Introduction

Members of the genus Rhinopithecus inhabit a wide range of habitats, which vary from the tropical evergreen broadleaf forests of Vietnam in R. avunculus to the high-altitude conifer forests of China in R. bieti. Rhinopithecus species have been documented living at 200–4600 m above sea level (Kirkpatrick and Grueter 2010). Snub-nosed monkeys have larger home ranges than most other colobines do, as well as much larger group sizes (Kirkpatrick and Grueter 2010). These groups are organized as multilevel societies consisting of several one-male, multifemale units (OMUs) associated with one or several satellite all-male units (AMUs) to form a stable and cohesive group; groups exceeding 400 individuals have been documented (Grueter 2013; Kirkpatrick and Grueter 2010). This complex multilevel social organization is relatively rare across nonhuman primates (Grueter et al. 2012). It is likely that the multilevel societies in Rhinopithecus species evolved from an ancestral Asian colobine that lived in separate OMUs (Grueter et al. 2012; Qi et al. 2014).

The Burmese or black snub-nosed monkey, Rhinopithecus strykeri, is the most recently discovered member of genus Rhinopithecus, bringing the total number of snub-nosed monkey species to five (Geissmann et al. 2011). It is closely related to R. bieti, the black-and-white snub-nosed monkey, in both morphology and genetics, especially to a R. bieti haplogroup in the southern distribution (Geissmann et al. 2011; Liedigk et al. 2012; Zhou et al. 2014). Preliminary surveys suggest that R. strykeri occurs only in Myanmar and China between the N’mai Hka River to the west and the Salween River to the east (Geissmann et al. 2011; Long et al. 2012; Ma et al. 2014). This species dwells in extremely harsh, mountainous terrain; its habitat consists of cool temperate rain forest, mixed temperate forest, and bamboo forest 1720–3700 m above sea level (Geissmann et al. 2011; Ma et al. 2014; Li et al. 2014). There are either three or four groups totaling 260–330 individuals in Myanmar (Geissmann et al. 2011), and up to 10 such groups totaling 490–620 individuals in China (Ma et al. 2014). Although the detailed distribution and life history of R. strykeri are still unknown, rapid population decline and habitat loss, especially in Myanmar, have pushed the species to the edge of extinction. The International Union for Conservation of Nature considers this new primate species Critically Endangered (Geissmann et al. 2012); therefore, comprehensive field research and conservation action are imperative.

The black snub-nosed monkey dwells in extremely harsh, mountainous terrain, with steep slopes and dense forests, and no monkeys have been habituated (Geissmann et al. 2011; Ma et al. 2014), making it difficult to track and observe them in their natural habitat. We here describe preliminary data on the social characteristics and ecology of a group of R. strykeri obtained using direct observation and infrared camera traps at Pianma, Yunnan, China.

Methods

Study Area and Study Group

We conducted the survey at Pianma (26°2.337′N, 98°39.127′E), located on the west slope of the southern part of the Gaoligongshan National Nature Reserve (Fig. 1) in Lushui county, Nujiang Lisu Autonomous Prefecture, Yunnan, China. The survey area was ca. 80 km2, with an elevation of ca. 1900–3800 m. Annual average temperature is 14.6–2.2°C and annual average rainfall is 1200–3900 mm; both vary with altitude (Xue 1995a). Forest types found at the site included 1) mid-mountain humid evergreen broadleaf forest (1800–2800 m), with Quercus kongshanensis and Lithocarpus variolosus as the dominant species; 2) Yunnan hemlock forest (2700–3100 m) with Tsuga dumosa and Rhododendron protistum as the dominant species; and 3) bamboo-conifer mixed forest (>3100 m), dominated by bamboo but including other species such as Abies delavayi, Ribes himalense, Gaultheria cardiosepala, and Rhododendron mallotum (Xue 1995b).

Fig. 1
figure 1

Gaoligongshan National Nature Reserve showing the location of Pianma and its typical vegetation zones. (A) Bamboo–conifer mixed forest. (B) Yunnan hemlock forest. (C) Mid-mountain humid evergreen broadleaf forest.

Full size image

Recent reports suggest that only one group of Rhinopithecus strykeri exists at Pianma (Li et al. 2014; Long et al. 2012; Ma et al. 2014). This group numbers ca. 80–100 individuals and uses an area of ca. 12 km2 in the central-southern part of Pianma (Li et al. 2014; Ma et al. 2014). We focused our study on this group based on recent reports and local knowledge.

Direct Observation and Population Counts

We conducted direct observation from 08:30 h to 18:00 h (GMT + 8) three to five times per week from May 5, 2013 to May 24, 2014. In addition to searching for monkeys themselves, we recorded all traces of activity of Rhinopithecus strykeri including feces, broken branches, and food litter. Once we found a monkey group or indirect evidence of their presence, we used a GPS receiver (South S720 GIS) to record the location and then attempted to follow, observe, and videorecord the monkeys. The GPS receiver used the WGS-84 reference coordinate system with single point accuracy to within 5 m of the true position.

Camera Trap Monitoring

We performed camera trap monitoring from November 18, 2013 to May 24, 2014. We deployed 30 camera traps (10 Ltl-Acorn 6210MC and 20 Ltl-Acorn 5210A) in the monkeys’ putative home range based on a 6-mo preliminary field survey that began on May 5, 2013. Both types of camera were equipped with a main passive infrared sensor and two side prep sensors to detect heat and motion. The infrared flash range was 25 m (infrared wavelength 850 nm). The sensors' maximum detection range was also 25 m (medium sensitive setting), and covered a 100° arc in front of the camera. Cameras operated 24 h per day and triggered when motion was detected. We attached cameras to tree trunks at a height of 30–50 cm facing animal tracks, water sources, mineral licking sites, and resting sites at altitudes ranging 2570–3240 m. We set cameras as follows: “Photo,” highest image quality (12 megapixels), medium trigger sensitivity, 1-s trigger interval, three shots per trigger, side prep sensors “on,” time and date stamp “on.” We recorded the geographic coordinates of each camera with a GPS during deployment. We used 8 GB Sandisk SDHC memory cards to record image data, and 8 (Ltl-Acorn 5210A) or 12 (Ltl-Acorn 6210MC) AA batteries to power the cameras. We checked cameras every 1–2 mo to replace SD cards or batteries as necessary.

Data Analysis

We examined each photo and cataloged each animal species, the number of individuals, their sex and age (if possible), and the date and time of the visit. We used Adobe Photoshop CC 2014 to enhance details of underexposed photos to assist in identification. We only used images in which individual Rhinopithecus strykeri were visible for further analysis. We recorded an independent visit of R. strykeri if one of the following three criteria were met: 1) consecutive photographs of different individuals, 2) consecutive photographs of individuals taken more than half an hour apart, or 3) nonconsecutive photos of individuals (O’Brien et al. 2003; Tan et al. 2013).

Based on live video of the monkeys collected during the preliminary survey, we categorized individual Rhinopithecus strykeri into the following age/sex classes based on body size, coloration of fur, and other traits: Adult males were the largest individuals in the band, with black/dark gray/brown fur, more noticeably erect and divided black fur on their heads, thicker tails, and pale pink faces and testes; adult females were also large but with less noticeably erect head fur, plus visible labia and vagina; juveniles were medium-sized individuals with deep gray to black fur; infants were the smallest individuals with dark to light gray fur and light gray faces. We considered all individuals that were carried by other group members to be infants. We logged individuals who could not be assigned to an age/sex class as uncertain.

We recorded the presence of a one-male, multifemale unit (OMU) when one adult male and several adult females and infants appeared in images. We also considered a single female to be a member of an OMU. We recorded different OMUs when different units appeared in images after an interval of time had elapsed and/or there was space between multiple OMUs. We identified all-male unit (AMU) by the presence of multiple males in one image or different males in consecutive images. We did not assume that a single male was an AMU member, because solitary males have been observed in another Rhinopithecus species, R. roxellana (Qi et al. 2014; Xiang et al. 2014; Zhao and Li 2009).

We estimated the group’s vertical range based on both location data collected during observation and camera site elevations. Because the minimum convex polygon (MCP) method can result in overestimates of total home range area when places that the animals do not use occur within the polygon (Grueter et al. 2009), we used the concave polygon method to “modify” MCP (Harris et al. 1990), excluding areas such as farmland, meadows, and roads that monkeys never visited. We entered all geographic coordinates obtained from camera traps and direct surveys into Google Earth Pro 7.1.

Ethical Note

Before conducting this study, we gained approval from the State Forestry Administration of China, the Gaoligongshan National Nature Reserve, the local government, and the Institutional Animal Care and Use Committee of Central South University of Forestry & Technology. Data collected were purely observational.

Results

We obtained 51 geographic coordinates for sites of Rhinopithecus strykeri from direct observation. We contacted the monkeys for 8 d and counted >100 individuals in a large cohesive group on October 17, 2013, when they crossed an open area. We found most traces of monkey activity between 2700 m and 2900 m (70.6 %, N = 51, Fig. 2), with the lowest site at 2469 m and the highest at 3076 m.

Fig. 2
figure 2

Vertical range of Rhinopithecus strykeri based on geographic coordinates obtained from camera traps and direct observation at Pianma, Yunnna, China from May 5, 2013 to May 24, 2014.

Full size image

We obtained 8990 images with a total of 18 species of mammals and 15 species of birds. Rhinopithecus strykeri triggered only 222 of these photographs. R. strykeri visited camera traps a total of 16 times at 7 different locations, and 14 of these visits (88 %) occurred at altitudes >2900 m (Table I, Fig. 2). We identified a total of 90 individual monkeys with 31 classed as adult males, 29 adult females, 7 juveniles, 7 infants, and 16 as uncertain. The ratio of adult males to adult females was 1.1, adult females to infants 4.1, and adult individuals to immature individuals 4.3 (Table I, Fig. 3).

Table I Camera trap visits by Rhinopithecus strykeri with the ratio of males to females, females to infants, and adults to immatures at Panma, Yunnan, China, from November 18, 2013 to May 24, 2014
Full size table
Fig. 3
figure 3

Rhinopithecus strykeri photographed by camera traps at Pianma, Yunnan, China from November 18, 2013 to May 24, 2014. (A) An adult male. The arrow points to its testes. (B) An adult female. The arrow shows the labia and vagina. (C) An adult female carrying an infant. The arrow shows the infant. (D) Uncertain individual, where vegetation and body orientation precluded age/sex classification. (E) Two juveniles playing (indicated by white circles). (F) An all-male unit (AMU) of seven individuals. (G) A one-male, multifemale unit (OMU) including one adult male, three adult females, and one infant. (H) An incomplete OMU, including two adult females and one infant. (I) One adult male and one adult female at a water source. The adult female is hidden by vegetation, but was identified in consecutive images and was drinking water on the ground.

Full size image

We obtained group counts of five OMUs and one AMU when individuals passed in front of cameras consecutively (Table II, Fig. 3) and also identified discrete behaviors such as drinking water and playing (Fig. 3). In two cases, the monkeys visited two different camera traps on the same day (Table I). On the morning of January 10, 2014, at 09:23 h, they visited camera no. 0007, which was deployed near a water source in a valley. At 16:58 h on the same day they visited no. 0004, which was deployed on a ridge ca. 1026 m away from the no. 0007 to the south. On April 22, 2014, the group visited camera no. 0011 which was deployed on a ridge at 10:21 h and later visited no. 0025, deployed on a nearby ridge, ca. 827 m to the south at 12:24 (Figs. 3 and 4).

Table II Largely complete count of five one-male, multifemale units (OMU) and one all-male unit (AMU) of Rhinopithecus strykeri by camera traps at Panma, Yunnan, China, from November 18, 2013 to May 24, 2014
Full size table
Fig. 4
figure 4

Preliminary estimate of the home range of Rhinopithecus strykeri at Pianma, Yunnna, China. Numbered cameras are those that captured images of R. strykeri. Data were gathered from May 5, 2013 to May 24, 2014.

Full size image

Analysis of consecutive images captured by no. 0025 on April 22 and April 28, 2014, and no. 0017 on April 17, 2014, showed that different OMUs and the AMU moved in the same direction but that there was always a space between the units (Table I, Fig. 3). We also observed multiple OMUs forming a large group without aggression from October 15 to October 17, 2013, during direct observation.

Combining all geographic coordinates, we estimated the vertical range of this group of Rhinopithecus strykeri to be 2400–3300 m (Fig. 2). Using the modified MCP method, our preliminary estimate of the home range was 22.9 km2 (Fig. 4).

Discussion

Our findings suggest that camera traps can be deployed successfully to survey Rhinopithecus strykeri. This contributes to a body of work using camera traps to investigate and monitor arboreal primates (Bezerra et al. 2014; Easton et al. 2011; Galvis et al. 2014; Huang et al. 2014; Kierulff et al. 2004; Olson et al. 2012). As a noninvasive, quantitative technique, infrared camera traps can collect data on relative abundance, distribution, social organization, population dynamics, behavior, and the reaction of primates to other species with minimum human disturbance; this is especially important when subjects are elusive, occur at low densities, are not distributed in a predictable manner, are not habituated, or are located in remote areas (Gerber et al. 2014; O’Connell et al. 2011). Researchers can deploy camera traps at designated locations to capture specific and rare behavior, or use camera traps in combination with other methods to learn more about primate life history (Bezerra et al. 2014; Blake et al. 2010; Boyer-Ontl and Pruetz 2014; Pebsworth et al. 2012; Tan et al. 2013).

Our results suggest that Rhinopithecus strykeri exhibits a multilevel social organization, comprising several OMUs and at least one AMU (Fig. 3), similar to other snub-nosed monkeys (R. bieti: Kirkpatrick et al. 1998; R. roxellana: Qi et al. 2014; R. brelichi: Xiang et al. 2009a; R. avunculus: Boonratana and Le 2013). The ratios of adult females to infants and adults to immatures of R. strykeri at Pianma based on photographic evidence are much higher than the ratios of 2 and 1 in stable populations of R. bieti and R. roxellana (R. bieti: Kirkpatrick et al. 1998; Xiang et al. 2013; R. roxellana: Tan et al. 2007). In line with the ratios of 4.7 and 2.5 reported earlier for our study group (Li et al. 2014), we suggest that the group is in decline. Hunting and habitat destruction or degradation may be to blame (Li et al. 2014; Ma et al. 2014). However, we could not monitor the entire group owing to the technical limitations of the camera traps (Swann et al. 2004), and it was difficult to identify the age and sex of every individual, especially when some images were blurred or not captured in proper body orientation. Differences in time spent on the ground between age/sex classes may also create bias in the observed ratios of females to infants. For example, female R. bieti without clinging infants spend more time on the ground than expected, while females with clinging infants spend less time on the ground than expected (Xiang et al. 2009b). Thus, we should be cautious when using data from camera traps alone to evaluate population parameters or population structure.

Our preliminary estimate of the total area used by Rhinopithecus strykeri, 22.9 km2, may be more reasonable than the previous estimate of 12 km2 (Li et al. 2014), as it is closer to the home range area of groups of R. bieti, R. roxellana, and R. brelichi, which usually exceed 20 km2 (R. bieti: Kirkpatrick et al. 1998; Ren et al. 2009; Xiang et al. 2013; R. roxellana: Li et al. 2000; Su et al. 1998; R. brelichi: Z. F. Xiang unpubl. data). The altitudinal range at Pianma, where R. strykeri ranged between ca. 2400 m and 3300 m, is consistent with previous work, as the reported vertical range of R. strykeri is 1720–3700 m above sea level in both Myanmar and China, with the greatest amount of activity at 2600–3100 m (Geissmann et al. 2011; Li et al. 2014; Ma et al. 2014). However, we did not find evidence that R. strykeri ranged below 2400 m or above 3300 m. We suggest that R. strykeri may not range frequently at lower or higher altitudes. The lower bound is likely due to human disturbance and forest degradation; little potential habitat exists at lower altitudes, especially beyond the boundary of the Gaoligongshan National Nature Reserve (Li et al. 2014; Ma et al. 2014). The upper bound may be attributed to extremely dense bamboo and a lack of large trees for sleeping, traveling and feeding in areas above 3300 m (Xue 1995b).

In sum, this study has demonstrated that camera traps can be a useful tool to study snub-nosed monkey ecology. Further research into the behavioral ecology and conservation biology of Rhinopithecus strykeri is essential.