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）、金头叶猴（卡巴叶猴,T.poliocephalus）、越南乌叶猴（T.hatinhensis）、印支黑叶猴（T.ebenus）、老挝乌叶猴（T.laotum）7种。迄今为止,对分布于中国的黑叶猴和白头叶猴的生态学已有较多研究,而对其他石山叶猴的研究较缺乏。本文对中国黑叶猴和白头叶猴的种群生态学、行为生态学、保护生物学研究进行综述,以促进叶猴生态学理论的发展和完善,为我国特有珍稀濒危动物保护提供基础资料。未来研究应关注石山叶猴的种群历史以及对栖息地破碎化和气候变化的适应机制等问题。     

Variations in diet composition of sympatric Trachypithecus francoisi and Macaca assamensis in the limestone habitats of Nonggang,China

Comparative studies of sympatric species are essential for understanding behavioral and ecological adaptation as well as the mechanisms that can reduce resource competition to allow coexistence.Fran?ois' langurs(Trachypithecus francoisi) and Assamese macaques(Macaca assamensis) are sympatric primate species found in the limestone seasonal rainforests of Nonggang Nature Reserve,southwestern Guangxi, China. To explore their different adaptation strategies, we collected data on diet using scan sampling at 15-min intervals. Our results revealed that Fran?ois' langurs showed a more flexible diet composition than Assamese macaques.Fran?ois' langurs increased dietary diversity and mature leaf consumption in response to seasonal scarcity of preferred young leaves and fruits, whereas Assamese macaques relied heavily on young bamboo leaves(Indocalamus calcicolus) in most months.These variations reflect the differences in digestive physiology, morphology, and the temporal and spatial distribution of food resources.     

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。     

白头叶猴与黑叶猴觅食行为的比较

开展近缘物种觅食行为比较对理解动物的行为可塑性及适应性具有重要意义。白头叶猴（Trachypithecus leucocephalus）和黑叶猴（T.francoisi）是近缘物种,体形大小相近,社会结构和栖息环境相似,是广西崇左白头叶猴国家级自然保护区喀斯特季节性雨林中邻域分布的灵长类。为了探索两个物种在喀斯特生境中是否有相似的觅食策略,我们于2012年1-12月采用瞬时扫描取样法对两种叶猴的觅食行为进行研究。结果表明,白头叶猴与黑叶猴在不同时段均为叶食性,树叶是两种叶猴各个时段主要食物,其中白头叶猴日均取食树叶77.0%±4.4%,黑叶猴日均取食68.9%±8.3%,两者对树叶的采食比例均没有显著的日时段差异（白头叶猴：χ²=6.602,df=11,P=0.830;黑叶猴：χ²=11.393,df=11,P=0.411）。两种叶猴的觅食行为都在猴群清晨离开夜宿石洞后和进入过夜山洞前的时段中频繁发生。白头叶猴在09：00-10：59和16：00-17：59出现觅食高峰,时间占比分别为41.7%和46.3%;黑叶猴同样在09：00-10：59和16：00-17：59的时间段内发生高频率的觅食行为,时间占比分别为31.3%和38.0%。此外,两种叶猴的觅食时间在大部分时段中的差异并不明显。白头叶猴和黑叶猴在石灰岩生境中具有相似的觅食策略,这意味着两种叶猴在取食生态学上可能采取相似的保护措施。     

How does the white-headed langur (Trachypithecus leucocephalus) adapt locomotor behavior to its unique limestone hill habitat?

Limestone hill habitats pose unique challenges to langurs. One of the characteristics of this habitat is its cliffs, which account for about 10–20% of the total area. We have never observed langurs falling from the cliffs during our 10-year field study. Five patterns of locomotion were exhibited by the white-headed langur: (1) arboreal ascent and descent, (2) arboreal quadupedalism, (3) terrestrial quadrupadelism, (4) moving on cliffs and (5) leaping on cliffs. Locomotor patterns varied according to the substrate, but terrestrial quadrupedalism accounted for more than 50% of locomotion time. Moving on cliffs and leaping on cliffs may be modes of locomotion unique to the white-headed langur, at least in terms of frequency. White-headed langurs have an intermembral index of 76 and, compared to langurs with a similar intermembral index, are more terrestrial. Further analysis indicates that greater terrestrialism may be the result of adaptation to their limestone habitat. Interestingly, white-headed langurs select caves on the cliff as their sleeping sites, and they exhibit special behaviors for exiting and entering the cave very early in the morning and late in the evening.     

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。     

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.     

Habitat quality and range use of white-headed langurs in Fusui, China

The socioecology of white-headed langurs (Trachypithecus leucocephalus) was studied in Fusui Precious Animal Reserve, Guangxi, China, in 1997/1998. Habitat quality was classified according to the level of human disturbance. Plant species diversity increased with habitat quality. Important foods for the langurs occurred more in high-quality habitat. Home range size varied from 28 to 48 ha, and the home range area per individual decreased as habitat quality increased. Small polygynous langur groups had poorly defended ranges, but large groups defended their ranges intensively. Only harem males were involved in group defence, apparently competing for females by defending their habitat. High-quality habitat was more attractive to females; accordingly, group size increased significantly with habitat quality.     

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.     

The phyletic position and systematics of the douc langurs of Southeast Asia

In recent years, two major questions concerning the phyletic relationships and systematic position of the douc langurs have arisen. These concern, firstly, the taxonomic level at which the doucs as a group should be distinguished and, secondly, the number of taxa of doucs that should be recognized. It has recently been demonstrated on the basis of an exhaustive phylogenetic analysis that the doucs are generically distinct from the snub-nosed langurs and that they should be referred to as species of Pygathrix and Rhinopithecus, respectively [Jablonski and Peng, Folia Primatologica 60:36–55, 1993]. The present investigation was directed toward testing this conclusion using an expanded data set and a different method of character coding, and toward addressing the question as to the number of species or subspecies of doucs that should be recognized. A wide variety of data from large samples of doucs (n = 38), snub-nosed langurs (n = 53), and an out group (macaques; n = 191) were assembled, coded, and analyzed using an interactive computerized program for phylogenetic analysis. The specimens of Pygathrix examined included skeletal specimens, skins, and, when possible, living animals representing the three recognized taxa of doucs, nemaeus nigripes, and moi. The data base for the study comprised 178 characters, including measurements of skeletal specimens (98 characters), qualitative (presence or absence) morphological features (36 characters), characteristics of the pelage (39 characters), and 5 miscellaneous characters. The conclusions of the study were that 1) as a group, the taxa of Pygathrix preserved a larger number of primitive features for the Pygathrix-Rhino-pithecus clade than did the taxa of Rhinopithecus; 2) the taxa of Pygathrix were less different from one another than are the species of Rhinopithecus were from one another; 3) the subspecies Pygathrix nemaeus moi Kloss, 1926 be synonymized with Pygathrix nemaeus nigripes, as suggested by Napier [Catalogue of Primates in the British Museum (Natural History) and Elsewhere in the British Isles. Port III Family Cercopithecidae, Sub-Family Colobinae. London, 1985]; 4) the extant doucs were best recognized as two subspecies, P. nemaeus nemaeus for the red-shanked douc and P. nemaeus nigripes for the black-shanked douc; and 5) the phylogeny of the doucs and snub-nosed langurs proposed by Jablonski and Peng[op cit.,1993] was found to be robust. © 1995 Wiley-Liss, Inc.     

Differences in molar wear gradient between adult macaques and langurs

Interspecific differences in the amount and form of molar wear in nonhuman primates are only beginning to be documented and understood. The purpose of this study was to look at the wear gradient between M₁ and M₂ in a sample of macaques and langurs to determine if differences in wear gradient could be related to differences in diet. A skeletal collection of wild shot Macaca fascicularis, Presbytis cristata, and Presbytis rubicunda from the Museum of Comparative Zoology at Harvard University was examined using photogrammetric techniques. X, Y, and Z coordinates were used to compute areas of dentin exposure on the buccal occlusal surfaces of M₁ and M₂. The relationship between these variables was examined using Bartlett’s three-group method and least-squares regression. Interspecific comparisons of the resultant y intercepts indicate that (I) M. fascicularis (as compared with P. cristata or P.) has more dentin exposed on M₁ when there is none exposed on M₂, and (2) P. cristata (as compared with P. rubicunda) has more dentin exposed on M₁ when there is none exposed on M₂. Factors that might be responsible for these differences are (a) differences in dentin/enamel structure, (b) differences in molar eruption timing, and (c) differences in behavior. An unusual intercusp sequence of dentin exposure in the langurs makes precise interpretations difficult. However, at the present time, behavioral differences among the species deserve further consideration as a cause of the observed differences in molar wear gradient.     

Learning the ropes: The ontogeny of locomotion in red-shanked douc (Pygathrix nemaeus), Delacour's (Trachypithecus delacouri), and Hatinh langurs (Trachypithecus hatinhensis) I. positional behavior

Recent studies at the Endangered Primate Rescue Center (EPRC) in the Socialist Republic of Vietnam's Cuc Phuong National Park by Byron et al. ([2002] Am. J. Phys. Anthropol. [Suppl.] 34:51) and Covert and Byron ([2002] Caring for Primates) revealed unexpected locomotor and postural behaviors in the red-shanked douc langur (Pygathrix nemaeus). This paper further elucidates the question of red-shanked douc suspensory behavior, and provides initial positional behavior data for two other rare Asian colobines, by comparing the ontogenetic positional behavior of red-shanked douc langurs, Delacour's langurs (Trachypithecus delacouri), and Hatinh langurs (Trachypithecus hatinhensis) at the EPRC. Two hundred and seven hours of positional behavior data were collected, with approximately equal amounts of data on each species, and equal amounts on adults and those less than 18 months in age. All young animals were more active than adults, used a wider repertoire of locomotor behaviors, and expressed suspensory behaviors more frequently than did the adults. Young animals also "invented" one new locomotor and two new postural behaviors. These differences are due to both play and explorative behavior, as well as to the youths' changing musculoskeletal systems. The number of positional behaviors utilized by the adults of these species is quite similar to one another (23-32), as is that utilized by the young (51-56). Douc langurs in both age categories used suspensory behaviors more frequently than did Delacour's and Hatinh langurs. Because the uniformity of enclosures offers a control, the results of this study generate hypotheses regarding adaptive radiations and niche partitioning in wild populations.     

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.     

贵州麻阳河自然保护区黑叶猴繁殖周期的初步研究

黑叶猴(Trachypithecus francoisi francoisi),属灵长目(Primates),猴科(Cercopithecidae),疣猴亚科(Colobinae)。分布于越南北部和中国的广西、贵州和重庆等地的山地岩溶地区(Fooden,1976;王应祥等,1999)。由于生境特殊,受人为活动影响较大(汪松,1998),该物种近20年来数量呈下     

Food availability,temperature, and day length drive seasonal variations in the positional behavior of white‐headed langurs in the limestone forests of Southwest Guangxi,China

Information on positional behavior contributes to the understanding of the ecological adaptation mechanisms in animals. We collected data on the positional behavior of white‐headed langurs (Trachypithecus leucocephalus) at the Guangxi Chongzuo White‐Headed Langur National Nature Reserve from September 2016 to August 2017 via instantaneous scan sampling method. This study aimed to examine the importance of positional behavior flexibility in limestone forests characterized by seasonal variations in climate and food resources. Our results indicated that langurs adopted leaping (47.92% ± 5.50%) and vertical climbing (40.13% ± 6.20%) as their predominant locomotor modes and sitting (83.08% ± 4.70%) as their predominant posture. Their positional behavior exhibited marked seasonal variations. More specifically, langurs used quadrupedal walking more frequently during the dry season than during the rainy months. In the stationary state, they sat more frequently during the dry season, whereas they laid and suspended more often during the rainy season. Their positional behavior was affected by fruit availability, day length, and temperature. Quadrupedal walking increased with the decrease in fruit availability, whereas leaping was positively correlated with fruit availability. Moreover, sitting was positively correlated with average temperature but negatively correlated with day length. Lying was also negatively correlated with temperature but positively correlated with day length. We conclude that white‐headed langurs adapt to limestone forests with positional behavior flexibility in response to seasonality. Our research provides evidence of the effects of food availability, ambient temperature, and day length on the positional behavior of white‐headed langurs, highlighting the need to understand their behavioral ecology and the influence of ecological factors on behavioral adaptation.     

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.     

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     

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.     

干扰生境下黑叶猴(Trachypithecus francoisi francoisi)日活动时间的分配

1999年至2000年,采用瞬间采样法对贵州省麻阳河国家级自然保护区干扰生境中的野生成年黑叶猴的日活动规律进行了研究。结果表明：干扰生境中野生成年黑叶猴在全年的行为时间分配中表现为休息和摄食所占比例最多,分别为35．41％和31．67％;其次是游走、拥坐和嬉戏,分别为14．44％、9．61％和8．54％;仅将很少时间用于理毛行为,为0．33％。与未干扰生境相比,干扰生境下黑叶猴全年中除用于休息的时间下降外,用于其余活动类型的时间均有所提高。研究还表明野生成年黑叶猴的活动规律在不同季节存在一定差异性。休息和摄食行为在各季节日活动规律中都存在显著高峰期,但高峰期持续时间和强度不同。游走、嬉戏和拥坐行为在各季节的日活动规律所占比例均较低。理毛行为存在季节有或无的现象。     

Food diversity and choice of white-headed langur in fragmented limestone hill habitat in Guangxi,China

We studied the diet and food choice of three groups of white-headed langurs (Trachypithecus leucocephalus) from July 2002 to June 2003 at Fusui Rare Animal Reserve, Guangxi, China. Data were collected from via focus group sampling, with continuous recording. A total of 109 plant species (including 19 unidentified species) were used as food by the white-headed langur. They spent 91.6% of total feeding time feeding on leaves, 4.2% on fruits and 3.3% on stems. Flowers and other food items accounted for only 0.3% and 0.6% of total feeding time, respectively. There were significant seasonal variations in the langurs’ diets with changes in the total number of species and the diversity of food species consumed. The langurs used significantly more plant species as food in the rainy season than in the dry season (36 species vs. 26.5 species). Dietary diversity was also significantly higher in the rainy season than in the dry season (2.6 vs. 2.4). No significant seasonal variation was found in the percentage of various plant parts in their monthly diets. Though the white-headed langur fed on many plant species, 11 species made up 84.9% of their diet. There were no significant correlations between the percentage of feeding time for main food plant species and their corresponding abundance in the habitat, content of water, crude protein, crude fiber and the ratio of crude protein to crude fiber. These results suggest that food choice of the white-headed langur is not influenced by their abundance and nutritional content.