Sleeping sites, sleeping trees, and sleep-related behaviors of black crested gibbons (Nomascus concolor jingdongensis) at Mt. Wuliang, Central Yunnan, China

Data on sleep-related behaviors were collected for a group of central Yunnan black crested gibbons (Nomascus concolor jingdongensis) at Mt. Wuliang, Yunnan, China from March 2005 to April 2006. Members of the group usually formed four sleeping units (adult male and juvenile, adult female with one semi-dependent black infant, adult female with one dependent yellow infant, and subadult male) spread over different sleeping trees. Individuals or units preferred specific areas to sleep; all sleeping sites were situated in primary forest, mostly (77%) between 2,200 and 2,400 m in elevation. They tended to sleep in the tallest and thickest trees with large crowns on steep slopes and near important food patches. Factors influencing sleeping site selection were (1) tree characteristics, (2) accessibility, and (3) easy escape. Few sleeping trees were used repeatedly by the same or other members of the group. The gibbons entered the sleeping trees on average 128 min before sunset and left the sleeping trees on average 33 min after sunrise. The lag between the first and last individual entering the trees was on average 17.8 min. We suggest that sleep-related behaviors are primarily adaptations to minimize the risk of being detected by predators. Sleeping trees may be chosen to make approach and attack difficult for the predator, and to provide an easy escape route in the dark. In response to cold temperatures in a higher habitat, gibbons usually sit and huddle together during the night, and in the cold season they tend to sleep on ferns and/or orchids.     

无量山大寨子黑长臂猿(Nomascus concolor jingdongensis)种群生存力

据2003年9月至2005年9月,对云南中部无量山大寨子黑长臂猿种群(5个群体)进行了观察,获得了群体大小、配偶体制、繁殖间隔、环境容纳量、死亡率、灾害的发生频率等种群参数,并结合近缘种的一些相关数据,利用旋涡模型(Vortex 914),对无量山大寨子地区黑长臂猿亚种群的动态进行了模拟分析。结果显示:大寨子亚种群是一个具有很强的潜在繁殖力的种群,如果没有偷猎,亚种群在100a之内不会灭绝,并且能迅速达到环境容纳量。但是每年如果有1只成年雄性和1只成年雌性被猎杀,该种群将会在第78年灭绝,且灭绝概率为100%。不同程度的死亡率对种群影响不大,但高死亡率显著延缓了种群到达环境容纳量的时间。环境容纳量对种群遗传多样性损失具有重要的影响,在没有猎杀的情况下,种群的长期存活需要一个较大的环境容纳量。因此,在黑长臂猿受到严格保护、且栖息地主要在保护区内的今天,严密监控火灾的发生,限制牲畜进入林区等人为干扰的影响,保护好黑长臂猿栖息地是首要工作之一。但如果能使其栖息地周围的森林植被得到恢复,增加其栖息范围,将有利于该地区黑长臂猿的发展。     

Status and distribution pattern of black crested gibbon (Nomascus concolor jingdongensis) in Wuliang Mountains, Yunnan, China: implication for conservation

The western black crested gibbon (Nomascus concolor), or black gibbon, one of the lesser apes (Hylobatidae), is mainly distributed in Yunnan, China. Of the four recognized subspecies, N. c. jingdongensis is endemic to the Wuliang Mountain, central Yunnan, China. Of all the subspecies, this one has the largest population of any black gibbon. However, the data were all based on brief estimates. We carried out an extensive field survey on population and group distribution of the black gibbon in the Wuliang Mountains by use of loud morning songs and interviews with local people. Ninety-eight groups were confirmed and located in the mid-montane range of Wuliang Mountains. More groups are found on the east slope and the southern region than in the west and the north. Gibbons are more disjunctly distributed on the west slope, especially in the northern part. Deforestation in the late 1950s, 1960s and 1970s was the main reason for rapid loss of habitat and population decline. Hunting was another key reason for population decline and, in many cases, the main reason for local extinction.     

Influence of food availability and climate on behavior patterns of western black crested gibbons (Nomascus concolor) at Mt. Wuliang,Yunnan, China

Food abundance and climatic factors can significantly affect the behavior of animals and constrain their activity budgets. The population of western black crested gibbons (Nomascus concolor) in Mt. Wuliang lives in montane forest and is close to the northern extreme of the distribution for gibbons (Hylobatidae). Their habitats show remarkable seasonal variation in terms of food availability, temperature, and rainfall. To understand behavioral adaptations of western black crested gibbons to different sets of ecological conditions, we examined relationships among food availability, mean temperature, rainfall, and behavior patterns by observing two groups for 1 year each. Our results revealed that activity budget was affected by food availability and mean temperature. The gibbons spent more time eating flowers when that resource was more available and spent less time moving when fruit was more available. The gibbons spent less time feeding and more time resting, and spent less feeding time on fruit and leaves when the mean temperature was lower. These results suggest that the gibbons displayed a pronounced preference for flowers as a food resource and adopted a time minimizer strategy when high‐nutrient food items (i.e., fruit) were more available. In addition, the gibbons adopted an energy‐conserving strategy during periods of low temperature. The flexibility of behavioral patterns in responding to food availability and temperature may potentially improve the gibbons’ prospects of surviving and reproducing in a northern montane forest.     

西黑冠长臂猿雄性取代前后鸣叫行为的变化

本文通过长时间的野外监测,首次报道了西黑冠长臂猿的一次雄性取代行为。一个研究群体(G3)中的1 只亚成年雄性长臂猿在10 岁左右取代了相邻群体(G2)中的成年雄性。整个取代过程持续了15 d时间。雄性取代发生前,G2 中雌雄的配对关系已经不稳固,这为雄性取代提供了机会。而G2 与G3 群的一次长时间冲突可能消耗了G2 中成年雄性大量体能,这为G3 中的亚成年雄性打败并取代G2 中的成年雄性创造了机会。本研究在取代发生后,对新形成群体的鸣叫行为进行了连续4 个月的监测。结果表明与处于稳定时期的G2 群相比,新形成群体的鸣叫频次更高,但每次二重唱中雌性的平均激动鸣叫次数降低。这证明了Geissmann (1986)提出的假说,新配对的群体应该在尽量短的时间内多练习二重唱,这样导致新配对群体的鸣叫频率明显升高。虽然经历了4 个月的合唱练习,新形成群体的激动鸣叫次数仍然偏低,并且两只雌性同时激动鸣叫的频次也比较低。这说明新形成的配对之间配合依然不默契,或者说明配对之间的关系还不稳定。     

Predation on giant flying squirrels (Petaurista philippensis) by black crested gibbons (Nomascus concolor jingdongensis) at Mt. Wuliang, Yunnan, China

Predation on vertebrates is infrequent in gibbons. In a 14-month field study of the central Yunnan black crested gibbon (Nomascus concolor jingdongensis) at Mt. Wuliang, Yunnan, China, we observed gibbons attacking, killing and eating giant flying squirrels (Petaurista philippensis). During 845 h of observation on one study group, the gibbons attacked giant flying squirrels 11 times, and succeeded in 4 cases. Although all members of the group attempted to attack the squirrels, all four successful attacks were made by the same adult female. The victims were infants in three cases and a juvenile or sub-adult in one case. Black crested gibbons also attacked adult giant flying squirrels by grabbing their long tails and throwing them from the canopy, but they failed to catch or kill the prey in three cases observed. Passive meat sharing occurred in three out of four successful cases. Besides hunting giant flying squirrels, the black crested gibbons also ate eggs or chicks in two birds’ nests and one lizard.     

东黑冠长臂猿鸣叫特征及气象因子对鸣叫的影响

鸣叫是长臂猿非常典型的一个特征,并且受到生物因素和非生物因素(如气象因子) 的影响。为了解东黑冠长臂猿的鸣叫特征以及气象因子对鸣叫的影响,2008 年8 月至2009 年10 月,采用全事件记录法对栖息在广西邦亮自然保护区3 个东黑冠长臂猿野生群体的鸣叫行为进行观察。结果表明东黑冠长臂猿倾向于在早晨鸣叫,有91.4% 的鸣叫发生在日出前0.5 h 至日出后3 h 之间,其中53.1% 的鸣叫发生在日出后1 h 内。平均每个群体的鸣叫频次为69.7% ,一个群体平均每天鸣叫1.24 次,鸣叫的平均持续时间为18.3 min。一次二重唱中,雌性平均激动鸣叫4.4 次。长臂猿鸣叫的起始时间在光照强度的影响下差异显著,阴天和雾天鸣叫的起始时间延后,且雾天最迟;降雨致使长臂猿体能的损失和光照强度减弱,从而引起鸣叫起始时间的延后和持续时间缩短;温度对长臂猿鸣叫的影响并不显著。     

Proximity association in polygynous western black crested gibbons (Nomascus concolor jingdongensis): network structure and seasonality

We investigated the structure and seasonality of the proximity network in a group of polygynous western black crested gibbons (Nomascus concolor) using social network analysis. The spatial proximity changed seasonally and was affected by temperature and rainfall. Preferred proximity association was not distributed randomly among individuals. Kinship was one explanation for the social structure, as offspring preferred to maintain close proximity with their mothers. The proximity of infants to mothers decreased with age, and independent offspring had lower proximity to mothers than dependent ones. We found that the adult male had different proximity relationships with two different adult females. The frequency of proximity between the male and the infant-carrying female was significantly higher than that between the male and the female who had immigrated carrying one offspring of uncertain paternity into the group. Infanticide avoidance and/or predation protection for dependent infants might explain the proximity relationship differences. Temperature influenced group proximity association, with individual proximity increasing in the cold months and decreasing in the hot months. Group proximity decreased in months with higher anthropogenic disturbance.     

无量山大寨子黑长臂猿一夫二妻制的群体结构及其行为学原因

2003年8月—2005年8月,对无量山大寨子5个黑长臂猿群体的结构和组成进行了观察。当一个群体在早晨鸣叫或依次通过树冠时,记录群体的结构和组成。每个群体都由1个成年雄性、2个成年雌性及其后代组成。2003年8月平均群体大小为6·2只;到2005年8月,平均群体大小发展为6·4只,其中有2个亚成年雄性从出生群迁出,且有3只幼猿出生。在3个群体(G1、G2和G3)中两个成年雌性都成功繁殖了后代。同一群体内两个成年雌性间无攻击或等级行为。2005年4月15日,当一只亚成年雌性进入G3的领域后,两只成年雌性对其进行追逐驱赶,并且干扰其与成年雄性配合进行二重唱,成年雄性没有直接驱赶流浪的亚成年雌性,10天后这只亚成年雌性离开了G3的领域。亚成年雄性经常与群体其他成员保持一定距离,并且在出生地通过独唱练习鸣叫。黑长臂猿可能通过亚成年雄性和雌性的迁出,及成年雌性对外来流浪雌性的驱赶维持这种一夫二妻的群体结构。     

无量山大寨子黑长臂猿(Nomascus concolor jingdongensis)种群生存力

据2003年9月至2005年9月,对云南中部无量山大寨子黑长臂猿种群（5个群体）进行了观察,获得了群体大小、配偶体制、繁殖间隔、环境容纳量、死亡率、灾害的发生频率等种群参数,并结合近缘种的一些相关数据,利用旋涡模型（Vortex 914）,对无量山大寨子地区黑长臂猿亚种群的动态进行了模拟分析。结果显示：大寨子亚种群是一个具有很强的潜在繁殖力的种群,如果没有偷猎,亚种群在100a之内不会灭绝,并且能迅速达到环境容纳量。但是每年如果有1只成年雄性和1只成年雌性被猎杀,该种群将会在第78年灭绝,且灭绝概率为100%。不同程度的死亡率对种群影响不大,但高死亡率显著延缓了种群到达环境容纳量的时间。环境容纳量对种群遗传多样性损失具有重要的影响,在没有猎杀的情况下,种群的长期存活需要一个较大的环境容纳量。因此,在黑长臂猿受到严格保护、且栖息地主要在保护区内的今天,严密监控火灾的发生,限制牲畜进入林区等人为干扰的影响,保护好黑长臂猿栖息地是首要工作之一。但如果能使其栖息地周围的森林植被得到恢复,增加其栖息范围,将有利于该地区黑长臂猿的发展。     

Individuality in male songs of wild black crested gibbons (Nomascus concolor)

This is the first study of vocal individuality in male songs of black crested gibbons. The sound recordings were carried out at two field sites, Pinghe, Ailao Mountains, and Dazhaizi, Wuliang Mountains, both located in Yunnan province, China. A total of 127 coda phrases of 38 male songs bouts of eight individual male gibbons were analyzed. Stepwise discriminant function analysis was used to examine the acoustic individuality of the males. We found that individuality among neighbors was very pronounced. Moreover, individuality within a site (i.e. among neighbors) is higher than among individuals between sites. Our finding suggests that black crested gibbons may actively increase their degree of vocal individuality against that of their immediate neighbors by vocal adjustment.     

云南中部无量山黑长臂猿(Nomascus concolor jingdongensis)栖息地乔木层物种多样性和结构特征

无量山是黑长臂猿景东亚种的唯一分布区,现栖息着98群500余只黑长臂猿。长臂猿是典型的树栖性灵长类动物,通过对无量山西坡大寨子地区250个样方的调查,分析了随海拔梯度升高,黑长臂猿栖息地植被乔木层物种多样性和结构的变化情况。共记录乔木111种,隶属于33科;木质藤本23种,隶属于18科。其中优势科主要有樟科(Lauraceae)、木兰科(Magnoliaceae)、壳斗科(Fagaceae)、山茶科(Theaceae)和杜鹃花科(Ericaceae)。根据不同海拔乔木层物种组成的差异,该区可划分为半湿润常绿阔叶林(2100~2300m)和中山湿性常绿阔叶林(2400~2600m)两种植被类型。多样性指数(Shannon-Wiener指数)随海拔升高在两种植被类型中均呈下降趋势;均匀度指数(Pielou指数)在半湿润常绿阔叶林中呈下降趋势,在中山湿性常绿阔叶林中无明显变化。半湿润常绿阔叶林中,阳坡的乔木物种多样性低于阴坡;而阳坡物种多样性在两种植被类型间差异显著。随着海拔的升高,乔木层的平均高度和上层乔木(Ⅰ层)的比例均逐渐降低,但下层乔木却呈上升趋势。6种优势乔木树种的种群年龄结构分析表明,该区植被的乔木层呈现稳定增长的趋势。     

东黑冠长臂猿鸣叫声谱分析

2007 年9 月至2009 年6 月,利用Sony TC - D5 Pro2 录音机、Sony C - 76 指向性话筒和Sony 录音磁带对广西邦亮自然保护区3 群东黑冠长臂猿的鸣叫进行了录音,对每群录音效果较好的5 个声音用Signal/ RTS 4.0 软件进行声谱分析。结果表明:东黑冠长臂猿叫声的频率较高,最高频率已经达到甚至超过了5 kHz;雄性的鸣叫声由起始音(boom)、简单的重复音节(aa notes)、调节前音节(pre-modulated note)和调节音句(modulated phrases)组成,雌性长臂猿一般只会发出一种固定而刻板的激动鸣叫,二者互相配合组成结构复杂的二重唱。通常,二重唱由成年雄性发起和结束,并占主导地位。同时,将东黑冠长臂猿二重唱的声谱结构与近缘种西黑冠长臂猿和海南长臂猿进行比较,结果显示雄性和雌性的叫声、以及二者配合发出的激动鸣叫序列在三者之间都有明显差异。因此,从声谱特征角度可以有效论证这三种长臂猿独立物种的分类地位。     

Effects of food and topography on ranging behavior of black crested gibbon (Nomascus concolor jingdongensis) in Wuliang Mountain, Yunnan, China

We studied the ranging behavior of a habituated group of black crested gibbons (Nomascus concolor jingdongensis) in a high, seasonal habitat on Mt. Wuliang, central Yunnan, China, between March 2005 and April 2006. Our results indicated that the total home range size for the study group was 129 ha, or 151 ha if the lacunae within the borders in which gibbons were not observed were included. This is a much bigger range size than that of other gibbon species. However, 69.7% of their activities occurred within 29 ha. The intensity of quadrant use was significantly correlated with the distribution of important food patches. The mean yearly daily path length was 1,391 m. Gibbons traveled farther when they spent more time feeding on fruit. To avoid often passing through ridges with little food, gibbons usually stayed in the same valley for successive days, and then moved on to another valley for another several days, which resulted in a concentrated ranging pattern.     

Population differences and acoustic stability in male songs of wild western black crested gibbons (Nomascus concolor) in Mt. Wuliang, Yunnan

Population differences and acoustic stability in male songs of the western black crested gibbon (Nomascus concolor) at Mt. Wuliang, Yunnan, were investigated using data collected over 4 years. Detectable vocal differences were found between the western and eastern populations within Mt. Wuliang. Discriminant functions calculated using the phrases recorded in 2007-2008 correctly classified phrases recorded in 2009, and discriminant functions produced from phrases recorded in 2007-2009 could correctly classify phrases recorded in 2010 for 4 of 5 males. Results showed that the male songs of western black crested gibbons remain relatively stable over years. In light of the acoustic individuality in male songs of this gibbon species, which has recently been proved, and the acoustic stability shown in this research, we suggest that the song of male individuals may be useful in monitoring individuals or family groups of this species.     

云南哀牢山平河黑长臂猿栖息地乔木结构分析

采用样方方法对栖息于云南省哀牢山平河(E101°17′16.1″,N24°20′09.5″,海拔2600m)的黑长臂猿(Nomascus concolor)栖息地乔木层结构进行了调查。调查中共记录到乔木57种隶属于23科37属;木质藤本植物9种隶属于6科8属。优势科主要为杜鹃花科(Ericaceae)、木兰科(Magnoliaceae)、山茶科(Theaceae)和壳斗科(Fagaceae)植物。主要树种重要值排序表明,露珠杜鹃(Rhododendron irroratum)为该地区最主要的优势种,在各坡位中均有广泛分布。乔木的多样性指数、均匀度指数在沟底明显降低,而乔木1层和2层所占的比例以及木质藤本的平均多度均随着坡位的下降而升高。与其他地区的长臂猿相比,哀牢山黑长臂猿的活动程度较低(10—22m),果实性食物种类较少。     

Gibbons under seasonal stress: the diet of the black crested gibbon (<Emphasis Type="Italic">Nomascus concolor</Emphasis>) on Mt. Wuliang,Central Yunnan,China

The diet of a habituated group of black crested gibbon (Nomascus concolor jingdongensis) was studied from March 2005 to April 2006 in the Wuliang Mountains, central Yunnan, China. Gibbons consumed 77 different plant species, one mammal-, two bird-, one lizard-, and two insect-species. Buds and leaves constituted 46.5% of the diet (21.0% vine leaves and buds, 19.2% tree leaves and buds, and 6.3% epiphyte leaves). Fruits, figs and flowers accounted for 25.5, 18.6 and 9.1% of the diet, respectively. There was marked seasonal variation in dietary proportions. Fruit varied from 0.3 to 82.7%; figs from 0 to 68.2%; tree leaves and buds from 1.5 to 83.3%; vine leaves and buds from 3.1 to 61.9%; and epiphyte leaves from 0 to 22.2% of the diet. Different food types dominated the diet in different months during the study period. The foli-frugivorous diet and extreme seasonal variation in the diet may be related to the harsh habitat of the study group.     

Phylogeny and distribution of crested gibbons (genus Nomascus) based on mitochondrial cytochrome b gene sequence data

Crested gibbons, genus Nomascus, are endemic to the Indochinese bioregion and occur only in Vietnam, Laos, Cambodia, and southern China. However, knowledge about the number of species to be recognized and their exact geographical distributions is still limited. To further elucidate the evolutionary history of crested gibbon species and to settle their distribution ranges, we analyzed the complete mitochondrial cytochrome b gene from 79 crested gibbon individuals from known locations. Based on our findings, crested gibbons should be classified into seven species. Within N. concolor, we recognize two subspecies, N. concolor concolor and N. concolor lu. Phylogenetic reconstructions indicate that the northernmost species, N. hainanus, N. nasutus, and N. concolor branched off first, suggesting that the genus originated in the north and successively migrated to the south. The most recent splits within Nomascus occurred between N. leucogenys and N. siki, and between Nomascus sp. and N. gabriellae. Based on our data, the currently postulated distributions of the latter four species have to be revised. Our study shows that molecular methods are a useful tool to elucidate phylogenetic relationships among crested gibbons and to determine species boundaries. Am. J. Primatol. 72:1047–1054, 2010. © 2010 Wiley‐Liss, Inc.