A preliminary study of food transfer in Sichuan snub-nosed monkeys (Rhinopithecus roxellana)

Food transfer happens regularly in a few nonhuman primates species that are also characterized by remarkable social tolerance. Sichuan snub-nosed monkeys (Rhinopithecus roxellana), or golden monkeys, which exhibit high social tolerance in their social relationships are thus of interest to see whether tolerance would extend to food transfer. In this study, branch feeding activity was observed in a semi-captive group of Sichuan snub-nosed monkeys, which consisted of 10 subjects that included a one-male unit (OMU) and an all-male unit (AMU). We recorded 1,275 food interactions over 27 days, and 892 instances of food transfer. The most commonly observed types of food transfer behavior were co-feeding (62.1%) and relaxed claim (22.8%). Of 892 food transfers, 756 (84.8%) took place in the OMU, most of which were among adults (34.7%) and among juveniles (42.1%). The transfer success rate was high in both the cases (87.9% for adults and 78.9% for juveniles). Food transfer in the AMU took place less often than that among adults in the OMU though with similar high transfer success. Food transfer between the OMU and AMU was limited to juvenile males from the OMU and adults from the AMU. These results provide the first evidence of food transfer in golden monkeys and suggest that tolerant social relationships in golden monkeys make transfer possible.     

Postconflict behavior among female Sichuan snub-nosed monkeys Rhinopithecus roxellana within one-male units in the Qinling Mountains, China

For group-living primates, the information on postconflict management is crucial for understanding primate competition and cooperation. However, such information is poorly known for snub-nosed monkeys, especially for wild populations. In this study, from September 2007 to June 2008, we investigated postconflict behavior among adult females Sichuan snub-nosed monkeys Rhinopithecus roxellana within one-male units in a wild, provisioned group in the Qinling Mountains of China by means of the time-rule method and the PC-MC method. We obtained a total of 81 PC-MC pairs and each individual was involved in only 0.004 aggressive behavior per observation hour. The first affiliative behavior was more likely to occur within the first minute after a conflict. The postconflict affiliative behaviors most often seen were contact-sit, embrace and grooming. The affiliative contacts between adult females occur due to selective attraction, I.e. Reconciliation. The pattern of postconflict affiliation demonstrates that the R. Roxellana belongs to a tolerant species.     

A preliminary study on the function of food begging in Sichuan snub-nosed monkeys (Rhinopithecus roxellana): challenge to begging for nutritional gain

Several hypotheses have been developed to explain what benefits a donor may gain from sharing food with another individual, with nutritional gain assumed to be the sole benefit for the beggar. Recently, it has been proposed that begging behaviour serves a social function in non-human primates. In this study, the nutritional-gain assumption was again challenged based on observations on a captive group of Sichuan snub-nosed monkeys (Rhinopithecus roxellana), or golden snub-nosed monkeys. The major findings from this study are that (1) beggars sometimes left their own branches or passed by available branches to beg for similar food from other individuals, (2) beggars occasionally ignored branches that were acquired by begging and (3) food begging occurred more frequently in the all-male unit after the social rank had changed between 2 individuals in this unit. Overall, these preliminary findings suggest that some begging behaviours in captive golden snub-nosed monkeys were not driven by nutritional gain only; instead, we propose that these begging behaviours could be interpreted as attempts at deriving social benefits.     

Social play behavior in infant Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in Qinling Mountains, China

We describe the development of social play behavior and assess factors influencing the development of play in infant Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Infant snub-nosed monkeys began to exhibit social play at 3 months of age, when they spent an average 0.89% of time engaging in this behavior (range: 0.7-1.12%). At 6 months of age, there was a significant increase in the proportion of time spent in social play, averaging 9.78% of observation time (range: 4.92-17.08%). However, from 7 to 9 months of age during the winter, social play decreased gradually before rising again from 10 months of age in the spring. Play behavior in infant snub-nosed monkeys is influenced by environmental temperature. Males were observed to play more than females, although further data on this are required. Social rank did not influence the social play of wild Sichuan snub-nosed monkey infants.     

川金丝猴食谱的地域性差异比较

对不同地区川金丝猴食物组成的比较有助于了解其对不同生境食物供应的适应性。本研究通过对陕西川金丝猴猴群食谱的长期记录,并汇集了国内对四川-甘肃和湖北的川金丝猴食性研究结果,集成了这三个地理种群川金丝猴各自的地域性食谱,共计有136 种植物(隶属35 科)被该物种作为采食对象。对来自这三个不同区域(陕西、四川-甘肃、湖北)的川金丝猴食谱组成的比较,发现有近半数的植物是三个地理种群共同的采食对象,但其食谱组成差异明显。这可能源于各地植物本身的多样性差异,及不同地理种群对各种食物采食偏好的不同所致。对其相关聚类分析结果显示,陕西和湖北的猴群在食谱组成上相近,但四川-甘肃的猴群与前两个地区猴群的食谱组成差异极大。然而湖北和四川-甘肃种群在食物的选择上采用了近乎相同的偏好倾向,而陕西的猴群与它们明显不同。我们初步分析认为造成食谱组成和采食偏好差异的原因可能是各地理种群活动地海拔带重叠度不同、森林类型不同、它们在不同林型中活动的时间分配不一。很明显,就我们目前所掌握的有关川金丝猴食谱组成来看,该物种不应该仅仅被认为是一个叶食性灵长类动物,而应该是一个泛化采食者。     

Activity budgets in a group of Sichuan snub-nosed monkeys in Shennongjia Nature Reserve, China

We examined time allocation by Sichuan snub-nosed monkeys Rhinopithecus roxellana in the montane,temperate and highly seasonal forests of the Shennongjia Nature Reserve in China,in order to improve our understanding of the ecological and social influences on monkey behavior.We collected data on activity budgets in relation to food availability in a group of monkeys from July 2003 to September 2004(except February 2004),using instantaneous scan samples.The monkeys spent 36.21% of daytime moving(n=21,269 reco...     

A Proximity-Based Social Network of a Group of Sichuan Snub-Nosed Monkeys (Rhinopithecus roxellana)

Studies of spatial proximity between individuals are important for an understanding of social structure because animals are more likely to interact with individuals in close spatial proximity. Here, we apply social network analysis to proximity data collected between 2001 and 2003 from an individually identified, provisioned, free-ranging band of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains, central China. We aimed to quantify the social network structure and to gain insight into each individual’s position within the social network. The overall network connectivity of the study band was sparse, with a low group density of 0.17. We identified nine one-male-multifemale units (OMUs) in the study band using hierarchical cluster analysis, which confirms that this species forms a multilevel society in its natural habitat. Based on sex differences in eigenvector and betweenness centralities, adult females have more important social roles than males. Among females, lactating females scored higher betweenness and eigenvector centralities than other females. However, our results do not suggest the existence of key individual(s) in the social network of the study band. The global clustering coefficient characteristic of the band was 0.3?±?0.1, with little variation between individuals, suggesting that the removal or death of any specific individual would not significantly disrupt its general network structure. Our results also show that proximity commonly occurs among unit members, but can also occur between females of different OMUs. These observations suggest that snub-nosed monkeys have a loose-knit or fluid rather than a rigid female-bonded social system, which may be a common trend for species living in multilevel societies.     

川金丝猴秦岭与岷山社群社会结构与空间分布差异性比较

对不同地区川金丝猴社会结构和空间分布的比较有助于了解其种群与环境的相互应答关系。在秦岭山脉和岷山山脉的不同地区选取3个观察群,对比它们之间社群结构和空间分布的差异。研究结果表明,尽管同属于仰鼻猴属川金丝猴种,由于栖息地环境的不同,导致社群结构和空间分布既存在相同点又存在一定的差异。对于社会结构,扎如沟群,大坪峪群与玉皇庙群表现出同样的最高进化水平的重层社会体系;但是构成这一社会体系的基本单位一雄多雌（One-male unit,OMU）,其成员整体数量上没有差异,但是OMU内雌雄比例不仅在3个观察群间存在差异,而且与同属其他物种相比也存在差异;对于空间分布,由于食物竞争压力和天敌捕食压力在不同的栖息地内影响不同,导致3个观察群空间分布呈梯度变化关系。研究结果不仅为川金丝猴种群动态,种群与环境的相互应答关系以及种群进化提供基础资料,而且希望能藉此推进我国相关领域研究的开展,为灵长类社会与行为生态学研究者启发思路,并为保护这些濒危物种提供科学依据。     

滇金丝猴雌性个体间的理毛行为

相互理毛行为广泛存在于社会性群居灵长类动物中,通常具有清洁卫生和社会交往功能。2012 年10 月至2013 年6 月,我们在云南白马雪山国家级自然保护区对一人工辅助投食滇金丝猴群,采用全事件取样法和焦点动物取样法收集了雌性个体间相互理毛的行为数据,包括理毛的部位、理毛的姿势、理毛的时间和回合数。研究结果表明:滇金丝猴雌性个体之间每次相互理毛的平均时间为5. 7 min。相互理毛部位较多的发生在自我理毛不能进行(达到)的部位(61.1% );在不能自我理毛部位的相互理毛行为持续时间长,平均9.7 min;在个体能够进行自我理毛部位的相互理毛持续时间短,平均为3. 2 min。相互理毛的姿势以对坐为主(48. 4% ),不同理毛姿势的理毛时间差异显著。新迁入家庭单元的雌性个体为理毛的首先发起者,但其获得被理毛的时间却并不多。滇金丝猴雌性个体相互理毛部位、理毛姿势和理毛时间的差异表明,它们之间的相互理毛行为符合卫生功能假说和社会功能假说。     

Identification of 13 Human Microsatellite Markers via Cross-species Amplification of Fecal Samples from Rhinopithecus bieti

Yunnan snub-nosed monkeys (Rhinopithecus bieti) are 1 of 3 snub-nosed monkey species endemic to China. Only ca. 1500 individuals remain in high-altitude forests 3000–4500 m above sea level on the Tibetan Plateau, making them the nonhuman primate living at the highest known elevation. It is one of the most endangered 25 primate species in the world. Proper knowledge of the population genetics and social system of Rhinopithecus bieti will contribute to more appropriate conservation management decisions. Cross-species amplification of human microsatellite loci has facilitated analysis of the population genetics and reproductive strategies of various primate species. We screened 72 human-derived markers to assess their utility in Yunnan snub-nosed monkeys. Thirteen of them produced reliable results and exhibited moderate levels of polymorphism.     

笼养川金丝猴理毛行为功能

<正>理毛行为(Grooming behavior)的定义是动物个体对自身或其同类个体体表(皮肤、毛发或羽毛等)进行的多种形式护理,包括对体表进行有规律的梳理,以及用舌头或嘴唇舔皮肤和毛发等(Veà et al., 1999)。在灵长类动物中,理毛行为大多表现为个体接触和探查自身或另一个体体表被毛,将毛发分开后从中拣出盐粒或皮肤寄生物放入口中咀嚼或直接用嘴咬食被毛下的盐粒或皮肤寄生物(李银华和李保国, 2002)。依据理毛接收对象的不同,可将     

Reciprocal altruism in bats and other mammals

In this paper five conditions are specified which must be met before reciprocal altruism, rather than kin selection, should be invoked. Four purported mammalian examples— social grooming in coati, cluster position in roosting pallid bats, information exchange among greater spear-nosed bats, and blood regurgitation among vampire bats—are examined to determine if reciprocal altruism is necessary to plausibly explain each situation. Results from a computer simulation which apportions the relative selective advantage of vampire bat food sharing to kin selection and reciprocal altruism are then presented. The results demonstrate that the increase in individual survivorship due to reciprocal food sharing events in this species provides a greater increase in inclusive fitness than can be attributed to aiding relatives. This analysis suggests that reciprocal altruism can be selectively more important than kin selection when altruistic behaviors in a relatively large social group occur frequently and provide a major fitness benefit to the recipient even when that recipient is related to the donor.     

唐家河国家级自然保护区川金丝猴生境适宜性评价

生境适宜性评价是濒危物种保护的重要基础。川金丝猴（Rhinopithecus roxellana）是栖息于温带森林的、中国特有的珍稀灵长类动物。位于岷山山系的四川唐家河国家级自然保护区是川金丝猴的重要分布地之一,但涉及该地区川金丝猴的生境信息却较缺乏。运用最大熵（Maximum entropy,MaxEnt）模型对四川唐家河国家级自然保护区川金丝猴不同季节的生境适宜性进行了研究,发现四个季节的训练集和验证集的受试者工作特征曲线下面积（Area under the receiver operator characteristic curve,AUC）值均超过0.8,说明模型预测结果较好。结果显示：（1）影响不同季节川金丝猴分布的主要因子是海拔、河流和道路。（2）川金丝猴的适宜生境面积存在季节性变化。其中,春季的适宜生境面积最大,为233.94 km²,占全区面积的58.48%;夏季的次之,为192.75 km²,占48.19%;秋冬季的适宜生境面积相对较低,分别为145.54 km²（占36.39%）和142.63 km²（占35.66%）。（3）川金丝猴的适宜生境分布具有明显的季节性垂直变化。研究揭示保护好完整的森林植被带对川金丝猴的生存具有重要意义,尤其要重视对人为干扰较强的低海拔生境的保护。     

Testing the Cognition of the Forgotten Colobines: A First Look at Golden Snub-Nosed Monkeys (Rhinopithecus roxellana)

Although our understanding of primate cognition is growing rapidly, little is known about the cognition of colobines. Here we report the results of a set of 5 experiments on colobine cognition using 17 golden snub-nosed monkeys (Rhinopithecus roxellana). These monkeys are folivores that form multilevel societies with groups of hundreds of individuals and relatively high fission–fusion dynamics. We investigated their sensitivity to human social cues and ability to inhibit impulsive behavioral responses. In three sociocognitive experiments we found that, like most other primates, they follow the gaze direction of a human demonstrator but there is no evidence that they use others’ social cues in a cooperative task to locate hidden food or in a competitive task to steal forbidden food. In two inhibitory control experiments, we found that the monkeys showed a low level of inhibitory control, comparable to that of other folivorous primates. These results suggest that phylogeny and folivory might have been important in shaping the cognition of golden snub-nosed monkeys. Moreover, this species’ large group size and relatively high fission–fusion dynamics may not have imposed a significant social challenge to their cognition, as social interactions occur mainly within basic social units.     

Diet and feeding behavior of Rhinopithecus bieti at Xiaochangdu, Tibet: adaptations to a marginal environment

The diet and feeding ecology of a wild subpopulation of black-and-white snub-nosed monkeys (Rhinopithecus bieti) were studied at Xiaochangdu in Honglaxueshan Nature Reserve, Tibet. This region is climatologically harsher than any other inhabited by non-human primates. Black-and-white snub-nosed monkeys fed on 48 parts of 25 plant species, at least three species of lichens and seven species of invertebrates. The number of food items exploited varied markedly among seasons, with dietary diversity being greatest in spring and summer. In winter, black-and-white snub-nosed monkeys had to subsist on fallback foods such as dried grass and bark. Ubiquitous lichens formed a major dietary constituent throughout the year, contributing about 75% of feeding records. Even though lichens act as a staple, our findings signify that the monkeys at Xiaochangdu prefer feeding on foliage, which is higher in protein content than the former. We provide evidence that black-and-white snub-nosed monkeys are able to cope with an array of food items other than lichens and hence can be regarded as feeding generalists. We discuss the results with reference to previous studies on other subpopulations living in habitats that are floristically more diverse and offer more plant food items than the marginal habitat at Xiaochangdu.     

Fecal Bacterial Composition of Sichuan Snub-Nosed Monkeys (<Emphasis Type="Italic">Rhinopithecus roxellana</Emphasis>)

The intestinal microbiota plays an important role in maintaining the health of its host, including human and nonhuman primates. Little is known about the intestinal bacterial composition of the Sichuan snub-nosed monkey (Rhinopithecus roxellana), which has been classified as Endangered on the International Union for Conservation of Nature Red List since 2003. We evaluated the fecal bacterial compositions of 11 Sichuan snub-nosed monkeys, including six young captive individuals (one sample from each), three adult captive individuals (four samples each), and two adult provisioned free-ranging individuals (four samples each). We also quantified fecal Bacteroides vulgatus, Bifidobacterium spp., and Lactobacillus spp., which are defined as probiotics in humans, using real-time polymerase chain reaction. We identified five major phyla in the collected samples, including Firmicutes (32.4 %), Bacteroidetes (14.7 %), Verrucomicrobia (8.8 %), Actinobacteria (4.4 %), and unclassified microbacteria (39.7 %). Fecal bacteria composition varied with age and different seasons. The fecal bacterial composition of the captive monkeys was less variable than that of provisioned free-ranging monkeys. B. vulgatus amounts were almost 100 times higher in the provisioned free-ranging monkeys (10¹²) than in the captive monkeys (10¹⁰). Our results provide an initial catalogue of gut microbiota in the Sichuan snub-nosed monkey, which helps to enrich our knowledge of gut microbiota in nonhuman primates.     

神农架川金丝猴投食群的社会行为谱

为探讨人工投食条件下川金丝猴的社会行为类型,2007年1月-2008年10月,采用行为取样法和全事件记录法对湖北神农架自然保护区投食猴群的社会行为进行观察。确定投食群有45种典型社会行为,其中打架、抢食、抱腰、吻背、爬伏、邀配与以往对笼养和野生川金丝猴的研究有差别。     

Nutrient Balancing by Captive Golden Snub-Nosed Monkeys <Emphasis Type="Italic">(Rhinopithecus roxellana</Emphasis>)

An organism’s fitness is tied closely to its ability to obtain food. However, many foods are nutritionally suboptimal on their own, forcing an individual to develop a feeding strategy that actively manages both type and amount of food consumed. Animals in captivity are additionally limited to human provisioned diets, which may be nutritionally inadequate and negatively affect behavior and health. We studied the nutritional intake of captive golden snub-nosed monkeys (Rhinopithecus roxellana) at two locations in China (132 days of continuous, sunrise to sunset focal samples of 7 individuals at each site) and used the Geometric Framework for nutrition to identify their feeding strategy and evaluate diet variation across sites, seasons, and age–sex classes. Captive golden snub-nosed monkeys had a mean nutrient intake of 75% carbohydrates (15% neutral detergent fiber, 60% total nonstructural carbohydrates), 12% fat, and 13% protein (by energy) that differed by location and season owing to differences in the type and amount of food items offered and consumed. Intake at one location differed from that of wild golden snub-nosed monkeys, suggesting that the captive diet was inadequate. These results highlight the importance of developing nutritionally adequate diets for captive animals based on an understanding of their nutritional requirements.     

Social Behavior,Reproductive Strategies,and Population Genetic Structure of <Emphasis Type="Italic">Lagothrix poeppigii</Emphasis>

For species of primates in which females emigrate, we would expect males within groups to be related to one another. Kin selection theory suggests that these males should associate preferentially with one another, be more affiliative and cooperative with one another than females are, and compete less overtly with one another over reproductive opportunities than males in female philopatric taxa do. Precisely these patterns of social behavior characterize well-studied populations of 2 of the 3 atelin primate genera: spider monkeys (Ateles) and muriquis (Brachyteles). For the third atelin genus, Lagothrix, patterns of intragroup social behavior have been less well-documented. We studied the social and reproductive behavior of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in Ecuador during a one-year observational study and subsequently used molecular techniques to investigate population genetic structure and dispersal patterns for this taxon. Among adult male woolly monkeys, both affiliative and agonistic interactions were rare, and males were seldom in close proximity to one another. Relationships among male woolly monkeys are best characterized as tolerant, especially in the context of mating wherein direct competition among males was minimal despite the fact that females mated with multiple males. Relationships among females were likewise generally tolerant but nonaffiliative, though females often directed harassment towards copulating pairs. Affiliative interactions that did occur among woolly monkeys tended to be directed either between the sexes—primarily from female to male—or from younger towards older males, and the proximity partners of females tended to be members of the opposite sex. These results suggest that bonds between the sexes may be more important than same-sex social relationships and that direct female-female competition is an important feature of woolly monkey reproductive biology. Our genetic results indicate that, as in other atelins, dispersal by females is common, but some male dispersal likely occurs as well. In some but not all groups we studied, nonjuvenile males within social groups were more closely related to one another on average than females were, which is consistent with greater male than female philopatry. However, differences in these patterns among our study groups may reflect local variation in dispersal behavior.     

Cooperative nest defence in red-winged blackbirds: reciprocal altruism,kinship or by-product mutualism?

Male red-winged blackbirds (Agelaius phoeniceus) often cooperate with their neighbours in defending nests against predators. Some studies have suggested that this is an example of by-product mutualism, whereas others have suggested the possibility of reciprocal altruism. No study has addressed the possibility of kin-selected cooperation in nest defence in this species. Reciprocal altruism, kin selection and by-product mutualism are not mutually exclusive alternatives, but few studies of territorial neighbours have tested for multiple mechanisms simultaneously. We test for these three possibilities in a population of red-winged blackbirds. We used simulated defections to test for reciprocal altruism. We used analysis of microsatellite loci to test for kin selection between adult male neighbours. We also used microsatellite loci to test for by-product mutualism resulting from nest defence of offspring sired on neighbouring territories. We found that male red-winged blackbirds cooperate in nest defence primarily as a form of reciprocal altruism. Experimental males reduced their level of nest defence relative to controls following simulated defection by a neighbour. In contrast to some earlier studies, we found no evidence for by-product mutualism: males did not defend nests where they had sired extra-pair offspring. We also found no evidence for kin selection: males were no more cooperative with more closely related neighbours. Considered alongside the results from other studies, our study suggests that mechanisms stabilizing cooperation in red-winged blackbirds may vary among populations.