The global magnitude and implications of legal and illegal wildlife trade in China
Y UNBO J IAO and T IEN M ING L EE
Abstract China is one of the largest consumer markets in is a major component of this global commerce. China is the international legal and illegal wildlife trade. An increas- a major supply source (Nijman, ; Petrossian et al., ing demand for wildlife and wildlife products is threaten- ), but since the s has become one of the world’s ing biodiversity, both within China and in other countries largest consumers of wildlife and wildlife products (Zhou where wildlife destined for the Chinese market is being & Jiang, ; UNODC, ), as a result of economic sourced. We analysed official data on legal imports of development and increasing consumer affluence. China’s CITES-listed species in five vertebrate classes (mammals, demand for wildlife appears to continue to expand as its af- reptiles, amphibians, birds and fish), and on enforcement fluent, urban population increases, and the culture of wild- seizures of illegally traded wildlife, during –. This life consumption spreads from the south to other parts of is the first study that collates and analyses publicly available the country (Zhang et al., ; Zhang & Yin, ). data on China’s legal and illegal wildlife trade and considers This demand drives unsustainable and often illegal a broad range of species. Specifically, we estimated the scale harvest and trade, threatening biological diversity within and scope of the legal and illegal wildlife trade, quantified and beyond China’s borders. The Red List of China’s the diversity of species involved, and identified the major Biodiversity (MEE & CAS, ) shows that % of the trading partners, hotspots and routes associated with illegal , Chinese vertebrate species that have been assessed trade. Our findings show that substantial quantities of wild- using the IUCN Red List categories and criteria are catego- life have been extracted globally for the Chinese market: rized as threatened. Overexploitation for food and use in during – over . million whole-organism equiva- traditional Chinese medicine is the most pervasive threat lents and million kg of derivatives of legally traded wildlife, to Chinese vertebrates (MEE & CAS, ). As wildlife plus over , illegally traded animals (alive and dead) populations are depleted within China, sourcing of com- and a substantial amount of animal body parts and prod- mercially valuable species has shifted to neighbouring coun- ucts, were imported into China. Although measures to tries in Asia, and to Africa (UNODC, ). As a result, reduce demand and alleviate poverty are crucial to curb the wild populations of highly coveted species, includ- unsustainable and illegal wildlife trade in the longer term, ing pangolins (Challender et al., ), Asian large felids China’s wildlife regulators and enforcers must take urgent (Lynam, ; Maheshwari & Niraj, ), bears (Garshelis measures to disrupt the supply chains from source to market. & Steinmetz, ), rhinoceroses and elephants (UNEP et al., ;Milliken,), and tortoises and freshwater tur- Keywords Biodiversity conservation, China, CITES, enforce- tles (Nijman & Shepherd, ) have experienced severe de- ment, illegal wildlife trade, regulation, wildlife products clines in China’s main source countries. As highlighted by Supplementary material for this article is available at the global outbreak of COVID- (WHO, ), this legal doi.org/./S and illegal wildlife trade threatens not only biodiversity but also human health, by facilitating the transmission of zoo- notic diseases from wild animals to people. Prior analyses of legal and illegal wildlife trade in China Introduction focused primarily on high-value species or wildlife products such as tigers (Wong, ), elephant ivory (Gao & Clark, nternational wildlife trade, whether legal or illegal, is a ) or bear bile (Foley et al., ), or on trade hotspots Iglobal business, with a value of traded and smuggled of these species and products such as Yunnan (Yi et al., goods of USD billions per year (Harfoot et al., ; ), Guangxi (Jiang et al., ) or Guangdong (Chow ‘ t Sas-Rolfes et al., ). Wildlife trade to and from China et al., ). There is a paucity of empirical studies that con- sider both the legal and illegal wildlife trade in the country
YUNBO JIAO (Corresponding author, orcid.org/0000-0001-6473-6357) School as a whole. of Law, Sun Yat-sen University, 135 West Xingang Road, Guangzhou 510275, Here, we aim to provide an evidence-based overview of China. E-mail [email protected] China’s role in transnational wildlife trade through an TIEN MING LEE ( orcid.org/0000-0003-2698-9358) School of Life Sciences, examination of empirical data on legal wildlife trade and en- School of Ecology and State Key Laboratory of Biological Control, Sun Yat- – sen University, Guangzhou, China forcement seizures of illegally traded wildlife during Received December . Revision requested March . . Specifically, we examined: ( ) the scale and scope of Accepted August . China’s legal and illegal trade, () the number and diversity
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, Downloadeddistribution, from https://www.cambridge.org/core and reproduction in any medium,. IP address: provided 170.106.40.139 the original work, on is 25 properly Sep 2021 cited. at 00:50:52, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/termsOryx, Page 1 of 8 © The Author(s),. https://doi.org/10.1017/S0030605320000800 2021. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605320000800 2 Y. Jiao and T. M. Lee
of species involved, () the major trading partners and Material ). With respect to the type of traded goods, () the hotspots and routes associated with China’s illegal China’s imports were dominated by live animals and skins, trade. This information can aid wildlife management au- accounting for and % of the total imports, respectively. thorities in China and source countries in improving their regulation of legal trade, and help cross-border wildlife law enforcement agencies formulate more tailored interception Most imported species A total of vertebrate species – and prevention strategies to disrupt illegal trade. were imported into China during . Of those, species were listed on CITES Appendix I, on Appendix II and on Appendix III. Overall, a relatively Methods small number of species accounted for the majority of imported wildlife (e.g. the brown caiman Caiman crocodilus We gathered data from two sources. For legal trade, we fuscus and the oriental ratsnake Ptyas mucosus; Supple- queried the CITES trade database (CITES, ) for all mentary Material ). Within the taxonomic groups, the ’ records of China s imports of five vertebrate classes (mam- most traded species constituted % of the imports of – mals, reptiles, amphibians, birds and fish) during mammals, % of reptile imports, % of bird imports (data downloaded on December ). This database has and nearly all fish imports. Ten species belonging to mul- been used in previous studies to examine trade of a selected tiple taxonomic groups accounted for % of all imports range of taxonomic groups or species at different geograph- of live animals, and five reptilian species together accounted ical scales (e.g. Jiang et al., ; Li & Jiang, ; Foster et al., for % of all imports of skins. ), but ours is the first to use it to quantify China’s global imports of all CITES-listed vertebrate species. For data on illegal trade, we collated information re- Purpose of imported wildlife The intended purpose of ported by TRAFFIC () on seizures of illegally traded legally imported wildlife varied between taxonomic groups wildlife for the same time period, including cases that (Supplementary Table , Supplementary Material ). Mam- involved China as the source, transit point or final desti- mals were imported primarily for the fur trade, and rep- nation of the seized wildlife, and seizure incidents occur- tiles for their skin, and for human consumption, traditional ring within and outside China (see Supplementary Material Chinese medicine and the pet trade. Birds were imported pri- for details). marily for the pet trade. Parrots (Psittaciformes), particularly members of the Psittacidae family, which are often traded as caged birds in China (Li & Jiang, ), were the most im- Results ported taxon. Fish trade was dominanted by the Siberian sturgeon Acipenser baerii and the Asian arowana Scleropages Legal trade formosus, which were introduced into China mainly for commercial captive breeding for human consumption (Chen Scale of China’s legal trade Our analysis of , CITES et al., ) and ornamental use (Tian et al., ), respectively. trade records showed that during –, an estimat- ed . . million whole-organism equivalents of wildlife (including . million live animals) and million kg of wild- Wild-caught vs captive-bred imports Captive-bred animals ’ life derivatives were legally imported into China. The mean comprised on average over half ( %) of China s annual annual import volume in whole-organism equivalents was imports for most of the study period (Supplementary . million, accounting for c. % of the legitimate global Fig. a, Supplementary Material ). At the level of taxo- wildlife imports, which were estimated at million per nomic groups, mammals were mostly wild-caught ( %of – year (Harfoot et al., ). The vast majority (%) of the annual mammal imports during ; Supplementary trade was for commercial purposes, followed by trade of Fig. b), whereas birds and fish were predominantly captive- animals for breeding in captivity (%). sourced ( % of annual bird imports and % of annual fish imports; Supplementary Figs d,e). Imported reptiles were wild and captive-sourced at approximately equal rates dur- Imports by taxonomic group and type of goods Whole- ing this period (Supplementary Fig. c). When looking spe- organism equivalents were mostly reptiles (n = million), cifically at the trade of skins, however, we found a transition followed by fish (n = . million) and mammals (n = . towards a higher proportion of wild-sourced products over million). China’s imports of birds (n = . million) and the study period: from %in to %in (Fig. ; amphibians (n = ,) were comparatively low, together Supplementary Material ). This was mainly driven by in- accounting for only % of the total imports. There was con- creased imports of wild-sourced reptile skins: the import siderable variability in the annual import volume of all volume in whole-organism equivalents rose by % from taxonomic classes (Supplementary Fig. , Supplementary , to , and the proportion of wild-caught reptile
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). Amongst the species listed on CITES Appendix I or II that were traded both legally and illegally, those that were imported legally from one country were often trafficked illegally from another country in the same region, particularly in East and South-east Asia (Supplementary Fig. ). Only eight species were sourced legally and illegally from the same country (e.g. in Malaysia: the Amboina box turtle Cuora amboinensis and the Sunda pangolin Manis javanica;inIndonesia:the Asian leaf turtle Cyclemys dentata and the black marsh turtle Siebenrockiella crassicollis). Overall, the seizures resulted in the FIG. 1 China’s skin imports during –,brokendownby confiscation of . , animals, including live (n = ,) wild-caught (CITES source codes W, R), captive-bred (source and dead specimens (n = ,). Reptiles were the taxonom- codes C, D, F) and other sources (source codes I, O, U or blank; ic group with the largest total number of specimens seized see Supplementary Material for details about the CITES source (n = ,). The number of seized mammals was much codes). smaller (n = ,), but mammals and their derivatives comprised % of all seizure incidents. skins in annual imports increased from to % during – (Fig. ). In contrast, imports of mammal furs were consistently dominated by wild-sourced supplies. Commonly trafficked species and derivatives The species and derivatives most commonly trafficked to China (Table ) Major trading partners A total of countries and terri- were bears (paws, gall bladders), elephant ivory (tusks, car- tories, from all continents except Antarctica, were reported vings, jewellery), leopards and tigers (pelts, bones), pangolins as the source of China’s legally imported vertebrate animals (live, meat, scales), rhinoceroses (horns), and lizards, snakes, and products during – (Fig. ). At the regional level, turtles and tortoises (live, shells). Elephant ivory, lizards, pan- Asia-Pacific was the biggest supplier, providing %of golins, snakes, turtles and tortoises in particular were traded on China’s imports; followed by Europe (%), Central and a substantial scale. For example, during –, seizures South America (%) and North America (%). Contrary involved the forfeiture of , kg of elephant tusks and ivory to its role as a major source in China’s illegal trade products by enforcement agencies within and outside China. (UNODC, ), Africa provided only a small share (%) This is c. %ofthe, kg of elephant ivory seized by of China’s legal wildlife imports. At the national level, CITES parties globally (including China) during the same per- source countries supplied % of China’s total imports, iod and reported to the Elephant Trade Information System with Colombia, Indonesia, Malaysia, Thailand, USA and (Milliken et al., , ). Using an estimated mean tusk Viet Nam consistently supplying large volumes of wildlife weight of . kg (Rosen & Smith, ), the impounded throughout the period studied. Of the species listed in ivory represents c. , elephants. CITES Appendix I, European countries exported the highest number of mammals and birds, and South-east Asian na- Smuggling routes and hotspots Seizure data suggest that tions exported the highest number of reptiles (Figs a–c; countries and areas predominantly in Africa (e.g. the Supplementary Material ). For species listed in Appendix Democratic Republic of the Congo, Kenya, Nigeria) and II, the number of vertebrate species exported was more Asia(e.g.Indonesia,Myanmar,Russia)areinvolvedinthe evenly distributed across the continents. South Africa and illegal trade of mammals and reptiles to China (Fig. ). The Japan exported the highest number of mammal species, majority of the trafficked mammal species originates from South Africa the highest number of bird species and African, East and South-east Asian countries (Fig. a), whereas – Indonesia the highest number of reptile species (Figs d f). South-east Asia is the centre of the illegal trade for reptilian species (Fig. b). Multiple routes exist for trafficking wildlife Illegal trade into China. Hong Kong is the most important entrance point for wildlife smuggled by sea from South-east Asia and Scale of China’s illegal trade Our analysis of wildlife sei- Africa into mainland China, but China’s terrestrial borders zures showed that a large diversity and volume of wildlife was are also commonly used in transnational wildlife trafficking. illegally traded to, from or via China during the study period. Authorities in all of China’s border areas, from the north-east The reported illegal trade involved animal species, with (Heilongjiang, Jilin) and north (Inner Mongolia), to the west species in seizures listed on CITES Appendix I, species (Xinjiang), upper south-west (Tibet) and south-west (Yunnan, in seizures on Appendix II and three species in five sei- Guangxi), have reported seizures involving large volumes zures on Appendix III. In addition, species recorded in il- of illegally traded wildlife (TRAFFIC, ; Supplementary licit trade were also legally imported (Supplementary Material Material ).
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FIG. 2 Most traded species in China’s wild-sourced skin imports in whole-organism equivalent terms during – (see also Supplementary Material ).
FIG. 3 Countries that legally traded vertebrate species to China during – (also see Supplementary Material ). Countries and territories are represented by their ISO code in the tile grid, in their approximate geographical location. China is marked by the black star. The colour of each tile represents the number of species imported to China. Countries and territories for which no data were available are shaded grey. The top panels show the number of CITES Appendix I-listed (a) mammal, (b) bird and (c) reptile species imported. The bottom panels show the number of Appendix II-listed (d) mammal, (e) bird and (f) reptile species imported.
Discussion there are numerous non-CITES listed species, trade in which is generally poorly documented and thus remains Limitations of data sources largely unknown (Janssen & Leupen, ). For example, only c. % of currently recognized reptile species are covered Although the CITES trade database and the TRAFFIC by CITES (Auliya et al., ). In addition, local use and Bulletin are amongst the few publicly available data sources domestic trade, which may account for the majority of glo- on legal and illegal wildlife trade (Lopes et al., ), both bal wildlife trade (Broad et al., ), are outside the regula- have limitations, and an analysis based on these two sources tory scope of CITES. Data on illegal trade are limited by the alone would lead to an underestimation of trade volumes. fact that not all illegal transactions are intercepted and not CITES is limited to regulating international trade for all seizures are reported by media (Underwood et al., ). c. , species listed in its three appendices. However, As such, seizure data are indicative not only of the presence
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TABLE 1 High-profile species and derivatives seizures of illegally traded wildlife destined for the Chinese market during – (data from TRAFFIC, ).
No. of Taxa Most seized derivatives Other derivatives seized seizures Main uses1 Mammals Bears 4,410 paws 46 gall bladders, 26 live, 13 heads, 49 Food, TCM 1 penis, 2 whole skins, 5 carcasses Elephants 118,689 kg ivory tusks & products 3,683 pieces of ivory tusk, 2,078 146 Decoration carvings & jewellery items Tigers 95 whole skins, 517 kg bones 288 pieces of bones, 8 carcasses, 38 Decoration, TCM 5 live cubs, 2 skulls, 2 skeletons Leopards 758 whole leopard skins 12 individuals (live & dead), 20 Decoration, TCM 4 skeletons, 3 heads Pangolins 16,188 individuals (live & dead), 110 Food, TCM 101,877 kg meat, 56,736 kg scales Rhinoceroses 268 horns 68 kg horn products 31 Decoration, TCM Reptiles 82 Food, TCM, pets, Snakes 55,455 individuals (live & dead) 25,652 skins, 2,829 kg meat leather products Lizards 10,643 individuals (live & dead) 4,964 kg meat Turtles & 43,942 individuals (live & dead) 3,573 kg meat, 1,953 kg shells tortoises
TCM, traditional Chinese medicine.
and scope of illegal trade, but also of the effectiveness of law illicit trade and the low rate of detection. In addition, the enforcement efforts to tackle it (UNODC, ). In add- reported volume of seized wildlife probably only covers a ition, the TRAFFIC Bulletin compiles only the more signifi- fraction of all global wildlife seizures related to China be- cant wildlife seizures and prosecutions (e.g. cases involving cause many seizures are not reported in the media. For interception of large-volume shipments or charismatic spe- example, data from the China Forestry Yearbook (NFGA, cies such as elephants or tigers) that have taken place world- –b) indicated that during –, Chinese for- wide since (TRAFFIC, ). estry police countrywide handled a total of , forest and wildlife-related criminal cases and million administra- Overview of legal and illegal trade tive cases, leading to apprehension of . million offenders and confiscation of . million animal individuals. Our analysis showed that China’s global wildlife trade, both The parallel existence of sizeable legal and illegal markets legal and illegal, is substantial in scale and scope (UNODC, challenges the ability of China’s wildlife authorities to prevent ; Harfoot et al., ). China’s legal imports of CITES- illegally traded wildlife from entering the legal commerce, and listed species are primarily destined for commercial markets to differentiate between legal and illegal products, particularly in four areas: the fashion industry, trade of pets and orna- as nearly half of the species recorded in illegal trade were also ments, traditional Chinese medicine, and human food. traded legally. In addition, Chinese legislation supports the Trade in non-CITES listed species can generally only be development of a farming industry for protected species and analysed through examining country-level records of such permits the commercial trade and utilization of farmed speci- trade, or via market surveys (Janssen & Shepherd, ). mens and related products (Li, ). This has created an addi- The China Forestry and Grassland Statistical Yearbook tional source of legal supply and another route for launder- (NFGA, –a) indicates that during –, ing illegally traded and wild-sourced specimens. There is China’s import value of non-CITES-listed species was USD evidence that legally registered farms have been used as stor- . billion, which is much less than that of CITES-listed spe- age and transfer facilities for laundering wild-caught animals cies (USD . billion). However, market surveys suggest that (Ma & Zong, ;Wang,), and that some local markets domestic trade in amphibians (Wang et al., ), birds (Li have become channels for illegal wildlife trade (EIA, ; et al., ), turtles and snakes (Chow et al., ;Ling, Jiang et al., ). As part of the efforts to control the corona- ) was dominated by non-CITES-listed species in terms virus pandemic and prevent future outbreaks of zoonotic of trade volume and species diversity. diseases, in February China passed a total ban on Although the reported scale of China’s illegal wildlife consumption of all terrestrial wildlife as food, regardless of trade is only % of its legal imports, this is probably a protection status and whether it is wild or captive-sourced gross underestimate because of the clandestine nature of (NPC-SC, ).
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Asian water monitor Varanus salvator, the reticulated python Python reticulatus and the Nile crocodile Crocodylus niloticus (Fig. ). The import volume of wild-sourced skins from these three species combined increased five-fold over the study period, and the majority were sourced in South-east Asia (especially Indonesia and Malaysia). One reason for this is that the demand for reptile skins for China’s leather industry exceeds the supply capacity of its do- mestic captive breeding programmes. Within China, attempts to breed V. salvator in captivity have failed (Xu et al., ). Only one python farming company exists in the country, with an annual output of c. , skins from captive-bred Burmese pythons Python bivittatus, all traded in domestic marketsforleatherproductsandChinese musical instruments (mainly Erhu; Natusch & Lyons, ). There are c. , individuals of alien crocodilian species (mostly the Nile crocodile, the Saltwater crocodile Crocodylus porosus and the Siamese crocodile Crocodylus siamensis)beingkeptin captivity across China (Gao & Zhang, ). Given this lim- ited domestic supply, China relies on supplies from abroad to meet the increased demand for reptile skins, and imports more than doubled in value since .In the country imported . t of reptile skins, with a total value of USD . million (UN Comtrade Database, ). Considering a mean weight of . kg for skins of smaller lizards and . kg for crocodile skins (UNODC, ), this implies an import of ,–. million reptile individuals into China that year. This trend applies not only to China: over half of legal FIG. 4 Countries and territories that illegally traded CITES Appendix I or II-listed (a) mammal and (b) reptile species to exports of CITES-listed reptile skins globally are from wild China during – (see also Supplementary Material ). sources (UNODC, ), and most of the legal python exports Countries and territories are represented by their ISO code in from South-east Asia are reportedly collected from the wild the tile grid, in their approximate geographical location. China is (Nijman & Shepherd, ). In addition, illegally traded, marked by the black star. The colour of each tile represents the wild-caught reptiles may be laundered into the legal supply number of species seized with China as the final destination. chain prior to export (Lyons & Natusch, ), and thus Countries and territories for which no data were available are recorded as legal wild-sourced trade. Indonesia, China’s shaded grey. major exporter of reptile skins, has a quota system in place for monitoring and regulating the harvest of wild reptiles, but its legal exports may also include illegally harvested Increasing trade in wild-sourced skins reptiles because collection activities are highly decentralized and informal, and discerning between legal and illegal reptile There are studies suggesting a shift from wild to captive skins is difficult (UNODC, ). sources in the legal wildlife trade globally (Harfoot et al., ), in the live reptile and amphibian trade in the USA (Herrel & van der Meijden, ) and in the consumption Conclusion of wildlife as food in China (CWCA & WildAid, ). Our analysis did not confirm this trend towards more captive- Although the long-term solution to unsustainable and sourced wildlife in China’s imports of vertebrates and their illegal wildlife trade must include measures to reduce de- derivatives, including meat (Supplementary Fig. f). On the mand and alleviate poverty, based on this first assessment contrary, both the import volume of wild-sourced skins and we propose that disrupting the supply chains from source their proportion in China’s annual skin imports have in- to market is an important and urgent short-term step. For creased markedly since .In, two-thirds of China’s international supply chains, this relies primarily on source skin imports were supplied by wild and ranching sources countries enacting enforceable schemes to verify the legality (Fig. ). This shift was largely driven by the increase in imports of traded goods (e.g. allowing only tagged crocodilian skins of wild-sourced skins of a few reptilian species, including the to be exported; CITES Secretariat, ), or imposing
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