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.     

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.     

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.     

Abundance and Distribution of Sympatric Gibbons in a Threatened Sumatran Rain Forest

Agile gibbons (Hylobates agilis) and siamangs (Symphalangus syndactylus) are sympatric small apes inhabiting threatened forests of Sumatra, Indonesia. We censused both species in the 3,568-km² Bukit Barisan Selatan National Park, at the southern limit of their ranges, over a 7-mo period in 2001. First, we monitored daily calling rates from known populations to develop probabilities of calling during a specified number of days and used the probability of calling at 1 time during 3 days to convert calling rates to abundance. Next, we used 3-day calibrated call count censuses (n=31) stratified by distance from forest edge and across a range of elevations to estimate species-specific group densities. We used group size from the known populations as well as data collected ad libitum during the census to convert group density to individual density. Agile gibbon group density averaged 0.67 km^–2 (SE = 0.082) and group size averaged 2.6 (SE = 0.73) for a population estimate of 4,479 (SE = 1,331) individuals. Siamang group density averaged 2.23 km^–2 (SE = 0.245), and group size averaged 3.9 (SE = 1.09) for a population estimate of 22,390 (SE = 8,138). Agile gibbon and siamang densities are negatively correlated, with agile gibbons more abundant in mid-elevation forests and siamangs most abundant in lowland and submontane forests. The small group sizes of agile gibbons indicate potential survival problems in infant and juvenile size classes. Although neither species is presently threatened by direct human disturbance, continued deforestation will jeopardize the long-term viability of both species in Bukit Barsian Selatan National Park and on Sumatra.     

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.     

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.     

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.     

Survey of Hylobates agilis albibarbis in a logged peat-swamp forest: Sabangau catchment, Central Kalimantan

Few data are available on gibbon populations in peat-swamp forest. In order to assess the importance of this habitat for gibbon conservation, a population of Hylobates agilis albibarbis was surveyed in the Sabangau peat-swamp forest, Central Kalimantan, Indonesia. This is an area of about 5,500 km² of selectively logged peat-swamp forest, which was formally gazetted as a national park during 2005. The study was conducted during June and July 2004 using auditory sampling methods. Five sample areas were selected and each was surveyed for four consecutive days by three teams of researchers at designated listening posts. Researchers recorded compass bearings of, and estimated distances to, singing groups. Nineteen groups were located. Population density is estimated to be 2.16 (±0.46) groups/km². Sightings occurring either at the listening posts or that were obtained by tracking in on calling groups yielded a mean group size of 3.4 individuals, hence individual gibbon density is estimated to be 7.4 (±1.59) individuals/km². The density estimates fall at the mid-range of those calculated for other gibbon populations, thus suggesting that peat-swamp forest is an important habitat for gibbon conservation in Borneo. A tentative extrapolation of results suggests a potential gibbon population size of 19,000 individuals within the mixed-swamp forest habitat sub-type in the Sabangau. This represents one of the largest remaining continuous populations of Bornean agile gibbons. The designation of the Sabangau forest as a national park will hopefully address the problem of illegal logging and hunting in the region. Further studies should note any difference in gibbon density post protection.     

A <Emphasis Type="Italic">FRUITFULL-like</Emphasis> gene is associated with genetic variation for fruit flesh firmness in apple (<Emphasis Type="Italic">Malus domestica</Emphasis> Borkh.)

The FRUITFULL (FUL) and SHATTERPROOF (SHP) genes are involved in regulating fruit development and dehiscence in Arabidopsis. We tested the hypothesis that this class of genes are also involved in regulating the development of fleshy fruits, by exploring genetic and phenotypic variation within the apple (Malus domestica) gene pool. We isolated and characterised the genomic sequences of two candidate orthologous FUL-like genes, MdMADS2.1 and MdMADS2.2. These were mapped using the reference population ‘Prima x Fiesta’ to loci on Malus linkage groups LG14 and LG06, respectively. An additional MADS-box gene, MdMADS14, shares high amino acid identity with the Arabidopsis SHATTERPROOF1/2 genes and was mapped to Malus linkage group LG09. Association analysis between quantitative fruit flesh firmness estimates of ‘Prima x Fiesta’ progeny and the MdMADS2.1, MdMADS2.2 and MdMADS14 loci was carried out using a mixed model analysis of variance. This revealed a significant association (P < 0.01) between MdMADS2.1 and fruit flesh firmness. Further evidence for the association between MdMADS2.1 and fruit flesh firmness was obtained using a case–control population-based genetic association approach. For this, a polymorphic repeat, (AT)_n, in the 3′ UTR of MdMADS2.1 was used as a locus-specific marker to screen 168 apple accessions for which historical assessments of fruit texture attributes were available. This analysis revealed a significant association between the MdMADS2.1 and fruit flesh firmness at both allelic (χ ² = 34, df = 9, P < 0.001) and genotypic (χ ² = 57, df = 32, P < 0.01) levels.     

Demography of agile gibbons (Hylobates agilis)

Demographic processes and the structure of a population of agile gibbons (Hylobates agilis) were investigated over 6 years in the Gunung Palung Reserve, Indonesia. Estimates of population size, density, and biomass revealed a population whose groups were stable in size and composition. Demographic processes place gibbons at risk, however, to short-term changes in their environment. Patterns of survival, fecundity, mortality, and dispersal combined to produce negative rates of growth. In addition, a top-heavy age-class distribution, with adults forming a large fraction of animals, makes it unlikely that this population could recover rapidly from a decline in numbers. Two behavioral factors, territoriality and monogamy, account for the size and stability of gibbon groups. Monogamy imposes limits on group size, while mating patterns and territoriality decrease the impact of sources of high mortality common in other primate species. These relationships underscore the fundamental importance of behavioral influence on demographic processes and social structure.     

Macrogeographical variability in the great call of Hylobates agilis: assessing the applicability of vocal analysis in studies of fine‐scale taxonomy of gibbons

Vocal characteristics have been used extensively to distinguish different taxonomic units of gibbons (family Hylobatidae). The agile gibbon (Hylobates agilis) has a disjunct distribution range in the Southeast Asian archipelago (remnants of the former Sunda landmass), and populations on different islands are currently recognized as distinct subspecies or even species. We recorded great calls from female agile gibbons from two populations on Sumatra and two populations on Borneo and examined the vocal variability on four levels: within‐individuals, between‐individuals, between‐populations and between‐islands. The primary objective was to evaluate the effect of geographical isolation on variability in song pattern and to test whether proposed island‐specific song characteristics exist, reflecting evolutionary divergence between Sumatran and Bornean agile gibbons. One hundred great calls were recorded from 20 females and analyzed for 18 spectral and temporal acoustic parameters. Principal component analysis followed by a nested ANOVA on components revealed a complex pattern of song variability not likely to reflect taxonomic or evolutionary relationship. We found no evidence that Sumatran and Bornean agile gibbons have evolved different vocal characteristics, refuting a distinction between them based on vocal characteristics. A high level of plasticity was found in great calls from the same individual, and generally the inferred pattern of variability suggested that ecological or social factors may confound any genetically based island dialects. Am. J. Primatol. 72:142–151, 2010. © 2009 Wiley‐Liss, Inc.     

Preliminary survey on the population and distribution of gibbons in yunnan province

Of the gibbons in China,Hylobates hoolock, H. lar, andH. concolor leucogenys are distributed only in Yunnan Province, whileH. c. concolor occurs limitedly in Yunnan Province and Hainan Island. During the periods from February to November 1984, and March to August 1985, the authors undertook surveys of the population and distribution of gibbons in 56 counties of 10 prefectures in Yunnan Province, and obtained the first reliable population and distribution data on the gibbons of this Province. The findings serve to fill an important blank in gibbon research in Yunnan and should pave the way for further research in the future.     

Reproductive and Life History Parameters of Wild Female <Emphasis Type="Italic">Macaca assamensis</Emphasis>

Information on basic reproductive parameters and life-history traits is crucial for the understanding of primate evolution, ecology, social behavior, and reproductive strategies. Here, we report 4 yr of data on reproductive and life-history traits for wild female Assamese macaques (Macaca assamensis) at Phu Khieo Wildlife Sanctuary, northeastern Thailand. During 2 consecutive reproductive seasons, we investigated reproductive behavior and sexual swelling size in 16 females and collected 1832 fecal samples. Using enzyme immunoassays, we measured fecal estrogen and progesterone metabolites to assess ovarian activity and timing of ovulation and to ascertain conceptions and pregnancies. Timing of reproduction was strictly seasonal (births: April–July, 86% in April–June, 4 yr, n = 29; conceptions: October–February, 65% in December–January, 2 yr, n = 17). Females showed no cyclic ovarian activity outside the mating season and conceived in their first or second cycle (mean: 1.2 cycles to conception, n = 13). Gestation length was on average 164.2 d (range: 158–170, n = 10), and females had their first infant at an age of 5 yr (n = 4). Interbirth intervals were bimodally distributed, with females giving birth on average every 13.9 or 23.2 mo. Shorter interbirth intervals were linked to early parturition within the birth season. Most females displayed subcaudal sexual swellings which, however, did not reliably indicate female reproductive status or fertility. Overall, our results fall within the range of findings reported for other macaque species. These results thus add to the growing body of information available for wild macaques, facilitating comparative studies for a better understanding of interspecific differences in social and reproductive patterns.     

Fecal Glucocorticoid Measurements and Their Relation to Rearing,Behavior, and Environmental Factors in the Population of Pileated Gibbons (<Emphasis Type="Italic">Hylobates pileatus</Emphasis>) Held in European Zoos

Pileated gibbons (Hylobates pileatus) are rated as endangered according to the International Union of Conservation of Nature (IUCN) Red List. The captive population suffers from poor breeding success and is threatened to become overaged. Although several factors are likely to contribute to the poor breeding success, one in particular may be chronic stress associated with prolonged periods of high glucocorticoid (GC) output. We investigated fecal GC levels of pileated gibbons (Hylobates pileatus) and their relationship to specific life-history variables and environmental factors. After validation of an enzyme immunoassay for the measurement of 5-reduced 3α,11β-dihydroxy cortisol metabolites to assess GC output reliably in pileated gibbons, we collected fecal samples over several days from all 36 European adult pileated gibbons located in 11 institutions and compared GC levels to intrinsic individual parameters, husbandry, behavior, and breeding history. Age, sex, and origin (wild vs. captive born) had no effect on GC levels. However, unnaturally reared gibbons had higher GC levels and showed more behavioral abnormalities than parent-reared individuals. Further, nonreproducing gibbons living in a pair without infants had higher GC concentrations than gibbons living in a family, bachelor group, or as singletons. With respect to environmental factors, a large size of the inside enclosure and the existence of visual protection from visitors was associated with lower fecal GC output. The data indicate that rearing and housing conditions appear to correlate to GC levels in pileated gibbons housed under captive conditions. It is hoped this knowledge will support the future management of the species in captivity and thus lead to a more successful breeding of this endangered primate.     

Genetic population structure of a reef goby, <Emphasis Type="Italic">Bathygobius cocosensis</Emphasis>, in the northwestern Pacific

To investigate the genetic population structure of a reef goby, Bathygobius cocosensis, in the northwestern Pacific in relation to major oceanic currents (North Equatorial and Kuroshio Currents), the mitochondrial DNA (mtDNA) phylogeny and demography of the species were inferred from partial nucleotide sequences of the mitochondrial NADH dehydrogenase 5 subunit (ND5) gene (945 bp). The resultant mtDNA tree and population genetic analyses showed that the Bonin Islands’ population apparently differed from the other populations in the Japan–Ryukyu–Guam region, which lie along the routes of the North Equatorial and Kuroshio Currents. A test calculation indicated the divergence date to be approximately 1 million years ago. The population expansion parameters indicated that the Bonin Islands’ population had survived during the fluctuations in sea level in the Pleistocene–Holocene age and that the population had expanded thereafter.     

Predation on giant flying squirrels (Petaurista philippensis) by black crested gibbons (Nomascus concolor jingdongensis) at Mt. Wuliang, Yunnan, China

Predation on vertebrates is infrequent in gibbons. In a 14-month field study of the central Yunnan black crested gibbon (Nomascus concolor jingdongensis) at Mt. Wuliang, Yunnan, China, we observed gibbons attacking, killing and eating giant flying squirrels (Petaurista philippensis). During 845 h of observation on one study group, the gibbons attacked giant flying squirrels 11 times, and succeeded in 4 cases. Although all members of the group attempted to attack the squirrels, all four successful attacks were made by the same adult female. The victims were infants in three cases and a juvenile or sub-adult in one case. Black crested gibbons also attacked adult giant flying squirrels by grabbing their long tails and throwing them from the canopy, but they failed to catch or kill the prey in three cases observed. Passive meat sharing occurred in three out of four successful cases. Besides hunting giant flying squirrels, the black crested gibbons also ate eggs or chicks in two birds’ nests and one lizard.     

Space use and territoriality of wolverines (<Emphasis Type="Italic">Gulo gulo</Emphasis>) in northern Scandinavia

Space use and territoriality influence population structure and dynamics and is therefore an important aspect in understanding the ecology of animals. We investigated spatial and temporal space use of wolverines (Gulo gulo) in northern Scandinavia. We estimated home ranges of 24 radio-marked individuals (17 females and seven males). Male home ranges (mean 669 km²; SE = 211) were significantly larger than female home ranges (mean 170 km²; Wilcoxon–Mann–Whitney; P = 0.001) and encompassed or included parts of up to five different females. Home range sizes of reproducing (170 km²; SE = 51) and barren (171 km²; SE = 63) adult females did not differ. Wolverines in Scandinavia exhibit intrasexual territoriality, with male home ranges totally exclusive and female home ranges either exclusive or with little home range overlap. Overlap between wolverine territories is most likely explained by intrasexual tolerance and kinship.     

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.     

Pileated Gibbon Density in Relation to Habitat Characteristics and Post‐logging Forest Recovery

ABSTRACT Although it is known that forest loss and degradation negatively impact most forest‐dwelling primates, such relationships are difficult to quantify because many primates are difficult to survey over large areas. Furthermore, recovery times are also difficult to assess due to a lack of long‐term data. Here, we determined how forest characteristics and habitat disturbance correlate with the abundance of pileated gibbons, Hylobates pileatus. We studied a population in Khao Ang Rue Nai Wildlife Sanctuary in southeastern Thailand, assessed its density using an auditory method combined with distance sampling at 24 randomly placed sample sites. In addition, we determined how simple forest structural characteristics and habitat disturbance correlate with the gibbon abundance. Average gibbon density per site was 1.02 ± 0.16 (SE) groups/km² (range 0–2.74). Bivariate analyses indicated that densities depended on food tree biomass, level of disturbance, evergreen forest cover, time since protection, and distance to the sanctuary boundary. Multiple regression analysis suggested evergreen forest cover and distance to boundary were the most influential factors. Because evergreen forest cover, time since protection, and habitat disturbance are correlated, these results suggest a direct dependence of gibbon densities on mature, undisturbed evergreen forest. While gibbons can persist in disturbed areas if the forest is protected, it appears that recovery to previous densities may take decades. We suggest that this is due to the slow pace of forest regeneration and/or poor recovery potential of gibbons.     

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.