Knowledge and attitudes about the use of pangolin scale products in Traditional Chinese Medicine (TCM) within China

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2020 The Authors. People and Nature published by John Wiley & Sons Ltd on behalf of British Ecological Society 1Department of Geography, University of Cambridge, Cambridge, UK 2Institute of Zoology, Zoological Society of London, London, UK


| INTRODUC TI ON
Pangolins (Mammalia: Pholidota) are a highly specialised order of mammals covered with scales instead of fur. They feed mostly on ants and termites, and play an important role in tropical and subtropical ecosystems across Asia and Africa by regulating populations of these insects (Cabana et al., 2017;Ofusori & Caxton-Martins, 2008).
Pangolins are recognised as global conservation priorities on the basis of evolutionary history (Collen et al., 2011), and the heavy exploitation of wild pangolin populations has led to the upgrading of IUCN threat category for all pangolin species in 2014: four African species were moved to Vulnerable, two Asian species to Endangered and the other two Asian species to Critically Endangered (IUCN, 2018).
Products involved in the illegal pangolin trade can be grouped into three types: meat, scales and body parts. Pangolin scales account for a large portion of the reported illegal trade. Heinrich et al. (2017) summarised international confiscation reports from 2010 to 2015 and found that more than 55,000 kg of scales was confiscated during this period. If the average weight of scales on one pangolin is around 500 g (Challender & Waterman, 2017;Zhou, Zhao, Zhang, Wang, & Wang, 2012), these data indicate that more than 100,000 pangolins were trafficked from 2010 to 2015. China has been identified as one of the major demand countries, and Traditional Chinese Medicine (hereafter TCM) has been shown to be linked with illegal trade in pangolin scales through illegal products found in markets and shops (Xu, Guan, Lau, & Xiao, 2016;Yin, Meng, Xu, & Liu, 2015).
Traditional Chinese Medicine dates back more than 5,000 years and is still widely used today in China (Chen & Xie, 1999). In 2016, TCM hospitals and clinics treated 962 million patients in China, and medical services provided through TCM treatment accounted for 15.8% of the total medical service provided in that year (National Health & Family Planning Commission of the PRC, 2017; Tang, Liu, & Ma, 2008). The use of pangolin scales in TCM can be traced back to AD 480 when prescriptions containing this ingredient were documented in the Bencao jing jizhu, which was later cited in the famous Compendium of Materia Medica (Li, 1578).
In addition to illegal pangolin products found in TCM markets, a legal market for pangolin scale medicine also exists to support TCM use in China (Xing et al., 2020). Regulations specify that: (a) pangolin scales can be legally traded for medicinal purposes by 711 certified hospitals in China; (b) the quantities of scales that can be traded every year are regulated through a quota system assigned by the Forestry and Grassland Administration at different administrative levels; (c) certification is required to trade and farm pangolins or pangolin products, and manufacture pangolin products; before 2017, importation of African pangolins and their products was still allowed with appropriate certification, but thereafter all pangolin species were included in CITES Appendix I at CoP17 (Johannesburg, 2016) and importation was banned; (d) products from legal pangolin farms can be traded if relevant certification is issued. However, there is no evidence of successful commercial farming to date (Hua et al., 2015;Hu, 2016;Li, 2017).
The only legal source of pangolin scales in the current TCM market in China is therefore the quota assigned by the Chinese government.
The pangolin scale quota system started in China in 2008. Sources of pangolin scales assigned in the quota included private-held or government-held stockpiles. Data on quotas assigned to the market are publicly available for the period 2008-2015. These data show that a total of 186,067 kg of pangolin scales were released to trade, with a mean annual quota of 26,581 ± 1,580 kg. [Corrections added on 7 November 2020, after first online publication: this sentence has been amended to reflect the correct average annual quota amounts].
The legal pangolin scale market is therefore of considerable size and requires similar levels of conservation attention to that focused on the general illegal scale trade. Even though large quantities of pangolin scales have been traded legally or illegally for TCM use, little attention has been paid to research in this area. This is particularly the case for TCM practitioners, who are key stakeholders in the pangolin scale trade since they are directly involved in using scale products and are important in making medical decisions (Bennett, Smith, & Irwin, 1999).
The few existing studies of pangolin scale trade have focused only on the presence/absence of illegal scale trade or analysing illegal trade reports, which revealed important findings such as the widespread availability of illegal products in TCM markets and key transit cities along illegal trading routes (Cheng, Xing, & Bonebrake, 2017;Xu et al., 2016;Yin et al., 2015). However, knowledge and attitudes of TCM practitioners about pangolin scale medicines are also crucial for regulating pangolin scale trade, since this stakeholder group has the potential to influence consumer behaviours and decide or guide consumption (Doughty et al., 2019;Tan & Freathy, 2011).
Based on these key gaps in the knowledge of the pangolin trade, we aim to provide new insights into how TCM practitioners and other TCM-related stakeholders (sellers and the general public) in two provinces in China understand and view this trade. We hypothesise that practitioners and other key stakeholders may not fully understand the legality and conservation impacts of pangolin trade, which might influence their attitude and consequently their behaviour. The insights gained through this approach should enable more effective identification of possible interventions that can provide essential information for TCM-related stakeholders to support effective pangolin conservation and better control of legal scale trade. Interviews with TCM practitioners/sellers were conducted face to face in Mandarin by the lead author. We accessed doctors in both Henan and Hainan, and wholesalers and TCM shops in Henan through social connections, primarily through introduction of potential respondents by friends or family members. We tried to reach as many of these respondents as possible within the research time period with no set sample size. We accessed pharmaceutical shops in Hainan through cluster sampling, which involved use of an online map (Baidu Map, similar to Google Map) to identify areas within each county where pharmaceutical shops were concentrated, and then conducted interviews in all shops in those areas. We aimed to survey 30 shops per county or all shops present in town centres. Shops that were found not to sell TCM products were removed from analysis.
Public surveys in Henan were conducted using online snowball sampling, and questionnaires were sent out through social connections in Kaifeng and Zhengzhou using online social media including WeChat and QQ. The target sample size for each municipality was Qualitative data were analysed using content analysis (Newing, Eagle, Puri, & Watson, 2010). Responses to open-ended questions were coded according to response type, codes were grouped into categories that formed clusters and cluster patterns were identified to describe the target groups. Maps used in this study were plotted using QGIS (QGIS Development Team, 2019).

| TCM practitioners and sellers
The medicinal value of pangolin scales was supported by most respondents working in hospitals (97.6%). In the 41 hospitals surveyed, only one doctor expressed uncertainty about the medicinal value of pangolin scales. However, the hospital in which this doctor worked also sold pangolin scales. Most doctors also showed a good understanding of the medicinal use of pangolin scales in TCM. Doctors from 31 hospitals (75.6%) listed specific symptoms that could be treated with prescriptions containing pangolin scales. These symptoms can be grouped into six categories ( illegal to sell pangolin scales, but a lot of shops ran a hidden trade.
In terms of their medicinal value, the wholesaler from Zhengzhou believed that pangolin scales could not be substituted because they were very effective even in small dosages, especially when treating tumours and liver diseases. One wholesaler and two shop owners also mentioned the widespread counterfeiting of pangolin scales in markets, including the use of fake scales made of pig or goat hoof, smoking scales with chemicals to increase their weight and including pangolin nails within scale products.

| General public
The general public in Henan and Hainan generally showed little knowledge of the pangolin trade. When asked about their knowledge of pangolins, only 7.2% of respondents from Hainan and 16.9% from Henan mentioned the medicinal value of pangolins.
Although most respondents in both provinces did not support trade in any pangolin products, respondents from both provinces were significantly more supportive of the trade of pangolin medicine products compared to trade for food or ornaments (z-test, p < 0.01; Figure 2).  Figure 3). However, 44% (Hainan) and 59% (Henan) of respondents did not know the source of these products, and only 4%-10% correctly understood that all pangolin products were wildsourced ( Figure 4). were also more likely to support trade, but this result was not statistically significant. Freelancers were more likely not to support the trade, but this was also not statistically significant. Hainan model results (Table 4) show that older respondents, respondents with previous experience of consuming pangolins, respondents who thought pangolin scale medicines were legal and respondents who thought pangolin products originated from farms or who did not know their origin were significantly more likely to support trade.

| D ISCUSS I ON
Our study shows that most TCM practitioners in sampled hospitals and pharmaceutical shops across two Chinese provinces believe pangolin scales have high medicinal value. We also confirm the important role that these TCM practitioners, rather than end consumers, play in deciding consumption of medicinal pangolin scale products. Few patients questioned the use of pangolin scales in prescriptions, and if so, they asked for substitutes due to the relatively high price of scales rather than for conservation reasons. These find- Without this knowledge, these important decision makers will not be able to make informed choices to avoid or refuse illegal products.
The results from our public survey revealed that the sampled general public has little understanding of the source of pangolin products ( Figure 4). Many respondents did not know where these products came from, while some believed that pangolin products were obtained from farmed animals. Awareness of the source of pangolin products was also found to be an influential factor that correlated with people's attitude towards the trade in our regression model for Hainan (Table 4). This finding further highlights the need for targeted education on the source of pangolin products, which may alter people's attitude towards pangolin products and their subsequent behaviours. Moreover, without understanding that pangolin products are all wild-sourced and threaten the survival of wild pangolin populations, the causal relationship between products sold in markets and conservation of threatened wild pangolins will not be appreciated.
Our models show that awareness of the legality of pangolin products was the strongest factor influencing people's supportiveness towards pangolin medicine in both provinces, as suggested by the highest standardised coefficient in our regression models  (Tables 3 and 4). This finding suggests that improving conservation awareness around legality of the trade might produce a more uniform and stronger positive impact on reducing demand for illegal pangolin products compared to other educational topics, such as awareness raising about wild pangolin population status, since other such factors have a weaker effect or are not significant in our regression models. Improving awareness of legality is also highlighted as an important activity by the lack of evidence in our study to suggest that the public can differentiate accurately between legal versus illegal pangolin scale products. Indeed, the opposite conclusion is indirectly supported by our observation that end sellers, who are often the key decision makers for pangolin scale consumption, lacked knowledge on relevant regulations.
More positively, our study shows the feasibility of encouraging TCM practitioners to use substitutes to replace pangolin scales.
More than 70% of doctors that we interviewed agreed that at least some current use of pangolin scales in TCM could be substituted by other ingredients. This finding is supported by previous studies that compared the medicinal effect of pangolin scales with other TCM ingredients such as pig hoof and different plant products (Burgess, Olmedo, Veríssimo, & Waterman, 2020;Ge, Tong, Qin, Li, & Gao, 2009;Li, Zhao, Chen, & Hou, 2008;Xing et al., 2020;Zhang, Tong, Gao, & Li, 2009). Most of the potential substitutes are from domesticated or cultivated species and are thus unlikely to be of conservation concern. However, there is still a need to evaluate the potential impacts to wild populations if the demand for substitutes is likely to increase (Phelps, Carrasco, & Webb, 2014).
Traditional Chinese Medicine communities could switch to other more sustainable substitutes if sufficiently motivated. One motivation for TCM doctors to use substitutes for pangolin scales could be caring for the well-being of their patients. Since the quality of illegal or counterfeit products cannot be guaranteed, the fact that illegal and counterfeit pangolin scale products are widespread in markets could therefore help motivate TCM practitioners to reconsider their choice of prescription (Xu et al., 2016;Yin et al., 2015). Two recent changes in policy might promote practitioners to actively consider using substitutes for pangolin scales if they are made aware of these changes.
Firstly, the National Healthcare Security Administration and the (2019)  Finally, it is important to recognise some limitations of this study.

Ministry of Human Resources and Social Security
The failure of snowball online surveying in Hainan led to our use of different sampling methods in the two study provinces. In addition to differences in knowledge of pangolin population status and source of products between the two regression models, the Henan model highlighted female respondents and respondents working as professionals or civil servants whereas the Hainan model highlighted older respondents as more likely to support trade. Although these province-level differences suggest that conservation campaigns might need to be regionally modified to accommodate local variation (Olmedo, Sharif, & Milner-Gulland, 2018;Wallen & Daut, 2018), they might also be due to our different sampling methods rather than underlying regional differences in attitudes and awareness. Secondly, only certain administrative regions in each province were surveyed, and our sample size is inevitably low compared to the total population living in each region. For reference, the population of Kaifeng is 2 million, the population of Zhengzhou is 7 million and the population of Baisha (the least populous region included in our study) is 30,000. Assessing the representativeness of the patterns seen in our study across wider demographic and geographical scales therefore needs further validation. Thirdly, although knowledge and attitudes of direct consumers are important to understand for trade regulation, individuals belonging to this stakeholder group are hard to pinpoint and underreporting is common in self-reporting surveys such as ours (Krumpal, 2013). This study therefore represents an assessment of people who currently support the pangolin TCM trade, rather than those who specifically report past experience of consuming pangolins. However, it is possible that factors influencing support towards trade may differ from those influencing actual consumption of products. To be successful at effecting behaviour change, campaigns that aim to change consumption may therefore need to be based on further evidence.
Moreover, only two wholesalers were interviewed, one from each wholesale market. Although these respondents showed a good understanding of the wholesale market they worked in, a greater sample size is definitely required to understand knowledge and attitudes of this stakeholder group.
Despite the potential caveats of the study, our results sug- These guidelines could include how to identify and report illegal products, how to identify pangolin scale ingredients in prescriptions and the importance and feasibility of actively consulting TCM practitioners for potential substitutes. Audience segmentation is preferred for public campaigns when possible, and our results suggest more localised segmentation might be needed. Thirdly, the TCM community should be recognised as a key stakeholder in pangolin trade and become more closely integrated into pangolin conservation activities. The role of TCM practitioners as healthcare professionals could help to reduce excessive and illegal demand not only on pangolins but potentially also on many other wildlife products. Therefore, we strongly urge that the TCM community should become more heavily involved in future efforts to conserve pangolins and other wildlife threatened by unsustainable medicinal trade. Nature Reserve for helping with public surveys in Hainan. We give special thanks to all anonymous respondents who participated in surveys and people who helped with social network access to respondents, and we also thank Dr Dan Challender for help with project development.

CO N FLI C T O F I NTE R E S T
Authors have no conflict of interest to declare.

AUTH O R S ' CO NTR I B UTI O N S
All authors contributed to conceiving the ideas and designing methodology; Y.W. collected and analysed the data and led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.

DATA AVA I L A B I L I T Y S TAT E M E N T
Raw data from survey and interview will not be shared publicly due to ethics requirement. Authors archived the synthesised data and r code through Zenodo at https://doi.org/10.5281/zenodo.3841995 (Wang, 2020).