Community-based study to demonstrate the presence and local perspectives of the Critically Endangered Chinese Pangolin Manis pentadactyla in Zhejiang Wuyanling, China

Illegal hunting and trading of the Chinese Pangolin Manis pentadactyla has pushed this Critically Endangered species close to extinction. While local reports have suggested its continued presence in mainland China, this has not been confirmed by a research group except for a survey of presumed pangolin burrows in 2004. We conducted a six-month field study using infrared camera surveillance and community questionnaire survey in Zhejiang Wuyanling National Nature Reserve in China, to determine the status of Chinese Pangolins and understand local attitudes towards the conservation of this species. Our study details the first verifiable documentation of two visual records of a Chinese Pangolin in the wild, demonstrating the suitability of pangolin habitat in Wuyanling region, and suggests an increasing awareness and strong willingness in local communities to conserve the Chinese Pangolin.


INTRODUCTION
The Chinese Pangolin Manis pentadactyla is listed as Critically Endangered by the IUCN primarily due to extensive poaching for their meat and scales ). It receives the highest level of protection from trade in CITES Appendix I (Challender & Waterman 2017). In China, the Chinese Pangolin is listed as a State Category II protected species under the Wildlife Protection Law, with protection from the Regulations on Implementation of Protection of Terrestrial Wild Animals (Zhang 2008). Despite this, the population of the Chinese Pangolin is thought to have declined by 89-94 % since the 1960s (Wu et al. 2004a). Little is known about the current distribution or population of this solitary and nocturnal species, few studies have been conducted in mainland China to detail the population of Chinese Pangolins (Wu et al. 2002). Recent reports suggest that some remnant individuals have been traded in illegal wildlife markets or confiscated from traders, but the provenance of these animals from mainland China has not been verified (Xu et al. 2016).
In 2013, our group recorded two camera-trap images of a pangolin (Manis spp.) within the Wuyanling National Nature Reserve (Zhang et al. 2017). The species was not identified due to limited characteristics recognisable in the images. Our current study was designed to further assess the presence of Chinese Pangolins in the reserve and understand local community attitudes towards the species' conservation. Wuyanling National Nature Reserve is located in Taishun County in southern Zhejiang Province (27.706,119.675) (Figure 1 , 2). The reserve was established in 1975 and is an important bird conservation area (BirdLife International 2019) consisting of subtropical evergreen broadleaf forest with highly diverse flora and fauna. Within an area of 18,861.5ha, the reserve contains 4,170 households with 15,444 residents officially registered with the local authorities, including 3,064 people residing in the core area and buffer zone, and 12,380 in the transition area. The number of residents actually living within the reserve is estimated to be less than 5,000, due to a large number having migrated to cities for work, according to the latest population census in 2017 (Taishun Government 2017).

Line transect and quadrat survey
Ten (10) line transects ranging 2-6 km in length (total 39.8km) and six quadrats (1.00 hm 2 /quadrat) were selected within the reserve extending from the uninhabited regions to the nearby villages. With limited resources, selection of the line transects and quadrats was based on the historical records of pangolin sighting, poaching, and releasing activities, and in an effort to cover the under-researched low-human disturbance areas. Diurnal surveys were conducted in each line transect and quadrat once per month for six months from July to December 2017 to identify and examine potential burrows for Chinese Pangolins. Observational environmental data were collected around each burrow, including estimated duration since burrow excavation, presence of termites and decayed wood, and pangolin faeces or other evidence of active occupation following the methods published in Wu et al. (2004b).

Camera traps surveillance
Sixty infrared camera traps (LTL Acorn 5210A, LTL Acorn 6210) were placed in three surveillance areas around the identified (potentially active) pangolin burrows from the line transect and quadrat surveys, and in the reserve's core area and its adjacent transition area where was not covered by the line transect and quadrat surveys, to maximize the chance of detection. All camera traps were placed 0.5-1 m above ground, with consideration of the ground slope, height of trees, and the inclination angle between 15°-30° to achieve the maximum diameter and range of camera coverage. The intervals between each camera trap and each surveillance area were >500m and >5,000m, respectively. Corresponding to the altitude range of potentially active burrows, the altitudes of camera traps ranged 313-1,128 m across four different vegetation types. All camera traps were installed on 1 July 2017 and active until 31 December 2017. Burrows presumed to be inactive or confirmed to be occupied by other species were omitted in the subsequent investigations, and all potentially active burrows were investigated by the monthly line transect or quadrat surveys and infrared camera traps for six months (Figure 1).

Community questionnaire survey
In order to understand local knowledge of and attitudes toward Chinese Pangolins, a standardized questionnaire was designed in Mandarin (Appendix 1) for community survey. We aimed to obtain a sample size of n=3,000 to be statistically representative, covering 60% of the permanent residents within the reserve at the maximum estimation of 5,000 in total. 1) Prior to recruitment and data collection, study staff from local village committee and Wuyanling National Natural

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Reserve Management Bureau conducted community meetings, house visits, and broadcasted the information in the village to introduce this study to generate interest in the community; 2) Recruitment was conducted at the community activity centre or town hall in each village where local residents who were interested in the project visited for further information and became potential participants; 3) Study staff informed all potential participants about the survey for consent before data collection; 4) After the completion of informed consent process, questionnaires were administered and one-onone interviews were conducted in a private setting to ensure confidentiality. Children aged 12-18 years were interviewed with the permission and presence of a parent or guardian (e.g., school teacher). From September to December 2017, a total of 3,041 questionnaires were distributed in 12 out of the 15 villages within the nature reserve. Three villages were omitted from the surveys because they had few residents (<50) or only a small area of these villages was under the administration of the nature reserve. Collected data were entered into IBM SPSS Statistics software Version 25 and analysed by cross-table and Pearson's chi-squared test. All results were translated into English for reporting.

Potentially active burrows for pangolins
A total of 33 burrows were located along nine line transects and in six quadrats in the initial field survey. During the monthly survey, burrows that were estimated to have been created more than 15 days or covered by spider webs and decayed leaves at the entrance were recorded as inactive. Active burrows for Chinese Pangolins were identified based on several environmental factors, including the presence of termitarium and decayed wood (e.g., Pinus massoniana, Cunninghamia lanceolate) around a burrow (<50m), fresh soil at the entrance, and suspect faeces (Image 1). As the survey was conducted from July to December, seasonal burrow characteristics in regard to the utilization of a burrow, and preferred locations for burrow excavation in summer and winter were considered in identifying the active Chinese Pangolin burrows (Wu et al. 2004b). Active burrows were found at five line transects and two quadrats, further examination confirmed five potentially active burrows for the Chinese Pangolins at two line transects and one quadrat during the six-month survey ( Table 1). Some of the active burrows from the initial survey were later confirmed by infrared cameras to be habitats for Chinese Ferret-Badger Melogale moschata, Mongoose Herpestes urva, or White-Bellied Rat Niviventer coninga.

Record of the Chinese Pangolin
A Chinese Pangolin was recorded by an infrared camera on 21 December 2017 during the study period, and another image of a Chinese Pangolin was recorded on 21 January 2018 at a different site (23km straight-line distance from the first recording site) during the preparation of this manuscript (Image 2). The identification of these individuals as the Chinese Pangolin Manis pentadactyla was confirmed by notable characteristics, including well-developed external ears with big ear pinna, short heads (neck to snout) covered by small scales, and soft, off-white hair on its underside and face. Their scales are larger than the scales of the Philippine Pangolin Manis culionensis but smaller than that of the Indian Pangolin Manis crassicaudata, and gradually increase in size behind the ears Cota-Larson 2017). While the Chinese Pangolin's geographic range sometimes overlaps with that of the Sunda Pangolin Manis javanica, it can also be distinguished by the scales on its flank or behind its ears. Additionally, there are no historic records of the presence of Sunda Pangolins in this region as well (Challender et al. 2014; IUCN SSC Pangolin Specialist Group 2019).

Demographic characteristics of community survey participants
Out of the 3,041 distributed questionnaires, data were collected from 2,654 anonymous participants (87.3% response rate) in 12 villages. Most of the participants (51.1% male; 48.9% female) were subsistence farmers (59.9%) who raise crops and domestic animals. Other significant groups were migrant workers (20.6%), students (12%) and government employees (2.5%) ( Table 2).

Knowledge and attitude about Chinese Pangolins
About half of the participants (49%) considered the Chinese Pangolin as endangered or critically endangered Image 1. Potential active burrows for Chinese Pangolins at Wuyanling: A-an active burrow excavated within 15 days with fresh soil | Btermites and decayed wood around active burrows. © Zhejiang Wuyanling Natinoal Nature Reserve Management Bureau.

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based on their experience and knowledge and 11% believed that it had become extinct locally, while some participants didn't think the Chinese Pangolin was endangered (21%) or expressed no knowledge of its current status (19%). For those participants who were aware of the Chinese Pangolin, they acquired the information mostly from social media platforms (31.4%), school teaching (30.2%), or television (24.1%), government campaign appeared to be a minor (7.1%) channel to disseminate the relevant information. More than half (58.6%) of the participants recognized the ecological value of Chinese Pangolins, but many still regarded the species as a valuable economic (12.7%), medical (20.5%), and food (6.6%) source, and 21% of the participants stated that they would support the use of pangolins or pangolin products for traditional Chinese medicine.

Pangolin consumption in local community
Majority of the participants who reported having consumed pangolin meat or relevant products (101, 3.8%) in their lifetimes were male (73.3%), subsistence farmers (82.2%), and over 50 years old (97%), which was significantly associated with age (p<0.001), gender (P<0.001), and occupation (p<0.001) ( Table 3). The taste and nutrition (34.1%), perceived medical benefits (25.4%), demonstration of wealth (15.9%), or simply out of curiosity (11.1%) were reported as the reasons of pangolin consumption. Some participants (11.9%) indicated consuming pangolins as a supplemental source of dietary protein a long time ago (the year was not specified). Other participants reported refusing to consume pangolins because of its illegality (39%), the perceived cruelty (38.4%), the cause of population decline (15.9%), or due to its expected bad taste (6.7%).

Community willingness for pangolin conservation
Most participants (95.3%) indicated that they would report pangolin hunting or trading activities to the forestry department's public security staff (61.3%) or the general public security staff (38.7%). Some participants, particularly those between 31-50 years old (p<0.001) regardless of their occupation, reported that they would like to reap the economic benefits of trading pangolins (4.7%). Many participants indicated their willingness to contribute to local pangolin conservation (60%) and  believed that informing the public about the species' protected status would help motivate public action to protect pangolins (60.4%). When asked to provide insights about the specific action that would help protect local Chinese Pangolins, participants emphasized the needs to strengthen law enforcement (21.9%), improve local participation in voluntary work (19.8%), disseminate information (19.7%), refuse to consume pangolin products (19.7%), and actively protect pangolin habitat (16.0%).

DISCUSSIONS
Our camera trap records of the Chinese Pangolin in 2017 and 2018, and the prior record in 2013 in Wuyanling (Zhang et al. 2017) suggest that Wuyanling National Nature Reserve contains a viable habitat for Chinese Pangolins. While samples were not collected for DNA analysis, the distinctive features of the Chinese Pangolin are evident in the video and images captured, confirming its presence (Video 1). Greater efforts needed to conduct initial fieldwork to identify potentially active burrows and increase the coverage of camera traps in Wuyanling region and other sites that are suspected to harbour extant populations of Chinese Pangolins to further understand the populations. In addition, camera traps were positioned at 0.5-1.0 m height in our study based on our experience in mammal surveillance, however, positioning camera traps lower around 30cm above ground may better record Chinese Pangolins and other small mammals in future study (Willcox et al. Table 3. Questionnaire results from local population in Wuyanling region (n = 2,654): consumption of pangolin products and its associations with the age, gender, and occupation.

Pangolin Products Consumption Yes No
Pearson chi-square  2019). We noted the existence of an estimated 5-10 burrow entrances grouped within an area of 300m 2 , suggesting Chinese Pangolins possibly create burrows in a cluster, which needs further study to confirm. Future field surveys should include collection of faeces or scales for DNA analysis, improved surveillance methods (e.g., distance sampling combined with confirmation of burrow occupancy, proper camera setting), and further understanding of the burrow ecology of Chinese Pangolins. With enhanced methodology, similar research can be conducted at other sites in China and across Asia. The characteristics of the habitat in Wuyanling could be used to identify other potential habitats where extant populations may be identified, as well as for the site selection to release confiscated Chinese Pangolins from the authorities in China. DNA testing of confiscated pangolins will be needed to ensure that only native species are released and the IUCN protocols on the appropriate release of animals into the wild would be followed (IUCN/SSC 2013).
The community survey identified male subsistence farmers over 50 years old as the main population in Wuyanling to have had consumed pangolins. The fact that younger population do not report consumption of pangolins (Nash et al. 2016) may be explained by the improved livelihoods over the past 40+ years leading to improved nutrition and reduced dependence on wildlife as an alternate source of protein. Significant social change has also occurred during this time, including the migration of people into cities for work which may have decreased exposure of younger people to the custom of wildlife consumption. The teaching of wildlife conservation principles in schools and opportunities

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for volunteering in conservation work may also contribute to the changing attitude and behaviour towards conservation of Chinese Pangolins. While the time frame of pangolin consumption among Wuyanling residents was not identified in the questionnaire, local knowledge about the current status of Chinese Pangolins as well as the frequent consumption reported by older participants suggest most consumption may have been historic. Further study will be conducted to understand the context of pangolin consumption behaviours to develop evidence-based behavioural change programs.
Our findings demonstrate an overall positive public attitude towards the ecological value of the Chinese Pangolin and its conservation. There is a significant awareness of the illegality of pangolin hunting and consumption in the communities, prompting the communities to report illegal hunting and refuse consumption. Constant education about the illegality of consumption and reinforced conservation needs of Chinese Pangolins via social media, television, and school programs is recommended to keep raising the awareness and motivate action in the communities for pangolin conservation. In addition, the marked community willingness to participate in pangolin conservation work suggests a potential for positive behavioural changes when effective programs implemented. With a remnant viable Chinese Pangolin population present in the wild in mainland China and a potential generational transformation in public perception of its conservation status, we believe there may still be an opportunity to avoid extinction of this Critically Endangered species. www.threatenedtaxa.org The Journal of Threatened Taxa (JoTT) is dedicated to building evidence for conservation globally by publishing peer-reviewed articles online every month at a reasonably rapid rate at www.threatenedtaxa.org. All articles published in JoTT are registered under Creative Commons Attribution 4.0 International License unless otherwise mentioned. JoTT allows allows unrestricted use, reproduction, and distribution of articles in any medium by providing adequate credit to the author(s) and the source of publication.