Case report: tularaemia in a white-handed gibbon (Hylobates lar), Germany.

In 2021, a white-handed gibbon (Hylobates lar) succumbed to illness shortly after transfer from one zoo to another in Germany, due to Francisella tularensis subsp. holarctica infection. To determine the source of infection, whole genome sequencing of the gibbon-derived isolate was performed and wild pest rodents (and captive squirrels) from both zoos were screened for F. tularensis. The F. tularensis whole genome sequence obtained from the gibbon was closely related to previous subclade B.281 sequences obtained from hares from Baden-Wuerttemberg, the same region where the gibbon was first housed. However, F. tularensis DNA was detected in one Norway rat from the receiving zoo. Therefore, neither zoo can be excluded as the source of infection.

Genetic analysis of hybridization between white-handed (Hylobates lar) and pileated (Hylobates pileatus) gibbons in a contact zone in Khao Yai National Park, Thailand.

Natural hybridization has played various roles in the evolutionary history of primates. Its consequences range from genetic introgression between taxa, formation of hybrid zones, and formation of new lineages. Hylobates lar, the white-handed gibbon, and Hylobates pileatus, the pileated gibbon, are largely allopatric species in Southeast Asia with a narrow contact zone in Khao Yai National Park, Thailand, which contains both parental types and hybrids. Hybrid individuals in the zone are recognizable by their intermediate pelage and vocal patterns, but have not been analyzed genetically. We analyzed mitochondrial and microsatellite DNA of 52 individuals to estimate the relative genetic contributions of the parental species to each individual, and the amount of introgression into the parental species. We obtained fecal samples from 33 H. lar, 15 H. pileatus and four phenotypically intermediate individuals in the contact zone. Both mitochondrial and microsatellite markers confirmed distinct differences between these taxa. Both H. lar and H. pileatus contributed to the maternal lineages of the hybrids based on mitochondrial analysis; hybrids were viable and present in socially normal reproductive pairs. The microsatellite analysis identified ten admixed individuals, four F1 hybrids, which corresponded to phenotypic hybrids, and six H. lar-like backcrosses. All 15 H. pileatus samples were identified as originating from genetically H. pileatus individuals with no H. lar admixture; hence, backcrossing is biased toward H. lar. A relatively low number of phenotypic hybrids and backcrossed individuals along with a high number of parental types indicates a bimodal hybrid zone, which suggests relatively strong bias in mate selection between the species.

A Behavioural Case Study of Early Social Isolation of a Subadult White-Handed Gibbon (Hylobates lar).

Our aim in this study was to analyse the effects of early social isolation on the behaviour of a white-handed gibbon (Hylobates lar) and at the same time to improve his level of welfare. The subject was a 6-year-old male, isolated from conspecific as well as other non-human primates since he was 3 months old. We presented the gibbon with a series of species-specific vocalisations, and we then introduced a 23-year-old conspecific female into his cage. Our subject did not respond to playbacks, whereas he immediately interacted positively with the conspecific female. After 2 days of presentation, the pair started to spend time in proximity to each other and initiated grooming through the wire-mesh dividing the cages. Four days later we recorded vocal duets. No obvious ste-reotypic behaviours were observed, and the prolonged isolation did not seem to compromise the ability of the young gibbon to socialise with the female conspecific. It appears that prolonged isolation does not always compromise the possibility of recovering socially in a satisfactory manner.

An analysis of white-handed gibbon male song reveals speech-like phrases.

OBJECTIVES: Our goal was to document song phrases of the white-handed gibbon (Hylobates lar), an Asian ape that produces elaborate songs, often in well-coordinated male/female duets. We focused on the male coda, which is produced during vocal turn-taking with one's mate, and particularly its phrases containing rapid spectral and temporal variation, to investigate if modulation rates resemble those of lip-smacking in other nonhuman primates and human speech rhythm. MATERIALS AND METHODS: We produced recordings from a large population of wild gibbons. Using terminology consistent with that used to describe vocalizations in other singing species, we analyzed coda phrases, overall coda properties, coda distinctiveness across individuals, and flexibility of phrase production within song bouts. RESULTS: Our song phrase-level analysis showed that male codas differed between individuals and increase in complexity within song bouts by the addition of the only two male-specific phrases of the species' repertoire. These phrases differ from all others of the species and from vocalizations typical of the larger, nonhuman great apes, in that they contain rapid within-phrase modulation. Their modulation rates (6.82 and 7.34 Hz) are similar to that of lip-smacking in other nonhuman primates and speech in humans and, like human speech, are produced exclusively during exhalation. One phrase type (trills) contains multiple notes per exhalation, another characteristic similar to speech but not most primate vocalizations. DISCUSSION: Our data highlight the complexity and flexibility of gibbon song, and show that particular phrase features likely arose from sexual selection pressures and possess similarities to human speech rhythm.

Leaf swallowing and parasite expulsion in Khao Yai white-handed gibbons (Hylobates lar), the first report in an Asian ape species.

Leaf swallowing behavior, known as a form of self-medication for the control of nematode and tapeworm infection, occurs widely in all the African great apes (Pan troglodytes schweinfurthii, P. t. troglodytes, P. t. verus, P. t. vellerosus, Pan paniscus, Gorilla gorilla graueri), except mountain gorillas. It is also reported to occur in a similar context across a wide array of other animal taxa including, domestic dogs, wolves, brown bears, and civets. Despite long-term research on Asian great and small apes, this is the first report of leaf swallowing in an Asian species, the white-handed gibbon (Hylobates lar) in Khao Yai National Park, central Thailand. We present the first evidence of leaf swallowing (Gironniera nervosa Planch CANNABACEA) behavior (N = 5 cases) and parasite (Streptopharagus pigmentatus) expulsion (N = 4 cases), recorded during 4,300 hr of direct animal observations during two distinct research projects. We recovered 4-18 rough, hairy, and hispid surfaced leaves from each sample, undigested and folded, from the freshly evacuated feces of five different individuals (2 males, 3 females, 5 to 34+ years old) living in three different social groups, between the hours of 06:00 to 10:30. Based on close inspection of the leaves, as observed in chimpanzees, it was clear that they were taken into the mouth, one at a time, folded and detached from the stem with the teeth before swallowing them whole. All instances occurred during the rainy season, the time when nematode worms were also found in the feces, although they were not found together with leaves in the same feces. These striking similarities in the details of leaf swallowing between white-handed gibbons and African great apes, and other animal species, suggest a similar self-medicative function.

Application of multicolor banding combined with heterochromatic and locus-specific probes identify evolutionary conserved breakpoints in Hylobates pileatus.

BACKGROUND: The question what makes Homo sapiens sapiens (HSA) special among other species is one of the basic questions of mankind. A small contribution to answer this question is to study the chromosomal constitution of HSA compared to other, closely related species. In order to check the types and extent of evolutionary conserved breakpoints we studied here for the first time the chromosomes of Hylobates pileatus (HPI) compared to HSA and Hylobates lar (HLA) by means of molecular cytogenetics. RESULTS: Overall, 68 new evolutionary conserved breakpoints compared to HSA could be characterized in this study. Interestingly, only seven of those were different compared to HLA. However, application of heterochromatic human DNA-probes provided evidence that observed high chromosomal rearrangement rates of gibbons in HPI happened rather in these repetitive elements than in euchromatin, even though most centromeric positions were preserved in HPI compared to HSA. CONCLUSION: Understanding genomes of other species and comparing them to HSA needs full karyotypic and high resolution genomic data to approach both: euchromatic and heterochromatic regions of the studied chromosome-content. This study provides full karyotypic data and previously not available data on heterochromatin-syntenies of HPI and HSA.

Gibbon (Hylobates lar) reintroduction success in Phuket, Thailand, and its conservation benefits.

We summarize the results from a long-term gibbon reintroduction project in Phuket, Thailand, and evaluate its benefits to conservation. Between October 2002 and November 2012, eight breeding families of white-handed gibbons (Hylobates lar) were returned to the wild in Khao Phra Thaew non-hunting area (KPT). Wild gibbons were extirpated from Phuket Island by the early 1980s, but the illegal wildlife trade has continued to bring young gibbons from elsewhere to the island's popular tourist areas as pets and photo props. The Gibbon Rehabilitation Project (GRP) has rescued and rehabilitated confiscated and donated captive gibbons since 1992 and aims to repopulate the island's last sizable forest area. Following unsuccessful early attempts at translocation in the 1990s, GRP has now developed specific methods for gibbon reintroduction that have led to the establishment of a small independent, reproducing population of captive-raised and wild-born gibbons on Phuket. Eleven infants have been born wild within the reintroduced population, including a second generation wild-born gibbon in September 2012. Benefits of the GRP project include restoration of the gibbon population on Phuket, rescue of illegally kept gibbons, public education, training of personnel in gibbon conservation work, and gaining experience which may prove useful in saving more severely threatened species. It is unlikely that gibbon (and other large primate) translocations will make a significant contribution to conservation of the species as a whole, and primate translocation projects should not be judged solely by this criterion.

Comprehensive characterization of evolutionary conserved breakpoints in four New World Monkey karyotypes compared to Chlorocebus aethiops and Homo sapiens.

Comparative cytogenetic analysis in New World Monkeys (NWMs) using human multicolor banding (MCB) probe sets were not previously done. Here we report on an MCB based FISH-banding study complemented with selected locus-specific and heterochromatin specific probes in four NWMs and one Old World Monkey (OWM) species, i.e. in Alouatta caraya (ACA), Callithrix jacchus (CJA), Cebus apella (CAP), Saimiri sciureus (SSC), and Chlorocebus aethiops (CAE), respectively. 107 individual evolutionary conserved breakpoints (ECBs) among those species were identified and compared with those of other species in previous reports. Especially for chromosomal regions being syntenic to human chromosomes 6, 8, 9, 10, 11, 12 and 16 previously cryptic rearrangements could be observed. 50.4% (54/107) NWM-ECBs were colocalized with those of OWMs, 62.6% (62/99) NWM-ECBs were related with those of Hylobates lar (HLA) and 66.3% (71/107) NWM-ECBs corresponded with those known from other mammalians. Furthermore, human fragile sites were aligned with the ECBs found in the five studied species and interestingly 66.3% ECBs colocalized with those fragile sites (FS). Overall, this study presents detailed chromosomal maps of one OWM and four NWM species. This data will be helpful to further investigation on chromosome evolution in NWM and hominoids in general and is prerequisite for correct interpretation of future sequencing based genomic studies in those species.

Extra-pair paternity confirmed in wild white-handed gibbons.

Knowledge of the genetic mating system of animal species is essential for our understanding of the evolution of social systems and individual reproductive strategies. In recent years, genetic methods have uncovered an unexpected diversity of paternal genetic contributions across diverse animal social mating systems, but particularly in pair-living species. In most pair-living birds, for example, genetic and behavioral observations have confirmed a previously unknown significance of extra-pair copulations (EPCs) and extra-pair paternity. Among mammals, white-handed gibbons (Hylobates lar) are also known to live in pairs and are traditionally believed to be single-male single-female breeders. However, at Khao Yai National Park, Thailand, behavioral observations have confirmed the occurrence of both EPCs and functional multi-male grouping, but knowledge about the genetic mating system is still unavailable. In this study, we genotyped 89 white-handed gibbons of the Khao Yai population based on fecal samplings and were able to determine paternity for 41 offspring through short tandem repeat analysis. We found that females' stable social partners sired the majority (90.5%) of offspring (N = 38), while only a few (7.1%) offspring (n = 2 confirmed cases; n = 1 inferred case) were conceived with extra-pair partners. The paternity of one offspring remained inconclusive (2.4%), because the offspring's genotype did not mismatch with the genotypes of two potential sires. Like other predominantly pair-living species, gibbons appear to follow a mixed-reproductive strategy. The genetic mating system of wild white-handed gibbons is best described as flexible, primarily monogamous and opportunistically promiscuous. Inc.

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.

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.

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.

Do line-transect surveys systematically underestimate primate densities in logged forests?

The rate at which social groups of primates are encountered in disturbed rain forest may be biased relative to undisturbed rain forest. A recently reported case study revealed a 25% reduction in postlogging raw encounter rates even though the true density of primates remained at the prelogging level. If biased raw encounter rates are typical of disturbed forests, and if they translate into equally biased line-transect density estimates, results of many comparative surveys might prove misleading (ie, apparent declines of primates in disturbed forest may not be real). Here a set of line-transect density estimates from logged forest are tested for systematic bias by comparing them to range-mapping density estimates, and the response of a Fourier series detectability function to several hypothetical patterns of bias in raw encounter rates is illustrated. Tests of line-transect density estimates from logged forest provide no evidence of systematic bias. The Fourier series results suggest that biased raw encounter rates may often be ameliorated by line-transect density estimators. Available evidence suggests that line-transect density estimates or similarly transformed encounter rates usually provide reliable comparative results within the limits of a particular study's resolution. In contrast, conclusions drawn directly from comparative raw encounter rates (without transforming them into density estimates) are more prone to error.

Differential detectability of primates between primary and selectively logged habitats and implications for population surveys.

Much information has been published concerning the accurary of various techniques commonly used for censusing primates. The sources of bias may vary according to the technique used. Accuracy may depend on population density as well as on differential visibility and hence detectability between areas. This paper provides evidence that primates may alter their behavior between areas of primary and selectively logged habitat, which in turn could affect census results. Adoption of cryptic behavior, changes in behavioral profile, and reduction in calling rates reduce the detectability of certain species. Increases in the frequency of subgrouping or in group dispersion may introduce a danger of overestimation of other species, unless differences in the size of foraging units are taken into account.

One-armed brachiation in gibbons (Hylobates lar).

The locomotor and postural behavior of Hylobates lar was studied in a seminaturalistic environment at the New York Zoological Park. A particular locomotor pattern, one-armed brachiation, was observed and filmed. Analysis indicated that the occurrence of one-armed brachiation as a preferred locomotor pattern was rare and was limited to the carrying of food. The limb and joint movements of one-armed brachiation closely resembled those of two-armed brachiation with differences occurring in the angular rotations of the support and the free arms. Analysis showed how a gibbon could maximize its forward momentum during one-armed brachiation. The adaptive value of one-armed brachiation is discussed in reference to brachiating while carrying food and to brachiating with a fracture of a forelimb. Finally, one-armed brachiation is discussed as an example of the concepts of locomotor totipotentiality and locomotor habit.