Small Apes Research Articles

Discrimination between the facial gestures of vocalising and non-vocalising lemurs and small apes using deep learning

Facial expression studies in animal communication are essential. However, manual inspection methods are only practical for small datasets. Deep learning techniques can help discriminate facial configurations associated with vocalisations over large datasets. We extracted and labelled frames of different primate species, trained deep-learning models to identify key points on their faces, and computed distances between them to identify facial gestures. We used machine learning algorithms to classify vocalised and non-vocalised gestures across different species. The algorithms showed higher-than-chance correct classification rates, with some exceeding 90 %. Our work employs deep learning to map primate facial gestures and offers an innovative application of pose estimation systems. Our approach facilitates the investigation of facial repertoire across primate species and behavioural contexts, enabling comparative research in primate communication.

Hormonal changes in northern white-cheeked gibbons (Nomascus leucogenys) after the death of a group member.

The small apes, gibbons and siamangs, are monogamous species with their social groups comprising of both parents and their offspring. Therefore, the loss of a member may elicit a stress response in the remaining members due to their strong bonds. Glucocorticoids (GCs) have been useful indicators of stress, but distinguishing between acute versus chronic stress may be limited when measuring these hormones alone. The adrenal hormone dehydroepiandrosterone-sulfate (DHEAS), a GC antagonist, has been implicated in the regulation of the stress response. Thus, the concomitant measurement of these hormones can help examine whether an event, such as the loss of a group member, elicited a stress response. In this brief report, we discuss the hormonal response of two zoo-housed northern white-cheeked gibbons (Nomascus leucogenys) (1 adolescent male and his mother) after the death of the adult male of the group. Baseline fecal samples were collected opportunistically from these two individuals 5months prior, and 3months following the death of their group member. A total of 25 samples were quantified for fecal GC metabolites (FGCMs) and DHEAS by enzyme immunoassay (EIA) to calculate the FGCMs:DHEAS ratio. Our results indicate an increase in FGCMs and FGCMs:DHEAS for the adolescent male, but not the adult female, following the death. Our findings suggest that the integration of FGCMs and DHEAS measurements can provide valuable information to interpret individual stress levels to the sudden change in the group's social structure.

Applying an eye tracking technique to gibbons: First study using scanpath measurements for visual stimuli

Compared to the abundance of research on cognition in various nonhuman primate species, studies of gibbons -- often called “the small apes” -- remain limited, despite the importance of gibbons for understanding evolutionary processes in humans and other apes. Over the past decade, eye tracking techniques have been established in chimpanzees and other nonhuman primates using the free-participation method, which requires no physical restraint of the subjects. We investigated the feasibility of using the same method to record visual scanpaths in gibbons. We attempted to measure the eye movements of three adult gibbons while they spontaneously viewed images, with no prior fixation training. Calibration was successful in all three individuals, with errors of less than one degree. In total, 24 stimuli were used, with landscape and nonhuman primate face photographs presented on one-quarter of the screen, to test the prediction that gibbons would change their viewing time depending on image category. All three gibbons viewed the images for longer than the background, and primate face images for longer than landscapes. These results are consistent with previous findings in other primate species that faces attract more attention than non-face stimuli, suggesting that this effect is common across primates. This study demonstrates the feasibility of using eye tracking with gibbons. Further studies on gibbon visual exploration and cognition may enhance our understanding of the phylogenetic origins of hominid intelligence as well as the unique evolution of gibbons.

Applying the human component model of parenting to other primates: Developmental patterns of mother-child interactions across primate species

The component model of human parenting has been extensively used to study parents’ interactions with their offspring and to examine variation across cultural contexts. The current study applies this model to nonhuman primates to investigate which forms of parenting humans share with other primates and how these interactions change over infants’ first year of life. We repeatedly observed 52 mother-infant pairs, including humans (N = 11), chimpanzees and bonobos (N = 21), and several species of small apes (N = 20), during different daily activities when infants were 1, 6, and 12 months of age. Humans differed from apes in their higher probability of face-to-face contact and the use of object stimulation. Moreover, parenting seemed to be characterized by more variability within humans than within and possibly between ape species. Overall, the component model of parenting appears to be an effective tool to study the functional systems of parenting behavior in a comparative developmental perspective, by allowing direct comparisons between human and non-human primate species across development.

Effects of chainsaw noise on the activity budgets and calling behaviour of the northern yellow‐cheeked crested gibbon (Nomascus annamensis)

Wild animals are increasingly subjected to noisier environments as the scale and scope of human activities, such as development and resource extraction, encroach into their habitats. Anthropogenic noise alters the behaviour and vocalisations of wild animals including primates, yet our understanding of how noise affects small apes is limited. The large population of endangered northern yellow‐cheeked crested gibbons (Nomascus annamensis) inhabiting Veun Sai‐Siem Pang National Park (VSSP), in northeastern Cambodia, is frequently exposed to noise produced from illegal selective logging activities within the park. To determine the impacts of chainsaw noise on the gibbons' activity budgets and calling probability, we collected behavioural data on the only habituated gibbon group in VSSP during two consecutive dry seasons between 2017 and 2019. Our analyses of scan and focal‐animal samples revealed that when chainsaws were active, the group rested more and scanned less. The gibbons called more on mornings when there was no chainsaw activity; however, the trend was non‐significant. These findings suggest that despite long‐term exposure, chainsaw noise variably impacts important aspects of gibbon behaviour.

Small apes adjust rhythms to facilitate song coordination

Song coordination is a universal characteristic of human music. Many animals also produce well-coordinated duets or choruses that resemble human music. However, the mechanism and evolution of song coordination have only recently been studied in animals. Here, we studied the mechanism of song coordination in three closely related species of wild Nomascus gibbons that live in polygynous groups. In each species, song bouts were dominated by male solo sequences (referred to hereafter as male sequence), and females contributed stereotyped great calls to coordinate with males. Considering the function of rhythm in facilitating song coordination in human music and animal vocalizations, we predicted that adult males adjust their song rhythm to facilitate song coordination with females. In support of this prediction, we found that adult males produced significantly more isochronous rhythms with a faster tempo in male sequences that were followed by successful female great calls (a complete sequence with "introductory" and "wa" notes). The difference in isochrony and tempos between successful great call sequences and male sequences was smaller in N.concolor compared with the other two species, which may make it difficult for females to predict a male's precise temporal pattern. Consequently, adult females of N.concolor produced more failed great call (an incomplete sequence with only introductory notes) sequences. We propose that the high degree of rhythm change functions as an unambiguous signal that can be easily perceived by receivers. In this regard, gibbon vocalizations offer an instructive model to understand the origins and evolution of human music.

Group densities of endangered small apes (Hylobatidae) in two adjacent forest reserves in Merapoh, Pahang, Malaysia

Small ape habitat is rapidly declining due to anthropogenic activities but the current population status of this endangered primate family in Malaysia remains unknown. Group densities of Hylobates lar and Symphalangus syndactylus in two adjacent forest reserves across the Sungai Yu Ecological Corridor (SYEC) in Merapoh, a critical connectivity area of the Central Forest Spine, were assessed. Vegetation assessment and satellite imagery were used to identify habitat characteristics and fixed-point active acoustic triangulation at six listening areas was conducted to estimate small ape group densities. Small ape habitat quality was high in the forested areas of the SYEC. The mean group density of H. lar across these six areas was 3.55 ± 0.9 groups km-² while the mean group density of S. syndactylus was 2.75 ± 1.0 groups km-². The mean group densities of small apes at SYEC were moderately high, compared with densities at other sites in the region, which suggests that the forests here constitute good habitat for both species, despite some observed anthropogenic disturbances. Both species occurred in all listening areas. A nationwide population census for small apes and regular monitoring to inform conservation planning are recommended. Further improvement to connectivity across the SYEC by installing artificial canopy bridges for arboreal animals is important to support the movement of small apes across habitat fragments in Merapoh.

Isochronous singing in 3 crested gibbon species (Nomascus spp.).

The search for common characteristics between the musical abilities of humans and other animal species is still taking its first steps. One of the most promising aspects from a comparative point of view is the analysis of rhythmic components, which are crucial features of human communicative performance but also well-identifiable patterns in the vocal displays of other species. Therefore, the study of rhythm is becoming essential to understand the mechanisms of singing behavior and the evolution of human communication. Recent findings provided evidence that particular rhythmic structures occur in human music and some singing animal species, such as birds and rock hyraxes, but only 2 species of nonhuman primates have been investigated so far (Indri indri and Hylobates lar). Therefore, our study aims to consistently broaden the list of species studied regarding the presence of rhythmic categories. We investigated the temporal organization in the singing of 3 species of crested gibbons (Nomascus gabriellae, Nomascus leucogenys, and Nomascus siki) and found that the most prominent rhythmic category was isochrony. Moreover, we found slight variation in songs' tempo among species, with N. gabriellae and N. siki singing with a temporal pattern involving a gradually increasing tempo (a musical accelerando), and N. leucogenys with a more regular pattern. Here, we show how the prominence of a peak at the isochrony establishes itself as a shared characteristic in the small apes considered so far.

Testing Hypotheses for the Emergence of Gestural Communication in Great and Small Apes (Pan troglodytes, Pongo abelii, Symphalangus syndactylus)

Gestural communication is crucial for primates. However, little is known about how gestural repertoires emerge through development. We conducted behavioural observations on captive apes, including 18 siamangs (Symphalangus syndactylus), 16 Sumatran orangutans (Pongo abelii), and 19 chimpanzees (Pan troglodytes), to test different hypotheses for the emergence of gestures (i.e., Phylogenetic Ritualization, Ontogenetic Ritualization, Social Negotiation, and Social Transmission hypotheses). Our results showed little variation in individual gestural repertories, and only one idiosyncratic gesture. Moreover, across subjects (N = 53), repertoire size did not increase with age and social centrality. When comparing repertoires across all possible combinations of conspecifics, including apes in different groups (N=273) for the four groups of siamangs and the two of orangutans, repertoire similarity was higher in dyads of the same group than of different groups, but it also increased with more observational effort and lower age difference between group members. Finally, when comparing repertoires across all dyads of conspecifics in the same group (N = 260), we found no differences in repertoire similarity depending on dyadic relationship quality. Overall, these results provide support for the Phylogenetic Ritualization hypothesis, according to which individuals are endowed with complete gestural repertories from birth. These repertoires are largely similar across individuals and groups, although they may be partially refined through social experiences.

Hylobates moloch(Primates: Hylobatidae)

AbstractHylobates moloch (Audebert, 1797), the Javan or silvery gibbon, is a pair-living small ape which is exclusively found in the western and central regions of the Indonesian island of Java. It represents the southernmost occurring species of the genus Hylobates and inhabits the canopy of tropical rainforests. It is foremost characterized by its long silvery-gray fur in combination with a lack of duet songs in mated pairs. Hylobates moloch is threatened by habitat loss as well as the illegal wildlife trade and is listed as “Endangered” (EN) by the IUCN Red List of Threatened Species.

Hainan Gibbons (Nomascus hainanus), the Most Threatened and Rarest Primate in the World

Gibbons (Hylobatidae) are exclusively arboreal small apes only inhabiting in tropical rainforests of Southeast Asia [1]. Gibbons in Nomascus have 52 chromosomes and adult males and females are almost the same body size.

Population densities of Hylobates agilis in forests with different disturbance histories in Ulu Muda Forest Reserve, Malaysia.

Small ape habitat throughout Malaysia is rapidly being lost, degraded, and fragmented, and the effects of these changes on the abundance on this taxon are currently unknown. This study assessed the group density of Hylobates agilis in virgin forest, previously logged forest (1960s–1990s), and recently logged forest (2015–2017) of the Ulu Muda Forest Reserve (UMFR), Kedah, Malaysia. We conducted fixed‐point active acoustic triangulation at nine survey areas to estimate group density. We used vegetation “speed plots” and satellite imagery to quantify habitat characteristics and used model selection to identify ecological predictors of group density variation. The estimated group density of H. agilis in UMFR was 4.03 ± 0.14 groups km−2, with an estimated total of 2927 ± 102 groups in areas below 450 m a.s.l. in UMFR. Group density did not differ significantly among habitat types. The best ecological predictors for group density were canopy cover and proportion of deforested area. Areas with recent deforestation were associated with relatively high group densities, suggesting compression of the populations persisting in these habitat types. The consistently high group densities detected in all forest types emphasizes the importance of degraded forest as habitat for H. agilis. Because of the threats to small apes in Malaysia, and the uncertain status of most populations, we recommend a nationwide population census and regular monitoring to inform conservation planning and implementation. Most urgently, we call for immediate and permanent protection of UMFR and other forests in the Greater Ulu Muda landscape to protect the globally significant populations of H. agilis, as well as other charismatic and threatened megafauna, birds, and flora in the area.

Формирование эмпирических понятий у приматов разных таксономических групп

Much has been written about categorization in primates. However, there is a dearth in comparative studies on the formation of concepts and faculty of judgement by analogy (the part of analogical reasoning) in primates of various taxonomic groups. Our study is a comparative investigation of the formation of empirical concepts and faculty of judgement by analogy in semi-monkeys (ring-tailed lemurs), Old World monkeys (rhesus macaques), small apes (white-handed gibbons) and children aged 4 to 5. The formation of empirical concepts included the ability to differentiate between different object features. Four images were presented per a trial. The number of features underlying a concept did not affect the formation of concepts in lemurs and macaques while it made a difference for gibbons and children. This might be due to the use of different learning strategies during the formation of concepts. The children were faster than the non-human subjects to form concepts based on one feature due to the faculty of judgement by analogy. However, they lost their advantage when the formation of the concept was based on two features. Gibbons had big difficulties when inhibitory control was necessary for inhibiting the previous concept to form a new one. The study focused on the inductive function of abstract thinking responsible for the formation of concepts based on one or two features and the deductive function of abstract thinking responsible for faculty of judgement by analogy in primates of various taxonomic groups.

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.

Anggaru Klawu: Metafora Fauna Endemik Indonesia Owa Jawa Dalam Penciptaan Busana Dengan Art Of Beat Style

Indonesia is a country which has a diversity of flora and fauna. One of the endemic faunas of Indonesia is the Javan Gibbon. The Javan Gibbon (Hylobates Moloch) is a species of small ape without a tail with long arms, gray hair, and a distinctive voice. The Javan gibbon is an animal that is startining become endangered animal and almost extinct so that the IUCN Redlist has categorized as an "endangered" or threatened extinct. Javan Gibbons are the source of ideas for creating ready-to-wear, ready-to-wear deluxe and haute couture clothing which are implemented with metaphorical theory based on selected keywords, namely diurnal, arboreal, monogamous, territorial, sound, long sleeves, attracting attention and art of beat. The foundation of this fashion creation is using the method of. Tjok Istri Ratna Cora Sudharsana, namely Frangipani. “FRANGIPANI, The Secret Steps of Art Fashion” which consists of ten stages in the process of crafty fashion designs. The result of this creation is expected to be able to introduce to many people that Indonesia has the Javan Gibbon as an endemic animal of Indonesia that must be preserved in order that it does not become extinct.

Divergence and introgression in small apes, the genus Hylobates, revealed by reduced representation sequencing.

Gibbons of the genus Hylobates, which inhabit Southeast Asia, show great diversity and comprise seven to nine species. Natural hybridisation has been observed in several species contact zones, but the history and extent of hybridisation and introgression in possibly historical and the current contact zones remain unclear. To uncover Hylobates species phylogeny and the extent of introgression in their evolution, genotyping by random amplicon sequencing-direct (GRAS-Di) was applied to 47 gibbons, representing seven Hylobates species/subspecies and two outgroup gibbon species. Over 200,000 autosomal single-nucleotide variant sites were identified. The autosomal phylogeny supported that divergence from the mainland species began ~3.5 million years ago, and subsequently occurred among the Sundaic island species. Significant introgression signals were detected between H. lar and H. pileatus, H. lar and H. agilis and H. albibarbis and H. muelleri, which all are parapatric and form ongoing hybrid zones. Furthermore, the introgression signals were detected in every analysed individual of these species, indicating a relatively long history of hybridisation, which might have affected the entire gene pool. By contrast, signals of introgression were either not detected or doubtful in other species pairs living on different islands, indicating the rarity of hybridisation and introgression, even though the Sundaic islands were connected during the Pliocene and Pleistocene glacial events.

Increase in social interactions of wild Northern Gray gibbons (Hylobates funereus) during the mast fruiting period in the Danum Valley Conservation Area, Sabah, Malaysia

In Southeast Asian forests, there are dramatic supra-annual peaks in fruit availability known as mast fruiting, followed by low-fruit periods. Gibbons are frugivorous small apes. In this study, we investigated how gibbons varied their social and calling behaviors in response to changes in fruit availability. Activity budget, travel distance, sleeping time, and song duration of two wild Northern Gray gibbon (Hylobates funereus) groups were investigated during both mast and non-mast fruiting periods at the Danum Valley Conservation Area, Sabah, Malaysia. Gibbons traveled longer, entered the sleeping tree later, and spent more time engaged in singing, playing, and grooming behaviors during the mast fruiting period. Playing and grooming are intra-group social interactions. Gibbon songs were sung antiphonally within and among groups, indicating that singing is both an intra- and inter-group social interaction. Furthermore, copulatory behaviors that occurred during female pregnancy were observed during the mast fruiting period, suggesting this might be a social interaction behavior rather than a reproductive activity. Our results show that gibbons extended their daily activity schedules during the mast fruiting period and spent this extra time on social interactions. We examined whether male song complexity increased during the mast fruiting period by using the Levenshtein distance method, but we did not find such a trend. In the mast fruiting period, gibbons may consume more energy than in the non-mast fruiting period. Social and calling behaviors are energetically costly. Our results show that there is a link between energy intake and social and calling behaviors.

Open-access platform to synthesize knowledge of ape conservation across sites.

Despite the large body of literature on ape conservation, much of the data needed for evidence-based conservation decision-making is still not readily accessible and standardized, rendering cross-site comparison difficult. To support knowledge synthesis and to complement the IUCN SSC Ape Populations, Environments and Surveys database, we created the A.P.E.S. Wiki (https://apeswiki.eva.mpg.de), an open-access platform providing site-level information on ape conservation status and context. The aim of this Wiki is to provide information and data about geographical ape locations, to curate information on individuals and organizations active in ape research and conservation, and to act as a tool to support collaboration between conservation practitioners, scientists, and other stakeholders. To illustrate the process and benefits of knowledge synthesis, we used the momentum of the update of the conservation action plan for western chimpanzees (Pan troglodytes verus) and began with this critically endangered taxon. First, we gathered information on 59 sites in West Africa from scientific publications, reports, and online sources. Information was compiled in a standardized format and can thus be summarized using a web scraping approach. We then asked experts working at those sites to review and complement the information (20 sites have been reviewed to date). We demonstrate the utility of the information available through the Wiki, for example, for studying species distribution. Importantly, as an open-access platform and based on the well-known wiki layout, the A.P.E.S. Wiki can contribute to direct and interactive information sharing and promote the efforts invested by the ape research and conservation community. The Section on Great Apes and the Section on Small Apes of the IUCN SSC Primate Specialist Group will guide and support the expansion of the platform to all small and great ape taxa. Similar collaborative efforts can contribute to extending knowledge synthesis to all nonhuman primate species.

Long‐term effects of forest fire on habitat use by siamangs in Southern Sumatra

AbstractForest fires can cause direct mortality to wildlife, and the associated habitat damage can reduce carrying capacity and population densities. However, little is known about long‐term responses of animals to fire in the wet tropics. From 2000‐2015, we examined siamang ranging patterns in habitat damaged by fire to assess the effects on these arboreal frugivores. We mapped home ranges (HR) of seven siamang groups inhabiting contiguous HR 3‐5, 10‐12, and 17–18 years post‐fire. We predicted that if habitat connectivity or quality improved over time in burned areas, HR should become larger and centroid locations should shift toward recovering areas. Since territoriality constrains siamang ranging, we examined effects of social and habitat factors on ranging. By 18 years post‐fire, tree density in the burned area had returned to the 1997 baseline, but composite LandSat images indicated that tree species composition differed in burned and unburned forest. Our data and the associated models indicated that HR sizes in burned forest increased over time whereas those in unburned forest did not. Centroid locations moved little (15.5 ± 6.9 m y−1) and their movement appeared to be predominantly influenced by social factors, although HR centroids in burned habitat shifted further into the burned area while those in adjacent unburned forest did not. In a large burned area unused by siamangs before 2012, two new groups were observed 15‐17 years post‐fire, although one subsequently disappeared. This is the first study of the long‐term effects of fire on small ape habitat use. By 18 years post‐fire, siamangs had incorporated some burned areas into their HR, but did not use heavily damaged areas. Reduced frugivore densities in burned areas may inhibit forest regeneration by disrupting seed dispersal.

Northern yellow-cheeked crested gibbons (Nomascus annamensis) travel and scan more at the cost of rest when in the presence of tourists

Abstract The tourism sector is a fast-growing contributor to the global economy, and nature-based tourism (NBT), particularly in Asia and Africa, is booming. Through the creation of jobs and revenue NBT has the potential to combat deforestation in regions that are economically poor, but of high biodiversity value. Inspired by the success of gorilla tourism in Uganda and Rwanda, several gibbon tourism projects have been initiated in Southeast Asia and China. Despite the existence of these programmes, no research has been done to investigate the impact of tourism on the behaviour of gibbons. To address this, we collected observational data on a group of northern yellow-cheeked crested gibbons (Nomascus annamensis) at Veun Sai-Siem Pang National Park (VSSPNP), Cambodia, in the presence and absence of tourists. We found there was a significant increase in the amount of time individuals spent scanning their environment and travelling at the cost of rest when in the presence of tourists. We also found that individuals were significantly more likely to self-groom in the presence of tourists. These results highlight the importance of scientific research in implementing successful, low-impact NBT programmes that consider animal behavioural changes. We are continuing to collect data on gibbons at VSSPNP and at Mt. Gaoligong National Nature Reserve, China with the aim of extending the IUCN’s best-practice guidelines for great-ape tourism to include the small apes.