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 endangered proboscis monkey (Nasalis larvatus) is a sexually highly dimorphic Old World primate endemic to the island of Borneo. Previous studies focused mainly on its ecology and behavior, but knowledge of its vocalizations is limited. The present study provides quantified information on vocal rate and on the vocal acoustics of the prominent calls of this species. We audio-recorded vocal behavior of 10 groups over two 4-month periods at the Lower Kinabatangan Wildlife Sanctuary in Sabah, Borneo. We observed monkeys and recorded calls in evening and morning sessions at sleeping trees along riverbanks. We found no differences in the vocal rate between evening and morning observation sessions. Based on multiparametric analysis, we identified acoustic features of the four common call-types "shrieks," "honks," "roars," and "brays." "Chorus" events were also noted in which multiple callers produced a mix of vocalizations. The four call-types were distinguishable based on a combination of fundamental frequency variation, call duration, and degree of voicing. Three of the call-types can be considered as "loud calls" and are therefore deemed promising candidates for non-invasive, vocalization-based monitoring of proboscis monkeys for conservation purposes.
The proboscis monkey, Nasalis larvatus, is an endemic species to the island of Borneo. It is listed in the IUCN Red List as Endangered with a decreasing population trend. Nevertheless, biological information, especially on the genetic diversity of the species, is still incomplete. Its fragmented distribution poses difficulties in gathering genetic samples along with its widespread distribution across Borneo. This study aims to determine the genetic variation and structure of N. larvatus with an emphasis on Malaysian Borneo populations to elucidate its gene flow. The genetic variation and structure of N. larvatus were examined using 50 sequences of the 1,434-bp cytochrome oxidase subunit I (COI) gene region of mitochondrial DNA. The COI sequences revealed low genetic variation among N. larvatus populations in Malaysian Borneo. This low genetic variability could be the result of inbreeding pressure that may have occurred due to the absence of population expansion in this species over the last 30,000 years. This is supported in our analysis of molecular variance, which showed that groups of N. larvatus are significantly differentiated possibly due to natural geographic barriers. This study provides baseline information on the genetic diversity among proboscis monkey populations in Borneo for the future genetic assessment of the species.
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.
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.
Crassignatha Wunderlich, 1995 is redefined to include species with six eyes in three diads, chelicerae fused only near the base, sculpturing on the carapace, one or two clasping spurs on tibia II, a bilateral scutum of the male abdomen, and globular spermathecae and adjacent copulatory openings in the female. A key and distribution map are provided for 24 Crassignatha species in this paper. Diagnoses and illustrated photographs are provided for 22 species from China, Malaysia, Thailand, and Vietnam. Thirteen species are described and documented as new to science: C. baihua Y. Lin & S. Li, sp. nov. (♂♀), C. bangbie Y. Lin & S. Li, sp. nov. (♀), C. changyan Y. Lin & S. Li, sp. nov. (♀), C. dongnai Y. Lin & S. Li, sp. nov. (♀), C. gucheng Y. Lin & S. Li, sp. nov. (♂♀), C. mengla Y. Lin & S. Li, sp. nov. (♂♀), C. nantou Y. Lin & S. Li, sp. nov. (♂♀), C. nasalis Y. Lin & S. Li, sp. nov. (♂♀), C. rostriformis Y. Lin & S. Li, sp. nov. (♂♀), C. shunani Y. Lin & S. Li, sp. nov. (♂♀), C. si Y. Lin & S. Li, sp. nov. (♂♀), C. thamphra Y. Lin & S. Li, sp. nov. (♀), and C. xichou Y. Lin & S. Li, sp. nov. (♀). Three new combinations are proposed: C. bicorniventris (Lin & Li, 2009), comb. nov., C. quadriventris (Lin & Li, 2009), comb. nov., and C. shiluensis (Lin & Li, 2009), comb. nov. are transferred from Patu Marples, 1951. DNA barcodes and genetic distances of seventeen species are obtained to confirm correct identification. Types of seven known Chinese Crassignatha species are re-examined, and the taxonomic placement of C. longtou Miller, Griswold & Yin, 2009 may be incorrect based on morphological and molecular data.
Understanding determinants shaping infection risk of endangered wildlife is a major topic in conservation medicine. The proboscis monkey, Nasalis larvatus, an endemic primate flagship species for conservation in Borneo, is endangered through habitat loss, but can still be found in riparian lowland and mangrove forests, and in some protected areas. To assess socioecological and anthropogenic influence on intestinal helminth infections in N. larvatus, 724 fecal samples of harem and bachelor groups, varying in size and the number of juveniles, were collected between June and October 2012 from two study sites in Malaysian Borneo: 634 samples were obtained from groups inhabiting the Lower Kinabatangan Wildlife Sanctuary (LKWS), 90 samples were collected from groups of the Labuk Bay Proboscis Monkey Sanctuary (LBPMS), where monkeys are fed on stationary feeding platforms. Parasite risk was quantified by intestinal helminth prevalence, host parasite species richness (PSR), and eggs per gram feces (epg). Generalized linear mixed effect models were applied to explore whether study site, group type, group size, the number of juveniles per group, and sampling month predict parasite risk. At the LBPMS, prevalence and epg of Trichuris spp., strongylids, and Strongyloides spp. but not Ascaris spp., as well as host PSR were significantly elevated. Only for Strongyloides spp., prevalence showed significant changes between months; at both sites, the beginning rainy season with increased precipitation was linked to higher prevalence, suggesting the external life cycle of Strongyloides spp. to benefit from humidity. Higher prevalence, epgs, and PSR within the LBPMS suggest that anthropogenic factors shape host infection risk more than socioecological factors, most likely via higher re-infection rates and chronic stress. Noninvasive measurement of fecal parasite stages is an important tool for assessing transmission dynamics and infection risks for endangered tropical wildlife. Findings will contribute to healthcare management in nature and in anthropogenically managed environments.