Attitudes Toward Bile Extraction from Living Bears: Survey of Citizens and Students in Beijing

Journal of Applied Animal Welfare Science

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Attitudes Toward Bile Extraction From Living Bears: Survey of Citizens and Students in Beijing

Zhao Liu, Zhigang Jiang, Aifang Yang, Bingbing Xu, Hongxia Fang, Zongping Xie, Ning Li, Chunwang Li, Zhibin Meng & Yan Zeng

To cite this article: Zhao Liu, Zhigang Jiang, Aifang Yang, Bingbing Xu, Hongxia Fang, Zongping Xie, Ning Li, Chunwang Li, Zhibin Meng & Yan Zeng (2017) Attitudes Toward Bile Extraction From Living Bears: Survey of Citizens and Students in Beijing, Journal of Applied Animal Welfare Science, 20:3, 205-218, DOI: 10.1080/10888705.2017.1283990 To link to this article: http://dx.doi.org/10.1080/10888705.2017.1283990

Published online: 15 Feb 2017.

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Download by: [124.152.84.67] Date: 04 June 2017, At: 02:48 JOURNAL OF APPLIED ANIMAL WELFARE SCIENCE 2017, VOL. 20, NO. 3, 205–218 http://dx.doi.org/10.1080/10888705.2017.1283990

ARTICLES Attitudes Toward Bile Extraction From Living Bears: Survey of Citizens and Students in Beijing Zhao Liua,b,c, Zhigang Jiangb,c,d, Aifang Yanga, Bingbing Xub, Hongxia Fangb, Zongping Xiea, Ning Lie, Chunwang Lib, Zhibin Mengb,d, and Yan Zengb,d aCollege of Agriculture and Biotechnology, Hexi University, Zhangye, Gansu, China; bKey Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China; cUniversity of Chinese Academy of Sciences, Beijing, China; dEndangered Species Scientific Commission of China, Beijing, China; eSchool of Life Science, Nanjing University, Nanjing, Jiangsu, China

ABSTRACT KEYWORDS Bear bile is a traditional Chinese medicine that has been used for millennia. Bear bile; bear farming; bile Several arguments support and oppose the use of bear farming in terms of extraction from living bears; conservation and nonhuman animal welfare. This study involved designing a animal welfare and rights; questionnaire and surveying a random sample of general citizens and college public attitudes students in Beijing to elicit their attitudes on bile extraction from living bears. Older people and people with lower education levels used more bear bile medicines. In total, 29.47% (n = 204) of citizens and 23.14% (n = 81) of students surveyed used bear bile medicine since 1990. Students were less willing to use bear bile medicines than citizens (p < .05). The level the respondents agreed with the blue side (against the extraction of bile from living bears; anti for short) was significantly higher than that for the red side (support the extraction of bile p

from living bears; pro for short; < .05). Additionally, college students had a more distinct attitude toward the opposing views, which indicates they were more inclined to oppose bile extraction from living bears.

Bear bile is a traditional Chinese medicine (TCM) and is principally made from the material extracted from the gallbladder of Asiatic black bears (Ursus thibetanus) and Eurasian brown bears (Ursus arctos; Chinese Pharmacopoeia Commission [CPC], 1977; Cooperative Group of Chinese Medicinal Animal Records, 1979; Ding, 1998). The only source of bear bile for a substantial period of time was from Asiatic black bears in the wild (Hu & Hu, 1998; International Union for Conservation of Nature [IUCN], 2013; Servheen, 1999). To satisfy the demand of 3 tons of bear bile per year before the 1970s, 10,000 Asiatic black bears were hunted and killed annually (Hu & Hu, 1998). From 1985 to 1989 (the early period of the bear-farming industry prior to the establishment of China’s Wildlife Protection Law), Asiatic black bears used for bile extraction were mainly captured from the wild (Fan & Song, 1997; IUCN, 2013). The traditional method of hunting wild bears for their gallbladders undoubtedly substantially damaged wild bear populations (Bi, 1988; Ma, Hu, & Zhai, 1994; Mills & Servheen, 1991). Asiatic black bears and Eurasian brown bears are listed as Class II national protected nonhuman animals and were listed in Appendix I of CITES in 1992 (CITES, 2013). The major threat to bears in China and Southeast Asia is the commercial trade of live wild bears and bear parts, notably gallbladders and bile (IUCN, 2013; Mills, 1995; Phillips & Wilson, 2002). Given this situation, bear farming was introduced, as it was thought to be an effective way to address the demand for bear bile (Li, Zhu, But, & Yeung, 1995). Bear farming and the technique of extracting bile from living bears were first introduced in China in 1984 and originated from North Korea (Fan,

CONTACT Zhao Liu [email protected] Building 5 No. 1 Courtyard, Beichen West Road, Chaoyang District, Beijing 100101, China; Zhigang Jiang [email protected] Institute of Zoology, Chinese Academy of Sciences, Building 5 No. 1 Courtyard, Beichen West Road, Chaoyang District, Beijing 100101. © 2017 Taylor & Francis Group, LLC 206 LIU ET AL.

2000; Fan & Song, 1997). Four hundred wild Asiatic black bears can be saved from being hunted when the bile from one farmed bear is extracted once a day for 10 years (Fan, 2000). China consumes 3 tons to 4 tons of farmed bear bile annually (Loeffler, Robinson, & Cochrane, 2009). Driven by potential economic interest, small bear farms began to appear in large numbers. However, because of bile extraction techniques and the lack of appropriate husbandry and management, the living conditions experienced by bears on farms were found to be extremely poor (Loeffler et al., 2009; Phillips & Wilson, 2002). Given this situation, the Chinese government implemented measures to standardize the management of bears in bear farming (Fan & Song, 1997; Feng et al., 2009). Regulations to inspect and address conditions of bear farms were stipulated by the Ministry of Forestry in 1993. These regulations also prohibit the capture of wild bears, stop the issuance of domestication licenses to new bear-raising farms, and shut down bear farms that seriously abuse bears or fail to comply with regulations. In 1996, the Ministry of Forestry of China announced that the husbandry and management of bears on farms must be improved, any behavior that could hurt or abuse bears must be prohibited, and only the free drip fistula method would be allowed (Fan & Song, 1997). In 2001, additional health products made from bear bile powder were not approved in China, and in 2005, regulations on the usage of bear bile in Chinese medicines were stipulated by the Chinese government (Feng et al., 2009). In 1997 and in 2008, the Ministry of Forestry stipulated technical regulations on bear farming to further improve the husbandry and welfare of the farmed bears in China. As of April 2010, the estimated number of bear farms in China had dropped from 480 farms to 97 farms in operation housing 7,000 to 10,000 bears, and the farms were considered more standardized (Meng, Huang, & Li, 2007). As a result of government regulations being implemented to address management of bear farms (Loeffler et al., 2009), the government of China alleged that public concerns about the welfare of bears on farms had basically been addressed (Fan, 2006). Effective

implementation of such legislation also requires government oversight and scientific research on the physical and psychological health of the bears for the assessment and monitoring of their welfare (Loeffler et al., 2009; Malcolm et al., 2013) Since the 1980s, consumers have had the options of illegal wild gall bladders; bile extracted from caged, live bears; or the chemically synthesized acid. Strong objections have been voiced against farming bears to collect their bile (Fan, 2001; International Fund for Animal Welfare, 1994; Mills & Servheen, 1991).Oneoftheprimaryargumentsfromthe“anti” view is that bear farms will inevitably cause severe pressure on wild bear populations due to continuous capture of bears to maintain or stock bear farms. Secondly, serious nonhuman animal welfare issues are caused by extracting bile from living bears (Fan, 2001). Recently, studies have shown that bear farming failed to protect wild bear populations in the early period of the bear-farming industry (Dutton, Hepburn, & Macdonald, 2011;Fengetal.,2009). Respect for the welfare of individual bears is reduced because these farming practices have placed bears in harsher conditions (Dutton et al., 2011;Fengetal.,2009). From a bioethical perspective, each species has the right to live, which is an intrinsic value irrelevant to the needs of humans (Naess, 1985; Norton, 2008). But from the perspective of interpersonal ethics, granting rights to nonhuman species is difficult (Lei, 2001). Whether we should grant the identical moral concern for nonhuman animals is an ethical debate (Lei, 2001; Rolston, 1988; Singer, 1990). Disputes about extracting bile from living bears involve conservation biology, economics, ethics, and animal welfare (Primack, 1993; Rolston, 1988). Conservation policy cannot be removed from the social and political environment in which the policy is implemented (Kirkpatrick & Emerton, 2010). The usage of bear bile was described in the earliest official pharmacopoeia of TCM in AD 659, and the current dispute about extracting bile is a problem of history, culture, and economy (Dutton et al., 2011; Feng et al., 2009). This practice has already become an important animal welfare issue and is gaining increasing attention in mainstream Chinese society (Feng et al., 2009; Meng et al., 2012). ATTITUDES TOWARD BILE EXTRACTION FROM LIVING BEARS 207

A relevant question is what are the public’s views and attitudes toward bile extraction from living bears? We conducted a social investigation of both citizens and college students living in Beijing, China.

Materials and methods This study was performed from January 2012 to March 2012 in Beijing. A stratified survey design was chosen to randomly select neighborhood committees and neighborhoods from a sample frame in Beijing in 2012. A random sample was then taken according to a random number table or using draw lots (Kish, 1987). A neighborhood committee is a formal organizational tier of local governance nested within a municipality (Gratwicke et al., 2008). Once a sample household was identified, face- to-face interviews were conducted at home with randomly selected household members who were 18 years or older and who had lived in Beijing for at least 1 year. The interviewers also obtained the accommodation information for students from the dormitory management committees, and the interviewers then randomly sampled the dormitories and students. All data collected through this study remained anonymous and confidential. Lastly, respondents were given a small gift to thank them for their participation (Dutton et al., 2011; Gratwicke et al., 2008). We designed attitude scale questions to determine the public’s attitude toward two opposing views on bile extraction from living bears. We list the opposing views on bile extraction from living bears in Table 1. The two opposing groups of views were named the red side (support bile extraction from living bears; pro for short) and blue side (against bile extraction from living bears; anti for short). The 7-point Likert scale was employed as a data collection instrument for the attitude questions. Seven points from 1 to 7 represented the following: completely disagree (1), somewhat disagree (2), slightly disagree (3), neutral (4), slightly agree (5), somewhat agree (6), and completely agree (7; Schiffman & Kanuk, 2004). At the end of this section of the questionnaire, respondents were asked to provide their attitudes toward bile extraction from living bears by taking the standpoints of the Asiatic black bears, humans, and

Table 1. Arguments for and against bile extraction from living bears. Argument no.a Blue side (anti) Red side (pro) 1 Black bears have rights to life, while a human has no Farmed black bears are humans’ assets, so humans right to extract bile from a living bear. have the right to extract bile from living bears. 2 Extracting bear bile from living bears is cruel and Bear bile is used for medicinal purposes, so extracting unacceptable. bear bile from live bears is acceptable. 3 Extracting bear bile causes pain to black bears; thus, they Farmed bears are just like domestic animals, so deserve sympathy. extracting bear bile from live bears is reasonable. 4 Extracting bear bile has not only seriously traumatized Black bears are not an ethical object to humans, so bears’ lives and health, but it is also obviously against there is no problem of morals regarding extracting bear ethics and morality. bile from living bears. 5 Farmed-source bear bile will stimulate consumer Farmed-source bear bile has the capacity to meet demand and profit from wild black bears, which also market demand and can undercut the demand for wild- encourages poaching. sourced bear bile and poaching. 6 We should legislate to ban extracting bear bile from We should legislate to improve the welfare of farmed living bears and remove the bear bile from TCM. black bears without banning bear bile extraction from living bears. 7 We should refuse to use bear bile products. If there is a need, we can use bear bile products. 8 We should use the substitutes for bear bile. If farmed-source bear bile has the capacity to meet the demand, we do not necessarily have to use the substitutes. Note. TCM = traditional Chinese medicine. aWe designed eight opposing views supportive of or against bile extraction from living bears and named the two opposite groups of views the blue side (against bile extraction from living bears; anti for short) and the red side (support bile extraction from living bears; pro for short). The 7-point Likert scale was employed as a data collection instrument for public attitude toward those arguments. Seven points from 1 to 7 represented the following: completely disagree (1), somewhat disagree (2), slightly disagree (3), neutral (4), slightly agree (5), somewhat agree (6), and completely agree (7). 208 LIU ET AL. themselves. The 7 points from 1 to 7 represented the following: completely agree (1), somewhat agree (2), slightly agree (3), neutral (4), slightly disagree (5), somewhat disagree (6), and completely disagree (7).

Data analysis Statistical analyses were used to study the information collected from the questionnaire. If the data were ranked, then a Wilcoxon test for two related samples and a Mann-Whitney U test for two independent samples were used. A Kruskal-Wallis H Test was used for several independent samples, and a Friedman test was used to test several related samples. The paired-samples t test, independent- samples t test, and one-way analysis of variance (ANOVA) were used for normally distributed data. A binary logistic regression model was used to estimate the relationship between the demographic variables and the use of bear bile medicines. A Pearson’s chi-square test was used to test the cross- tables data. We also established curvilinear regression models for the frequency of bear bile medicine use by the respondents (Quinn & Keough, 2002). The Statistical Package for the Social Sciences Version 17.0 and Matrix Laboratory (MATLAB) R2009b were used for the statistical analysis and to produce the statistical graphs. We collected demographic information from respondents in the first part of the questionnaire (de Vaus, 2002). These demographics included age, gender, education level, monthly income level, place of origin, and urban or rural origin.Gendersweremaleandfemale.Agegroups included 18 to 24 years, 25 to 34 years, 35 to 44 years, 45 to 59 years, and older than 60 years old. Education levels included junior high school and lower, senior high school/technical secondary school, college diploma, bachelor’s degree, and master’s degree and greater. Monthly income was divided into the following groups: 0, less than 2,000 yuan, 2,000 to 4,000 yuan, 4,000 to 6,000 yuan, 6,000 to 8,000 yuan, 8,000 to 10,000 yuan, and more than 10,000 yuan. Places of origin were classified into six regions: Northeast China, Eastern China, Beijing, Northern China, Western China, and Central-Southern China. Origins included whether the region was urban or rural. We analyzed demographic data from the citizens, not inclusive of college students. We investigated the consumption of 62 types of bear bile medicines from Chinese Pharmacopoeia (CPC, 1979), the State Food and Drug Administration’s drug database (http://app1.sfda.gov.cn/datasearch/face3/ base.jsp), and the Yaozh’s database (http://db.yaozh.com). The investigated contents mainly included the medicine used, scores indicating the curative effects of each medicine used, and the willingness of the respondent to reuse the medicine.

Results Influence of demographics on consumption of bear bile medicine We conducted a questionnaire survey among 692 citizens and 350 college students in Beijing from January 2012 to March 2012. In total, 82.92% (n = 864) of the collected questionnaires were valid (excluding incomplete or incorrectly completed questionnaires). There were significant differences in the number of bear bile medicines used by the citizens among different age groups (Kruskal- Wallis H, χ2 = 13.7, p <.01) and different education levels (Kruskal-Wallis H, χ2 = 19.9, p < .01). A binary logistic regression analysis showed that the model was statistically significant (χ2 = 27.50, df = 14, p < .01). The regression coefficients for age and education level were .18 and –.26, respectively, indicating a significant influence on the use of bear bile medicine (p < .05; Table 2). Older people and people with lower education levels used more bear bile medicines. Education level was negatively correlated with age (r = –.28, p < .01), indicating a mild autocorrelation between the two variables in the model. The other variables had no significant influence on the use of bear bile medicine (p > .05). ATTITUDES TOWARD BILE EXTRACTION FROM LIVING BEARS 209

Table 2. Binary logistic model used to estimate relationship between demographic variables and use of bear bile medicine. Variable Coefficient SE Wald p value Variable Coefficient SE Wald p value Sex 0.107 .177 0.368 .544 Northeast China 0.603 .427 1.993 .158 Age 0.182 .073 6.153 .013 Eastern China 0.357 .404 0.781 .377 Education level –0.260 .088 8.640 .003 Central-Southern China 0.424 .416 1.041 .308 Monthly income 0.154 .079 3.856 .050 Rural –0.239 .189 1.591 .207 Beijing 0.083 .397 0.044 .834 Intercept –1.503 .630 5.683 .017 Northern China 0.349 .390 0.801 .371 Note. AIC = 818.581; Correct no. = 98.6%; Correct = 6.3%; Total correct = 70.8%; Cutoff = 0.5.

Consumption and use of bear bile medicine In total, 29.47% (n = 204) of citizens and 23.14% (n = 90) of students had used bear bile medicines since 1990. The per-capita bile use of citizens (0.55 ± 0.04) was significantly greater than that of students (0.42 ± 0.05; Z = –2.279, p < .05). The top 10 most frequently used medicines in each subject group are listed in Table 3. In the top 20 most frequently used medicines, citizens (2.15 ± 0.41%) used bear bile medicines with a significantly higher frequency than students (1.84 ± 3.66%; paired-sample t test, t = 2.33, df = 19, p < .05). The number of different bear bile medicines used by the respondents (x) and ratio of respondents who used this number of medicines (y) was fitted with an exponential function model, indicating that most respondents did not use bear bile medicines, and the ratio of respondents who used this number of bear bile medicines decreased with the increasing number of bear bile medicines used by the respondents (Table 4). The survey results showed that the major purpose for using bear bile medicines was for the treatment of diseases compared with using it for preventive health care (citizens, 79.37%; students, 69.39%; see Table 5). Both groups of respondents rated the curative effects of bear bile medicine higher than 4.5, indicating those medicines were “slightly effective” to “somewhat effective.” Students provided a significantly lower score for both the “curative effects” and “willingness to reuse” compared with citizens (curative effects, Z = –2.74, p <

.01; willingness to reuse, Z = –2.20, p < .05). Students were unwilling to use bear bile medicines because their

Table 3. Top 10 most frequently used bear bile medicines by citizens or students. %of %of respondents Used by Functions and respondents Rank Used by citizens Functions and indications who use students indications who use 1 Xiong dan chuan Clearing heat and 7.23 Feng re qing Clearing heat and 7.14 bei kou fu ye relieving cough kou fu ye resolving phlegm 2 Feng re qing kou Clearing heat and 6.94 Xiong dan yan Removing nebula for 4.29 fu ye resolving phlegm yao shui improving eyesight 3 Hou yan wan Relieving throat 3.61 Xiong dan Clearing heat and 3.43 inflammation chuan bei kou relieving cough fu ye 4 Xiong dan yan Removing nebula for 3.03 Hou yan wan Relieving throat 3.43 yao shui improving eyesight inflammation 5 Fu fang xiong Removing nebula for 2.46 Qing laing yan Diminishing 2.57 dan di yan ye improving eyesight yao gao inflammation and bacteriostasis 6 Xiong dan jiu Soothing liver/gallbladder 2.46 Fu fang xiong Removing nebula for 1.71 dan di yan ye improving eyesight 7 Xiong dan die da Reducing rheumatism 2.17 Xiong dan die Reducing rheumatism 1.71 gao da gao 8 Fu fang xiong Relieving throat 1.88 Xiong dan jiu Soothing liver/ 1.71 dan bo he han inflammation gallbladder pian 9 Xiong dan wan Clearing heat and 1.73 Te ling yan yao Reducing inflammation 1.43 removing nebula and improving eyesight 10 Xiong dan jiao Clearing heat, relieving 1.45 Xiong dan wan Clearing heat and 1.14 nang pain, and removing removing nebula nebula 210 LIU ET AL.

Table 4. Regression model for number of different bear bile medicines used by the respondents (x) against the ratio of respondents who used this number of medicines (y). 2 Subjects Model type kR SEE AIC ymax,x Citizens Exponential 4 .9998 8.03E-05 –134.97 0.699, 0 Students Exponential 4 .9986 7.18E-04 –76.92 0.769, 0

Table 5. Comparison of consumption of bear bile medicines. Purpose Mann-Whitney U Used for Used for preventive Usage Curative Willingness to Curative effects versus Subject treatment health care quantity effects reuse willingness to reuse Citizens 79.37% 20.63% 0.55 ± 0.04 4.85 ± 0.06 4.25 ± 0.09 Z = –3.51, p < .01 Students 69.39% 30.61% 0.42 ± 0.04 4.56 ± 0.10 3.95 ± 0.12 Z = –3.82, p < .01

scores for “willingness to reuse” (3.95 ± 0.12) were lower than the neutral level (Point 4; Table 5). Both the students’ and citizens’ scores for the “willingness to reuse” were significantly lower than those for “curative effects” (students, Z = –3.51, p < .01; citizens, Z = –3.82, p <.01).

Balance between differing views on bile extraction from living bears The survey showed that 46.53% (n = 322) of citizens and 53.71% (n = 188) of students had heard of “bile extraction from living bears.” If respondents had not heard about bile extraction, a brief explanation of the background of bile extraction was provided in the questionnaire, including how bile is extracted from living bears and information related to the free drip fistula method. A

Wilcoxon test showed that the level of agreement among the respondents about each of the eight views of the blue side (anti) was significantly higher than that of the red side (pro; citizens, Z = – 45.62, p < .01; students, Z = –38.62, p < .01). A Mann-Whitney U test showed that except for Argument 6, the level of agreement among students with the blue side (anti) was higher than that among citizens (Z = –10.17, p < .01). The level of agreement among students with each of the views on the red side (pro) was significantly lower than that of citizens (Z = –10.83, p < .01; Table 6). The study showed that both citizens (2.95 ± 0.07) and students (2.56 ± 0.08) disagreed with bile extraction from living bears. Additionally, the level of agreement among students was significantly lower than that among citizens (Z = –2.78, p < .01). A one-way ANOVA indicated a significant difference among citizens’ or students’ selection frequencies of different attitude scales toward the blue side (anti) or the red side (pro) (blue-side citizens, F = 132.445, df1 =6,df2 = 21.410, p < .01; red-side citizens, F = 26.377, df1 =6,df2 = 27.632, p < .01; blue-side students, F = 106.253, df1 =6,df2 = 22.722, p < .01; red-side students, F = 19.847, df1 =6,df2 = 34.229, p < .01). The attitude scales with the highest frequency of selection were the following: Attitude Scales 6 and 7 (somewhat agree and completely agree) for blue-side (anti) citizens (p < .01) and Attitude Scale 2 (somewhat disagree) for red-side (pro) citizens (p < .01); Attitude Scale 7 (completely agree) for blue-side (anti) students (p < .01) and Attitude Scales 1 and 2 (completely disagree and somewhat disagree) for red-side (pro) students (p < .01; Figure 1). A paired-samples t test showed that the range value of the respondents’ selection frequency of different attitude scales toward the blue-side (anti) views was significantly higher than that of the red side (pro) (citizens, t = 4.375, p < .01; students, t = 6.271, p < .01), showing that the variation in selection of the blue side (anti) was greater than that of the red side (pro). Namely, those respondents had a more flexible attitude toward the blue side (anti) than the red side (pro). Statistical analyses showed that the standard deviations of the agreement with the red side (pro) were significantly higher than those with the blue side (anti; p < .01), indicating a greater degree of dispersion on the red side (pro) than the blue side (anti). The kurtosis (a measure of the

Table 6. Comparison of the mean ± (SE) attitudes scales toward arguments for and against the bile extraction from living bears. Citizens Students Citizens versus students

Arguments Blue side Red side Blue versus red Blue side Red side Blue versus red Blue side Red side BEARS LIVING FROM EXTRACTION BILE TOWARD ATTITUDES 1 6.04 ± 0.05 3.18 ± 0.07 Z = –19.19, p < .01 6.22 ± 0.06 2.68 ± 0.08 Z = –14.94, p < .01 Z = –2.72, p < .01 Z = –4.15, p < .01 2 5.86 ± 0.05 3.35 ± 0.07 Z = –17.51, p < .01 6.09 ± 0.07 2.88 ± 0.09 Z = –14.16, p < .01 Z = –3.61, p < .01 Z = –3.96, p < .01 3 5.91 ± 0.05 3.11 ± 0.06 Z = –19.53, p < .01 6.31 ± 0.05 2.59 ± 0.08 Z = –15.53, p < .01 Z = –5.87, p < .01 Z = –4.79, p < .01 4 5.58 ± 0.06 2.72 ± 0.06 Z = –18.86, p < .01 5.94 ± 0.07 2.15 ± 0.07 Z = –15.20, p < .01 Z = –4.01, p < .05 Z = –5.82, p < .01 5 5.58 ± 0.06 3.90 ± 0.07 Z = –13.32, p < .01 6.05 ± 0.07 3.59 ± 0.10 Z = –12.43, p < .01 Z = –5.73, p < .01 Z = –2.67, p < .01 6 5.41 ± 0.06 3.50 ± 0.07 Z = –14.31, p < .01 5.53 ± 0.08 3.19 ± 0.09 Z = –11.86, p < .01 Z = –1.55, p > .05 Z = –2.52, p < .05 7 5.11 ± 0.06 4.15 ± 0.07 Z = –8.00, p < .01 5.33 ± 0.09 3.93 ± 0.10 Z = –7.91, p < .01 Z = –2.34, p < .05 Z = –2.13, p < .05 8 5.74 ± 0.05 3.67 ± 0.07 Z = –16.17, p < .01 6.05 ± 0.06 2.95 ± 0.08 Z = –14.61, p < .01 Z = –3.60, p < .01 Z = – 5.92, p < .01 Total 5.65 ± 0.02 3.45 ± 0.02 Z = –45.62, p < .01 5.94 ± 0.03 2.99 ± 0.03 Z = –38.62, p < .01 Z = –10.17, p < .01 Z = –10.83, p < .01 211 212 LIU ET AL.

Figure 1. Selection frequencies of different attitude scales (agreement degree) about the blue side’s (anti) or red side’s (pro) views of citizens (a) and students (b) on the extraction of bile from living bears. Different letters show significant differences (p < .05). concentration of a distribution around its mean) representing the agreement with the blue side (anti) was mostly a positive number, whereas the kurtosis with the red side (pro) was mostly a negative number. The kurtosis of the blue side (anti) was significantly greater than that of the red side (pro) (p < .01), indicating a flatter peak for the red side (pro), a sharper peak for the blue side (anti), and more concentrated value distribution for the blue side (anti; Figure 1).

Standard deviations representing citizens’ agreement with the two views were significantly higher than those representing students’ agreement (p < .01), indicating a greater degree of dispersion in the agreement of citizens with the two views than in the agreement of students. The skewness indicating the agreement of citizens with the red side (pro) was significantly lower than that of the students (t = –4.71, p < .01), and the kurtosis indicating the agreement of citizens with the red side (pro) was significantly smaller than that of students (t = –3.98, p < .01), showing that the distribution of the agreement of citizens with the red side (pro) was flatter than that of the agreement of students (Table 7).

Attitudes toward living-bear bile extraction from different standpoints According to our Friedman test, significant differences were noted among the attitudes of citizens or students toward living bear bile extraction based on different standpoints (citizens, χ2 = 539.916, p < .01; students, χ2 = 384.839, p < .01). A Wilcoxon test showed that most respondents believed that bile extraction from living bears was more detrimental when viewed from the standpoint of Asiatic black bears than from their personal standpoint (citizens, t = –13.843, p < .01; students, t = –12.068, p < .01) and that bile extraction from living bears was more detrimental when viewed from their personal standpoint than from the standpoint of humans (citizens, t = –12.234, p < .01; students, t = –9.642, p < .01; Table 8). A Mann-Whitney U test showed that from the standpoint of Asiatic black bears, students held a more negative attitude toward bile extraction from living bears than did citizens (Z = –5.149, p < .01). Our Crosstabs test showed a significant difference among the selection frequencies of citizens and students from different standpoints (citizens, χ2 = 373.814, df = 12, p < .01; students, χ2 = 322.401, df = 12, p < .01). Attitude Scale 7 (completely wrong) was the most selected by citizens and students when they viewed living bear bile extraction from the standpoint of Asiatic black bears or

Table 7. Descriptive statistics of including standard deviations, skewness, and kurtoses of attitude scores toward opposite views. Citizens Students Citizens versus students Standard deviation Skewness Kurtosis Standard deviation Skewness Kurtosis Independent

Arguments Blue Red Blue Red Blue Red Blue Red Blue Red Blue Red Statistics Two sides t test BEARS LIVING FROM EXTRACTION BILE TOWARD ATTITUDES 1 1.28 1.79 –1.74 0.47 2.77 –1.08 1.17 1.53 –1.92 0.71 4.01 –0.44 Standard Blue t = 5.29, p < .01 2 1.37 1.78 –1.51 0.38 1.81 –1.16 1.29 1.62 –1.57 0.57 2.13 –0.62 error Red t = 4.69, p < .01 3 1.23 1.65 –1.61 0.54 2.69 –0.90 0.98 1.43 –1.90 0.75 4.37 –0.18 Skewness Blue side t = 1.14, p > .05 4 1.48 1.61 –1.08 0.97 0.42 –0.03 1.30 1.31 –1.31 1.28 1.42 1.33 Red t = –4.71, p < .01 5 1.57 1.87 –1.21 –0.07 0.56 –1.31 1.36 1.85 –1.59 0.08 1.90 –1.23 Kurtosis Blue side t = –2.11, p > .05 6 1.56 1.85 –0.94 0.33 –0.11 –1.18 1.52 1.74 –0.82 0.39 –0.18 –0.90 Red t = –3.98, p < .01 7 1.68 1.85 –0.63 –0.23 –0.75 –1.25 1.60 1.80 –0.52 –0.22 –0.85 –1.03 8 1.31 1.84 –1.39 0.12 1.63 –1.31 1.07 1.58 –1.18 0.45 1.08 –0.69 Mean 1.43 1.78 –1.26 0.31 1.13 –1.03 1.28 1.61 –1.35 0.50 1.74 –0.47 Standard error .06 .03 .13 .13 .46 .15 .07 .07 .18 .16 .64 .28 Paired t test t = –6.58, p < .01; t = –7.11, p < .01; t = –4.45, p < .01; t = –5.41, p < .01; t = –6.32, p < .01; t = –3.47, p < .05 213 214 LIU ET AL.

Table 8. Comparison of attitudes toward extraction of bile from living bears from different standpoints. Standpoint of Standpoint of a Personal Black bears versus Human versus black bears human standpoint Friedman test χ2 human personal Citizens 6.379 ± 0.038a 4.837 ± 0.063c 5.438 ± 0.058b 539.916, p < .01 Z = –17.601, p < .01 Z = –12.234, p < .01 Students 6.623 ± 0.047d 4.843 ± 0.083c 5.509 ± 0.073b 384.839, p < .01 Z = –13.642, p < .01 Z = –9.642, p < .01 Note. Different letters represent significant differences (p < .05). their personal standpoint. The neutral scale appeared the most frequently when the standpoint of humans was considered (Figure 2).

Discussion Consumption of bear bile products Bear bile is an expensive and uncommonly used TCM (Ding, 1998), and the active ingredient in bile, ursodeoxycholic acid, can be purified from bile collected from slaughterhouses or farms (Dutton et al., 2011; Feng et al., 2009). A nonrandom survey of 50 TCM doctors revealed that a majority (65%) ranked bear bile as an “important though not essential” medicine, and only 8% felt that bear bile was an irreplaceable medicine in China (Mills, 1995). This survey showed that 29.47% (n = 204) of citizens and 23.14% (n = 81) of students claimed to have used bear bile medicines, but the use frequencies of the top 20 most frequently used medicines were low (citizens, 2.15 ± 0.41%; students, 1.84 ± 3.66%), and more than 70% of users claimed that they rarely used bear bile medicine. On this occasion, no special technique was used to encourage an honest answer to these sensitive questions (Dutton et al., 2011; Solomon, Jacobson, Wald, & Gavin, 2007). It is therefore reasonable to surmise that the number of consumption activities was likely to be biased. Older people and people with lower education are more likely to make use of bear bile medicine (Dutton et al., 2011). One reason for this use is that older people are more likely to suffer from diseases and would use TCMs more often for treatment or preventive health care (Gratwicke et al., 2008). We also found that citizens with a higher education level were mainly young people, and the surveyed college students used bear bile products significantly less frequently than did the surveyed citizens (p < .01). Therefore, young people with a higher education level used bear bile products less often.

Figure 2. Selection frequencies of different attitude scales (agreement degree) toward the extraction of bile from living bears by citizens (a) and students (b) from different standpoints including Asiatic black bears’ standpoints, humans’ standpoints, and personal standpoints. ATTITUDES TOWARD BILE EXTRACTION FROM LIVING BEARS 215

There is a wide variety of bear bile alternatives available depending on the illness (Dutton et al., 2011; World Society for the Protection of Animals [WSPA], 2005). In addition, studies have shown that usage of bear bile negatively affects bears in the wild (Livingstone & Shepherd, 2016) and the ability of farm animal-based products, such as bear bile, to reduce demand for wild animal products is at best limited (Dutton et al., 2011). A high percentage of people claimed that they rarely used bear bile medicines and bear bile might be replaced by alternatives (Ding, 1998; Dutton et al., 2011; Mills, 1995;WSPA,2005). This may be an opportunity with great potential to engage the TCM industry to use alternatives to bear bile. Respondents stated that the bear bile medicine used was effective, yet they expressed fairly low willingness to buy and reuse the medicine. Our study indicated that the curative effect score was high, but the usage intention score of respondents, notably for students, was significantly lower than the curative effect score (p < .01). The treatment outcome of medicine is an important factor that influences the purchasing behavior of consumers with respect to drugs (Wang, 2006). Consumers take action based on their perception, previous knowledge, and experience (Schiffman & Kanuk, 2004). This situation for the respondents may also be related to the perception of moral and ethical disputes caused by bile extraction from living bears. The scores reported by the students for curative effects and willingness to reuse were significantly lower than the scores reported by citizens (p < .01), expressing an unwillingness to reuse bear bile. College students and recent graduates are more likely to get involved with environmental nongovernmental organizations (NGOs), and they generally have a high level of animal protection awareness (Yang, 2005). Recently, animal protection and welfare issues have also been gaining increasing attention in mainstream Chinese society (Meng et al., 2012). People’s attitudes and views can influence and change their intentions, buying behaviors, and habits (Kotler & Roberto, 1989; Schiffman & Kanuk, 2004).

Attitude toward bile extraction from living bears The respondents held a clear position on arguments about extracting bile from living bears and especially college students tended to not support bile extraction from living bears. China’s government and other concerned organizations such as environmental NGOs publicized the environmental concerns of the wildlife trade, and public education has already become a powerful tool for increasing awareness of wildlife consumption and knowledge of protection (Nowell & Xu, 2007; Wasser & Jiao, 2010; Zhang, Hua, & Sun, 2008). Studies have shown that in China, the public has generally been supportive of wildlife conservation (Gratwicke et al., 2008; Nowell & Xu, 2007; Zhang et al., 2008; Zhang & Yin, 2014). In China, college students have received a systematic higher education and represent the mainstream opinion among young people. Additionally, these students have a higher awareness of wildlife protection (Zhang, Li, & Wang, 2011). Notably, young college students or recent graduates are drawn to environmental NGOs and activities in search of social experience and self-fulﬁllment (Yang, 2005). We found that college students were more opposed to farming bears to extract bile than were citizens. A clear correlation was noted between higher wildlife conservation awareness and higher levels of education (Nowell & Xu, 2007). In addition to being part of NGOs, the public also could play important roles in this issue by raising awareness and sharing survey information that might assist governments (Feng et al., 2009). According to the distribution characteristics of the attitude data covering the arguments of living bear bile extraction, we found that respondents had a more ambivalent attitude toward the red side (pro) than the blue side (anti). A dilemma occurs between bear bile being used as traditional medicine and animal protection (Feng et al., 2009). Supporting endangered wildlife conservation often involves conflicts with select human interests. Therefore, this conservation is often onerous or difficult to fulfill because of the real sacrifice required (Taylor, 2011). Compared with citizens, 216 LIU ET AL. college students had a more definitive attitude toward the two sides and were more inclined to not support bile extraction from living bears. Animal welfare research in China has been limited, in large part due to a lack of funding (Meng et al., 2012). In 2002, a survey study showed that a high percentage of college students expressed empathy toward animals and opposed animal cruelty (Zu, Li, & Su, 2005). In the case of bile extraction from living bears, our results showed that respondents do consider animal welfare and animal rights. Current college students are China’s future political, economic, and opinion leaders; therefore, their attitudes toward animals and the changes in their attitudes over time will have a direct effect on animal welfare consciousness in China (Zu et al., 2005). Compared with citizens, students were more inclined to be against the extraction of bile from living bears. Relevant educational materials of animal welfare should also be distributed through collaborations with schools and community groups in an effort to educate and influence the largest possible cross-section of society (Meng et al., 2012). College students and general citizens have a high level of animal protection awareness, which will promote the formation and enforcement of animal protection laws and policies (Yang, 2005; Zhang et al., 2011). Respondents had different attitudes toward living bear bile extraction when answering from different standpoints. The degree of wrongness in bear bile extraction decreased in order from the standpoints of Asiatic black bears, the participants, and humans (Table 8). Attitudes toward the world and all living things are an issue to be addressed by ethics. Anthropocentric ethical theories eliminate nonhuman existence from the subjects of moral concerns (Norton, 2008). In new environmental ethics, subjects for moral concern should not be limited to humans but should also include nonhuman species (Fox, 1990; Norton, 2008). To view the position of nonhuman species in the natural world from the perspective of a biocentric outlook is to reject the concept of human superiority over other living things (Taylor, 2011). The disputes over bile extraction from living bears and the results of our study have shown that

the public has recognized the importance of wildlife protection and animal welfare. To correct the mistreatment of animals on farms requires more than implementing “more humane” rearing methods (Regan, 1986). It is our collective responsibility to actively pursue a resolution that is palatable to all sides of the debate for animal welfare (McMahon, Harcourt, Bateson, & Hindell, 2013). Additionally, the public can bear their share of moral and ethical responsibilities and expand their circle of moral subjects to a wider area (Noss, 1992; Primack, 1993; Rolston, 1988).

Conclusion and animal welfare implications Although select older people are more likely to use bear bile medicines, bear bile is an unnecessary medicine in TCM. Respondents showed a fairly low willingness to reuse bear bile medicines even when the medicines were considered effective. This unwillingness may be related to their perception of the ethical arguments caused by bile extraction from living bears. Notably, the public in Beijing held beliefs that were more against the use of bear bile extracted from living bears. The study showed a growing conservation consciousness, and these moral responsibilities might help protect endangered species. The limitations of this study were that this survey was conducted in Beijing, so firm conclusions cannot be drawn about other areas throughout China, such as rural areas or other cities that may have different viewpoints.

Acknowledgments

We thank all members of the Wildlife and Behavioral Ecology Group, Institute of Zoology (IOZ)/Chinese Academy of Sciences (CAS), and all investigators who participated in the investigation. We are grateful for the recommendations from the members of the expert panel for this project. ATTITUDES TOWARD BILE EXTRACTION FROM LIVING BEARS 217

Funding This study was supported by the Knowledge Innovation Project of the Chinese Academy of Sciences (KSCX2-EW-Z-4).

References

Bi, P. F. (1988). Progress and prospects for research on bear ecology. Journal of Agricultural Science Yanbian University, 2,69–75. Chinese Pharmacopoeia Commission. (1977). Chinese pharmacopoeia. Beijing, China: Chinese Medicine Science and Technology Press. Convention on International Trade in Endangered Species (CITES) of Wild Fauna and Flora. (2013). CITES Appendices I, II and III. Retrieved from http://www.cites.org/ Cooperative Group of Chinese Medicinal Animal Records. (1979). Chinese medicinal animal records (Book I). Tianjing, China: Tianjing Science and Technology Press. de Vaus, D. A. (2002). Surveys in social research (5th ed.). London, England: Routledge. Ding, A. W. (1998). Famous and precious Chinese traditional medicine pedigree. Nanjing, China: Jiangsu Science and Technology Press. Dutton, A. J., Hepburn, C., & Macdonald, D. W. (2011). A stated preference investigation into the Chinese demand for farmed vs. wild bear bile. PLoS ONE, 6, e21243. Fan, Z. Y. (2000). Status of black bear and bear farming industry in China. Daziran, 4,40–42. (in Chinese) Fan, Z. Y. (2001). The development of bear farming in China. In D. Williamson & M. J. Phipps (Eds.), Proceedings of the Third International Symposium on the Trade in Bear Parts (p. 101). Hong Kong, China: TRAFFIC East Asia. Fan, Z. Y. (2006). The problem analysis and the development pondering of bear farming. Science and Technology of Tianjin Agriculture and Forestry, 1,4–10. (in Chinese) Fan, Z. Y., & Song, Y. L. (1997). Current status and conservation of bears in China and Chinese bear farms. In D. F. Williamson & A. L. Gaski (Eds.), Proceedings of the Second International Symposium on the Trade of Bear Parts (pp. 5–19). Washington, DC: TRAFFIC USA and World Wide Fund for Nature or World Wildlife Fund, USA (WWF- US). Feng, Y., Siu, K., Wang, N., Ng, K. M., Tsao, S. W., Nagamatsu, T., & Tong, Y. (2009). Bear bile: Dilemma of

traditional medicinal use and animal protection. Journal of Ethnobiology and Ethnomedicine, 5,2. Fox, W. (1990). Towards a transpersonal ecology: Developing new foundations for environmentalism. Boston, MA: Shambala. Gratwicke, B., Mills, J., Dutton, A., Gabriel, G., Long, B., Seidensticker, J.,. . . Zhang, L. (2008). Attitudes toward consumption and conservation of tigers in China. PLoS ONE, 3, e2544. Hu, J. C., & Hu, T. Q. (1998). Protection and utilization of Chinese bear: Origination and evolution of bear. Hainan, China: Hainan International News Press. International Fund for Animal Welfare. (1994). Moon bears tortured for satisfying human needs. Massachusetts, USA: International Fund for Animal Welfare. International Union for Conservation of Nature. (2013). The 2013 IUCN red list of threatened species. Gland, Switzerland: Author. Retrieved from http://www.iucnredlist.org. Kirkpatrick, R. C., & Emerton, L. (2010). Kill tiger to save them: Fallacies of the farming argument. Conservation Biology, 24, 655–659. Kish, L. (1987). Statistical design for research. New York, NY: John Wiley and Sons. Kotler, P., & Roberto, E. L. (1989). Social marketing: Strategies for changing public behavior. New York, NY: Free Press. Lei, Y. (2001). The deep ecology thought research. Beijing, China: Tsinghua University Press. Li, Y. W., Zhu, X. Y., But, P. P. H., & Yeung, H. W. (1995). Ethnopharmacology of bear gall bladder: I. Journal of Ethnopharmacology, 47,27–31. Livingstone, E., & Shepherd, C. R. (2016). Bear farms in Lao PDR expand illegally and fail to conserve wild bears. Oryx, 50, 176–184. Loeffler, I. K., Robinson, J., & Cochrane, G. (2009). Compromised health and welfare of bears farmed for bile in China. Animal Welfare, 18, 225–235. Ma, Y. Q., Hu, J. C., & Zhai, Q. L. (1994). Bears of China. Chendu, China: Sichuan Scientific and Technical Press. Malcolm, K. D., McShea, W. J., Van Deelen, T. R., Bacon, H. J., Liu, F., Putman, S.,. . . Brown, J. I. (2013). Analyses of fecal and hair glucocorticoids to evaluate short- and long-term stress and recovery of Asiatic black bears (Ursus thibetanus) removed from bile farms in China. General and Comparative Endocrinology, 185,97–106. McMahon, C. R., Harcourt, R., Bateson, P., & Hindell, M. A. (2013). Animal welfare and conservation, the debate we must have: A response to Draper and Bekoff. Biological Conservation, 158, 424. Meng, S., Huang, H. K., & Li, Z. (2007). Bear breeding and conservation of its resource in China. Chinese Journal of Wildlife, 28(1), 27–32. 218 LIU ET AL.

Meng, X., Hamer, R., Meng, Q. H., Wang, P., Meng, F. L., Li, H. L.,. . . Zhou, Y. J. (2012). Animal welfare development in China. Science, 338, 1150–1151. Mills, J. A. (1995). Asian dedication to the use of bear bile. In D. A. Rose & A. L. Gaski (Eds.), Proceedings of the International Symposium on the Trade of Bear Parts for Medicinal Use (pp. 107–112). Washington, DC: TRAFFIC USA and World Wildlife Fund. Mills, J. A., & Servheen, C. (1991). The Asian trade in bears and bear parts. Washington, D.C.: World Wildlife Fund and TRAFFIC USA. Naess, A. (1985). Identification as a source of deep ecological attitudes. In M. Tobias (Ed.), Deep ecology (pp. 256–270). San Diego, CA: Avanti. Norton, B. G. (2008). Environmental ethics and weak anthropocentrism. Environmental Ethics, 6, 131–148. Noss, R. F. (1992). The Wildlands Project: Land conservation strategy. Wild earth, special issue, 10–25. Nowell, K., & Xu, L. (2007). Taming the tiger trade. Hong Kong, China: TRAFFIC, East Asia. Phillips, T., & Wilson, P. (2002). The bear bile business: The global trade in bear products from China to Asia and beyond. London, England: World Society for the Protection of Animals (WSPA). Primack, R. B. (1993). Essentials of conservation biology. Sunderland, MA: Sinauer. Quinn, G. P., & Keough, M. J. (2002). Experimental design and data analysis for biologists. Trans. Z. G. Jiang, C. W. Li, & Y. Zeng. Beijing, China: Higher Education Press. Regan, T. (1986). A case for animal rights. In M. W. Fox & L. D. Mickley (Eds.), Advances in animal welfare science (pp. 179–189). Washington, DC: The Humane Society of the United States. Rolston, H. (1988). Environmental ethics: Duties to and values in the natural world. Philadelphia, PA: Temple University Press. Schiffman, L. G., & Kanuk, L. L. (2004). Consumer behavior (8th ed.). Upper Saddle River, NJ: Pearson Prentice Hall. Servheen, C. (1999). The trade in bears and bear parts. In C. Servheen, S. Herrero, & B. Peyton (Eds.), Bears: Status survey and conservation action plan (pp. 33–38). Gland, Switzerland: International Union for Conservation of Nature (IUCN). Singer, P. (1990). Animal liberation (2nd ed.). New York: New York Review of Books. Solomon, J., Jacobson, S. K., Wald, K. D., & Gavin, M. (2007). Estimating illegal resource use at a Ugandan park with the randomized response technique. Human Dimensions of Wildlife, 12,75–88. Taylor, P. W. (2011). Respect for nature: A theory of environmental ethics. Princeton, NJ: Princeton University Press. Wang, M. X. (2006). Medicine consumer behavior. Beijing, China: People’s Medical Publishing House. ’

Wasser, R. M., & Jiao, P. B. (2010). Understanding the motivations: The first step toward influencing China s unsustainable wildlife consumption. Beijing, China: TRAFFIC East Asia. World Society for the Protection of Animals (WSPA). (2005). Finding herbal alternatives to bear bile. London, England: Author. Yang, G. (2005). Environmental NGOs and institutional dynamics in China. The China Quarterly4, 181,4 –66. Zhang, L., Hua, N., & Sun, S. (2008). Wildlife trade, consumption and conservation awareness in Southwest China. Biodiversity and Conservation, 17, 1493–1516. Zhang, L., & Yin, F. (2014). Wildlife consumption and conservation awareness in China: A long way to go. Biodiversity and Conservation, 23, 2371–2381. Zhang, S. X., Li, C. J., & Wang, B. (2011). Empirical research on college students’ consciousness of animal protection. Journal of Ecology and Rural Environment, 27(6), 104–108. (in Chinese with English abstract) Zu, S. X., Li, P. J., & Su, P. F. (2005). Animal welfare consciousness of Chinese college students’ findings and analysis. China Information, 19(1), 67–95.