An Ecological Assessment of Critically Endangered Chinese Pangolin Manis pentadactyla (Mammalia: Pholidota: Manidae) in the Midhills Region of Nepal

The Chinese Pangolin (Manis pentadactyla) is a “Critically Endangered” insectivorous mammal. There is a lack of information on the ecology, distribution and behavior of this species in Nepal, even though community forests in the Midhills Region of Nepal are considered to be prime habitats for the species. We conducted an ecological assessment of the habitat use of this species in nine community forests covering an area of 170.69 ha in Balthali village in Kavrepalanchok district, Nepal. We divided each forest into 50 × 50 m grids and searched for Chinese Pangolin burrows along 50 m transects in each grid. We categorized burrows into two types, new and old burrows, and recorded 10 environmental variables for each burrow. We found a total of 542 burrows, including 323 old burrows and 219 new burrows. The average width and height of a burrow opening was 21.66 ± 3.94 cm (n = 542) and 22.42 ± 5.02 cm (n = 542). The total density of burrows in the study area was 3.1 ha −1 , with new burrows density of 1.2 ha −1 and old burrows density of 1.8 ha −1 . We found most burrows in sites with an elevation range of 1400 - 1500 m above sea level, gentle slopes, brown colored soil, high density of tree crown cover and undergrowth vegetation, southern exposure, within 150 m from a water source and less than 200 m from a human settlement. Our study has generated base-line data on the habitat use of Chinese Pangolin, which we hope will help in designing site-specific action plans for Chinese Pangolin conservation in Kavrepalanchok district, Nepal. do not low and Our We additional range,


Introduction
The Chinese Pangolin (Manis pentadactyla) is a small burrowing insectivorous mammal found in China, Hong Kong, India, Lao People's Democratic Republic, Myanmar, Nepal, Thailand, Bangladesh, Vietnam and Bhutan [1]. The species is listed as "Critically Endangered" on the International Union for Conservation of Nature Red List of Threatened Species [1]. The Chinese Pangolin is one of the most illegally trafficked species in the world due to the high economic value of its scales and meat [2] [3] and it is listed in Appendix I of the Convention on International Trade in Endangered Species of Wild Fauna and Flora [4]. In Nepal, the Chinese Pangolin is protected by the National Parks and Wildlife Conservation Act of 1973, but illegal hunting and trapping is common for export as well as for local consumption and traditional medicine [5] [6]. However, the first Pangolin Park in Nepal has recently been established and the growing interest in this species and the potential benefits from ecotourism will hopefully support its conservation [7].
Chinese Pangolins excavate burrows to search for termites, as well as for resting locations to avoid the cold weather [8] [9]. The locations of their burrows during different seasons can indicate habitat preference in terms of the environmental variables existing in the area [10]. Understanding the importance of environmental variables such as elevation, crown cover, undergrowth vegetation, slope, aspect, distance from water source and human settlement is vital for conservation planning for the species [10] [11] [12]. Pangolins occupy a variety of habitats within their geographical range [12], so the design and implementation of a conservation strategy for this endangered species require a thorough knowledge of their population and habitat ecology [1]. In Nepal, the geographic distribution, population size and status of Chinese Pangolins remain poorly understood as few studies have been carried out in the country [ [18]. The aim of our study was to increase the understanding of Chinese Pangolin's habitat use in Nepal by assessing their burrow locations in nine community forests in Nepal. Open Journal of Ecology rests. Nepal has an active community forestry program, which gives communities authority to manage national forests near their villages; this program is recognized as providing a range of economic and social benefits to communities, including reducing conflict with wildlife [19]. The community forests in Balthali village are dominated by tree species like Pinus roxburghii, Prunus cerasoides, Rhododendron spp., Alnus nepalensis, Choerospondias axillaris and Schima wallichii. There were many community forests in a Balthali village, so before selecting the study sites we communicated with District forest officers (DFO) for information on the presence of Chinese Pangolins in these community forests.
We further verified information provided by DFOs through meetings with each community forest user groups and our preliminary field observations. We then selected nine community forests having an altitude range of 1300 -1600 m in  Table 1).

Methods
We conducted our field surveys from 27 March 2019 to 3 May 2019. We investigated habitat use of Chinese Pangolins by counting burrows in nine community forests and recording environmental variables at each burrow. Chinese Pangolin sightings in the wild are very rare due to its nocturnal behavior and habit of remaining in burrows during the day [10]. Chinese Pangolins satisfy their   [20], Bhutan [21] and China [10] [22].
In each community forest, we walked along the boundary and recorded the boundary's Geographic Position System (GPS) coordinates using a handheld Garmin GPS Map 60 CSx. We processed the boundary coordinates using Arc  [20]. Our study area which is situated in central mid-hill region of Nepal is well outside the Indian Pangolin range [20]. Thus, all the burrows identified originated from Chinese Pangolin.
We recorded the GPS location of each Chinese Pangolin burrow encountered along transects using a handheld Garmin GPS Map 60 CSx. We measured the height and width of the burrow opening using a measuring tape. We categorized the Chinese Pangolin burrows into two types following the Pangolin Monitoring Guideline for Nepal [20]: New burrows which were still actively used and old burrows, which were no longer being used. In New burrows, we observed freshly dug soil with fresh footmarks, no dry fodder and seedling vegetation in burrows and presence of many fresh scratches. In old burrows, we observed compact and dry soils with presence of spider webs and burrow entrances fully covered by grasses, smaller branches and dried leaves.

Results
We surveyed 679 transects and found burrows in 16.9% of them ( Figure 2). We recorded a total of 542 burrows in our nine study sites (Table 1; Figure 2). We classified 219 burrows as New/active and 323 burrows as Old/inactive. The total density of burrows in the study area was 3.1 ha −1 . The density of new burrows was 1.2 ha −1 and the density of old burrows was 1.8 ha −1 . There was considerable variation in burrow density between the nine sites. The highest burrow density was recorded in Kamaladevi CF with 11.9 ha −1 and the lowest burrow density was recorded in SanuGaun CF with 0.38 ha −1 (Table 1).  We measured 10 environmental variables associated with burrows and the occurrence frequency (P o ) of each environmental variable (Table 2). We recorded the highest frequency (76%) of burrows in the middle elevation rage (1401 -1500 m), followed by 16% in the low elevation range (1300 -1400 m) and 8% burrows in the highest elevation range (1501 -1559 m; Figure 2). We found most burrows (91%) in gentle slopes < 30˚ (   [20] [22] and Heath [2] has shown that the burrows widen into larger chambers behind the openings. Around each new burrow, we observed numerous incompletely dug smaller burrows with shallower openings and less depth with presence of ants and termites, which we classified as feeding burrows. Chinese Pangolins dig burrows for living (resident) and feeding purposes [24]. Chinese Pangolins stay in the living burrows and will forage in an area 50 -100 cm in circumference around their living burrows for several days [2]. Chinese Pangolin digs a hole (5 -10 cm deep) as latrine sites to deposit urine and feces and cover the hole with soil [2] [24]. Chinese Pangolins burrow depths differ in summer and winter due to differences in termite distributions [2] [22] and burrow opening diameter is dependent on the body size of the pangolin residing in the living burrow [12]. We did not find differences in burrow opening width and height between new and old burrows, whereas Karawita et al. [12] reported that the burrow width, height and depth of a related species (Indian Pangolin) differed between resting and feeding burrows. The Chinese Pangolin's living burrow design includes a 30˚ upward sloping tunnel [25] whereas, the Indian Pangolin's living burrow design includes a 10˚ -20˚ downward sloping tunnel [12].

Discussion
We recorded Chinese Pangolins burrows in nine community forests, and there was considerable variation in burrow density between community forests.
Anthropogenic activities like livestock grazing, guard dogs, hunting inside community forests, forest fire and construction of foot trails could result in detrimental effects on Chinese Pangolin survival [26] and could explain the variation of burrow density between our nine community forests. We recorded most of  [10] recorded most burrows at an elevation range of 750 -1500 m and fewer burrows at 1501 -1700 m. In Nepal, though sympatric distribution is recorded for Chinese Pangolin and Indian Pangolin [20], Indian Pangolin burrows are recorded at an elevation of 675 m [18]. The predicted elevation ranged from 132 m to 2704 m for both Pangolins [18] and the greatest potential distribution of Chinese Pangolin is in the mid-hill region between 1000 -3000 m in Nepal [17]. We have conducted our study in a relatively small area (170.69 ha) and could not include samples from a wide range of elevation, so elevation preference may not be applicable to other Chinese Pangolin habitats.
All burrows in our study area were on gentle slopes (<30˚). This finding contrasts with the finding of Wu et al. [10] who reported that Chinese Pangolins in China prefer steeper slopes because digging burrows in steep slopes save energy for Chinese Pangolins as well as reducing damage to burrow entrance from heavy rainfall [3]. Heath et al. [27] also noted that high energy consumption is required in digging burrows. However, studies carried out by Bhandari and Chalise [11] and Rai [28] reported the maximum number of burrows at 20˚ -30˚ in Nepal.
Rai [28] recorded the presence of soft clay loam and sandy loam soil in a slope gradient of 20˚ -30˚ in community forests of Dolakha district, midhills Nepal.
We found that most burrow sites had a southern exposure, which is consistent with Wu et al. [10] who reported that Chinese Pangolins in China prefer burrowing entrance exposure facing the sun (i.e., south direction), which helps to maintain burrow temperature in winter. Our survey was conducted during winter, which is when a southern exposure would be helpful. Chinese Pangolins have slow metabolisms, so an optimum temperature of at least 18˚C during winter should be present to keep these animals warm inside their burrows [3] [29]. We observed that 90% of the burrows had internal temperatures less than 20˚C, and we recorded difference between the inside and outside burrow temperatures.
However, Bao et al. [29] in a study of air temperature changes in burrows of  [18]. Termite and ant species, which are common prey of Chinese Pangolin, are more common in dense forest canopies [30]. However, in some habitats having open canopy closure and dense undergrowth vegetation could discourage pangolins from making living burrows in those habitats [12].
We found that most burrows were located in sites with brown soil and low soil moisture (0% -15%), which is consistent with other studies [11] [15] [16] [31]. Chinese Pangolin's preferred food is termites, which tend to colonize in moist soils because of higher moisture content making the soil soft and easier to dig burrows [3] [32]. Chinese Pangolins have been reported to feed on 23 species of ants and 12 species of termites [24] and consume all life stages of these preys [33]. However, we acknowledge that soil moisture fluctuates in burrows, and we were not able to record soil moisture on multiple days.
Most of the burrows in our study area were less than 200 m from human settlements since community forests are generally located near villages. In turn, community forests are often located near cultivated land, which are rich in ants and termites, so most of the burrows were recorded close to human settlement.
Cultivated areas are considered as potential habitat for Chinese Pangolins in Nepal [17]. Other studies have reported that anthropogenic activities have a negative impact on Chinese Pangolin survival near human settlements [26] and that collection of fuel wood and fodder, grazing livestock inside the community forest, spraying insecticides and pesticides in agricultural lands close to community forests are major threats to Chinese Pangolins [34]. Most of the burrows in our study area were less than 150 m from a stream because two major rivers, Rosi and Ladku, as well as many small streams are present in the area. Our finding was consistent with other studies that report that Chinese Pangolins drink water frequently [16] and that Chinese Pangolin burrows are rarely found in dry areas [11].
Our study analyzed a larger number of burrows than any previous study in Nepal and has provided a detailed ecological understanding of Chinese Pangolin burrows in association with different environmental variables in community forests in Nepal. We found that Chinese Pangolins prefer burrowing at elevations between 1401 -1500 m in sites with gentle slopes, high forest canopy, high undergrowth, brown soil, southern exposure, and do not prefer sites with higher elevation, steep slopes, northern exposure, low crown cover and low undergrowth vegetation. Our findings will help conservation agencies to support the community forest user groups in developing strategic measures to conserve Chinese Pangolins. We recommend that additional studies involving modern scientific techniques, such as camera traps and genetic studies, be conducted to assess the status, distribution and population size of Chinese Pangolins in these areas and throughout their range, in order to conserve the most highly trafficked mammal species in the world.