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.     

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.     

Sympatry between white-handed gibbons (Hylobates lar) and pileated gibbons (H. pileatus) in Southeastern Thailand

White-handed gibbons (Hylobates lar) are not known to occur to the east or southeast of Bangkok. The reliably documented localities ofH. lar nearest to this area are about 120 km northeast of Bangkok. There, in the Kao Yai National Park, is the only known zone of contact betweenH. lar and the pileated gibbon (H. pileatus), another species of the so-calledlar group. Unpublished documents dating from 1925 indicate, however, that sympatry between these two species may also have existed in the region of Sriracha, about 80 km southeast of Bangkok. Therefore, a large zone of overlap in the distribution of the two species may originally have existed. In most parts of this hypothetical zone, gibbon habitat appears to have been destroyed, with the Khao Yai Park possibly representing the last remnant of the once large contact zone.     

Female reproductive parameters in the Javan gibbon (Hylobates moloch)

Javan gibbons (Hylobates moloch) are one of the most endangered gibbon species in the world. Data on the reproductive biology of the species are almost nonexistent, and a general understanding of the female reproductive biology of this species is important for both ex situ and in situ conservation. Using 18 years of data from 11 captive individuals, we provide new information on the reproductive biology of Javan gibbons based on sexual swelling and menstrual bleeding, including reproductive development, interbirth intervals, and ovarian cycle lengths. Menarche and the onset of sexual swelling occurred at 6.2 and 6.5 years respectively, followed by a period of adolescent sterility of about 1.5 years. Average age at first birth was 8.8 years, and interbirth intervals were about 2.3 years, decreasing to 1.0 year during cases of infant mortality at or shortly after birth. Ovarian cyclicity was measured through periods between menstrual bleeding and sexual swelling. Menstrual bleeding indicates the start of a new ovarian cycle, while sexual swelling normally occurs near the time of ovulation. Menstrual bleeding intervals gave a cycle length of 25.6 days, while sexual swelling intervals gave a cycle length of 27.3 days. These both correspond closely to cycle lengths in other gibbon species, as well as hormonal studies in Javan gibbons. In particular, observing the presence/absence of swellings was found to be a useful and easy method to monitor female ovarian cycles, and could be a practical noninvasive technique for caretakers and researchers. Zoo Biol 29:449–456, 2010. © 2009 Wiley‐Liss, Inc.     

Sexual swellings in wild white-handed gibbon females (Hylobates lar) indicate the probability of ovulation

Conspicuous sexual swellings in the females of some primate species have been a focus of scientific interest since Darwin first wrote about them in 1871. To understand these visual signals, research focused on exaggerated sexual swellings of Old World primates. However, some primate species develop much smaller sexual swellings and it is as yet unclear if these smaller swellings can serve similar functions as those proposed for exaggerated swellings, i.e. advertising fertility to attract mates. We studied the temporal patterns of sexual swellings, timing of ovulation and female reproductive status in wild white-handed gibbons (Hylobates lar) at Khao Yai National Park, Thailand, where this species has a variable social organization. We established fecal progestogen profiles in fifteen cycles of eight cycling females and, to detect swellings outside the menstrual cycle, five pregnant and six lactating females. In 80% of menstrual cycles, ovulation and maximum swelling phase (duration: ? 9.3 days; 42.8% of cycle length), overlapped tightly. The probability of ovulation peaked on day 3 of the maximum swelling period. Nevertheless, the temporal relationship between maximum swelling and probability of ovulation varied from day -1 to day 13 of the swelling period and three times ovulations fell outside the maximum swelling phase. The different swellings phases occurred in similar proportions in cycling and pregnant, but not lactating females, which were rarely swollen. Despite their smaller size, gibbons' sexual swellings probably serve functions similar to those suggested for exaggerated swellings by the graded-signal hypothesis, which predicts that sexual swellings indicate the probability of ovulation, without allowing males to pinpoint its exact time.     

Homosexual behaviour in wild white-handed gibbons (Hylobates lar)

Homosexual mounting in apes and prosimians is rare. Male-male mounting was observed between an adult male white-handed gibbon and an adolescent male in the same group. The behaviour is discussed in terms of the gibbon group's social structure and the development of the adolescent. It is suggested that this behaviour provides reassurance for the adolescent gibbon.     

Taxonomic note: Bunopithecus: A genus-level taxon for the hoolock gibbon (Hylobates hoolock)

The recent discovery that the hoolock gibbon (Hylobates hoolock [Harlan, 1834]) has a karyotype distinct from all other hylobatids provides a new and strong motive for revising gibbon taxonomy and establishing hoolocks in a separate, higher taxon. Revising Groves's taxonomy of 1972, we propose that hoolock, along with the fossil species sericus, occupy a subgenus, Bunopithecus. With the newly added taxon, the genus Hylobates would thus contain four subgenera: Bunopithecus, Hylobates, Nomascus, and Symphalangus.     

Are <Emphasis Type="Italic">Hylobates lar</Emphasis> Extirpated from China?

The Nangunhe Nature Reserve in Southwest Yunnan (PRC) has long been presumed to be the last stronghold of lar (or white-handed) gibbons (Hylobates lar) in China and the likely last place of occurrence of Hylobates lar yunnanensis. We conducted a comprehensive survey to assess the status of lar gibbons at Nangunhe. We found no visual or auditory evidence of them still residing at the reserve and therefore tentatively conclude that lar gibbons have become extinct in China. It appears that large-scale destruction of primary forests in the 1960s and 1970s brought about an initial decline in their numbers, and subsequent uncontrolled hunting has resulted in their extirpation. The situation for the six Chinese ape taxa is nothing less than disastrous, with 1 taxon assumed to have become extinct during the last few years, 1 taxon not having been confirmed since the 1980s, and 2 species at the very brink of extinction with only tens of individuals remaining in China.     

Preliminary observations of wild black-crested gibbons (Hylobates concolor concolor) in Yunnan province,people's republic of China

Black-crested gibbons (Hylobates concolor concolor), which inhabit the subtropical forests of southern China and northern Vietnam, have until now never been the subject of any systematic behavioral or ecological field study. This report presents the findings of a three-month field study of wild black-crested gibbons in the Wuliang and Ailao Mountain Game Reserves in Yunnan Province, People's Republic of China. The sites visited consisted of temperate, subtropical, broadleaf evergreen forests, with trees belonging to the families Elaeocarpaceae, Fagaceae, Lauraceae, Magnoliaceae, and Theaceae. Black-crested gibbons were documented from four sites visited and were found to be polygynous, with an average group size of seven to eight animals. The family groups were observed to comprise one adult male, from one to four adult females, and numerous offspring of various ages. Both sexes of this species emit interactive songs, and various features of this loud vocal behavior were analyzed and are discussed here. Since all other gibbon species were found to inhabit only tropical rain forests and live in strictly monogamous family groups, some of the ecological and evolutionary implications of these findings are also presented.     

Hypertrichosis in a gibbon (Hylobates muelleri)

A case of facial hypertrichosis in a museum specimen of a Bornean gibbon (Hylobates muelleri) is described. Apparently, hypertrichosis has not previously been reported to occur in nonhuman primates. Similar pathological conditions are known to occur in humans, but it is unknown whether any of the numerous forms of human hypertrichosis is equivalent to this case in gibbons.     

Reassessment of age of sexual maturity in gibbons (hylobates spp.)

From studies of both wild and captive animals, gibbons are thought to reach sexual maturity at about 6 to 8 years of age, and the siamang (Hylobates syndactylus) at about 8 to 9 years. However, a review of the literature reveals that in most cases the exact age of the maturing animals was not known and had to be estimated. This study presents seven case reports on captive gibbons of known age. Captive males of the white-cheeked crested gibbon (H. leucogenys leucogenys) and of the siamang (H. syndactylus) can breed at the age of 4 and 4.3 years, respectively. Similarly, hybrid females (H. lar × H. moloch) and siamang females can breed at 5.1 and 5.2 years, respectively. This finding may help to improve the breeding success of captive gibbon populations. It is not clear whether gibbons reach sexual maturity earlier in captivity or whether sexual maturity is also reached by 5 years of age in the wild. Possible implications for the interpretation of group size regulation and of reproductive strategies of wild gibbons are discussed.     

Coexistence of monogamy and polygyny in black-crested gibbon (Hylobates concolor)

All gibbons are monogamous and territorial with the exception ofHylobates concolor. This paper reports the coexistence of monogamy and polygyny in black-crested gibbons. Based on the fact of two adult females and two offspring of the same age category in one group and other reasons, we suppose that the two adult females have bred in a single group, i.e. a polygynous one. The other main reasons are: (1) a large home range makes it possible for more individuals to live in one group; (2) mutual tolerance among two females; and (3) selection pressure favouring polygyny.     

Interactions between lar gibbons and pig-tailed macaques at fruit sources

Interactions are reported between white-handed gibbons (Hylobates lar) and pig-tailed macaques (Macaca nemestrina) in Khao Yai National Park, Thailand, in which gibbons selected ripe fruit from sources before macaques arrived on 4 occasions during June and July of 1989. The macaques foraged near gibbons or from shared fruit sources during 13% of gibbon observation time. Gibbons made their presence known in fruit trees when macaques approached on 3 occasions and macaques did not enter fruit trees occupied by gibbons. An aggressive interaction is reported in which a single white-handed gibbon vigorously excluded 22–28 macaques from a rare and valuable fruit tree (Sandoricum koetjape). The observations suggest that exploitative and interference competition may exist between these species.     

Songs of hybrid gibbons (Hylobates lar × H. muelleri)

Two hybrid offspring, one male and one female, were produced by a Hylobates muelleri female mated to a Hylobates lar male at Micke Grove Zoo, Lodi, California. Songs of the hybrids were studied at adulthood and compared to the parental-type songs. The hybrid female song is uniquely different from either parental type. The hybrid male song resembles the male song of H. lar, but contains an element that may be unique to H. muelleri. The study demonstrates the utility of sound-spectographic analysis of hybrid vocalizations to further understanding of primate behavioral inheritance.     

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.     

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.     

Home-range characteristics and the influence of seasonality on female reproduction in white-handed gibbons (Hylobates lar) at Khao Yai National Park, Thailand

A three-year (2001-2003) study was carried out on the home range characteristics of seven wild white-handed gibbon (Hylobates lar) groups focusing on the spatio-temporal distribution of food resources at Khao Yai National Park in northeastern Thailand. These results were combined with 23 years (1980-2003) of reproductive performance data on seven females from the same focal groups. Reproductive performance was equal among females with regard to birth, weaning and maturation ratios, and independent of variation in food availability. Offspring mortality, however, was significantly positively correlated with home-range size. In addition, there was an increase in offspring mortality just after weaning, suggesting that the increase in the daily distance traveled by juveniles contributed to this mortality. Conceptions clustered during the first half of the year when food production was at its peak, which presumably allowed females to accumulate sufficient body reserves to resume ovarian cycling. Our results place Khao Yai gibbons closer to Cercopithecidae than great apes in terms of the temporal pattern of reproductive events, though gestation, lactation, inter-birth interval, and offspring maturation are considerably longer in gibbons, placing them closer to the other apes. Our findings underline the unique phylogenetic position of these small-bodied apes in terms of reproductive patterns in primates.     

Food Preferences and Nutrient Composition in Captive White-handed Gibbons, <Emphasis Type="Italic">Hylobates lar</Emphasis>

We aimed to assess spontaneous food preferences in captive white-handed gibbons and to analyze whether they correlate with nutrient composition. Via a 2-alternative choice test, we repeatedly presented 3 male Hylobates lar with all possible binary combinations of 10 types of food that are part of their diet in captivity and found the following rank order of preference: grape > banana = fig > apple > pear > honeydew melon > carrot > tomato > cucumber > avocado. Correlational analyses revealed a highly significant positive correlation between the food preference ranking and the total carbohydrate, fructose, and glucose contents of the foods (p < 0.01, respectively). With the exception of the trace mineral selenium (p < 0.05), there was no other significant correlation with any other macro- or micronutrient. In addition, the food preferences were stable across the day because rankings obtained from tests performed at 0900, 1200, and 1500 h, respectively, did not differ significantly (p > 0.05). Our results suggest that captive white-handed gibbons are not opportunistic, but selective feeders with regard to maximizing net gain of energy because only the content of carbohydrates, but not the contents of total energy, proteins, or lipids significantly correlate with the displayed food preferences. Further, the results suggest that captive Hylobates lar, in contrast to their free-ranging conspecifics, do not display marked changes in their food selection across the day.     

How Reliable are Density Estimates for Diurnal Primates?

Primate population assessments provide the basis for comparative studies and are necessary prerequisites in determining conservation status. The most widely used assessment method is line transect sampling, which generates systematic data quickly and comparatively inexpensively. In contrast, the presumably most reliable method is long-term monitoring of known groups, which is both slow and costly. To assess the reliability of various analytical methods, we compared group and population densities for white-handed gibbons (Hylobates lar carpenteri) and Phayre’s leaf monkeys (Trachypithecus phayrei crepusculus) derived from transect walks with those from long-term group follows at Phu Khieo Wildlife Sanctuary, Thailand. Our assistants and we regularly walked a 4-km transect over 30 mo (480 km total), resulting in 155 gibbon sightings and 125 leaf monkey sightings. We then estimated densities via 1) DISTANCE and 2) the Kelker method based on perpendicular distances (PD) or animal-to-observer distances (AOD). We compared the 3 estimates to values based on known home ranges (95% kernels), accounting for home range overlap, combined with group size data. Analyses of line transect data consistently overestimated group densities for both species, while underestimating group size for leaf monkeys. Quality of results varied according to the group size and spread of each species. However, we found, in accordance with previous studies, that values derived via AOD (or its derivations) matched most closely with population estimates based on home range data.