Introduction

Species in different parts of their geographic range may evolve different adaptations to environmental variations, and are likely to vary in behavior1. Due to natural processes and human interference, some wide-ranging species have been confined into isolated habitats with different ecological conditions2.

Snub-nosed monkeys (Rhinopithecus spp.) are an endangered Asian colobine that lives in temperate forests of mountainous highlands. This genus contains 5 species. Of these, the golden snub-nosed monkey (Rhinopithecus roxellana), with the northernmost habitat of all colobines3, was once widely distributed in China2. Unfortunately, most of their populations have vanished under the influence of increased human activities during past thousand years2,4,5. Deteriorating environments and accelerated deforestation restricted this species to fragmented and limited areas under the effect of geographic isolation2,6,7,8,9, which led to differentiation into three subspecies: Rhinopithecus roxellana roxellana (in Minshan mountains of Sichuan and Gansu province), R. r. qinlingensis (in Qinling mountains of Shaanxi province) and R. r. hubeiensis (in Shennongjia mountains of Hubei province)10,11.

These isolated habitats exhibit different environmental conditions. For instance, the habitat of R. r. qinlingensis is a mostly deciduous broadleaf forest area in Qinling, Shaanxi8, while R. r. hubeiensis in Shennongjia, Hubei lives in a mixed coniferous broadleaf forest area12. The R. r. roxellana population in Sichuan is distributed in areas with deciduous and evergreen broadleaf forest11. The differentiation of these three subspecies provides an example and offers insights to explore the adaptive mechanism of intraspecies evolutionary radiation.

Previous studies mainly focused on the first two subspecies, R. r. qinlingensis and R. r. hubeiensis. Studies revealed behavioral differentiation between those two subspecies, such as foraging preference divergence4,13,14,15. However, due to the precipitous mountain habitat, little knowledge is available on the nominate subspecies (R. r. roxellana) in Sichuan, even though the first specimen of this species was discovered there and named in 1870 A.D.11. These monkeys are shy of humans and move rapidly across steep cliffs and deep gorges, which make them difficult to follow and study. Owe to this lack of the basic information, how golden snub-nosed monkeys shaped to varied environments still remains unclear.

We conducted a two-year study based on field observation of R. r. roxellana in Laohegou National Nature Reserve in Sichuan province and report here the information for this subspecies. Based on the behavior observation, we conducted a study on the diet, activity budget and social organization of R. r. roxellana. With the assistance of remote sensing and global positioning system (GPS) technology, we confirmed the home range of golden snub-nosed monkeys in Laohegou, Sichuan. Here, we present the first detailed data on R. r. roxellana from the wild. Our results would provide evidence to further explore intraspecific adaptations in varied habitats in primates.

Materials and Methods

Study area

We carried out this study in Laohegou (LHG) Nature Reserve in Minshan Mountains (104°32′ −104°45′ E, 32°25′ −32°36′ N), **wu county, Mianyang city, Sichuan province, China. Based on data of China Meteorological Administration (Website: http://www.cma.gov.cn, in Chinese), climate in this area (1,100–3,100 m asl.) has a subtropical monsoon climate with a cold and dry winter and cool and moist summer. Annual average temperature is 14.7 °C (ranged from −7–37 °C). The relative humidity ranges between 60–80%, and annual average sunshine duration ranges between 867.2–1289.4 hours. The study area has a high frequency of rainy days especially in spring, but the amount of daily rainfall is small (annual precipitation: 760.4 mm–1230.5 mm). In this study, we defined seasons as follows16: spring (Mar. 6–Jun. 1), summer (Jun. 2–Aug. 27), autumn (Aug. 28–Nov. 22), and winter (Nov. 23–Mar. 5).

Study animals

The basic composition of golden snub-nosed monkey society is one male multi-female plus offspring (OMU)3. OMUs do not avoid each other, but move, forage and rest together to form a breeding band17. Young male normally emigrate from their natal groups before sexual maturity, and form all male units, several of which coalesce into an all male band (AMB)18,19. All male band follows around the breeding band, all together comprising a herd18. These different social levels represent socially and spatially distinct components of the multilevel society18,20.

According to previous survey and field research, the staff of the Laohegou Nature Reserve identified 4 herds of monkeys during their daily patrols, each herd has a relatively independent home range (government report: Improvement of golden snub-nosed monkey at Laohegou, in Chinese), including herd A (distributed in Da-pian-gou and ** site to the feeding site.

Figure 3
figure 3

Variation in the activity budget among age-sex classes of R. r. roxellana in Laohegou, Sichuan province.

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Home range

In LHG, the golden snub-nosed monkey mainly lived in the broadleaf forest. The average elevation of their distribution area was 1853m (90.0% of the habitat was between 1400–2200 m, with 6.8% between 2200–3100 m and 3.2% between 1100–1400 m). Based on the results of Kernel Density Estimation Method22, the home range size of herd A, B, and D was 49.1 km2 (Fig. 1). Home range of herd B was 12.3 km2, and population density was 10.6 individuals/km2, with total of 130 individuals.

Social organization

The herd B contained breeding band (BB) and all-male band (AMB). The BB was composed of 12 one male units (OMUs), with a 1:4.2 mature sex ratio (M/F) (Table 4). The size of the OMUs ranged from 3 to 14 individuals (mean = 8.3 ± 3.5), with 2.7 ± 1.3 adult females, 1.5 ± 1.2 sub-adult females, 2.6 ± 1.4 juveniles and 0.5 ± 0.5 infants (Table 5). There were 31 males in the AMB, including 6 adult males, 10 sub-adult males, and 15 juveniles. At the same time, we found that a solitary monkey existed in some area.

Table 4 Social composition of R. r. roxellana in herd B, Laohegou Nature Reserve, Sichuan (spring).
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Table 5 Comparison of unit composition in Shaanxi, Hubei and Sichuan (spring).
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Discussion

Our result suggested leaves were the largest dietary component for R. r. roxellana in spring. Golden snub-nosed monkeys in Sichuan would spend more time on feeding and resting, instead of moving. The home range is 49.1 km2, while the unit size of R. r. roxellana is relatively smaller (8.3 ± 3.5 individuals, ranged from 3 to 14). Our result might provide basic and valuable information to compare between subspecies under different ecological factors.

Dietary composition makes a regional difference within species in our study. In spring, leaves (Sorbus zahlbruckneri Schneid, IIex polyneura, et al.) were the largest dietary component for the populations in Sichuan, while monkeys primarily fed on barks and lichens in Shaanxi, and lichens for the population in Hubei.

Intraspecific variation of diet might be linked to the availability of potential food resources25. Different patterns of food availability might induce various food preferences26,27. For R. roxellana, the population in Sichuan distribute in areas with deciduous and evergreen broadleaf forest where trees sprouted new leaves earlier in spring compared with habitats for other two populations. At the field site of Zhouzhi, Shaanxi, the habitat for R. r. qinlingensis is a mostly deciduous broadleaf forest area13. At the field site for R. r. hubeiensis at Shennongjia, Hubei, monkeys lives in a mixed coniferous broadleaf forest area28. The budding time and forest type for R. r. roxellana may provide high availability of taking foliage as important food resource.

Foliage contains relatively higher concentrations of protein compared with other diet composition of R. roxellana27. As a key nutrient, protein provides enough energy to keep healthy for living organisms. Golden snub-nosed monkey prefer to feed on leaves of trees rather than other food sources. Lichens or barks, as alternative food sources, would only been taken as a proximate response to ecological conditions with deficiency of highly nutritious food29.

For achievement of a balance between food intake and consumption, primates acquire nutrition and energy from foraging various food to ensure enough fuel for the digestive process and maintenance of a functioning body30. Therefore, monkeys perform different activity budget and energy investment based on various environmental and social conditions28,31. A number of studies show that activity budget is largely influenced by diet26,29,32,33,34,35,36. For instance, folivorous monkeys, such as langurs, are found to spend considerable time feeding on bulky leaves, and resting to allow for the digestion and fermentation process of the cellulose in their plant diet37,38,39,40.

In our study, compared with other two subspecies, the feeding time and resting time of R. r. roxellana are both increased, while moving time is decreased, which is consistent with the folivorous diet in this population. R. r. roxellana might have to spend more time in resting because they consumed more indigestible fiber from foliage to be digested27. In addition, times spent on locomotion and food seeking activities can be reduced under habitat with high levels of food abundance. Thus, our result might suggest that the activity budget of the golden snub-nosed monkey would vary between different ecological conditions, since the diet differentiation.

Compared to 22.5 km2 of home range in Zhouzhi, Shaanxi13, and 40 km2 in Shennongjia, Hubei41, R. r. roxellana in Laohegou, Sichuan had the largest home range (49.1 km2). One possible reason to explain this inconsistency may be ascribed to the special attributes of our study site. The leaves contained in the diet of R. r. roxellana were scattered and dispersed, which means individuals and groups have to expand their foraging areas to cater for the requirement of energy and nutrition. However, under this assumption, R. r. roxellana may spend more time on moving, which is contrast to our result about activity budget. More data and evidences are needed to explore the specific mechanism in future.

Population density in Sichuan is the highest with 10.6 individuals per km2, comparing with other populations: 4.0 individuals per km2 in Shaanxi13 and 4.8 individuals per km2 in Hubei41. As population density, basically determined by the capability of a habitat to provide sufficient energy and nutrition for the corresponding population, were also found as another dependent factor affected by geographic features and habitat ecology42. Compared with other two populations, we suggest that the food abundant of the habitat in Sichuan may be greater. Thus, it can be capable of supporting a larger number of individuals within a particular range.

We used whole year data in species in Hubei and Shaanxi, since previous studies suggested social combination of golden snub-nosed monkeys remained stable for several months, even years21. Our result suggested that unit size and social composition were different among these three subspecies of golden snub-nosed monkeys (Table 5). In our field site of Sichuan, we found larger numbers of social units. The unit size of R. r. roxellana is relatively smaller (8.3 ± 3.5, ranged from 3 to 14), compared to other subspecies in Hubei and Shaanxi.

The social organization of primates would be influenced by multiple ecological factors. One possible reason to explain this smaller unit size is the food abundance in habitat of Sichuan, which would lead to males occupy relatively average resource. Since in R. roxellana, female choice would initial and impact the male takeover43, females would have more options to choose with such equally distributed resource. Under this circumstance, numbers of one male unit would increase and the group size would be smaller. However, it is hard to determine what specific factor and mechanism influenced the smaller unit size in our case. More evidence is needed to test relevant hypothesis. Our result suggested that the pattern of the social organization would show differentiation under different ecological condition, even in the same species.

In conclusion, our study firstly provides detailed data on diet, activity budget, home range and social organization of R. r. roxellana under different habitats, compared with other two subspecies. Our result might provide evidence that the behavioral and dietary flexibility of R. roxellana enables the golden snub-nosed monkey to survive in different conditions. These results may contribute to an improved understanding of intraspecific adaptations to varied environments and flexible behavioral strategies of primates.