We conducted research at Dazhaizi on the western slopes of Mt. Wuliang, Jingdong County, Yunnan Province, China (Fan et al., 2015). Between 1 700 m to 2 700 m a.s.l., vegetation consists mainly of primary semi-humid evergreen broadleaf forests and mid-mountain humid evergreen broadleaf forests (Fan et al., 2009), which are typical habitat for langurs in Mt. Wuliang. The annual air temperature in the area is 16.1–18.3 °C and annual precipitation is >1 500 mm on average (Fan & Jiang, 2008; Fan et al., 2007; Guan, 2013). Air temperature changes seasonally, with the lowest monthly mean temperature (~10 °C) found in December and January and highest (~20 °C) found in June, July, and August. Rainfall also changes seasonally, with more than 80% of annual precipitation occurring in the wet season (May to October) and little rainfall occurring in the remaining dry season months (Fan & Jiang, 2008; Guan, 2013).
Three species of primate, including Indo-Chinese gray langurs, western black crested gibbons (Nomascus concolor), and stump-tailed macaques (Macaca arctoides), live in the study area (Fan et al., 2008). Large raptor predators, including hawk eagles (Nisaetus cirrhatus) and black eagles (Ictinaetus malaiensis), are regularly encountered. Terrestrial predators, such as yellow-throated martens (Martes flavigula) are common, whereas leopards (Panthera pardus and Neofelis nebulosa) are rarely reported (Fan et al., 2015; Jiang et al., 1994; Liu, 2017; Yu, 2004). Local people graze cows and goats and collect forest products such as mushrooms and herbal medicines (Fan, 2007). Illegal hunting and logging have not been recorded in the study area since 2003 because of the long-term study and conservation of the western black crested gibbons (Hu et al., 2018).
Trachypithecus crepusculus is listed as a National Class I Protected Species under Chinese Wildlife Conservation Law (Fan & Ma, 2018). There are no current population estimates of T. crepusculus in China; however, a recent survey indicated that approximately 2 000 Indo-Chinese gray langurs reside at Mt. Wuliang (Ma et al., 2015). Its conservation status has not yet been assessed by the IUCN because it was not considered a separate species until recently (He et al., 2012; Mittermeier et al., 2013; Rowe & Myers, 2016).
We studied a group of Indo-Chinese gray langurs inhabiting the evergreen broadleaf forests in the Dazhaizi area and collected data over 27 months during two periods (June 2012 to August 2013 and February 2015 to January 2016). As the only group of T. crepusculus in China, the study group has been monitored since 2008, including research on its activity budgets, dietary patterns, and population dynamics (Fan et al., 2015). The number of individuals in the study group increased from 70–80 in 2012 to more than 120 in 2014. In March 2014, the group split into two, with approximately 70–80 and 50 individuals in group A and group B, respectively (Fan et al., 2015). After group fission, we collected data on group A, which consisted of a similar number of individuals as the original group.
We followed the study group for more than 5 d on average per month (mean: 5.6±1.9 days, range: 2–11 days per month; n=27 months). Once the group split into subgroups, we followed the largest subgroup. We estimated the group center and recorded it every half hour using a GPS device (Garmin eTrex20). We observed langurs at less than 20 m, except when they were on inaccessible cliffsides. We collected behavioral data using instantaneous scan sampling at 10 min intervals (Altmann, 1974). Each scan lasted for a maximum duration of 3 min, during which time we recorded the age-sex class, behavior, and stratum of each visible individual. We classified the target langurs into five age-sex classes: i.e., adult male, adult female, adult female with clinging infant, juvenile, and infant. We estimated the age classes by body size and identified sex of adult langurs by external genitalia. We classified langur behaviors into six categories: i.e., (1) resting: inactive including self-grooming; (2) feeding: catching, swallowing, or chewing food; (3) traveling: moving including walking, climbing, running, and leaping; (4) geophagy: licking the surface of a rock for mineral matter; (5) social behaviors: grooming and playing; and (6) other, rare activities such as fighting, copulating, and drinking water. We estimated strata use as the height of langurs from the ground, divided into seven categories: i.e., ground; 1–5 m; 6–10 m; 11–15 m; 16–20 m; 21–25 m; and >25 m. Two research assistants estimated the heights of langurs during the study. During previous habitat surveys, they participated in the measurements of >4 500 trees using laser range finders and could accurately estimate tree heights to each category.
We collected terrestriality data of five Trachypithecus species from previous literature that provided the proportion of time spent by langurs on the ground (Table 1). In the paper reporting strata use of Francois’ langurs in different habitats, the results were shown as a figure (Zhou et al., 2013). We used image digitizing software Engauge Digitizer (v4.1) to obtain values from this figure.
Species Forest cover (%) Terrestriality (%) Habitat Location Method for collecting behavior data Sample size References T. crepusculus 78.00 2.9 Evergreen broadleaf forest Dazhaizi, China 10 min scan 43 347 records, 2–11 d/mon,
This study T. obscurus 73.00 6.0 Limestone Khao Lommuak, Thailand 15 min scan 14 341 records, 5–20 d/mon,
Aggimarangsee, 2004 T. leucocephalus 68.15 30.0 Limestone Fusui, China 10 min scan 10 570 records Huang et al., 2002; Xiong et al., 2009 T. francoisi 59.48 39.2 Limestone Fusui, China 10 min scan 7 030 records Xiong et al., 2009 T. poliocephalus 58.34 54.0 Limestone Cat Ba Island, Vietnam 10 min scan 549 h, 180 d,
Hendershott et al., 2018 T. delacouri 41.40 79.0 Limestone Van Long, Vietnam Focal animal 13 976 bouts,
372 h, 203 d,
Workman, 2010; Workman & Schmitt, 2012
Table 1. Habitat characteristics and terrestriality of six Trachypithecus species
We graphed the maximum convex polygon of the home range of our study group using group location data collected every half hour (Fan et al., 2015). We obtained GPS coordinates or research site maps from studies on comparative Trachypithecus species. For each langur species, we digitized and georeferenced their range in ArcMap (v10.0), and randomly selected 100 points within the range. We then derived forest cover from 30 m×30 m grids where the selected points were located using Global Forest Change 2000–2017 (https://earthenginepartners.appspot.com/science-2013-global-forest/download_v1.5.html) and calculated the average value of these points to represent forest cover of each site.
To test Prediction 1, we calculated the percentage of records across all behaviors in each stratum monthly and obtained a mean value from the monthly value to represent the strata use pattern of the group over the whole study period. We then determined differences in record proportions among strata. Specifically, we calculated the percentage of behavioral records in different forest strata for different age-sex classes and tested differences using the Kruskal-Wallis test. We used the Mann-Whitney U test to examine differences in strata use between wet and dry seasons. We also calculated the percentage of records for each behavior type in every stratum and examined the variation in the proportion of each behavior type in different forest strata using the Kruskal-Wallis test.
To test Prediction 2, we applied simple linear regression to analyze the relationship between habitat forest cover and proportion of terrestrial activities in Trachypithecus species. We set the confidence interval to 95%. To exclude the effect of habitat type on terrestriality, we reperformed this analysis after excluding T. crepusculus from the dataset and focused on five limestone species, i.e., T. obscurus, T. leucocephalus, T. francoisi, T. poliocephalus, and T. delacouri. To test Prediction 3, we compared strata use patterns between our study group and a group of Francois’ langurs inhabiting different habitats (Zhou et al., 2013) using the cross-tab X2 test. All statistical analyses were performed using IBM SPSS Statistics 21.0. All data collection protocols complied with the current laws of China.
Living in forests: strata use by Indo-Chinese gray langurs (Trachypithecus crepusculus) and the effect of forest cover on Trachypithecus terrestriality
- Received Date: 2019-12-19
- Accepted Date: 2020-04-26
- Available Online: 2020-05-09
- Publish Date: 2020-07-01
- Behavioral flexibility /
- Habitat degradation /
- Strata use /
- Trachypithecus /
- Indo-Chinese gray langur
Abstract: Studies on behavioral flexibility in response to habitat differences and degradation are crucial for developing conservation strategies for endangered species. Trachypithecus species inhabit various habitats and display different patterns of strata use; however, the effect of habitat structure on strata use remains poorly studied. Here, we investigated strata use patterns of Indo-Chinese gray langurs (Trachypithecus crepusculus) in a primary evergreen forest in Mt. Wuliang, southwest China, from June 2012 to January 2016. In addition, we compared T. crepusculus strata use and terrestriality with five other Trachypithecus species from previous studies. Unlike langurs living in karst forests, our study group was typically arboreal and spent only 2.9% of time on the ground. The group showed a preference for higher strata when resting and lower strata (<20 m) when moving. The langurs primarily used time on the ground for geophagy, but otherwise avoided the ground during feeding. These strata use patterns are similar to those of limestone langurs (T. francoisi) when using continuous forests. At the genus level (n=6 species), we found a negative relationship between habitat forest cover and terrestriality. This negative relationship was also true for the five limestone langur species, implying limestone langurs increase territoriality in response to decreased forest cover. Our results document behavioral flexibility in strata use of Trachypithecus langurs and highlight the importance of the protection of continuous forests to promote langur conservation.
|Citation:||Chi Ma, Wei-Guo Xiong, Li Yang, Lu Zhang, Peter Robert Tomlin, Wu Chen, Peng-Fei Fan. Living in forests: strata use by Indo-Chinese gray langurs (Trachypithecus crepusculus) and the effect of forest cover on Trachypithecus terrestriality. Zoological Research, 2020, 41(4): 373-380. doi: 10.24272/j.issn.2095-8137.2020.047|