This is the first report on inter-individual relationships within a one-male group of proboscis monkeys (Nasalis larvatus) based on detailed identification of individuals. From May 2005 to 2006, focal and ad libitum data of agonistic and grooming behaviour were collected in a forest along the Menanggul River, Sabah, Malaysia. During the study period, we collected over 1,968 h of focal data on the adult male and 1,539 h of focal data on the six females. Their social interactions, including agonistic and grooming behaviour, appeared to follow typical patterns reported for other colobines: the incidence of social interaction within groups is low. Of 39 agonistic events, 26 were displacement from sleeping places along the river, 6 were the α male threatening other monkeys to mediate quarrels between females and between females and juveniles, and 7 were displacement from feeding places. Although the agonistic behaviour matrix based on the 33 intra-group agonistic events (excluding events between adults and juveniles and between adults and infants) was indicative of non-significant linearity, there were some specific dominated individuals within the group of proboscis monkeys. Nonetheless, grooming behaviour among adult females within a group were not affected by the dominance hierarchy. This study also conducted initial comparisons of grooming patterns among proboscis monkeys and other primate species. On the basis of comparison of their grooming networks, similar grooming patterns among both-sex-disperse and male-philopatric/female-disperse species were detected. Because adult females in these species migrate to groups repeatedly, it may be difficult to establish the firm grooming exchange relationship for particular individuals within groups, unlike in female-philopatric/male-disperse species. However, grooming distribution patterns within groups among primate species were difficult to explain solely on the basis of their dispersal patterns. Newly immigrated females in some species including proboscis monkeys are eager to have social interactions with senior group members to improve their social position.
A group of proboscis monkeys (Nasalis larvatus) consisting of an alpha-male, six adult females, and several immatures was observed from May 2005-2006. We collected over 1,968 hr of focal data on the adult male and 1,539 hr of focal data on the six females in a forest along the Menanggul River, Sabah, Malaysia. Availability and seasonal changes in plant species consumed by the focal monkeys were determined by vegetation surveys carried out across an area of 2.15 ha along 200-500 m trails in riverine forest. A total of 188 plant species were consumed by the focal monkeys. The activity budget of members of our study group was 76.5% resting, 19.5% feeding, and 3.5% moving. Young leaves (65.9%) and fruits (25.9%) accounted for the majority of feeding time. Over 90% of fruit feeding involved the consumption of unripe fruits and in the majority of case both the fruit flesh and seeds were eaten. Although fruit eating was rare in some months, during other times of the year time fruit feeding exceeded the time devoted to young leaves. We found that monthly fruit availability was positively related to monthly fruit eating and feeding activity, and seasonal fluctuations in dietary diversity were significantly affected by fruit eating. These results suggest that fruit availability and fruit-eating behaviors are key factors that influence the activity budget of proboscis monkeys. Earlier assumptions that colobine monkeys are obligate folivores do not apply well to proboscis monkeys and certain other colobines. Our findings may help contribute to a better understanding of the dietary adaptations and feeding ecology of Asian colobines.
In this study, we have reported two direct observations of individuals from a one-male group of proboscis monkeys (Nasalis larvatus) being killed by clouded leopards (Neofelis diardi) in the riverine forest along the Menanggul river, a tributary of the Kinabatangan river in Sabah, Malaysia. One of the two individuals was an infant female and the other was a juvenile female. Based on literature reviews and the observations reported here, we suggest that clouded leopard and crocodile might be significant potential predators of proboscis monkeys of any age or sex and that predation threats elicit the monkeys' anti-predator strategies. Moreover, the observations of the monkeys' behaviour when the group is attacked by a predator suggest that the adult males in one-male groups play an important role as protectors.
From May 2005-2006, selections of river crossing locations and sleeping sites used by a one-male group (BE-Group) of proboscis monkeys (Nasalis larvatus) were investigated along the Menanggul River, tributary of the Kinabatangan River, Sabah, Malaysia. The frequency of river crossings for focal monkeys in the BE-Group was significantly higher at locations with narrow branch-to-bank distances. Branch-to-bank distances were defined as the distances between the longest tree branches extending over the river and the bank of river on each side. This was measured in areas crossed by the monkeys. The focal monkeys used locations with a higher probability of successful river crossings that did not require jumping into the water and swimming across than those that did. The frequency of sleeping site usage by the BE-Group was positively correlated with the frequency of using river crossing locations by the focal monkeys. Previous reports on predation of proboscis monkeys indicate that clouded leopards (Neofelis diardi) and crocodilians (Tomistoma schlegeli and Crocodylus porosus) may be the major terrestrial and aquatic predators of these monkeys. The selection of river crossing locations by proboscis monkeys may be influenced both by the threat of these predators and the location of suitable and protected sleeping sites. Finally, sleeping sites locations that offer arboreal escape routes may protect proboscis monkeys from leopard attack.
Knowledge about the feeding ecology and dietary overlap of sympatric primates is essential for understanding how animals avoid or reduce interspecific competition. From April 2014 to March 2015, we investigated the feeding ecologies of two sympatric primates, a hindgut fermenter, the long-tailed macaque (Macaca fascicularis) and a foregut fermenter, the dusky langur (Trachypithecus obscurus obscurus), in a mixed landscape consisting of urban and agro-forested areas and forest fragments in Malaysia. We collected a total of 5570 and 4029 of feeding records for M. fascicularis and T. o. obscurus, respectively, using the 10-min scan sampling method. Food availability and seasonal changes in plant species consumed by both study groups were determined by vegetation surveys carried out across an area of 1.6 ha. A total of 113 and 130 plant species were consumed by M. fascicularis and T. o. obscurus, respectively. Leaves (51%) and fruits (40%) accounted for the majority of the feeding records in T. o. obscurus, whereas fruits (32%) and anthropogenic foods (27%) together with leaves (15%) and insects (6%) accounted for the majority of the feeding records for M. fascicularis. Throughout the year, there were 59 consumed plant species common to both species, and the dietary overlap was the highest for fruits. Although leaves were always more abundant than fruits in our study site, the amount of monthly fruit eating by the two species showed a significant correlation with that of fruit availability. Monthly fruit availability had a positive effect on overall monthly dietary overlap while flower and leaf availability had a negative effect. We showed that fruit was the preferred food resource of two sympatric species with different digestive systems. This could have implications for resource competition, interspecific competition, and niche separation, which should be investigated in more detail.
Colobine monkeys have complex, multichambered, foregut-fermenting stomachs with either three ("tripartite") or four ("quadripartite," adding the praesaccus) chambers where a commensal microbiome digests plant cell walls and possibly detoxifies defensive plant chemicals. Although different potential functions for the praesaccus have been suggested, little evidence exists to support any of the proposed functions. To address the issue of the function of the praesaccus, we collated literature data on diet and compared tripartite and quadripartite species. Our results suggest that the praesaccus is an adaptation to a dietary niche with a particularly high reliance on leaves as fallback foods in colobine clades with quadripartite stomachs, and a higher reliance on fruits/seeds as foods at times of high fruit availability in clades with tripartite stomachs. This supports the notion that a large gut capacity is an important characteristic by which folivores survive on a high fiber diet, and that this large gut capacity may not be necessary for some species if there are seasonal peaks in fruit availability.
Assessments of the welfare status of captive and semi-captive animals often compare how their expression of natural behaviors differs from that of free-ranging conspecifics. From December 2015-2016, we recorded and analyzed the activity budget and postural behaviors of three orangutans in Bukit Merah Orang Utan Island (BMOUI) to evaluate their welfare status. The orangutans' activity budget was dominated by resting (60%), feeding (13%), playing (14%), and moving (9%). Behavioral categories followed a similar trend: resting > feeding > moving > playing, except that the subadult male spent significantly more time playing than the two adults. The most predominant posture was sitting (47.0%), followed by pronograde standing (29.4%), lying (10.5%), and clinging (4.5%). Our results suggest that orangutans on BMOUI engage in less feeding but more resting, and show less postural diversity than free-ranging individuals. We propose that appropriate interventions to shift activity budgets, especially feeding vs. resting, and postural behaviors of captive orangutans toward those found in free-ranging orangutans might be beneficial for their welfare and survival.
Understanding social organization is fundamental for the analysis of animal societies. In this study, animal single-file movement data-serialized order movements generated by simple bottom-up rules of collective movements-are informative and effective observations for the reconstruction of animal social structures using agent-based models. For simulation, artificial 2-dimensional spatial distributions were prepared with the simple assumption of clustered structures of a group. Animals in the group are either independent or dependent agents. Independent agents distribute spatially independently each one another, while dependent agents distribute depending on the distribution of independent agents. Artificial agent spatial distributions aim to represent clustered structures of agent locations-a coupling of "core" or "keystone" subjects and "subordinate" or "follower" subjects. Collective movements were simulated following two simple rules, 1) initiators of the movement are randomly chosen, and 2) the next moving agent is always the nearest neighbor of the last moving agents, generating "single-file movement" data. Finally, social networks were visualized, and clustered structures reconstructed using a recent major social network analysis (SNA) algorithm, the Louvain algorithm, for rapid unfolding of communities in large networks. Simulations revealed possible reconstruction of clustered social structures using relatively minor observations of single-file movement, suggesting possible application of single-file movement observations for SNA use in field investigations of wild animals.
To understand the effects of environmental factors on a social system with multilevel society in proboscis monkey units, the temporal change of the local density of sleeping sites of monkeys was investigated along the Menanggul river from May 2005 to 2006 in Malaysia. Proboscis monkeys typically return to riverside trees for night sleeping. The sleeping site locations of a one-male unit (BE-unit) were recorded and the locations of other one-male and all-male units within 500 m of the BE-unit were verified. In addition, environmental factors (food availability, the water level of the river, and the river width) and copulation frequency of BE-unit were recorded. From the analyses of the distance from the BE-unit to the nearest neighbor unit, no spatial clumping of the sleeping sites of monkey units on a smaller scale was detected. The results of a Bayesian analysis suggest that the conditional local density around the BE-unit can be predicted by the spatial heterogeneity along the river and by the temporal change of food availability, that is, the local density of monkey units might increase due to better sleeping sites with regard to predator attacks and clumped food sources; proboscis monkeys might not exhibit high-level social organization previously reported. In addition, this study shows the importance of data analysis that considers the effects of temporal autocorrelation, because the daily measurements of longitudinal data on monkeys are not independent of each other.
In non-human primates, the daily feeding rhythm, i.e., temporal fluctuation in feeding activity across the day, has been described but has rarely received much analytical interpretation, though it may play a crucial part in understanding the adaptive significance of primate foraging strategies. This study is the first to describe the detailed daily feeding rhythm in proboscis monkeys (Nasalis larvatus) based on data collected from both riverbank and inland habitats. From May 2005 to May 2006, data on feeding behavior in a group of proboscis monkeys consisting of an alpha-male, six adult females and immatures was collected via continuous focal animal sampling technique in a forest along the Menanggul River, Sabah, Malaysia. In both the male and females, the highest peak of feeding activity was in the late afternoon at 15:00-17:00, i.e., shortly before sleeping. The differences in the feeding rhythm among the seasons appeared to reflect the time spent eating fruit and/or the availability of fruit; clearer feeding peaks were detected when the monkeys spent a relevant amount of time eating fruit, but no clear peak was detected when fruit eating was less frequent. The daily feeding rhythm was not strongly influenced by daily temperature fluctuations. When comparing the daily feeding rhythm of proboscis monkeys to that of other primates, one of the most common temporal patterns detected across primates was a feeding peak in the late afternoon, although it was impossible to demonstrate this statistically because of methodological differences among studies.
Tourists are attracted to the Bukit Melawati Kuala Selangor (BMKS) of Peninsular Malaysia, a small hill park, for both its status as a historical site and the free-ranging silvered langurs (Trachypithecus cristatus) that come for provisioning. We assessed the population trends and group sizes of T. cristatus over 10 years in the BMKS and examined their ranging patterns. Comparisons of observed populations between 2005 (190 individuals) and 2017 (193 individuals) revealed the stable demography and group sizes of the six T. cristatus groups in the BMKS. Based on a total of 185 location points of the six groups in 2017, their mean ranging area was 3.6 ha with a range of 0.86-6.93 ha with extensive spatial overlap. We also found a significant positive relationship between the six groups' ranges and group sizes in 2017. Additionally, qualitative ecological comparisons with a previous study on T. cristatus in 1965 (before provisioning) suggest that the artificial food supply in the study area could modify the population dynamics and socioecology of T. cristatus. The modifications might alter their range size and territoriality in the BMKS. Overall, we found that provisioning had negative effects on the ecology of T. cristatus in the BMKS. Therefore, modifying management policies, such as banning feeding and implementing educational programs, may contribute to their proper conservation.
Necrophilic behavior (attempted copulation with corpses) has been scarcely reported in non-human primates, especially in the wild. Here is the first case of necrophilic behavior observed in wild stump-tailed macaques in Thailand. Six groups of total N > 460 individuals have been identified and habituated. The corpse of an adult female was found and directly observed for 2 days and by camera trap for 3 days. The cause of death could not be identified, but no prominent physical injury was detected. Within 3 days of the observation, three different males attempted copulation with the corpse. Noteworthy for this observation was that not only males in the group of the dead female but also males from different groups interacted with the corpse. Taken together, these observations suggest that some cues emanating from the corpse coupled with a nonresistant/passive orientation may have triggered these responses in the males. Given that necrophiliac responses have been scarcely reported in non-human primates, our findings provide new insight into these behaviors and to comparative thanatology in general.
Although the role of primates in seed dispersal is generally well recognized, this is not the case for colobines, which are widely distributed in Asian and African tropical forests. Colobines consume leaves, seeds and fruits, usually unripe. A group of proboscis monkeys (Colobinae, Nasalis larvatus) consisting of 1 alpha-male, 6 adult females and several immatures, was observed from May 2005 to May 2006. A total of 400 fecal samples from focal group members covering 13 months were examined, with over 3500 h of focal observation data on the group members in a forest along the Menanggul River, Sabah, Malaysia. Intact small seeds were only found in 23 of 71 samples in Nov 2005, 15 of 38 in Dec 2005 and 5 of 21 in Mar 2006. Seeds of Ficus (all <1.5 mm in length) were found in all 3 months and seeds from Antidesma thwaitesianum (all <3 mm) and Nauclea subdita (all <2 mm) only in Nov and Dec, which was consistent with members of the study group consuming fruits of these species mostly at these times. To our knowledge, these are the first records of seeds in the fecal samples of colobines. Even if colobines pass relatively few seeds intact, their high abundance and biomass could make them quantitatively significant in seed dispersal. The potential role of colobines as seed dispersers should be considered by colobine researchers.
Three strains (YZ01T, YZ02 and YZ03) of Gram-stain-positive, facultatively anaerobic rods were isolated from the forestomach contents collected from a captive male proboscis monkey (Nasalis larvatus) at Yokohama Zoo in Japan. Phylogenetic analysis of the 16S rRNA gene sequences revealed that these strains belonged to the genus Lactobacillus. Based on the sequence similarity of the 16S rRNA gene, Lactobacillus delbrueckii subsp. indicus JCM 15610T was the closest phylogenetic neighbour to YZ01T. Sequence analyses of two partial concatenated housekeeping genes, the RNA polymerase alpha subunit (rpoA) and phenylalanyl-tRNA synthase alpha subunit (pheS) also indicated that the novel strains belonged to the genus Lactobacillus. The average nucleotide identity and digital DNA-DNA hybridization (dDDH) between L. delbrueckii subsp. indicus and YZ01T were 85.9 and 31.4 %, respectively. The phylogenetic tree based on the whole genomic data of strains YZ01T, YZ02 and YZ03 suggested that these three strains formed a single monophyletic cluster in the genus Lactobacillus, indicating that it belonged to a new species. The DNA G+C content of strain YZ01T was 51.6 mol%. The major fatty acids were C16 : 0 and C18 : 1 ω9c. Therefore, based on phylogenetic, phenotypic and physiological evidence, strains YZ01T, YZ02 and YZ03 represent a novel species of the genus Lactobacillus, for which the name Lactobacillus nasalidis sp. nov. is proposed with the type strain YZ01T (=JCM 33769T=DSM 110539T).
Many species of terrestrial animals, including primates, live in varied association with the aquatic (e.g., riverine or coastal) environment. However, the benefits that each species receive from the aquatic environment are thought to vary depending on their social and ecological characteristics, and thus, elucidating those benefits to each species is important for understanding the principles of wild animal behaviour. In the present study, to gain a more complete picture of aquatic environment use, including social and ecological factors in primates, factors affecting riverine habitat utilization of two macaque species (Macaca nemestrina and M. fascicularis) were identified and qualitative comparisons were made with sympatric proboscis monkeys (Nasalis larvatus), which have different social and ecological characteristics. Temporal variation in sighting frequency of macaques at the riverbanks was positively related to the fruit availability of a dominant riparian plant species and negatively related to the river water level which affects the extent of predation pressure. Riverine utilization of macaques was greatly influenced by distribution and abundance of food (especially fruit) resources, possibly in association with predation pressure. Additionally, qualitative ecological comparisons with sympatric proboscis monkeys suggest that the drivers of riverine utilization depend on the feeding niches of the species, and different anti-predator strategies resulting from their differing social structures.
One of the goals for primate feeding ecology is to understand the factors that affect inter- and intra-specific variations. Therefore, a detailed description of basic feeding ecology in as many populations as possible is necessary and warrants further understanding. The black-and-white colobus (Colobus guereza) or guereza is widely distributed in Africa and is one of the well-studied colobines in terms of their feeding; they demonstrate considerable variation in their diets in response to local conditions. We studied the diet of a group of guerezas in the Kalinzu Forest, Uganda, for over 30 consecutive months using behavioral observation (4308 h in total), phenology, and vegetation surveys. A total of 31 plant species were consumed by the study group. This study group was predominantly folivorous; the majority of their feeding time was involved in feeding on young leaves (87%). However, during certain times of the year, fruits and seeds accounted for 45% of monthly feeding time. Young leaves of Celtis durandii were by far the most important food, which constituted 58% of the total feeding records. There was a significant increase in the consumption of fruits and flowers once young leaf availability was low, but their consumption of fruits did not significantly increase even when fruit availability was high. Their monthly dietary diversity increased as the number of available plants with young leaves declined, suggesting that much of the dietary diversity in the study group may be attributable to the young leaf portion of their diet. Our findings may help contribute to a better understanding of the dietary adaptations and feeding ecology of guerezas in response to local environmental conditions.
Colobine monkeys are known for the anatomical complexity of their stomachs, making them distinct within the primate order. Amongst foregut fermenters, they appear peculiar because of the occurrence of two different stomach types, having either three ('tripartite') or four ('quadripartite', adding the praesaccus) chambers. The functional differences between tri and quadripartite stomachs largely remain to be explained. In this study, we aim to compare the apparent digestibility (aD) in tripartite and quadripartite colobines. Hence, we measured the aD in two colobine species, Nasalis larvatus (quadripartite) and Trachypithecus cristatus (tripartite), in two zoos. We also included existing colobine literature data on the aD and analysed whether the aD of fibre components is different between the stomach types to test the hypothesis of whether quadripartite colobines show higher aD of fibre components than tripartite colobines did. Our captive N. larvatus specimen had a more distinctively varying nutrient intake across seasons with a larger seasonal variation in aD than that of a pair of T. cristatus, which mostly consumed commercial foods with a lower proportion of browse and less seasonal variation. We observed higher aD of dry matter (DM), neutral detergent fibre (NDF) and acid detergent fibre (ADF) in the N. larvatus specimen, suggesting a higher gut capacity of N. larvatus provided by the additional praesaccus forestomach chamber. Based on the analysis of literature data for aD, we also found that quadripartite species achieved higher fibre digestibility at similar dietary fibre levels compared with tripartite species, supporting the hypothesis that the additional gut capacity offered by the praesaccus facilitates a longer retention and hence more thorough microbial fermentation of plant fibre.
Inferring the latent structures of social organisations is a central theme in animal ecology. Sophisticated theoretical frameworks underpin the study of various primate social systems. Single-file movements, defined as serially ordered patterns of animals, reflect intra-group social relationships and provide a key to understanding social structures. Here, we analysed automated camera-trapping data on the order of progression of single-file movements in a free-ranging group of stump-tailed macaques to estimate the social structure of the group. The sequence of single file movements showed some regularities, particularly for adult males. Social network analysis identified four community clusters (subgroups) corresponding to the social structures reported for these stumptailed macaques, i.e. males that had copulated more frequently with females were spatially clustered with females, but males that had copulated less frequently were spatially isolated from females. Our results suggest that stumptailed macaques move in regular, socially determined patterns that reflect the spatial positions of adult males and are related to the social organisation of the species.