Eco-evolutionary dynamics of gut phageome in wild gibbons (Hoolock tianxing) with seasonal diet variations.

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.

Wild gibbons plan their travel pattern according to food types of breakfast.

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.

Gut microbiome responds compositionally and functionally to the seasonal diet variations in wild gibbons.

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.

Where to sleep next? Evidence for spatial memory associated with sleeping sites in Skywalker gibbons (Hoolock tianxing).

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.

Effects of cold weather on the sleeping behavior of Skywalker hoolock gibbons (Hoolock tianxing) in seasonal montane forest.

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.

Ecology and social system of northern gibbons living in cold seasonal forests.

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.

How many remnant gibbon populations are left on Hainan? Testing the use of local ecological knowledge to detect cryptic threatened primates.

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.

Rhythmic displays of female gibbons offer insight into the origin of dance.

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.

Effects of group density, hunting, and temperature on the singing patterns of eastern hoolock gibbons (Hoolock leuconedys) in Gaoligongshan, Southwest China.

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/km(2) ) 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.

Understanding stable bi-female grouping in gibbons: feeding competition and reproductive success.

INTRODUCTION: Species of the order Primates are highly gregarious with most species living in permanent heterosexual social groups. According to theory in socioecology maximum social group size is limited by rates of intra-group feeding competition and associated increases in travel costs. Unlike other hylobatids, which are predominantly pair living, cao vit gibbons (Nomascus nasutus), and two other species of crested gibbon (Nomascus spp.) living in northern seasonal forest, regularly exhibit larger bi-female groups. To better understand the ability of northern gibbons to live in stable bi-female groups, we examined food distribution, feeding competition and reproductive success over a period of six years in a small cao vit gibbon population at Bangliang, Guangxi, China. RESULTS: In general, we found weak evidences for within-group contest or scramble competition in our two study groups, which we attribute to high spatial and temporal heterogeneity in the distribution of their important food species. Nevertheless, the larger of the two groups studied increased feeding time and group spread during lean periods, factors that may limit cao vit gibbon group size to a maximum of two breeding females. Relative to tropical pair-living gibbons, there is no evidence that cao vit gibbons travel farther or spend more time feeding, but they did consume more leaves and buds and less fruit and figs. Despite their highly folivorous diet, the average inter-birth interval is comparable to tropical gibbon populations, and the survival rate of infants and juveniles in our study groups is high. CONCLUSION: Cao vit gibbons do not suffer obvious costs in terms of feeding competition and reproductive success by living in bi-female groups, but within-group feeding competition may determine the upper the limit of cao vit gibbon group size to a maximum of two breeding females. These findings contribute to a growing body of evidence that bi-female grouping can be a stable grouping pattern of gibbons in certain habitats and further emphasize the flexibility of gibbon social organization.

Effects of tsaoko (Fructus tsaoko) cultivating on tree diversity and canopy structure in the habitats of eastern hoolock gibbon (Hoolock leuconedys).

In this study, the quadrat method was used to study the effects of tsaoko (Fructus tsaoko) plantation on tree diversity and canopy structure of two natural habitats of eastern hoolock gibbon (Hoolock leuconedys): Nankang (characterized by extensive tsaoko plantation) and Banchang (relatively well reserved and without tsaoko plantation). Totally, 102 tree species from 25 families and 16 woody liana species from 10 families were recorded in Nankang, whereas 108 tree species from 30 families and 17 woody liana species from 12 families were recorded in Banchang. Although the tree species between two habitats is different, both habitats are characterized by enriched food resources for eastern hoolock gibbons, sharing similar dominant plant families. Due to tsaoko plantation, tree density proportion and diversity of forest layerⅠ (>20 m) in Nankang were both significantly decreased, but the tree density of layerⅡ (10-20 m) increased. Likewise, in conjunction with these behavioral observations, we also address potential impacts of tsaoko plantation on the behavior of eastern hoolock gibbon.

Individuality and stability in male songs of cao vit gibbons (Nomascus nasutus) with potential to monitor population dynamics.

Vocal individuality and stability has been used to conduct population surveys, monitor population dynamics, and detect dispersal patterns in avian studies. To our knowledge, it has never been used in these kinds of studies among primates. The cao vit gibbon is a critically endangered species with only one small population living in a karst forest along China-Vietnam border. Due to the difficult karst terrain, an international border, long life history, and similarity in male morphology, detailed monitoring of population dynamics and dispersal patterns are not possible using traditional observation methods. In this paper, we test individuality and stability in male songs of cao vit gibbons. We then discuss the possibility of using vocal individuality for population surveys and monitoring population dynamics and dispersal patterns. Significant individuality of vocalization was detected in all 9 males, and the correct rate of individual identification yielded by discriminant function analysis using a subset of variables was satisfactory (>90%). Vocal stability over 2-6 years was also documented in 4 males. Several characters of cao vit gibbons allowed long-term population monitoring using vocal recordings in both China and Vietnam: 1) regular loud calls, 2) strong individuality and stability in male songs, 3) stable territories, and 4) long male tenure. During the course of this research, we also observed one male replacement (confirmed by vocal analysis). This time- and labor-saving method might be the most effective way to detect dispersal patterns in this transboundary population.

Ranging behavior of eastern hoolock gibbon (Hoolock leuconedys) in a northern montane forest in Gaoligongshan, Yunnan, China.

Generally, food abundance and distribution exert important influence on primate ranging behavior. Hoolock gibbons (genus Hoolock) live in lowland and montane forests in India, Bangladesh, Myanmar and China. All information about hoolock gibbons comes from studies on western hoolock gibbons (Hoolock hoolock) living in lowland forest. Between August 2010 and September 2011, we studied the ranging behavior of one habituated group of eastern hoolock gibbon (H. leuconedys) living in a seasonal montane forest in Gaoligongshan, Yunnan, China. Results show that the study group did not increase foraging effort, calculated in this study as the daily path length, when fruit was less available. Instead, the gibbons fed more on leaves and decreased traveling to conserve energy. They relied heavily on a single food species in most study months which was patchily distributed within their total (14-month) home range, and during most months they used only a small portion of their total home range. In order to find enough food, the group shifted its monthly home range according to the seasonal availability of food species. To satisfy their annual food requirements, they occupied a total home range of 93 ha. The absence of neighboring groups of gibbons and the presence of tsaoko cardamom (Amomum tsaoko) plantations may also have influenced the ranging behavior of the group. Further long-term studies of neighboring groups living in intact forests are required to assess these effects.

Locomotion behavior of cao vit gibbon (Nomascus nasutus) living in karst forest in Bangliang Nature Reserve, Guangxi, China.

The cao vit gibbon is a critically endangered species. Only approximately 110 individuals remain in degraded karst forest along the China-Vietnam border. Karst forest is unusual gibbon habitat. Currently, the canopy height of cao vit gibbon habitat is approximately 10 m. Research on the locomotor behavior of gibbons living in this particular forest type might provide important insight into locomotor stability and variability of gibbons. We used 5 min scan samples to record the locomotion mode, support use and canopy strata of gibbons in 3 groups for 2096 h between January 2008 and December 2009. Although cao vit gibbon habitat has a lower canopy in comparison to that of other forests inhabited by gibbons, cao vit gibbons displayed a similar overall locomotor pattern to other gibbon species (Symphalangus syndactylus, Hylobates lar and Hylobates agilis) in which brachiation dominate their locomotor behavior. Cao vit gibbons spent most of their time travelling on inclined branches (2-10 cm) in the middle stratum through the forest canopy. Adult females appear to more often employ safer modes of locomotion (bridging more often and brachiation less), while adult males choose riskier modes (leaping more and climbing less). As gibbons increased in body weight, as they grew from infant to adult, they tended to use larger supports. This research documented that locomotor behavior in Hylobatidae is strongly determined by anatomical characters, but cao vit gibbons also show the ability to use various supports, enabling them to survive in karst forest.

Seasonal variation of diet and time budget of Eastern hoolock gibbons (Hoolock leuconedys) living in a northern montane forest.

Most gibbons dwell in the tropical forests of Southeastern Asia, but eastern hoolock gibbons (Hoolock leuconedys) survive in high montane forest ranging from 1,600 to 2,700 m a.s.l. in Gaoligongshan (>24°30'N), Yunnan, China. To assess the behavioral adaptations of hoolock gibbons to the montane forest, we related temperature and food availability within the habitat to the seasonal behavioral patterns of a family group and a solitary female between August 2010 and September 2011 in Nankang, Gaoligongshan National Nature Reserve. The maximum temperature was 29.2 °C and the minimum temperature was -0.3 °C during the period. The monthly mean temperature was <10 °C between December and February, making Nankang the coldest gibbon habitat reported so far. Nonfig fruit and fig availability declined to nearly zero in cold months. The family group increased resting and decreased travel and social behaviors when the monthly mean temperature was low. Compared with other gibbon populations, the hoolock gibbons spent proportionally less time feeding on figs and other fruit than other gibbon populations except Nomascus concolor and Symphalangus syndactylus. Only 36 species of plants provided nonfig fruit or figs, which is less than the number of fruit species consumed by any other gibbon population observed during a similar period of time (about 1 year). Hoolock gibbons shifted their diet to leaves and increased feeding time when fruit was not available. We conclude that diet flexibility and an energy-conserving strategy during the cold season when fruit is scarce have enabled the hoolock gibbons to survive in a northern montane forest.

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.

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.

Social structure and group dynamics of the Cao Vit gibbon (Nomascus nasutus) in Bangliang, Jingxi, China.

The Cao Vit gibbon (Nomascus nasutus) was rediscovered in 2002 in Vietnam and then in 2006 in China. This is the only known population with about 110 individuals located along the China-Vietnam border. Little is known about it other than its population size and distribution. We describe the social structure and group dynamics of the Cao Vit gibbons in China based on 2 years of monitoring from 2007 to 2009. Four established study groups at this site consisted of 1 adult male, 2 adult females and 2-6 offspring. Two juveniles in 2 groups disappeared during the research. Four infants were born in 3 groups from November 2008 to February 2009. In 2 of the groups, both adult females had dependent infants. These observations suggest that Cao Vit gibbons live in polygynous groups, contrary to the usual monogamous group with only 1 adult female, but nevertheless similar to the social organization of both N. concolor and N. hainanus. We observed a coordinated dispersal of 1 adult male and 2 large juveniles, and the male formed a pair with a newly arrived female. Our observations support a growing awareness of variability in gibbon social organization.