Decision-making process during collective movement initiation in golden snub-nosed monkeys (Rhinopithecus roxellana).

Collective decision-making is important for coordination and synchronization of the activities among group-living animals and the mechanisms guiding such procedure involve a great variety of characteristics of behavior and motivation. This study provides some evidence investigating collective movement initiation in a multi-level social band of the golden snub-nosed monkeys (Rhinopithecus roxellana) located in the Mts. Qinling, China. We collect 1223 datum records relevant to decision initiation from six OMUs. The results indicate that collective movement initiation could be divided into two continual but relatively independent processes: decisions on moving direction and movement implementation. In both processes, adult individuals are more likely to initiate the decision-making, while other adults vote on initiator's preference, with a threshold, a supporting number required for a success. Thus, voting behavior and quorum fulfillment contribute to a successful decision-making. Adult individuals play important role in making decisions for moving direction and implementation. For a successful collective movement initiation, the individuals being more central in grooming network initiate decisions more frequently than the others, and attract voters more easily. Furthermore, following the initiation, at least four positive voters are required for a direction decision and at least three positive voters are needed for the decision on movement implementation, which could be considered as the threshold of quorum numbers required for a successful decision. This study has provided some very interesting information and scientific evidence in understanding social structure and behaviors of the nonhuman primates with a social structure very similar to humans'. Thus, some results can directly be referred to the comprehension of human social structure and behavior.

Female choice impacts residential male takeover in golden snub-nosed monkeys (Rhinopithecus roxellana).

In primate species with social systems consisting of one-male breeding units (OMUs), resident male takeover represents a major challenge to individual reproductive success and mating strategies. The golden snub-nosed monkey (Rhinopithecus roxellana) is characterized by large multilevel societies (MLS) comprised of several OMUs and all-male units (AMUs); however, the factors and mechanisms associated with resident male takeover, which offer important insight into primate reproduction and social strategies, are still poorly understood. Based on 5-year monitoring data from a free-ranging herd of golden monkeys from the Qinling Mountains in China, we categorized three phases of an OMU, that is, a rising phase, developing phase, and declining phase. The rising and declining phases were unstable periods in which male takeover in an OMU might occur. Factors causing takeover, such as leader male rank, fighting ability, reproduction rate, and affiliation (proximity, allogrooming), were analyzed for males and females and for different OMUs. Results indicated that the new resident male's fighting ability was lower than that of the former resident male in 23 cases. After replacement, the rank order of the new resident male significantly declined. Females involved in a takeover increased their distance from the resident male and decreased mating frequency during the three months prior to takeover. Females with infants under one-year-old had a marked effect on the specific time of takeover occurrence. These results suggested that female choice was the main factor deciding whether a takeover attempt was successful. Furthermore, rather than male conflict, females more often initiated and affected takeover and outcome, implying that the social status and competitive ability of the males played lesser roles during takeover.

Variation in gaze-following between two Asian colobine monkeys.

Gaze-following is a basic cognitive ability found in numerous primate and nonprimate species. However, little is known about this ability and its variation in colobine monkeys. We compared gaze-following of two Asian colobines-François' langurs (Trachypithecus francoisi) and golden snub-nosed monkeys (Rhinopithecus roxellana). Although both species live in small polygynous family units, units of the latter form multilevel societies with up to hundreds of individuals. François' langurs (N = 15) were less sensitive to the gaze of a human experimenter than were golden snub-nosed monkeys (N = 12). We then tested the two species using two classic inhibitory control tasks-the cylinder test and the A-not-B test. We found no difference between species in inhibitory control, which called into question the nonsocial explanation for François' langur's weaker sensitivity to human gaze. These findings are consistent with the social intelligence hypothesis, which predicted that golden snub-nosed monkeys would outperform François' langurs in gaze-following because of the greater size and complexity of their social groups. Furthermore, our results underscore the need for more comparative studies of cognition in colobines, which should provide valuable opportunities to test hypotheses of cognitive evolution.

Tending a dying adult in a wild multi-level primate society.

Responses of nonhuman species to dying and dead conspecifics range from hard-wired, fixed-action patterns - as in social insects - to varied, flexible behaviors with cognitive and emotional correlates - as in some larger-brained mammals [1,2]. Comparative thanatology addresses issues that include empathy, compassion, and conceptual understanding of death across species [1-3]. Several aspects of how great apes react to illness, injury and death of others recall human behavior in comparable situations [1-5]. However, the extent to which more distantly related primates share these responses is largely unknown. Here, we describe behaviors shown toward a dying adult female in wild Sichuan snub-nosed monkeys (Rhinopithecus roxellana) [6] and argue that empathy and compassion surrounding death extend beyond humans and their closest evolutionary relatives.

Female reproductive success in a species with an age-inversed hierarchy.

In most group-living mammals, reproductive success declines with increasing age and increases with increasing rank. Such effects have mainly been studied in matrilineal and in "age positive" hierarchies, which are stable and in which high ranking females often outperform low ranking ones. These relationships are less well-understood in age-inversed dominance hierarchies, in which a female's rank changes over time. We analyzed demographic data of 2 wild, unprovisioned groups of gray langurs (Semnopithecus schistaceus) near Ramnagar, Nepal covering periods of 5 years each. Female rank was unstable and age-inversed. We measured reproductive success via birth rates (57 births), infant survival (proportion of infants surviving to 2 years) and number of offspring surviving to 2 years of age (successful births) for 3 age and 3 rank classes. We found that old females performed significantly worse than expected (birth rate P = 0.04; successful births P = 0.03). The same was true for low ranking females (P = 0.04, and P < 0.01, respectively). Infant survival was highest for young and middle-aged as well as for high and middle ranking females. Overall, the results for these unstable hierarchies were rather similar to those for stable hierarchies of other mammals, particularly several nonhuman primates. Compared to a provisioned population of a closely related species, the wild and unprovisioned population examined (i) showed stronger age effects, while (ii) female reproductive success was equally affected by rank. Future comparative studies are needed to examine whether captive or provisioned populations deviate predictably from wild populations.

Postconflict Conciliation within One-Male Breeding Units in Sichuan Snub-Nosed Monkeys in the Qinling Mountains, China.

This study analyzed conflict and postconflict (PC) conciliation between males and females within one-male breeding units in Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains, China. The PC matched-control and time rule methods were used to collect and analyze data recorded from September 2013 to June 2014. The conciliatory tendency among individuals following conflict was 82.07%, and affiliation occurred within a few minutes after the conflict, which was not significantly different between mating and nonmating seasons. The PC conciliation scenarios were different from those reported from captivity. Lumbar hold and grooming were the most common expressions in reconciliation. In addition, bystander affiliation was uniquely found, which may be associated with the more terrestrial locomotion of R. roxellana, compared with other colobines.

Sickness behaviour associated with non-lethal infections in wild primates.

Non-lethal parasite infections are common in wildlife, but there is little information on their clinical consequences. Here, we pair infection data from a ubiquitous soil-transmitted helminth, the whipworm (genus Trichuris), with activity data from a habituated group of wild red colobus monkeys (Procolobus rufomitratus tephrosceles) in Kibale National Park, Uganda. We use mixed-effect models to examine the relationship between non-lethal parasitism and red colobus behaviour. Our results indicate that red colobus increased resting and decreased more energetically costly behaviours when shedding whipworm eggs in faeces. Temporal patterns of behaviour also changed, with individuals switching behaviour less frequently when whipworm-positive. Feeding frequency did not differ, but red colobus consumption of bark and two plant species from the genus Albizia, which are used locally in traditional medicines, significantly increased when animals were shedding whipworm eggs. These results suggest self-medicative plant use, although additional work is needed to verify this conclusion. Our results indicate sickness behaviours, which are considered an adaptive response by hosts during infection. Induction of sickness behaviour in turn suggests that these primates are clinically sensitive to non-lethal parasite infections.

Sleeping site selection by proboscis monkeys (Nasalis larvatus) in West Kalimantan, Indonesia.

Primates spend at least half their lives sleeping; hence, sleeping site selection can have important effects on behavior and fitness. As proboscis monkeys (Nasalis larvatus) often sleep along rivers and form bands (aggregations of one male groups) at their sleeping sites, understanding sleeping site selection may shed light on two unusual aspects of this species' socioecology: their close association with rivers and their multilevel social organization. We studied sleeping site selection by proboscis monkeys for twelve months at Sungai Tolak, West Kalimantan, Indonesia to test two main hypotheses regarding the drivers of sleeping site selection: reduction of molestation by mosquitoes and anti-predator behavior. We identified to genus and collected data on the physical structure (diameter at breast height, relative height, branch structure, and leaf coverage) of sleeping trees and available trees in three forest types. We used resource selection function models to test specific predictions derived from our two hypotheses. The monkeys preferred to sleep in large trees with few canopy connections located along rivers. The selection of large emergent trees was consistent with both of our main hypotheses: decreased molestation by mosquitoes and reduced potential entry routes for terrestrial predators. Although we are only beginning to understand how sleeping sites might influence behavior, grouping, and potential survival of this species, our study has shown that proboscis monkeys (at Sungai Tolak) have a very strong preference for large trees located near the river. As these trees are often the first to be logged by local villagers, this may exacerbate the problems of forest loss for these endangered monkeys.

[Spring food selection by Rhinopithecus bieti at Mt. Lasha in relation to phytochemical components].

Food selection by folivorous primates is thought to relate to macronutrients, micronutrients and plant secondary metabolites. However, few studies explain their effects on food choices. This study was designed to clarify the effect of phytochemical components on Rhinopithecus bieti food choice by analyzing the chemical composition of food samples collected from March to May in 2010 and 2011 at Mt. Lasha in northwest Yunnan, China. Compared with non-foods, there was more phosphorous and crude protein, less total sugar and a lower ratio of calcium to phosphorus in selected foods. However, no differences were found in crude fat, crude ash, calcium and tannin content between foods and non-foods. Phytochemical constituents may influence food choices; the monkeys preferred foods with high phosphorus and low Ca/P, low calcium, low sugar and low tannins. Rhinopithecus bieti foraged high quality foods such as buds and young leaves to meet their nutritional needs after a long winter. Therefore, if tannin content in food did not exceed the enduring threshold of R. bieti, the nutrient intake was prioritized by phosphorus and calcium regulation when the need for macronutrients dominated by protein was satisfied.

Personality as a predictor of general health in captive golden snub-nosed monkeys (Rhinopithecus roxellana).

Increasing studies in human and animals have shown that personality is related to biological profile and affects health outcomes. Understanding the link between personality and health will contribute to preventing illness and promoting well-being in non-human primates. The present study examined whether personality predicted health outcomes in captive golden snub-nosed monkeys (Rhinopithecus roxellana). Personality was measured by rating on a list of traits and four factors (Aggressiveness, Sociability, Mellowness, and Excitability) were extracted. Morbidity was measured by occurrence, duration, and number of illnesses, as well as (mean and maximum) digestive dysfunction symptoms scores. Morbidity measurements were coded from illness history which was recorded during the 27 months since the personality assessment. The results showed that lower Aggressiveness predicted greater number of illness, longer illness duration, and more serious digestive dysfunction. In addition, Mellowness, Excitability, and age by Sociability interaction influenced digestive function significantly. Low mellow individuals, high excitable individuals, high sociable younger individuals and low sociable older individuals had poorer digestive function. The present study demonstrated that personality was associated with morbidity in captive R. roxellanae and stress might contribute to this association. Personality assessment provided useful information on individual vulnerability. Carefully looking for early signs of illness among vulnerable individuals is expected to reduce health risks, which would promote welfare in captive non-human primates.

Daytime birth and parturition assistant behavior in wild black-and-white snub-nosed monkeys (Rhinopithecus bieti) Yunnan, China.

Few quantitative descriptions of parturition behavior have been reported in wild nonhuman primates because the majority of births occur at night. We have recorded a daytime birth event of a primiparous black-and-white snub-nosed monkey (Rhinopithecus bieti). The partum stage lasted 4 min 30 s, and the female skillfully severed the umbilical cord, ingested the placenta, and held and licked the newborn infant. During this period, the laboring female received delivery assistance from a multiparous female in same one-male unit (OMU) and female juveniles from same OMU showed great interesting during the partum. Our case study suggested that there might be considerable individual variation in birth-related behaviors.

Market powers predict reciprocal grooming in golden snub-nosed monkeys (Rhinopithecus roxellana).

Social grooming is a common form of affiliative behavior in primates. Biological market theory suggests that grooming can be traded either for grooming or other social commodities and services. When no other services are exchanged, grooming is predicted to be approximately reciprocated within a dyad. In contrast, the amount of reciprocal grooming should decrease as other offered services increase. We studied grooming patterns between polygamous male and female in golden snub-nosed monkeys (Rhinopithecus roxellana) from the Qinling Mountains of central China and found that about 29.7% of grooming bouts were reciprocated. However, the durations of grooming bouts offered and returned was asymmetrical within dyads. In bisexual dyads, more grooming was initiated by females than males, which became more pronounced as the number of females per one-male unit increased. The rate of copulation per day for each female was positively correlated with the total duration of grooming time females invested in males.. Females without an infant (non-mothers) directed more grooming towards females with an infant (mothers) and were significantly more likely to be non-reciprocated. There was a significant negative relationship between non-mother and mother grooming duration and the rate of infants per female in each one-male unit. High-ranking females also received more grooming from low-ranking females than vice versa. The rate of food-related aggressive interactions was per day for low-ranking females was negatively correlated with the duration of grooming that low-ranking females gave to high-ranking females. Our results showed that grooming reciprocation in R. roxellana was discrepancy. This investment-reciprocity rate could be explained by the exchange of other social services in lieu of grooming.

Demography of Simakobu (Simias concolor) and the impact of human disturbance.

Asian colobines typically live in small one-male groups (OMGs) averaging five adult females, but Simias concolor (simakobu or pig-tailed langur) is considered an exception because mostly adult male-female pairs have been reported. However, based on their phylogenetic position and marked sexual dimorphism, simakobu are also expected to form OMGs with multiple females. The preponderance of small groups could be the result of human disturbance (hunting or habitat disturbance) reducing group size in the recent past. To investigate this possibility, we documented the demography of ten wild simakobu groups from January 2007 until December 2008 at an undisturbed site, the Peleonan Forest, Siberut Island, Indonesia. We assessed the population-specific size and composition of groups and documented demographic changes due to births, disappearances, and dispersals throughout our 2-year study. We found OMGs with 3.0 adult females on average in addition to all-male groups, but no adult male-female pairs. The ratio of 0.5 infants per adult female (and 0.64 births per female-year in focal groups) suggested that birth rates were similar to those of other Asian colobines. In 5.1 group-years, we observed six dispersal events and six temporary presences (i.e., less than 3 months' residency). Both males and females dispersed, and juveniles seemed to disperse more frequently than adults. To assess the impact of human disturbance on simakobu demography, we compiled data for seven additional populations from the literature and compared them using multiple regressions. Adult sex ratio and the number of immatures per group were influenced negatively by hunting and positively by habitat disturbance while reproductive rates were not significantly affected by either variable. These findings suggest that adult male-female pairs may result from hunting pressure reducing group size, and that conservation action to reduce hunting in the Mentawai Islands is needed to ensure the survival of this critically endangered species.

Male dispersal in a provisioned multilevel group of Rhinopithecus roxellana in Shennongjia Nature Reserve, China.

Most Old World monkeys show male-biased dispersal. We present the first systematic data on male dispersal in a provisioned multilevel group of Rhinopithecus roxellana, based on 4.5 years of field observations in Shennongjia National Nature Reserve, China. We evaluated both ultimate (inbreeding avoidance and male mating competition) and proximate (food availability and predation risk) factors influencing male dispersal. The focal group contained 34-53 individuals, in 3-4 one-male units (OMUs) and 1 all-male unit (AMU). We observed 37 dispersal events involving 10 of 11 adults, 7 of 8 subadults, and 7 of 15 juveniles. Most interunit transfers within the focal group occurred around the months of mating season. Adult males competed for the leader positions of OMUs mainly through aggressive takeovers, and young males transferred from the OMUs to the AMU at the median age of 41 months, forced out by leader males. No young males older than 4 years remained in natal or non-natal OMUs. The male mating competition hypothesis was supported. The young males emigrated voluntarily from the focal group at the average age of 58.6 months, and no young emigrating male was observed to return, suggesting inbreeding avoidance also played a role in the dispersal of young males. Most emigration/immigration events were parallel dispersal and occurred during intergroup encounters, suggesting increased predation risk during the dispersal period. Males were more likely to emigrate/immigrate during the months when preferred foods were most available. We compared the dispersal patterns in R. roxellana with those in gelada baboons and hamadryas baboons, both living in multilevel societies. Similar to R. roxellana, young male geladas disperse at puberty, but they may return and breed in their natal groups. Males in hamadryas also disperse, but much less commonly than in R. roxellana. Provisioning may have influenced results, and confirming studies on unprovisioned groups would be valuable.

Ranging behavior of the François' langur (Trachypithecus francoisi) in limestone habitats of Nonggang, China.

Ranging behavior is an important aspect of animal behavior that researchers use to investigate ecological influences on individual behavior. We collected data on the ranging behavior of one group of François' langurs (Trachypithecus francoisi) between August 2003 and July 2004 in a limestone habitat within Nonggang Nature Reserve, China. We evaluated the influences of food availability, water resources and sleeping sites on ranging behavior. During the study period, the total home range size for the study group was 64.5 or (69.3 ha if the lacunae within the borders in which langurs were not observed were included), and the mean daily path length was 541 m. These are well within the range of variation reported in Trachypithecus species. The monthly range size was between 9.8 and 23.3 ha, and monthly range size correlated negatively with young leaf availability. The langurs tended to use a larger range size during young leaf-lean periods. The langurs did not use their home range uniformly, and 74% of their activities occurred within 35% of their home range. The most heavily used quadrats in the home range were located near the most frequently used sleeping sites, suggesting that sleeping sites have a significant influence on the ranging behavior of François' langurs in limestone habitats.

Social play behavior in infant Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in Qinling Mountains, China.

We describe the development of social play behavior and assess factors influencing the development of play in infant Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Infant snub-nosed monkeys began to exhibit social play at 3 months of age, when they spent an average 0.89% of time engaging in this behavior (range: 0.7-1.12%). At 6 months of age, there was a significant increase in the proportion of time spent in social play, averaging 9.78% of observation time (range: 4.92-17.08%). However, from 7 to 9 months of age during the winter, social play decreased gradually before rising again from 10 months of age in the spring. Play behavior in infant snub-nosed monkeys is influenced by environmental temperature. Males were observed to play more than females, although further data on this are required. Social rank did not influence the social play of wild Sichuan snub-nosed monkey infants.

Inter-unit contests within a provisioned troop of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains, China.

Numerical superiority does not always ensure victory in intergroup contests. Although group size is likely to determine the maximum resource holding potential (RHP) of a group, the realized RHP is the collective outcome of individual group members' choices about participation in any given contest. For any group member, the choice about participation should be based on the assessment of costs and benefits that are affected by both ecological and social factors. In this study, we studied inter-unit contests in a provisioned troop of Sichuan snub-nosed monkeys (Rhinopithecus roxellana). We spent 368 hr in contact with 9 one-male units sharing the same home range, during which we recorded 148 inter-unit contests at a provisioning site. Inter-unit contests always started as inter-individual contests. Contests escalated only when the two individuals were of different age-sex classes and one was an adult male. When a contest escalated, additional individuals were likely to get involved, and the outcome of the contest depended on unit members' choices about participation. The superiority in the number of participants rather than the superiority in unit size led to victory in inter-unit contests, given that the difference in unit size did not predict a difference in the number of participants. Unit members were more likely to support others in inter-unit contests in winter when food was sparse than in spring when food was abundant. In addition, unit members were more likely to support others in escalated contests than in those resulting in displacement, indicating that they tended to alter the outcome of a contest to gain immediate benefit. Although males initiated most inter-unit contests, a clear win-loss was most likely when females joined the fight. This sex difference may reflect the benefits to males vs. females of living in a multi-level society.

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.

Folivory or fruit/seed predation for Mesopithecus, an earliest colobine from the late Miocene of Eurasia?

Here we compare dental microwear textures from specimens of the fossil genus Mesopithecus (Cercopithecidae, Colobinae) from the late Miocene of Eastern Europe with dental microwear textures from four extant primate species with known dietary differences. Results indicate that the dental microwear textures of Mesopithecus differ from those of extant leaf eaters Alouatta palliata and Trachypithecus cristatus and instead resemble more closely those of the occasional hard-object feeders Cebus apella and Lophocebus albigena. Microwear texture data presented here in combination with results from previous analyses suggest that Mesopithecus was a widespread, opportunistic feeder that often consumed hard seeds. These data are consistent with the hypothesis that early colobines may have preferred hard seeds to leaves.

Social dynamics of the golden snub-nosed monkey (Rhinopithecus roxellana): female transfer and one-male unit succession.

Among primates that form multilevel societies, understanding factors and mechanisms associated with the movement of individuals between groups, clans, and one-male social units offers important insight into primate reproductive and social strategies. In this research we present data based on an 8-year field study of a multilevel troop of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains of China. Our study troop contained 78-126 individuals, and was usually organized into 6-8 one-male units (OMU). The majority of OMUs were composed of networks of unrelated females and their offspring. We found that 59.7% (43/72) of subadult and adult females in our study troop transferred between OMUs (n=66) or disappeared (n=7) from the troop. In the majority of cases, two or more females transferred together into new OMUs or troops. In R. roxellana, new OMUs formed in several ways. During 2001-2008, 16 adult males appeared in the study troop. Over this period, we observed 13 different males who became harem leaders either by taking over an existing harem or by attracting females from other OMUs into their harem. We also observed four OMUs from a neighboring troop to successfully immigrate into the study troop. The number of individuals in these newly immigrated OMUs was significantly smaller than that number of individuals in resident OMUs. During harem formation, fighting between adult males was rarely observed, and female mate choice appeared to play a crucial role in harem male recruitment and replacement. These results suggest that golden snub-nosed monkeys are organized in a nonmatrilineal social system. Female mate choice and possibly incest avoidance appear to play important roles in female transfer, male tenure, and OMU stability.