Vocal fingerprinting reveals a substantially smaller global population of the Critically Endangered cao vit gibbon (Nomascus nasutus) than previously thought.

The cao vit gibbon (Nomascus nasutus) is one of the rarest primates on Earth and now only survives in a single forest patch of less than 5000 ha on the Vietnam-China border. Accurate monitoring of the last remaining population is critical to inform ongoing conservation interventions and track conservation success over time. However, traditional methods for monitoring gibbons, involving triangulation of groups from their songs, are inherently subjective and likely subject to considerable measurement errors. To overcome this, we aimed to use 'vocal fingerprinting' to distinguish the different singing males in the population. During the 2021 population survey, we complemented the traditional observations made by survey teams with a concurrent passive acoustic monitoring array. Counts of gibbon group sizes were also assisted with a UAV-mounted thermal camera. After identifying eight family groups in the acoustic data and incorporating long-term data, we estimate that the population was comprised of 74 individuals in 11 family groups, which is 38% smaller than previously thought. We have no evidence that the population has declined-indeed it appears to be growing, with new groups having formed in recent years-and the difference is instead due to double-counting of groups in previous surveys employing the triangulation method. Indeed, using spatially explicit capture-recapture modelling, we uncovered substantial measurement error in the bearings and distances from field teams. We also applied semi- and fully-automatic approaches to clustering the male calls into groups, finding no evidence that we had missed any males with the manual approach. Given the very small size of the population, conservation actions are now even more urgent, in particular habitat restoration to allow the population to expand. Our new population estimate now serves as a more robust basis for informing management actions and tracking conservation success over time.

Adult male-female social bond advertising: The primary function of coordinated singing intensity in a small ape.

Adult male and female coordinated singing occur in diverse animal taxa. Adult male-female social bond advertising and strengthening have been proposed as two important functional hypotheses of coordinated singing. Here we studied these two functions in four groups of cao vit gibbon (Nomascus nasutus), a small ape that lives in polygynous family groups and adult members coordinated their sex-specific songs to produce complex duets or trios (three members sing together), using 6-year field behavioral data. In this study, we used the number of successful great call sequences per bout or per minute, and latency period from start of the adult male call to the first successful great call sequence to represent singing intensity. We used the proportion of proximity, behavioral synchronization, and grooming between adult male and female to represent bond strength. We used linear mixed-effects model to investigate the correlation between singing intensity and adult male-female social bond strength. We found a negative correlation between all three bond strength indicators and female latency period (N = 209), and a positive correlation between the number of successful great call sequences per bout (N = 253) and per minute (N = 254) and proximity. We used paired Wilcoxon signed-rank test to investigate if adult gibbons increase bond strength after singing. We found proximity (hourly level: N = 45; daily level: N = 54), behavioral synchronization (hourly level: N = 57; daily level: N = 49), and grooming (daily level: N = 34) in most of the groups did not increase significantly after singing in an hourly or daily level. Together, these results indicate that cao vit gibbon coordinated singing serves primarily in adult male-female social bond advertising and distinct singing intensity indicators advertise different information on adult male-female social bond strength.

Primates Can Be a Rallying Symbol to Promote Tropical Forest Restoration.

With 60% of all primate species now threatened with extinction and many species only persisting in small populations in forest fragments, conservation action is urgently needed. But what type of action? Here we argue that restoration of primate habitat will be an essential component of strategies aimed at conserving primates and preventing the extinctions that may occur before the end of the century and propose that primates can act as flagship species for restoration efforts. To do this we gathered a team of academics from around the world with experience in restoration so that we could provide examples of why primate restoration ecology is needed, outline how primates can act as flagship species for restoration efforts of tropical forest, review what little is known about how primate populations respond to restoration efforts, and make specific recommendations of the next steps needed to make restoration of primate populations successful. We set four priorities: (1) academics must effectively communicate both the value of primates and the need for restoration; (2) more research is needed on how primates contribute to forest restoration; (3) more effort must be put into Masters and PhD level training for tropical country nationals; and finally (4) more emphasis is needed to monitor the responses of regenerating forest and primate populations where restoration efforts are initiated. We are optimistic that populations of many threatened species can recover, and extinctions can be prevented, but only if concerted large-scale efforts are made soon and if these efforts include primate habitat restoration.

Infant loss during and after male replacement in gibbons.

According to the sexual selection hypothesis, infanticide during resident male replacement is an adaptive strategy that has evolved because the killing of unweaned offspring sired by previous males shortens the inter-birth intervals of the mothers whose infants are targeted and thereby increases the reproductive fitness of the perpetrator. To test this hypothesis, we describe previously unreported cases of primary male replacement for two gibbon species (Hylobates lar and Nomascus nasutus), and review all other reported cases of primary male replacement in gibbons. Overall, infants were present in nearly half of all cases (16/33, 48%) and of the 18 infants present during replacement, 50% (N = 9) disappeared within 2 months of the event. In four of the five cases where there was sufficient demographic information to identify the likely sire of the subsequent offspring of females that lost infants, the new male was believed to be the sire. Infants were also less likely to die or disappear if the new male and original resident male were possible kin. However, there was no significant difference in the age of infants between those that died or disappeared following replacement and those that survived to weaning (p = .630). Our review of takeover-related infant loss in gibbons confirms that periods of male instability are risky for unweaned infants and that replacing males benefit from infant loss. Nevertheless, variability in the context of infant loss and difficulties related to data collection in the field make it difficult to test competing hypotheses concerning the mechanisms and functions of infanticide in the small apes.

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.

Food selection in relation to nutritional chemistry of Cao Vit gibbons in Jingxi, China.

The Cao Vit gibbon (Nomascus nasutus) has only one population with about 110 individuals living in a degraded karst forest along the China-Vietnam border. Investigation of food choice in relation to chemical nutrition will offer important insights into its conservation. We studied the food choice of two groups of Cao Vit gibbons using instantaneous scan sampling in Bangliang National Nature Reserve, Guangxi, China, over 4 years, and analyzed the chemical components (total nitrogen, TN; water-soluble sugar, WSS; crude fat, CF; neutral detergent fiber, NDF; acid detergent fiber, ADF; acid detergent lignin, ADL; condensed tannin, CT; and ash) of 48 food plant parts and 22 non-food plant parts. Fruits and figs that are rich in sugar are important food resources for gibbons. For other food types, flowers are a good source of total nitrogen and carbohydrates, and leaves and buds provide sources of protein and minerals. Cao Vit gibbons selected fruits that contain less total nitrogen, less acid detergent fiber and more water-soluble sugar than non-food fruits. Several food species that were heavily consumed by Cao Vit gibbons are suggested as potential tree species for ongoing habitat restoration.

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.

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.

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.

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.

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.