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Inter- and intraspecific variation in the diets of sympatric siamang (Hylobates syndactylus) and lar gibbons (Hylobates lar).

Studies of the siamang (Hylobates syndactylus continentis) and the lar gibbon (Hylobates lar lar) where they co-occur in mainland Asia have demonstrated interspecific dietary segregation based on body size and have suggested that observed levels of frugivory represent metabolically based maxima for these species. I studied sympatric groups of siamang (H. s. syndactylus) and lar gibbons (H. l. vestitus) at Ketambe in northern Sumatra (Indonesia) in order to assess the magnitude of within- and between-species variation in diets. The insular subspecies are considerably more frugivorous (60-70% of feeding time) than mainland conspecifics (35-50%). This is primarily because Sumatran hylobatids spend about twice as much time (approx. 45% of feeding) eating fig fruits (Ficus spp., Moraceae). A higher density of figs at Ketambe (compared to Kuala Lompat) may account for this behavioral difference. Enhanced frugivory has been achieved at the expense of folivory, which is much reduced in Sumatra--especially in H. lar (4% of diet)- and is limited almost entirely to immature foliage. The expected decline in protein intake resulting from diminished folivory in Sumatra may be counterbalanced by observed increases in insectivory, which is especially pronounced in lar gibbons. Interspecific dietary segregation emerges most clearly in how individuals of each species supplement their similarly fig-dominated diets. Siamang rely more on immature foliage--primarily from lianas, which generate young leaves more reliably and abundantly than trees do. Conversely, lar gibbons exploit the pulpy fruit of trees and lianas more heavily than siamang do. This general pattern occurs where the two species coexist in Malaysia, thereby suggesting a substantive interspecific difference that is somewhat greater in the insular populations.

Animals↗

Conserved chromosome segments in Hylobates hoolock revealed by human and H. leucogenys paint probes.

A complete comparative chromosome map of the white-browed gibbon (Hylobates hoolock, 2n = 38), white-cheeked gibbon (Hylobates leucogenys, 2n = 52), and human has been established by hybridising H. leucogenys chromosome-specific paints and human 24-colour paints onto H. hoolock metaphase chromosomes. In the 18 H. hoolock autosomes, we identified 62 conserved segments that showed DNA homology to regions of the 25 H. leucogenys autosomes. Numerous interchromosomal rearrangements differentiate the karyotypes of H. leucogenys and H. hoolock. Only H. hoolock chromosome 10 showed homology to one entire autosome of H. leucogenys. The hybridisation of human 24-colour paints not only confirmed most of the chromosome correspondences between human and H. hoolock established previously but also helped to correct five erroneous assignments and revealed three new segments. Our results demonstrate that the karyotypes of the extant gibbons have arisen mainly through extensive translocation events and that the karyotype of H. hoolock more closely resembles the ancestral karyotype of Hylobates, rather than the karyotype of H. leucogenys.

Animals↗

Complex, compound inversion/translocation polymorphism in an ape: presumptive intermediate stage in the karyotypic evolution of the agile gibbon Hylobates agilis.

Karyotypic variation in five gibbon species of the subgenus Hylobates (2n = 44) was assessed in 63 animals, 23 of them wild born. Acquisition of key specimens of Hylobates agilis (agile gibbon), whose karyotype had been problematic due to unresolved structural polymorphisms, led to disclosure of a compound inversion/translocation polymorphism. A polymorphic region of chromosome 8 harboring two pericentric inversions, one nested within the other, was in turn bissected by one breakpoint of a reciprocal translocation. In double-inversion + translocation heterozygotes, the theoretical meiotic pairing configuration is a double inversion loop, with four arms of a translocation quadrivalent radiating from the loop. Electron-microscopic analysis of synaptonemal complex configurations consistently revealed translocation quadrivalents but no inversion loops. Rather, nonhomologous pairing was evident in the inverted region, a condition that should preclude crossing over and the subsequent production of duplication-deficiency gametes. This is corroborated by the existence of normal offspring of compound heterozygotes, indicating that fertility may not be reduced despite the topological complexity of this polymorphic system. The distribution of inversion and translocation morphs in these taxa suggests application of cytogenetics in identifying gibbon specimens and avoiding undesirable hybridization in captive breeding efforts.

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An electromyographic study of the pectoralis major in atelines and Hylobates, with special reference to the evolution of a pars clavicularis.

Among primates there is striking variation in the extent of the origin of pectoralis major from the clavicle. A significant clavicular attachment (pars clavicularis) occurs only in Alouatta, Lagothrix, Hylobates, Pan (troglodytes, paniscus and gorilla), and Homo. Interpreting this trait in nonhuman primates as an adaptation to frequent use of a mobile forelimb in climbing and suspension is contraindicated by the absence of a clavicular origin in Ateles and Pongo. We have undertaken a telemetered electromyographic study to determine any special role of the most cranial part of the pectoralis major in comparison to its caudal part, and to the deltoid, during vertical climbing, pronograde quadrupedalism, and armswinging in Ateles, Lagothrix, Alouatta, and Hylobates. The results show that the cranial pectoralis major possesses a role not shared by the caudal fibers: initiation of the recovery phase of the locomotor cycle. When ability to execute rapid or powerful recovery of the adducted forelimb is required in an animal with a shoulder joint lying on a plane cranial to that of the manubrium, the movement will be facilitated if the origin of the pectoralis major is extended onto the clavicle. Such is the case in nonhuman primates possessing this trait. The absence of a clavicular origin in Ateles and Pongo may be related to diminished selective pressures to perfect locomotor modes such as pronograde quadrupedalism, armswinging, or climbing thick vertical trunks, that demand rapid or powerful recovery of the adducted forelimb. If the arboreal ancestor of humans had evolved a clavicular origin of pectoralis major, this animal would be preadapted for certain uses of the forelimb in its bipedal descendant.

Alouatta↗

Genome size and constitutive heterochromatin in Hylobates muelleri and Symphalangus syndactylus and in their viable hybrid.

Genome size was measured as the amount of Feulgen-stained DNA in six species of the family Hylobatidae and in a hybrid of the gibbon (Hylobates muelleri) and siamang (Symphalangus syndactylus). The family, on the whole, exhibits a wider range of genome sizes than pongids; in particular, the siamang has about 15% more DNA than the 44-chromosome Hylobates species of the "lar" group. Quantitative analysis of C-heterochromatin in hybrid metaphases showed that the difference in genome size of the parental species correlates with the amount of C-band-positive material. Hylobatids are the only group of primates in which karyotype diversification has taken place with a massive quantitative change in constitutive heterochromatin.

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Responses of gibbons (Hylobates lar) to their mirror images.

Nine gibbons (Hylobates lar) and one gibbon-siamang crossbreed were observed during exposure to their mirror images over two 30 minute baseline condition periods (mirror off) and four 30 minute treatment condition periods (mirror on). Greater frequencies and durations of gazing at the mirror and mirror-contingent behaviors were noted during the reflective conditions than for nonreflective conditions. Despite two subjects' apparent use of the mirror to view body parts otherwise not visible to them, no subjects passed a modified mark test. One subject exhibited limited aggressive displays toward the mirror, but no subjects exhibited abnormal behaviors in the presence of the mirror. The results expand on and confirm similar findings by Lethmate and Dücker [Zeitschrift fur Tierpsychologie 33:248-269, 1973].

Animals↗

Sleeping sites, sleeping places, and presleep behavior of gibbons (Hylobates lar).

The sleeping habits of wild white-handed gibbons (Hylobates lar) were investigated to assess the risk of predation and predation-avoidance behavior. Sleeping sites were distributed throughout home ranges, including areas where they overlapped with neighbors, and appeared to be selected independently of habitat characteristics. Individuals did not build night nests or otherwise manipulate the vegetation around the sleeping place but slept on open branches. Group members usually slept in separate trees, and, except for females with infants, they never shared a sleeping place. Sleeping trees were entered several hours before dusk and were used for about 14-17 h. The majority of sleeping trees were used only once, and fewer were selected repeatedly by the same or other group members. Usually females with infants went into a sleeping tree first, then juveniles, and last were mostly subadult and adult males. Intragroup competition over access to a sleeping place was observed once. Average time difference between the first and last group member to enter a sleeping tree was 13 min. The sequence of departure from sleeping trees was more variable. Gibbon sleeping habits seem to primarily reflect adaptations to minimize predation risk. The predation-risk hypothesis was indirectly supported by observations of mobbing pythons, alarm calls given in response to birdes of prey flying low over the canopy, and more importantly by 1) the predominant use of large sleeping trees, which were among the tallest trees available, particularly by adult females with small infants and juveniles, 2) an unpredictable long-term pattern of reuse of sleeping places, and 3) inconspicuous presleep behavior.

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Linear enamel hypoplasia in gibbons (Hylobates lar carpenteri).

This study describes the expression of linear enamel hypoplasia (LEH), a sensitive dental indicator of physiological stress, in Thailand gibbons (Hylobates lar carpenteri). Previous studies of enamel hypoplasia in hominoids have focused on great apes, with little attention given to the expression of this stress indicator in gibbons. In that gibbons differ from both monkeys and great apes in numerous life history features, LEH expression in gibbons might be expected to show significant differences from both. In this study, 92 gibbon specimens from two sites in Thailand were compared with several samples of monkeys and great apes in their expression of LEH. The intertooth distribution of LEH in gibbons was compared to that of chimpanzees and rhesus monkeys. Gibbon populations from both sites exhibit LEH frequencies intermediate between those of the monkey samples, in which LEH prevalence is usually low, and those of the great ape samples, in which LEH prevalence is high. Gibbons differ significantly from monkeys, but not great apes, in the number of individuals whose teeth record multiple stress events. Multiple episodes of stress are rarely recorded in the teeth of monkeys, while multiple stress events occur with higher frequency in gibbons and great apes. Taxonomic variation in the duration of crown formation, the prominence and spacing of perikymata on dental crowns, life history features, and/or experience of physiological stress may explain these patterns. The intertooth distribution of LEH in gibbons is, for different reasons, unlike that of either chimpanzees or rhesus monkeys. The mandibular canines of gibbons have significantly more LEH than any of their other teeth. Aspects of crown morphology, perikymata prominence/spacing, enamel thickness, and crown formation spans are potential causes of taxonomic variation in the intertooth distribution of LEH.

Animals↗

External forces and torques generated by the brachiating white-handed gibbon (Hylobates lar).

We compared the kinetics of brachiation to bipedal walking and running. Gibbons use pectoral limbs in continuous contact with their overhead support at slow speeds, but exhibit aerial phases (or ricochetal brachiation) at faster speeds. This basic interaction between limb and support suggests some analogy to walking and running. We quantified the forces in three axes and torque about the vertical axis generated by a brachiating White-handed gibbon (Hylobates lar) and compared them with bipedal locomotion. Handholds oriented perpendicular to the direction of travel (as in ladder rungs) were spaced 0.80, 1.20, 1.60, 1.72, 1.95, and 2.25 m apart. The gibbon proportionally matched forward velocity to stride length. Handhold reaction forces resembled ground reaction forces of running humans except that the order of horizontal braking and propulsion were reversed. Peak vertical forces in brachiation increased with speed as in bipedal locomotion. In contrast to bipedalism, however, peak horizontal forces changed little with speed. Gait transition occurred within the same relative velocity range as the walk-run transition in bipeds (Froude number = 0.3-0.6). We oriented handholds parallel to the direction of travel (as in a continuous pole) at 0.80 and 1.60 m spacings. In ricochetal brachiation, the gibbon generated greater torque with handholds oriented perpendicular as opposed to parallel to the direction of travel. Handhold orientation did not affect peak forces. The similarities and differences between brachiation and bipedalism offer insight into the ubiquity of mechanical principles guiding all limbed locomotion and the distinctiveness of brachiation as a unique mode of locomotion.

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Genital swelling in females of the monogamous gibbon, Hylobates (H.) lar.

Cyclical changes in the vulvae of five adult lar gibbons (Hylobates [H.] lar) were studied and compared with those of eight lowland gorillas. The results reveal that the gibbons have relatively conspicuous and specialized sexual swellings that alter shape and appearance during the ovarian cycle. At maximum extent, the genital swellings of gorillas are relatively and absolutely smaller than those of gibbons, and lack the distinctive coloration seen in the genital swellings of the smaller apes. We conclude that the female gibbon's sexual swelling is a far more conspicuous and effective signal of estrus status than that of the gorilla, and that this is not explicable in terms of allometry. Previous investigators have pointed to one-male mating systems, monogamous pair-bonding, or an arboreal habitat as reasons that some primates should have less conspicuous signals of estrus than others. Our findings for the gibbon are the reverse of these predictions, and indicate that sexual selection other than by intermale competition for estrous females is implicated in the ultimate causation of the gibbon's swelling. The adaptive value and significance of the female gibbon's sexual signals remain unclear, however.

Animals↗

Articular structure and function in Hylobates, Colobus, and Papio.

It has been demonstrated in clinical and experimental studies that subarticular trabecular bone responds to mechanical loads transmitted across joints through changes in mass and structural organization. We investigated differences in mass, volume, and density of subarticular trabecular bone of the humeral and femoral head in Hylobates syndactylus, Colobus guereza, and Papio cynocephalus. Our hypothesis was that variations in trabecular properties between taxa may reflect differences in mechanical loading associated with different locomotor repertoires. A nondestructive method for measuring trabecular properties using optical luminance data measured from radiographs was developed. We also examined the relationship between internal trabecular properties and the external size and surface area of the humeral and femoral heads in these taxa. Our results suggest that internal and external articular structure are relatively independent of each other and may be adapted to different aspects of the mechanical environment. Differences in trabecular mass between taxa appear to correspond to differences in the magnitudes of mechanical loads borne by the joint, whereas articular volume and surface area are related primarily to differences in joint mobility. Because of the apparent physiological "de-coupling" of articular mass and volume, variations in articular density (mass/volume) are difficult to interpret in isolation. Comparisons of internal and external articular structure may provide new ways to reconstruct the locomotor/positional behavior of extinct taxa.

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Genomic reorganization and disrupted chromosomal synteny in the siamang (Hylobates syndactylus) revealed by fluorescence in situ hybridization.

We employed in situ hybridization ("chromosome painting") of chromosome-specific DNA libraries of all human chromosomes to establish homologies between the human and siamang karyotypes (Hylobates syndactylus, 2n = 50). Numerous intra- and interchromosomal rearrangements have led to a massive reorganization of the siamang karyotype. There have been a minimum of 33 translocations. The 24 siamang autosomes are composed of 60 recognizable segments that show DNA homology to regions of the 22 human autosomes. Only two autosomes have not been involved in translocations. The siamang presents a case, in a primate closely related to humans, in which chromosome morphology and synteny are highly disturbed in a manner similar to that encountered among rodents.

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The external genitalia of female gibbons, Hylobates (H.) lar.

The external genitalia of one perimenarcheal and five adult female white handed-gibbons (Hylobates (H.) lar) were examined to clarify their gross anatomy. It was found that the vulval structures were complex and exhibited inter-individual variation in arrangement. This complexity appears to result from an ontogenetic process by which the tissues of the vaginal rim (the labia minora) bud-off and extrude extensions toward the vagina immediately prior and subsequent to menarche. Two of these lobular structures surround the urethral meatus and constitute a urethral eminence. The tissues of the vulva, excluding the clitoris with associated prepuce and frenulum and vestigial labia majora, undergo cycles of tumescence and detumescence during intermenstrual intervals. The complex form of the external genitalia and the presence of a swelling cycle are unusual for a monogamous species, are contrary to current applications of sexual selection theory, and raise questions about the significance of mate choice in hominoid evolution.

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A classification efficiency test of spectral karyotyping and multiplex fluorescence in situ hybridization: identification of chromosome homologies between Homo sapiens and Hylobates leucogenys.

Two digital fluorescence microscopy systems, spectral karyotyping (SKY) and multiplex fluorescence in situ hybridisation (M-FISH), are used with multicolour probe sets to assist in the detection of chromosome aberrations. We have compared the resolution of the two methods in their ability to identify karyotype rearrangements, which have occurred during the divergence of Homo sapiens and Hylobates leucogenys in evolution. A 24-color human paint kit distinguishes 74 conserved autosomal segments in H. leucogenys, some of which are difficult to resolve. We examined the extent to which the SKY and M-FISH techniques are able to detect the smallest of these bands. We have found this to be a rigorous test of multicolour chromosome classification systems. We conclude from our results that both systems are able invariably to classify the majority of conserved segments but differ in the efficiency of detection of small inserts.

Animals↗

Genomic reorganization in the concolor gibbon (Hylobates concolor) revealed by chromosome painting.

We employed fluorescence in situ hybridization (FISH) of specific DNA libraries of all human chromosomes to establish homologies between the human karyotype and the karyotype of Hylobates concolor (2n = 52). Numerous intra- and interchromosomal rearrangements have led to a massive reorganization in the karyotype of H. concolor. There have been a minimum of 31 translocations. The 25 H. concolor autosomes are composed of 63-67 recognizable segments that show DNA homology to regions of the 22 human autosomes. Only 1 autosome, homologous to human chromosome 21, has not been involved in translocations. We compared the gene mapping data for H. concolor with our in situ hybridization and found that in most cases these data are confirmed by our results. H. concolor presents a case in a primate closely related to humans, in which chromosome morphology and synteny are highly disturbed in a manner similar to that encountered in rodents.

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Histological reconstruction of dental development and age at death in a juvenile gibbon (Hylobates lar).

Although research on dental development in great apes and modern humans has provided comparative models for life history, growth and development in hominin evolution, almost nothing is known about dental development in their sister group, the hylobatids. Hylobatids are of interest because they differ in important life history variables from other catarrhines of similar body mass, and can help to provide more general models for the factors underlying patterns of dental development. This study uses histological techniques to reconstruct developmental sequence, crown formation times, root extension rates, daily rates of enamel and dentine formation, and age at death in a single specimen of Hylobates lar. Thin sections were prepared of permanent mandibular teeth and analyzed by polarized light microscopy. Age at death was determined to be 2.88 yrs calibrated from a pattern of accentuated growth increments. At this age, permanent teeth in occlusion include I1, I2, and M1. Developing permanent teeth include C1, P3, P4, and M2. P3 lags behind P4 in development, and there is no indication of M3 present in the crypt. Differences between the gibbon specimen and great apes include greater prenatal development of M1, accelerated incisor development relative to molars and prenatal development of I1, no overlap between M2 and M3 crown development, shorter crown formation times, and slower root extension rates of 4-5 micron daily in the molars. Root extension rates are higher in the incisors. The periodicity of growth increments is four days, more similar to macaques than to other hominoids. Daily formation rates for enamel of 1.2-4.9 micron and dentine of 1.7-4.9 micron are similar to those reported for other catarrhines.

Age Determination by Teeth↗

New host record for the entodiniomorphid ciliate, Troglodytella abrassarti, from siamangs (Hylobates syndactylus).

Examination of faecal samples from several diarrhoeic siamangs Hylobates syndactylus (Anthropoidea: Hylobatidae) revealed the presence of numerous entodiniomorphid ciliates whose morphological and ultrastructural characteristics were consistent with those of Troglodytella abrassarti previously recorded from chimpanzees, orangutans and gorillas (Anthropoidea: Pongidae).

Animals↗