CITES search strategy and data extraction
During the period 1975 and 2013 a total of 316 separate clouded leopard trade records (including seizures) was officially received by CITES according to the comparative tabulation report (Appendix of ESM 1). It is important to note that to date the CITES records have not differentiated between specimens of Neofelis diardi and Neofelis nebulosa and the search term ‘Neofelis spp.’ did not retrieve any records. The majority (71 %; n = 223) of these CITES trade records referred to live clouded leopards (Appendix of ESM 1). The remainder referred to clouded leopard derivatives including skins (11 %), specimens (10 %), body parts (5 %), bones (2 %) and unspecified ‘derivatives’ (1 %) (with no additional descriptive data being provided) (Appendix of ESM 1).
Each CITES trade transaction record should be composed of data relating to both export and import aspects of a transaction, including the type and quantity of items traded. However, CITES WCMC acknowledges that trade between two countries, involving the same shipments, frequently fails to show perfect correlation (UNEP-WCMC 2014). We found that 43 % (n = 137) of the 316 clouded leopard CITES records provided export data only, 48 % provided import data only and only 9 % provided both export and import data (Appendix of ESM 1). The number of CITES trade transaction records lacking export data and import data is not a recent phenomenon and has remained constant feature since records began in 1975 (UNEP-WCMC 2014).
Derivative trade recorded by CITES
In total, 22 % (n = 70) of the 316 CITES records referred to the legal trade in clouded leopard derivatives (Appendix of ESM 1). CITES records indicate that in terms of quantity, a total of 820 derivatives was legally exported via 37 trade transactions and 427 derivatives was legally imported via 40 trade transactions between 1975 and 2013 (Table 1). However, we found that the information regarding the units used to describe these legal derivative imports and exports were provided for only 7 % (n = 5) of export records (four cubic centimeters, 10 flasks, five grams and 32 mm in total) and 6 % (n = 4) of import records (three centimeters, five grams and 52 mm in total) respectively (Table 1). As this information is required fully to comprehend and compare the quantity of derivatives involved we restricted our more detailed analyses to the number of live clouded leopards traded and CITES recorded seizures only.
Table 1 A full list of the clouded leopard export and import trade terms provided by CITES Parties during 1975 and 2013
Live trade recorded by CITES
In total, 70 % (n = 222) of the 316 CITES records referred to the legal trade in live clouded leopards (Appendix of ESM 1). According to the CITES comparative tabulation report, a total of 212 live clouded leopards was legally exported via 127 trade transactions during the period 1975 and 2013 (Table 1). Throughout this time, annual live exports varied between 1 and 6 animals with a mean average of 4 animals via an average of 2 trade transactions per year. In contrast, according to the same CITES data source, a total of 304 live clouded leopards was legally imported via 115 trade transactions during the same time period (Table 1). Throughout this time, annual live imports varied between 1 and 100 animals (the latter figure being an outlier; Fig. 3) with a mean average of 5 animals via an average of 2 trade transactions per year.
Linear trends analysis revealed that the quantity of live clouded leopard exported (R
2 = 0.06) and imported (R
2 = 0.04) both appear to have remained relatively constant during the period 1975 and 2013 (Fig. 3). However, in recent years (2008 and 2013) a relatively high volume of legal live trade has been recorded (Fig. 3). During this 6 years period alone, a total of 35 live animals was exported and 141 was imported. Notably, live imports peaked in 2009, largely due to a consignment (representing 33 % of all live imports) of 100 captive bred live individuals of unknown geographic origin that was imported into Japan from the Republic of Korea (Appendix of ESM 1).
With regards to live imports, since 1975 when CITES record keeping first began, the live trade in clouded leopards appears to have shifted away from animals of unspecified origin for zoological purposes and towards that of captive animals primarily intended for commercial use (Fig. 3). During the initial period (1975 and 1981) no commercial breeding for commercial use was reported by CITES (Fig. 3). In contrast, during the most recent period (1998 and 2013) 56 % (n = 100) of imported live clouded leopards were reported to have been commercially bred in captivity for commercial use (Fig. 3).
Between 1975 and 2013, the legal export of live clouded leopards was reported from a total of 20 countries (Fig. 4). Surprisingly, the majority of exporters (75 %, n = 15) fall outside of the known geographical range of these species. Over the past 38 years the USA has been the most active exporter recorded by CITES with the majority of its 61 live clouded leopards (61 %; n = 37 [individual clouded leopards]) traded for commercial purposes (Fig. 4). During the same time period, China (n = 37) and Thailand (n = 17) have been the two most active range country exporters in this regard. The CITES database also indicates that Cambodia (n = 2), Malaysia (n = 2) and Vietnam (n = 4) have been the only other range countries to have legally exported live clouded leopards since record keeping began (Fig. 4).
Between 1975 and 2013, the legal import of live clouded leopards was reported from a total of 25 countries (Fig. 4). The majority of importing countries (92 %, n = 23) also fall outside of the known geographical range of this species. Over the past 38 years Japan has been the most active importer recorded by CITES with majority of its 131 live clouded leopards (85 %; n = 111 [individual clouded leopards]) traded for commercial purposes (Fig. 4). During the same time period, the USA was the second most active importer on record in this regard, with 31 % (n = 10) of its 32 live clouded leopards traded for commercial purposes (Fig. 4). The CITES database also indicates that Cambodia (n = 1) and Malaysia (n = 8) have been the only range countries to have legally imported live clouded leopards since record keeping began (Fig. 4).
Seizures recorded by CITES
In total, 8 % (n = 24) of the 316 CITES records referred to the seizure of illegally traded live clouded leopards and their derivatives (Appendix of ESM 1). According to the CITES comparative tabulation report, only one illegal seizure of a live clouded leopard was made during the period 1975 and 2013 (Table 1). The records indicate that this individual of unknown origin was exported from Hong Kong for zoological purposes and was confiscated in 1991 upon arrival in Germany (Appendix of ESM 1). During the same period 23 seizures involving clouded leopard derivatives took place (Table 1). In total, 52 % of CITES derivative seizure records involved skins (n = 12), 22 % involved bodies, 22 % involved bone items, and 4 % involved unspecified items (Fig. 5; Table 1).
We found that further analysis regarding the quantity of CITES items seized on import was not possible as unit data (required to describe and compare clouded leopard derivative seizures) was completely lacking (Table 1). In total 17 % (n = 4) of the 23 derivative seizure records involved clouded leopard items that were exported from unknown sources (Appendix of ESM 1). One (4 %) seizure of a ‘plate’ was made on arrival in the USA following unlawful export from the UK (Table 1). The remaining 18 derivative seizure records involved body parts that were all exported from seven countries within Asia including Vietnam (26 %; n = 6), Thailand (22 %), China (13 %), Indonesia (4 %), Lao PDR (4 %), Philippines (4 %) and Taiwan (4 %) (Appendix of ESM 1).
All of the 23 derivative seizures recorded took place upon import into three non-Asian countries, namely the Netherlands (4 %; n = 1), New Zealand (4 %) and the USA (92 %) (Appendix of ESM 1). With regards to CITES purpose codes 22 % of all seizures was reported to be for personal use and 4 % was reported to be for zoological use (Appendix of ESM 1). However, no purpose code information was provided for the majority of derivative seizures (74 %) (Appendix of ESM 1).
Literature review
There were 127 sources (103 scientific papers and 24 grey reports) included in the literature review (Fig. 2). The mean rate of publication on clouded leopards between 1975 and 2013 was five papers and 0.6 reports per annum. The earliest paper and report included was published in 1986 and 2000 respectively (Fig. 6). Linear trends analysis revealed that the numbers of papers (R
2 = 0.53) and reports (R
2 = 0.39) mentioning these cats in the context of trade have increased over the past four decades (Fig. 6). Scientific attention peaked in 2011 (n = 18) and NGO attention peaked in 2012 (n = 5) (Fig. 6).
Only 14 (11 %) of these 127 sources (four papers and ten reports) focused primarily on issues related to the trade in clouded leopards (Fig. 2). With regards to the scale of the trade, three (21 %) of these 14 trade focused sources referred solely to the domestic trade within India. One (7 %) referred solely to cross border international trade between particular source and sink countries. Nine (64 %) referred to both domestic and international trade and one (7 %) failed to distinguish between the two (Appendix of ESM 2).
Although it was not the main focus, the trade in clouded leopards was mentioned in an additional 28 (22 %) of these 127 sources (25 papers and three reports) (Fig. 2). For example trade in clouded leopards was briefly alluded to in the introduction and/or discussion of many of the papers included in this study or mentioned in passing as part of wider discussions regarding threats to general biodiversity in grey reports. However, a total of 22 (52 %) of all trade related sources (n = 42) failed to provide any specific information regarding clouded leopard trade chains (Appendix of ESM 2).
Summary of published information
A total of 18 (43 %; 7 papers and 11 reports) of all trade related sources cited countries of illegal domestic trade concern including: Cambodia (5 %; n = 2), China (5 %), India (14 %), Indonesia (7 %), Lao PDR (2 %), Malaysia (2 %), Myanmar (7 %), Nepal (2 %), Thailand (7 %) and Vietnam (2 %) (Fig. 7). With regards to international trade, a total 14 (33 %; 5 papers and 9 reports) sources cited ‘sink’ countries (the final intended destinations) of illegal trade concern including: China (17 %; n = 7), Hong Kong (2 %), Indonesia (2 %), Korea (2 %), Myanmar (5 %), Russia (2 %), Taiwan (2 %), Thailand (10 %), USA (2 %), and Vietnam (5 %) (Fig. 7). Historic records of live specimens for use as pets into the UK and the Netherlands during the early 1900 s were also cited in two of the papers.
Unlike any of the scientific papers included in this study, three grey reports (7 % of all trade related sources) provided specific information regarding certain towns with trade markets that are known to have engaged in the illegal trade of clouded leopards and their derivatives. Specific sites of particular concern include Kawthaung in south Myanmar; Keng Larb, Mong Hsat, Mong La, Mong Mit, Panghsang, and Tachilek in the Shan and Wa states of northern Myanmar; Boten, Thakek and Vieng Thong in Lao PDR; and Muang Sing and Nam Teuk in China (Fig. 7).
A total of 19 (45 %; 16 papers and 3 reports) of the 42 trade related sources failed to provide any specific information on the type of clouded leopard trade referred to within (Fig. 5). However, a total of 21 sources (50 %) specifically mentioned the trade in clouded leopard skins for ornamental purposes (Fig. 5) citing Cambodia (2 %), China (2 %), India (14 %), Indonesia (7 %), Laos PDR (7 %), Malaysia (2 %), Myanmar (12 %), Nepal (2 %), Thailand (5 %) and Vietnam (2 %) as source countries of concern (Fig. 7).
A total of 15 (36 %) sources referred to the trade in meat for subsistence (Fig. 5) citing China (2 %), India (10 %), Indonesia (10 %), Laos PDR (5 %), Malaysia (2 %), Myanmar (12 %), Nepal (2 %), Thailand (5 %) and Vietnam (2 %) as source countries (Fig. 7). A total of 15 (36 %) sources referred to trade in bones for medicinal purposes (Fig. 5) citing China (2 %), India (10 %), Indonesia (5 %), Laos PDR (5 %), Malaysia (2 %), Myanmar (12 %), Nepal (2 %), Thailand (5 %) and Vietnam (2 %) as source countries of concern (Fig. 7).
A total of nine (21 %) sources referred to trade in live animals as exotic pets for recreational purposes (Fig. 5) citing India (5 %), Indonesia (10 %), Laos PDR (5 %), Malaysia (2 %), Myanmar (12 %), Nepal (2 %), Thailand (2 %) and Vietnam (2 %) as source countries of concern (Fig. 7). Only 16 (38 %) of these clouded leopard trade-focused sources provided any information regarding the volume of trade.
One report (2 %) provided specific information relating to clouded leopard enforcement seizures made between 1997 and 2013 (TRAFFIC 2013). In total, it detailed seven different seizures made within China (29 %; n = 2), Indonesia (14 %), Thailand (29 %), USA (14 %), and Vietnam (14 %). In total, these seizures involved at least three bodies, one full skeleton, three full skins and 100 skin pieces (TRAFFIC 2013). India (West Bengal) was specifically cited as a source country for one seizure (14 %) (TRAFFIC 2013). No source country data was provided for the other remaining seizures (86 %) (TRAFFIC 2013).
The majority (91 %; n = 38) of the sources that mentioned trade in any way referred to the negative conservation impacts caused by the illegal sourcing of wild caught clouded leopards. However, none of the scientific papers referred to the potential negative conservation impacts posed through legal captive breeding facilities (e.g. laundering of wild caught individuals). None of the sources included in this literature review referred to the negative animal welfare impacts associated with the trade in either wild caught or captive bred clouded leopards. However, technical and welfare challenges experienced by conservation (i.e. non commercial) captive breeding programs were extensively documented.
These breeding programs have been characterized by high incidence of male aggression (Kitchener 1999) to the extent that there have been at least 25 known fatal attacks on females in captivity recorded over the past 20 years (DeCaluwe et al. 2013). To negate infanticide cubs are often hand reared in captivity (DeCaluwe et al. 2013). Clouded leopards are also very sensitive to changes in their environment with exposure to novel objects, loud noises and new people documented as stressors (DeCaluwe et al. 2013). These generally anxious animals display a diversity of stress behavior in captivity including hair plucking, tail chewing, pacing and excessive hiding (Wielebnowski et al. 2002).
Expert opinion
We approached 40 clouded leopard experts and received formal responses from a total of 24 individuals (60 %). We received 17 completed questionnaires from individuals with a working knowledge from eight of the known clouded leopard range countries including Bhutan (6 %; n = 1); Cambodia (6 %); India (6 %); Indonesia (18 %); Lao PDR (6 %); Malaysia (18 %); Myanmar (18 %) and Thailand (24 %). We were unable to obtain any formal responses from individuals working in China, Bangladesh or Nepal. The remaining eight respondents did not fill in a questionnaire but provided additional informed insight.
A total of 13 of the 17 questionnaire respondents (77 %) provided information regarding specific illegal trade activity. The majority (65 %; n = 11) stated direct observation as a source of their information. However, verbal reports from trusted contacts (35 %), media reports (12 %), scientific papers (12 %), published reports (6 %) and unpublished reports (6 %) were also cited. A total of seven respondents (41 %) described illegal activity that had taken place within 6 months prior to questionnaire distribution. The remaining respondents (35 %; n = 6) all referred to activity that had taken place within the last 10 years.
A total of 15 questionnaire respondents (88 %) cited countries of domestic illegal trade concern including: Bhutan (6 %; n = 1), Cambodia (6 %), India (6 %), Indonesia (18 %), Lao PDR (6 %), Malaysia (12 %), Myanmar (18 %) and Thailand (18 %) (Fig. 7). With regards to sink countries, a total of 14 respondents (82 %) cited sink countries of international illegal trade concern including: China (47 %; n = 8), India (6 %), Myanmar (6 %), Tibet (6 %), Thailand (7 %) and Vietnam (12 %) (Fig. 7). Experts reported China as sourcing illegal derivatives from at least five different clouded leopard range countries (Cambodia, India, Lao PDR, Myanmar and Thailand) (Fig. 7).
Some of the 17 questionnaire respondents were able to provide specific information regarding certain towns where illegal trade activity is known to have occurred. Specific sites of particular concern include Phobjikha in Bhutan; Phnom Penh in Cambodia; Digboi, Kokrajhar and Seijosa in India; Jakarta in Indonesia; Bakun dam, Kapit, Nabawan, Pensiangan and Sematan in Malaysia; Bangkok, Ban Pa Deng, Ranong and Songkhla in Thailand; and Khaw Thaung, Laiza, Putao, Naung Shwe, and Tachilek in Myanmar (Fig. 7).
Discussions with remaining experts identified two additional key reports that were not encountered during our main literature review. Information provided therein brings attention to a number of additional towns with illegal trade markets known to engage in big cat trade along the borders of China, India and Nepal (Nowell and Pervushina 2014). Specific sites of particular concern include: Burang (China); Dharchula, Imphal, Leh, Moreh, Raxaul, and Siliguri (India); and Biratnagar, Birgunj, and Zhangmu (Nepal) (Fig. 7).
With regards to the frequency of illegal trade type and intended use cited, expert opinion broadly reflected CITES seizure records and our literature review. A total of 13 (77 %) questionnaire respondents specifically mentioned clouded leopard skins for decorative purposes, eight (47 %) reported trade in meat for subsistence consumption, six (35 %) reported trade in bones for use as traditional medicine and two (12 %) reported trade in live animals for use as exotic pets (Fig. 5). Only two questionnaire respondents (12 %) failed to provide any specific information on the type and intended use of clouded leopard trade within their selected country (Fig. 5). Two experts (12 %) cited concerns that clouded leopard derivatives were being sourced as an alternative to tiger derivatives.
None of the 17 questionnaire respondents referred to illegal activity related to the captive breeding of clouded leopards. However, discussions with one expert confirmed that this is of potential concern (Anonymous pers. comms. 2014). Undercover footage taken in early 2014 confirmed the presence of clouded leopards at the Muang Thong Tiger Farm in Lao PDR (Hargreaves 2014; Anonymous pers. comms. 2014) and a further 27 at Ubon zoo (a known supplier of wildlife for commercial use) in Thailand (Environment for Nature Vietnam (ENV) 2014) (Fig. 8). Film footage taken in mid 2014 also confirmed the presence of a juvenile clouded leopard at the Rhino and Lion Nature Reserve in South Africa (also a supplier of wildlife for commercial use) (World Animal Protection 2015). Discussions with three experts also confirmed that illegal activity regarding to clouded leopards could also be easily observed online. For example, four photos featuring four clouded leopard carcasses were posted by members of a single Malaysian online social media group entitled ‘Bakunparadise’ between April 24th and November 08th 2014 (Facebook 2014) (Fig. 8).
According to the 17 questionnaire respondents, illegal direct take from the wild is currently having a medium to high negative impact [mean average score of 5 (n = 15)] on the conservation of clouded leopards. In their opinion, this type of activity is also having a medium negative impact on their welfare [mean average score of 4 (n = 16)]. These same respondents indicated that illegal trade in these species is increasing [mean average score of 5 (n = 15)] with respondents specifically citing India (n = 1; 6 %), Indonesia (6 %), Laos PDR (6 %), Malaysia (6 %), Myanmar (6 %) and Thailand (24 %) as source countries of increasing concern. All respondents also stated that current efforts to address it are inadequate [mean average score of 2 (n = 15)].