Group size and stability: Why do gibbons and spider monkeys differ?

Gibbons and spider monkeys have similar diets, body size, and locomotor patterns. They are therefore expected to be subject to similar socioecological rules. However their grouping patterns differ. Gibbons live in small stable groups, whereas spider monkey form unstable sub-groups that vary from small to large during different seasons. If similar principles apply to the two species, food abundance should vary more for spider monkeys than for gibbons; food density should be similar for the two species when spider monkey sub-groups are the same size as gibbon groups; and the highest level of food abundance should be higher for spider monkeys than for gibbons. These predictions are upheld for a comparison of particular populations ofHylobates muelleri andAteles geoffroyi.     

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。     

邦亮东黑冠长臂猿日食性与活动节律的季节性变化

日食性变化和活动节律是动物行为的重要方面,通过对日食性变化与活动节律的研究,可以了解食物、温度和光照时间等环境因素的变化对动物行为的影响,以及动物在行为上的应对策略。2009 年1 -12 月,在广西靖西县邦亮东部黑冠长臂猿自治区级自然保护区内,采用瞬时扫描取样法对2 群东黑冠长臂猿觅食行为和活动节律进行了研究。结果显示,东黑冠长臂猿的活动和食性在旱季和雨季都具有明显的节律。鸣叫只发生在12:00之前,但旱季的鸣叫时间偏晚。在日节律上,东黑冠长臂猿在离开过夜树后和进入过夜树前各有一个取食高峰,07:00 喜欢取食果实和无花果,16:00 也选择更多的果实,但无花果较少,13:00 - 15:00 取食更多的叶和芽。在10:00 - 12:00,其用于休息和社会活动的时间增加。在雨季,东黑冠长臂猿以果实和无花果为主要食物,并且花大量时间觅食无脊椎动物;但在旱季,其食物以叶和芽为主。与之相适应,东黑冠长臂猿在旱季通过减少移动增加休息来节约能量开支和应对低温,同时它们增加取食的时间以获得等价的能量和营养。雨季时社会行为的比例明显高于旱季,而且其高峰出现在08:00 - 10:00,但旱季社会行为主要出现在11:00 - 14:00。在雨季东黑冠长臂猿没有出现休息高峰,相反在旱季10:00 左右出现一个明显的休息高峰。上述行为节律体现了东黑冠长臂猿对环境季节性变化的良好适应,使其能够在寒冷并且退化的喀斯特森林中生存繁衍。     

Sleeping Tree Selection of Cao Vit Gibbon (Nomascus nasutus) Living in Degraded Karst Forest in Bangliang,Jingxi, China

We studied the sleep‐related behavior of two Cao Vit gibbon (Nomascus nasutus) groups in Bangliang Nature Reserve in Jingxi County, China between January 2008 and December 2009 to test four hypotheses related to sleeping tree selection (predation avoidance, thermoregulation, food access, and range defense). Gibbons entered sleeping trees 88 ± SD 37 min before sunset before their main potential nocturnal predator become active. They usually moved rapidly and straight to sleeping trees and kept silent once settled. Over the course of the study, gibbon groups used many (87 and 57 per group) sleeping trees and reused them irregularly. They also tended to sleep in relatively tall trees without lianas, choosing small branches close to the treetop. These behaviors would make it difficult for potential terrestrial predators to detect and approach the gibbons. Therefore, these results strongly support the predation avoidance hypothesis. Gibbons tended to sleep closer to ridges than to valley bottoms and they did not sleep at lower elevations in colder months. They thus appeared not to select sleeping trees to minimize thermoregulatory stress. Gibbons very rarely slept in feeding trees, instead generally sleeping more than 100 m away from the last feeding trees of the day or the first feeding tree of the next morning. These patterns led us to reject the food access hypothesis. Lastly, we did not find evidence to support the range defense hypothesis because gibbons did not sleep in overlap areas with neighbors more often than expected based on the proportion of overlap and exclusively used areas. Am. J. Primatol. 74:998‐1005, 2012. © 2012 Wiley Periodicals, Inc.     

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.     

Interactions between lar gibbons and pig-tailed macaques at fruit sources

Interactions are reported between white-handed gibbons (Hylobates lar) and pig-tailed macaques (Macaca nemestrina) in Khao Yai National Park, Thailand, in which gibbons selected ripe fruit from sources before macaques arrived on 4 occasions during June and July of 1989. The macaques foraged near gibbons or from shared fruit sources during 13% of gibbon observation time. Gibbons made their presence known in fruit trees when macaques approached on 3 occasions and macaques did not enter fruit trees occupied by gibbons. An aggressive interaction is reported in which a single white-handed gibbon vigorously excluded 22–28 macaques from a rare and valuable fruit tree (Sandoricum koetjape). The observations suggest that exploitative and interference competition may exist between these species.     

Sumatran Orangutans and a Yellow-Cheeked Crested Gibbon Know What Is Where

In their natural habitats orangutans and gibbons have to solve spatial problems to find enough food, which is distributed over large areas and available at different times of the year. Therefore both species should evolve spatial memory skills to remember spatial locations and their content. We conducted 2 studies in a 1900-m² naturalistic outdoor enclosure. In the 1st study, we hid kiwi pieces in 10 different locations and placed kiwi pieces in a visible location. Individuals of both species approached significantly more food locations in the test condition than in the control condition in which no food was hidden. In the 2nd study, we hid 2 types of food in 10 different locations so that individuals had to remember which food type was where. We hid bananas on trees (banana condition) and grapes under bamboo shrubs (grape condition). We also placed oranges in full view (control condition) to rule out the possibility that finding food may automatically trigger an indiscriminate search. Individuals approached the banana locations more often in the banana than in the other 2 conditions. Some orangutans, but not the gibbon, also approached the grape locations more often in the grape than in the other 2 conditions. Individuals often returned to locations in which they previously found food and rarely revisited locations in the same session. We detected little influence of the food quantity and no influence of the distance to each location on the subjects' foraging behavior.     

Black-footed ferret (Mustela nigripes) behavioral development: aboveground activity and juvenile play

We studied the behavioral development of black-footed ferrets (Mustela nigripes) from 6 to 16 post-natal weeks. At 6 weeks of age, kits are still lactating and depend on their mother for survival, while at 16 weeks, ferret young start achieving independence from their mother and littermates. Behavioral observations were obtained by placing videomonitors in the litters’ cages, nest boxes and in outdoor naturalistic enclosures. Captive-raised black-footed ferrets displayed nocturnal activity patterns, although they tended to appear aboveground at certain daytime hours presumably influenced by the established feeding and cleaning regimes. Growing ferrets began emerging aboveground at approximately 7 post-natal weeks and diel activity steadily increased as kits matured. The most manifest behavioral changes (appearance of new motor patterns, increase in aboveground play and in neck-biting behaviors) occurred from post-natal week 8 to week 12. This coincides with the period of maximum growth for ferrets and with a sensitive phase for the development of food preferences in this species. Changes from the 12 to the 16 post-natal weeks involved an increase in aboveground activity, including a higher frequency of scent-marking behaviors. Information provided in this study has important implications for enhancing the captive management of this endangered carnivore.     

Use of the forest canopy by the agile gibbon

Brachiation was the main form of locomotion and took place along branches and boughs in the upper canopy. The posture during feeding depended on the substrate, with the gibbons sitting on branches but hanging in twigs. During foraging the gibbons hung more, even on branches, but as only short stops were made this is probably to increase mobility. Feeding on fruit took place mainly in the middle canopy on small trees; feeding on leaves and foraging occurred evenly throughout the middle and upper canopies. Gibbons are light mobile animals with a rapid and direct form of locomotion that enables them to exploit dispersed food sources and to defend a large territory.     

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.     

Demography of Agile Gibbons (<Emphasis Type="Italic">Hylobates agilis</Emphasis>) in a Lowland Tropical Rain Forest of Southern Sumatra,Indonesia: Problems in Paradise

Gibbons are among the best-studied Asian primates, but few studies address their demography and life history strategies. We used annual censuses to study the demography of agile gibbons (Hylobates agilis) between 1998 and 2009 in rain forests of Bukit Barisan Selatan National Park, Indonesia. The population declined from 22 individuals (9 groups) to 14 individuals (5 groups) over the 12 yr of study. Infant survival to the juvenile age class was 33.3%, and 16.7% of infants survived to the subadult age class. The interbirth interval was 3.83 ± 1.15 yr and birth rate was 0.22–0.28 infants female^–1 yr^–1. Two groups colonized the study area but subsequently disappeared. We documented 7 immigrations, 17 disappearances, and ≥10 transients in the population. Compared to lar gibbons (Hylobates lar) and Bornean white-bearded gibbons (Hylobates albibarbis), Way Canguk’s agile gibbon population is characterized by slow reproduction, low survival, and high group turnover. We hypothesize that, although the habitat is high in fruit resources, agile gibbons may be displaced or excluded from the best fruit resources by larger and more numerous competitors, incurring costs of decreased opportunities to forage and increased travel, and leading to higher mortality for young agile gibbons. The reproductive potential of this agile gibbon population is insufficient to compensate for high mortality, and the population is unlikely to persist without immigration from outside the area. Given the agile gibbons’ endangered status and limited capacity to respond demographically to change, it is likely that intensive management interventions will be required to conserve this species.     

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.     

Comparisons of Suspensory Behaviors Among <Emphasis Type="Italic">Pygathrix cinerea</Emphasis>, <Emphasis Type="Italic">P. nemaeus</Emphasis>, and <Emphasis Type="Italic">Nomascus leucogenys</Emphasis> in Cuc Phuong National Park,Vietnam

In our study at the Endangered Primate Rescue Center of Cuc Phuong National Park, Vietnam, we aimed first to assemble a positional behavioral profile of captive gray-shanked (Pygathrix cinerea) and red-shanked (P. nemaeus) doucs that relates to the use of forelimb suspensory postures and arm-swinging locomotion. The profile is of interest because researchers have documented that red-shanked doucs more frequently use suspensory postures and locomotions than other colobines do. We confirmed that red-shanked doucs commonly use suspensory positional behaviors and also that gray-shanked doucs use suspensory behaviors at similar or even higher frequencies than those of red-shanked doucs. Our second goal was to assemble a preliminary kinematic profile of suspensory locomotion in Pygathrix within the context of the arm-swinging locomotion exhibited by northern white-cheeked gibbons, Nomascus leucogenys. Mean forelimb angles at initial contact and release of arm-swinging behaviors were remarkably consistent among gibbons and doucs despite the fact that gibbons typically used more continuous brachiation. Doucs also exhibit a greater range of forelimb angles than gibbons do. In addition, trunk orientation tends to be less vertical at initial contact for doucs than for gibbons, perhaps owing to the frequent use of quadrupedal sequences directly before or after forelimb suspension. Our behavioral and kinematic analyses add to the emerging realization that Pygathrix is capable of, and frequently expresses, a range of suspensory positional behaviors, including brachiation.     

The extraordinary athletic performance of leaping gibbons

The distance that animals leap depends on their take-off angle and velocity. The velocity is generated solely by mechanical work during the push-off phase of standing-start leaps. Gibbons are capable of exceptional leaping performance, crossing gaps in the forest canopy exceeding 10 m, yet possess none of the adaptations possessed by specialist leapers synonymous with maximizing mechanical work. To understand this impressive performance, we recorded leaps of the gibbons exceeding 3.7 m. Gibbons perform more mass-specific work (35.4 J kg(-1)) than reported for any other species to date, accelerating to 8.3 ms(-1) in a single movement and redefining our estimates of work performance by animals. This energy (enough for a 3.5 m vertical leap) is 60 per cent higher than that achieved by galagos, which are renowned for their remarkable leaping performance. The gibbons' unusual morphology facilitates a division of labour among the hind limbs, forelimbs and trunk, resulting in modest power requirements compared with more specialized leapers.     

Cues to Androgens and Quality in Male Gibbon Songs

Animal vocal signals may provide information about senders and mediate important social interactions like sexual competition, territory maintenance and mate selection. Hence, it is important to understand whether vocal signals provide accurate information about animal attributes or status. Gibbons are non-human primates that produce loud, distinctive and melodious vocalizations resembling more those of birds than of other non-human primates. Wild gibbons are characterized by flexibility in social organization (i.e., pairs and multimale units) as well as in mating system (i.e., monogamy and polyandry). Such features make them a suitable model to investigate whether the physiology (hormonal status) and socio-demographic features find their correspondence in the structure of their songs. By combining male solo song recordings, endocrine outputs using non-invasive fecal androgen measures and behavioral observations, we studied 14 groups (10 pair-living, 4 multimale) of wild white-handed gibbons (Hylobates lar) residing at Khao Yai National Park, Thailand. We collected a total of 322 fecal samples and recorded 48 songs from 18 adult animals. Our results confirmed inter-individuality in male gibbon songs, and showed a clear correlation between androgen levels and song structures. Gibbons with higher androgen levels produced calls having higher pitch, and similarly adult individuals produced longer calls than senior males. Thus, it is plausible that gibbon vocalizations provide receivers with information about singers'' attributes.     

Concordance between vocal and genetic diversity in crested gibbons

Background  

Gibbons or small apes are, next to great apes, our closest living relatives, and form the most diverse group of contemporary hominoids. A characteristic trait of gibbons is their species-specific song structure, which, however, exhibits a certain amount of inter- and intra-individual variation. Although differences in gibbon song structure are routinely applied as taxonomic tool to identify subspecies and species, it remains unclear to which degree acoustic and phylogenetic differences are correlated. To trace this issue, we comparatively analyse song recordings and mitochondrial cytochrome b gene sequence data from 22 gibbon populations representing six of the seven crested gibbon species (genus Nomascus). In addition, we address whether song similarity and geographic distribution can support a recent hypothesis about the biogeographic history of crested gibbons.     

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.     

Variation in the leaping of lemurs

Locomotor diversity among lemurids has been ignored by placing most species into a category of arboreal quadrupeds. Recent field studies have shown that leaping behaviors comprise a relatively large amount of their travel. In this contribution I detail a study of captive lemurs locomoting on a designed support network and/or in outdoor enclosures. Associations between support context, leaping behaviors, and landing kinematics are detailed for Hapalemur griseus, Eulemur rubriventer, Eulemur fulvus, Eulemur mongoz, and Varecia variegata. In-air body position, including the amount and location of trunk flexion, coupled with the extent of shoulder and hip flexion dictates limb use at landing. Limb strike pattern when landing onto the same support type varies interspecifically. The kinematic variation in leaping behaviors may well have implications for functional analyses of the postcranium. © 1996 Wiley-Liss, Inc.     

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.     

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。