Turtles and tortoises have long been utilized in East and Southeast Asia for food, medicines, and pets, and China is the largest consumer country in the world (Gibbons et al. 2000; van Dijk et al. 2000; Moll and Moll 2004). The annual trade volume of live turtles in Asia have exceeded 13,000 metric tons (1 metric ton = 1000 kg), and a high proportion of them are believed to be collected from the wild (van Dijk et al. 2000). Due to burgeoning demand in the market following rapid economic growth, over one-half of freshwater turtle and tortoise species from Southeast and East Asia have been severely threatened by overexploitation for food and traditional medicines (Jenkins 1995; Klemens and Thorbjarnarson 1995; van Dijk et al. 2000). The issues of live turtle trade and farming industries have received more attention than other animal products and raw materials for sentimental reasons and due to data availability problems (e.g., Cheung and Dudgeon 2006; Gong et al. 2006; Shiau et al. 2006; Shi et al. 2007, 2008). Until now, little is known about the magnitude of turtle-shell trade for the TCM market, and it is difficult if not impossible to assess the impact of this trade on chelonian fauna.

Turtle shells (plastrons from hard-shelled species and carapaces from soft-shell species) have long been used as an ingredient for traditional Chinese medicines (TCM) in many societies with Chinese cultural origins and affinities in East and Southeast Asia and other overseas Chinese communities around the world (van Dijk et al. 2000). Unfortunately, the trade in turtle shells has never been systematically monitored and few long-term data are available. Chen et al. (2000) have reported that > 136 metric tons of turtle shells were traded in the TCM market of Taiwan per year during 1992–1998. In Taiwan, the supply of turtle shells depends mainly on import from China and Southeast Asia (Yen 1992; Tsai and Chang 2001). Because the TCM market is a closed community and the domestic trade is poorly documented due to the limited oversight by the responsible agencies, we thus rely on the available data from the international trade statistics of customs reporting systems. Because almost all of the raw materials of turtle-shell products used in Taiwan's TCM market were imported from abroad, the data will provide a general overview of the market scale.

Chang (1997) reported that at least 20 nonmarine chelonian species have been found in the TCM market of Taiwan. The most common species were Cuora amboinensis, Malayemys subtrijuga, and Siebenrockiella crassicollis. Although > 25% of the species were Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES)-listed, they represented < 1% of the total trade volume (Tsai and Chang 2001; Lo et al. 2006). With widespread concerns for the conservation of turtles and tortoises in Asia (Gibbons et al. 2000; van Dijk et al. 2000), most of the target species, including most of the common species in the TCM market and all species from China, have been listed on CITES Appendix II or III (populations in China) in 2000–2005 to monitor and regulate the uncontrolled trade in East and Southeast Asia (C. amboinensis in 2000, S. crassicollis in 2003, M. subtrijuga and Mauremys reevesii in 2005). CITES was adopted in 1973 with the aim to ensure that international trade in specimens of wild fauna and flora does not threaten their survival through controls on and monitoring of the trade in species listed in its appendices. CITES listing has added restrictions on previously unregulated trade of most turtle and tortoise species in East and Southeast Asia. Thus, we predict that the trade volume of turtle shells in the TCM market should have decreased significantly if the CITES listing has worked effectively.

In this paper, we attempt to show an overall picture of trade volume and provide data on large-scale turtle-shell trade in Taiwan's TCM market. The species involved in the trade are identified. We also discuss the effectiveness of CITES listing for many target species on the international trade volume of turtle shells in East and Southeast Asian regions.

METHODS

The import data of turtle shells were obtained from the customs trade database created by the Directorate General of Customs, Ministry of Finance, Republic of China (Taiwan; http://web.customs.gov.tw/statistic/statistic/mnhstatisticen.asp). In the customs trade data, the Harmonized System (HS) is commonly used as the basis of customs tariffs and the analysis of international trade statistics. For most wildlife trade analysis, the HS code is for relatively broad taxa and may be misleading to a certain degree (Blundell and Mascia 2005; Thompson and Alam 2005; Gerson et al. 2008). However, in the case of turtle-shell trade, the customs trade data can provide an overall picture of the market. The turtle-shell products in the database were shown in good item description as “tortoise shell, terrapin plastron (including for Chinese drugs)” for hard-shelled species and “pieh chia k'o (Amydae carapax) (including for Chinese drugs)” for soft-shell species. This database is the only source of total quantitative data on the turtle-shell trade by month, importing country, weight in kg and value in New Taiwan Dollar (NTD); 1 NTD = 0.029 US dollars). Moreover, the raw materials of turtle-shell products for TCM, unlike other live animals or fresh meats, are duty-free goods items in tariff rate and relatively low-priced. The trade volume and monetary values recorded in the database should have been accurately declared.

The trade data of CITES-listed species were retrieved and confirmed from the United Nations Environment Programme-World Conservation Monitoring Centre CITES trade database (http://www.unep-wcmc.org/cirestrade/). This database holds the official records of the international trade of CITES-listed species.

To identify the species of turtles and tortoises involved in the TCM market, a general survey was conducted from 1996 to 2002 (mainly by H.-C. Chang). Although partial species lists have been mentioned in previous studies, including 20 species (including 1 questionable species, Manouria emys) in Chang (1997) and 33 species (including 1 invalid species, Cuora hainanensis, and 1 questionable species, Mauremys megalocephala) in Tsai and Chang (2001), we provide a more detailed and revised species list in this report.

A total of 14 importers, 12 manufacturers for “Gui Ban Jiao” (tortoise plastron jelly) and “Gui Lu Er Xian Jiao” (tortoise shell and deer-antler syrup), and 1 manufacturing company of traditional medicines were investigated and sampled. Because the TCM market is a closed community, it is impossible to collect detailed quantitative data from these stakeholders. The species composition was estimated roughly only for the common species observed. Because the price of turtle shells is usually judged by the appearance and quality of raw materials, we can identify the samples to species level (Fig. 1). When the species of plastron specimens could not be identified at first sight during market surveys, specimens were purchased and attempts were made to identify to the species level where possible.

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RESULTS

Trade Volume and Monetary Value

According to the customs trade statistics for 1999–2008, as much as 1,989,248 kg (1989 metric tons) of hard-shelled turtle shells have been imported into Taiwan from China and Southeast Asian countries, with an average of 198,925 kg (198.9 metric tons)/y over the period (Table 1). The total amount of soft-shell turtle shells imported was 290,419 kg (290 metric tons), averaging 29,042 kg (29.0 metric tons)/y (Table 2). A total of 7 countries were involved in the international trade; China and Indonesia were the main suppliers of hard-shelled turtle shells to the TCM market of Taiwan, contributing 39.2% and 33.7% of total trade volume, respectively. Cambodia also supplied 18.4% of the total trade volume. Soft-shell turtle shells were imported from 6 countries, and China alone accounted for 84.6% of the total trade volume.

Table 1. The trade records of shells from hard-shelled turtles and tortoises (in weight: kg) imported into Taiwan from different countries in 1999–2008.

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Table 2. The trade records of shells from soft-shell turtles (in weight: kg) imported into Taiwan from different countries in 1999–2008.

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Although turtle shells are relatively cheaper than live turtles in the market, the total monetary value was large, amounting to 143.54 million NTD (= 4.16 million USD). In monetary value, China was the most important source country, accounting for 46.8% of total amount, followed by 33.2% from Indonesia.

Long-term trends in turtle-shell trade are complex. We have not found significant reduction in the trade volume of turtle shells in the Taiwanese market after CITES listing of most target species from 2000 to 2005 (Fig. 2). Ironically, the annual average trade volume increased dramatically in 2002 (326,761 kg), then decreased gradually. Even though most of the common species traded in the TCM market have been listed on CITES II, the trade volume was still huge, reaching 183,745, 169,071, and 151,028 kg in 2006, 2007, and 2008, respectively. The number of exporting countries involved has decreased in the trade records. No trade records of turtle shells were found from South Asia, such as Bangladesh and Pakistan, in 1992–1998. In 2006–2008/2009, turtle shells were only imported from China, Indonesia, and Vietnam to Taiwan. The trends in monetary value and average price were highly variable (Fig. 3), with a peak in total monetary value in 2004. The average price both of hard-shelled and soft-shell species dropped greatly in 2002 and 2003, then increased in hard-shelled chelonians thereafter. It increased in 2004, then dropped gradually.

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Surprisingly, we have not found any record of CITES-listed turtles or tortoises traded for medicinal purposes on the CITES trade database. Only 2360 live turtles and tortoises of 25 species from Indonesia, Malaysia, and Thailand have been reported in 1999–2007. The large-scale international trade of turtle-shell products was not overlooked by the monitoring system of CITES.

Species Composition

In the domestic market survey conducted in 1996–2002, a total of 39 chelonian species, 37 hard-shelled and 2 soft-shell, were identified in Taiwan's TCM market (Table 3), including many endangered and CITES-listed species. Among them, 87.2% (34 species) had been listed on CITES Appendices by 2005. In comparison with the previous studies, we identified 6 additional species and revised 1 species. Similar to the previous results, Cuora amboinensis, Malayemys subtrijuga, and Siebenrockiella crassicollis were the most commonly found species; they constituted over 75% of the market. Mauremys reevesii was the most valuable species in the TCM market, and it accounted for 10%–15% of the market. The large-sized Orlitia borneensis were observed only from 2 traders, and they were used as ingredients of Gui Lu Er Xian Jiao. This species accounted for about 1%–3% of the total volume in weight. Meanwhile, judging from the natural distribution range, 8 species were recorded exclusively from South Asia, indicating that extensive trans-shipment may have occurred in the TCM trade. Only 3 non-Asian species were identified (i.e., Trachemys scripta elegans from North America, Stigmochelys pardalis from Africa, and Astrochelys radiata from Madagascar).

Table 3. Chelonian species found in the traditional Chinese medicinal market of Taiwan surveyed in 1996–2002.

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In the soft-shell turtle shells, only 2 species were identified, Pelodiscus sinensis, mainly imported from China, and Amyda cartilaginea from Southeast Asia.

DISCUSSION

Traditionally, turtle shells have been used as a common ingredient in TCM prescriptions. It is well-known that turtle shell is used for the production of guilinggao (turtle jelly), a glue-like residue produced by long-term boiling of turtle shells and some other herbal ingredients. According to traditional medicinal texts, the raw materials of hard-shelled turtles and soft-shells come chiefly from China, and mainly from M. reevesii and P. sinensis (Yen 1992). It is believed that plastron of M. reevesii is more effective than other counterparts. It is widely accepted that turtle shells have broad pharmaceutical effects. In Taiwan, turtle shells were used in the formula of “Gui Lu Er Xian Jiao” and “Gui Ban Jiao”. Gui Lu Er Xian Jiao is a semifluid extract of turtle plastron and deer-antler jelly, usually mixed with some herbal ingredients such as ginseng and Lycium berries (Goji). Gui Ban Jiao is a glue-like jelly, extracted from turtle shells by long-term boiling.

Turtle shells are usually regarded as byproducts from the consumption of turtle meat (Tsai and Chang 2001), but the specific collection of turtle plastron has been reported (Jenkins 1995). In the customs trade data of Taiwan, limited amounts of frozen turtle meat and dried turtle offal have been imported from Hong Kong and Indonesia, indicating that turtles and tortoises may have been traded in other forms. The high demand for turtle shells in the TCM market may have greatly exceeded the supply as byproducts, especial for hard-shelled species. The shells of P. sinensis were usually used as a byproduct in restaurants and mainly originated from turtle farms. In the TCM market, shells were traded in whole piece of plastron in hard-shelled turtles, and unlikely to be the byproduct of turtle meat (usually consumed as turtle soup in Asia). A great proportion of turtle shells may have been obtained from wild-caught individuals for TCM purposes. In China, numerous species, including M. reevesii and P. sinensis, have been farmed extensively (Shi et al. 2008). Some of the turtle shells used in the TCM market may come from farms (obtained from dead individuals), or they may be byproducts of meat consumption in species such as Trachemys scripta elegans, M. reevesii, and P. sinensis. Some high-priced or non-Asian species found in the TCM market, such as Cuora trifasciata, Stigmochelys pardalis, and Astrochelys radiata, may also be a byproduct of dead individuals from turtle farms.

The average amount of hard-shelled turtle shells imported into Taiwan alone exceeded 198 metric tons/y in 1999–2008; the trade volume has increased greatly compared to the 136 metric tons/y reported previously in 1992–1998 (Chen et al. 2000). The market in Taiwan represents only a fraction of the regional trade volume of turtle-shell products, and the total regional trade volume may add up to several times this amount. In the TCM community, only plastron was used due to traditional customs; although, there was no apparent difference in the chemical composition between carapace and plastron bone (Yang 1988). In medium-sized geoemydids, each piece of plastron weighs approximately 50–200 g (T.-H. Chen, pers. obs.). The massive trade volume for turtle shells in the TCM market suggests that shells of millions of turtles and tortoises have been consumed per year in Taiwan alone. For the case of Taiwan, observed levels of usage and trade of turtle shells appear to be unsustainable and may have a great impact on chelonian faunas in source areas.

Turtle shells, unlike many other animal products, were not traded at species-specific levels. The shipments of turtle-shell products were usually mixed with multiple species, and some items confused TCM importers and dealers. The commercial supplies of turtle shell in the TCM community are not categorized and priced based on species. Rather, they are roughly sorted by the appearance, coloration, size, and countries of origin, mainly into 7 categories: 1) Sui plastron or golden coin plastron (Mauremys reevesii plastron)—the most valuable item in the market (however, some Malayemys subtrijuga have also been lumped in this category); 2) Chihmi plastron (Mauremys mutica plastron)—often mistaken to be Malayemys subtrijuga in the market, with genuine plastron of M. mutica found in this category much less frequently than M. subtrijuga; 3) black plastron—mainly Siebenrockiella crassicollis; 4) big plastron—Orlitia borneensis; 5) Mekong River plastron or foreign plastron—mainly Indotestudo elongata; 6) Indonesian plastron—mainly Cuora amboinensis; 7) other items—a variety of species. For soft-shell turtles, the carapaces of Pelodiscus sinensis were usually used in TCM. However, shells imported from Southeast Asia were mainly from Amyda cartilaginea. In TCM markets of mainland China, Lissemys punctata and Pelochelys bibroni (likely P. cantorii) have been reported to be mixed with P. sinensis (Wang et al. 2000).

In long-term trends, we have not found a significant reduction in trade volume for the past 17 years. There have been fewer exporting countries because only 3 countries occurred in the trade records in 2006–2008. Part of this may have been due to a reduction in supply (overharvesting in some countries), and trade restriction (most turtles are listed on CITES Appendices). In the trade data, the source countries have shifted occasionally, suggesting that species composition in TCM market may have changed. However, the trade volume of the main target species, such as M. reevesii and P. sinensis from China, and C. amboinensis, M. subtrijuga, S. crassicollis, and A. cartilaginea from Indonesia, have not decreased (H.-C. Chang, pers. obs.).

In customs trade data, only the exporting countries of turtle shells can be obtained; however, the precise trade routes were difficult to trace. The species composition indicates that a significant proportion of TCM trade consists of re-exports or trans-shipments. Some species distributed in South Asia have been identified in the market, and some South Asian species, such as Morenia ocellata and Pangshura tecta, have been found in the raw materials imported both from China and South Asia (H.-C. Chang, pers. obs.).

Numerous studies have demonstrated that sustainable use of long-lived reptiles is problematic because longevity in chelonians is usually associated with delayed sexual maturity and low fecundity (Congdon et al. 1994). The unsustainable use of nonmarine turtles and tortoises has been discussed extensively in the literature (e.g., Gibbons et al. 2000; Moll and Moll 2004; Schlaepfer et al. 2005). They are especially vulnerable to uncontrolled exploitation. Overexploitation accompanied by habitat destruction has caused the observed decline in the chelonian populations in Asia. If the present trend in the TCM market continues, many wild populations of chelonian species will continue to be seriously threatened.

It has been generally argued that free-trade policy may facilitate growth of wildlife trade and threaten the sustainability of many wild populations (Rose 1992). In Taiwan, turtle shells for TCM can be imported freely under loose regulations; no species-specific declarations are required. Under CITES regulations, the international trade of live animals, their parts and raw materials both from wild-caught and captive-bred CITES-listed species should have been regulated and controlled through exporting permits and quotas. Although CITES listing cannot by itself solve the turtle trade problem, it relies on the support of trading nations and their willingness to take necessary action through trade management. Although Taiwan is not a signatory of CITES, the international trade of CITES-listed species still has to be regulated and reported by a monitoring system compliant with CITES standards. Better legal enforcement by trading nations is needed to regulate the large-scale turtle-shell trade.

It has been also been argued that it is difficult to identify and check the species composition of turtles and tortoises traded in the market or on the border. In the TCM community, raw materials of turtle shells were usually priced by the quality and source of origin. Most of the plastrons were kept intact, and the specimens of most common turtles can be identified to species level with a well-illustrated identification guide. Although raw materials of turtle shell can be identified to species level using molecular tools (e.g., Hsieh et al. 2006; Lo et al. 2006), it is a time- and labor-consuming process. Because most of the target and common species of turtles and tortoises traded in East and South Asia have been listed in CITES Appendices, every shipment of international trade of turtle shells needs appropriate documentation and has to be inspected thoroughly.

From the case of the TCM market in Taiwan, we strongly urge the trading nations, both the importing and the exporting countries, to take a serious look at the large-scale turtle-shell trades in East and Southeast Asia. Rather than just CITES-listing most of the traded species and regulating trade in whole live animals, responsible agents also have to take action to regulate the trade of turtle shells which may detrimentally threaten the regional chelonian fauna, especially in source regions.