Sichuan Snub-nosed Monkeys Research Articles

Do deposed adult male Sichuan snub-nosed monkeys Rhinopithecus roxellana roam as solitary bachelors or continue to interact with former band members?

Do deposed adult male Sichuan snub-nosed monkeys Rhinopithecus roxellana roam as solitary bachelors or continue to interact with former band members?

The evidence of Coxsackievirus B3 induced myocarditis as the cause of death in a Sichuan snub‐nosed monkey (Rhinopithecus roxellana)

A 5-year-old female Sichuan snub-nosed monkey died at the zoological garden from infection with coxsackievirus B3. The diagnosis was made on the basis of pathologic features, immunohistochemistry, microbiological detection, and reverse transcription-polymerase chain reaction (RT-PCR). Histologic examination of formalin-fixed, paraffin-embedded tissues revealed a severe degree of predominantly lymphocytic infiltration of the cardiac muscle. Picornaviridae-like virions were found in the supernatants of cardiac muscle tissues homogenates, in the pericardial fluid, and in Vero cell cultures, by electron microscopy. Coxsackievirus B3 particles were detected in cardiac muscle cells by immunofluorescence. RT-PCR performed on an extract of cardiac muscle tissue revealed a DNA sequence specific for coxsackievirus B3. This is the first report of a Sichuan snub-nosed monkey dying from a virus.

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.

Prey capture and meat-eating by the wild colobus monkey Rhinopithecus bieti in Yunnan, China

AbstractIf it is true that extant primates evolved from an insectivorous ancestor, then primate entomophagy would be a primitive trait. Many taxa, however, have undergone a dietary shift from entomophagy to phytophagy, evolving a specialised gut and dentition and becoming exclusive herbivores. The exclusively herbivorous taxa are the Malagasy families Indriidae and Lepilemuridae, and the Old World Monkey subfamily Colobinae, and among these meat-eating has not been observed except as an anomaly, with the sole exception of the Hanuman langur (Semnopithecus entellus), which feeds on insects seasonally, and a single observation of a nestling bird predated by wild Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Here, we describe the regular capture of warm-blooded animals and the eating of meat by a colobine, the critically endangered Yunnan snub-nosed monkey (Rhinopithecus bieti). This monkey engages in scavenge hunting as a male-biased activity that may, in fact, be related to group structure and spatial spread. In this context, meat-eating can be regarded as an energy/nutrient maximization feeding strategy rather than as a consequence of any special characteristic of meat itself. The finding of meat-eating in forest-dwelling primates might provide new insights into the evolution of dietary habits in early humans.

Eurasian blackbird predated by wildRhinopithecus roxellanain the Qinling Mountains, China

Although there are some reports that have described primates eating animals, it is unknown whether predation on vertebrates exists in herbivorous leaf-eating primates. We have witnessed firsthand wild Sichuan snub-nosed monkeys (Rhinopithecus roxellana) preying on and consuming Eurasian blackbirds (Turdus meruld) in the Qinling Mountains of China. This event suggests that R. roxellana, which has previously been described as a herbivorous leaf-eating primate, may be partially carnivorous and the correct classification of this species would be omnivorous. Furthermore, food-share behavior among higher-ranked members occurs in a one-male unit when vertebrate prey is hunted by this species.

First evidence on foot preference during locomotion in Old World monkeys: a study of quadrupedal and bipedal actions in Sichuan snub-nosed monkeys (Rhinopithecus roxellana)

This is the first report of foot preference during locomotion in Old World monkeys. Foot preferences during the quadrupedal walking action and the bipedal shifting action of a naturalistic group of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in Zhouzhi National Nature Reserve in the Qinling Mountains of China were investigated. Twelve of 21 individuals tested on quadrupedal action and all 21 individuals tested on bipedal action exhibited a significant foot preference. Both significant right- and left-footed preferences were observed; sex affected neither direction nor strength of foot preference in both actions. The finding that 61.90% of focal R. roxellana showed a right-foot preference, both in quadrupedal action based on the footed index and in bipedal action based on the z-score, is in partial agreement with the postural origin hypothesis on footedness. Foot preference was significantly stronger in bipedal action than in quadrupedal action, supporting the view that posture could be a crucial factor influencing foot preference as well as hand preference in this species.

Response of a Group of Sichuan Snub‐Nosed Monkeys to Commercial Logging in the Qinling Mountains, China

Habitat destruction is one of the greatest threats to primates worldwide. To understand the impact of forest logging on the habitat use of primates in temperate mixed forest, we compared the range, habitat used, population size, and diet of a troop (ERT) of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains before (1989), during (1997), and after (2002-2003) commercial logging. Logging significantly changed the composition of the forest and the food supply for the troop. Some areas were heavily logged and formed patches in the forest that lacked canopy cover. The troop moved 7 km away from their original range when logging took place and returned to their original range after logging stopped, but they avoided heavily logged areas that lacked canopy cover. Their movement indicated some degree of site fidelity in this species. Diet and home range changed after logging, but the population size remained stable, which suggests that this species has some ability to adapt to habitat changes. Our results may reflect a natural flexibility in primates to adapt to the changing food resources in temperate areas with marked seasonal variations in food availability and distribution. This flexibility may have contributed to their higher degree of resilience to habitat alterations caused by human activities compared with tropical forest primates that have a more specialized diet. Our findings provide important baseline information that will help decision makers in their efforts to conserve primates, especially in temperate regions, and to sustainably manage primate habitat.

Mate competition and reproductive correlates of female dispersal in a polygynous primate species (Rhinopithecus roxellana)

Different mating systems in group-living animals have characteristic behavioral correlates that are primarily related to mate competition. Mate competition may push individuals to selectively make dispersal decisions for the purpose of maximizing of opportunities for reproduction. The Sichuan snub-nosed monkey (Rhinopithecus roxellana) is a polygynous primate species endemic to China. We provide the first data on female dispersal in a free-ranging group of R. roxellana in the Zhouzhi National Nature Reserve, Qinling Mountains, China. Both adult and subadult female dispersal occurred. Immigration/emigration rates of adult females are higher than those of subadult females. Mate competition is one apparent driving force behind adult female dispersal, and inbreeding avoidance is the possible proximate factor influencing subadult female dispersal. Adult female R. roxellana employ various reproductive strategies related to dispersal, which may increase their reproductive success.

Female social dynamics in a provisioned free‐ranging band of the Sichuan snub‐nosed monkey (Rhinopithecus roxellana) in the Qinling mountains, China

Little information is available on the social dynamics of the Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Here, we provide 5-year observational data on a provisioned free-ranging band in the Qinling Mountains, central China, from October 2001 to December 2005. The results of this study suggested that females place a high priority on maintaining long-term relationships with other female in their one-male units (OMUs). Females had more social interactions with unit members than with nonunit individuals. They showed relatively high rates of affiliation with their unit females, intermediate levels with the resident males, and low levels with individuals outside the unit. Females had few interactions with other resident males. Social interactions, especially affiliative interactions, were more symmetrical between focal females and their unit females than between focal females and the resident males. Thus female social interactions appeared to resemble those of other female-bonded primate societies. On the other hand, female transfers occurred sometimes. We recorded 11 cases of female immigration and 5 cases of female disappearance, 1 case of female intraband shift, and 2 cases of "merging of OMUs," which suggested that unit females might be loose-knit in this species. We discussed influencing factors on female Sichuan snub-nosed monkey social dynamics, by comparing them with those of Hamadryas and gelada baboons that also have multilevel societies.

Benefits to Female Helpers in Wild Rhinopithecus roxellana

To assess what female Sichuan snub-nosed monkeys (Rhinopithecus roxellana) gain from allowing others to care for their infants, we collected behavioral data on 12 mother-infant dyads at Zhouzhi National Nature Reserve in the Qinling Mountains, China. Mothers’ feeding time significantly increased when infants were cared for by other group members versus when they were cared for by the mothers themselves. The time mothers spent autogrooming and receiving grooming also increased when they were temporarily relieved of maternal duties; however, mothers did not groom other individuals more when they were not encumbered by infants. There are several benefits that mothers gain from having helpers care for their infants: They gain more time to feed and thus increase their feeding efficiency. Mothers have more time to engage in hygienic and maintenance activities because they autogroom and receive allogrooming more. Lastly, mothers save energy when their infants are with helpers. Wild Sichuan snub-nosed monkey mothers meet their basic survival and maintenance needs because of helping behavior.

Dominance relationships among one‐male units in a provisioned free‐ranging band of the Sichuan snub‐nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains, China

We studied the dominance relationships among one-male units (OMUs) in a provisioned free-ranging band of the Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains of central China from 2001 to 2005. The band was composed of 6-8 OMUs that stayed in the band for several years. Linear dominance orders could be detected using displacement interactions with directional asymmetry among OMUs in 82.3+/-5% of interactions, and ambiguous and reversed interactions in 17.7+/-5%. The dominance rank of OMUs was positively related with the duration of their stay in the band, and this may be attributed to the association of the resident male with adult females, rather than the fighting ability of resident males, as males do not fight seriously with each other. Subordinate units were observed to merge with dominant units resulting in an elevation of their rank order. The linear dominance relationship among OMUs in the Sichuan snub-nosed monkeys may have evolved as a result of competition for preferred food trees.

Hand preference during unimanual and bimanual reaching actions in Sichuan snub‐nosed monkeys (Rhinopithecus roxellana)

Hand preferences were investigated during one unimanual action (food-reaching) and one bimanual action (mount-reaching) in a semi-free-ranging group of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in Zhouzhi National Nature Reserve, Qinling Mountains of China. Nine of 14 individuals tested on the unimanual food-reaching action and all six individuals tested on the bimanual mount-reaching action exhibited a manual preference. Both significant right- and left-handed preferences were observed in the two actions. Sex did not affect either direction or strength of hand preference in the unimanual action. Hand preference for the bimanual action was stable over time, and the strength of hand preference was significantly stronger in the bimanual action than in the unimanual action.

First wild evidence of neonate nipple preference and maternal cradling laterality in Old World monkeys: A preliminary study from Rhinopithecus roxellana

Although captive or free-ranging settings offer a more controlled environment for assessing non-human primate laterality, research on wild populations provides evidence of how laterality is affected by natural environmental conditions and, thus may yield potential insights into the evolution of laterality. This study of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) constitutes the first report on asymmetric patterns of early mother-infant interactions among Old World monkeys in the wild. It was found that neonate nipple preference and maternal cradling laterality are both evident on the individual level. Although there is no significant group-level preference direction, the group preference strength on both measures is evident. Moreover, neonate nipple preference is not significantly correlated with maternal cradling laterality on either LBI scores or the direction (LBI scores: r=0.174, p=0.632; direction: r=0.624, p=0.054). Taken together, it is possible to suggest that wild R. roxellana show independent orientation laterality from the first week of life.

Impact of Male Takeover on Intra-Unit Sexual Interactions and Subsequent Interbirth Interval in Wild Rhinopithecus roxellana

Data were collected on sexual interactions before and after a male takeover of a one-male unit (OMU) of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains, China. The original unit consisted of an adult male, 2 adult and 2 subadult females, 2 female juveniles and a single infant. Following the takeover, the new resident male copulated with 1 adult female, which was not lactating. Subsequent to the disappearance of her infant, the second (lactating female) entered breeding condition and began to solicit copulation with the new resident male. The subadult females also engaged in matings with the new male. The new resident male was observed mating, on 3 occasions, with females in 2 other OMUs. These are the first observations of sexual behaviour in free-ranging Sichuan snub-nosed monkeys after an OMU takeover. Sexual interactions play an important role in establishing relationships between the new male and resident females in the OMU.

A preliminary study of food transfer in sichuan snub‐nosed monkeys (Rhinopithecus roxellana)

Food transfer happens regularly in a few nonhuman primates species that are also characterized by remarkable social tolerance. Sichuan snub-nosed monkeys (Rhinopithecus roxellana), or golden monkeys, which exhibit high social tolerance in their social relationships are thus of interest to see whether tolerance would extend to food transfer. In this study, branch feeding activity was observed in a semi-captive group of Sichuan snub-nosed monkeys, which consisted of 10 subjects that included a one-male unit (OMU) and an all-male unit (AMU). We recorded 1,275 food interactions over 27 days, and 892 instances of food transfer. The most commonly observed types of food transfer behavior were co-feeding (62.1%) and relaxed claim (22.8%). Of 892 food transfers, 756 (84.8%) took place in the OMU, most of which were among adults (34.7%) and among juveniles (42.1%). The transfer success rate was high in both the cases (87.9% for adults and 78.9% for juveniles). Food transfer in the AMU took place less often than that among adults in the OMU though with similar high transfer success. Food transfer between the OMU and AMU was limited to juvenile males from the OMU and adults from the AMU. These results provide the first evidence of food transfer in golden monkeys and suggest that tolerant social relationships in golden monkeys make transfer possible.

Population Structure and Ranging Patterns of Rhinopithecus roxellana in Zhouzhi National Nature Reserve, Shaanxi, China

We describe the population structure and ranging patterns of a troop of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) based on a study conducted between November 2002 and November 2003 in Zhouzhi National Nature Reserve, Shaanxi Province, China. The troop comprised several 1-male units and an all-male unit. Opportunistic censuses revealed that there were ≥112 individuals in the troop. The adult sex ratio (male vs. female) was 1:3.7. The ratios of adults to immatures and infants to adult females were 1:0.7 and 1:2, respectively. Via a grid system, we estimated the home range of the troop to be 18.3 km2, of which 7.4 km2 was the core area. The subjects exhibited distinct seasonal ranging patterns. Their movement across the home range was extensive in spring and restricted in autumn. In addition, reuse of quadrats was highest in winter and lowest in spring in comparison with other seasons. The daily path length (DPL) varied from .75 to 5 km, with a mean of 2.1 km. Seasonal analysis showed that DPL is significantly shorter in winter than in spring or summer; however, there is no significant difference between the DPLs of spring and summer or those of spring and autumn. The monkeys occupied elevations 1500–2600 m above sea level; the annual mean of altitudinal range is 2137 m. Contrary to early studies that reported Rhinopithecus roxellana migrates to lower elevations in winter, we found no evidence supporting a seasonal altitudinal shift. Using the highest troop count and home range estimate, and considering the extent of range overlap between neighboring troops, we calculated the population density and biomass of Rhinopithecus roxellana to be 7.2 individuals/km2 and 68.3 kg/km2, respectively. The temporal and spatial distribution of food resources may be the most important determinant of ranging behavior in Rhinopithecus roxellana, though understanding the relationship between resource distribution and seasonal range use may require further investigation.

Terrestriality and tree stratum use in a group of Sichuan snub-nosed monkeys

Morphological characters allow the Sichuan snub-nosed monkey (Rhinopithecus roxellana) to use multiple tree levels, but very few studies have quantified the terrestriality and tree stratum use of the species. I investigated the terrestriality and tree stratum use in a group of the monkeys from July 2003 to September 2004 (except February) in the Qianjiaping area of Shennongjia Nature Reserve, China. I collected data on the vertical position of individual monkeys in forest in relation to behavior types, diet, age/sex classes, vegetation types, tree height, and distribution of predators. The monkeys were much more arboreal than they were thought to be. They spent 97.1% of their time in trees (n=21,234 records) and 2.9% on the ground, and mainly used the middle (74.4%) and upper strata (17.4%). The monkeys displayed all behavioral types except searching in the middle and upper strata. The percentage of use of a stratum (except the low stratum) varied among months, and there was a difference in the percentage of use of a stratum among age/sex classes and between vegetation types. Approximately 94.2% of trees used by the monkeys were >6 m tall. They mainly fed on lichens, young leaves, mature leaves, flowers, fruits or seeds, and buds in the middle and upper strata, bark in the low and middle strata and herbs on the ground. Wolf (Canis lupus), leopard (Panthera pardus), and golden eagle (Aquila chrysaetos) are predators threatening the survival of individual monkeys in the study site. The results suggested that the seasonal vertical distribution of food items eaten in forest, predators, and vegetation types had important effects on the terrestriality and tree stratum use of the monkeys.

Copulation behavior within one-male groups of wild Rhinopithecus roxellana in the Qinling Mountains of China

This study was conducted using focal animal sampling on the west ridge group of the Sichuan snub-nosed monkey (Rhinopithecus roxellana) located in the Zhouzhi National Nature Reserve on the north slope of the Qinling Mountains, from 8 July 2003 to 24 May 2004. The difference in the average frequency of copulations for each focal male for each month was significant (F=3.068, P=0.016, one-way ANOVA test) with the majority of copulations occurring between September and November. Duration of intromission ranged from 2 to 39 s, with a mean of 16.0+/-0.4 s. Females initiated 627 courtship attempts (96.2%), while males only initiated 3.8%. Both adult females (72.8%) and sub-adult females (27.2%) were involved in sexual interference acts. Females who gave birth in 2004 performed more sexual interference acts than would be expected by chance in the reproductive period of 2003 (X2=13.73>X2(0.005,2), df=2, P<0.005). Male response to female interference was equally divided into "solicitor mounting" and "interrupter mounting". The resident males of one-male units were not observed to mount both the solicitor and the interrupter or mount neither following female solicitation interruptions. Three post-conception copulations were also observed in this study. These results suggest a skewed sexual competition, with multiple females competing for a single male, which was shown by courtship attempts and female interference.

Dominant relationships among one-male harems of Sichuan snub-nosed monkeys in the Qinling Mountains, China

Dominant relationships among one-male harems of Sichuan snub-nosed monkeys in the Qinling Mountains, China

Isolation and characterization of 11 microsatellite loci for the Sichuan snub-nosed monkey, Rhinopithecus roxellana

We report on the isolation and characterization of 11 microsatellite loci in the Sichuan snub-nosed monkey (Rhinopithecus roxellana) from AC-enriched genomic libraries. 20 microsatellite loci were screened from the libraries, of which 11 were polymorphic. The number of observed alleles among 32 samples of snub-nosed monkey ranged from three to nine. The observed and expected heterozygosity were 0.071–0.815 and 0.201–0.819, respectively. The high variability revealed in this study should be useful tools for further study on social structure and population genetics of snub-nosed monkey in the future.