Gut microbiota variations in wild yellow baboons (Papio cynocephalus) are associated with sex and habitat disturbance.

Although male and female mammals differ in biological traits and functional needs, the contribution of this sexual dimorphism to variations in gut bacteria and fungi (gut microbiota) in relation to habitat type has not been fully examined. To understand whether the combination of sex and habitat affects gut microbiota variation, we analyzed 40 fecal samples of wild yellow baboons (Papio cynocephalus) living in contrasting habitat types (intact, well-protected vs. fragmented, less protected forests) in the Udzungwa Mountains of Tanzania. Sex determination was performed using the marker genes SRY (Sex-determining Region Y) and DDX3X-DDX3Y (DEAD-Box Helicase 3). Samples were attributed to 34 individuals (19 females and 15 males) belonging to five social groups. Combining the results of sex determination with two amplicon sequencing datasets on bacterial (V1-V3 region of the 16S rRNA gene) and fungal (ITS2) gut communities, we found that overall, baboon females had a significantly higher gut bacterial richness compared to males. Beta diversity estimates indicated that bacterial composition was significantly different between males and females, and this was true for individuals from both well- and less protected forests. Our results highlight the combined role of sex and habitat type in shaping variation in gut microbial communities in wild non-human primates.

Group size and mating system predict sex differences in vocal fundamental frequency in anthropoid primates.

Vocalizations differ substantially between the sexes in many primates, and low-frequency male vocalizations may be favored by sexual selection because they intimidate rivals and/or attract mates. Sexual dimorphism in fundamental frequency may be more pronounced in species with more intense male mating competition and in those with large group size, where social knowledge is limited and efficient judgment of potential mates and competitors is crucial. These non-mutually exclusive explanations have not been tested simultaneously across primate species. In a sample of vocalizations (n = 1914 recordings) across 37 anthropoid species, we investigated whether fundamental frequency dimorphism evolved in association with increased intensity of mating competition (H1), large group size (H2), multilevel social organization (H3), a trade-off against the intensity of sperm competition (H4), and/or poor acoustic habitats (H5), controlling for phylogeny and body size dimorphism. We show that fundamental frequency dimorphism increased in evolutionary transitions towards larger group size and polygyny. Findings suggest that low-frequency male vocalizations in primates may have been driven by selection to win mating opportunities by avoiding costly fights and may be more important in larger groups, where limited social knowledge affords advantages to rapid assessment of status and threat potential via conspicuous secondary sexual characteristics.

Interactions between parasitic helminths and gut microbiota in wild tropical primates from intact and fragmented habitats.

The mammalian gastrointestinal tract harbours a highly complex ecosystem composed of a variety of micro- (bacteria, fungi, viruses, protozoans) and macro-organisms (helminths). Although most microbiota research focuses on the variation of single gut components, the crosstalk between components is still poorly characterized, especially in hosts living under natural conditions. We investigated the gut micro-biodiversity (bacteria, fungi and helminths) of 158 individuals of two wild non-human primates, the Udzungwa red colobus (Procolobus gordonorum) and the yellow baboon (Papio cynocephalus). These species have contrasting diets and lifestyles, but live sympatrically in both human-impacted and pristine forests in the Udzungwa Mountains of Tanzania. Using non-invasive faecal pellets, helminths were identified using standard microscopy while bacteria and fungi were characterized by sequencing the V1-V3 variable region of the 16S rRNA gene for bacteria and the ITS1-ITS2 fragment for fungi. Our results show that both diversity and composition of bacteria and fungi are associated with variation in helminth presence. Although interactions differed by habitat type, in both primates we found that Strongyloides was negatively associated and Trichuris was positively associated with bacterial and fungal richness. To our knowledge, this is one of the few studies demonstrating an interaction between helminth and gut microbiota communities in wild non-human primates.

Correction: Altitude and human disturbance are associated with helminth diversity in an endangered primate, Procolobus gordonorum.

[This corrects the article DOI: 10.1371/journal.pone.0225142.].

Raw milk and fecal microbiota of commercial Alpine dairy cows varies with herd, fat content and diet.

The factors that influence the diversity and composition of raw milk and fecal microbiota in healthy commercial dairy herds are not fully understood, partially because the majority of metataxonomic studies involve experimental farms and/or single factors. We analyzed the raw milk and fecal microbiota of 100 healthy cows from 10 commercial alpine farms from the Province of Trento, Italy, using metataxonomics and applied statistical modelling to investigate which extrinsic and intrinsic parameters (e.g. herd, diet and milk characteristics) correlated with microbiota richness and composition in these relatively small traditional farms. We confirmed that Firmicutes, Ruminococcaceae and Lachnospiraceae families dominated the fecal and milk samples of these dairy cows, but in addition, we found an association between the number of observed OTUs and Shannon entropy on each farm that indicates higher microbiota richness is associated with increased microbiota stability. Modelling showed that herd was the most significant factor affecting the variation in both milk and fecal microbiota composition. Furthermore, the most important predictors explaining the variation of microbiota richness were milk characteristics (i.e. percentage fat) and diet for milk and fecal samples, respectively. We discuss how high intra-herd variation could affect the development of treatments based on microbiota manipulation.

Loss of protozoan and metazoan intestinal symbiont biodiversity in wild primates living in unprotected forests.

In light of the current biodiversity crisis, investigating the human impact on non-human primate gut biology is important to understanding the ecological significance of gut community dynamics across changing habitats and its role in conservation. Using traditional coproscopic parasitological techniques, we compared the gastrointestinal protozoan and metazoan symbiont richness of two primates: the Udzungwa red colobus (Procolobus gordonorum) and the yellow baboon (Papio cynocephalus). These species live sympatrically in both protected and unprotected forests within the Udzungwa Mountains of Tanzania with distinct ecological adaptations and diets. Our results showed that terrestrial and omnivorous yellow baboons had 2 (95% CI 1.47-2.73) and 3.78 (2.62-5.46) times higher gut symbiont richness (both including and excluding rare protozoans) compared to the arboreal and leaf-eating Udzungwa red colobus in unprotected and protected forest, respectively. We also found a consistent depletion of symbiont richness in red colobus living in the unprotected forest fragment compared to the continuous protected forests [the latter having 1.97 times (95% CI 1.33-2.92) higher richness], but not in yellow baboons. Richness reduction was particularly evident in the Udzungwa red colobus monkeys, confirming the pattern we reported previously for gut bacterial communities. This study demonstrates the impact of human activities even on the microbiodiversity of the intestinal tract of this species. Against the background of rapid global change and habitat degradation, and given the health benefits of intact gut communities, the decrease in natural gut symbionts reported here is worrying. Further study of these communities should form an essential part of the conservation framework.

The Gut Microbiota Communities of Wild Arboreal and Ground-Feeding Tropical Primates Are Affected Differently by Habitat Disturbance.

Human exploitation and destruction of tropical resources are currently threatening innumerable wild animal species, altering natural ecosystems and thus, food resources, with profound effects on gut microbiota. Given their conservation status and the importance to tropical ecosystems, wild nonhuman primates make excellent models to investigate the effect of human disturbance on the diversity of host-associated microbiota. Previous investigations have revealed a loss of fecal bacterial diversity in primates living in degraded compared to intact forests. However, these data are available for a limited number of species, and very limited information is available on the fungal taxa hosted by the gut. Here, we estimated the diversity and composition of gut bacterial and fungal communities in two primates living sympatrically in both human-modified and pristine forests in the Udzungwa Mountains of Tanzania. Noninvasively collected fecal samples of 12 groups of the Udzungwa red colobus (Procolobus gordonorum) (n = 89), a native and endangered primate (arboreal and predominantly leaf-eating), and five groups of the yellow baboon (Papio cynocephalus) (n = 69), a common species of least concern (ground-feeding and omnivorous), were analyzed by the V1-V3 region of the 16S rRNA gene (bacterial) and ITS1-ITS2 (fungal) sequencing. Gut bacterial diversities were associated with habitat in both species, most likely depending on their ecological niches and associated digestive physiology, dietary strategies, and locomotor behavior. In addition, fungal communities also show distinctive traits across hosts and habitat type, highlighting the importance of investigating this relatively unexplored gut component.IMPORTANCE Gut microbiota diversity has become the subject of extensive research in human and nonhuman animals, linking diversity and composition to gut function and host health. Because wild primates are good indicators of tropical ecosystem health, we developed the idea that they are a suitable model to observe the consequences of advancing global change (e.g., habitat degradation) on gut microbiota. So far, most of the studies focus mainly on gut bacteria; however, they are not the only component of the gut: fungi also serve essential functions in gut homeostasis. Here, for the first time, we explore and measure diversity and composition of both bacterial and fungal microbiota components of two tropical primate species living in highly different habitat types (intact versus degraded forests). Results on their microbiota diversity and composition are discussed in light of conservation issues and potential applications.

Altitude and human disturbance are associated with helminth diversity in an endangered primate, Procolobus gordonorum.

Gastrointestinal parasites colonizing the mammalian gut influence the host immune system and health. Parasite infections, mainly helminths, have been studied intensively in both humans and non-human animals, but relatively rarely within a conservation framework. The Udzungwa red colobus monkey (Procolobus gordonorum) is an endangered endemic primate species living in the Udzungwa Mountains of Tanzania, a global biodiversity hotspot. Since this endemic primate species is highly sensitive to human disturbance, here we investigate whether habitat type (driven by natural and human-induced factors) is associated with helminth diversity. Using standard flotation and sedimentation techniques, we analyzed 251 fecal samples belonging to 25 social groups from four different forest blocks within the Udzungwa Mountains. Five parasitic helminth taxa were recovered from Udzungwa red colobus, including Trichuris sp., Strongyloides fulleborni, S. stercoralis, a strongylid nematode and Colobenterobius sp. We used Generalized Linear Mixed Models to explore the contribution of habitat type, altitude and fecal glucocorticoid levels (as biomarkers of stress) in predicting gut parasite variation. Although some parasites (e.g., Trichuris sp.) infected more than 50% of individuals, compared to others (e.g., Colobenterobius sp.) that infected less than 3%, both parasite richness and prevalence did not differ significantly across forests, even when controlling for seasonality. Stress hormone levels also did not predict variation in parasite richness, while altitude could explain it resulting in lower richness at lower altitudes. Because human activities causing disturbance are concentrated mainly at lower altitudes, we suggest that protection of primate forest habitat preserves natural diversity at both macro- and microscales, and that the importance of the latter should not be underestimated.

Effects of anthropogenic disturbance on primate density at the landscape scale.

Accurate estimations of the abundance of threatened animal populations are required for assessment of species' status and vulnerability and conservation planning. However, density estimation is usually difficult and resource demanding, so researchers often collect data at local scales. However, anthropogenic pressures most often have landscape-level effects, for example, through habitat loss and fragmentation. We applied hierarchical distance sampling (HDS) to transect count data to determine the effect of habitat and anthropogenic factors on the density of 3 arboreal primate species inhabiting 5 distinct tropical forests across a landscape of 19,000 km2 in the Udzungwa Mountains of Tanzania. We developed a novel, multiregion extension of HDS that allowed us to model density and detectability jointly across forests without losing site-specific information. For all species, the effect of anthropogenic disturbance on density was overwhelmingly negative among metapopulations: -0.63 Angolan colobus (Colobus angolensis palliatus) (95% Bayesian CI -1.03 to -0.27), -0.54 Udzungwa red colobus (Procolobus gordonorum) (-0.89 to -0.22), and -0.33 Sykes' monkey (Cercopithecus mitis monoides) (-0.63 to -0.07). Some responses to habitat factors were shared, notably the negative effect of elevation and the positive effect of climber coverage. These results are important for conservation science and practice because: the among-populations negative responses to anthropogenic disturbance provides a foundation for development of conservation plans that hold at the landscape scale, which is a comprehensive and cost-efficient approach; the among-species consistency in responses suggests conservation measures may be generalized at the guild level, which is especially relevant given the functional importance of primates in tropical rainforests; and the greater primate densities in areas at low elevation, which are closer to human settlements, point to specific management recommendations, such as the creation of buffer zones and prioritization of areas for protection.

Efectos de la Perturbación Antropogénica sobre la Densidad de Primates a Escala de Paisaje Resumen Se requieren estimaciones correctas del tamaño de las poblaciones de animales amenazados para evaluar el estado y la vulnerabilidad de las especies y así planear su conservación. Sin embargo, la estimación de la densidad es usualmente complicada y demanda recursos, así que los investigadores con frecuencia recolectan la información a escala local, a pesar de que la presión antropogénica suele tener efectos a nivel del paisaje; por ejemplo, la pérdida del hábitat y la fragmentación. Aplicamos un muestro jerárquico a distancia (HDS, en inglés) para contar datos por transecto y determinar el efecto de los factores del hábitat y los factores antropogénicos sobre la densidad de tres especies de primates arbóreos en un paisaje de 19,000 km2 en las montañas de Udzungwa en Tanzania. Desarrollamos una novedosa extensión multiregión de HDS que nos permitió modelar en conjunto la densidad y la facilidad de detección en los bosques sin perder información específica del sitio. Para todas las especies, el efecto de la perturbación antropogénica sobre la densidad fue abrumadoramente negativa entre las metapoblaciones: −0.63 para el colobo angoleño (Colobus angolensis palliatus) (95% bayesiano CI de −1.03 a −0.27), −0.54 para el colobo rojo de Udzungwa (Procolobus gordonorum) (de −0.89 a −0.22), y −0.33 para el mono de Syke (Cercopithecus mitis monoides) (de −0.63 a −0.07). Los monos compartieron algunas respuestas a los factores de hábitat, notoriamente los efectos negativos de la elevación y el efecto positivo de la cobertura de plantas trepadoras. Estos resultados son importantes para la ciencia y práctica de la conservación ya que: las respuestas negativas a las perturbaciones antropogénicas entre las poblaciones proporcionan los cimientos para el desarrollo de planes de conservación que serán válidos a nivel de paisaje, la cual es una estrategia completa y rentable; la consistencia de las respuestas entre las especies sugiere que las medidas de conservación pueden estar generalizadas a nivel de gremio, lo cual es de suma relevancia dada la importancia funcional de los primates en los bosques tropicales; y la densidad mayor de primates en áreas con elevación baja, las cuales están próximas a los asentamientos humanos, señalan hacia recomendaciones específicas de manejo, como la creación de zonas de amortiguamiento y la priorización de áreas para proteger.

Optimizing field and analytical procedures for estimating densities of arboreal and threatened primates in tropical rainforest.

The application of distance sampling to primate density estimation is challenging and susceptible to estimation biases, mainly due to the difficulties of properly accounting for variation in species' detectability and of accurately sampling the spread of the social groups. We apply a hierarchical distance sampling approach to primate data, to account for a comprehensive set of environmental covariates of both detectability and abundance, and we propose a novel field routine to measure the spread of groups during transect sampling. We confirm the good potential of this approach, given we obtained refined estimates of primate density (as measured by the Akaike Information Criterion) in comparison to estimates from models without covariates.

Impending extinction crisis of the world's primates: Why primates matter.

Nonhuman primates, our closest biological relatives, play important roles in the livelihoods, cultures, and religions of many societies and offer unique insights into human evolution, biology, behavior, and the threat of emerging diseases. They are an essential component of tropical biodiversity, contributing to forest regeneration and ecosystem health. Current information shows the existence of 504 species in 79 genera distributed in the Neotropics, mainland Africa, Madagascar, and Asia. Alarmingly, ~60% of primate species are now threatened with extinction and ~75% have declining populations. This situation is the result of escalating anthropogenic pressures on primates and their habitats-mainly global and local market demands, leading to extensive habitat loss through the expansion of industrial agriculture, large-scale cattle ranching, logging, oil and gas drilling, mining, dam building, and the construction of new road networks in primate range regions. Other important drivers are increased bushmeat hunting and the illegal trade of primates as pets and primate body parts, along with emerging threats, such as climate change and anthroponotic diseases. Often, these pressures act in synergy, exacerbating primate population declines. Given that primate range regions overlap extensively with a large, and rapidly growing, human population characterized by high levels of poverty, global attention is needed immediately to reverse the looming risk of primate extinctions and to attend to local human needs in sustainable ways. Raising global scientific and public awareness of the plight of the world's primates and the costs of their loss to ecosystem health and human society is imperative.

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.

Integrating field and satellite data for spatially explicit inference on the density of threatened arboreal primates.

Spatially explicit models of animal abundance are a critical tool to inform conservation planning and management. However, they require the availability of spatially diffuse environmental predictors of abundance, which may be challenging, especially in complex and heterogeneous habitats. This is particularly the case for tropical mammals, such as nonhuman primates, that depend on multi-layered and species-rich tree canopy coverage, which is usually measured through a limited sample of ground plots. We developed an approach that calibrates remote-sensing imagery to ground measurements of tree density to derive basal area, in turn used as a predictor of primate density based on published models. We applied generalized linear models (GLM) to relate 9.8-ha ground samples of tree basal area to various metrics extracted from Landsat 8 imagery. We tested the potential of this approach for spatial inference of animal density by comparing the density predictions for an endangered colobus monkey, to previous estimates from field transect counts, measured basal area, and other predictors of abundance. The best GLM had high accuracy and showed no significant difference between predicted and observed values of basal area. Our species distribution model yielded predicted primate densities that matched those based on field measurements. Results show the potential of using open-access and global remote-sensing data to derive an important predictor of animal abundance in tropical forests and in turn to make spatially explicit inference on animal density. This approach has important, inherent applications as it greatly magnifies the relevance of abundance modeling for informing conservation. This is especially true for threatened species living in heterogeneous habitats where spatial patterns of abundance, in relation to habitat and/or human disturbance factors, are often complex and, management decisions, such as improving forest protection, may need to be focused on priority areas.

Sexual selection on male vocal fundamental frequency in humans and other anthropoids.

In many primates, including humans, the vocalizations of males and females differ dramatically, with male vocalizations and vocal anatomy often seeming to exaggerate apparent body size. These traits may be favoured by sexual selection because low-frequency male vocalizations intimidate rivals and/or attract females, but this hypothesis has not been systematically tested across primates, nor is it clear why competitors and potential mates should attend to vocalization frequencies. Here we show across anthropoids that sexual dimorphism in fundamental frequency (F0) increased during evolutionary transitions towards polygyny, and decreased during transitions towards monogamy. Surprisingly, humans exhibit greater F0 sexual dimorphism than any other ape. We also show that low-F0 vocalizations predict perceptions of men's dominance and attractiveness, and predict hormone profiles (low cortisol and high testosterone) related to immune function. These results suggest that low male F0 signals condition to competitors and mates, and evolved in male anthropoids in response to the intensity of mating competition.

Primates in Human-Modified and Fragmented Landscapes: The Conservation Relevance of Modelling Habitat and Disturbance Factors in Density Estimation.

Accurate density estimations of threatened animal populations is essential for management and conservation. This is particularly critical for species living in patchy and altered landscapes, as is the case for most tropical forest primates. In this study, we used a hierarchical modelling approach that incorporates the effect of environmental covariates on both the detection (i.e. observation) and the state (i.e. abundance) processes of distance sampling. We applied this method to already published data on three arboreal primates of the Udzungwa Mountains of Tanzania, including the endangered and endemic Udzungwa red colobus (Procolobus gordonorum). The area is a primate hotspot at continental level. Compared to previous, 'canonical' density estimates, we found that the inclusion of covariates in the modelling makes the inference process more informative, as it takes in full account the contrasting habitat and protection levels among forest blocks. The correction of density estimates for imperfect detection was especially critical where animal detectability was low. Relative to our approach, density was underestimated by the canonical distance sampling, particularly in the less protected forest. Group size had an effect on detectability, determining how the observation process varies depending on the socio-ecology of the target species. Lastly, as the inference on density is spatially-explicit to the scale of the covariates used in the modelling, we could confirm that primate densities are highest in low-to-mid elevations, where human disturbance tend to be greater, indicating a considerable resilience by target monkeys in disturbed habitats. However, the marked trend of lower densities in unprotected forests urgently calls for effective forest protection.

Habitat fragmentation is associated to gut microbiota diversity of an endangered primate: implications for conservation.

The expansion of agriculture is shrinking pristine forest areas worldwide, jeopardizing the persistence of their wild inhabitants. The Udzungwa red colobus monkey (Procolobus gordonorum) is among the most threatened primate species in Africa. Primarily arboreal and highly sensitive to hunting and habitat destruction, they provide a critical model to understanding whether anthropogenic disturbance impacts gut microbiota diversity. We sampled seven social groups inhabiting two forests (disturbed vs. undisturbed) in the Udzungwa Mountains of Tanzania. While Ruminococcaceae and Lachnospiraceae dominated in all individuals, reflecting their role in extracting energy from folivorous diets, analysis of genus composition showed a marked diversification across habitats, with gut microbiota α-diversity significantly higher in the undisturbed forest. Functional analysis suggests that such variation may be associated with food plant diversity in natural versus human-modified habitats, requiring metabolic pathways to digest xenobiotics. Thus, the effects of changes in gut microbiota should not be ignored to conserve endangered populations.

Cues to androgens and quality in male gibbon songs.

Animal vocal signals may provide information about senders and mediate important social interactions like sexual competition, territory maintenance and mate selection. Hence, it is important to understand whether vocal signals provide accurate information about animal attributes or status. Gibbons are non-human primates that produce loud, distinctive and melodious vocalizations resembling more those of birds than of other non-human primates. Wild gibbons are characterized by flexibility in social organization (i.e., pairs and multimale units) as well as in mating system (i.e., monogamy and polyandry). Such features make them a suitable model to investigate whether the physiology (hormonal status) and socio-demographic features find their correspondence in the structure of their songs. By combining male solo song recordings, endocrine outputs using non-invasive fecal androgen measures and behavioral observations, we studied 14 groups (10 pair-living, 4 multimale) of wild white-handed gibbons (Hylobates lar) residing at Khao Yai National Park, Thailand. We collected a total of 322 fecal samples and recorded 48 songs from 18 adult animals. Our results confirmed inter-individuality in male gibbon songs, and showed a clear correlation between androgen levels and song structures. Gibbons with higher androgen levels produced calls having higher pitch, and similarly adult individuals produced longer calls than senior males. Thus, it is plausible that gibbon vocalizations provide receivers with information about singers' attributes.

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.

Effects of social status and stress on patterns of gastrointestinal parasitism in wild white-handed gibbons (Hylobates lar).

Although gibbons (family Hylobatidae) are typically monogamous, polyandrous groups occur regularly. Stress associated with elevated intragroup competition among males in polyandrous groups may increase susceptibility to infectious disease. To better understand this interplay, as well as to provide the first comprehensive assessment of parasitism in free-ranging gibbons, we characterized the richness of gastrointestinal parasites and examined their prevalence in males from 14 groups (10 pair-living, 4 multi-male) of white-handed gibbons (Hylobates lar) at Khao Yai National Park, Thailand. From September 2008 to May 2009, 324 fecal samples were collected from 23 individually recognizable male gibbons and screened for gastrointestinal helminths and protozoa after isolation via fecal floatation, sedimentation, and immunofluorescent antibody detection. A total of 10 parasite species recovered, including seven nematodes, two protozoans, and one trematode. Parasite richness and species-specific prevalence were examined relative to social organization (pair-living vs. multi-male), male status (primary vs. secondary), age (subadult, adult, senior), fecal glucocorticoid levels, and time of the year. No relationship was found between parasite richness and sociodemographic or physiological factors. Similarly, prevalence of infection with parasite species was not associated with the majority of sociodemographic factors; however, Ternidens sp. and Balantidium coli varied seasonally and Trichuris sp. decreased with increasing age. Moreover, observational data suggest that competition is low in this gibbon population, and our findings are consistent with those observations in that cooperative defense may offset stress and reduce susceptibility to infection.