Effects of protected areas on survival of threatened gibbons in China.

Establishing protected areas (PAs) is an essential strategy to reduce biodiversity loss. However, many PAs do not provide adequate protection due to poor funding, inadequate staffing and equipment, and ineffective management. As part of China's recent economic growth, the Chinese government has significantly increased investment in nature reserves over the past 20 years, providing a unique opportunity to evaluate whether PAs can protect threatened species effectively. We compiled data from published literature on populations of gibbons (Hylobatidae), a threatened taxon with cultural significance, that occurred in Chinese reserves after 1980. We evaluated the ability of these PAs to maintain gibbon habitat and populations by comparing forest cover and human disturbance between reserves and their surrounding areas and modeling the impact of reserve characteristics on gibbon population trends. We also assessed the perspective of reserve staff concerning PA management effectiveness through an online survey. Reserves effectively protected gibbon habitat by reducing forest loss and human disturbance; however, half the reserves lost their gibbon populations since being established. Gibbons were more likely to survive in reserves established more recently, at higher elevation, with less forest loss and lower human impact, and that have been relatively well studied. A larger initial population size in the 1980s was positively associated with gibbon persistence. Although staff of all reserves reported increased investment and improved management over the past 20-30 years, no relationship was found between management effectiveness and gibbon population trends. We suggest early and emphatic intervention is critical to stop population decline and prevent extinction.

Efectos de las Áreas Protegidas sobre la Supervivencia de Gibones Amenazados en China Resumen El establecimiento de áreas protegidas (APs) es una estrategia esencial para la reducción de la pérdida de la biodiversidad. Sin embargo, muchas APs no proporcionan una protección adecuada debido a un mal financiamiento, personal y equipamientos inadecuados y un manejo poco efectivo. Como parte del reciente crecimiento económico en China, el gobierno del país ha incrementado significativamente la inversión en las reservas naturales durante los últimos 20 años, proporcionando así una oportunidad única para evaluar si las APs pueden proteger a las especies amenazadas de manera efectiva. Recopilamos datos de la literatura publicada sobre las poblaciones de gibones (Hylobatidae), un taxón amenazado que cuenta con importancia cultural, que se presentaron en las reservas chinas después de 1980. Evaluamos la habilidad de estas APs para mantener el hábitat y las poblaciones de gibones al comparar la cobertura del bosque y la perturbación humana entre las reservas y las áreas vecinas y al modelar el impacto de las características de la reserva sobre las tendencias poblacionales de los gibones. También evaluamos la perspectiva del personal de la reserva con respecto a la efectividad en el manejo de la AP por medio de una encuesta en línea. Las reservas protegieron efectivamente al hábitat de los gibones mediante la reducción de la pérdida del bosque y de la perturbación humana; sin embargo, la mitad de las reservas perdieron su población de gibones desde su establecimiento. Los gibones tuvieron mayores probabilidades de sobrevivir en las reservas establecidas más recientemente, a una elevación más alta, con menor pérdida de bosque y menor impacto humano, y las cuales han sido relativamente bien estudiadas. Un tamaño de población inicial mayor durante la década de 1980 estuvo asociado positivamente con la permanencia de los gibones. Aunque el personal de todas las reservas reportó un incremento en la inversión y mejoras en el manejo durante los últimos 20-30 años, no encontramos una relación entre la efectividad en el manejo y las tendencias poblacionales de los gibones. Sugerimos que una intervención temprana y empática es crítica para detener la declinación poblacional y prevenir la extinción.

Gibbons exploit information about what a competitor can see.

How much nonhuman animals understand about seeing has been the focus of comparative cognition research for decades. Many social primates (and other species) are sensitive to cues about what others can and cannot see. Whether this sensitivity evolved in primates through shared descent or convergent evolution remains unclear. The current study tested gibbons-the apes that are least studied yet most distantly related to humans and one of the less social primates-in two food-competition tasks. Specifically, we presented eastern hoolock gibbons, Hoolock leuconedys, and silvery gibbons, Hylobates moloch, with a choice between a contested piece of food visible to both themselves and a human competitor and an uncontested piece visible only to themselves. Subjects successfully stole the uncontested food when the competitor turned away his body (N = 10, experiment 1) and his head (N = 9, experiment 2). However, when the head of the experimenter was oriented towards the contested piece of food, whether the competitor opened or closed his eyes made no difference. Subjects' sensitivity to body- and head-orientation cues was comparable to that of chimpanzees, rhesus macaques, and ring-tailed lemurs-species living in much larger groups than gibbons. These findings support the continuity hypothesis that sensitivity to body- and head-orientation cues is a product of shared descent among primates.

Are social media reports useful for assessing small ape occurrence? A pilot study from Peninsular Malaysia.

Citizen science-based research has been used effectively to estimate animal abundance and breeding patterns, to monitor animal movement, and for biodiversity conservation and education. Here, we evaluate the feasibility of using social media observations to assess the distribution of small apes in Peninsular Malaysia. We searched for reports of small ape observations in Peninsular Malaysia on social media (e.g., blogs, Facebook, Instagram, Twitter, YouTube, iNaturalist, etc.), and also used online, radio, print messaging, and word of mouth to invite citizen scientists such as birders, amateur naturalists, hikers, and other members of the public to provide information about small ape observations made during their activities. These reports provided new information about the occurrence of all three species of small apes (Hylobates agilis, Hylobates lar, and Symphalangus syndactylus) in Peninsular Malaysia. Social media users reported observations of small apes in almost every state. Despite the fact that small apes are believed to occur primarily in the interior of large forested areas, most observations were from fairly small (<100 km2 ) forests near areas of high traffic and high human population (roads and urban areas). This suggests that most outdoor enthusiasts primarily visit well-traveled and easily accessible areas, which results in biased sampling if only incidental observations reported on social media are used. A more targeted approach specifically soliciting reports from citizen scientists visiting large, less-accessible forests may result in better sampling in these habitats. Social media reports indicated the presence of small apes in at least six habitats where they had not been previously reported. We verified the reported data based on whether reports included a date, location, and uploaded photographs, videos and/or audio recordings. Well-publicized citizen science programs may also build awareness and enthusiasm about the conservation of vulnerable wildlife species.

How Target Animacy Affects Manual Laterality in Hylobatidae: The First Evidence in Northern White-Cheeked Gibbons (Nomascus leucogenys).

Our study presents the first evidence on how target animacy impacts on manual laterality in the Hylobatidae and contributes to filling the knowledge gap between monkeys and great apes in primate evolution of emotional lateralization. Eleven captive individuals of northern white-cheeked gibbons (Nomascus leucogenys) were chosen as focal subjects. There were significantly more ambipreferent individuals than left/right-handed individuals for both inanimate (χ2(1, n = 11) = 7.364, p = 0.007) and animate (χ2(1, n = 11) = 4.455, p = 0.035) targets, meaning no significant group-level hand preference. The right hand was more frequently used than the left hand for inanimate targets whereas the left hand was more frequently used than the right hand for animate targets, although the interaction between target animacy and hand use was not significant (proportion: F1, 10 = 0.283, p = 0.607; rate: F1, 10 = 0.228, p = 0.643). Our findings in N. leucogenys could not fully support either the tool use theory or the right hemisphere hypothesis.

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.

A distance sampling approach to estimate density and abundance of gibbon groups.

All 18 species of gibbons are considered threatened with extinction and listed on the IUCN Red List of Threatened Species. Because gibbons (Hylobatidae) are one of the most threatened primate families, a great need exists to determine and monitor their status effectively. To meet this need, we employed distance sampling methods to estimate the density and number of gibbon groups. We focused on southern yellow-cheeked crested gibbon in the Nam Cat Tien sector of Cat Tien National Park, Vietnam, from July to October, 2016. We used an auditory point count method at 48 listening posts to detect gibbon groups. We estimated our detection probability of calling groups of gibbons within 1,200 m of a listening post was 0.63 (95% CI: 0.54-0.74). In addition, we estimated the daily calling probability of a gibbon group to be 0.46 (95% CI: 0.33-0.59) and interpreted this as the probability that a group was available to be detected. We adjusted our group density and abundance estimates by both detection and availability probabilities. Ultimately we estimated 325 (95% CI: 232-455) gibbon groups in the Nam Cat Tien sector. Our results suggest that Cat Tien National Park contains one of the largest populations of southern yellow-cheeked crested gibbon in Vietnam. Our methods are one way of avoiding underestimation of gibbon group density and abundance by incorporating uncertainty in gibbon group availability and detection.

Molecular phylogeny confirms the subspecies delineation of the Malayan Siamang (Symphalangussyndactyluscontinentis) and the Sumatran Siamang (Symphalangussyndactylussyndactylus) based on the hypervariable region of mitochondrial DNA.

Siamangs (Symphalangussyndactylus) are native to Peninsular Malaysia, Sumatra and southern Thailand and their taxonomical classification at subspecies level remains unclear. Morphologically, two subspecies were proposed as early as 1908 by Thomas namely Symphalangus s.syndactylus and Symphalanguss.continentis. Thus, this study aims to clarify the Siamang subspecies status, based on mtDNA D-loop sequences. Faecal samples were collected from wild Siamang populations at different localities in Peninsular Malaysia. A 600-bp sequence of the mitochondrial D-loop region was amplified from faecal DNA extracts and analysed along with GenBank sequences representing Symphalangus sp., Nomascus sp., Hylobates sp., Hoolock sp. and outgroups (Pongopygmaeus, Macacafascicularis and Papiopapio). The molecular phylogenetic analysis in this study revealed two distinct clades formed by S.s.syndactylus and S.s.continentis which supports the previous morphological delineation of the existence of two subspecies. Biogeographical analysis indicated that the Sumatran population lineage was split from the Peninsular Malaysian population lineage and a diversification occurrred in the Pliocene era (~ 3.12 MYA) through southward expansion. This postulation was supported by the molecular clock, which illustrated that the Peninsular Malaysian population (~ 1.92 MYA) diverged earlier than the Sumatran population (~ 1.85 MYA). This is the first study to use a molecular approach to validate the subspecies statuses of S.s.syndactylus and S.s.continentis. This finding will be useful for conservation management, for example, during Siamang translocation and investigations into illegal pet trade and forensics involving Malayan and Sumatran Siamangs.

Interspecific variation in the diet of Symphalangussyndactylus and Macacanemestrina at Genting Highlands, Pahang, Peninsular Malaysia.

Primate communities in the Genting Highlands consist of a single species of Hylobatidae and four species of Cercopithecidae, which are known to exhibit social interaction behaviour. Thus, a study on the diets of Symphalangussyndactylus (siamang; family Hylobatidae) and Macacanemestrina (pig-tailed macaque; family Cercopithecidae) was carried out at Genting Highlands, in order to compare the dietary preferences and interspecific competition between the two primate families. A DNA metabarcoding approach was used to analyse diet intake using non-invasive samples based on the trnL region. Based on the 140 amplicon sequence variants (ASVs) generated, 26 plant orders, 46 different families, 60 genera and 49 species were identified from 23 different plant classes. Fabaceae and Moraceae were classified as the most preferred plants at the family level for S.syndactylus; meanwhile, Piperaceae and Arecaceae were classified as the most preferred for M.nemestrina. Only six out of the 60 different plant genera classified in this study, were found to be consumed by both species. Therefore, the low similarity of preferred plants in the diets between the two families suggests that there is little interspecific competition. These findings are important for future conservation management of highland primates, especially in the Genting Highlands.

Sleeping trees and sleep-related behaviours of the siamang (Symphalangus syndactylus) in a tropical lowland rainforest, Sumatra, Indonesia.

Sleeping tree selection and related behaviours of a family group and a solitary female siamang (Symphalangus syndactylus) were investigated over a 5-month period in northern Sumatra, Indonesia. We performed all day follows, sleeping tree surveys and forest plot enumerations in the field. We tested whether: (1) physical characteristics of sleeping trees and the surrounding trees, together with siamang behaviours, supported selection based on predation risk and access requirements; (2) the preferences of a solitary siamang were similar to those of a family group; and (3) sleeping site locations within home ranges were indicative of home range defence, scramble competition with other groups or other species, or food requirements. Our data showed that (1) sleeping trees were tall, emergent trees with some, albeit low, connectivity to the neighbouring canopy, and that they were surrounded by other tall trees. Siamangs showed early entry into and departure from sleeping trees, and slept at the ends of branches. These results indicate that the siamangs' choice of sleeping trees and related behaviours were strongly driven by predator avoidance. The observed regular reuse of sleeping sites, however, did not support anti-predation theory. (2) The solitary female displayed selection criteria for sleeping trees that were similar to those of the family group, but she slept more frequently in smaller trees than the latter. (3) Siamangs selected sleeping trees to avoid neighbouring groups, monopolise resources (competition), and to be near their last feeding tree. Our findings indicate selectivity in the siamangs' use of sleeping trees, with only a few trees in the study site being used for this purpose. Any reduction in the availability of such trees might make otherwise suitable habitat unsuitable for these highly arboreal small apes.

An Exploration of the Value of Elective Health Checks in UK Zoo-Housed Gibbons.

Elective health checks form an important part of the preventative healthcare of many zoo-housed animals. These procedures are not without risk or financial expenditure, meaning careful cost-benefit analysis is required when determining the frequency and intensity with which they are implemented. This study evaluated the value of elective health checks (n = 74) carried out on 33 gibbons at a single UK zoological collection from 2011 to 2018. Data were categorised by health check type, animal age, clinical findings and outcome. Univariable binary logistic regression and multivariable modelling were used to identify factors associated with the likelihood of actionable (clinically significant) outcomes. In total, 51.35% of all elective health checks resulted in an actionable outcome. Elderly heath checks had 13.64 times greater odds of an actionable outcome and 34 times greater odds of a significant radiographic finding, when compared to routine (non-elderly) health checks. Our findings suggest that 75% wild longevity is a suitable threshold for identifying elderly captive gibbons and increasing health check frequency. Whilst further work is needed to ascertain whether these findings can be extrapolated to other collections and/or species, this study demonstrates how the analysis of clinical data can aid in the implementation of an effective and evidence-based preventative healthcare plan.

Postural effect on manual laterality during grooming in northern white-cheeked gibbons (Nomascus leucogenys).

Investigations on manual laterality in non-human primates can help clarify human evolutionary origins of hand preference and cerebral cognition. Although body posture can influence primate hand preference, investigations on how posture affects hylobatid manual laterality are still in their infancy. This study focused on how spontaneous bipedal behavioral tasks affect hand preference in Hylobatidae. Ten captive northern white-cheeked gibbons (Nomascus leucogenys) were chosen as focal subjects. Unimanual grooming during sitting posture and supported bipedal posture were applied as behavioral tasks. The gibbons displayed a modest tendency on left-hand preference during sitting posture and right-hand preference during supported bipedal posture, although no group-level hand preference was detected for either posture. From the sitting to supported bipedal posture, 70% of individuals displayed different degrees of right-side deviation trends. The strength of manual laterality in the supported bipedal posture was higher than that in the sitting posture. We found significant sex differences in manual laterality during supported bipedal posture but not during sitting posture. Thus, to a certain degree, bipedal posture in N. leucogenys facilitates stronger hand preference, elicits a rightward trend in manual laterality, and produces sex-specific hand preference.

Gibbon Aggression During Introductions: An International Survey.

Little is known regarding the prevalence of aggression seen during introductions of captive gibbons (Hylobatidae). In this study, an online survey was developed to quantify and collect contextual details regarding the frequency and types of aggression seen during introductions of captive gibbons (Hylobatidae). Nineteen percent of institutions (17 institutions) reported observing aggression, and 6 of these institutions recorded multiple instances of aggression, though a vast majority of these cases resulted in mild injuries or none at all. The female was the primary aggressor in 23% of cases, the male was the primary aggressor in 58% of cases, and both were the primary aggressor in 1 case. Although these aggressive interactions were often not associated with a known cause, 27% of cases were associated with food displacement. In most cases, management changes, including trying new pairings, greatly reduced situational aggression, suggesting that individual personalities may play a factor in aggression. These data begin to explain the extent of aggression observed in captive gibbons; future studies will address possible correlations with aggression and introduction techniques.

Banding patterns of the chromosomes of Presbytis cristatus pyrrhus and P. obscurus.

The G- and Q-bands and the location of the nucleolar organizer regions (NOR) in the chromosomes of Presbytis obscurus and the Q- and C-bands of P. cristatus pyrrhus are described. Their chromosomes are compared to those of Macaca mulatta and to other Cercopithecidae and Hylobatidae. The origin of the two different banding patterns of pair no. 1 in our specimen of P. cristatus pyrrhus is discussed.

Neonatal weight in gibbons (Hylobates spp.).

Neonatal and birth weights of gibbons have mostly been reported for single individuals, and larger samples (n = 2-8) have apparently been published for only two species of gibbons (Hylobates lar and H. syndactylus). In addition, a critical examination of the few published neonatal weights of gibbons shows that several of them should not be used. Neonatal weights are here defined as weights taken on infants up to seven days old, whereas birth weights include only those taken on the day of birth. This paper presents neonatal weights for six representative species of gibbons (H. lar, H. leucogenys, H. moloch, H. muelleri, H. pileatus, H. syndactylus) and some of their hybrids. Most of our data stem from surviving animals that were subsequently hand-reared and include 80 infants, thus making the previously available dataset 5 times larger. Our neonatal weights fall roughly into three different classes: neonates of the lar group (about 390 g, n = 27), the concolor group (about 510 g, n = 7), and the siamang (about 540 g, n = 46). This grouping corresponds not only to taxonomic units within the hylobatids, but also to grouping of gibbons by adult body weight. No weight difference between males and females is evident in our sample, and hybrids of the lar group do not appear to differ in weight from pure species. True birth weights (i.e., weights recorded on the day of birth) are available for only a few individuals. These weights are, on average, 7% higher than neonatal weights, but the difference is not statistically significant. Additional samples of neonatal weights suggest that infants that die on the day of birth weigh, on average, 17% less, twins weigh 29% less, and infants born by Cesarean section weigh 19% more than our reference sample of neonates. © 1995 Wiley-Liss, Inc.

One step beyond: Different step-to-step transitions exist during continuous contact brachiation in siamangs.

In brachiation, two main gaits are distinguished, ricochetal brachiation and continuous contact brachiation. During ricochetal brachiation, a flight phase exists and the body centre of mass (bCOM) describes a parabolic trajectory. For continuous contact brachiation, where at least one hand is always in contact with the substrate, we showed in an earlier paper that four step-to-step transition types occur. We referred to these as a 'point', a 'loop', a 'backward pendulum' and a 'parabolic' transition. Only the first two transition types have previously been mentioned in the existing literature on gibbon brachiation. In the current study, we used three-dimensional video and force analysis to describe and characterize these four step-to-step transition types. Results show that, although individual preference occurs, the brachiation strides characterized by each transition type are mainly associated with speed. Yet, these four transitions seem to form a continuum rather than four distinct types. Energy recovery and collision fraction are used as estimators of mechanical efficiency of brachiation and, remarkably, these parameters do not differ between strides with different transition types. All strides show high energy recoveries (mean  = 70±11.4%) and low collision fractions (mean  = 0.2±0.13), regardless of the step-to-step transition type used. We conclude that siamangs have efficient means of modifying locomotor speed during continuous contact brachiation by choosing particular step-to-step transition types, which all minimize collision fraction and enhance energy recovery.