Hylobates Lar Research Articles

Localization of Nucleolar Organizer Regions (NORs) of 4 Gibbon Species in Thailand by Ag-NOR Banding Technique

Summary Localization of nucleolar organizer regions (NORs) of four gibbon species in Thailand was studied. Blood samples were taken from 1 male each of the following 3 species: white-handed gibbon (Hylobates lar), pileated gibbon (H. pileatus), and white-cheeked gibbon (Nomascus leucogenys): and 1 female of the dark-handed gibbon (H. agilis). These were subjected to standard whole blood T-lymphocyte culture. The samples were harvested by colchicine-hypotonic-fixation-air-drying technique and were followed by the Ag-NOR banding technique. The results showed that the H. lar had NORs on chromosome pair 13 (submetacentric chromosomes) while the H. agilis had NORs on chromosome pair 10 (submetacentric chromosomes) and H. pileatus had NORs on chromosome pair 15 (metacentric chromosomes). In addition, the N. leucogenys showed 5 positions with NORs on chromosomes pairs 23, 24 (acrocentric chromosomes) and the Y-chromosome (submetacentric chromosome). These results are useful to confirm marker chromosomes of gibbons and also comprise basic genetic information for these animals. Kew words Gibbon, Karyotype, Chromosome, Idiogram, Ag-NOR banding. Thailand is tropical country thus its weather and surrounding are suitable for organism that causes high diversity. Wild animals are one element that show the diversity and also important in ecology and food chain. The destruction of forest causes wild animal extinction or risk of extinction includes animal in family Hylobatidae. There were 13 families, 60 genera and 232 species of animals in order Primate (Wilson and Cole 2000); however, only 3 families, 5 genera, and 13 species were found in Thailand. Thai gibbon species consists of 4 species, white-handed gibbon (Hylobates lar Linnaeus 1771), agile gibbon or dark-handed gibbon (Hylobates agilis Cuvier 1821), pileated gibbon (Hylobates pileatus Gray 1842), and white-cheeked gibbon (Nomascus leucogenys Ogilby 1840) (Lekagul and McNeely 1988, Giessmann 1995) (Fig. 1). These species are listed as protected species in Wild Animal Reservation and Protection Act (1992), and in the International Union for the Conservation of Nature (IUCN) as vulnerable species. The Convention on International Trade in Endangered Species (CITES) of wild fauna and flora also listed these species in Appendix I (Brokelman 1981).

Interspecific territoriality in gibbons (Hylobates lar and H. pileatus) and its effects on the dynamics of interspecies contact zones

We investigated the ecology and interspecific interactions of the two gibbon species (Hylobates lar and H. pileatus) that overlap in distribution within a narrow zone of contact in the headwaters of the Takhong River at Khao Yai National Park in central Thailand. The zone is about 10-km wide, with phenotypic hybrids comprising 6.5% of the adult population. We compared species with respect to diet, territory size, intra- and interspecific group encounters, and territory quality. The two gibbon species exploited the same types of resources within their territories despite variation in the relative abundance of food-plant species between territories. The gibbons were interspecifically territorial, and males of both species displayed aggressive behaviors at both intraspecific and interspecific territorial boundaries. There was no marked difference in the amount of overlap between territories of conspecific and heterospecific pairs of groups. Although the habitat was not homogeneous, territory quality did not vary significantly between species. The species have not diverged in habitat preference or in diet. Neither species dominated in interspecific encounters, and both were reproducing well in the contact zone. We analyzed the potential consequences of several types of interspecific interactions on individual dispersal options and on the structure of the contact zone. Interference competition through interspecific territoriality affects the dispersal of individuals into the range of the other species. In general, territorial competition coupled with limited hybridization leads to predictions of a narrow contact zone or parapatry between species; thus, behavioral and ecological interactions between species need to be considered as potential factors in explaining range borders of primate species.

The anti-predator behaviour of wild white-handed gibbons (Hylobates lar)

Predation on gibbons is rarely observed in the wild. However, the gibbons' moderate body size and relatively small social groups suggest high vulnerability to predation. To assess the role of predation and to study their anti-predator behaviour, we presented visual predator models to nine groups of wild white-handed gibbons at Khao Yai National Park, Thailand. We measured subjects' immediate and delayed responses to four potential predators: tiger, clouded leopard, crested serpent eagle and reticulated python. Subjects reliably approached all four predators. In response to tigers and leopards, they additionally produced predator-specific songs and defecated copiously. In terms of delayed responses, distance between mated adults decreased, but only after exposure to the tiger model. In response to eagles and pythons, gibbons consistently vocalised, but this did not always include predator singing, and we found no long-term effects in overall activity or strata use. However, during 6 of 26 predator encounters, the gibbons produced songs with a structure that was intermediate between a duet song and a predator song more than 20 min after the predator encounter, indicating a long-term effect on their vocal behaviour. This study demonstrates that gibbons discriminate between different potential predators and respond to them with adaptive anti-predator behaviour, which include predator-specific vocal responses. We conclude that gibbons are not immune to predation and that terrestrial predators elicit consistent immediate and delayed anti-predation responses.

Is grooming used as a commodity in wild white-handed gibbons, Hylobates lar?

Biological market theory is an extension of the idea of reciprocal altruism, as a mechanism to explain altruistic acts between unrelated individuals in a more flexible system of exchanging commodities. In nonhuman primates, social grooming has been used to test predictions in both contexts: reciprocal altruism or biological markets. Specifically, in species in which males cannot coerce females to mate, males may attempt to interchange grooming for mating, particularly when females are fertile and mating opportunities are more likely to arise. We tested whether wild white-handed gibbon males from Khao Yai National Park, Thailand, increased their grooming activity when the female partner was fertile. Adult females and males of our study population are codominant (in terms of aggression), they live in pairs or small multimale groups and mate promiscuously. We analysed grooming episodes during 2760 observation-hours in 12 groups separately for females’ reproductive condition (cycling/pregnant/ lactating) based on noninvasive measures of ovarian hormone activity. We found that males groomed females more than vice versa and more grooming was exchanged when females were cycling than during pregnancy or lactation. The number of copulations/day was elevated when females were cycling, and females copulated more frequently with males on days when they received more grooming. When males increased their grooming efforts, females also increased their grooming of males, perhaps to equalize give and take. Although grooming might be reciprocated because of intrinsic benefits of receiving grooming, we conclude that males also interchange grooming as a commodity for sexual opportunities during a female’s fertile period.

Demography of Agile Gibbons (Hylobates agilis) 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.

First isolation of the anamorph ofKazachstania heterogenicafrom a fatal infection in a primate host

We describe the isolation of the anamorph of the ascomycetous yeast Kazachstania heterogenica from a fatal infection in a 2 year, 9-month-old female white-handed gibbon (Hylobates lar). The yeast was observed in histological sections (lung and intestine) and co-isolated with the bacterium Escherichia coli from different internal organs. This is the first report of the recovery of this yeast from a fatal infection in a primate host.

Anatomical Contributions to Hylobatid Taxonomy and Adaptation

Compared with the great apes, the small-bodied hylobatids were treated historically as a relatively uniform group with 2 genera, Hylobates and the larger-bodied Symphalangus. Four genera are now recognized, each with a different chromosome number: Hoolock (hoolock) (38), Hylobates (44), Nomascus (crested gibbon) (52), and Symphalangus (siamang) (50). Previous morphological studies based on relative bone lengths, e.g., intermembral indices; molar tooth sizes; and body masses did not distinguish the 4 genera from each other. We applied quantitative anatomical methods to test the hypothesis that each genus can be differentiated from the others using the relative distribution of body mass to the forelimbs and hind limbs. Based on dissections of 13 hylobatids from captive facilities, our findings demonstrate that each of the 4 genera has a distinct pattern of body mass distribution. For example, the adult Hoolock has limb proportions of nearly equal mass, a pattern that differentiates it from species in the genus Hylobates, e.g., H. lar (lar gibbon), H. moloch (Javan gibbon), H. pileatus (pileated gibbon), Nomascus, and Symphalangus. Hylobates is distinct in having heavy hind limbs. Although Symphalangus has been treated as a scaled up version of Hylobates, its forelimb exceeds its hind limb mass, an unusual primate pattern otherwise found only in orangutans. This research provides new information on whole body anatomy and adds to the genetic, ecological, and behavioral evidence for clarifying the taxonomy of the hylobatids. The research also underscores the important contribution of studies on rare species in captivity.

Social monogamy and the threat of infanticide in larger mammals

The evolution of social monogamy in larger mammals is difficult to explain because males usually do not invest much in direct offspring care and might achieve greater fitness by deserting a pregnant female to reproduce with additional females elsewhere. It has been hypothesized that socially monogamous males remain with the female year-round to protect their offspring from infanticide by new immigrant males. We investigated this idea by analyzing all cases of infant loss in a wild population of white-handed gibbons (Hylobates lar; Primates), in which most groups were socially monogamous and some polyandrous (137.5 group years). We examined the influence of (a) male intruder pressure on male immigration rates and (b) the presence of a new male in the group on infant loss. We found no relation between intruder pressure and male immigration rates. Infant loss was lowest (4.5%) for stable monogamy (probable father stayed from conception through infancy) and intermediate (25.0%; p = 0.166) for stable polyandry. If a new male immigrated after conception, however, the infant was lost in all cases (p < 0.01) independent of the presumed father’s presence. Overall, 83.3% of infant losses were associated with the presence of a presumably unrelated male. Although the sample size is small, our results provide the first true support for the idea that the risk of infanticide is an important factor in the evolution of social monogamy in larger mammals.

Brief communication: Three‐dimensional motion analysis of hindlimb during brachiation in a white‐handed gibbon (Hylobates lar)

In brachiating gibbons, it is thought that there is little movement in the hindlimb joints and that lateral body movement is quite limited. These hypotheses are based on naked-eye observations, and no quantitative motion analyses of the hindlimbs have been reported. This study quantitatively describes the three-dimensional movements of the lower trunk and distal thigh during continuous-contact brachiation in a white-handed gibbon (Hylobates lar) to evaluate the roles of the trunk and hindlimb. The results revealed that the lower trunk moved both laterally and vertically. The lateral movement of the lower trunk resulted from the lateral inclination of the trunk by gravity. The vertical movement of the trunk was converted into forward velocity, indicating an exchange between potential and kinetic energy. We also observed flexion and extension of the hip, although the excursion was within a small range. In addition, the lateral movement of the hindlimb in thedirection opposite to that of trunk movement helped to reduce the lateral sway of the body. These results suggest that during continuous-contact brachiation a gibbon uses hip flexion and extension motions to increase the kinetic energy in the swing. In addition, fine motions of the hip may restrict the lateral sway of the center of body mass.

Electrically Elicited Vocalizations in the Gibbon Hylobates lar (Hylobatidae), and their Behavioral Significance

Electrically Elicited Vocalizations in the Gibbon Hylobates lar (Hylobatidae), and their Behavioral Significance

Muscle moment arms of the gibbon hind limb: implications for hylobatid locomotion

Muscles facilitate skeletal movement via the production of a torque or moment about a joint. The magnitude of the moment produced depends on both the force of muscular contraction and the size of the moment arm used to rotate the joint. Hence, larger muscle moment arms generate larger joint torques and forces at the point of application. The moment arms of a number of gibbon hind limb muscles were measured on four cadaveric specimens (one Hylobates lar, one H. moloch and two H. syndactylus). The tendon travel technique was used, utilizing an electro-goniometer and a linear voltage displacement transducer. The data were analysed using a technique based on a differentiated cubic spline and normalized to remove the effect of body size. The data demonstrated a functional differentiation between voluminous muscles with short fascicles having small muscle moment arms and muscles with longer fascicles and comparatively smaller physiological cross-sectional area having longer muscle moment arms. The functional implications of these particular configurations were simulated using a simple geometric fascicle strain model that predicts that the rectus femoris and gastrocnemius muscles are more likely to act primarily at their distal joints (knee and ankle, respectively) because they have short fascicles. The data also show that the main hip and knee extensors maintain a very small moment arm throughout the range of joint angles seen in the locomotion of gibbons, which (coupled to voluminous, short-fascicled muscles) might help facilitate rapid joint rotation during powerful movements.

Identification of human specific gene duplications relative to other primates by array CGH and quantitative PCR

In order to identify human lineage specific (HLS) copy number differences (CNDs) compared to other primates, we performed pair wise comparisons (human vs. chimpanzee, gorilla and orangutan) by using cDNA array comparative genomic hybridization (CGH). A set of 23 genes with HLS duplications were identified, as well as other lineage differences in gene copy number specific of chimpanzee, gorilla and orangutan. Each species has gained more copies of specific genes rather than losing gene copies. Eleven of the 23 genes have only been observed to have undergone HLS duplication in Fortna et al. (2004) and in the present study. Then, seven of these 11 genes were analyzed by quantitative PCR in chimpanzee, gorilla and orangutan, as well as in other six primate species ( Hylobates lar, Cercopithecus aethiops, Papio hamadryas, Macaca mulatta, Lagothrix lagothricha, and Saimiri sciureus). Six genes confirmed array CGH data, and four of them appeared to have bona fide HLS duplications ( ABCB10, E2F6, CDH12, and TDG genes). We propose that these gene duplications have a potential to contribute to specific human phenotypes.

Frequent gene conversion events between the X and Y homologous chromosomal regions in primates

BackgroundMammalian sex-chromosomes originated from a pair of autosomes. A step-wise cessation of recombination is necessary for the proper maintenance of sex-determination and, consequently, generates a four strata structure on the X chromosome. Each stratum shows a specific per-site nucleotide sequence difference (p-distance) between the X and Y chromosomes, depending on the time of recombination arrest. Stratum 4 covers the distal half of the human X chromosome short arm and the p-distance of the stratum is ~10%, on average. However, a 100-kb region, which includes KALX and VCX, in the middle of stratum 4 shows a significantly lower p-distance (1-5%), suggesting frequent sequence exchanges or gene conversions between the X and Y chromosomes in humans. To examine the evolutionary mechanism for this low p-distance region, sequences of a corresponding region including KALX/Y from seven species of non-human primates were analyzed.ResultsPhylogenetic analysis of this low p-distance region in humans and non-human primate species revealed that gene conversion like events have taken place at least ten times after the divergence of New World monkeys and Catarrhini (i.e., Old World monkeys and hominoids). A KALY-converted KALX allele in white-handed gibbons also suggests a possible recent gene conversion between the X and Y chromosomes. In these primate sequences, the proximal boundary of this low p-distance region is located in a LINE element shared between the X and Y chromosomes, suggesting the involvement of this element in frequent gene conversions. Together with a palindrome on the Y chromosome, a segmental palindrome structure on the X chromosome at the distal boundary near VCX, in humans and chimpanzees, may mediate frequent sequence exchanges between X and Y chromosomes.ConclusionGene conversion events between the X and Y homologous regions have been suggested, mainly in humans. Here, we found frequent gene conversions in the evolutionary course of primates. An insertion of a LINE element at the proximal end of the region may be a cause for these frequent conversions. This gene conversion in humans may also be one of the genetic causes of Kallmann syndrome.

Visual preference in a human-reared agile gibbon (Hylobates agilis)

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.

Mechanical constraints on the functional morphology of the gibbon hind limb

Gibbons utilize a number of locomotor modes in the wild, including bipedalism, leaping and, most of all, brachiation. Each locomotor mode puts specific constraints on the morphology of the animal; in some cases these may be complementary, whereas in others they may conflict. Despite several studies of the locomotor biomechanics of gibbons, very little is known about the musculoskeletal architecture of the limbs. In this study, we present quantitative anatomical data of the hind limb for four species of gibbon (Hylobates lar, H. moloch, H. pileatus and Symphalangus syndactylus). Muscle mass and fascicle lengths were obtained from all of the major hind limb muscles and the physiological cross-sectional area was calculated and scaled to remove the effect of body size. The results clearly indicate that, for all of the species studied, the major hip, knee and ankle extensors are short-fascicled and pennate. The major hip and knee flexors, however, are long-fascicled, parallel muscles with relatively small physiological cross-sectional areas. We hypothesize that the short-fascicled muscles could be coupled with a power-amplifying mechanism and are predominantly useful in leaping. The long-fascicled knee and hip flexors are adapted for a wide range of joint postures and can play a role in flexing the legs during brachiation.

Are Hylobates lar 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.

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.

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.

Functional differences within a guild of tropical mammalian frugivores

Many plants interact with groups of mutualist pollinators and seed dispersers. A key issue for both basic ecology and conservation is whether the different species within these guilds of mutualist animals are functionally equivalent. Comparing the relative effects of sympatric mutualists is important for understanding the evolution of multispecies mutualisms and for predicting mutualism stability in the face of anthropogenic change. However, empirical comparisons of the population-level impacts of mutualist animals on their host plant are rare, particularly for seed dispersal mutualisms in species-rich ecosystems. We compared the influence of three seed-dispersing tropical mammals, lar gibbons (Hylobates lar), sambar deer (Rusa unicolor), and red muntjac deer (Muntiacus muntjak), on the demography of a shared host tree in Thailand, Choerospondias axillaris (Anacardiaceae). Sambar and muntjac dispersed far more C. axillaris seeds than did gibbons. While sambar deposited many seeds under female tree canopies, muntjac were the only disperser to move seeds to open microhabitats, where C. axillaris seed germination, seedling survival, and initial growth are enhanced. Using stage-based population models, we assessed how disperser-specific seed dispersal, variation in the frequency of canopy gap formation, and their interaction influenced the potential population growth of C. axillaris. Large differences in dispersal quantity and small differences in dispersal quality among sambar and gibbons resulted in similar and negligible impacts on the tree's population dynamics. Muntjac, by taking some of the seeds to open microhabitats, are projected to have a greater positive impact on C. axillaris demography than either sambar or gibbons. Model comparisons of population-level species impacts may allow us to predict which ecological interactions are at risk from loss of critical species.

Superior olivary complex organization and cytoarchitecture may be correlated with function and catarrhine primate phylogeny

In the mammalian auditory system, the medial nucleus of the trapezoid body and the lateral superior olive (MNTB-LSO system) contribute to binaural intensity processing and lateralization. Localization precision varies with the sound frequencies. As recency of common ancestry with human beings increases, primates have improved low-frequency sensitivity and reduced sensitivity to higher frequencies. The medial part of the MNTB is devoted to higher frequency processing. Thus, its high-frequency-dependent function is nearly lost in humans and its role in binaural processing as part of the contralateral pathway to the LSO remains questionable. Here, Nissl-stained sections of the superior olivary complex of man (Homo sapiens), bonobo (Pan paniscus), chimpanzee (Pan troglodytes), gorilla (Gorilla gorilla), orangutan (Pongo pygmaeus), gibbon (Hylobates lar), and macaque (Macaca fascicularis) were compared to reveal differences and coincidences. From chimpanzees to humans, the size of the LSO decreased, and the MNTB as a compact nucleus nearly disappears. From chimpanzees to humans, the LSO/MNTB ratio increases dramatically too, whereas the LSO/MSO ratio remains 1.1; a finding that probably corresponds to the phylogenetic proximity between the species.