Ranging behavior of eastern hoolock gibbon (Hoolock leuconedys) in a northern montane forest in Gaoligongshan,Yunnan, China

Generally, food abundance and distribution exert important influence on primate ranging behavior. Hoolock gibbons (genus Hoolock) live in lowland and montane forests in India, Bangladesh, Myanmar and China. All information about hoolock gibbons comes from studies on western hoolock gibbons (Hoolock hoolock) living in lowland forest. Between August 2010 and September 2011, we studied the ranging behavior of one habituated group of eastern hoolock gibbon (H. leuconedys) living in a seasonal montane forest in Gaoligongshan, Yunnan, China. Results show that the study group did not increase foraging effort, calculated in this study as the daily path length, when fruit was less available. Instead, the gibbons fed more on leaves and decreased traveling to conserve energy. They relied heavily on a single food species in most study months which was patchily distributed within their total (14-month) home range, and during most months they used only a small portion of their total home range. In order to find enough food, the group shifted its monthly home range according to the seasonal availability of food species. To satisfy their annual food requirements, they occupied a total home range of 93 ha. The absence of neighboring groups of gibbons and the presence of tsaoko cardamom (Amomum tsaoko) plantations may also have influenced the ranging behavior of the group. Further long-term studies of neighboring groups living in intact forests are required to assess these effects.     

Effects of cold weather on the sleeping behavior of Skywalker hoolock gibbons (Hoolock tianxing) in seasonal montane forest

Considering the high energetic costs of maintaining constant body temperature, mammals must adjust their thermoregulatory behaviors in response to cold temperatures. Although primate daytime thermoregulation is relatively well studied, there is limited research in relation to nighttime strategies. To investigate how Skywalker hoolock gibbons (Hoolock tianxing) cope with the low temperatures found in montane forests, we collected sleep‐related behavior data from one group (NA) and a single female (NB) at Nankang (characterized by extensive tsaoko plantations) between July 2010 and September 2011, and one group (BB) at Banchang (relatively well‐managed reserve forest) between May 2013 and May 2015 in Mt. Gaoligong, Yunnan, China. The annual mean temperature was 13.3°C at Nankang (October 2010 to September 2011) and 13.0°C at Banchang (June 2013 to May 2015) with temperatures dropping below ?2.0°C at both sites, making them the coldest known gibbon habitats. The lowest temperatures at both sites remained below 5.0°C from November to March, which we, therefore, defined as the “cold season”. The hoolock gibbons remained in their sleeping trees for longer periods during the cold season compared to the warm season. Sleeping trees found at lower elevations and closer to potential feeding trees were favored during cold seasons at both sites. In addition, the gibbons were more likely to huddle together during cold seasons. Our results suggest that cold temperatures have a significant effect on the sleeping behavior of the Skywalker hoolock gibbon, highlighting the adaptability of this threatened species in response to cold climates.     

Antipredation Sleeping Behavior of Skywalker Hoolock Gibbons (<Emphasis Type="Italic">Hoolock tianxing</Emphasis>) in Mt. Gaoligong,Yunnan, China

Studying sleeping behavior can provide key information for understanding the ecology of a species. Antipredation is an important factor that affects primate sleeping behavior. We studied antipredation sleeping behavior in skywalker hoolock gibbons (Hoolock tianxing). We studied one group (NA) and a solitary female (NB) at Nankang from July 2010 to September 2011, and another group (BB) at Banchang from May 2013 to December 2014 in Mt. Gaoligong, Yunnan, China. Over the study period, we recorded 67 sleeping trees for members of group NA over 92 days, 17 trees for the solitary female NB over 22 days, and 159 trees for members of group BB over 186 days. Skywalker hoolock gibbons at both sites rarely used the same tree on consecutive days (N = 3 at both sites). They traveled fast to enter sleeping tree a mean of 160 ± SD 43 min before sunset at Nankang, and a mean of 192 ± SD 40 min before sunset at Banchang. They seldom (Nankang: 14%, N = 183 observations; Banchang: 25%, N = 548 observations) defecated in sleeping trees. They slept at sites with more tall and large trees and preferred to sleep on tall trees in the site. They slept on branches of small diameter and closer to tree tops. Our study suggests that antipredation plays an important role in skywalker hoolock gibbons’ sleeping tree selection and sleeping behavior. In addition, our data suggest potential effects of habitat degradation on gibbons’ sleeping behavior. Tall trees are especially important for gibbons in degraded forest and should be protected.     

Habitat Characteristics of the Endangered Hoolock Gibbons of Bangladesh: The Role of Plant Species Richness

Hoolock gibbons ( Hoolock hoolock ) are endangered small apes occurring in Bangladesh, India, Myanmar, and south China. All known populations have undergone declines primarily due to habitat destruction or alteration. We examined the influence of area of natural forests, area of plantations, area of agricultural land and edible plant species richness on the hoolock gibbon numbers from 22 sites in Bangladesh using multiple regression analysis. Area of natural forests and plantations were not linked to hoolock gibbon numbers, whereas area of agricultural land and edible plant species richness were both significantly linked. Higher edible plant species richness was directly related to hoolock gibbon numbers, while the area of agricultural land was inversely related. This is the first quantitative study illustrating the importance of these two variables with hoolock gibbon numbers. We also analyzed the existing habitat characteristics in two of the largest hoolock gibbon populations in Bangladesh: Lawachara (42 individuals) and Kaptai (84 individuals). Trees in Lawachara were generally smaller compared to those in Kaptai. Artocarpus , Tectona , and Dipterocarpus were the three most important genera in both sites, although Artocarpus was more important in Lawachara. Each site also had an abundant variety of tree species utilized by hoolock gibbons for food. We discuss the current context of primate conservation in Bangladesh and suggest that the current conservation priority for gibbons in the country should be protection and improvement of habitat.     

Habitat characterization of western hoolock gibbons Hoolock hoolock by examining home range microhabitat use

Conserving a species depends on an understanding of its habitat requirements. Primatologists often characterize the habitat requirements of primates using macroscale population-based approaches relying on correlations between habitat attributes and population abundances between sites with varying levels of disturbance. This approach only works for species spread between several populations. The populations of some primates do not fulfill these criteria, forcing researchers to rely on individual-based (microscale) rather than population-based approaches for habitat characterization. We examined the reliability of using micro-scale habitat characterizations by studying the microhabitat preferences of a group of wild western hoolock gibbons (Hoolock hoolock) in order to compare our results to the habitat preferences of western hoolock gibbons identified during a macroscale study of populations across Bangladesh. We used stepwise discriminant analysis to differentiate between the areas of low, medium, and high usage based on microhabitat characteristics (tree species availability, altitude, canopy connection, distance from forest edge, and levels of human disturbance). The gibbons used interior forest habitat with low food tree availability most frequently for sleeping and socializing, and used edge habitat containing high food tree availability for medium periods for feeding. These results indicate that the gibbons prefer interior forest but are frequently forced to visit the forest edge to feed. Therefore, the optimal habitat would be interior forest away from human disturbance with high sleeping-tree and feeding-tree availability. These habitat preferences are consistent with the habitat attributes of Bangladesh’s largest remaining western hoolock gibbon populations, which live in areas containing low agricultural encroachment and high food-tree availability. Microhabitat use studies can be used to characterize the habitat requirements of a species, but should include multiple scales of analysis wherever possible.     

云南高黎贡山自然保护区白眉长臂猿种群及数量现状初报

经2003~2006年访问和现场调查,表明白眉长臂猿在高黎贡山自然保护区约有15~20群,25~40只。它们主要分布在中山湿性常绿阔叶林。栖息环境的急剧恶化和人类猎捕是造成白眉长臂猿数量下降的两个主要原因。提出应加强白眉长臂猿的栖息地保护和消除生境隔离,加强公众保护宣传教育和加强白眉长臂猿的生态生物学等基础研究。     

The first finding of chromosome variations in wild-born western hoolock gibbons

Hoolock gibbons (genus Hoolock) are a group of very endangered primate species that belong to the small ape family (family Hylobatidae). The entire population that is distributed in the northeast and southeast of Bangladesh is estimated to include only around 350 individuals. A conservation program is thus necessary as soon as possible. Genetic markers are significant tools for planning such programs. In this study, we examined chromosomal characteristics of two western hoolock gibbons that were captured in a Bangladesh forest. During chromosome analysis, we encountered two chromosome variations that were observed for the first time in the wild-born western hoolock gibbons (Hoolock hoolock). The first one was a nonhomologous centromere position in chromosome 8 that was observed in the two examined individuals. The alteration was identical in the two individuals, which were examined by G-band and DAPI-band analyses. Chromosome paint analyses revealed that the difference in the centromere position was due to a single small pericentric inversion. The second variation was a heterozygous elongation in chromosome 9. Analysis by sequential techniques of fluorescence in situ hybridization with 18S rDNA and silver nitrate staining revealed a single and an inverted tandem duplication, respectively, of the nucleolus organizer region in two individuals. These chromosome variations provide useful information for the next steps to consider the evolution and conservation of the hoolock gibbon.     

高黎贡山赧亢白眉长臂猿春季食物选择

2007年3月9日—4月28日,在高黎贡山赧亢跟踪观察白眉长臂猿(Hoolock hoolock)的春季食性及取食行为,将其行为分为食果、食果汁和食叶。采用瞬时扫描法记录白眉长臂猿的取食行为,取食的种类、部位和地点等。在其活动区域内,以取食树为中心设置20m×20m的利用样方和以随机方式设置同样大小的可利用样方各19个。在样方内收集与取食树及食物资源相关的6个因子的数据。统计食物种类和资源量、选择指数、取食点的选择性等。结果表明,赧亢白眉长臂猿春季取食的食物共10种,其中果实类植物3种,果汁类植物1种,嫩叶类植物6种。10种食物中,白眉长臂猿对印度木荷(Schima khasiana)的果实和缅甸木莲(Maglietia haokeri)的嫩叶呈弱选择,对其他8种食物资源均呈强选择。Mann-WhitneyU-检验结果表明,利用样方和可利用样方间的食物资源量及食物种类数均差异极显著,以利用样方的资源量大,每一样方食物种类较多。果实是赧亢白眉长臂猿春季的主要食物资源,而嫩叶是补充。呈强选择的食物并不一定是取食频次高的食物;反之,取食频次高的食物也不一定呈强选择。白眉长臂猿常选择易处理的果实和粗灰分含量少的嫩叶,且果实是它摄取水分的主要来源。白眉长臂猿通常选择食物资源和种类相对集中的区域取食,这可以减少动物因寻找食物所耗费的能量,同时获得多种食物,满足其生理对营养的需求。     

Are Montane Forests Demographic Sinks for Bornean White‐bearded Gibbons Hylobates albibarbis?

I estimated habitat-specific population densities for a population of Bornean white-bearded gibbons Hylobates albibarbis inhabiting seven distinct forest types at Gunung Palung National Park, West Kalimantan, Indonesia. Population densities in montane forests (0.44 individuals/km²) were almost ten times lower than those in the next best habitat (upland granite forest; 4.2 individuals/km²) and far lower than those in lowland forest types. Demographic data on 33 gibbon groups living across the seven forest types showed that reproduction was substantially depressed in montane forests compared to high-quality lowland habitats. A simple model suggests that montane forests are demographic sinks for gibbons at Gunung Palung. Follow-up data from observations of montane groups 5 yr after the initial observation period support this result. As high-quality lowland forests (source habitat for gibbons) are being disproportionately lost in and around Gunung Palung National Park due to illegal logging and conversion to oil palm plantations, an increasing percentage of the remaining forest in the park comprises sink habitat for gibbons. This result has disquieting implications for the long-term viability of gibbon populations at Gunung Palung. In addition, as montane forests are generally low-quality habitat for most rainforest vertebrates, and since lowland forests are being lost at alarming rates across the tropics, source-sink population dynamics similar to those I describe here may characterize populations of other tropical vertebrate species.     

云南高黎贡山大塘东部白眉长臂猿鸣叫行为

通过2009年10月至2010年7月监测高黎贡山大塘的3群东部白眉长臂猿的鸣叫行为,收集了10个月(200d)的数据,发现东部白眉长臂猿的鸣叫行为主要发生在黎明后4h内;平均每次鸣叫持续14min59s,不同群体间鸣叫持续时间不同。天气情况影响东部白眉长臂猿的鸣叫开始时间(相对黎明)和持续时间,在雨天鸣叫相对黎明开始时间较晚,持续时间也较长。东部白眉长臂猿鸣叫频率在10月和11月明显高于其他月份,可能与食物(果实)的丰富度有关。根据研究结果,建议对东部白眉长臂猿的调查最好集中在10月或11月;每天监测时间至少持续至黎明后4h,以覆盖长臂猿90%以上的鸣叫;如果出现下雨天气,应适当延长调查时间。     

高黎贡山赧亢白眉长臂猿食性及日取食量

通过确定白眉长臂猿的取食特征及日取食量,探讨不同个体间和春、秋季间日取食量是否存在差异,分析影响日取食量和取食特征的因素,为白眉长臂猿日能量需求及其营养容纳量研究奠定基础。2007—2008年春、秋季,在高黎贡山赧亢采用焦点动物取样法观察和记录数据。结果发现,白眉长臂猿取食36种食物的40个部位,其果实的食物单元、取食速度、单个鲜重值等取食特征不同于嫩叶。春、秋季白眉长臂猿每日取食果实量所占百分比最高、嫩叶所占百分比次之、茎和花所占百分比最低。春、秋季家群中雌猿的日取食量均高于雄猿。与家群的雌猿相比,独猿(♀)春季的日取食量稍高。在春季,独猿取食果实持续时间约为家群的2倍,而取食嫩叶的则与家群几乎相等。相同个体秋季的日取食量高于春季的,且春、秋季日取食各部位的量所占百分比也不同。分析结果表明,食性及日取食部位的量反映了白眉长臂猿选择食物的最基本策略。雌雄个体大小差异、能量消耗、食物特征、动物生理需求等因素影响白眉长臂猿的日取食量。白眉长臂猿取食持续时间与觅食树的食物资源量相关。     

Food selection in relation to nutritional chemistry of Cao Vit gibbons in Jingxi,China

The Cao Vit gibbon (Nomascus nasutus) has only one population with about 110 individuals living in a degraded karst forest along the China–Vietnam border. Investigation of food choice in relation to chemical nutrition will offer important insights into its conservation. We studied the food choice of two groups of Cao Vit gibbons using instantaneous scan sampling in Bangliang National Nature Reserve, Guangxi, China, over 4 years, and analyzed the chemical components (total nitrogen, TN; water-soluble sugar, WSS; crude fat, CF; neutral detergent fiber, NDF; acid detergent fiber, ADF; acid detergent lignin, ADL; condensed tannin, CT; and ash) of 48 food plant parts and 22 non-food plant parts. Fruits and figs that are rich in sugar are important food resources for gibbons. For other food types, flowers are a good source of total nitrogen and carbohydrates, and leaves and buds provide sources of protein and minerals. Cao Vit gibbons selected fruits that contain less total nitrogen, less acid detergent fiber and more water-soluble sugar than non-food fruits. Several food species that were heavily consumed by Cao Vit gibbons are suggested as potential tree species for ongoing habitat restoration.     

Influence of Forest Seasonality on Gibbon Food Choice in the Rain Forests of Barito Ulu,Central Kalimantan

We describe the diet of two hybrid gibbon groups (Hylobates mulleri x H. agilis) in relation to forest seasonality. We collected data over 12 mo in lowland dipterocarp forest in the Barito Ulu research area, Central Kalimantan, Indonesia. Although non-fig fruit was the main dietary item (52–64% of diet), gibbon diet was most strongly influenced by the availability of flowers. During periods when flowers were most abundant and the gibbons increased consumption of them, they also ate figs or young leaves more often. We suggest that although flowers are nutritionally rich sources of food, providing relatively high levels of protein compared to fruit, they are unlikely to satiate gibbon hunger and they seek dietary bulk from figs or young leaves, because they are easily obtained. Rainfall also influenced food choice, and non-fig fruit availability had a weak influence on fruit selection for one group. The group concentrated feeding on the fruit of a few species when fruit was most abundant and ate a greater diversity of species when fruit was scarce. Gibbon diet appeared not to be influenced by changes in availability of figs, young leaves and diversity of fruiting species.     

Diet and ranging behavior of the endangered Javan gibbon (Hylobates moloch) in a submontane tropical rainforest

Altitude influences forest structure and food abundance and distribution, which in turn affect primate feeding and ranging patterns. Javan gibbons (Hylobates moloch) are endemic to forests spanning a broad range of altitudes on Java, Indonesia. Most information about Javan gibbon behavior comes from studies in lowland forests, while the vast majority of wild gibbons remaining inhabit hill and lower montane forests. We studied the diets, activity patterns, and ranging behavior of three gibbon groups in hill/lower montane (950-1,100?m asl) forest in the Gunung Halimun-Salak National Park (GHSNP) from April 2008 to March 2009. The mean home range size was 37?ha and the mean daily path length was 1,180?m. The study groups spent 36% of time feeding, 41% resting, 15% traveling, 6% engaging in social behavior, and 2% in aggressive interactions. Fruit was the most important food (63% of feeding time) followed by leaves (24%), and flowers (12%). Our results suggest that Javan gibbons in higher elevation habitats have substantially larger home ranges than lowland populations, despite broad similarity in their activity budgets and diets. Conservation managers should consider the effects of altitude and habitat quality on gibbon ranging behavior when developing habitat corridors, selecting sites for translocation or reintroduction projects, and designating and managing protected areas.     

白眉长臂猿鸣叫的时间特征

滇西白眉长臂猿(Hylobateshoolock)鸣叫主要发生在上午,最早开始于黎明时分,最晚则在下午16:30以后。平均开始时间为09:05,SD=1095min(N=70,范围07:12～16:30),持续时间为197min,SD=934min(N=55,R=4～50)。多数鸣叫发生在07:00～10:00之间(80%)。不同季节鸣叫发生时间有显著差异,可能与黎明时间(光亮度)不同有关,但持续时间无差异。同一季节异地间鸣叫持续时间差异显著。气候、猿群密度、栖息地状态对鸣叫有一定影响,但未见明显相关性。与黑长臂猿的种间比较表明,白眉长臂猿的鸣叫声在时间分布上有较大的散开度,持续时间也较长,二者有显著差异。     

Behavioral responses of Cao Vit gibbon (Nomascus nasutus) to variations in food abundance and temperature in Bangliang, Jingxi, China

The Cao Vit gibbon is a critically endangered species with only about 110 individuals remaining in a degraded karst forest along the China-Vietnam border. Behavioral data from this site are particularly useful in understanding gibbon behavioral adaptations to different sets of ecological conditions and will contribute to the conservation of the species. We studied seasonal variation in the time budget and diet of the Cao Vit gibbon in response to variation in food availability and ambient temperature by observing two groups for 1,379 hr between January and December 2009. We used 5-min scan samples to record the activity of gibbons. Both ambient temperature and food availability varied from month to month. Gibbon groups increased resting time and huddled together in sleeping places in cold months. Gibbons spent more time feeding on fruit when fruit was more abundant suggesting that fruit was their preferred food. Alternatively, leaf eating was negatively correlated with leaf availability which suggested that leaves may be used as a fallback food. Gibbons increased their diet diversity when they ate more leaves. This might be a strategy to cope with toxins or digestion inhibitor accumulation associated with feeding from a limited number of leaf species. Individuals consumed more buds when Broussonetia papyrifera produced buds in March and April. During this period, they decreased traveling time and engaged in less frequent social interactions. Gibbons spent more time searching for and feeding on invertebrates during June and October. However, we did not collect data on invertebrate abundance and therefore cannot determine the relationship between invertebrate feeding and availability. We conclude that flexibility in consuming diverse food types and food species, and in responding to the availability of preferred foods, has enabled the Cao Vit gibbon to survive in a degraded karst forest habitat.     

Modeling the Ecological and Phenological Predictors of Fruit Consumption by Gibbons (Hylobates albibarbis)

Understanding the ecological interactions between plant reproductive strategies and frugivore feeding behavior can offer insight into the maintenance of tropical forest biodiversity. We examined the role of plant ecological and phenological characteristics in influencing fruit consumption by the White‐bearded gibbon (Hylobates albibarbis) in Gunung Palung National Park, Indonesian Borneo. Gibbons are widespread across Borneo, highly frugivorous and perform important seed dispersal services. We compare multiple models using information criteria to identify the ecological and phenological predictors that most strongly influence gibbon fruit use of 154 plant genera. The most important predictors of resource use were the overall abundance of a genus and the consistency of fruit availability. Plant genera can maintain constant fruit availability as a result of (1) individual stems fruiting often or (2) stems fruiting out of synchrony with each other (asynchrony). Our results demonstrate that gibbons prefer to feed on plant genera that provide consistent fruit availability due to fruiting asynchrony. Because gibbons feed more often on genera that fruit asynchronously, gibbons are more likely to disperse seeds of plant genera with this reproductive strategy. Research on other frugivorous species is needed to determine whether the results for gibbons are generalizable more broadly. Finally, these results suggest that asynchronously fruiting plant genera may be particularly important for habitat restoration in tropical forests designed for frugivore conservation.     

Gibbons (Nomascus gabriellae) provide key seed dispersal for the Pacific walnut (Dracontomelon dao), in Asia's lowland tropical forest

Understanding the mutualisms between frugivores and plants is essential for developing successful forest management and conservation strategies, especially in tropical rainforests where the majority of plants are dispersed by animals. Gibbons are among the most effective seed dispersers in South East Asia's tropical forests, but are also one of the highly threatened arboreal mammals in the region. Here we studied the seed dispersal of the Pacific walnut (Dracontomelon dao), a canopy tree which produces fruit that are common in the diet of the endangered southern yellow-cheeked crested gibbon (Nomascus gabriellae). We found that gibbons were the most effective disperser for this species; they consumed approximately 45% of the fruit crop, which was four times more than that consumed by macaques – the only other legitimate disperser. Gibbons tracked the temporal (but not spatial) abundance of ripe fruits, indicating this fruit was a preferred species for the gibbon. Both gibbons and macaques dispersed the majority (>90%) of the seeds at least 20 m away from parent crowns, with mean dispersal distances by gibbons measuring 179.3 ± 98.0 m (range: 4–425 m). Seeds defecated by gibbons germinated quicker and at greater rates than seeds spat by macaques, or in undispersed fruits. Gibbon-dispersed seeds were also more likely to be removed by unknown seed predators or unknown secondary dispersers. Overall, gibbons play a key role in the regeneration of the Pacific walnut. Our findings have significant implications both for the management of the Pacific walnut tree dominating tropical rainforest as well as the reintroduction program of the Southern yellow-cheeked crested gibbon.     

Comparison of point transect distance and traditional acoustic point-count sampling of hoolock gibbons in Htamanthi Wildlife Sanctuary,Myanmar

Effective conservation demands more accurate and reliable methods of survey and monitoring of populations. Surveys of gibbon populations have relied mostly on mapping of groups in “listening areas” using acoustical point-count data. Traditional methods of estimating density in have usually used counts of gibbon groups within fixed-radius areas or areas bounded by terrain barriers to sound transmission, and have not accounted for possible decline in detectability with distance. In this study we sampled the eastern hoolock gibbon (Hoolock leucogenys) population in Htamanthi Wildlife Sanctuary (WS), Myanmar, using two methods: the traditional point-count method with fixed-radius listening areas, and a newer method using point-transect Distance analysis from a sample point established in the center of each listening point array. The basic data were obtained by triangulating on singing groups from four LPs for 4 days, in 10 randomly selected sample areas within the sanctuary. The point transect method gave an average density of 3.13 groups km⁻², higher than the estimates of group density within fixed-radius areas without correction for detectability. A new method of analysis of singing probability per day (p[1]) gave an estimate of 0.547. Htamanthi WS is an important conservation area containing an estimated 7000 (95% confidence interval: 5000–10,000) hoolock groups. Surveys at Htamanthi WS and locations in the Hukaung Valley suggest that the extensive evergreen forests in northern Myanmar have the capacity to support 2–4 (average about 3) groups of hoolock gibbons per km², but most forests in its range have yet to be surveyed.     

笼养白眉长臂猿的繁殖初探

本文报道了白眉长臂猿（Ｈｙｌｏｂａｔｅｓ ｈｏｏｌｏｃｋ）在笼养条件下繁殖成功。经过笼养条件下３例白眉长臂猿繁殖结果的分析认为：舭舒环境、饲养、雌雄猿的配对以及雌猿自身哺育幼仔能力等,呈影响繁殖能否成功的因素。