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.
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.
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.
Free-living animals must make dietary choices in terms of chemical and physical properties, depending on their digestive physiology and availability of food resources. Here we comprehensively evaluated the dietary choices of proboscis monkeys (Nasalis larvatus) consuming young leaves. We analysed the data for leaf toughness and digestibility measured by an in vitro gas production method, in addition to previously reported data on nutrient composition. Leaf toughness, in general, negatively correlated with the crude protein content, one of the most important nutritional factors affecting food selection by leaf-eating primates. This result suggests that leaf toughness assessed by oral sensation might be a proximate cue for its protein content. We confirmed the importance of the leaf chemical properties in terms of preference shown by N. larvatus; leaves with high protein content and low neutral detergent fibre levels were preferred to those of the common plant species. We also found that these preferred leaves were less tough and more digestible than the alternatives. Our in vitro results also suggested that N. larvatus were little affected by secondary plant compounds. However, the spatial distribution pattern of plant species was the strongest factor explaining the selection of the preferred leaf species.
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.
Reducing the size of food particles is crucial for herbivores. Seasonal dietary changes are known to influence animals' chewing efficiency. Proboscis monkeys (Nasalis larvatus) are foregut fermenters, with a high chewing efficiency allowing them to achieve very fine faecal particles. In this study, we investigated how proboscis monkeys' chewing efficiency varies between wet and dry seasons, hypothesising differences possibly related to diet change. Faecal particle size analysis is an established approach to estimate chewing efficiency in mammalian herbivores. We analysed 113 proboscis monkey faecal samples collected in the Lower Kinabatangan Wildlife Sanctuary, between 2015 and 2017. By following standard sieve analysis protocols, we measured a mean particle size MPS0.025-8 of 0.45 ± 0.14 mm, and confirmed a previous result that proboscis monkeys have a very low faecal MPS. This study highlights a seasonal influence on proboscis monkeys' chewing efficiency, with smaller MPS (better chewing efficiency) during the wet season. During that time of the year, individuals may potentially change their diet, as all faecal samples contained intact seeds. Whether the seasonal MPS difference in proboscis monkeys is smaller than in other colobines due to their "rumination" strategy remains to be investigated.
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 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.
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.