Inter-individual relationships in proboscis monkeys: a preliminary comparison with other non-human primates

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.     

Daily feeding rhythm in proboscis monkeys: a preliminary comparison with other non-human primates

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.     

Regurgitation and remastication in the foregut-fermenting proboscis monkey (Nasalis larvatus)

Although foregut fermentation is often equated with rumination in the literature, functional ruminants (ruminants, camelids) differ fundamentally from non-ruminant foregut fermenters (e.g. macropods, hippos, peccaries). They combine foregut fermentation with a sorting mechanism that allows them to remasticate large particles and clear their foregut quickly of digested particles; thus, they do not only achieve high degrees of particle size reduction but also comparatively high food intakes. Regurgitation and remastication of stomach contents have been described sporadically in several non-ruminant, non-primate herbivores. However, this so-called 'merycism' apparently does not occur as consistently as in ruminants. Here, to our knowledge we report, for the first time, regurgitation and remastication in 23 free-ranging individuals of a primate species, the foregut-fermenting proboscis monkey (Nasalis larvatus). In one male that was observed continuously during 169 days, the behaviour was observed on 11 different days occurring mostly in the morning, and was associated with significantly higher proportions of daily feeding time than on days when it was not observed. This observation is consistent with the concept that intensified mastication allows higher food intake without compromising digestive efficiency, and represents an expansion of the known physiological primate repertoire that converges with a strategy usually associated with ruminants only.     

Effects of water level on sleeping-site selection and inter-group association in proboscis monkeys: why do they sleep alone inland on flooded days?

A one-male group (BE-Group) of proboscis monkeys was studied along the Menanggul River, a tributary of the Kinabatangan River, Sabah, Malaysia, from May 2005 to 2006. It has generally been assumed that proboscis monkeys only set up their sleeping sites along the riverbank; however, when more than 1 m of water covered the forest floor for more than 700 m inland from the riverbank during the seasonal flood, the BE-Group slept inside the forest. It seems that the sleeping-site selection of the BE-Group was not influenced by food availability during the flooded months because the food availability by the vegetational survey did not vary much between flooded and non-flooded months. In addition, feeding behaviors of the focal monkey in the BE-Group also did not vary much between flooded and non-flooded days. On the other hand, the water level statistically influenced the sleeping-site selection. The proboscis monkeys remained in inland forest during the flooded days because of the reduced predation threat, as terrestrial predators such as clouded leopards are prevented from foraging by deep water covering the forest floor. On non-flooded days when the BE-Group slept at the riverbank, they frequently slept close to other one-male groups on the riverside trees. Contrastingly, when the group slept inside the forest on flooded days when the water level was high, they slept away from other groups. This difference in the need for one-male groups to sleep close to each other might be attributed to the decreased predation threat during high water level in the flooded days.     

Selection of river crossing location and sleeping site by proboscis monkeys (Nasalis larvatus) in Sabah, Malaysia

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.     

Faecal particle size in free-ranging primates supports a ‘rumination’ strategy in the proboscis monkey (<Emphasis Type="Italic">Nasalis larvatus</Emphasis>)

In mammalian herbivores, faecal particle size indicates chewing efficiency. Proboscis monkeys (Nasalis larvatus) are foregut fermenters in which regurgitation and remastication (i.e. rumination) was observed in the wild, but not with the same consistency as found in ruminants and camelids. To test whether this species has exceptional chewing efficiency among primates, as ruminants have among mammals, we compared faecal particle size in free-ranging specimens with those of 12 other primate species. The discrete mean faecal particle size (dMEAN) increased with body mass (M) as dMEAN (mm) = 0.65 (95 % confidence interval 0.49–0.87) M ^{0.33 (0.23–0.43)} in simple-stomached species. At 0.53 ± 0.09 mm, dMEAN of proboscis monkeys was particularly small for their average M (15 kg) and significantly smaller than values of two other foregut fermenting primate species. While we cannot exclude other reasons for the exceptional chewing efficiency in proboscis monkeys, this represents circumstantial evidence for regular use of rumination in this species. Thus, proboscis monkeys might be a model for convergent evolution towards rumination in a non-ungulate taxon.     

Aerial surveys give new estimates for orangutans in Sabah, Malaysia

Great apes are threatened with extinction, but precise information about the distribution and size of most populations is currently lacking. We conducted orangutan nest counts in the Malaysian state of Sabah (North Borneo), using a combination of ground and helicopter surveys, and provided a way to estimate the current distribution and size of the populations living throughout the entire state. We show that the number of nests detected during aerial surveys is directly related to the estimated true animal density and that a helicopter is an efficient tool to provide robust estimates of orangutan numbers. Our results reveal that with a total estimated population size of about 11,000 individuals, Sabah is one of the main strongholds for orangutans in North Borneo. More than 60% of orangutans living in the state occur outside protected areas, in production forests that have been through several rounds of logging extraction and are still exploited for timber. The role of exploited forests clearly merits further investigation for orangutan conservation in Sabah.     

Ranging Behavior of Proboscis Monkeys in a Riverine Forest with Special Reference to Ranging in Inland Forest

We observed a unimale group (BE-Group) of proboscis monkeys (Nasalis larvatus) comprising an α-male, 6 adult females, and several immatures from May 2005 to May 2006. We followed the group for 2014 h along the Menanggul River, Sabah, Malaysia (118°30′E, 5°30′N). Observations focused mainly on ranging behavior. We determined availability and seasonal changes in plant species consumed by the members of the group by vegetation surveys in a 2.15-ha area along 200–500 m trails in the riverine forest. During the observation period, the group ranged ≤800 m from the riverbank, within a total range of 138.3 ha. The daily path length of the group ranged from 220 to 1734 m (mean, 799 m), and daily path length correlates negatively with fruit availability. The monkeys were apt to remain within a small range in fruit-abundant seasons. Because the monkeys preferred to feed on fruits of dominant plant species in the study area, their daily path length may decrease on days when they feed on fruits. The core areas of the group’s home range were along the river because the monkeys typically returned to riverside trees to sleep. The group most often used areas that were nearer the riverbank and where the availability of fruits was higher. The most frequently used grids were the ones where the group often had sleeping sites and crossed the river. Avoiding predation may be the main reason for river crossing and selecting particular sleeping sites; hence not only food availability but also the risk of predation appears to influence the ranging of the BE-Group.     

Assessments made easier: examining the use of a rating-based questionnaire to capture behavioral data in rehabilitant orangutans (Pongo pygmaeus morio)

Rehabilitation and release are commonly used for confiscated, surrendered, and rescued primates. To improve release efficacy it is important to generate accurate behavioral profiles of release candidates. Research on primates traditionally uses observer ratings to measure individual differences. This method is easily implemented, but its validity has been questioned. We evaluated whether observer ratings reflect behavioral data indicating forest adaptation in 18 free-ranging rehabilitant orangutans (Pongo pygmaeus morio). In 2017, we used a species-specific questionnaire to measure how often orangutans engaged in behaviors linked to living successfully in the wild (e.g., nest building) and the extent to which they express personality traits that may influence forest adaptation. We collected 11 months of observational data on 17 of the orangutans concurrently to validate the questionnaire items, and collected further questionnaire data for 16 of the individuals in 2019. We used regularized exploratory factor analysis (REFA) and parallel analysis to condense the ratings and determine that two factors could be reliably extracted. We conducted another REFA using the observational data, and calculated factor congruence coefficients following procrustean rotation. The first of the two factors represented forest skills and human aversion, and was congruent with observational data. The second factor reflected boldness, sociability, and exploration, and was not congruent with observational data. Ratings correlated significantly with observations for all five questionnaire items reflecting adaptation to forest life, and for three of seven items reflecting personality traits. We conclude that ratings can be a valid approach to obtain individual-based behavioral information reflecting forest adaptation in free-ranging rehabilitant orangutans, and may be particularly useful in summarizing behaviors relevant to forest adaptation that are otherwise challenging to gather in primates.

     

Comparisons of Intraunit Relationships in Nonhuman Primates Living in Multilevel Social Systems

Multilevel social systems have evolved in several species of cercopithecoid primates and appear to be an effective means of changing group size amid variation in environmental conditions. Larger groupings of these species fission and fuse, making intraunit relationships essential to maintain the integrity of the smallest social units. We examine these intraunit relationships in four primates with multilevel social systems: proboscis monkeys (Nasalis larvatus), snub-nosed monkeys (Rhinopithecus roxellana), hamadryas baboons (Papio hamadryas), and geladas (Theropithecus gelada), using social network analysis. The proboscis monkeys and hamadryas baboons were wild and unprovisioned, whereas the snub-nosed monkeys and geladas were partly provisioned. Comparison of eigenvector centrality coefficients revealed a phylogenetic difference in the key individuals maintaining social networks between the colobines and the cercopithecines: females were more central in proboscis and snub-nosed monkeys, with males generally peripheral to social interaction, whereas males were more central than females in geladas and hamadryas. A comparison of sex differences in clustering coefficients, however, revealed a significant difference only in geladas, suggesting that one-male–multifemale units in this species become more unstable when females, but not males, are removed from social networks. Taken together, our results reveal the strongest differences between geladas, characterized by female philopatry and male dispersal, and the three species with bisexual dispersal. These results demonstrate the potential for social network analysis to reveal the social bonds most important for maintaining cohesion of the smallest units of primate multilevel societies. This, in turn, can serve as a proxy, in the absence of long-term data, for underlying patterns of sex-biased dispersal and philopatry.