Characteristics and Risk Assessment of International Trade in Tortoises and Freshwater Turtles in China
ABSTRACT
Commercial exploitation of freshwater turtles and tortoises has increased significantly in China since the 1990s, which has expedited the listing of some turtle species in Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) Appendix II. We assessed the risk to tortoises and freshwater turtles native to China by analyzing biological and socio-economic variables. The Principal Component Analysis model with VARIMAX rotation was used to categorize these species into groups. We found that many turtles in significant trade are at high risk of overexploitation. Except for Pelodiscus sinensis and Mauremys reevesii, most tortoises and freshwater turtles are classified in the same group and have similar risks. Listing several (but not all) chelonian species in the CITES Appendices will not resolve the chelonian trade crisis because many species may be substituted in trade. We recommend listing more Chinese turtles in the CITES Appendices.
There is a long history of exploitation of turtles and tortoises in China. Their shells were used as currency, luxury adornments, and materials for carving oracles and art products in ancient China. Utilization of turtles and tortoises (whole body, shell, or shell gel, produced by boiling turtle shells) as traditional medicine has been recorded in many ancient pharmaceutical and medical books. These products were considered useful to cure weakness, vertigo, agitation, and insomnia (Gao 1996). Some traditional Chinese medicines contain turtle or tortoise parts. Turtles and tortoises are also released into ponds in temples by Buddhists as symbol of longevity. Cuora trifasciata, generally called Golden Coin Turtles, are kept as a symbol of wealth.
Although the exploitation of turtles and tortoises has existed in China for thousands of years, the scale and impact of the trade was limited in earlier times. The combination of habitat degradation and overexploitation has resulted in population decreases of turtles and tortoises in China in recent years (Zhao 1998). Habitat degradation is a serious problem in China. Environmental pollution has expanded from urban cities to rural areas, while wetlands have gradually decreased. From the 1950s to the 1970s, about 12,000 km2 of lakes and wetlands (34.2% of the total lakes and wetlands area in the 1940s) were drained in southern China (Yang et al. 1982). Chelonians have been overexploited. Wang and Mao (1998) reported that about 2500–3000 kg of Pelodiscus sinensis was harvested in Shanxi Province of China each year, and they considered that yield unsustainable. Fan et al. (1998) reported that from 1985 to 1994, the quantity of P. sinensis decreased about 50% along a 32-km–long road in Jiaocheng County, Shanxi Province. The situation became worse when eating turtles and tortoises became fashionable in Guangdong, Guangxi, Hainan, and some southeastern provinces in the 1990s (Altherr and Freyer 2000; Lau and Shi 2000). Some researchers reported the status of illegal trade in turtles (Li and Li 1998; Gong et al. 2006). Because of their vulnerability to human hunting, long life span, and low reproductive rate, chelonians are more sensitive to overexploitation than other wild animals.
Thirty-six turtle species were included in the China Red Data Book of Endangered Animals—Amphibia and Reptilia (Zhao 1998), which almost account for all the turtles and tortoises native to China. Among the 36 species, 8 were critically endangered, 16 were endangered, 1 was vulnerable, 6 had insufficient data, 3 were extinct or extinct in the wild, 1 was conservation dependent, and 1 was unevaluated.
Some turtles consumed in China are bred in captivity (Endangered Species Import and Export Management Office of the People's Republic of China 2002). Although these farms satisfy part of the market demand, exploitation of wild populations of turtles and tortoises is still prominent because of people's interest in wild harvested animals. Many people believe that wild animals have better medicinal effects and fewer artificial chemicals. The exploitation has spread to other Southeast Asian countries. Import of tortoises and freshwater turtles into China, particularly from bordering countries, has been quite active during recent years (Li and Li 1998). Wu and Zhang (2001) investigated the wildlife market in Shanghai and found that 9 species of tortoises and freshwater turtles were imported from other countries. Smuggling of turtles and tortoises from other Asian countries to China has been reported (Yang et al. 2000). In recent years, large volumes of tortoises and freshwater turtles were imported into China. This phenomenon has caused worldwide concern (Ades et al. 2000; Lau and Shi 2000; van Dijk 2000). The Chinese government has noted this trend and has taken some measures (Meng et al. 2002), including designating ports, suspending turtle and tortoise import from 3 countries, reducing permitted import quantities, and revising the Customs Harmonized System Code (hereafter referred to as HS Code). Several additional species of tortoises and freshwater turtles have been listed in the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) Appendices since 2000.
Have these problems been solved after the listing of some chelonian species in the CITES Appendices? Which additional measures might be helpful for chelonians' survival? Which additional species should be set as conservation priorities? Some researchers have tried to identify priority species based on available information (Warren 1997; Filippi and Luiselli 2000; Dhar et al. 2000; Reed and Shine 2002; Zhou and Jiang 2005). Filippi and Luiselli (2000) considered both the biological and socio-economic pressures when assessing the risk status of species, but only one social factor, illegal collecting, was considered. Through assessing both biological and socio-economic characteristics, Zhou and Jiang (2005) identified 4 snake species that need priority conservation action out of more than 200 snake species native to China. In this paper, the dynamics of international trade in tortoises and freshwater turtles in China is reviewed and the potential risk of chelonians is evaluated by analyzing their biological and socio-economic characteristics in an attempt to identify species needing additional protection.
METHODS
Identification of Species in Significant Trade
According to the laws and regulations of China, the import or export of chelonians and their products (both CITES and non-CITES species) is subject to a permit from the Endangered Species Import and Export Management Office of the People's Republic of China (CITES Management Authority of China, hereafter referred to as CNMA). The earliest import and export data kept by the CNMA started in 1981, when China became a party of CITES. However, before 1998, most turtles and tortoises were only classified as “aquatic products” in HS code, therefore some shipments passed through customs without any permits issued by CNMA. In 1998, a revised version of the HS Code was jointly promulgated by the Customs General Bureau of China and CNMA, which designated a separate code for turtles and tortoises. Since then, international trade data collected by CNMA are quite comprehensive. The import and export data from 1998 to 2004 were analyzed in this study. Since these data were the records of issued permits, they might be higher than the actual trade volume because shipments are frequently smaller than the maximum permitted quantity due to supply issues, but shipments may not be larger than the quantity stated in the permit.
While considering the dynamics of import and export, we focused on the data related to hard-shelled turtles and tortoises belong to Geoemydidae, Platysternidae, and Testudinidae, with the exception of Trachemys scripta and Chrysemys picta. We took this approach because 1) the fishery authority of China suspended the importation of soft-shell turtles (referring to species belonging to the family Trionychidae, mainly P. sinensis from captive breeding in Southeast Asia) since 1999 to prevent the introduction of infectious disease to native populations; 2) Cheloniidae and Dermochelyidae species have been protected under CITES for many years, and their trade volume is quite low; 3) T. scripta and C. picta are produced through captive breeding and neither of these species is used for producing medicine; 4) in 2002, in order to limit the introduction of exotic species, CNMA suspended the import of live turtles or tortoises whose shell size was less than 10 cm in diameter; and 5) Amyda cartilaginea and other soft-shell turtles were often mixed with P. sinensis in trade, so the trade data of these species are not accurate.
Considering that the overall quantity of turtles and tortoises is difficult to calculate because of various difficult-to-identify product forms, we analyzed the trade volume of live individuals only. It was assumed that the weight of an average live turtle is equal to 1 kg. The following variables were chosen to evaluate the risks faced by turtles and tortoises. The biological data were taken from Yao (1980), Zhang and Zhang (1993), Zhao (1997), Zhang et al. (1998), and Zhao (1998), and Song (2002). The risk factor of each variable was categorized from 0 to 2, representing the level of risk the species was facing. Species with scores >1 were considered vulnerable, while those species with a score >1.5 as endangered. For species that are extremely rare and only had 3 or fewer factors available for scoring, the average score of that species was not calculated.
The biological factors were as follows:
a) Habitat breadth: inhabits 4 habitat types (such as lake, river, pond, rice field, and plateau; for tortoises, inhabits hill, mountainous region, and plateau areas), risk factor = 0; inhabits 2 to 3 types of habitats, risk factor = 1; only inhabits one type of habitat, risk factor = 2.
b) Maturity age: 4 or fewer years, risk factor = 0; 5 to 9 years old, risk factor = 1; 10 or more years, risk factor = 2.
c) Annual reproductive output: ≥ 20, risk factor = 0; 10 to 19, risk factor = 1; < 10, risk factor = 2.
The socio-economic variables were as follows:
d) Medical value: no medical value, risk factor = 0; used by rural people, risk factor = 1; cited by formal or official medical dictionary as curing several kinds of diseases, risk factor = 2. Scores were estimated according to Gao (1996), Chen et al. (1999), Jiangsu New Medicine College (1979), and Medicinal Material Corporation of China (1994).
e) Price as food (PF): ≤ 7 US dollars/individual, risk factor = 0; 7 to 12 USD/individual, risk factor = 1; 12 to 24 USD/individual, risk factor = 1.5; > 24 USD/individual, risk factor = 2. Scores were estimated according to the survey in Shanghai market taken by the Wildlife Conservation Society (Wildlife Conservation Society et al. 2000).
We assessed species of Geoemydidae, Platysternidae, and Testudinidae in China. Pelodiscus sinensis and Trachemys scripta elegans (although not a native species of China) were also assessed as a comparative standard. The Principal Component Analysis (PCA) model with VARIMAX rotation was used to analyze the matrix composed of the above scores, and the variables above were summarized into 2 components. Then these species were grouped according to a 2-dimensional plot. The software SPSS for Windows was used for data analysis (Norušis 2007). The nomenclature used in this paper follows the one proposed by Fritz and Havaš (2006).
RESULTS
International Trade Dynamics
Tables 1 and 2 summarize the export and import of tortoises and freshwater turtles in China from 1998 to 2004.
Turtles and tortoises were exported from China in many forms, including as live animal, shell, raw medicinal material, patented Traditional Chinese Medicine, medical liquor, health products, and specimens. The top 3 forms in trade were live animal, shell, and raw medicinal material, with the quantity of shell being the largest. The export of shell decreased from 1998 to 2001 but increased in 2002. The export of live individuals decreased continuously. If we presume that 15–25% of the weight of turtle is contributed by its shell, then the shell and live individuals exported from China from 1998 to 2002 required about 170,000 to 290,000 hard-shell turtles and tortoises each year. Of course, the shells exported may include those originated from live turtles and tortoises imported into China.
The turtles and tortoises imported into China were 3 types: live, shell, and dried body fragments. The import of live turtles and tortoises into China increased sharply; in 2002, the quantity of import was about 2 million individuals, which was twice the amount in 2001 and 5 times the amount in 1998. More than 10 species of turtles and tortoises were listed in CITES Appendix II at the 12th Conference of the Parties of CITES in November 2002. From 2003, the import quantity of these species decreased, apparently because of permit requirements resulting from CITES listing.
Species in Significant International Trade
The top 2 species in trade were Mauremys reevesii and Cuora amboinensis, which made up 49% of the total export. Other main species were C. mouhotii, C. flavomarginata, Platysternon megacephalum, M. mutica, and Indotestudo elongata. These 7 species made up 87% of the total export (Fig. 1A). The top 3 imported species were Heosemys grandis, Siebenrockiella crassicollis, and C. amboinensis and made up 68% of the total import. Other species in significant trade were H. annandalii, Notochelys platynota, Orlitia borneensis, H. spinosa, and Malayemys subtrijuga. These 8 species accounted for 99% of the combined import trade volume (Fig. 1B).
Citation: Chelonian Conservation and Biology 7, 1; 10.2744/CCB-0662.1
Risk Assessment for Tortoises and Freshwater Turtles in China
The scores of the hard-shell tortoises and turtles in China, as well as P. sinensis and T. scripta elegans are presented in Table 3. Data for some species endemic to China were not recorded in the literature. Even so, some rare species, such as C. zhoui and Ocadia philippeni, were still assigned scores higher than 1.7. Except for M. reevesii, P. sinensis, and T. scripta elegans (average score <1), most species are statistically assessed to be endangered or vulnerable.
PCA and Category of Species
Table 4 shows the rotated component matrix from the PCA model. Component 1 is mainly related to biological factors; whereas, component 2 is mainly related to socio-economic factors, including price as food and medical value. The average score for 4 species were not calculated since the scores of some factors were deficient.
The species with available data for 5 factors fell into 4 separate groups (Fig. 2). Group 1 included P. megacephalum, C. flavomarginata, C. trifasciata, M. mutica, M. sinensis, and Manouria impressa. Most of these species have median habitat breadth, either low annual reproductive or late maturity, and median or high commodity value. Manouria impressa is a species with both biological or social-economic pressure and would fall into another group if we divided this group into subgroups.
Citation: Chelonian Conservation and Biology 7, 1; 10.2744/CCB-0662.1
Group 2 was composed of M. reevesii and P. sinensis. They have large habitat breadth, either high annual reproductive or early mature age, and high or median commodity value.
Group 3 included Cyclemys dentata, C. galbinifrons, I. elongata, Sacalia quadriocellata, and Geoemyda spengleri. These species have median habitat breadth, low annual reproduction, and late age of maturity, but commercial value is not high.
Group 4 was T. scripta elegans. This species has wide habitat breadth, relatively early age at maturity, high annual reproductive, and low commercial value.
Group 5 included rare or endemic species in China. These species have narrow distribution and deficient biological data. These species could not be analyzed with the PCA model because of data deficiency, and the content of the group was determined artificially.
DISCUSSION
Since 1998, the quantity of turtles and tortoises imported into China has increased significantly; although, the Chinese government took measures to reduce trade such as designating trade ports, limiting export countries, and increasing permit requirements. Export volume decreased gradually. The Chinese government suspended commercial export of live specimens of any chelonian species except P. sinensis and C. reevesii. If we considered that 1) from 1998 to 2001, the export volume of shell decreased (although it increased in 2002, the shells might come from turtles and tortoises imported into China), and 2) the recorded number of live individuals imported into China is about 400,000 to 1,000,000, while the export is only about 170,000 to 290,000 each year; we conclude that China has shifted from a net exporter to a net importer of turtles and tortoises.
This phenomenon indicates that either domestic demand is increasing or the domestic resource is decreasing, or both. Considering the view of other researchers (Fan et al. 1998; Zhao 1998), it appears that the wild resource of turtles and tortoises in China has been decreasing, and the traders have begun to look for new sources in neighboring countries. According to our survey on markets in Guangzhou, the price of 1 turtle in Southeast Asia is about 1 USD, the import price is about 1.5 USD, but the retail price in a Chinese market is about 4–5 USD. Such a high profit is another reason driving traders to import turtles. The CITES parties should ensure the export will not be detrimental to the survival of that species, but review on significant trade is a long procedure, and sometimes traders may get permits without limitation. Thus, listing turtle and tortoise species in CITES cannot effectively protect these species, except if parties make a nondetriment finding on a case by case basis.
According to the survey taken by CNMA in 2002, there are turtle farms breeding M. reevesii, M. sinensis, and M. mutica in China. All turtles in captivity were estimated or calculated at about 5 million individuals. Since 2001, it is estimated that 2.6 to 3 million turtles have been produced by farms, which could partially satisfy the market demand (Endangered Species Import and Export Management Office of the People's Republic of China 2002). However, work done by Shi et al. (2007) considered that turtle farms are a problem mainly because they are the primary purchasers of wild-caught turtles because farm-raised turtles show a marked decrease in reproductive capability.
Comparing Tables 1 and 2, it is clear that the variety of products or specimens is much less in imports than it is in exports. This means that China is not only a range and consumer country, but also a processing country for turtles and tortoises. Zhang et al. (1998) considered that C. amboinensis may be only distributed in the southwest fringe of China (but without reliable field records); thus, all or at least a very large proportion of the large quantity of this species comes from imports.
Although the evaluating scores used in this study are arbitrary, the results are still comparable with results from other sources. For example, the risks calculated for M. reevesii and P. sinensis are relatively low. This is similar to the assessment in the China Red Data Book of Endangered Animals (Zhao 1998). In this study, most tortoises and freshwater turtle species in China are considered endangered or vulnerable except M. reevesii and P. sinensis. Among the species in significant trade, the average scores of I. elongata, C. flavomarginata, and P. megacephalum are higher than or equal to 1.5, so they should be prioritized for conservation action.
Except for some rare species, most turtles and tortoises in China appear in international trade. Considering that identifying turtles and tortoises is generally difficult, some rare species may also be mixed with others in trade.
Because turtles usually have low reproductive rates and late maturity, the exploitation of turtles and tortoises is generally considered to be unsustainable. The 12th and 13th Conference of Parties of CITES, which were held in 2002 and 2004, respectively, decided to include several additional turtle species involved in international trade in CITES Appendix II. The CITES Animals Committee is reviewing the status of selected species in significant trade, which will be helpful for monitoring and controlling trade. However, the procedure of significant trade review takes a long time. The Chinese government cannot formulate import quotas to control the trade volume, because it lacks the legal framework to do so. Indonesia and Malaysia are the only exporting countries in Southeast Asia which have set export quotas for CITES species. Information on wild populations is often insufficient, nondetriment findings are not strictly implemented, and the traders may obtain export permits without quantity limitation, and the import countries do not have the mechanism to reduce import quantities if a legal permit for export is provided, so the trade volume is not controlled efficiently.
The reproductive period of tortoises and freshwater turtles is usually long, and some references are still deficient for the species endemic to China. Therefore, some important parameters (e.g., survivorship of juveniles, age at maturity, population density) for species assessment are unavailable. This deficiency might affect species assessment. For example, high mortality of juveniles may counteract the high reproductive rate, and the risk to species may be underestimated. For some rare species, the scores of some variables are absent. All these affect the result of this study; the average score coming from only 3 or 4 factors may not accurately represent the threat that the species is facing.
Some variables may be correlated with each other. For example, species with high medicinal value usually also have high food value. The market price of tortoises and turtles is a result of supply and demand, socio-economic pressure, and population density.
In this study, many species fell into one group due to the following reasons: 1) these species face similar biological and socio-economic pressures, such as long reproductive periods, maturity at late age, and potential to substitute for each other as traditional medicine, and 2) because of limited information, we only chose 5 variables and only estimated the risk scores using 3 categories instead of 4 or more categories as other studies (e.g., Filippi and Luiselli 2000; Zhou and Jiang 2005). However, the results still indicated that listing only some chelonian species in CITES will not solve the problem, since most of the species face similar pressures. If we control or suspend trade in 1 species, the traders will quickly shift to other species that are not subject to legislated control.
MANAGEMENT IMPLICATIONS
Many researchers have reported the decrease of tortoises and turtles worldwide (Gibbons et al. 2000). Habitat degradation, environmental pollution, and alien species problems jointly imperil the survival of chelonians, but the most serious problem is over-exploitation. Gong et al. (2006) investigated the turtle trade in Nanmao, Hainan Province and considered that the main factors leading to illegal trade in turtles were a cultural tradition of turtle use, lack of conservation education, incentive for financial rewards, and insufficient law enforcement. Emergency efforts should be taken to enhance conservation of chelonians in China, including the following:
Enhance Conservation and Management of Natural Habitat
Currently, China has only 2 nature reserves established especially for protecting turtles and tortoises: one aimed to protect sea turtles located in Hainan Province; another aimed to protect Testudo horsfieldii located in the Xinjiang Uigur Autonomous Region. We need to establish more reserves to improve the survival of chelonians in China.
Enhance Legislation
The analysis above indicates that most turtle or tortoise species in China face similar risks (including biological and socio-economic pressure), but only some have been listed in CITES Appendix I or II (although most of them are in Appendix III as an interim measure), or listed as the national key protected wild animals (5 species are protected by Chinese law). Species in Appendix III of CITES are not subject to nondetriment finding, while species that are not nationally protected do not have sufficient control on exploitation.
In order to control both international and national trade, we recommend listing all turtle and tortoise species in China, except P. sinensis, in CITES Appendix I or II because the Chinese law will regard those species in CITES as national key protected species automatically. Although M. reevesii has less biological pressure than other hard-shelled species according to the analysis above, and captive breeding of this species is common, CITES listing or national protection is still important to protect wild population for the following reasons: 1) this species still faces quite high socio-economic pressure; 2) farms may purchase wild caught individuals to improve the captive population (Shi et al. 2007); 3) generally people, except the experts on chelonians, can easily identify P. sinensis, but mix all hard-shelled turtles.
Establish an Effective Management System for Turtle Farming, Enhance Research on Captive Breeding of Turtles, and Prohibit Collection from the Wild
In 2003, the State Forestry Administration of China promulgated a list of 54 wildlife species that can be bred successfully in captivity and are therefore allowed for commercial trade. The list includes P. sinensis and T. scripta. This is a good initiative for wildlife management. But further measures should be taken to manage farms, including formulating turtle farm standards; reviewing the licenses of all turtle farms; registering detail information; labeling all live turtles and their parts or products; closing farms without adequate techniques; and combating illegal collecting, purchasing, and selling activities of farm owners.
Establish a Trade Monitoring System in China
The national and international markets should be periodically investigated to discover species of conservation concern.
Carry Out Surveys on Wild Populations of Chelonians
This will serve as the baseline for monitoring, conservation, and management.
Carry Out Projects on Public Awareness
Projects should include trying to change the consumptive habits of people living in the southern provinces of China, thus decreasing the market demand for wild turtles and tortoises.
Composition of live turtles and tortoises exported from China (A) and imported into China (B) during 1998–2002.
Two-dimensional plot of scores for individual species of chelonians on components 1 and 2 using a VARIMAX rotation model PCA, showing 4 separate groups of species. Abbreviation of species: Cd: Cyclemys dentata, Cf: Cuora flavomarginata, Ct: Cuora trifasciata, Cg: Cuora galbinifrons, Gs: Geoemyda spengleri, Ie: Indotestudo elongata, Mi: Manouria impressa, Mr: Mauremys reevesii, Mmu: Mauremys mutica, Ms: Mauremys sinensis, Pm: Platysternon megacephalus, Ps: Pelodiscus sinensis, Sq: Sacalia quadriocellata, Ts: Trachemys scripta elegans. The positions of C. flavomarginata and Platysternon megacephalus overlap, the positions of M. sinensis and C. trifasciata overlap, and the positions of M. reevesii and P. sinensis overlap.
