Group harmony in gibbons: Comparison between white-handed gibbon (Hylobates lar) and siamang (H. syndactylus)

The siamang (Hylobates syndactylus) is exceptional among gibbons in that its area of distribution almost completely overlaps those of other gibbons, namely the white-handed gibbon (H. lar) and the agile gibbon (H. agilis) of the lar group. The siamang has almost twice the body weight of the gibbons of the lar group (ca. 11 kg vs. 5–6 kg), and it has been suggested that distinct ecological and behavioural differences exist between the siamang and its two sympatric species. The siamang has been claimed to differ from the white-handed gibbon “in the closer integration and greater harmony of group life” (Chivers, 1976, p. 132). However, few quantitative data exist to support this hypothesis. In the present study, intra-group interactions in captive family groups of white-handed gibbons and siamangs (two groups of each species) were recorded by focal-animal sampling. These data failed to show a consistent association between species and most of the behavioural patterns recorded, such as frequency of aggression, percentage of successful food transfer, frequency of social grooming bouts, and duration of social grooming/animal/hr. A significant difference was found for only two of the variables: Individual siamangs in this study showed longer grooming bout durations, and made fewer food transfer attempts than lar individuals. Only the first of these two differences is consistent with the hypothesis mentioned above, whereas the lower frequency of food transfer attempts in siamangs is the opposite of what should be expected under the hypothesis. On the other hand, two of these behavioural patterns showed a significant correlation with the parameters group size and individual age: Both individuals in larger groups and younger individuals tended to show shorter grooming bouts and a smaller proportion of successful food transfers. Our findings indicate that social cohesion within these gibbon groups may be much more flexible according to and depending on social or ecological influences and less rigidly linked to specific gibbon taxa than previously assumed. A considerably larger number of gibbon groups would have to be compared to provide reliable evidence for or against species-specific differences in group cohesion. Another finding of this study—a positive correlation between the frequency of aggression and grooming—is discussed in the light of the functional interpretations commonly attributed to allogrooming behaviour in primates.     

Gibbons (Nomascus gabriellae) provide key seed dispersal for the Pacific walnut (Dracontomelon dao), in Asia's lowland tropical forest

Understanding the mutualisms between frugivores and plants is essential for developing successful forest management and conservation strategies, especially in tropical rainforests where the majority of plants are dispersed by animals. Gibbons are among the most effective seed dispersers in South East Asia's tropical forests, but are also one of the highly threatened arboreal mammals in the region. Here we studied the seed dispersal of the Pacific walnut (Dracontomelon dao), a canopy tree which produces fruit that are common in the diet of the endangered southern yellow-cheeked crested gibbon (Nomascus gabriellae). We found that gibbons were the most effective disperser for this species; they consumed approximately 45% of the fruit crop, which was four times more than that consumed by macaques – the only other legitimate disperser. Gibbons tracked the temporal (but not spatial) abundance of ripe fruits, indicating this fruit was a preferred species for the gibbon. Both gibbons and macaques dispersed the majority (>90%) of the seeds at least 20 m away from parent crowns, with mean dispersal distances by gibbons measuring 179.3 ± 98.0 m (range: 4–425 m). Seeds defecated by gibbons germinated quicker and at greater rates than seeds spat by macaques, or in undispersed fruits. Gibbon-dispersed seeds were also more likely to be removed by unknown seed predators or unknown secondary dispersers. Overall, gibbons play a key role in the regeneration of the Pacific walnut. Our findings have significant implications both for the management of the Pacific walnut tree dominating tropical rainforest as well as the reintroduction program of the Southern yellow-cheeked crested gibbon.     

Interspecific spacing between gibbons (Hylobates klossii) and langurs (Presbytis potenziani) on Siberut Island,Indonesia

Spatial arrangement and social interactions of two sympatric and ecologically similar primate species, Hylobates klossii and Presbytis potenzianai, are described from field observations made between July 1972 and October 1974 on Siberut Island, Indonesia. Gibbon territories and langur home ranges overlap extensively. Because gibbons have the ability to supplant langurs at shared food sources, langurs are at a competitive disadvantage. To avoid or decrease the frequency of hostile interactions with gibbons, langurs locate their core areas on boundaries between adjacent gibbon territories, which permits langurs to retreat across these barriers in response to gibbon movements. Langurs further enhance segregration by leaving their sleeping trees earlier than gibbons, gaining additional feeding time on contested food sources. This form of interspecific spatial organization between gibbons and langurs resembles certain predator-prey spacing systems, where territorial boundaries between adjacent predators serve as sanctuaries for prey populations.     

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.     

Visual preference in a human-reared agile gibbon (<Emphasis Type="Italic">Hylobates agilis</Emphasis>)

Visual preference was evaluated in a male agile gibbon. The subject was raised by humans immediately after birth, but lived with his biological family from one year of age. Visual preference was assessed using a free-choice task in which five or six photographs of different primate species, including humans, were presented on a touch-sensitive screen. The subject touched one of them. Food rewards were delivered irrespective of the subject’s responses. We prepared two types of stimulus sets. With set 1, the subject touched photographs of humans more frequently than those of other species, recalling previous findings in human-reared chimpanzees. With set 2, photographs of nine species of gibbons were presented. Chimpanzees touched photographs of white-handed gibbons more than those of other gibbon species. The gibbon subject initially touched photographs of agile gibbons more than white-handed gibbons, but after one and two years his choice patterns resembled the chimpanzees’. The results suggest that, as in chimpanzees, visual preferences of agile gibbons are not genetically programmed but develop through social experience during infancy.     

High interannual variation in the diet of a tropical forest frugivore (Hylobates lar)

Frugivores must deal with seasonal changes in fruit availability and changes from year to year, as most species of tropical forest fruiting trees have considerable interannual variation in phenology and many are mast fruiters. We quantified seasonal and interannual changes in the fruit diet in a frugivore and important seed disperser, the white‐handed gibbon, Hylobates lar, in Thailand. We used 40‐d following data during April and May replicated in six consecutive years to study interannual variability in the diet and compared it with seasonal changes measured in monthly samples of the same size collected in three successive years. The 40‐d periods of following also allowed us to measure the decline in dietary similarity with time over a finer scale. We measured fruit diet similarity between replicated 5‐d periods using the percentage overlap (Renkonen's) index and Jaccard's similarity index. Seasonally, average dietary overlap between adjacent months was low, and similarity approached zero after four months. Average rate of decline in similarity exceeded 20 percent per 5‐d period. Variation in fruit species in the diet between years was high and was correlated with interannual variation in fruiting phenology. The strongest correlation occurred in the case of Nephelium melliferum, a highly preferred species that dominated the diet in good fruiting years. It is difficult to separate changes in food species preference from changes in availability from year to year. We devised a relative measure of preference that depends on the degree to which the gibbons rely on prior knowledge to find sources.     

The yellow-cheeked gibbon (Hylobates gabriellae) in nam bai cat tien (southern vietnam) revisited

Data concerning the status, habitat, and vocalizations of yellow-cheeked crested gibbons (Hylobates gabriellae) were collected during a short field trip to the Nam Bai Cat Tien National Park (southern Vietnam). Nam Bai Cat Tien may be the southernmost locality where crested gibbons (i.e. theHylobates concolor group) still survive. Fewer songs were heard at Nam Bai Cat Tien National Park than at other crested gibbon sites visited by the author. At least two gibbon groups appear to have been greatly reduced in number since previous surveys in the park. There is some evidence that both the gibbon population and the gibbon habitat in Nam Bai Cat Tien are disturbed. The first case of a great call solo song in wild gibbons of theconcolor group is reported. Great calls ofH. gabriellae are described and documented with sonagrams for the first time. They differ from those previously described forH. leucogenys.     

Modeling the Ecological and Phenological Predictors of Fruit Consumption by Gibbons (Hylobates albibarbis)

Understanding the ecological interactions between plant reproductive strategies and frugivore feeding behavior can offer insight into the maintenance of tropical forest biodiversity. We examined the role of plant ecological and phenological characteristics in influencing fruit consumption by the White‐bearded gibbon (Hylobates albibarbis) in Gunung Palung National Park, Indonesian Borneo. Gibbons are widespread across Borneo, highly frugivorous and perform important seed dispersal services. We compare multiple models using information criteria to identify the ecological and phenological predictors that most strongly influence gibbon fruit use of 154 plant genera. The most important predictors of resource use were the overall abundance of a genus and the consistency of fruit availability. Plant genera can maintain constant fruit availability as a result of (1) individual stems fruiting often or (2) stems fruiting out of synchrony with each other (asynchrony). Our results demonstrate that gibbons prefer to feed on plant genera that provide consistent fruit availability due to fruiting asynchrony. Because gibbons feed more often on genera that fruit asynchronously, gibbons are more likely to disperse seeds of plant genera with this reproductive strategy. Research on other frugivorous species is needed to determine whether the results for gibbons are generalizable more broadly. Finally, these results suggest that asynchronously fruiting plant genera may be particularly important for habitat restoration in tropical forests designed for frugivore conservation.     

Influence of Forest Seasonality on Gibbon Food Choice in the Rain Forests of Barito Ulu,Central Kalimantan

We describe the diet of two hybrid gibbon groups (Hylobates mulleri x H. agilis) in relation to forest seasonality. We collected data over 12 mo in lowland dipterocarp forest in the Barito Ulu research area, Central Kalimantan, Indonesia. Although non-fig fruit was the main dietary item (52–64% of diet), gibbon diet was most strongly influenced by the availability of flowers. During periods when flowers were most abundant and the gibbons increased consumption of them, they also ate figs or young leaves more often. We suggest that although flowers are nutritionally rich sources of food, providing relatively high levels of protein compared to fruit, they are unlikely to satiate gibbon hunger and they seek dietary bulk from figs or young leaves, because they are easily obtained. Rainfall also influenced food choice, and non-fig fruit availability had a weak influence on fruit selection for one group. The group concentrated feeding on the fruit of a few species when fruit was most abundant and ate a greater diversity of species when fruit was scarce. Gibbon diet appeared not to be influenced by changes in availability of figs, young leaves and diversity of fruiting species.     

Human predation and Kloss's gibbon (Hylobates klossii) sleeping trees in Siberut Island,Indonesia

Kloss's gibbons (Hylobates klossii) and Mentawai langurs (Presbytis potenziani) on Siberut Island, Indonesia, both sleep in emergent trees 34–55m tall, situated on crests and upper slopes of hills. They differ in that 91% of gibbon sleeping trees examined were free of lianas, whereas 89% of langur sleeping trees were draped with thick, woody lianas hanging from the branches to the ground. Because indigenous hunters climb lianas to shoot primates in treetops, gibbons are less susceptible than langurs to nocturnal human predation. Hence, the gibbons' preference for—and apparent control of—the limited supply of vineless trees gives them an advantage over langurs.     

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.     

Cross-species amplification of human microsatellite markers using noninvasive samples from white-handed gibbons (Hylobates lar)

Analysis of the population genetic structure and reproductive strategies of various primate species has been facilitated by cross-species amplification (i.e., the use of microsatellite markers developed in one species for analysis of another). In this study we screened 47 human-derived markers to assess their utility in the white-handed gibbon (Hylobates lar). Only eight produced accurate, reliable results, and exhibited levels of polymorphism that were adequate for individual identification. This low success rate was surprising given that human microsatellite markers typically work well in species (such as macaques) that are evolutionarily more distant from humans than are gibbons. In addition, we experienced limited success in using a set of microsatellite markers that have been reported to be useful in the closely-related H. muelleri, and applying our set of microsatellite markers to samples obtained from one H. pileatus individual. Our results emphasize the importance of extensively screening potential markers in representatives of the population of interest.     

Comparative locomotor ecology of gibbons and macaques: Selection of canopy elements for crossing gaps

To examine functional questions of arboreal locomotor ecology, the selection of canopy elements by Bornean agile gibbons (Hylobates agilis) and long-tailed macaques (Macaca fascicularis) was contrasted, and related to locomotor behaviors. The two species, and in some cases, the macaque sexes, varied in their use of most structural elements. Although both species traveled most frequently in the main canopy layer (macaques: 56%, gibbons: 48%), the gibbons strongly preferred the emergent canopy layer and traveled higher than the macaques (31 vs. 23 m above ground) in larger trees (48 vs. 26 cm dbh). Macaques preferred to cross narrower gaps (50% were in the class 0.1–0.5 m wide) than gibbons (42% were 1.6–3.0 m wide), consistent with the maximum gap width each crossed (3.5 m for macaques, 9 m for gibbons). Macaques could cross only 12% of the gaps encountered in the main canopy, and < 5% of the gaps in each of the other four layers. In contrast, all layers appear relatively continuous for gibbons. Specialized locomotor modes were used disproportionately at the beginning and end of travel segments, further indicating that behavior was organized around gap crossings. A model is defined, the Perceived Continuity Index (PCI), which predicts the relative use of canopy strata for each species, based on the percentage of gaps a species can cross, the frequency of gaps, and median length of continuous canopy structure in each canopy layer. The results support the hypothesis that locomotor behaviors, and strategies of selecting canopy strata for travel, are strongly constrained by wide gaps between trees and are ultimately based on selection for efficient direct line travel between distant points. © 1994 Wiley-Liss, Inc.     

Demography of Agile Gibbons (<Emphasis Type="Italic">Hylobates agilis</Emphasis>) in a Lowland Tropical Rain Forest of Southern Sumatra,Indonesia: Problems in Paradise

Gibbons are among the best-studied Asian primates, but few studies address their demography and life history strategies. We used annual censuses to study the demography of agile gibbons (Hylobates agilis) between 1998 and 2009 in rain forests of Bukit Barisan Selatan National Park, Indonesia. The population declined from 22 individuals (9 groups) to 14 individuals (5 groups) over the 12 yr of study. Infant survival to the juvenile age class was 33.3%, and 16.7% of infants survived to the subadult age class. The interbirth interval was 3.83 ± 1.15 yr and birth rate was 0.22–0.28 infants female^–1 yr^–1. Two groups colonized the study area but subsequently disappeared. We documented 7 immigrations, 17 disappearances, and ≥10 transients in the population. Compared to lar gibbons (Hylobates lar) and Bornean white-bearded gibbons (Hylobates albibarbis), Way Canguk’s agile gibbon population is characterized by slow reproduction, low survival, and high group turnover. We hypothesize that, although the habitat is high in fruit resources, agile gibbons may be displaced or excluded from the best fruit resources by larger and more numerous competitors, incurring costs of decreased opportunities to forage and increased travel, and leading to higher mortality for young agile gibbons. The reproductive potential of this agile gibbon population is insufficient to compensate for high mortality, and the population is unlikely to persist without immigration from outside the area. Given the agile gibbons’ endangered status and limited capacity to respond demographically to change, it is likely that intensive management interventions will be required to conserve this species.     

Relic of ancient recombinations in gibbon ABO blood group genes deciphered through phylogenetic network analysis

The primate ABO blood group gene encodes a glycosyl transferase (either A or B type), and is known to have large coalescence times among the allelic lineages in human. We determined nucleotide sequences of ca. 2.2 kb of this gene for 23 individuals of three gibbon species (agile gibbon, white-handed gibbon, and siamang), and observed a total of 24 haplotypes. We found relics of five ancient intragenic recombinations, occurred during ca. 2–7 million years ago, through a phylogenetic network analysis. The coalescence time between A and B alleles estimate precede the divergence (ca. 8 MYA) of siamang and common gibbon lineages. This establishes the coexistence of divergent allelic lineages of the ABO blood group gene for a long period in the ancestral gibbon species, and strengthens the non-neutral evolution for this gene.     

A preliminary study of the wild siamang gibbon (Hylobates syndactylus) at Fraser's Hill,Malaysia

The wild siamang gibbon was studied at Fraser's Hill, Malaysia. The study area was covered with a well developed forest and offered a suitable habitat for siamang gibbons. Other primates living in this area were the white-handed gibbon, the duskey leafmonkey, the banded leaf-monkey, and the pig-tailed monkey. The siamang gibbon groups observed have a monogamous structure consisting of one pair of adult individuals and one or more subadults which are assumed to be the offspring of the adults. The adult male showed behavior typical of a group leader. As subadults become older, they tend to become spatially separated from the mother group. Each group was observed to range freely within an exclusive area of the forest into which no other group was observed to intrude. Each group emitted loud vocalizations which seemed to maintain the spacing between the groups.     

Life History and Reproductive Strategies of Khao Yai <Emphasis Type="Italic">Hylobates lar</Emphasis>: Implications for Social Evolution in Apes

Among primates, great apes have the most extended life histories and they also appear socially specialized because of their flexible association patterns and sociosexual relationships. Researchers have hypothesized that such subtle social commonalities in combination with a slow life pace lead to great apes advanced cognition. Small apes, in contrast to great apes, are commonly believed to be socially inflexible, and little comparative life history data exist for wild populations. We investigated how the small white-handed gibbon (Hylobates lar) fits into a great ape life history and sociality framework. We followed the life histories of adults in 12 groups over ca. 18 yr at Khao Yai National Park, Thailand. Results demonstrate that the life histories of white-handed gibbons closely resembled those of other apes. Mean female age at first reproduction was late (11.06 yr), and mean interbirth interval (41 ± 9.1 mo) and juvenile period (9.5 ± 1.8 yr) were long. Multimale grouping of 2 adult males and 1 female was a common alternative (21.2% groups) to the traditional hylobatid pair-living social organization in our population. Female sexual partnerships include a variety of polyandrous mating strategies for both pair-living females and females in multimale groups. From our long-term study a picture of social complexity materializes that resembles social complexities in other apes. In conclusion, we infer that gibbons share commonalities postulated to unite great apes based on similar life histories and very flexible social and sexual relationships.     

Is gibbon ape leukaemia virus still a threat?

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Concordance between vocal and genetic diversity in crested gibbons

Background  

Gibbons or small apes are, next to great apes, our closest living relatives, and form the most diverse group of contemporary hominoids. A characteristic trait of gibbons is their species-specific song structure, which, however, exhibits a certain amount of inter- and intra-individual variation. Although differences in gibbon song structure are routinely applied as taxonomic tool to identify subspecies and species, it remains unclear to which degree acoustic and phylogenetic differences are correlated. To trace this issue, we comparatively analyse song recordings and mitochondrial cytochrome b gene sequence data from 22 gibbon populations representing six of the seven crested gibbon species (genus Nomascus). In addition, we address whether song similarity and geographic distribution can support a recent hypothesis about the biogeographic history of crested gibbons.