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.
Ogata and Seino [Zoo Biol, 2015, 34:76-79] sequenced the mitochondrial D-loop of five proboscis monkeys Nasalis larvatus from Yokahama Zoo, Japan, that were imported from Surabaya Zoo, Indonesia. They compared their sequences with those of 16 proboscis monkeys from Sabah, Malaysia, and on the basis of a haplotype network analysis of 256 base pairs concluded that the northern Malaysian and southern Indonesian populations of proboscis monkeys are genetically differentiated. I provide information on the origin of the Indonesian proboscis monkeys, showing that they were the first-generation offspring of wild-caught individuals from the Pulau Kaget Strict Nature Reserve in the province of South Kalimantan. Using a phylogenetic approach and adding additional sequences from Indonesia and Malaysia, I reanalyzed their data, and found no support for a north-south divide. Instead the resulting tree based on 433 base pairs sequences show two strongly supported clades, both containing individuals from Indonesia and Malaysia. Work on captive individuals, as reported by Ogata and Seino, can aid in developing appropriate markers and techniques, but to obtain a more complete understanding of the genetic diversity and differentiation of wild proboscis monkeys, more detailed geographic sampling from all over Borneo is needed.
In this study, we sequenced a partial segment of the mitochondrial control region from 21 proboscis monkeys of the Klias peninsula, the last large population remaining on the west coast of Sabah, Malaysia. Our results showed that this population retains substantial genetic variation, and subpopulations from different river systems in the central and southern portions of the Klias share multiple haplotypes. We also compared our data with previously generated sequences from 2 eastern populations of proboscis monkeys in Sabah and found little evidence of regional genetic structure. Based on these results, we argue that conservation efforts should focus on restoring connectivity between central and southern Klias peninsula proboscis monkeys and discuss future analyses needed to better understand the mitochondrial structure of proboscis monkeys in Sabah.
Male proboscis monkeys have uniquely enlarged noses that are prominent adornments, which may have evolved through their sexually competitive harem group social system. Nevertheless, the ecological roles of the signals encoded by enlarged noses remain unclear. We found significant correlations among nose, body, and testis sizes and a clear link between nose size and number of harem females. Therefore, there is evidence supporting both male-male competition and female choice as causal factors in the evolution of enlarged male noses. We also observed that nasal enlargement systematically modifies the resonance properties of male vocalizations, which probably encode male quality. Our results indicate that the audiovisual contributions of enlarged male noses serve as advertisements to females in their mate selection. This is the first primate research to evaluate the evolutionary processes involved in linking morphology, acoustics, and socioecology with unique masculine characteristics.
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.
The predation pressure put on primates by diurnal birds of prey differs greatly between continents. Africa and South America have specialist raptors (e.g. crowned hawk-eagle Stephanoaetus coronatus and harpy eagle Harpia harpyja) whereas in Asia the only such specialist's (Philippine eagle Pithecophaga jefferyi) distribution is largely allopatric with primates. The almost universal absence of polyspecific groups in Asia (common in Africa and South America) may indicate reduced predation pressure. As such there is almost no information on predation pressures on primates in Asia by raptors. Here we report successful predation of a juvenile banded langur Presbytis femoralis (~2 kg) by a changeable hawk-eagle Spizaetus cirrhatus. The troop that was attacked displayed no signs of being alarmed, and no calls were made before the event. We argue that in insular Southeast Asia, especially, large Spizaetus hawk-eagles (~2 kg) are significant predators of arboreal colobines. Using data on the relative size of sympatric Spizaetus hawk-eagles and colobines we make predictions on where geographically we can expect the highest predation pressure (Thai-Malay Peninsula) and which colobines are least (Nasalis larvatus, Trachypithecus auratus, P. thomasi) and most (P. femoralis, T. cristatus) affected.
Successful or unsuccessful female transfers were observed seven times during a 32-month field study of proboscis monkeys (Nasalis larvatus) inhabiting a riverine forest along a tributary of the Kinabatangan River, Sabah, Malaysia. In all cases, the females voluntarily left their own groups and immediately joined with another one. When adult females tried to shift to other groups, adult males called them back to their own groups, but appeared to be indifferent to subadult females. When the adult females returned, the males never attacked the females physically, but instead often emitted herding sounds to them. One subadult female was repelled by a resident adult female. When one adult female transferred into a new one-male group, she left her behind son in an all-male group. The number of females often fluctuated in most study groups, with this fluctuation being more prominent among subadult females than adult females. It is likely that female transfer in proboscis monkeys is not a rare occurrence and that it is especially common among sub-adult females.
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.
The disjunct distribution of Presbytis femoralis subspecies across Sumatra (P. f. percura), southern (P. f. femoralis) and northern (P. f. robinsoni) Peninsular Malaysia marks the unique vicariance events in the Sunda Shelf. However, the taxonomic positions and evolutionary history of P. f. femoralis are unresolved after decades of research. To elucidate this evolutionary history, we analyzed 501 base pairs of the mitochondrial HVSI gene from 25 individuals representing Malaysia's banded langur, with the addition of 29 sequences of Asian Presbytis from Genbank. Our results revealed closer affinity of P. f. femoralis to P. m. mitrata and P. m. sumatrana while maintaining the monophyletic state of P. f. femoralis as compared to P. f. robinsoni. Two central theses were inferred from the results; (1) P. f. femoralis does not belong in the same species classification as P. f. robinsoni, and (2) P. f. femoralis is the basal lineage of the Presbytis in Peninsular Malaysia. Proving the first hypothesis through genetic analysis, we reassigned P. f. femoralis of Malaysia to Presbytis neglectus (Schlegel's banded langur) (Schlegel in Revue Methodique, Museum d'Histoire Naturelle des Pays-Bas 7:1, 1876) following the International Code of Zoological Nomenclature (article 23.3). The ancestors of P. neglectus are hypothesized to have reached southern Peninsular Malaysia during the Pleistocene and survived in refugium along the western coast. Consequently, they radiated upward, forming P. f. robinsoni and P. siamensis resulting in the highly allopatric distribution in Peninsular Malaysia. This study has successfully resolved the taxonomic position of P. neglectus in Peninsular Malaysia while providing an alternative biogeographic theory for the Asian Presbytis.
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.
In animal husbandry, diets should help in maintaining a healthy body condition, support reproduction, and promote species-specific longevity. It is recommended to feed folivorous primates kept in zoos a high-fiber diet, i.e., leaves, although satisfying such a requirement is challenging in temperate regions because it is difficult to obtain fresh leaves, especially in autumn and winter. As equally important for their appropriate treatment, it is valuable to provide details of clinical reports of medical problems and pathological findings, although such clinical reports are rather limited. Therefore, in foregut-fermenting proboscis monkeys (Nasalis larvatus), we (1) described the individual clinical reports of renal disease and weight loss at the Yokohama Zoological Gardens in Japan, (2) determined the nutritional profile of the diets supplied to these animals because other potential triggers for their renal disease and weight loss could be excluded, (3) modified the diet regimen to minimize weight loss and the development of hypercalcemia and hypophosphatemia, and (4) assessed the effects of such dietary modification by comparing the body weight and the Ca and P concentrations and the Ca/P ratios in the blood before and after diet modification with a comparison of these measurements between zoo and free-ranging individuals. Based on the nutritional profile of the diets, we concluded that the reported cases of renal failure might be caused by consumption of leaves with a Ca/P ratio far above the appropriate level in autumn and winter. Additionally, the dietary modification of minerals and metabolizable energy achieved certain beneficial effects on zoo-kept proboscis monkeys.
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.
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.
The development of GPS tags for tracking wildlife has revolutionised the study of home ranges, habitat use and behaviour. Concomitantly, there have been rapid developments in methods for estimating habitat use from GPS data. In combination, these changes can cause challenges in choosing the best methods for estimating home ranges. In primatology, this issue has received little attention, as there have been few GPS collar-based studies to date. However, as advancing technology is making collaring studies more feasible, there is a need for the analysis to advance alongside the technology. Here, using a high quality GPS collaring data set from 10 proboscis monkeys (Nasalis larvatus), we aimed to: 1) compare home range estimates from the most commonly used method in primatology, the grid-cell method, with three recent methods designed for large and/or temporally correlated GPS data sets; 2) evaluate how well these methods identify known physical barriers (e.g. rivers); and 3) test the robustness of the different methods to data containing either less frequent or random losses of GPS fixes. Biased random bridges had the best overall performance, combining a high level of agreement between the raw data and estimated utilisation distribution with a relatively low sensitivity to reduced fixed frequency or loss of data. It estimated the home range of proboscis monkeys to be 24-165 ha (mean 80.89 ha). The grid-cell method and approaches based on local convex hulls had some advantages including simplicity and excellent barrier identification, respectively, but lower overall performance. With the most suitable model, or combination of models, it is possible to understand more fully the patterns, causes, and potential consequences that disturbances could have on an animal, and accordingly be used to assist in the management and restoration of degraded landscapes.
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.
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.
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.
The choice of a sleeping site is crucial for primates and may influence their survival. In this study, we investigated several tree characteristics influencing the sleeping site selection by proboscis monkeys (Nasalis larvatus) along Kinabatangan River, in Sabah, Malaysia. We identified 81 sleeping trees used by one-male and all-male social groups from November 2011 to January 2012. We recorded 15 variables for each tree. Within sleeping sites, sleeping trees were taller, had a larger trunk, with larger and higher first branches than surrounding trees. The crown contained more mature leaves, ripe and unripe fruits but had vines less often than surrounding trees. In addition, in this study, we also focused on a larger scale, considering sleeping and non-sleeping sites. Multivariate analyses highlighted a combination of 6 variables that revealed the significance of sleeping trees as well as surrounding trees in the selection process. During our boat surveys, we observed that adult females and young individuals stayed higher in the canopy than adult males. This pattern may be driven by their increased vulnerability to predation. Finally, we suggest that the selection of particular sleeping tree features (i.e. tall, high first branch) by proboscis monkeys is mostly influenced by antipredation strategies.
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.