Niche separation of sympatric macaques, Macaca assamensis and M. mulatta, in limestone habitats of Nonggang, China

Comparative studies of sympatric species are essential in understanding those species’ behavioral and ecological adaptations as well as the mechanisms that can reduce resource competition enough to allow coexistence. We collected data on diet, activity budget and habitat use from two sympatric macaque species, the Assamese macaque (Macaca assamensis) and the rhesus macaque (M. mulatta), in a limestone seasonal rainforest of Nonggang Nature Reserve, southwestern Guangxi, China. Our results show that the two sympatric macaques differ in diet, activity budget, and habitat use: (1) out of the 131 plant species that were used by both macaque species as food over the year, only 15 plant species (11 %) were shared. Rhesus macaques used more plant species as major foods, and had higher dietary diversity and evenness indexes than Assamese macaques. (2) Assamese macaques fed predominantly on leaves, whereas rhesus macaques fed more selectively on fruits. The rhesus macaques’ diet varied according to season, and was significantly correlated to season fluctuation in fruit availability. (3) Assamese macaques devoted more time to resting, and less time to feeding than rhesus macaques (4) Assamese macaques were present mostly on the cliff, and tended to stay on the ground, whereas rhesus macaques were present mostly on the hillside, and showed preference to lower and middle canopy. The observed differences in diet and habitat use between the two macaque species represent behavioral patterns enabling their coexistence.     

Comparison of locomotor behaviour between white-headed langurs Trachypithecus leucocephalus and Francois' langurs T.fran(c)oisi in Fusui, China

We studied the locomotor behaviour of white-headed langurs Trachypithecus leucocephalus and Fran(c)ois' langurs T.fran(c)oisi to test two hypotheses: (1) these monkeys have evolved locomotor ability to support their activities on limestone hills,and (2) Fran(c)ois' langurs have evolved more diverse locomotor skills than white-headed langurs. Data were collected from 1996 - 1998 and in 2005 in Fusui Nature Reserve,Guangxi,and showed that the two species had similar locomotor types,but Francois' langurs had more locomotor modes (26) than white-headed langurs (12). Quadrupedal walking and leaping were two major types,and white-headed langurs were more arboreal than Fran(c)ois' langurs. We suggest that,while keeping their ancestral locomotor types,the two species have evolved new types allowing them to live on limestone cliffs. Compared to white-headed langurs,Francois' langurs have more diverse locomotor modes that probably have allowed them to live in more habitat types. As an evolutionary outcome,Fran(c)ois' langurs have a larger distribution range.     

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.     

喀斯特石山生境中熊猴的雨季食物组成

开展食物组成研究为人们了解灵长类对栖息地的反应提供了很好的途径,对深刻理解动物的行为可塑性及适应性具有重要意义。猕猴属(Macaca)为果食性灵长类,但是不同种类的食性差异很大;即使便同一物种,其不同地理种群也因其栖息环境不同,食物组成存在差异。一般说来,热带地区的种类比生活在较高纬度的种类采食更多的果实。于2012年7—9月,采用瞬时扫描法对广西弄岗自然保护区石山中的两群熊猴(Macaca assamensis)进行了跟踪和观察,对猴群的雨季食物组成及其日时段变化规律进行了研究。结果表明:研究期间熊猴共采食45种植物,其中乔木30种,灌木3种,藤本11种,草本1种。平均每月采食植物22.3种。嫩叶和果实是熊猴的主要食物,分别占食物组成的52.4%和46.1%(其中未成熟果实占21.3%,成熟果实占24.8%)。另外,花占食物组成的0.9%,成熟叶和其它部位分别占0.3%。石山特有植物芸香竹(Bonia saxatilis)的嫩叶提供了43.8%的食物。9种主要植物分别占食物组成的2%,共为猴群提供了85.5%的食物。分析还发现熊猴并不是严格按照环境中的植物生物量来选择食物。嫩叶在弄岗熊猴的食物中的比例高于其他地理种群,而果实低于其他地理种群,这可能与喀斯特石山中果实的丰富度和可利用性较低有关。熊猴一天中不同时间段的食物组成并不相同,主要表现在:熊猴上午时间段对成熟果实和总果实的采食比例高于下午时间段,而嫩叶的采食比例低于下午时间段。另外,不同时间段的食物组成受外界温度的影响,表现为温度与嫩叶的觅食比例成正比,与成熟果实和总果实的觅食比例成反比。这可能与猴群采取的能量平衡策略有关。对熊猴的食物组成的日时段变化规律进行首次报道,研究结果将有助于深入理解熊猴对喀斯特石山生境的适应策略。     

Interannual variation in food choice of white‐headed langur inhabiting limestone forests in Fusui,southwest Guangxi,China

Food habits are important factors in the adaptation of wild nonhuman primates. White‐headed langurs (Trachypithecus leucocephalus) are endemic to heavily fragmented limestone forests and adapt to unique living environments via flexible food selection strategies. In this study, we compared the dietary data for white‐headed langurs living in Chongzuo White‐headed Langur National Nature Reserve in 2013 and 2016 to evaluate interannual variations in diet. Our results indicated that young leaves were the main food source for langurs, accounting for 52.4% (SD 25.4%) and 65.2% (SD 22.4%) of their diet in 2013 and 2016, respectively. The pattern of plant part consumption was similar between the two years. The consumption of young leaves varied with the availability of young leaves, whereas the consumption of mature leaves was negatively correlated with young leaf availability. The consumption of plant species and diet diversity were higher in 2013 than in 2016. In both 2013 and 2016, although diet diversity varied with the consumption of mature leaves, it was negatively correlated with the consumption and availability of young leaves. Dietary interannual variation is likely to either be linked to phenological variations or indicate that white‐headed langurs have a flexible ecological adaptation coping with habitat fragmentation.     

Nutrient contents predict the bamboo‐leaf‐based diet of Assamese macaques living in limestone forests of southwest Guangxi,China

Determining the nutrient factors influencing food choice provides important insight into the feeding strategy of animals, which is crucial for understanding their behavioral response to environmental changes. A bamboo‐leaf‐based diet is rare among mammals. Animals’ food choice and nutritional goals have been explained by several frameworks; however, the influence of nutrients on food choice in bamboo‐leaf‐based macaques is not yet available. Assamese macaques (Macaca assamensis) inhabiting limestone forests are characterized by such a bamboo‐leaf‐based diet, predominantly consuming young leaves of Bonia saxatilis, a shrubby, karst‐endemic bamboo. We studied the feeding behavior of one group of Assamese macaques using instantaneous scan sampling in limestone forests of the Guangxi Nonggang National Nature Reserve in southwest Guangxi, China. We compared the nutrient content of staple food and nonfood items and examine the role of key nutrients in the food selection of macaques. Our results showed that young leaves of bamboo B. saxatilis contained more water, crude protein, phosphorus, and less tannin than nonfood items. Furthermore, staple foods contained a higher content of water and less content of calcium than nonfood items. More specifically, quantities of water, crude protein, calcium, and phosphorus in food items were critical factors affecting feeding time on a specific plant item. Our results suggest that young bamboo leaves could meet macaques’ required protein and water intake, while enabling them to maintain their mineral balance, consequently facilitating to maintain the primates’ bamboo‐leaf‐diet in the limestone forest. Our findings confirm the effects of nutrient contents in food choice of Assamese macaques, highlighting the importance of the nutrient contents in maintaining their bamboo‐based diet and the need to increase the knowledge on their nutritional strategy adapted to the bamboo‐dominated diet inhabiting the unique limestone habitat.     

贵州麻阳河自然保护区黑叶猴利用洞穴的观察

非人灵长类利用洞穴是非常稀少的现象。2003年11—12月和2004年初在贵州麻阳河自然保护区观察到黑叶猴(Trachypithecusfranoisi)有利用洞穴的现象。白天有二群(分别为10和14只)在栖息地附近活动,黄昏前回到悬崖边几个喀斯特地形山洞中的一个洞。躲避风雨等不良的气候条件、获得矿物质、安全等因素可能是黑叶猴利用洞穴的原因。     

Resource partitioning in sympatric langurs and macaques in tropical rainforests of the central Western Ghats, south India

In a competitive sympatric association, coexisting species may try to reduce interspecific interactions as well as competition for similar resources by several ecological and behavioral practices. We studied resource utilization of three sympatric primate species namely, lion-tailed macaques (Macaca silenus), bonnet macaques (M. radiata) and Hanuman langurs (Semnopithecus entellus) in a tropical rainforest of the central Western Ghats, south India. We studied resource use, tree-height use, foraging height, substrate use when consuming animal prey and interspecific interactions. The results revealed that across the year, there was very limited niche overlap in diet between each species-pair. Each primate species largely depended on different plant species or different plant parts and phenophases from shared plant species. Primate species used different heights for foraging, and the two macaque species searched different substrates when foraging on animal prey. We also recorded season-wise resource abundance for the resources shared by these three primate species. While there was low dietary overlap during the dry season (a period of relatively low resource abundance), there was high dietary overlap between the two macaque species during the wet season (a period of high resource abundance for the shared resources). We observed only a few interspecific interactions. None of these were agonistic, even during the period of high niche overlap. This suggests that the sympatric primate species in this region are characterized by little or no contest competition. Unlike in some other regions of the Western Ghats, the lack of interspecific feeding competition appears to allow these primates, especially the macaques, to remain sympatric year-round.     

Factors Influencing Interannual and Intersite Variability in the Diet of <Emphasis Type="Italic">Trachypithecus francoisi</Emphasis>

Comparative studies of the diet of the same species in different habitats, and over the long term, are essential to understanding a species’ behavioral and ecological plasticity. Moreover, such studies can help researchers and managers evaluate a species’ capacity to cope with changes in habitat quality resulting from natural processes or human disturbance, which is important for developing conservation strategies. We compared dietary data for François’ langur (Trachypithecus francoisi) collected at Nonggang and Fusui Nature Reserves, Guangxi Province, China, over 2 separate study periods to evaluate interannual and intersite variation in diet. Young leaves were the preferred staple foods for langurs, whereas mature leaves and seeds served as fallback foods in response to seasonal shortage in the abundance of young leaves. Species composition of the diets and the percentage of feeding records for plant species varied between the 2 study periods. The langurs at both study sites fed selectively, and they did not base their diet simply on the abundance of plant species in the habitat. However, the plant species eaten by langur groups inhabiting the 2 different reserves were markedly different, and the top 10 food species eaten by the Fusui group showed no overlap with those eaten by the Nonggang group. The variation may be related to differences in forest composition resulting from different level of human disturbance. In summary, our results indicate that François’ langurs exhibit a comparable dietary pattern both temporally and geographically, but there is marked interannual and intersite difference in species composition of the langur diet.     

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.     

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...     

Diet of <Emphasis Type="Italic">Pygathrix nigripes</Emphasis> in Southern Vietnam

Black-shanked douc langurs (Pygathrix nigripes) are Southeast Asian colobines about which primatologists know very little, but they are classed as endangered because of population decline due to habitat loss. Two preliminary studies have shown that this monkey is primarily folivorous, but there are few details of plant selection or seasonal changes in diet. We set out to observe douc langurs directly in the wild to quantify the diet during wet and dry seasons. We confirmed that the species relies on foliage throughout the year, but it includes significant proportions of fruit and flowers in its diet when those items are available. The douc langurs selected various parts from 152 species of plants in 2 national parks, but there did not appear to be favorite species that were heavily selected over others. In both the wet and dry seasons, the black-shanked douc langurs ate mostly leaves, but the diversity of plants consumed increased and the proportion of fruit eaten almost doubled in the wet season. There were diurnal shifts in food selection, but we found no evidence that the douc langurs were foraging strategically to maximize their protein or energy intake.     

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.     

Distribution of Assamese macaques (Macaca assamensis) in the Inner Himalayan region of Bhutan and their mtDNA diversity

The distributions of Assamese macaques (Macaca assamensis) and rhesus macaques (M. mulatta) in Bhutan have been only partially documented. In order to investigate the distribution patterns of these species, we conducted field observation and genetic assessment with mitochondrial DNA (mtDNA) typing of macaques in the Inner Himalayas of Bhutan. There were 24 sightings of macaque groups, and all were visually identified as Assamese macaques. No groups of rhesus macaques were sighted in this survey area, in contrast with the survey results in the Nepalese Himalayas. Molecular phylogenetic analysis revealed that the Bhutan macaques are closer in proximity to their counterparts in the Indo-Chinese region (Thailand and Laos) than to rhesus macaques in China, Laos and India. However, clustering results suggested the marked differentiation of the macaques in Bhutan from the Assamese macaques in Indo-China. We tentatively conclude that the macaques of the Inner Himalayan regions in Bhutan are Assamese macaques and that they appear to be of a lineage distinct from Assamese macaques in the Indo-Chinese region (subspecies M. a. assamensis). The degree of mtDNA diversity suggests that the Assamese macaques in Bhutan are of a more ancient ancestry than M. a. assamensis, thereby supporting the speciation hypothesis of the expansion of a sinica-group of macaques from South Asia to Southeast and then to East Asia (Fooden; Fieldiana Zool 45:1–44, 1988). Assignment of Assamese macaques in Bhutan to M. a. pelops is premature due to the lack of molecular data and recent taxonomic controversy. The mtDNA diversity of Assamese macaques was greater than that of rhesus macaques, suggesting the earlier speciation of Assamese macaques. The significance of the ecogeographic segregation model of macaque distribution is discussed in relation to the evolutionary range expansion into the Himalayan regions in South Asia.     

桂林七星公园猕猴的食物组成及季节性变化

觅食是动物最重、最常见的行为,动物通过觅食获取其生长发育、繁殖和运动所需要的营养与能量.     

弄岗黑叶猴旱季食物营养组分及其对食物选择的影响

正蛋白质与纤维素的比值以及能量高低是影响灵长类动物食物选择的重要因素(Oftedal,1991;Waterman and Kool,1994;Chapman and Chapman,2002;Wasserman and Chapman,2003;Hanya et al.,2007;Huang et al.,2010),但它们是否影响疣猴的食物选择目前尚具有较大的争议。Waterman     

The diet of the capped langur (Presbytis pileata) in a moist deciduous forest in Bangladesh

Capped langurs (Presbytis pileata) in Madhupur National Park in north-central Bangladesh have an annual diet that is comprised largely of mature leaves (42% of 20,460 total feeding records). Among colobine monkeys, only some populations of red colobus (Procolobus badius) have a diet richer in mature leaves. New leaves (11%) and fruit (24%) are the other annually important dietary items. Seasonal breakdown of this diet, however, revealed that during the monsoon months of May through September theP. pileata diet is approximately 50% fruit, including pulpy ripe fruit. This is also the period of maximum fruit availability. Data on diet and food availability indicate that while capped langurs subsist on mature leaves during the dry season (80% of diet from November to March), they select fruit and new leaves and switch to these foods whenever they are available. These data support the hypothesis that the colobine feeding strategy is adapted to cope with seasonal food scarcity.     

Preliminary study of the genetic diversity of eastern Assamese macaques (Macaca assamensis assamensis) in Thailand based on mitochondrial DNA and microsatellite markers

Human overpopulation, deforestation, invasion of agricultural areas, and livestock are the primary causes for population fragmentation of wildlife. The distribution range of species of the genus Macaca is constantly decreasing and becoming increasingly fragmented due to forest deterioration. Assamese macaques (M. assamensis) are classified as near threatened in the International Union for Conservation of Nature (IUCN) Red List of Threatened Animals (2008) and have been declared a protected wildlife animal according to Wildlife Preservation and Protection Act, B.E.2535 (1992) of Thailand. As studies of the population history and genetic diversity of Assamese macaques in Thailand are currently lacking, we aimed at a first investigation of their genetic diversity based on mitochondrial DNA [hypervariable regions 1 and 2 (HV1, HV2) and cytochrome B (CYTB) regions], as well as 15 microsatellite markers of five sampling sites distributed across Thailand. Our results indicate that Assamese macaques in Thailand are diverse, with eight maternal haplotypes and a low inbreeding coefficient in the Phu Khieo Wildlife Sanctuary (PKWS) population. Moreover, our phylogenetic and median-joining network analysis based on mitochondrial (mt)DNA suggests a population distribution in accordance with the evolutionary scenario proposed for M. sinica. Today, the population of Assamese macaques is fragmented, and conservation strategies are needed to ensure the maintenance of genetic diversity of this primate species.     

三种笼养灵长类活动时间分配的比较研究

采用焦点动物法和连续记录法对3种笼养灵长类活动时间分配进行比较研究。结果表明,川金丝猴Rhi-nopithecus roxellanae和熊猴Macaca assamensis用于休息的时间多于猕猴Macaca mulatta,移动时间则相反;川金丝猴和猕猴用于理毛的时间多于熊猴。不同性别年龄组之间的活动时间分配有差异,主要表现在川金丝猴母亲用于理毛的时间明显多于成年儿子,用于玩耍的时间则相反;猕猴成年雄性的移动时间和理毛时间多于成年雌性,玩耍时间则少于成年雌性;熊猴成年雌性的移动时间多于成年雄性,与成年个体相比,幼体花更多的时间用于玩耍,而相应的减少了其休息时间。