Protected areas (PAs) are essential to the success of global biodiversity conservation, and effectiveness evaluations with quantitative indexes are critically needed to enhance PA performance. Although species richness has been widely used as an index, it is naturally different among ecoregions, making large scale comparison across ecoregions inappropriate. Here, we suggest using the completeness index (CI) and defaunation index (DI) of animal communities as alternative indexes. We compiled a camera-trapping dataset consisting of over 2,023,000 camera days and 619,000 independent detections of 98 medium- and large-bodied mammals (MLMs) in 115 Chinese nature reserves. We then assessed CI and DI of MLMs for each reserve, and identified the environmental and social economic variables that may affect these indexes. We found that CIs and DIs varied greatly among these reserves, and we provided a list of reserves with high conservation priority (with high CIs) and those require restoration efforts (with high DIs). Furthermore, we found that medium-bodied mammals had a higher DI than large-bodied, herbivores had a higher DI than omnivores, and protected species had a higher DI than unprotected species. We also found that MLM communities were better retained in PAs with higher elevation and lower temperature. PA size, the reduction of human disturbances by PA, and scientific research also contributed to MLM community conservation. Our study provides suggestions to improve PA management in China, and demonstrates a new framework to evaluate conservation effectiveness of PAs across ecoregions.

Wild animals face numerous challenges in less ideal habitats, including the lack of food as well as changes in diet. Understanding how the gut microbiomes of wild animals adapt to changes in food resources within suboptimal habitats is critical for their survival. Therefore, we conducted a longitudinal sampling of three gibbon species living in high-quality (Nomascus hainanus) and suboptimal (Nomascus concolor and Hoolock tianxing) habitats to address the dynamics of gut microbiome assembly over one year. The three gibbon species exhibited significantly different gut microbial diversity and composition. N. hainanus showed the lowest alpha diversity and highest nestedness, suggesting a more specialized and potentially stable microbial community in terms of composition, while H. tianxing displayed high species turnover and low nestedness, reflecting a more dynamic microbial ecosystem, which may indicate greater sensitivity to environmental changes or a flexible response to habitat variability. The gut microbial community of N. concolor was influenced by homogeneous selection in the deterministic process, primarily driven by Prevotellaceae. In contrast, the gut microbial communities of H. tianxing and N. hainanus were influenced by dispersal limitation in the stochastic process, driven by Acholeplasmataceae and Fibrobacterota, respectively. Further, the microbial response patterns to leaf feeding in N. hainanus differed from those of the other two gibbon species. In conclusion, this first cross-species comparative study provides initial insights into the different ecological adaptive strategies of gut microbiomes from a point of community assembly, which could contribute to the long-term conservation of wild primates.In this study, we conducted longitudinal sampling of three gibbon species living in high-quality (Nomascus hainanus) and suboptimal (Nomascus concolor and Hoolock tianxing) habitats to address the dynamics of gut microbiome (composition, alpha diversity, beta diversity and assembly process) over one year.

Understory plantation of cardamom (genus Amomum) is an ancient and widespread agroforestry practice in the eastern Himalayas and Southeast Asia, an area that supports high regional biodiversity. Cardamom provides an important cash income to rural people, and governments encourage cardamom cultivation as a replacement for slash-and-burn agriculture to alleviate poverty, aligning with the principles of the Globally Important Agricultural Heritage Systems (GIAHS) program initiated by the FAO. This program recognizes and supports traditional agricultural practices that contributes to biodiversity conservation and sustainable development. In this context, cardamom agroforestry not only supports local economies but also provides crucial habitat for animals, including the newly described skywalker hoolock gibbon (Hoolock tianxing). Nearly half of the remnant population of the skywalker hoolock gibbon lives in cardamom agroforest. In order to evaluate if gibbons could survive in cardamom agroforest for a relatively long term, we compared foraging behavior of gibbons over a year living in cardamom agroforests (group NA) and well-preserved forests (group BB) in Mt. Gaoligong, Yunnan, China. In response to habitat degradation caused by cardamom plantation, group NA increased feeding time and spent more time feeding on leaves. Notably, they consumed nuts of Castanopsis hystrix which is an unusual food type for gibbons. On the contrary, members of group BB rarely ate nuts though Castanopsis hystrix is abundant within its home range. However, group NA did not occupy a large home range, or travel longer in time or distance than group BB. We also monitored female reproduction of five groups for 5–13 years. Two adult females living in agroforests successfully reared two or three offspring with an inter-birth interval of five years. In addition, we surveyed group size of 16 groups (9 in agroforest vs. 7 in well preserved forests) from 2017 to 2023, and we found no significant difference in group size between habitats. Our results suggested that cardamom agroforest can sustain skywalker hoolock gibbons provided it is not too fragmented and hunting is prohibited.

It has been extensively studied that the gut microbiome provides animals flexibility to adapt to food variability. Yet, how gut phageome responds to diet variation of wild animals remains unexplored. Here, we analyze the eco-evolutionary dynamics of gut phageome in six wild gibbons ( Hoolock tianxing ) by collecting individually-resolved fresh fecal samples and parallel feeding behavior data for 15 consecutive months. Application of complementary viral and microbial metagenomics recovers 39,198 virulent and temperate phage genomes from the feces. Hierarchical cluster analyses show remarkable seasonal diet variations in gibbons. From high-fruit to high-leaf feeding period, the abundances of phage populations are seasonally fluctuated, especially driven by the increased abundance of virulent phages that kill the Lachnospiraceae hosts, and a decreased abundance of temperate phages that piggyback the Bacteroidaceae hosts. Functional profiling reveals an enrichment through horizontal gene transfers of toxin-antitoxin genes on temperate phage genomes in high-leaf season, potentially conferring benefits to their prokaryotic hosts. The phage-host ecological dynamics are driven by the coevolutionary processes which select for tail fiber and DNA primase genes on virulent and temperate phage genomes, respectively. Our results highlight complex phageome-microbiome interactions as a key feature of the gibbon gut microbial ecosystem responding to the seasonal diet.

Planning for the future is a complex skill that is often considered uniquely human. This cognitive ability has never been investigated in wild gibbons (Hylobatidae). Here we evaluated the movement patterns from sleeping trees to out-of-sight breakfast trees in two groups of endangered skywalker gibbons (Hoolock tianxing). These Asian apes inhabit a cold seasonal montane forest in southwestern China. After controlling for possible confounding variables including group size, sleeping pattern (sleep alone or huddle together), rainfall and temperature, we found that food type (fruits or leaves) of the breakfast tree was the most important factor affecting gibbon movement patterns. Fruit breakfast trees were more distant from sleeping trees compared with leaf trees. Gibbons left sleeping trees and arrived at breakfast trees earlier when they fed on fruits compared with leaves. They travelled fast when breakfast trees were located further away from the sleeping trees. Our study suggests that gibbons had foraging goals in mind and plan their departure times accordingly. This ability may reflect a capacity for route-planning, which would enable them to effectively exploit highly dispersed fruit resources in high-altitude montane forests.

Wild animals may encounter multiple challenges especially food shortage and altered diet composition in their suboptimal ranges. Yet, how the gut microbiome responds to dietary changes remains poorly understood. Prior studies on wild animal microbiomes have typically leaned upon relatively coarse dietary records and individually unresolved fecal samples. Here, we conducted a longitudinal study integrating 514 time-series individually recognized fecal samples with parallel fine-grained dietary data from two Skywalker hoolock gibbon (Hoolock tianxing) groups populating high-altitude mountainous forests in western Yunnan Province, China. 16S rRNA gene amplicon sequencing showed a remarkable seasonal fluctuation in the gibbons' gut microbial community structure both across individuals and between the social groups, especially driven by the relative abundances of Lanchnospiraceae and Oscillospiraceae associated with fluctuating consumption of leaf. Metagenomic functional profiling revealed that diverse metabolisms associated with cellulose degradation and short-chain fatty acids (SCFAs) production were enriched in the high-leaf periods possibly to compensate for energy intake. Genome-resolved metagenomics further enabled the resolving metabolic capacities associated with carbohydrate breakdown among community members which exhibited a high degree of functional redundancy. Our results highlight a taxonomically and functionally sensitive gut microbiome actively responding to the seasonally shifting diet, facilitating the survival and reproduction of the endangered gibbon species in their suboptimal habitats.

Finding suitable sleeping sites is highly advantageous but challenging for wild animals. While suitable sleeping sites provide protection against predators and enhance sleep quality, these sites are heterogeneously distributed in space. Thus, animals may generate memories associated with suitable sleeping sites to be able to approach them efficiently when needed. Here, we examined traveling trajectories (i.e., direction, linearity, and speed of traveling) in relation to sleeping sites to assess whether Skywalker gibbons (Hoolock tianxing) use spatial memory to locate sleeping trees. Our results show that about 30% of the sleeping trees were efficiently revisited by gibbons and the recursive use of trees was higher than a randomly simulated visiting pattern. When gibbons left the last feeding tree for the day, they traveled in a linear fashion to sleeping sites out-of-sight (> 40 m away), and linearity of travel to sleeping trees out-of-sight was higher than 0.800 for all individuals. The speed of the traveling trajectories to sleeping sites out-of-sight increased not only as sunset approached, but also when daily rainfall increased. These results suggest that gibbons likely optimized their trajectories to reach sleeping sites under increasing conditions of predatory risk (i.e., nocturnal predators) and uncomfortable weather. Our study provides novel evidence on the use of spatial memory to locate sleeping sites through analyses of movement patterns, which adds to an already extensive body of literature linking cognitive processes and sleeping patterns in human and non-human animals.

开展灵长类动物栖息地食物的可获得性研究,对于了解它们的进化稳定策略具有十分重要的科学意义,也能够指导珍稀灵长类动物的保护管理.通过对川金丝猴取食行为的观察和植物物候的观测研究发现,不同季节之间川金丝猴对芽、花、叶、果实/种子的取食存在显著的季节性差异;保护区川金丝猴主要食物(花、叶、果实/种子)的可获得性在不同月份之间存有显著差异,5月芽的可获得性达到最大值44.5％,6月花的可获得性最高51.3％,8月树叶的可获得性最高97.7％,9月果实/种子的可获得性最大,达到64％.研究结果表明,保护区川金丝猴群的不同季节食谱构成与栖息地内食物的可获得性呈显著的正相关性;猴群对栖息地类型和海拔带的利用强度与食物的可获得性存在密切关联.

2016年12月—2017年12月,利用红外相机技术对重庆金佛山国家级自然保护区的兽类及地栖鸟类多样性进行了监测.共布设60台红外相机,获得有效照片15079张,鉴定出兽类4目10科15种,鸟类4目8科19种;其中,国家一级重点保护野生动物2种,国家二级重点保护野生动物13种,占物种总数的44.1％.红色名录评估为极危(CR)的1种、濒危(EN)的1种、易危(VU)的4种、近危(NT)的8种,占物种总数的41.2％.兽类中小麂Muntiacus reevesi和猕猴Macaca mulatta的相对多度指数较高,鸟类中红腹角雉Tragopan temminckii和红腹锦鸡Chrysolophus pictus的较高,它们不同月份的活动分别呈现不同的峰谷特征,但均表现出春夏季较活跃.本研究监测结果将有助于了解保护区内兽类和鸟类的多样性、种群相对多度及分布等重要基础信息,为保护区今后开展工作提供有效资料并指明方向.

Gibbons’ loud morning songs are hypothesized to function in territorial defense. To efficiently defend their territory, gibbons could sing more frequently along the territory boundary. Alternatively, singing may advertise occupancy of a territory, regardless of the singer’s location. Further, gibbons should choose singing sites that facilitate sound transmission. We investigated singing site choice of two groups of cao vit gibbon ( Nomascus nasutus ) from 2008-2009 and 2012-2013, in Bangliang Gibbon Nature Reserve, Guangxi, China. We did not find that groups sang more frequently than expected at the periphery of their home ranges, which does not support the boundary defense hypothesis. Instead, groups sang from the core area or irrespective of locations within an established territory, supporting the hypothesis that they advertise continuous occupancy of territories through regular singing. Singing locations were at significantly higher elevation than non-singing locations for both groups in the two study periods, supporting the hypothesis that cao vit gibbons choose singing locations to maximize sound transmission and minimize signal attenuation in karst forest. Thus, although the sample size is small, our study suggests that gibbons display flexibility in their choice of singing sites in different environments to ensure they can defend their territory.

2014年11月和2015年8月,采用社区访查和样线法对大理永平金光寺省级自然保护区开展兽类多样性调查,同时结合文献资料,认为该保护区现有兽类122种,隶属9目27科.中国国家I级重点保护野生动物有熊猴、云豹和豹3种,国家II级重点保护野生动物18种;CITES附录I收录的有10种,附录II收录的有12种.保护区兽类区系以东洋界物种为主(占76.2％),分布型以东洋型(41.8％)和南中国型(22.1％)物种为主.保护区分布有一群水鹿(20～30只),本次调查可反映大中型兽类基础信息,为物种保护和管理提供基础数据.

Although many species are threatened by hunting or resource extraction from indigenous human communities, traditional ecological knowledge (TEK) of local communities has the potential to support management and conservation of natural resources and wildlife. The newly described skywalker hoolock gibbon (Hoolock tianxing) is found on the border of China and Myanmar, and a large proportion of the remaining population in China occurs outside nature reserves. We surveyed this species across its range in China, and interviewed 622 people in 99 villages to evaluate the relationship between gibbon status and TEK of local communities. The total confirmed population was estimated to be less than 150 individuals. Gibbon subpopulations appear to have remained stable from 2009 to 2017 both within and outside nature reserves. Sociological and environmental correlates of gibbon survival outside the reserve were: (1) more Lisu than Han people present in villages; (2) greater forest cover; (3) greater distance from county towns; (4) existence of traditional taboos on hunting gibbons; and (5) higher dependency on forest resources by villagers. Interviewees living closer to surviving gibbon populations were more knowledgeable about gibbons, although interviewees living more than 25km away also knew more about gibbons. Formal education level was also correlated with better knowledge of gibbons, and men were better informed about gibbons than women. TEK appears to limit poaching of gibbons, thus contributing to their survival. The persistence of gibbons outside nature reserves may depend on incorporating TEK within community-based conservation strategies.

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.

Gibbons in China represent the northernmost margin of present day gibbon species distribution (around N25°). Compared to tropical habitats, northern gibbon habitats are characterized by low temperatures and remarkable seasonal variation in fruit abundance. How gibbons adapt to their cold and seasonal habitats and what ecological factors affect their sociality are key questions for understanding their ecology and social system evolution, the elucidation of which will contribute to the conservation of these special populations/species. According to preliminary short-term studies, northern gibbons consume more leaves and use larger home ranges than tropical gibbons. Interestingly, some Nomascus groups consist of more than one adult female. However, these preliminary results are not well understood or incorporated into current socio-ecological theories regarding gibbon species. To better understand northern gibbons, our team has systematically studied three habituated groups of Nomascus concolor, three groups of N. nasutus, and two habituated groups of Hoolock tianxing since 2002. In this paper, we stress the challenges facing gibbons living in northern habitats and summarize their behavioral adaptations to their harsh environments. We also describe the northern gibbon social system and discuss the potential relationships between their ecology and sociality. Finally, we highlight future research questions related to northern gibbons in 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.

为了解珍稀濒危灵长类对植物群落结构的影响,对黑白仰鼻猴现存分布区(龙马山)和灭绝分布区(天子山)的植物群落结构进行比较分析.于2014年1月1日至15日在龙马山和天子山黑白仰鼻猴生境内采用样方法收集植被数据.结果显示:(1)龙马山铁杉树高小于天子山的(t=2.60,df=236,P=0.01),而冠幅却大于天子山的(t=10.49,df=236,P<0.001);龙马山华山松冠幅大于天子山的(t=7.46,df=190,P<0.001);龙马山其他乔木树高和胸径都小于天子山的(t=7.19,df=527,P<0.001;t=4.11,df=527,P<0.001);(2)龙马山的灌木高度、盖度以及草本层高度低于天子山的(Z=4.78,P<0.001;Z=6.24,P<0.001;Z=3.71,P<0.001);(3)植物多样性指数、均匀度指数和优势种重要值差异均无统计学意义.结果表明黑白仰鼻猴的存在对森林结构中的乔木、灌木及草本都有一定的影响,而对植物多样性作用不明显,改变森林生态系统演替的进程.

Many non‐human primates produce species‐specific loud calls to communicate within and between groups over long distances. Understanding these calling patterns can provide insights into how individuals modify their behavior in response to environmental variables as well as help to design efficient bioacoustic survey techniques. Eastern hoolock gibbons in Gaoligongshan inhabit the coldest habitat of all gibbon populations, but both conservation and research efforts on this population have been minimal. We studied singing patterns of two habituated and two unhabituated groups at two sites in Gaoligongshan between July 2010 and June 2015. We systematically collected data of their calls, and its relationship to temperature, group density, and hunting pressure over at least 1 year for each group. Our goal was to elucidate how these factors affect singing patterns of eastern hoolock gibbons. We found that adult pairs coordinated their singing to produce duet bouts that lasted for an average of 25.5 min. The singing rate (number of bouts/number on monitoring days*100%: 7.5–31.4%) was notably lower than other gibbon populations, presumably due to low group density (about 0.5 groups/km2) and prevalence of hunting at the study site. Cold temperature also affected gibbons’ singing behavior. Our study groups called, on average, 2.5 hr after sunrise, probably foraging first in the early morning after long nights in this cold habitat delayed singing. Furthermore, mean temperatures in the morning (8:00–12:00 am) were higher on singing days than on non‐singing days, and one group called less frequently when monthly mean temperature was below 10°C. Our findings indicate that both hunting pressure from humans and low temperatures suppress calling behavior in hoolock gibbons. Such information is critical in evaluating the use of duetting as a monitoring technique for this endangered gibbon species. Am. J. Primatol. 78:861–871, 2016. © 2016 Wiley Periodicals, Inc.

Dance is a universal art form practiced by all human societies and has many functions including sexual attraction, social cohesion, and the therapeutic release of energy. Dance also has been reported in a small number of non-human primate species, in particular apes. However, its function has not been systematically evaluated. We observed 357 intentional, rhythmic, and nonverbal dance displays performed by four adult female cao vit gibbons ( Nomascus nasutus ) residing in four polygynous groups during 3000 h of observation in Bangliang, Guangxi, China. Females used dance to solicit copulations, as well as to promote a social bond with the group’s lone adult male. In addition, this display appears to represent a form of non-aggressive competition among adult females living in the same group. We found that a female who had a weaker social relationship with the breeding male increased her social and sexual access to the male by an increase in dancing frequency. Given that gibbons dance in various behavioral contexts, and appears to serve several important social and sexual functions, a greater understanding of this form of gestural communication offers an instructive model for examining the origin and evolution of dance in humans and other apes.

For Critically Endangered “species of extreme rarity,” there is an urgent need to clarify the potential survival of remnant populations. Such populations can be difficult to detect using standard field methods. Local ecological knowledge (LEK) represents an important alternative source of information, but anecdotal reports of rare or possibly extinct species can contain uncertainty and error. The Hainan gibbon ( Nomascus hainanus ), the world's rarest primate species, is confirmed to only survive as a tiny remnant population in Bawangling National Nature Reserve, China, but unverified gibbon sightings have been reported from other forest areas on Hainan. We conducted a large‐scale community interview survey to gather new data on patterns of primate LEK from 709 respondents around seven reserves across Hainan, to investigate the possibility of gibbon survival outside Bawangling and assess whether LEK can provide useful information for conservation management of cryptic remnant populations. Comparative LEK data for gibbons and macaques are consistent with independent data on the relative status of these species across Hainan. Local awareness and experience of gibbons was low across Hainan, including at Bawangling, but we recorded recent anecdotal gibbon reports from most reserves. A follow‐up field survey at Limushan Provincial Nature Reserve did not detect gibbons, however, and documented intensive wildlife exploitation within this reserve. All other surveyed landscapes showed some statistically lower levels of respondent awareness, experience, or sighting histories of gibbons compared to Bawangling, and are therefore considered biologically unlikely to support gibbons. Unverified LEK data can provide important insights into the possible status of cryptic remnant populations when assessed carefully and critically in relation to data from known populations.