Primates

, Volume 47, Issue 4, pp 374–382

Social organization of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains, Central China

Authors

    • Primate Research InstituteKyoto University
    • Northwest University
  • Kunio Watanabe
    • Primate Research InstituteKyoto University
  • Baoguo Li
    • Northwest University
  • Chia L. Tan
    • The Zoological Society of San Diego
Original Article

DOI: 10.1007/s10329-006-0178-8

Cite this article as:
Zhang, P., Watanabe, K., Li, B. et al. Primates (2006) 47: 374. doi:10.1007/s10329-006-0178-8

Abstract

Sichuan snub-nosed monkeys were observed for 197 days from 2000 to 2003 in the Qinling Mountains, Central China. The study group was provisioned in 2001 allowing detailed observations of social organization based on individual identification. The group was composed of 45–82 monkeys, all of which belonged to one of 6–8 one-male units (OMU) that foraged to form one big group. The average unit size was 9.0±2.3, 8±1.5 in the winter and 11.1±2.0 in the spring. Immigration or emigration of one-male units to or from the foraging group was observed, as was migration of individuals in and out of OMU, especially for by subadult females and juveniles. Group size therefore tended to fluctuate with the number of OMU and the number of young monkeys present in the group. The OMU in the study area were smaller than those in Shennongjia area. The factors influencing the size of these OMU and the entire group are discussed.

Keywords

Group compositionIndividual identificationMulti-tier social groupOne-male unitSichuan snub-nosed monkeys (Rhinopithecus roxellana)

Introduction

Of the three species of Chinese snub-nosed monkeys, Sichuan snub-nosed monkeys (Rhinopithecus roxellana roxellana) are the most widely distributed (Ren et al. 1998). These monkeys exclusively inhabit temperate forests in the mountainous highlands of central and southwestern China, at 1,500–3,400 m above sea level (Hu et al. 1980; Chen et al. 1989; Li et al. 2000). At least 39 groups, or about 3,800–4,000 individual Sichuan snub-nosed monkeys, are known to live in the Qinling Mountains, Central China (107°24’–108°27’E and 33°32’–33°57’N) (Hu et al. 1980; Chen et al. 1982; Li et al. 2000). Owing to its specialized digestive physiology, this species is able to consume buds, flowers, leaves, bark and lichen, all of which are widely available (Li et al. 2000), therefore potentially reducing feeding competition among individuals (Happel and Cheek 1986).

Unusual features shared by all species of Chinese snub-nosed monkeys are their strong sexual dimorphism and multi-tier social aggregations involving an extremely large number of individuals (Chen et al. 1989; Kirkpatrick 1998; Ren et al. 2000). It has been reported that one-male-units (OMUs) are the basic social unit within groups of Sichuan snub-nosed monkeys with many OMU forming one big group (Ren et al. 2000). Precise information on the organization of OMU and groups is, however, scarce because individual identification is difficult (Ren et al. 2000; Fukuda et al. 2002). These monkeys are not accustomed to human observation and therefore have to be studied from a distance of 50–200 m using high magnification spotting scopes (Chen et al. 1989; Ren et al. 2000). By observation from long distance, several authors described OMUs as small family units (Chen et al. 1989) or small reproductive units (Shi et al. 1982) while, alternatively, others argued that Sichuan snub-nosed monkeys form multi-male/multi-female groups (Hu et al. 1980; Liu 1989; Fukuda et al. 2002).

Seasonal fluctuations in the group size of Sichuan snub-nosed monkeys were reported (Hu et al. 1980; Shi et al. 1982; Schaller 1985; Kirkpatrick 1995). These seasonal changes are thought to be common, but the patterns of fluctuation have been shown to differ depending on the population. For example, the group size in Shennongjia was shown to increase in autumn while that in Choushuigou, Wolong, it increased in summer and decreased in winter (Hu et al. 1980; Schaller 1985; Kirkpatrick 1995). Moreover, in Baihe, group size and numbers of units changed, but not in relation to seasons (Shi et al. 1982). The factors influencing seasonal variation and roles of individual group members remain unknown, partly because no detailed observations of individuals have so far been conducted.

Since 1995, Sichuan snub-nosed monkeys, have been studied in the Qinling Mountains, Central China (Li et al. 2000), partly under semi-habituated conditions, and in 2001, one foraging group was successfully provisioned. Since then, it has become possible to observe this group from 0.5 to 20 m, and a number of adults and subadults have been identified. This paper reports more precise information on social organization based on individual identification by close up observation and seasonal changes in group composition.

Methods

Study area and study group

The study was carried out in an area surrounding Yuhuangmiao village in Zhouzhi National Nature Reserve, Shaanxi Province, China (Fig. 1, 33°48′N, 108°16′E) (Chen et al. 1989; Li et al. 2000). The reserve is located in the temperate zone on the northern slope of the Qinling Mountains and the study area ranged from 1,400 to 2,396 m above sea level. The average annual temperature during the study period was 6.4°C with a minimum of −8.3°C in January and maximum of 21.7°C in July. The vegetation varies with altitude from deciduous broadleaf forests at low elevations to mixed coniferous broadleaf forests above 2,200 m and coniferous forests above 2,600 m (Li et al. 2000).
https://static-content.springer.com/image/art%3A10.1007%2Fs10329-006-0178-8/MediaObjects/10329_2006_178_Fig1_HTML.gif
Fig. 1

Location of the study group of Sichuan snub-nosed monkeys (Rhinopithecus roxellana roxellana) (group number 20)

Two foraging groups of Sichuan snub-nosed monkeys live in the study area; separated by the Nancha River, they are known as the East Ridge Group and West Ridge Group. The study group (West Ridge Group) has a range of 9.2 km2 in winter and 14.1 km2 in spring, tending to migrate to lower elevations in winter (Li et al. 2000). They traveled 1,800–2,800 m in a day before being provisioned and preferred to forage in deciduous broadleaf forest (Chen et al. 1989; Li et al. 2000). When regular food items are scarce, they consume arboreal lichen, an uncommon food item for primates (Li et al. 2003). For more information on the study group, see Li et al. (2000, 2003), Ren et al. (2001), Zhang et al. (2003) and Qi et al. (2004).

Food provisioning

To achieve better observation, provisioning of the study group was commenced on 24 October 2001. Based on accessibility and the desire to avoid human disturbance, we set up a 15×30 m provisioning site at Sanchakou (1,646 m above sea level), Gongni valley (33°48′68″N, 108°16′18″E), in an area in which the group normally foraged. Provisions were first consumed by one juvenile on 12 November. Every morning at about 0900 hours, our assistants searched for the monkeys and led them to the provisioning site, at which point we began our observations. Food was provided daily at 0900, 1200 and 1400 hours in the form of about 3.5 kg corn grain and 20 kg sliced radish (about 200 g per monkey per day in total). After spring 2002, sliced apples were sometimes provided. Artificial factors such as leading monkeys to the provisioning site by assistants, especially in the early periods, might have influenced the monkeys’ behavior and social activities. However, they soon habituated to the provisioning site, therefore reducing outside influence. After successful habituation, the group could be observed daily. At night, the monkeys’ roosts were ordinarily located within a radius of 3 km of the provisioning site.

Age-sex classification

Individual identification of adult monkeys was completed in November 2001. Individual monkeys were identified by age/sex class, body size, pelage color, body disabilities, and other distinguishable individual features such as the shape of the granulomatous flanges on both sides of the upper lip.

Monkeys were categorized into seven age/sex classes as follows.

Adult males (estimated at more than 7 years old)

Adult males have outstandingly large bodies covered with extremely long, brilliantly golden guard hairs across the entire dorsum and, particularly, the cape area; the dorsum, crown to nape, cape, arms and outer thighs are all deep brown making them conspicuous among group members. A median brown crest with upright hairs, the shape of which is very useful for individual identification, is prominent. The granulomatous flanges are very obvious. Sometimes when their mouths are open, long canines are visible.

Adult females (estimated at more than 5 years old)

Adult females have smaller bodies, about half the size of adult males (Fleagle 1988). The dorsum, crown to nape, cape, arms and outer thighs are brown to deep brown in some older females. The entire dorsum and cape area is overlain with brilliantly golden guard hairs, but they are much shorter than those of adult males. Their median brown crest shows microbanding, which is also very useful for identification. Some individuals have visible granulomatous flanges, but they are much smaller than those of adult males. Their breasts and nipples are large and easily visible. Infants or newborns hanging beneath the abdomen are sometimes visible when the females are walking or climbing.

Subadult males (estimated at 5–7 years old)

Subadult males have a similar sized but more slender body than adult males. The golden guard hairs on the cape are shorter and sparser than those of adult males, and their granulomatous flanges while smaller than those of adult males are ordinarily larger than those of adult females. Their median brown crest shows microbanding.

Subadult females (estimated at 3–4 years old)

Subadult females are smaller than adult females (about two-thirds the size). Their body hair is brown, gradually turning golden, but they lack golden guard hairs. Their median brown crest shows microbanding. Their breasts and nipples are smaller than those of adult females.

Juveniles (estimated at 1–3 years old)

Their body size is small (less than two-thirds that of adult females). Their body hair is light brown, gradually turning reddish gold. The dorsum, crown to nape, cape, arms and outer thighs are brown. Neither golden guard hairs in the dorsum or cape area nor a median brown crest are recognizable. Sexual discrimination is difficult because of their underdeveloped external genital organs. They are usually observed actively playing.

Infants (estimated at 3 months to 1 year old)

Their hair is light brownish gray or light brown, appearing white in sunshine. They are sometimes observed playing with juveniles or other infants, but spend most of their time beside their mothers or sucking milk from adult females. The sex of individuals cannot be distinguished.

Newborn baby (estimated at less than 3 months old)

Their hair is a dark to light gray, turning light brownish gray after about 2 months. They rarely leave their mothers or the females carrying them. Their sex is indistinguishable.

Data collection

Observations were made for 197 days from March 2000 to January 2003 (Table 1). Observations were prolonged in winter and spring, when vegetations were less dense and monkeys ranged less. Movement of the foraging group in the forest was followed on a daily basis with the help of assistants. Initially, group composition was recorded and social interactions were observed from afar, usually 50–200 m or more, from opposite slopes. Group composition has been checked when they cross an area of open slope on 4 occasions from 17 March to 3 May 2000 and on 14 occasions from 19 February to 20 March 2001. After successful provisioning, observations were mostly conducted around the provisioning site. One group consistently visited the provisioning site and no other group or solitary males were around the group. The composition and members of each OMU and the entire foraging group were determined when monkeys took food at the provisioning site. In total, the group has been checked 71 times from 24 October 24 to 8 December 2001; 60 times from 10 January to 6 February 2002; 45 times from 6 March 6 to 12 April 2002; 64 times from 11 November to 4 January 2003 (Table 1). Individuals appearing at the provisioning site were monitored daily and changes in group composition were noted continuously. Monkeys moved with their units when they were foraging in the provisioning site. Individuals within a 2-m radius of adult males were noted (Table 2). Notable incidents such as fights between OMUs and copulation within and/or between OMUs were also recorded.
Table 1

The composition of the study group

Observation period

Adult males

Adult females

Sub-adult males

Sub-adult females

Juveniles

Infants

Total

Newborns

17 March – 3 May 2000

13(13±0.8)

28(28±0.8)

7(7±0.8)

18(17.8±1)

10(10±1.8)

6(6±0.8)

82(81.5±3)

13

19 February –20 March 2001

4(4±0)

9(8.9±0.3)

0(0±0)

0(0±0.3)

2(2.1±0.4)

3(3±0)

18(18±0.5)

0

24 October –8 December 2001

8(7.9±0.1)

26(25.8±0.6)

0(0±0)

8(8.0±0.5)

13(13.1±2.7)

8(7.9±0.5)

63(62.7±3.1)

0

10 January –6 February 2002

6(5.9±0.1)

18 (18.2±0.4)

0(0±0)

6(5.9±0.5)

10(9.9±2.6)

5(5±0)

45(44.7±1.8)

0

6 March – 12 April 2002

8(7.8±1.4)

26 (25.9±1.5)

0(0±0)

12(12.3±1.8)

21(21.3±2)

0(0±0)

67(67.3±3.9)

15

11 November 2002 – 4 January 2003

8 (8±0)

28(27.9±0.4)

0(0±0)

6(6±1.4)

15(14.8±2)

8(8.1±0.5)

65(64.8±2.3)

0

The values ± SDs given in parenthesis were likely caused by miscounts

Table 2

Spatial association between adult males and females at feeding time

Females

Males

HT (167)

HD (102)

CM (167)

JZT (139)

DZ (83)

TT (105)

ZZ (116)

BZT (81)

XiaoKeng

0.84

0.02

0.07

0.04

0.1

0.03

0.04

0.04

YuanLian

0.75

0.09

0.05

0.01

0.13

0

0.04

0

BaiBei

0.01

0.75

0.03

0.06

0.06

0.04

0.01

0

FaQia

0.02

0.64

0.05

0.08

0.02

0.02

0.03

0.04

AoXian

0.04

0.56

0.05

0.1

0

0

0.03

0.1

BaiTouNvXia

0.04

0.5

0.08

0.06

0.04

0.02

0.01

0.05

BaiXian

0.08

0.12

0.72

0.04

0.02

0.05

0.04

0

HeiWei

0.06

0.05

0.71

0.06

0.04

0.01

0.03

0

TieMao

0.05

0.08

0.63

0.04

0.06

0.03

0.07

0.05

DuanWeiHou

0.05

0.02

0.02

0.77

0.11

0

0

0.08

KuanBanHou

0.07

0.04

0.04

0.76

0.07

0

0

0.02

ZaiBanHou

0.15

0.02

0

0.71

0.07

0.04

0.03

0.07

HongXinMeia

0.1

0.05

0

0.61

0.1

0.01

0.03

0.11

ZaMao

0.02

0.08

0.03

0.09

0.63

0.04

0.05

0.05

GuoGaiTou

0.04

0.08

0.04

0.08

0.58

0.03

0.03

0.01

HuaXin

0.07

0.13

0

0.03

0.52

0.01

0.06

0.02

HeiDian

0.08

0.06

0.08

0.07

0.33

0.07

0.08

0.01

ShuangHang

0

0.03

0.01

0.04

0.05

0.71

0.07

0.06

HeiXian

0

0.03

0.05

0.02

0.05

0.65

0.09

0.1

BanHeiXian

0.07

0.08

0

0.04

0.04

0.65

0.06

0.7

PianFen

0.05

0.05

0.03

0.06

0.08

0.49

0.12

0.12

CiTuTou

0

0

0

0.02

0

0.01

0.72

0.05

BaiXuan

0

0.04

0

0.05

0.04

0.03

0.54

0.02

BeiTou

0

0.06

0.08

0.06

0

0.01

0.04

0.52

XiangChang

0.01

0.02

0.04

0.04

0.04

0.03

0.03

0.43

ZaMaora

0

0.03

0.1

0.08

0.02

0.02

0.03

0.39

The number of scans for each adult male is shown in parenthesis; a total of 183 scans were made at the provisioning site. Values indicate the frequency with which each adult female was observed within 2 m of each subject adult male in winter 2001. Based on spatial approximation in provisioning sites, underlined values show statistically significant associations (P<0.05) between particular females and males during the study period. HT, z=−2.3, P<0.05; HD z=−3.1, P<0.01; CM, z=−2.8, P<0.01; JZT, z=−3.2, P<0.01; DZ, z=−3.1, P<0.01; TT, z=−3.2, P<0.01; ZZ, z=−2.3, P<0.05; BZT, z=−2.5, P<0.05

aThe two females emigrated from the group on 9 and 23 March 2002 respectively

Social interactions between individuals were recorded continuously, overall 445, 30-min sessions of focal animals were collected (Altmann 1974). Focal animals were randomly selected daily from all age/sex classes, except newborns. During each focal sampling session, all social behaviors were recorded and individuals within 2 m of the focal animals were noted once every 10 min. If grooming occurred, the age/sex class of the participants, body parts groomed, distance to the nearest animals, and spatial distribution were noted.

The U-test and Chi-square tests were used to determine significant behavioral differences among associated and unassociated animals.

Results

Changes in group size

The composition of the study group was first recorded from March to May in 2000. Overall, 82 (81.5±3.0) monkeys including 13 (13±0.8) adult males and 28 (28±0.8) adult females were counted. In addition, 13 newborns had been born by the end of the observation period (Table 1). In February and March 2001, the group broke up into several small groups with one composed of 18 monkeys foraging the area around Sanchakou valley. This small group, that was recognized by the adult male “DZ” and the adult female “Duan WeiHou” maintained close association and its membership was stable during the 1-month study period. The other groups (at least two) scattered to remote areas within the range of the original study group. In September 2001, when we revisited the area and commenced provisioning in October, we found a large group composed of more than 60 individuals. The adult male “DZ” and adult female “Duan WeiHou” were observed in the group, and this group ranged in the same area as former study groups. From October to December 2001, individual identification of all adult monkeys was established, allowing more precise observations and the tracking of further group changes. The study group was composed of 63 animals, including 8 adult males and 26 adult females. This composition was fairly stable and did not fluctuate during the study period (Table 1).

Group size changed primarily based on the numbers of adult males and females. By January 2002, the group size had decreased to 45 monkeys, including only 6 adult males and 18 adult females. By March 2002, 2 adult males and 8 adult females had joined the group, which consequently increased in size to 67 monkeys. Fifteen newborns were born by end of the observation period and two subadult females were counted as adult females after giving birth. By November 2002, the group size had decreased to 65, but the composition of adult males and adult females remained stable.

Newborn babies were only observed from March to May, indicating the birth season of this species in the study area. In the birth season of 2000, prior to provisioning, the birth ratio (number of newborns : adult females) reached 46%; in 2002, the birth ratio was 58%. It is therefore possible that about half the adult females gave birth in a year during this period. The number of newborn babies in 2002 decreased significantly by the end of the year after 6 months of the birth season, and mortality (disappearance or death of newborns) within 6 months after the birth season reached 50%. The number of infants tended to decrease until reaching 1 year of age (Table 1).

Another characteristic influencing group size is fluctuating numbers of juveniles and subadult females. From December 2001 to March 2002, the number of subadult females increased 50% and that of juveniles increased 62%. From April 2002 to January 2003, however, the number of subadult females and juveniles decreased 50% respectively. The number of subadult females and juveniles, therefore, tended to increase in spring (March–May) and decreased in winter (December–February) (see later sections).

One-male units

When monkeys appeared at the provisioning site, it was clearly recognizable that all group members were closely associated with one specific adult male. By observing the association patterns between adult males and females in focal sessions, the members of each OMU were clearly discernible (Table 2). The adult male HT was always near to two adult females, Xiao Keng and Yuan Lian, both of who remained in very close proximity to him throughout the day. All other males also had close associations with adult females and each association pattern was always fixed. All adult members clearly belonged to one specific OMU and no transitional individuals were observed (Table 2).

The membership of each OMU was stable (Table 3). In November 2001, eight OMUs were recognized in the study group; namely, HT, HD, CM, TT, JZT, DZ, ZZ, and BZT. In general, one OMU included only 1 adult male with 2–5 (3.3±0.9) adult females, 0–2 (1.1±0.6) subadult females, 1–4 (2.0±0.9) juveniles and 0–2 (1.0±0.8) infants and newborn babies. The size of the OMUs ranged from 5 to 14 individuals (average: 9.0±2.3) with 8±1.5 in the winter and 11.1±2.0 in the spring (Table 3). Animals in the same unit were tolerant of each other and always maintained close associations. When adult members of a different OMU approached within 2 m, aggressive behaviors (threats, chasing, and so on) and avoidance were usually observed. If agonistic encounters between OMUs occurred, members of the same OMU supported each other. In 438 cases of 500 inter-unit encounters recorded at the provisioning site, focal animals aggressed or counter-aggressed together toward opponent units in cooperating with their unit members. While in 62 cases, focal animals aggressed toward members of their units. It was usually done by adult males toward his unit members in order to mediate aggressions between units, such as threat with lips smack, mounting adult females of their units, drag and holding.
Table 3

Composition of one-male-units (OMUs) in the study group

https://static-content.springer.com/image/art%3A10.1007%2Fs10329-006-0178-8/MediaObjects/10329_2006_178_Tab3_HTML.gif

Note The total numbers of adult males, adult females, and newborn babies are shown by M, F and B, respectively, and the size of the OMU is shown by S. + indicates increased numbers of newborn babies or adults. − indicates adults who have disappeared

aThe resident male, Hong Dian, of the HD unit was replaced by a previously solitary male, Dao Ba, in August 2002

Males mounted females in the same unit (192 times) significantly more often than they mounted females in other units (16 times) (n=208, X2=1089.6, P<0.01). Inter-unit copulation occurred when the adult female was located far away from the adult male of her relevant OMU. Grooming was also conducted mostly between members of the same unit, with grooming between different unit members being very rare, excluding that between young monkeys. During individually identified grooming sessions, a total of 2,411 allogrooming bouts was recorded and of these, inter-unit grooming between adults was infrequent (14 male-female and 69 female-female grooming instances; 83 in total, 7.6%), compared with intra-unit grooming (1,099 instances, 92.4%).

In the course of their daily activities, females kept closer contact with each other than to adult males and juveniles in the OMU. Approximating and affinitive interactions such as grooming were frequently observed between adult females. In addition, adult females, together with other females, sometimes chased off the adult male of their unit. Males often stayed solitary, far from the other unit members who tended to rest together in a tree.

Sometimes, juveniles and infants of different units intermingled with each other while playing or grooming. This was especially true when unit members approached the provisioning site, leaving juveniles of different OMUs waiting on nearby trees. Ordinarily, juveniles approached the provisioning site with their units but did not stay for long periods of time. Juveniles therefore seemed to move more freely, interacting more frequently with other unit members. Nevertheless, they kept a close association with their own unit members when at rest and while traveling and they were frequently observed rest close to adult males of their units.

OMU emigration and immigration

From October to December 2001, the study group was composed of eight OMUs (Table 3). However, in January 2002, after a 1-month interruption of observation, only six of these OMUs appeared at the provisioning site; the HD and DZ units never appeared near the provisioning site during this 1-month observation period. In March 2002, after another 1-month interruption of observation, these two units once again appeared at the provisioning site, joining the rest of the group, and all eight OMUs continued to appear until April 2002. In November 2002, when we revisited the site, one unit, ZZ, did not appear while one new unit, HTU, was seen (Table 3). There were no noticeable behavioral differences toward the newly joined OMU, compared to those previously observed. All OMUs composing the group during each observation period were stable from day to day. In other words, a recombination of OMUs occurred when we left the field or stopped provisioning.

The number of females in the group prior to provisioning, in March 2000, was almost the same as that in October 2001, after provisioning eight OMUs were confirmed (Table 1). Combination of OMUs might not be apparently influenced by provisioning, although composition of additional males and subadult males varied by provisioning. It is likely that more adult and subadult males foraged with the group in 2000 and March 2001 prior to provisioning. The group composition in February 2001 also implied the presence of two additional adult males in relation to the number of adult females being equivalent to those of two units. Two adult males in the group seemed always foraged a distance away from the females, whereas additional males and subadult males were not observed in the group around the provisioning site.

Immigration of one adult female into the JZT unit was observed on March 23, 2002. This adult female appeared with the JZT unit, showing no special attention to the other OMU members. Similarly, other members of this unit showed no specific responses, such as aggression or avoidance, to the additional female. Two females, Hong XinMei and Za Maor, disappeared from the group on March 9 and 23, 2002, respectively, for no obvious reasons (Table 2). On 10 August 2002, when we conducted another study on the group around the provisioning site, the adult male, HD, was supplanted by a solitary male, DB, who was not in the group before. This was the only case of a solitary male appearing in the group. DB followed HD unit and fight with HD male many times. One week later, females in HD unit tended to associate with DB and, consequently, HD was replaced by the solitary male. HD left the group soon after he was defeated.

There are indications that subadult females and juveniles moved between groups more frequently than other group members. Four subadult females joined the HD, CM, DZ and BZT units during the period of December 2001–March 2002, while four subadult females also disappeared from these units between April and November 2002. A further five juveniles joined the HD, CM, JZT and BZT units during the period of January to March 2002, while six juveniles disappeared from the HD, CM, TT, JZT and DZ units between April and November 2002. Subadult females and juveniles therefore joined new units in spring, disappearing before winter. It was difficult to confirm whether the same individuals repeatedly moved between units or not. Temporarily associated adolescents were, however, observed, influencing the overall size of the study group.

Discussion

It has been reported that Chinese snub-nosed monkeys form multi-tier societies consisting of several OMUs that include one adult male plus a number of adult females and their offspring (Chen et al. 1989; Ren et al. 2000). However, large foraging groups might lead observers to conclude multi-male and multi-female society of this species (Fukuda et al. 2002). Our observations confirmed the suggestion of OMUs in a wild population of Sichuan snub-nosed monkeys. Females of this species formed several close associations, which consistently approximated to the specific adult males. Copulations occurred mostly within the OMUs. Members of the OMUs in the study group remained stable for several months, or even years, and the combination of OMUs within the group was fairly stable throughout the study periods, though some left and/or joined. Unit members, both males and females, supported each other for the conflicts against other units in the provisioning site or around it. During 13 months of observation, only one adult male was ousted by an outside male, suggesting that their tenure within an OMU covers a fairly long period. Furthermore, most females seemed to stay in the same OMU, while immature males seemed to leave their natal OMUs at an early age since no subadult males were confirmed in any unit. These results therefore suggest that OMUs are the fundamental social unit for Sichuan snub-nosed monkeys.

The size of the group fluctuates primarily with the number of OMUs foraging together. It is also possible that provisioning influenced the number of OMU appearing at the provisioning site, since changes to OMUs were always accompanied with breaks in provisioning. The observations of group splitting before provisioning indicate that temporal splitting of the group might also occur in natural circumstances. When provisioning was recommenced in Yuhuangmiao area, assistants entered the forest and led the monkeys back to the provisioning site. Monkeys (or OMUs) foraging together at this time were therefore introduced to the provisioning site. During provisioning, these OMUs might be led to the site every day while other OMUs/monkeys within the range of the group but not grouped together might not approach the provisioning site. Foraging groups in Shennongjia area seems also composed by several OMUs. Group size in the same area varied widely (from 95 to 335) during different observing periods; large groups ordinarily included more OMUs than small groups (Ren et al. 2000)

Other factors influencing group size are numbers of males and young monkeys. Before provisioning, it is very likely that there were additional adult males in the group. These additional males might have left the group when the group appeared at the provisioning site and, even if they did visit the provisioning site, they might not have obtained any food since competition was likely severe between OMUs (Zhang et al. 2003). Further, the number of subadult females and juveniles also fluctuated seasonally. Many subadult females and/or juveniles disappeared from the group in winter and immigrated in spring. The factors influencing this dispersal and fusion remain unknown. However, these findings suggest these monkeys can survive independently from their natal groups. A similar pattern of dispersal and fusion has been observed in groups of monkeys in Shennongjia (Ren et al. 2000). In Shennongjia, it was suggested that juveniles who leave the group might join all-male groups. In our study, all-male groups were observed, but information on them remains very scarce.

The size of OMUs in the study group was smaller than that observed in Shennongjia (mean 19; range 7 to 52 adults in one unit) (Ren et al. 2000). However, in Shennongjia, the population density was five times higher than that at the present study site (Chen et al. 1989; Ren et al. 2000). Feeding competition among OMUs in the Qinling Mountains may therefore be weaker than that in Shennongjia. Moreover, the habitat of Shennongjia monkeys is temperate evergreen forests, which may supply higher-quality foods scattered in smaller patches (Li 2001). The Sichuan snub-nosed monkeys in the Qinling Mountains live in forest where lower-quality foods are distributed evenly (Li et al. 2000). Less competition for foods might therefore have resulted in the smaller size of OMUs in the Qinling Mountains group.

Fission and fusion have been already reported for two species of Chinese snub-nosed monkeys, Rinopithecus roxellana and R. brelichi (Hu et al. 1980; Shi et al. 1982; Schaller 1985; Kirkpatrick 1995), but patterns of seasonal fluctuation in group size differ between populations, and depending on the season and time scale (Kirkpatrick 1998). Our observations indicate that independent OMUs could be the basic unit of social organization for these monkeys. The number of adult males with their own units also contributes to fluctuating group size, as do numbers of subadult and juvenile monkeys. In addition, all-male groups might join the group during the mating season, also resulting in seasonal fluctuations (Ren et al. 2000). However, our sporadic observations indicated no aggregation of adult males or subadult males during the mating season (August–October).

The sizes of foraging groups in the Qinling Mountains seem smaller than those in Shennongjia (Hu et al. 1980; Chen et al. 1989; Kirkpatrick 1995; Ren et al. 2000; Zhang et al. 2003). Compared with the OMUs in the Qinling Mountains, there are more females (7±4) in the OMUs of the Shennongjia group, suggesting that more males are excluded from the breeding units. The appearance of additional males and subadult males around OMUs seems to be more frequent in Shennongjia than in the Qinling Mountains (Ren et al. 2000). We therefore suggest that the lower frequency of potential harassment by non-breeding males in the Qinling Mountains might have caused the OMUs to aggregate less cohesively than in Shennongjia.

Aggregation of OMUs might also be influenced by ecological factors, and feeding competition is probably not the main factor for large foraging groups of this species. The size of the study group tended to be smaller in winter than spring when food is distributed in smaller patches (Li 2001). This tendency was also observed with the Choushuigou group in Wolong (Hu et al. 1980; Schaller 1985). Inter-group encounters by the study group are rarely observed, and even when they did occur, individuals usually tended to avoid contest and leave separately, or join one another (Chen et al. 1989; Ren et al. 2000). Potential predators, such as panthers (Panthera pardus), jackals (Cuon alpinus), lynxes (Lynx lynx), wolves (Canis lupus), and goshawks (Accipiter gentilis), might be one factor affecting aggregation (Hu et al. 1980; Shi et al. 1982; Zhang et al. 1999). Group sizes in Shennongjia where more potential predators are found are ordinarily larger than those in the Qinling Mountains (Kirkpatrick et al. 1998). Moreover, adults of the study group frequently coming to the ground to travel, forage or rest, may indicate a reduced predator pressure in Qinling Mountains (Ren et al. 2001).

Acknowledgements

We thank Dr. K. Wada for indispensable support during this research project. Thanks are also due to Dr. J.A. Phillips for critical reading of the manuscript. The authors are very grateful to Zhouzhi Nature Reserve and, in particular, Mr. P.J. He (Director of Zhouzhi Nature Reserve) for giving us permission to carry out our research. We also thank Drs. S.T. Guo and X.G. Qi (Northwest University) as well as local assistants for assistance in the field. This study was supported by the National Natural Science Foundation of China (30370202), The Zoological Society of San Diego, USA, the Nippon Life Insurance Foundation, Japan, and the Daiko Foundation, Japan.

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© Japan Monkey Centre and Springer-Verlag 2006