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

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

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

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

叶猴(Presbytis)、金丝猴(Rhinopithecus)、长臂猿(Hylobates)自由取食时的利手现象

本文报道叶猴、金丝猴、长臂猿自由取食时的利手现象。本研究共用金丝猴12只(雄性8只,雌性4只),叶猴25只(雄性16只、雌性9只),长臂猿5只(雄性3只,雌性2只)。对每个动物而言,总观察次数不少于30次,其结果显示:在雄性金丝猴中,62.5％的动物显示右利,25％显示主利,12.5％无利手现象。在雄性叶猴中,62.5％的动物显示右利,18.7％显示左利,18.7％无利手现象。在3只雄性长臂猿中,2只显示右利,一只无利手现象。 统计结果表明:雄性金丝猴有明显的右利手现象(P<0.05),雄性叶猴右利手现象接近显著(P=0.06),长臂猿因观察数量太少,未进行统计。 在上述三种动物中,雌性个体无利手现象。 木工作结果提示:(1)雄性金丝猴,叶猴在自由取食时具有右利手现象,长臂猿也可能有右利手现象,(2)大脑两半球的不对称性与性别有关。     

Mechanisms of force and power production in unsteady ricochetal brachiation

Brachiators travel by swinging beneath handholds, and it is not obvious how these animals manage to accelerate and decelerate in a horizontal direction, especially when moving rapidly. Most previous analyses focused on brachiation in highly constrained laboratory conditions that induced steady-state locomotion. Emerging understanding of brachiation suggests that much of gibbon locomotory behavior and morphology must be considered within the context of the complexities of the natural environment: the forest canopy is three-dimensional, with high variation in handhold availability and properties. The goal of this paper is to quantify the active mechanisms by which gibbons can dynamically control their velocity.Force production and kinematics were analyzed from a white-handed gibbon Hylabates lar during ricochetal brachiation. Both the mechanisms of force production and power input may be inferred for accelerating and decelerating brachiation by combining force data with kinematics. Examples of steady-state, accelerating, and decelerating ricochetal brachiation are highlighted.Gibbons are able to produce net horizontal impulses by releasing early (resulting in a loss of potential energy, but an accelerating horizontal impulse) or delaying release (associated with an increase in potential energy, and a decelerating horizontal impulse).Torque about the shoulder, leg-lifting (or dropping), and elbow flexing (or straightening) are discussed as potential mechanisms for controlling energy within the brachiating system. Of these possibilities, leg-lifting and arm-flexing were observed as mechanisms of adding mechanical energy. Net energy loss, and substantial torques about the shoulder, were not observed.     

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.     

黑长臂猿(Hylobates concolor)鸣叫行为研究

本文基于对云南黑长臂猿多年的野外研究,报道其鸣叫行为的一些特性。黑长臂猿通常在上午鸣叫,且大多数发生在930分以前,鸣叫的起始时间具季节性变化,有两个较为集中的时间,一个在730分左右,另一个在830分左右,然而起始时间并不与日出时间一致。黑长臂猿平均每两天鸣叫一次,日鸣叫发生频次在50％左右,鸣叫的发生也随着季节而变化。鸣叫的持续时间无群体的差异,一次鸣叫的平均时间在12分钟左右（除了GG群）,但群体在不同季节鸣叫时间长短不一。本文的研究结果同时还表明一个群体的鸣叫并未引起邻近其它群体的鸣叫。     

Longitudinal patterns of reproduction in wild female siamang (Hylobates syndactylus) and white-handed gibbons (Hylobates lar)

I present the 6- year reproductive histories of three wild female siamang (Hylobates syndactylus)and four white-handed gibbons (Hylobates lar)at the Ketambe Research Station (Sumatra, Indonesia). Reproductive output varied considerably among females. Two females failed to gestate: both were nulliparous young adult H. lar,one of which remained unpaired for 4 years after dispersing from her group, while the other lost her recently acquired mate to another female. Only one- (a white-handed gibbon)- gave birth more than once, yielding interbirth intervals of 22 and 31 months. Pair bond stability or reduced interspecific feeding competition or both factors may have contributed to the brevity of these intervals. The other females- one H. lar,and three H. syndactylus-each gave birth once, suggesting minimum interbirth intervals exceeding 4–5 years (H. lar)and 3 years (H. syndactylus)in these individuals. Even given the pronounced variation observed among H. lar,these data suggest that interbirth intervals may often exceed the 2- to 3- year interval commonly attributed to these two species. Sources of reproductive failure were 1) maternal abandonment of the neonate due to impaired ability to provide maternal care (H. syndactylus,),(2) premature or stillbirth (H. syndactylus,),and (3) pregnancy termination (H. lar).These data and a review of information on longevity and age at menarche suggest that the actual lifetime reproductive output of a siamang or white-handed gibbon female may often fall far short of the 10 offspring/lifetime originally proposed for these species. Indeed, females may rear as few as five offspring to weaning in a lifetime, which is a figure reminiscent of the reproductive potential of some pongids. Finally, variance in female reproductive success is higher than expected in these monogamous species, which suggests that females (and males) are under strong selective pressure to exert mate choice, possibly through acquisition of (new) mates and extrapair copulations. Future research must clarify the availability of opportunities for paired adults to engage in these sociosexual behaviors.     

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.     

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.     

Sexual dimorphism in Laccopithecus robustus, a late miocene hominoid from China

Laccopithecus robustus is a siamang-sized fossil ape from the Miocene site of Lufeng, China. The species is known from a partial cranium, numerous mandibles, and scores of isolated teeth. This species shows striking dental similarities to Pliopithecus from the Miocene of Europe and a number of cranial similarities to extant gibbons. Laccopithecus differs from extant gibbons and resembles other fossil and extant apes in showing marked sexual dimorphism in the size and shape of the canines and anterior lower premolars. Evidence for sexual differences in either the size or shape of other teeth is less clear. There is some evidence for a sexual size dimorphism based on the variability of molar teeth.     

黑长臂猿的分布、现状与保护

黑长臂猿 (Hylobates concolor)是现生 1 1种长臂猿中其系统地位最低的灵长类。历史时期长臂猿曾广泛分布在我国南部的大部省区。自公元 4世纪以来 ,它们的分布发生了很大变化。分布区从北到南 ,从东到西急剧缩小 ,现黑长臂猿缩小到只在海南岛、云南南部和越南北部 ,已分化为 6个亚种。分布于我国的 5亚种中 ,海南亚种 (H . c. hainanus)现今仅20余只 ,是最濒危的一个亚种 ;.北部湾亚种 (H.c.nasutus) 50年代曾在广西西南部发现 ,60 -70年代已绝迹 ;指名亚种 (H.c.concolor)主要分布于越南北部、滇南和滇中哀牢山。滇南约有100余只 ,滇中哀牢山可能有40 - 60群 ,180 - 240只 ;景东亚种 (H . c. jingdongensis)为滇中无量山的特有亚种 ,现有100 - 116群 ,430 - 500只 ;滇西亚种 (H . c. furvogaster) ,只分布在滇西南的沧源、镇康、云县和耿马等地 ,约有 2 6-42群 ,100 - 150只。现今 ,黑长臂猿的分布区已不足1000Km2 ,总数量约1000只 ,为高度濒危的灵长类动物。造成黑长臂猿濒危的主要原因是 :热带和南亚热带原始森林的被破坏和缩小、人类活动的干扰使生境破碎和恶化、过度猎捕和长臂猿自身的生物学弱点。目前 ,中国的黑长臂猿已在 9个自然保护区中得到保护。     

A comparative analysis of internal cranial anatomy in the hylobatidae

Craniometric studies on the hylobatids using external metrics (Creel and Preuschoft, 1976 , 1984 ) sorted hylobatid populations into primary species groupings which are in accordance with the four currently recognized generic‐level groupings. The goal of the current study was to assess the relative orientations of the orbits, palate, and basioccipital clivus among the hylobatid genera in an effort to further clarify whether the lesser apes differ significantly in these internal cranial features and how that variation patterns across the groups. Nine angular variables quantifying orbital, palatal, and basioccipital clivus orientations were measured on lateral view radiographs of adults representing three of the four hylobatid genera: Hylobates; Nomascus; and, Symphalangus. The interspecific adult hylobatid means for the angular variables were analyzed using t‐test contrasts. The total sample was further subjected to discriminant function analysis (DFA) to test for the ability of craniofacial angular variables to distinguish the hylobatid genera from one another. The three hylobatid genera displayed significant morphological differentiation in orbital, palatal, and posterior skull base orientations. Normal, jackknifed, and cross‐validation DFA procedures correctly identified the hylobatids 50–100% of the time. The observed morphological patterns generally mapped onto the findings of earlier external craniometric hylobatid studies and suggest concordance between specific internal and external cranial features. This article is the first comprehensive study of variation in internal cranial anatomy of the Hylobatidae and includes the first published craniofacial angular data for Nomascus. Am J Phys Anthropol 143:250–265, 2010. © 2010 Wiley‐Liss, Inc.     

Responsiveness of a male Mueller's gibbon to his own species-song,that of a lar gibbon,and a synthetic song of similar frequency

The study compared the responsiveness of a captive male Mueller's gibbon to audio recordings of dawn songs of wild-living male Mueller's gibbons and lar gibbons, and to a synthetic song constructed from screech owl vocalizations. Though wild-caught, the subject had not been exposed to songs of his own species for at least 10 years, and in fact, only rarely performed the dawn song himself. Initially, the subject responded vigorously to all three recordings, with no preference being shown for the recording of his own species. However, a very strong preference for Mueller's vocalizations did develop following a period of concentrated and exclusive exposure to Mueller's songs.     

Interactive singing of a male Mueller's gibbon with a simulated neighbor

This study provides evidence for interactive singing, or countersinging, in the dawn song of a male Mueller's gibbon. Tape-recorded answering calls from a simulated neighbor were initiated at the subject's baseline rate (every 18 sec), then successively at every 14 sec, 10 sec, 18 sec, 22 sec, and 26 sec. Two types of evidence for interactive singing were considered. First, the subject's initiation rate significantly increased when the initiation rate of the simulated neighbor increased (but did not decrease when the simulated neighbor's rate decreased). Second, the subject's rate of interruption of the simulated neighbor's vocalizations remained at the same low level regardless of the initiation rate of the simulated neighbor; these interruption rates were, in all cases, significantly lower than would have been expected by chance if interactive singing were not occurring. Evolutional value of interactive singing is considered in relation to demonstration of individual fitness and achievement of clear communication between neighboring groups.     

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.     

Interspecific spacing between gibbons (Hylobates klossii) and langurs (Presbytis potenziani) on Siberut Island,Indonesia

Spatial arrangement and social interactions of two sympatric and ecologically similar primate species, Hylobates klossii and Presbytis potenzianai, are described from field observations made between July 1972 and October 1974 on Siberut Island, Indonesia. Gibbon territories and langur home ranges overlap extensively. Because gibbons have the ability to supplant langurs at shared food sources, langurs are at a competitive disadvantage. To avoid or decrease the frequency of hostile interactions with gibbons, langurs locate their core areas on boundaries between adjacent gibbon territories, which permits langurs to retreat across these barriers in response to gibbon movements. Langurs further enhance segregration by leaving their sleeping trees earlier than gibbons, gaining additional feeding time on contested food sources. This form of interspecific spatial organization between gibbons and langurs resembles certain predator-prey spacing systems, where territorial boundaries between adjacent predators serve as sanctuaries for prey populations.     

Hypertrichosis in a gibbon (Hylobates muelleri)

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

Lethal territorial aggression in a white-handed gibbon

During an intergroup conflict an adult male white-handed gibbon (Hylobates lar) from one group was attacked and wounded by the adult male of a neighboring group. The wounded male's calling behavior, general activity level, feeding, and participation in territorial defense declined dramatically in the days following the injury as he instead spent long periods resting and tending the wound. The normal and healthy appearance of this male prior to injury, the circumstances of the fight that caused the injury, the resultant deterioration in normal maintenance and social behavior, and finally the apparent infection of the wound by insect larvae all suggested that his disappearance 24 days later was the result of death due directly or indirectly to the wound he had suffered. The observations reported here suggest that the ritualization of territorial aggression in this species has not eliminated risks of serious injury and death. © 1993 Wiley-Liss, Inc.     

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.     

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.