size did not influence male alarm calling duration. We found that males only ceased calling shortly after all individuals in his group had given at least one alarm call. This shows that males keep track of and thus remember which group members have called.

Language evolution: the origin of meaning in primates.

Research on alarm calls has yielded rare glimpses into the minds of our closest relatives. A new study suggests that primates monitor the effect alarm calls have on others.

Artificial weaning of Old World monkeys: benefits and costs.

Permanent mother-infant separation prior to natural weaning is a common hus-bandry practice in monkey breeding colonies. In the United States, all eight Re-gional Primate Research Centers have such colonies. Under undisturbed conditions, Old World monkey mothers wean their infants at the age of about 1 year (Hall & DeVore, 1965; Poirier, 1970; Roonwal & Mohnot, 1977; Southwick, Beg, & Siddiqi, 1965). Natural weaning is a gradual process. It implies that the mother, over a period of several weeks or months, more and more consistently discourages her infant to suck on her breasts. Once the mother stops nursing the infant for good, the affectionate bond between the two is not broken (Altmann, Altmann, Hausfater, & McCuskey, 1977; Lindburg, 1971; Poirier, 1970; Roonwal & Mohnot, 1977). The young usually remains in the ma-ternal group at least until prepuberty. Under confinement conditions, artificial weaning is an abrupt occurrence that takes place several months prior to the biologically normal age of weaning. It im-plies that the still-nursed infant is taken away from the mother and subsequently reared alone or with other artificially weaned infants.

Differential energy budget and monopolization potential of harem holders and bachelors in Hanuman langurs (Semnopithecus entellus): preliminary results.

The demographic structure in the Hanuman langur (Semnopithecus entellus) population of Jodhpur is extreme, in that some single males monopolize harems with, on average, 25 adult females. It has been proposed that extratroop males, which live in all-male bands, inhabit low-quality habitats and suffer from reduced food provisioning and longer daily travel distances. To compare the resulting energetic consequences for harem holders and bachelors, I estimated their gross energy intake and daily energetic expenditures. This analysis revealed no clear-cut differences between the two classes of males in time spent feeding on provisioned food, daily path length, gross energy intake, and energy expenditure. Due to the small sample size and other limitations of the study design, the hypothesis under investigation can not be evaluated conclusively. The preliminary results suggest, however, that energy budgets of harem holders and bachelors do not differ markedly. The importance of direct ecological pressures to males for our understanding of variation in group composition is highlighted.

DNA analyses support the hypothesis that infanticide is adaptive in langur monkeys.

Although the killing of dependent infants by adult males is a widespread phenomenon among primates, its causes and consequences still remain hotly debated. According to the sexual selection hypothesis, infanticidal males will gain a reproductive advantage provided that only unrelated infants are killed and that the males increase their chances of siring the next infants. Alternatively, the social pathology hypothesis interprets infanticide as a result of crowded living conditions and, thus, as not providing any advantage. Based on DNA analyses of wild Hanuman langurs (Presbytis entellus) we present the first evidence that male attackers were not related to their infant victims. Furthermore, in all cases the presumed killers were the likely fathers of the subsequent infants. Our data, therefore, strongly support the sexual selection hypothesis interpreting infanticide as an evolved, adaptive male reproductive tactic.

Female dispersal, social organization, and infanticide in langurs: are they linked to human disturbance?

Female dispersal in gregarious animals can involve the desertion of a site, desertion of a social group, or both. Group desertion may be related to inbreeding avoidance. Group fidelity may result from cooperation among females in a group. Site fidelity will be more likely when food can be monopolized and when the population density is close to habitat saturation. The degree of habitat saturation was approximated with a measure of human disturbance. The influence of these various factors on the incidence of female dispersal was investigated for langur populations using data from the literature. The results suggest that female dispersal in langurs involved site desertion, not group desertion. The incidence of female dispersal may affect the social organization of langurs. I propose that when females do not disperse, male takeovers prevail, whereas in populations where female dispersal regularly occurs bisexual groups are disbanded or new groups are formed, a process I call female split-merger. Male takeover is thought to occur when site fidelity is high, female split-merger when site fidelity is low. These processes were indeed found to occur in these circumstances. The dispersal of females might prevent infanticide, whereas male takeover might promote it. Indeed, in studies with male takeover, more infants fell victim to infanticide than in studies with female split-merger. Therefore, female dispersal in langurs is an effective female counterstrategy to infanticide. The factor that had the most profound effect on female dispersal, social organization, and infanticide was habitat saturation. Habitat saturation was measured as the degree of human disturbance, and its influence on the behavior of langurs is probably of relatively recent date. This may lead to an evolutionary transient situation and may explain the discrepancy between current socioecological theories and the behavior of langurs in populations lacking female dispersal.

Lack of hand preference in wild Hanuman langurs (Presbytis entellus).

Although there is a vast literature on laterality of hand-use in nonhuman primates, the Colobinae have been notably overlooked. Ten manual activities of differing complexity were studied in five male and five female adult Hanuman langurs (Presbytis entellus) from a well habituated, wild population at Ramnagar, in southern Nepal. The activities recorded were carry, eat, hit, hold, idle, manipulate, reach, retrieve, self-groom and social groom. This study aimed to examine handedness across tasks and across subjects in a natural population. The overall result was a lack of preference for subjects and patterns. Only in the eating activity did four individuals show significant hand preference, though they were not unidirectional. Eat seemed to be loosely associated with hold due to the requirements of the strata which the monkeys utilize. These results suggest that hand use is unlateralized in P. entellus. Those individuals exhibiting some hand preferences can be viewed as statistical exceptions or perhaps subject to experiential differences. The results are discussed in terms of their evolutionary significance and methodological implications.

Determinants of female dispersal in Thomas langurs.

Female dispersal occurs in a number of primate species. It may be related to: avoidance of inbreeding, reduction in food competition, reduction of predation risk, or avoidance of infanticide in combination with mate choice. Female dispersal was studied for a 5-year period in a wild population of Thomas langurs (Presbytis thomasi) that lived in one-male multi-female groups. Juvenile and adult individuals of both sexes were seen to disperse. Females appeared to transfer unhindered between groups, mostly from a larger group to a recently formed smaller one. They transferred without their infants and when not pregnant, and seemed to transfer preferentially during periods when extra-group males were harassing their group. During these inter-group encounters extra-group males seemed to try to commit infanticide. Thus, the timing of female transfer was probably closely linked to infanticide avoidance. Moreover, females seemed to transfer when the resident male of their group was no longer a good protector. The observations in the present study suggest that females transferred to reduce the risk of infanticide. Female dispersal may have another ultimate advantage as well, namely inbreeding avoidance. Due to the dispersal of both females and males the social organization of Thomas langurs was rather fluid. New groups were formed when females joined a male; male takeovers were not observed. Bisexual groups had only a limited life span, because all adult females of a bisexual group could emigrate. This pattern of unhindered female dispersal affects male reproductive strategies, and in particular it might lead to infanticidal behavior during inter-group encounters.

What a maleless group can tell us about the constraints on female transfer in Thomas's langurs (Presbytis thomasi).

During a long-term study of wild Thomas's langurs (Presbytis thomasi), the adult male of one of the bisexual study groups, group M, suddenly disappeared. Just after the adult male's disappearance, the females of group M actively avoided other groups and sometimes formed subgroups. Infants were attacked by extra-group males and 1 infant disappeared. After about 2 months, the females initiated affiliative interactions with males of neighbouring groups. Aggressive interactions between females of group M and females of other groups were also observed. Females of group M did not leave their home range in spite of efforts by adult males to lead them away. After about 4.5 months, a former all-male band member joined group M. The coincidences of this case suggest that increased infanticide risk, increased food competition, loss of knowledge of the home range and loss of established social relationships could be important constraints on female transfer. A comparison with 5 other studies of 1-male groups in which the adult male disappeared showed that proximate factors, such as the presence of infants, the size of neighbouring groups and the presence of extra-group males, influence female decisions.