Differential responses of non-human primates to seasonal temperature fluctuations.

Non-human primates (NHPs) can adapt to conditions outside of their natural habitat and climatic ranges but this can be influenced by inherent evolutionary traits or plasticity of species that evolved in diverse environmental conditions. In this study, we investigated how five species of NHPs that have natural distributions across a range of climatic conditions responded to seasonal temperature changes in a captive environment. The activity levels of NHPs were affected by temperature changes over the season, where activity levels were generally reduced at the lower and higher temperature ranges. Species that are naturally found within narrower and warmer climatic ranges, compared to those found in colder environments with wider fluctuations in temperature, showed more marked changes in activity levels in response to temperature changes. In lower temperature conditions, three out of five species showed significantly lower activity levels; whereas in higher temperature conditions, the activity levels of all species did not significantly decrease. The frequency of thermoregulation behaviours was higher, and use of artificial thermoregulatory sources lower, for species that did not substantially adjust their activity levels in different temperature conditions. Our results suggest that NHPs largely retained the evolutionary traits related to thermoregulation, according to the different ambient conditions they evolved in and may have low behavioural plasticity in adapting to conditions outside of their natural ranges. These results provide insights for improving conservation and captive management and may have implications for understanding NHP resilience to the increasing impact of global climate change.

Sleeping site and tree selection by Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in Baihe Nature Reserve, Sichuan, China.

For non-human primates to optimize their survival chances, sleeping site selection is crucial as they spend much of their time sleeping. We studied sleeping site and tree selection by a group of wild Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the temperate forests of Baihe Nature Reserve, Sichuan, China, to assess if certain site and tree characteristics were selected. We identified a total of 39 sleeping sites and 111 sleeping trees over a period of 1 year. We compared nine sleeping site and six sleeping tree variables related to the environment, habitat, and vegetation structure. We found that certain characteristics of sleeping sites and sleeping trees predicted their selection by R. roxellana. On a larger spatial scale, sleeping sites were selected based mainly on four factors: canopy height, slope direction, slope gradient, and vegetation type. They also selected sites with trees that were taller and larger, had larger crown diameters and higher bole branches. On a smaller spatial scale, they selected larger trees with larger crown diameters. The selection of these characteristics could be explained in terms of predator avoidance and thermoregulation efficiency, although it was difficult to delineate which was more important. This could be due to some characteristics of R. roxellana, that is, large groups living in temperate climates, which required a balanced strategy for sleeping site and tree selection in order to optimize their survival chances.

Seasonal variation of energy expenditure in Japanese macaques (Macaca fuscata).

Animals living in seasonal environments must adapt to a wide variation of temperature changes which requires flexible adjustments of time budget and metabolic processes for efficient thermoregulation. The Japanese macaque (Macaca fuscata) is one of only a handful of nonhuman primate species that experience seasonal climates over a wide temperature range. We used behavior observations, accelerometer sensors and the doubly-labelled water (DLW) method to measure activity and total daily energy expenditure (TDEE) of M. fuscata housed in captivity but exposed to natural seasonal variations at day lengths ranging from 10 to 12 h and temperature ranging from 0° to 32°C. Although overall activity was significantly lower in winter compared to summer and autumn, we found no effect of temperature on day-time activity. However nocturnal inactivity and mean length of sleeping bouts significantly increased along a gradient of decreasing temperatures from summer through winter, suggesting the importance of adaptive behavioral thermoregulation in this species. Energy expenditure that was unaccounted for by Basal Metabolic Rate (BMR) and physical activity i.e. expended through diet-induced thermogenesis or thermoregulation was between 14% and 32%. This residual energy expenditure differed between summer/autumn and winter and was relatively consistent across individuals (approximately 5-8% higher in winter). The percentage of body fat and residual energy expenditure were negatively correlated, supporting that fat storage was higher when less energy was required for thermoregulation. Our results suggest that physiological mechanisms like behavioral and autonomic thermoregulation enable M. fuscata to adapt to wide fluctuations in environmental conditions which provide insights into the evolutionary adaptations of nonhuman primates in seasonal climate.

The influence of kinship and dominance hierarchy on grooming partner choice in free-ranging Macaca mulatta brevicaudus.

In group-living animals, individuals do not interact uniformly with their conspecifics. Among primates, such heterogeneity in partner choice can be discerned from affiliative grooming patterns. While the preference for selecting close kin as grooming partners is ubiquitous across the primate order, the selection of higher-ranking non-kin individuals as grooming partners is less common. We studied a group of provisioned rhesus macaques (Macaca mulatta brevicaudus) on Hainan Island, China, to examine rank-related benefits of grooming exchanges and the influence of kin relationships. We tested four hypotheses based on Seyfarth's model: (1) there will be kin preference in grooming relationships; (2) grooming between non-kin individuals will be directed up the dominance rank; (3) grooming between non-kin individuals will reduce aggression from higher-ranking ones; and (4) non-kin individuals will spend more time grooming with adjacent ranked ones. We found that grooming relationships between kin individuals were stronger than those between non-kin individuals. For non-kin relationships, lower-ranking individuals received less aggression from higher-ranking ones through grooming; a benefit they could not derive through grooming exchanges with individuals related by kinship. Individuals spent more time grooming adjacent higher-ranking non-kin individuals and higher-ranking individuals also received more grooming from non-kin individuals. Our results supported Seyfarth's model for predicting partner choice between non-kin individuals. For relationships between kin individuals, we found results that were not consistent with prediction for the exchanges of aggression and grooming, indicating the importance to control for the influence of kinship in future studies.

Small-scale variability in a mosaic tropical rainforest influences habitat use of long-tailed macaques.

Pristine habitats have generally been considered to be the most important ecological resource for wildlife conservation, but due to forest degradation caused by human activities, mosaics of secondary forests have become increasingly prominent. We studied three forest types in a mosaic tropical forest consisting of short secondary forest (SS), tall secondary forest (TS) and freshwater swamp forest (SF). These forests differed in stand structure and floristic composition, as well as phenological productivity of fruits, flowers and young leaves. We examined habitat use of long-tailed macaques (Macaca fascicularis) in relation to indices of phenological activity. The macaques used the SS for feeding/foraging more than the TS and the SF. This was because the SS had higher productivity of fruit, which is a preferred food resource for macaques. Stem densities of young leaves in the SS and the TS also influenced habitat use, as they provided more clumped resources. Use of SF was limited, but these forests provided more species-rich resources. Our results showed that M. fascicularis responded to small-scale variability in phenological activity between forest types found in a heterogeneous mosaic forest, with young secondary regrowth forests likely providing the most important food resources. Mosaic landscapes may be important as they can buffer the effects of temporal food resource variability in any given forest type. In our increasingly human-altered landscapes, a better understanding of the role of secondary forest mosaics is crucial to the conservation and management of wildlife habitats and the animals they support.

Environmental complexity and feeding enrichment can mitigate effects of space constraints in captive callitrichids.

Non-human primates housed in zoos and laboratories often exhibit reduced activity and this poses welfare concerns. We examined the effects of enclosure types of differing size and environmental complexity on the activities of two species of callitrichids. We found that cotton-top tamarins housed in an enclosure of larger size and more environmental complexity showed higher activity levels, which was mainly contributed by more feeding/foraging activity. By contrast, Goeldi's monkeys housed in an enclosure of larger size and more environmental complexity showed lower activity levels, which was mainly contributed by less locomotory activity. In both species, off-exhibit groups housed in smaller enclosures did not show significantly less locomotory activity which would have been expected, as larger availability spaces should allow more opportunities for locomotion. Furthermore, the feeding enrichment had significant effects on increased feeding/foraging activity for both cotton-top tamarins and Goeldi's monkeys, irrespective of enclosure type. These results suggested that environmental complexity (or application of feeding enrichment) that provided more opportunities for natural foraging could have a larger effect on overall activity levels compared with larger enclosure sizes that should provide more locomotion opportunities. More importantly, it showed that even when enclosure space and complexity were limited, increased opportunities for foraging through the application of enrichment could increase species-typical behaviours. Such inexpensive, easy to implement enrichment methods should be applied to provide more complex environments for captive non-human primates, particularly in situations where there are logistical and/or cost constraints to the modification of physical exhibits.

Diet, activity, habitat use, and ranging of two neighboring groups of food-enhanced long-tailed macaques (Macaca fascicularis).

We conducted observations of two neighboring groups of food-enhanced long-tailed macaques (Macaca fascicularis) over a period of one year. We examined their diet, behavior, habitat use, and ranging and how within-population variability reflected differential utilization of anthropogenic food resources. The group that consumed more anthropogenic food spent less time feeding on wild fruits and flowers, less time resting, and more time locomoting. They used forest habitats less often, and had a larger total home range and mean monthly home range. Some of these results contrasted with previous studies of food-enhanced primates which reported that food-enhancement resulted in smaller home ranges, shorter daily ranges, less time traveling and feeding, and more time resting. These contrasting patterns may relate to the nature of anthropogenic foods. In most studies of food-enhanced primates, anthropogenic food resources were abundant and concentrated but the macaques in this study used anthropogenic foods mainly from a few refuse sites where they had limited access, and from dispersed and irregular human provisioning. The group consuming more anthropogenic food therefore showed more spatially dispersed feeding activity and home range use, an effect that was likely further enhanced by lower natural food resource availability within their home range. The Singapore macaque population shows small-scale variability in feeding and ranging behavior, contributing to the complexity of their adaptive variability in a human-altered habitat. Our findings could have important implications for mitigating human-macaque conflict as measures applied at a higher spatial or population level may achieve highly inconsistent results, intensifying the challenges for wildlife managers.

Establishment of a captive all-male group of proboscis monkey (Nasalis larvatus) at the Singapore Zoo.

Surplus male proboscis monkeys at the Singapore Zoo pose a considerable problem for maintenance and maximizing of exhibition potential. In 2008, a new exhibit was constructed to house and display a group of six proboscis monkey males born in Singapore Zoo. To document and monitor the all-male group establishment in the new exhibit, we conducted observations on intragroup interactions between the monkeys, spatial use of their new exhibit, and visitor effects on their behavior. We found contact aggressive interactions between the monkeys to be consistently lower than noncontact aggressive interactions and by week six of introduction to the new exhibit, contact aggression was almost nonevident. Affiliative interactions also developed between individuals in the group, with an interface of aggressive and socioreconcilatory behavior influenced by food competition and a dominance hierarchy. This was evident from significantly higher overall aggression and affiliation during feeding times compared to nonfeeding times, and this was reduced when food competition was mitigated by modifying the feeding regime. We measured the groups' spatial use of the exhibit and the relation to behavior, crowd size, and density. Our results showed that the proboscis monkeys utilized the available exhibit space, were largely unaffected by visitor crowd size and density, and were able to exhibit a variety of natural behaviors, including swimming. Our accomplishment in maintaining and displaying an all-male group of proboscis monkeys in captivity provides viable options for more comprehensive captive management and breeding programs for this endangered species.

Macaque-human interactions and the societal perceptions of macaques in Singapore.

Humans and long-tailed macaques (Macaca fascicularis) interface in several locations in Singapore. We investigated six of these interface zones to assess the level of conflict between the two species. We observed macaque-to-human interactions and distributed questionnaires to residents and visitors of nature reserves. We observed an average of two macaque-to-human interactions per hour at the sites, which included affiliative or submissive behaviors (46.9%), aggression (19.1%), taking food and other items (18.5%) searching bins, cars, and houses (13.4%), and nonaggressive contact (2.1%). Two-thirds of interactions occurred when a human was carrying food or food cues, and one-quarter occurred when a human provoked macaques. Only 8% of interactions occurred without a clear human-triggered context. Our interview showed one-third of respondents experienced nuisance problems from macaques. They had items taken from them (50.5%) and received threats (31.9%). Residents reported more nuisance problems than visitors, and their perceptions toward macaques differed. Residents were more aware of the consequences of food provisioning and that there were regulations against feeding. Residents fed macaques less and held more negative sentiments toward macaques. Nearly half of the interviewed people held neutral attitudes toward macaques and only 26.2% of respondents thought conflict with macaques warranted urgent action. Nearly two-thirds of the respondents supported education programs to ameliorate human-macaque conflict, and less than 15% supported removing or eradicating macaques. 87.6% felt that it is importance to conserve and protect macaques. Our results show that human-macaque conflict exists in Singapore, but that it may not be severe. Human behavior is largely responsible for macaque-to-human interactions, and thus could be lessened with management of human behavior in interface zones (i.e. restrict food carrying and provocation). Moreover, our interviews shows people living in Singapore value macaques, do not wish them entirely removed, prefer education-based solutions, and consider conservation and protection of them important.