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.     

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.     

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.     

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.     

Grooming site preferences in wild white-handed gibbons (Hylobates lar)

During a four-month study of wild white-handed gibbons in Thailand one group was observed for 131 hr. The individuals spent 5.2% of their activity period allogrooming. Several body sites received more respectively less allogrooming than expected. Surface areas easy to clean by autogrooming such as the belly received significantly less allogrooming than expected. Upper body areas which are likely to be infested by parasites and other matter received significantly more allogrooming than lower body parts. Thus, grooming in gibbons seems to reflect a primarily hygienic function.     

Behavioural development of twin siamangs (Hylobates syndactylus)

Multiple births are very rare among gibbons. The birth of siamang twins at the Zürich Zoo in 1992 therefore presented a valuable opportunity to observe the development of the twins and to contrast it with a survey of previous reports on the development of single offspring of siamang and gibbons of thelar group. Furthermore, the hypothesis that the presence of twins among siamang may facilitate the occurrence of helping behaviour (defined as the care of offspring by individuals other than their parents) was re-examined (Dielentheis et al., 1991). The Zürich twins (one male and one female) were observed for a total of 74 hr during their first year of life. The results show that: (1) The twins exhibited more rapid behavioural development than that reported for single offspring. (2) A clear difference between the twins was observed: the female twin developed more rapidly than the male. (3) Neither the twins' father nor their older sisterRama was ever observed carrying the twins. The hypothesis ofDielentheis et al. (1991) is hence not supported by the present study, although it is possible that the older sisterRama did not carry the twins because she was younger than the juvenile in that study. (4) Siamangs may have a longer maturation period than gibbons of thelar group.     

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.     

Sterile pyuria in a population of wild white‐handed gibbons (Hylobates lar)

Urinalysis is an emerging method for monitoring the health and energy balance of wild primates. Here, we report the first urinalysis of wild gibbons. We used multi‐reagent test strips to monitor the health status of 52 individual white‐handed gibbons (Hylobates lar) inhabiting Khao Yai National Park, Thailand. Most urinary reference values were within normal ranges; however, regardless of age‐ and sex‐class or monthly fruit productivity, we found unexpectedly high rates of urinary leukocytes (50% and 90% of individuals in 2001–2003 and 2006, respectively). In contrast to previous studies of African apes, this finding is coupled with the near absence of urinary nitrites, demonstrating pervasive levels of sterile pyuria. This result is the first reported case of sterile pyuria in a population of wild primates. The etiology of human sterile pyuria is diverse, but in all cases it is diagnostic of systemic inflammation. We discuss the potential causes of sterile pyuria in the gibbons of Khao Yai. Am. J. Primatol. 71:880–883, 2009. © 2009 Wiley‐Liss, Inc.     

Effects of social status and stress on patterns of gastrointestinal parasitism in wild white‐handed gibbons (Hylobates lar)

Although gibbons (family Hylobatidae) are typically monogamous, polyandrous groups occur regularly. Stress associated with elevated intragroup competition among males in polyandrous groups may increase susceptibility to infectious disease. To better understand this interplay, as well as to provide the first comprehensive assessment of parasitism in free‐ranging gibbons, we characterized the richness of gastrointestinal parasites and examined their prevalence in males from 14 groups (10 pair‐living, 4 multi‐male) of white‐handed gibbons (Hylobates lar) at Khao Yai National Park, Thailand. From September 2008 to May 2009, 324 fecal samples were collected from 23 individually recognizable male gibbons and screened for gastrointestinal helminths and protozoa after isolation via fecal floatation, sedimentation, and immunofluorescent antibody detection. A total of 10 parasite species recovered, including seven nematodes, two protozoans, and one trematode. Parasite richness and species‐specific prevalence were examined relative to social organization (pair‐living vs. multi‐male), male status (primary vs. secondary), age (subadult, adult, senior), fecal glucocorticoid levels, and time of the year. No relationship was found between parasite richness and sociodemographic or physiological factors. Similarly, prevalence of infection with parasite species was not associated with the majority of sociodemographic factors; however, Ternidens sp. and Balantidium coli varied seasonally and Trichuris sp. decreased with increasing age. Moreover, observational data suggest that competition is low in this gibbon population, and our findings are consistent with those observations in that cooperative defense may offset stress and reduce susceptibility to infection. Am J Phys Anthropol 150:602–608, 2013. © 2013 Wiley Periodicals, Inc.     

Behavioral responses of two Malaysian primates (Hylobates lar andPresbytis melalophos) to selective logging: Vocal behavior,territoriality, and nonemigration

The durations of logging operations may be regarded as critical periods in which primates will be required to make rapid adjustments in behavioral patterns. Primates are extremely difficult to observe during logging operations, but their behavioral response may be interpreted from analysis of calling patterns. In Hylobates lar,increased calling frequencies of groups may be indicative of intruder pressure, as may reduced calling frequencies of animals which are avoiding confrontation with conspecifics or avoiding detection by loggers. In Presbytis melalophosthe function of calling is to mediate intergroup avoidance, such that differential calling frequencies would not be expected. Where reduction in calling occurs it is probably directed toward concealment from loggers. Groups do not emigrate from active logging areas and movement outside of established territories occurs only to a very limited extent.     

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.     

Brief report: Occurrence of anti-resonance in the song of the siamang (Hylobates syndactylus)

The duetting behavior of siamangs (Hylobates syndactylus) has previously been observed as representing a complex, interactively organized, and standardized set of vocal features. Anti-resonance in the bitonal screams of 15 males was observed. The sound energy of the fundamental frequency of the first note of these screams are absorbed, the result being a fundamental frequency which was virtually filtered out. The implications and consequences of such a rare phenomenon as anti-resonance in the vocal behavior in gibbons is discussed.     

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.     

Individuality in the songs of wild agile gibbons (Hylobates agilis) of Peninsular Malaysia

Recordings were made and analyzed of the female dominated duet songs by eight adult pairs of wild agile gibbons from two sites in Peninsular Malaysia. A statistical analysis of their songs revealed that individuality occurred throughout the females' songs from both sites. Individuality in gibbon songs may allow singing individuals to more efficiently and effectively locate and identify neighboring nonmate conspecifics.     

Gibbon foraging decisions and the marginal value model

We use data from an observational field study of frugivory in two sympatric gibbons, lar (Hylobates lar) and siamang (H. syndactylus), to test assumptions and predictions of the marginal value model (MVM). A key prediction of the MVM is that marginal gain rates at the time of leaving the patch are equal across patch types. We found that this is not the case for gibbons: rates of energy intake at the end of feeding sessions were significantly different for different types of fruit, and we could not attribute this to temporal variation in fruit availability. Initial and final caloric intake rates were highly correlated. This suggests that gibbons do not adjust the time spent in patches in order to maximize the average rate of energy intake. Similar results were obtained for all other currencies considered. Gibbon foraging appears to satisfy several, but not all, assumptions of the MVM. As required by the model, fruit patches occur as discrete units, patches are encountered sequentially, travel time between patches exceeds search time between items within a patch, search for and search within patches are incompatible activities, and intake rates decline over time spent in a patch. However, the declining rates we detected may be an effect of satiation instead of patch depletion, patches probably are not encountered at random, and group members may not forage independently. Thus, our results suggest that the MVM is not an adequate model of gibbon foraging behavior, but they do not invalidate the MVM per se.