Comparison of Activity Budgets, Diet, and Habitat Utilization between Provisioned and Wild Groups of the François' Langur (Trachypithecus francoisi) in Mayanghe National Nature Reserve, China.

The endangered François' langur (Trachypithecus francoisi) is only found from southern China to northeastern Vietnam. This study evaluates behavioral differences between provisioned (Ts, 7 individuals) and wild (Tn, 13 individuals) family groups in Mayanghe National Nature Reserve, China. Scan sampling every 5 min for 12 h daily between the months of March 2013 and February 2014 was used to record behaviors in seven categories. Tn exhibited three main feeding periods daily, whereas Ts showed more variable behavioral patterns that relied on provisions. The Tn alpha male showed twice the amount of guarding behavior compared with the Ts alpha male. The proportion of each habitat type utilized differed significantly between Tn and Ts (χ2[4] = 17,131.4, p < 0.01). Additionally, dietary diversity differed between the two groups: Tn fed on 61 plant species, whereas Ts fed on 43 plant species. Tn rarely ate sweet potato and corn other than discarded remnants of human food (0.2% of their total food sources), whereas these foods represented 21.8% of Ts food sources. We compared data for the two troops to understand this species' activities under human interference, in particular to determine whether provisioning is a suitable strategy for their conservation.

Effect of Group Size on Time Budgets and Ranging Behavior of White-Headed Langurs in Limestone Forest, Southwest China.

The ecological constraints model is well supported by data from most frugivorous primates; however, the prediction power of the model is weak for folivorous primates. From September 2016 to August 2017, we collected comparative data on time budgets, daily path lengths and diets of four groups of white-headed langurs (Trachypithecus leucocephalus), including two large groups (G-DS and G-ZWY) and two small groups (G-LZ and G-NN) in Chongzuo White-Headed Langur National Nature Reserve, Guangxi Province, Southwest China. The aim was to obtain evidence of foraging competition and to test the ecological constraints model on this highly folivorous primate in its karst habitat. The results showed that langurs in the larger groups spent more time traveling, less time resting, and had a longer average daily path length than those in the small groups. Diet composition and dietary diversity were not significantly different between the large and small groups. Our study demonstrates that langurs from large groups suffer scramble competition in limestone forests and supports the validity of the ecological constraints model for folivores.

Lichen as a Biomonitor for Vehicular Emission of Metals: A Risk Assessment of Lichen Consumption by the Sichuan Snub-Nosed Monkey (Rhinopithecus roxellana).

Two lichen species, Usnea aciculifera and Usnea luridorufa, were used as biomonitors for the deposition of traffic-related metals in China's Shennongjia National Nature Reserve. The suitability of the two lichen species for use as biomonitors was compared. The health threat to the Sichuan snub-nosed (aka golden) monkey (Rhinopithecus roxellana) from consuming lichen with elevated metal concentrations due to vehicular traffic was then assessed. Lichens, with large surface areas and neither roots nor stomata, efficiently absorb both particulate and gaseous air pollutants. The resulting data was used to assess the effect of heavy metal accumulation on the lichens as well as the health risk imposed on the monkeys as lichen is a primary food source. Lichen samples were collected in the core area of the reserve at three locations of varying traffic intensity. A forth site in the reserve, with no proximate traffic, was used as the control. Results show: (1) lichen from high traffic sites has significantly higher concentrations of Fe, Cd, Pb Zn, and Cr than lichen collected from the control site; (2) vehicular traffic is the primary source of metals in lichen; (3) U. luridorufa collected at high traffic sites displayed decreased photosynthetic efficiency, an indication of stress; (4) intake of Cd and Pb from vehicle emissions in the Shennongjia National Nature Reserve could adversely affect snub-nosed monkey health. This research advances the science of biomonitoring, contributes to environmental protection efforts in China's nature reserves and helps improve food safety for Sichuan snub-nosed monkey, a national treasure of China.

Preliminary report on Sichuan golden snub-nosed monkeys (Rhinopithecus roxellana roxellana) at Laohegou Nature Reserve, Sichuan, China.

Comparative studies of subspecies under different ecological environments offer insights into intraspecies evolutionary adaptive mechanisms. Golden snub-nosed monkeys (Rhinopithecus roxellana) include three subspecies in China classified mainly by their morphological variations: R. r. roxellana (Sichuan and Gansu province), R. r. qinlingensis (Shaanxi province) and R. r. hubeiensis (Hubei province). These three subspecies live in three isolated area with different environments. Past works focused on the last two subspecies, but little information of habitat and behaviors of the nominated subspecies (R. r. roxellana) is available to date. We conducted a two-year study on the diet, activity budget, home range and social organization of 4 herds of R. r. roxellana, based on a total of 106 days' observation in Laohegou (LHG) Nature Reserve, Sichuan province. By using scan sampling method, our results suggest that the R. r roxellana feeds predominantly on leaves (77.5%), and spends more time feeding (40.0%) and resting (27.0%) while compared to the other two subspecies. Kernel Density Estimation Method based on GPS technology confirms that R. r roxellana has relatively larger home ranges (49.1 km2). The unit size (8.3 ± 3.5 individuals) of R. r roxellana is also smaller. Therefore, it is possible that differences in food availability in relation to habitats have important impacts on the feeding strategy and social system of the golden snub-nosed monkey. These results provide data to further explore intraspecific adaptations of living primates.

Deciphering the Social Organization and Structure of Wild Yunnan Snub-Nosed Monkeys (Rhinopithecus bieti).

The social organization of natural groups of Rhinopithecus bieti (Yunnan snub-nosed monkey) is virtually unknown. We studied the demography and social structure of a free-ranging group at Samage Forest, China, for nearly 2 years. This study confirmed that R. bieti exhibits a multilevel social organization of core 1-male units (OMUs) that congregate in a band of >400 members. Even though the band appeared to be unified for the most part, we also witnessed occasional fission-fusion. OMUs were cohesive entities, and their members were spatially and socially isolated from members of other OMUs. Large all-male units associated with the band, and when they closely followed OMUs there was a tendency for elevated male aggression. Within OMUs, females associated preferentially with males and vice versa, resulting in a bisexually bonded society. Contrary to other Asian colobines, R. bieti were comparatively social, with grooming occupying 7.3% of the time. Social grooming was primarily a female affair, but males also participated in grooming networks. The integration of males into the social network of the OMU is thought to help to maintain OMU integrity and cohesion with other social units being in close proximity.

Was Mesopithecus a seed eating colobine? Assessment of cracking, grinding and shearing ability using dental topography.

Extant colobine monkeys have been historically described as specialized folivores. However, reports on both their behavior and dental metrics tend to ascribe a more varied diet to them. In particular, several species, such as Pygathrix nemaeus and Rhinopithecus roxellana, are dedicated seasonal seed eaters. They use the lophs on their postcanine teeth to crack open the hard endocarp that protects some seeds. This raises the question of whether the bilophodont occlusal pattern of colobine monkeys first evolved as an adaptation to folivory or sclerocarpic foraging. Here, we assess the sclerocarpic foraging ability of the oldest European fossil colobine monkey, Mesopithecus. We use computed microtomograpy to investigate the three-dimensional (3D) dental topography and enamel thickness of upper second molars ascribed to the late Miocene species Mesopithecus pentelicus from Pikermi, Greece. We compare M. pentelicus to a sample of extant Old World monkeys encompassing a wide range of diets. Furthermore, we combine classic dietary categories such as folivory with alternative categories that score the ability to crack, grind and shear mechanically challenging food. The 3D dental topography of M. pentelicus predicts an ability to crack and grind hard foods such as seeds. This is consistent with previous results obtained from dental microwear analysis. However, its relatively thin enamel groups M. pentelicus with other folivorous cercopithecids. We interpret this as a morphological trade-off between the necessity to avoid tooth failure resulting from hard food consumption and the need to process a high amount of leafy material. Our study demonstrates that categories evaluating the cracking, grinding or shearing ability, traditional dietary categories, and dental topography combine well to make a powerful tool for the investigation of diet in extant and extinct primates.

Are simakobu (Simias concolor) loud calls energetically costly signals?

OBJECTIVES: Male vocal displays play an important role in sexual selection in many species. If there are costs or constraints, calls may convey honest information about the caller. We studied the loud calls of male simakobu (Simias concolor), a sexually dimorphic primate that resides in one-male groups, on Siberut Island, Indonesia. MATERIALS AND METHODS: We combined behavioral and ecological data with acoustic analysis to determine the influence of energy costs and status on calling effort. Based on all-day follows (n = 107) and loud-call recordings (n = 186), we determined how calling rates and durations varied in relation to short-term (time of day, temperature, travel distance) and long-term (fruit availability, physical condition) measures of energy availability and expenditure. RESULTS: We found that males avoided calling at the hottest times of the day, and produced shorter calls at higher temperatures, supporting the hypothesis that calls are influenced by thermoregulation costs. A peak of longer duration calls just before sunrise, however, could not be explained by energy constraints, but we hypothesize that this pattern is related to the fact that dawn calls occur in choruses, motivating males to call longer than their neighbors. Contrary to predictions, calling rates increased with decreasing fruit availability and did not appear to be energetically costly. DISCUSSION: We hypothesize that calling rates instead reflect strategies involving feeding and/or mate competition, signaling the motivation, rather than fighting ability, of the caller. Overall, results only weakly support the hypothesis that the timing and duration-but not rate-of simakobu loud calls are influenced by energy costs. Am J Phys Anthropol 161:44-52, 2016. © 2016 Wiley Periodicals, Inc.

Folivory as a Constraint on Social Behaviour of Langurs in South India.

Folivory, being a dietary constraint, can affect the social time of colobines. In the present study, we compared food items and activity budgets of two closely related species of colobines inhabiting South India, i.e. the Hanuman langur (Semnopithecus hypoleucos) and Nilgiri langur (Semnopithecus johnii), to determine whether folivory had an impact on social time in these species. Our study established that Nilgiri langurs were more folivorous than Hanuman langurs. Nilgiri langurs spent much less time on social activities, but more time on resting, although the social organization of S. hypoleucos was similar to that of the Nilgiri langur. The enforced resting time for fermentation of leafy food items may have reduced the time available for social interactions, which in turn affected the social time in Nilgiri langurs. By comparing the data from previous studies on other Hanuman langur species, we found that S. hypoleucos spent a similar amount of time on social activities as Semnopithecus entellus. Hence, the social behaviour of S. entellus and S. hypoleucos is phylogenetically highly conservative.

Affiliative interactions between one-male units in a band of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) living in the Qinling Mountains, China.

We studied affiliative behaviors that occurred within and between one-male units (OMUs) in a band of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) living in the Qinling Mountains, China for 3 years from 2002 to 2004. During the birth season, females handling infants of other females affiliatively interacted with females in neighboring OMUs as well as with females in their own OMU. After these interactions, affiliative encounters occurred without conflict between the OMUs. In the mating season, females sometimes presented their genitals to males of other OMUs. These interactions may facilitate the maintenance of a higher level social organization, a band. Therefore, the band composed of OMUs and all male group(s) is the basic unit of social structure of this species. Almost all other Asian colobines have OMUs that either maintain distance from each other or engage in territorial defense, so these OMUs would not be expected to form a band. Contrary to these species, the 3 species of Rhinopithecus spp. inhabiting China form a band composed of OMUs, because infants and females may function as a bridge connecting OMUs.

Differences in the activity budgets of Yunnan snub-nosed monkeys (Rhinopithecus bieti) by age-sex class at Xiangguqing in Baimaxueshan Nature Reserve, China.

The activity budgets of primates reflect their survival strategy. Despite existing data on the activity budgets of Yunnan snub-nosed monkeys (Rhinopithecus bieti), little is known about how activity budgets vary between age-sex classes. This study provides the first detailed activity budgets subdivided by age-sex class, based on observations of the largest habituated group of R. bieti at Xiangguqing in Baimaxueshan Nature Reserve. This study was conducted from June 2008 to May 2009. We found that adult females spent more time feeding (44.8%) than adult males (39.5%), juveniles (39.1%) and infants (14.2%). Females allocated significantly more time to feeding than to any other activity. Adult males allocated more time to miscellaneous activities (12.5%) than adult females (3.8%). Juveniles allocated less time to grooming than adults. Infants were being groomed 6.9% of the time, the highest proportion among all age-sex classes. Adults spent more time feeding, while immature individuals allocated more time to moving and other activities. There are several reasons why activity budgets can vary by age-sex class: (1) differential reproductive investment between males and females; (2) developmental differences among the age categories, and (3) social relationships between members of different age-sex classes, particularly dominance. These variations in activity budgets among the different age-sex classes may become a selective pressure in this species.

Supply and demand determine the market value of access to infants in the golden snub-nosed monkey (Rhinopithecus roxellana).

According to a biological market paradigm, trading decisions between partners will be influenced by the current 'exchange rate' of commodities (good and services), which is affected by supply and demand, and the trader's ability to outbid competitors. In several species of nonhuman primates, newborn infants are attractive to female group members and may become a desired commodity that can be traded for grooming within a biological market place. We investigated whether grooming was interchanged for infant handling in female golden snub-nosed monkeys (Rhinopithecus roxellana) inhabiting the Qinling Mountains of central China. R. roxellana exhibit a multilevel social organization characterized by over 100 troop members organized into 6-11 one-male units each composed one adult male and several adult females and their offspring. Behavioral data were collected over the course of 28 months on grooming patterns between mothers with infants less than 6 months old (N = 36) and other adult female troop members. Our results provide strong evidence for the interchange of grooming for access to infants. Grooming for infant access was more likely to be initiated by potential handlers (nonmothers) and less likely reciprocated by mothers. Moreover, grooming bout duration was inversely related to the number of infants per female present in each one-male unit indicating the possibility of a supply and demand market effect. The rank difference between mothers and handlers was negatively correlated with grooming duration. With increasing infant age, the duration of grooming provided by handlers was shorter suggesting that the 'value' of older infants had decreased. Finally, frequent grooming partners were allowed to handle and maintain access to infants longer than infrequent groomers. These results support the contention that grooming and infant handling may be traded in R. roxellana and that the price individuals paid for access to infants fluctuated with supply and demand.

Patch depletion behavior differs between sympatric folivorous primates.

Food competition in group-living animals is commonly accepted as a critical determinant of foraging strategies and social organization. Here we examine food patch depletion behavior in a leaf-eating (folivorous) primate, the guereza (Colobus guereza). Snaith and Chapman (2005) studied the sympatric folivorous red colobus (Procolobus rufomitratus), which shares many food resources with the guereza. They determined that red colobus deplete the patches (feeding trees) they use, while we found contrary evidence for guerezas using the same methods. We found that the time guerezas spent feeding in a patch was affected by neither tree size, an indicator of food abundance, nor the size of the feeding group, an indicator of feeding competition. For their principal food item (young leaves), intake rate remained constant and coincided with a decrease in the distance moved to find food within a patch, implying that guerezas do not deplete patches. This points to a fundamental difference in the use of food by guerezas and red colobus, which may be linked to the large difference in their group sizes and/or to a disparity in their digestive physiologies. However, further analyses revealed that the number of feeders within a patch did not affect patch depletion patterns in either species, leaving the potential for a physiological basis as the most plausible explanation. Our research highlights the need for a more critical examination of folivorous primate feeding ecology and social behavior, as all folivorous primates are typically lumped into a single category in socioecological models, which may account for conflicting evidence in the literature.

Nocturnal sleeping habits of the Yunnan snub-nosed monkey in Xiangguqing, China.

Weather, predation, and social organization are hypothesized to influence sleeping habits of nonhuman primates at night. To investigate how the Yunnan snub-nosed monkey (Rhinopithecus bieti) prepares for and behaves during cold nights in their harsh alpine forest habitat (above 3,000 m), we studied the sleeping habits of the 171 one-male units (OMU) in one group for 12 months at Xiangguqing in the Baimaxueshan Nature Reserve, China. It took 20.2 min from the time the study group entered a sleeping site until they fell asleep. This duration was consistent over seasons. On average, sleeping time was 11.5 hr per night over the year. Seasonal mean lengths of sleeping time varied significantly, however, and ranged from 10 to 13 hr per night, correlating with night length. Two sleeping styles were distinguishable: solitary sleeping and huddled sleeping. That adult males in OMUs principally slept alone. This is likely to reflect night-time guarding behavior. Female-juvenile and female-infant dyadic huddles were the most prevalent sleeping unit (42% of all observed data), and the monkeys employed female-biased huddling during nocturnal sleep. Huddled sleeping group size showed significant seasonal variation, with the largest huddle (eight individuals) occurring in winter. Climate and social organization profoundly influence the nocturnal sleeping habits of R. bieti, while huddling behavior may help shield animals from cold nights and provide additional protection against predators.

A Bayesian analysis of the temporal change of local density of proboscis monkeys: implications for environmental effects on a multilevel society.

To understand the effects of environmental factors on a social system with multilevel society in proboscis monkey units, the temporal change of the local density of sleeping sites of monkeys was investigated along the Menanggul river from May 2005 to 2006 in Malaysia. Proboscis monkeys typically return to riverside trees for night sleeping. The sleeping site locations of a one-male unit (BE-unit) were recorded and the locations of other one-male and all-male units within 500 m of the BE-unit were verified. In addition, environmental factors (food availability, the water level of the river, and the river width) and copulation frequency of BE-unit were recorded. From the analyses of the distance from the BE-unit to the nearest neighbor unit, no spatial clumping of the sleeping sites of monkey units on a smaller scale was detected. The results of a Bayesian analysis suggest that the conditional local density around the BE-unit can be predicted by the spatial heterogeneity along the river and by the temporal change of food availability, that is, the local density of monkey units might increase due to better sleeping sites with regard to predator attacks and clumped food sources; proboscis monkeys might not exhibit high-level social organization previously reported. In addition, this study shows the importance of data analysis that considers the effects of temporal autocorrelation, because the daily measurements of longitudinal data on monkeys are not independent of each other.

Fallback foods of temperate-living primates: a case study on snub-nosed monkeys.

Only a few primate species thrive in temperate regions characterized by relatively low temperature, low rainfall, low species diversity, high elevation, and especially an extended season of food scarcity during which they suffer from dietary stress. We present data of a case study of dietary strategies and fallback foods in snub-nosed monkeys (Rhinopithecus bieti) in the Samage Forest, Northwest Yunnan, PRC. The snub-nosed monkeys adjusted intake of plant food items corresponding with changes in the phenology of deciduous trees in the forest and specifically showed a strong preference for young leaves in spring. A non-plant food, lichens (Parmeliaceae), featured prominently in the diet throughout the year (annual representation in the diet was about 67%) and became the dominant food item in winter when palatable plant resources were scarce. Additional highly sought winter foods were frost-resistant fruits and winter buds of deciduous hardwoods. The snub-nosed monkeys' choice of lichens as a staple fallback food is likely because of their spatiotemporal consistency in occurrence, nutritional and energetic properties, and the ease with which they can be harvested. Using lichens is a way to mediate effects of seasonal dearth in palatable plant foods and ultimately a key survival strategy. The snub-nosed monkeys' fallback strategy affects various aspects of their biology, e.g., two- and three-dimensional range use and social organization. The higher abundance of lichens at higher altitudes explains the monkeys' tendency to occupy relatively high altitudes in winter despite the prevailing cold. As to social organization, the wide temporal and spatial availability of lichens strongly reduces the ecological costs of grouping, thus allowing for the formation of "super-groups." Usnea lichens, the snub-nosed monkeys' primary dietary component, are known to be highly susceptible to human-induced environmental changes such as air pollution, and a decline of this critical resource base could have devastating effects on the last remaining populations. Within the order Primates, lichenivory is a rare strategy and only found in a few species or populations inhabiting montane areas, i.e., Macaca sylvanus, Colobus angolensis, and Rhinopithecus roxellana. Other temperate-dwelling primates rely mainly on buds and bark as winter fallback foods.

Group structure and physical characteristics of Simakobu monkeys (Simias concolor) on the Mentawai Island of Siberut, Indonesia.

We present data on group structure and physical characteristics from free-ranging Simias concolor. Mean group size (n = 3) was 8.7 +/- 1.1 individuals with an average adult male:female sex ratio of 1:3. All individuals were sexed and allocated into three categories (infants, juveniles plus subadults and adults) on the basis of their physical development. Within age categories, head-body lengths ranged from 19.6 to 25, 34 to 44 and 42 to 53 cm. Corresponding body weights ranged from 0.5 to 0.9, 2.35 to 4.4 and 5.2 to 7.85 kg, respectively; on average adult males were 13% larger and 23% heavier than adult females. Results indicate that for S. concolor living in undisturbed habitat (i) group sizes are larger than previously reported and (ii) polygyny is the most likely mating system. Both results support an earlier proposal that group size and social organization in Simakobu monkey are related to the degree of habitat disturbance.

Social organization of black-and-white snub-nosed monkeys (Rhinopithecus bieti) at Deqin, China.

Data on social organization of two bands of black-and-white snub-nosed monkeys (Rhinopithecus bieti) were collected when the monkeys were crossing an open spot at Nanren and Bamei (northwest of Yunnan, China) using a sampling rule where individuals within one social unit are spatially closer to each other than individuals between social units. The typical pattern of social organization in this sample was multiple adult females (AFs) and their offspring with one adult male (AM) in a one-male unit (OMU), similar to that of many other colobines. In such units, on average one male is associated with 4.0 AFs and 2.5 of their offspring. Moreover, there are multimale/multifemale units and monogamous units besides OMUs. All bisexual units traveled together with at least one all-male unit as a cohesive band. In two bands of monkeys, 87% of AMs in bisexual units were within OMUs, 7.8% within monogamous units and 5.2% within multimale, multifemale units. In the Bamei band, 6.7% of AMs were in the all-male unit. The size of OMUs in the Nanren band was larger than that of the Bamei band, with more AFs and juveniles, which may be related to better conservation in the Nanren band's habitat. For the Nanren band, the average number of AFs in OMUs varied across time, increasing from 4.3 in 1994 to 5.1 in 2001, and then decreasing to 3.8 in 2005. This article suggests three possible explanations for this variation, but more data are needed for these hypotheses to be tested.

Diet and activity budget of Rhinopithecus roxellana in the Qinling Mountains, China.

We collected data on diet and daytime activity budget, and investigated the phenology of food trees and food abundance for a group of Rhinopithecus roxellana on the East Ridge of Yuhuangmiao in the Qinling Mountains from November 2001 to December 2003. We calculated the seasonal activity budget using data collected by scan sampling from 84 full-day observations (winter 16, spring 18, summer 28, autumn 22 days). During scan sampling we recorded behavioral states, and the food items and species consumed. The subjects consumed 84 plant species, including trees and shrubs of 29 families, and lichens. Food species varied seasonally. The overall diet of R. roxellana consisted of 29.4% fruit/seeds, 29.0% lichens, 24.0% leaves, 11.1% bark, 4.2% buds, 1.3% twigs and 1.0% unidentified items. Because the abundance of different food items varied seasonally, the monkeys had to shift their major food items seasonally. The annual activity budget of R. roxellana was 36.2% time spent resting, 35.8% feeding, 22.9% moving, and 5.1% other behavior. Seasonal changes in activity budget were observed. R. roxellana spent more time moving in autumn, when the quality of the food might be highest, and least time moving in winter when the food quality might be lowest. Thus, this type of monkey has a passive foraging strategy.

Preliminary results from a field study of wild Guizhou snub-nosed monkeys (Rhinopithecus brelichi).

The Guizhou snub-nosed monkey, Rhinopithecus brelichi, is a large-bodied colobine confined to the subtropical semi-deciduous forests of Fanjing Mountain Reserve in Guizhou province, southwest China. Field work beginning in 1979 and including 10 months of intensive study in 1991 has revealed several aspects of the behavior and ecology of this species that are distinct from other colobines, including the closely related species R. roxellana and R. bieti. The Guizhou snub-nosed monkey is arboreal, traveling through the trees by quadrupedal walking, climbing, leaping, semibrachiation and (occasionally) by full brachiation. Terrestrial locomotion is use occasionally. Social organization centers around family groups of 5-10 individuals with a single adult male. Many family groups range and rest together in large, semicohesive bands. These bands may split up or coalesce temporarily to form large aggregations of over 400 animals and perhaps more. All-male groups of 2-5 adult or subadult males are found on the periphery of the bands.