Primate numts and reticulate evolution of capped and golden leaf monkeys (Primates: Colobinae)

A recent phylogenetic study of langurs and leaf monkeys of South Asia suggested a reticulate evolution of capped and golden leaf monkeys through ancient hybridization between Semnopithecus and Trachypithecus. To test this hybridization scenario, I analysed nuclear copies of the mitochondrial cytochrome b gene (numts) from capped, golden and Phayre’s leaf monkeys. These numts were aligned with mitochondrial cytochrome b sequences of various species belonging to the genera Semnopithecus and Trachypithecus. In the phylogenetic tree derived from this alignment, the numts fell into three distinct clades (A, B and C) suggesting three independent integration events. Clade A was basal to Semnopithecus, and clades B and C were basal to Trachypithecus. Among the numts in clades A and C were sequences derived from species not represented in their respective sister mitochondrial groups. This unusual placement of certain numts is taken as additional support for the hybridization scenario. Based on the molecular dating of these integration events, hybridization is estimated to have occurred around 7.1 to 3.4 million years ago. Capped and golden leaf monkeys might have to be assigned to a new genus to reconcile their unique evolutionary history. Additionally, northeast India appears to be a ‘hot spot’ for lineages that might have evolved through reticulate evolution.     

Molecular systematics and conservation of the langurs and leaf monkeys of South Asia

Numerous morphology-based classification schemes have been proposed for langurs and leaf monkeys of South Asia but there is very little agreement between them. An incorrect classification scheme when used as a basis for biogeographic studies can support erroneous hypotheses. Further, lack of taxonomic resolution will also confound conservation efforts, given that conservation biologists use traditional morphology-based-classification schemes to prioritize species for conservation. Here, I have revisited recent molecular phylogenetic studies done on langurs and leaf monkeys of South Asia. Results from these studies are in turn used to derive a rational and scientific basis for prioritizing species for conservation. Molecular data support the classification of langurs of the Indian subcontinent—Hanuman, Nilgiri and purple-faced langurs—in the genus Semnopithecus, whereas Phayre’s leaf monkey along with other Southeast Asian leaf monkeys form another distinct clade (Trachypithecus). The phylogenetic position of capped and golden langurs remains unresolved. Molecular data suggest that they are closely related to each other but this group might have evolved through past hybridization between Semnopithecus and Trachypithecus. Additionally, genetic data also support the splitting of the so-called Hanuman langurs into at least three species. The scores for taxonomic uniqueness of langurs and leaf monkeys of South Asia were revised using this molecular phylogeny-based classification. According to the revised scores, Phayres leaf monkey and golden langur are priority species for conservation followed by capped and Nilgiri langurs.     

Understanding primate‐human interaction: Socioeconomic correlates of local awareness and attitude toward the endangered golden langur Trachypithecus geei (Khajuria, 1956) in Bhutan

Despite the golden langur's (Trachypithecus geei) endangered and totally protected status, local awareness and attitude toward this species is poorly understood. We investigated local awareness and attitude in Bhutan by interviewing 1,143 households in the districts of Dagana, Sarpang, Trongsa, Tsirang, and Zhemgang, and analyzing data through a conditional inference tree analysis. Most respondents were not aware of the golden langur's nationally protected (53%; n = 604) and globally endangered status (64%; n = 730), but their location of residence (inside/outside a protected area; p < .001) and education level (p < .001) significantly influenced awareness. The majority of respondents (87%; n = 999) liked the golden langur but the attitude was significantly influenced primarily by whether or not they experienced crop damage by golden langurs (p < .001), and subsequently by location of residence (p < .001), local belief (p < .01), gender (p < .05), and personal encounter with a golden langur (p < .001). Socioeconomic variables like age, education level, and annual income did not influence attitude. We recommend environmental education and awareness campaigns outside protected areas, and intensifying existing programs inside protected areas to forge harmonious human‐golden langur coexistence.     

Status of Trachypithecus geei in a Rubber Plantation in Western Assam, India

Golden langurs (Trachypithecus geei) are an endangered species in a limited area of Northeast India and Bhutan. They are confined to a forest belt in western Assam between the Manas River in the east, Sankosh in the west and Brahmaputra in the south along the Indo-Bhutan border. Due to habitat destruction, their populations are restricted to fragmented forest pockets, especially in India. We compared data on an isolated population of golden langurs in the rubber plantation of Nayakgaon in the Kokrajhar district of Assam, May 2002 with an earlier census in 1997. We counted a total of 52 individuals in 3 troops in 2002. The average troop size is 17.3 (r = 7–26). The ratio of adult male to adult females is 1:3.16. Of the total population 9.6% were adult males, 21.1% were adult females, 17.3% subadult males, 7.7% subadult females, 19.2% juveniles and 25% infants. In 1997 Srivastava et. al., recorded 38 individuals in 5 troops with an average troop size of only 7.6 . Apparently troop fusion has occurred. The increased population is encouraging.     

Phylogenetic position of the langur genera <Emphasis Type="Italic">Semnopithecus</Emphasis> and <Emphasis Type="Italic">Trachypithecus</Emphasis> among Asian colobines,and genus affiliations of their species groups

Background  

The evolutionary history of the Asian colobines is less understood. Although monophyly of the odd-nosed monkeys was recently confirmed, the relationships among the langur genera Presbytis, Semnopithecus and Trachypithecus and their position among Asian colobines remained unclear. Moreover, in Trachypithecus various species groups are recognized, but their affiliations are still disputed. To address these issues, mitochondrial and Y chromosomal sequence data were phylogenetically related and combined with presence/absence analyses of retroposon integrations.     

Status and distribution of golden langurs (Trachypithecus geei) in Assam, India

The distribution of golden langurs (Trachypithecus geei) is limited to a small area of western Assam in northeast India and Bhutan between the rivers Manas in the east, Sankosh in the west, and Brahmaputra in the south. It is one of the most seriously endangered primate species of India. A comparative analysis based on satellite images taken in 1988 and 1998 showed a 50% loss of original golden langur habitat. Data on population dynamics collected using line transect and total count methods are presented here. An average group size of 8.2 (range 4.0-22.0) individuals was recorded. A total of 1,064 individuals were counted living in 130 groups. The sex ratio was 1.9-2.5 adult females for each adult male. A low percentage of juveniles and infants suggests that the population is unstable. Most of the groups had only one adult male. Small group sizes, isolated distribution, proportionately few infants and juveniles, and degrading habitat are all causes of concern. Demographic trends indicate a decline in the golden langur population.     

Reproductive Strategies of <Emphasis Type="Italic">Trachypithecus pileatus</Emphasis> in Arunachal Pradesh,India

We studied reproductive behavior of free-ranging capped langurs (Trachypithecus pileatus) in the Pakhui Wildlife Sanctuary, Arunachal Pradesh, India. Four species of primates —Trachypithecus pileatus, Macaca mulatta, M. assamensis, and Nycticebus bengalensis— live there. We studied the mating seasons, mating frequency, copulatory attempts, time spent in copulation, and interval between 2 successive copulations, gestation length, and interbirth interval of 4 groups of capped langurs during 2001–2003. We observed 2 mating seasons in a year. The first was larger, comprising 5 months (September–January), and the second was short, April and May. Mating was intensive in the morning session (0600–1000 h); 57% of total mating events occurred then. The average gestation period was 200 d. November was the most favorable month for breeding. In a year, 107 mating events occurred involving 5 adult females. Average time per mounting attempt is 12 s. Duration of mounting was the maximum in November. Interbirth interval was 23 months and 10 d. The birth season was 129 days, December–April; 53% of births occurred in February and March. Average birth rate is 0.386 birth/female/yr.     

Food Choice of White-Headed Langurs in Fusui,China

We studied the feeding ecology of white-headed langurs (Trachypithecus leucocephalus) from September 1997 to September 1998 in Fusui Rare and Precious Animal Reserve, SW Guangxi, China. We collected data in the central part of a group of limestone hills where the main population pool of langurs was located. The langurs fed on 50 plant species (belonging to 42 genera from 28 families) out of 164 species in the habitat (belonging to 112 genera from 48 families). Most of the food plant species were not common in the habitat. There are 16 important food species, including 6 key species. White-headed langurs were extremely folivorous, feeding mainly on young leaves (75% of total feeding records) of a broad range of less common plant species, which were in less disturbed areas. Thus, langur groups in high quality habitat had greater access to preferred foods, and the future of langurs in the Reserve may depend on immediate cessation of tree felling.     

Molecular phylogeny and biogeography of langurs and leaf monkeys of South Asia (Primates: Colobinae)

The two recently proposed taxonomies of the langurs and leaf monkeys (Subfamily Colobinae) provide different implications to our understanding of the evolution of Nilgiri and purple-faced langurs. Groves (2001) [Groves, C.P., 2001. Primate Taxonomy. Smithsonian Institute Press, Washington], placed Nilgiri and purple-faced langurs in the genus Trachypithecus, thereby suggesting disjunct distribution of the genus Trachypithecus. [Brandon-Jones, D., Eudey, A.A., Geissmann, T., Groves, C.P., Melnick, D.J., Morales, J.C., Shekelle, M., Stewart, C.-B., 2003. Asian primate classification. Int. J. Primatol. 25, 97-162] placed these langurs in the genus Semnopithecus, which suggests convergence of morphological characters in Nilgiri and purple-faced langurs with Trachypithecus. To test these scenarios, we sequenced and analyzed the mitochondrial cytochrome b gene and two nuclear DNA-encoded genes, lysozyme and protamine P1, from a variety of colobine species. All three markers support the clustering of Nilgiri and purple-faced langurs with Hanuman langur (Semnopithecus), while leaf monkeys of Southeast Asian (Trachypithecus) form a distinct clade. The phylogenetic position of capped and golden leaf monkeys is still unresolved. It is likely that this species group might have evolved due to past hybridization between Semnopithecus and Trachypithecus clades.     

Food Items Consumed by White-headed Langurs in Fusui, China

We studied the socioecology of white-headed langurs (Trachypithecus leucocephalus) from September 1997 to September 1998 in Fusui Precious Animal Reserve, SW Guangxi, China. We collected data on climate, phenology of food plant species, and foods consumed by langurs living in habitats with different levels of human disturbance. Feeding records showed that the most food is from less common plant species. Young leaves were the staple food item in all langur groups, and consumption correlates with availability. Consumption of mature leaves is not significantly correlated with their availability, but the langurs fed on them, and other food items such as fruits and seeds, when the availability of young leaves was low. Langurs in different areas had broadly similar diets, but they varied most in the proportion of supplementary items such as fruit. Groups in more disturbed habitat did not increase the overall proportion of mature leaves in their diet, but instead maintained their intake of young leaves from a greater diversity of species, and incorporated more immature fruit. Conservationists should direct efforts toward protection of rare plant species providing preferred food items, particularly supplementary foods at times when, and in areas where, preferred food items are less available.     

Habitat Quality and Activity Budgets of White-Headed Langurs in Fusui,China

Within a species, habitat quality may be a factor causing different activity budgets between populations. The habitat of white-headed langurs (Trachypithecus leucocephalus) has been seriously disturbed in Fusui Rare and Precious Animal Nature Reserve, China, where we carried out a study of their socioecology from September 1997 to September 1998. We collected data on langur activity budgets from the main population located in the central part of a group of limestone hills. We classified habitat quality into 4 grades according to the extent of human disturbance. We showed that the two main study groups of white-headed langurs spent on average 50% of time resting, 13% feeding, 18% moving (including foraging), 11% grooming, and 7% playing. Langur time budgets showed no significant seasonal change, but they differed among different sex-age classes. Infants and juveniles spent about 20.3% of time playing, whereas adults spent only 0.2% playing. The group in high quality habitat engaged less in feeding and more in playing than the group in low quality habitat did. Habitat quality influenced the playing time of young white-headed langurs and may be vital to their successful maturation.     

Diet of the Delacour's langur (Trachypithecus delacouri) in Van Long Nature Reserve,Vietnam

The six limestone langur taxa of Southeast Asia inhabit the rugged limestone karst mountains, although the reason for their current restriction to this habitat is unclear. From August 2007 to July 2008, I collected data on the diet and feeding behavior of the critically endangered Delacour's langur (Trachypithecus delacouri) in Van Long Nature Reserve, Vietnam. I used these data to evaluate the hypothesis that limestone langurs are found on karst habitat because they depend on endemic limestone plants. Feeding accounted for 29% of the langurs' activity budget. Young leaves dominated the diet monthly, seasonally, and annually. The annual diet consists of nearly 79% foliage with almost 60% young leaves. Despite a distinct wet and dry season, over the study period, seasonal variation in plant part consumption was slight. Fruit and seeds were a small contribution to the diet. Delacour's langurs ate 42 of 145 available species, and they concentrated on a subset of this number. Five plant species comprised more than 60% of the diet and 16 species comprised more than 93%. More than half of the diet came from climbers. Delacour's langurs are among the most highly folivorous of studied colobines and, along with the closely related T. leucocephalus of southern China, the most folivorous of the Asian langurs. Whether high folivory is owing to a lack of available fruits and seeds in limestone habitats is unknown. What is certain, however, is that the plant species most important in the Delacour's langurs' diet at VLNR, throughout the study, were not plants endemic to limestone. Feeding dependence alone, therefore, cannot explain the current distribution of limestone langurs on karst habitat. Am. J. Primatol. 72:317–324, 2010. © 2009 Wiley‐Liss, Inc.     

Further observations on the golden langur (Presbytis geei Khajuria, 1956), with a note to capped langur (Presbytis pileatus Blyth, 1843) of Assam

In continuation of the field work that was initiated in the summer of 1973 another field trip to the same area of Goalpara district was undertaken in the winter of 1973 and later on a survey of Manas sanctuary was made in winter of 1976 to collect further information about golden langur. This report incorporates the results of these two field studies and includes such information as the characteristics of the study area, total number of langur groups observed, their size and composition, food items utilised by them during winter months, inter-group and inter-specific relationships, etc. It also includes, incidentally, observations of the capped langur in the Manas sanctuary and remarks on allopatry of distribution of golden and capped langurs in this sanctuary. The range of distribution of golden langur on the Indian side and present status and future of these monkeys have been discussed. The social organisation of the golden langur has been compared with that of other langurs and the concentrations of the former in Jamduar and Raimona forests during the winter months have been compared with those in summer months.     

Gut microbiome,diet, and conservation of endangered langurs in Sri Lanka

Understanding the mechanisms by which organisms respond to environmental change is critical to conservation biology. Recent research indicates that the gut microbiome may mediate mammalian responses to the environment and can be used as a biomarker to understand host ecological strategies. Here, we explore the relationship between the gut microbiome, host dietary niche, and potential resilience to habitat alteration using two closely related, sympatric non-human primate species: the tufted gray langur (Semnopithecus priam) and the purple-faced langur (Semnopithecus vetulus). The gray langur is suspected to be a habitat generalist less perturbed by anthropogenic disturbance, while the purple-faced langur is suspected to be a specialist more sensitive to disturbance. To test these characterizations, we assessed the gut microbiome using 16S rRNA gene amplicon sequencing of fecal samples collected from Kaludiyapokuna Forest Reserve, Sri Lanka (gray langur n = 50 samples, purple-faced langur n = 7 samples). Our results demonstrate that despite strong gut microbial similarities, gray langurs had a more diverse gut microbiome that harbored Prevotella and Akkermansia, taxa involved in starch degradation, while the purple-faced langur gut microbiome harbored Roseburia, Clostridium, and Ruminococcus, taxa involved in processing plant structural carbohydrates. Compared to related species in other locations, both Sri Lankan langurs harbored more pathogenic bacteria. These differences suggest that gray langurs have more generalist diets, making them more resilient to anthropogenic change, but also indicate that they are not impervious to human encroachment. Our findings suggest that microbiome analyses are an important tool for langur ecology and conservation, and should be integrated into ongoing studies.     

广西扶绥白头叶猴对栖息地的选择与利用

为了解白头叶猴（Trachypithecus leucocephalus）的栖息地利用规律及其影响因素,2016年2月至2017年1月,采用瞬时扫描取样法对广西崇左白头叶猴国家级自然保护区一群白头叶猴的栖息地利用进行了研究。结果表明,白头叶猴对山体不同部位的利用存在显著性差异（χ² =39.467,df=3,P<0.001）,其中,对崖壁（56.75±9.55）%的利用比例最大,其次是对山坡（39.42±10.93）%和山顶（2.98±2.54）%的利用,而对山脚（0.84±1.47）%的利用频率最低。白头叶猴对不同微生境类型的利用存在差异（χ²=27.709,df=3,P<0.001）,其中对乔木（49.37±12.31）%的利用比例最大,其次是裸岩（24.05±13.61）%,随后依次为藤本（15.48±8.01）%和灌木（10.87±5.45）%。白头叶猴主要在山坡上觅食,利用崖壁移动、休息,进行社会活动;主要利用裸岩进行社会活动,觅食、移动、休息主要发生在乔木上。从整体来看,白头叶猴在雨季对乔木的利用频率显著大于旱季（Z=-2.680,n=12,P=0.007）;雨季在山坡觅食频率显著大于旱季（Z=-2.517,n=12,P=0.012）,而在崖壁觅食频率刚好相反（Z=-2.842,n=12,P=0.004）;白头叶猴雨季在乔木休息的频率显著大于旱季（Z=-2.355,n=12,P=0.019）。白头叶猴对栖息地的利用受到温度的影响。白头叶猴对乔木的总体利用频率随着平均温度的升高而增加（r=0.664,n=12,P=0.018）;觅食时,对崖壁、裸岩的利用频率均与平均温度成负相关关系（崖壁：r=-0.685,n=12,P=0.014;裸岩：r=-0.600,n=12,P=0.039）;休息时,对乔木的利用频率与平均温度呈正相关关系（r=0.650,n=12,P=0.022）。不同季节,白头叶猴对栖息地的利用方式不同。白头叶猴的栖息地利用模式可能是在觅食利益和捕食风险之间作出的权衡,并受到环境温度的影响。     

Distribution and Population Densities of Diurnal Primates in the Karst Forests of Phong Nha – Ke Bang National Park,Quang Binh Province,Central Vietnam

We studied the status and distribution of the diurnal primates in the Phong Nha – Ke Bang National Park (PNKB NP) from April to August 2007. In the past, researchers reported 9 primate species and subspecies for the karst forests of PNKB NP, which constitutes the most important protected area for the endangered Hatinh langur (Trachypithecus hatinhensis) in Vietnam. All 9 primate taxa are threatened due to hunting pressure and habitat loss. We applied line transect sampling in 4 areas. During a total of 117 transect inspections along 12 different transect routes, we confirmed 5 primate taxa and the analysis of population densities resulted in 2143 (±467) Hatinh langurs, 1316 (±871) red-shanked douc langurs (Pygathrix nemaeus), 930 (±489) stump-tailed macaques (Macaca arctoides), 986 (±883) eastern Assamese macaques (M. a. assamensis), and 18 (±18) southern white-cheeked crested gibbons (Nomascus siki) in the whole PNKB NP, which covers an area of ca. 85,000 ha. We could not detect the 2 nocturnal lorises, Bengal slow lorises (Nycticebus bengalensis) and pygmy slow lorises (N. pygmaeus), as well as rhesus macaques (Macaca mulatta) and northern pig-tail macaques (M. leonina). The distribution of the primates predominantly depended on human impact. We could not recognize a correlation between habitat constitution and abundance of primates. The population density estimates showed a much higher density of the Hatinh langur than previously assumed. Thus the importance of the PNKB NP for the conservation of this endangered langur increased significantly.     

Diet and Food Choice of Trachypithecus francoisi in the Nonggang Nature Reserve, China

We studied the diet and food choice of 1 group of Fran?ois’ langurs (Trachypithecus francoisi) from August 2003 to July 2004 in the Nonggang Nature Reserve, Guangxi province, China. The langurs consumed 90 plant species, including 14 unidentified species. Leaves constituted 52.8% of the diet (38.9% young leaves and 13.9% mature leaves). Fruits and seeds accounted for 17.2% and 14.2%, respectively. Flowers and other items—including petioles, stems, roots, and bark—contributed to 7.5% and 7.4% of the diet, respectively. The langur diet varied according to season. They fed on more young leaves from April to September. Consumption of seeds, petioles, and stems increased between October and March, when young leaves were scarce. The diet shift corresponded to higher dietary diversity during the young leaf-lean period. Though the langurs fed on many plant species, 10 species accounted for 62.2% of the diet, only 2 of which were among the 10 most common tree species in vegetation quadrants, and the percentage of feeding records on a plant species and the percentage of individuals of the species in vegetation quadrants does not correlate significantly. Fran?ois’ langurs fed selectively, and they did not base their diet simply on the abundance of plant species in the habitat.     

Seasonal Variation in the Activity and Dietary Budgets of Cat Ba Langurs (<Emphasis Type="Italic">Trachypithecus poliocephalus</Emphasis>)

Primate activity budgets are dictated by food availability and distribution; thus primates living in seasonal environments must adapt their behaviors to accommodate fluctuations in resources. Cat Ba langurs (Trachypithecus poliocephalus), a Critically Endangered Asian colobine and a member of the limestone langur group (francoisi superspecies group within genus Trachypithecus), live only in fragmented and disturbed habitats on Cat Ba Island, northeastern Vietnam. This study aimed to assess the behaviors and diet of Cat Ba langurs by group, age, sex, and season. We predicted they would have high rates of inactivity and foraging, low rates of social behaviors, with seasonal variation that reflects an energy-maximizing strategy. We conducted behavioral observations through scan sampling over an 11-month period and found that Cat Ba langurs spent a significant portion of their day inactive (57 %) followed by foraging (18 %), socializing (13 %), locomoting (10 %), and engaging in “other” behaviors (2 %). Their diet was made up primarily of leaves (83 %) followed by flowers (8 %), fruit (6 %), and stems (3 %). We found groups to differ in diet and activity, which is likely owing to differences in demographics and home range between groups. Seasonally, the animals ate more leaves and spent more time foraging in the dry season than the wet season, suggesting that they are energy maximizers. Cat Ba langurs have activity and dietary budgets similar to those of other limestone langurs, and respond to a presumed seasonal fluctuation in food availability similarly.     

中国石山叶猴生态学研究进展

喀斯特石山是一类特殊环境,生存在喀斯特石山的动物形成特殊的行为机制以适应这一特殊的环境.石山叶猴是仅分布于喀斯特石山地区的珍稀濒危灵长类动物,属疣猴亚科乌叶猴属的一个种组,包括黑叶猴(Trachypithecus francoisi)、白头叶猴(T.leucocephalus)、德氏叶猴(T.delacouri)、金头...     

Are Limestone Hills a Refuge or Essential Habitat for White-Headed Langurs in Fusui,China?

We studied the ecology of white-headed langurs (Trachypithecus leucocephalus) in Fusui Precious Animal Reserve, Guangxi, China, in 1997/1998 and conducted surveys of them in 1996–1997 and 2003. We collected data on vegetation fragments and the activities of white-headed langurs at different levels on limestone hills. The langurs selected less fragmented habitats with less human disturbance. They spent ca. 60% of the day at lower levels of the hills during maintenance activities, including feeding. When humans were absent, the langurs even came to the ground. The hills themselves were used as a refuge from human disturbance but were not otherwise essential habitat. Results of this study have implications for improving conservation management for the langurs.