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.
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.
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.
Primates, like other mammals, exhibit an annual reproductive pattern that ranges from strictly seasonal breeding to giving birth in all months of the year, but factors mediating this variation are not fully understood. We applied both a categorical description and quantitative measures of the birth peak breadth based on daily observations in zoos to characterise reproductive seasonality in 141 primate species with an average of 941 birth events per species. Absolute day length at the beginning of the mating season in seasonally reproducing species was not correlated between populations from natural habitats and zoos. The mid-point of latitudinal range was a major factor associated with reproductive seasonality, indicating a correlation with photoperiod. Gestation length, annual mean temperature, natural diet and Malagasy origin were other important factors associated with reproductive seasonality. Birth seasons were shorter with increasing latitude of geographical origin, corresponding to the decreasing length of the favourable season. Species with longer gestation periods were less seasonal than species with shorter ones, possibly because shorter gestation periods more easily facilitate the synchronisation of reproductive activity with annual cycles. Habitat conditions with higher mean annual temperature were also linked to less-seasonal reproduction, independently of the latitude effect. Species with a high percentage of leaves in their natural diet were generally non-seasonal, potentially because the availability of mature leaves is comparatively independent of seasons. Malagasy primates were more seasonal in their births than species from other regions. This might be due to the low resting metabolism of Malagasy primates, the comparatively high degree of temporal predictability of Malagasy ecosystems, or historical constraints peculiar to Malagasy primates. Latitudinal range showed a weaker but also significant association with reproductive seasonality. Amongst species with seasonal reproduction in their natural habitats, smaller primate species were more likely than larger species to shift to non-seasonal breeding in captivity. The percentage of species that changed their breeding pattern in zoos was higher in primates (30%) than in previous studies on Carnivora and Ruminantia (13 and 10%, respectively), reflecting a higher concentration of primate species in the tropics. When comparing only species that showed seasonal reproduction in natural habitats at absolute latitudes ≤11.75°, primates did not differ significantly from these two other taxa in the proportion of species that changed to a less-seasonal pattern in zoos. However, in this latitude range, natural populations of primates and Carnivora had a significantly higher proportion of seasonally reproducing species than Ruminantia, suggesting that in spite of their generally more flexible diets, both primates and Carnivora are more exposed to resource fluctuation than ruminants.
The uniquely enlarged noses of male proboscis monkeys are prominent adornments, and a sexually selected male trait. A recent study showed significant correlations among nose, body, and testis sizes and clear associations between nose size and the number of females in a male's harem. However, to date, the analyses of other common male traits, i.e., canines, are lacking. Whereas male nose size had a positive correlation with body size, we unexpectedly found a negative correlation between body and canine sizes. We explain this by an interaction between sexual and natural selection. Larger noses in males may interfere with the use of canines, thereby reducing their effectiveness as weapons. Additionally, longer canines are opposed by natural selection because the larger gape it imposes upon its bearer reduces foraging efficiency, particularly in folivores. This unique case of decoupling of body and canine size reveals that large canines carry an ecological cost.
Foregut fermentation is well known to occur in a wide range of mammalian species and in a single bird species. Yet, the foregut microbial community of free-ranging, foregut-fermenting monkeys, that is, colobines, has not been investigated so far. We analysed the foregut microbiomes in four free-ranging proboscis monkeys (Nasalis larvatus) from two different tropical habitats with varying plant diversity (mangrove and riverine forests), in an individual from a semi-free-ranging setting with supplemental feeding, and in an individual from captivity, using high-throughput sequencing based on 16S ribosomal RNA genes. We found a decrease in foregut microbial diversity from a diverse natural habitat (riverine forest) to a low diverse natural habitat (mangrove forest), to human-related environments. Of a total of 2700 bacterial operational taxonomic units (OTUs) detected in all environments, only 153 OTUs were shared across all individuals, suggesting that they were not influenced by diet or habitat. These OTUs were dominated by Firmicutes and Proteobacteria. The relative abundance of the habitat-specific microbial communities showed a wide range of differences among living environments, although such bacterial communities appeared to be dominated by Firmicutes and Bacteroidetes, suggesting that those phyla are key to understanding the adaptive strategy in proboscis monkeys living in different habitats.
Understanding the natural diet of species may provide useful information that can contribute to successful captive maintenance. A common problem experienced with captive foregut-fermenting primate (colobine) diets is that they are deficient in fiber and therefore highly digestible. This may contribute to gastrointestinal disorders often observed in zoos. An approach to obtain information relevant for the improvement of diets is to compare the nutrient composition of feces from free-ranging and captive individuals. In theory, fecal material can be considered a proxy for diet intake integrated over a certain period of time. We collected fecal samples from eight free-ranging proboscis monkey (Nasalis larvatus, a highly endangered colobine species) groups from a secondary forest along the Kinabatangan River and four from a mixed mangrove-riverine forest along the Garama River, Sabah, Borneo, Malaysia. We also collected fecal samples from 12 individual captive adult/sub-adult proboscis monkeys from three different zoos. We confirmed that feces from free-ranging monkeys contained more fiber and less metabolic fecal nitrogen than those from captive specimens, indicating a less digestible diet in the wild. Modifying the diets of captive colobines to include more fiber, comparable to those of free-ranging ones, may contribute to their health and survival.
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).
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.
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.
The digestive tract of animals, and the patterns how passage markers are excreted from them, have been fruitfully compared to chemical reactor models from engineering science. An important characteristic of idealized reactor models is the smoothness of the curves plotting marker concentrations in outflow (i.e., faeces) over time, which is the result of the assumed complete mixing of the marker with the reactor contents. Published excretion patterns from passage experiments in non-primate mammals appear to indicate a high degree of digesta mixing. In order to assess whether marker excretion graphs from primates differ from ideal outflow graphs, we performed passage experiments in eight individuals of three foregut-fermenting species (Pygathrix nemaeus, Trachypithecus auratus and Semnopithecus vetulus), and added them to available marker excretion curves from the literature. In the resulting collection, 23 out of a total of 25 patterns in foregut fermenters (21 individuals of 10 species from 7 studies), and 13 out of 15 in hindgut fermenters (9 individuals of 2 species from 2 studies), showed an irregular, 'spiky' pattern. We consider this proportion to be too high to be explained by experimental errors, and suggest that this may indicate a taxon-wide characteristic of particularly incomplete digesta mixing, acknowledging that further data from less related primate species are required for corroboration. Our hypothesis is in accordance with previous findings of a comparatively low degree of 'digesta washing' (differential retention of particulate and fluid digesta) in primates. Together with literature findings that suggest a low chewing efficiency in primates compared to other mammals, these observations indicate that in contrast to other herbivores, the success of the primate order is not derived from particularly elaborate adaptations of their ingestive and digestive physiology.
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.
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.
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.
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.
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.
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.
Digestive tract measurements are often considered species specific, but little information exists on the degree to which they change during ontogeny within a species. Additionally, access to anatomical material from nondomestic species is often limited, with fixed tissues possibly representing the only available source, though the degree to which this material is representative in terms of dimensions and weight is debatable. In the present study, the macroscopic anatomy of the digestive tract (length of intestinal sections, and tissue weights of stomach and intestines) of 58 Lemur catta [ranging in age from 1 month (neonates) to 25 years], which had been stored frozen (n = 27) or fixed in formalin (n = 31), was quantified. Particular attention was paid to the caecum and the possible presence of an appendix. The intraspecific allometric scaling of body mass (BM)0.46[0.40;0.51] for total intestine length and BM0.48[0.41;0.54] for small intestine length was higher than the expected geometric scaling of BM0.33, and similar to that reported in the literature for interspecific scaling. This difference in scaling is usually explained by the hypothesis that, to maintain optimal absorption, the diameter of the intestinal tube cannot increase geometrically. Therefore, geometric volume gain of increasing body mass is accommodated for by more-than-geometric length scaling. According to the literature, not all L. catta have an appendix. No appendix was found in the specimens in the present study. The proportions of length measurements did not change markedly during ontogeny, indicating that the proportions of the foetus are representative of those of the adult animal. By contrast, width and tissue-mass scaling of the caecum indicated disproportionate growth of this organ during ontogeny that was not reflected in its length. Compared to overall intraspecific variation, the method of storage (frozen vs. formalin) had no relevant impact on length or weight measurements.
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.