Amphibians and reptiles have been used as a source of food, souvenirs, traditional and modern medicine, and pets (Paugh et al. 2001). Tortoises represent only a small part of this huge exploitation. The international trade is not the only factor threatening the survival of reptile species and populations, but its impact, together with other negative factors, such as habitat modification and destruction, the introduction of exotic species, and pollution of the environment, is remarkable.

Turtles, in general, face significant conservation challenges, which are particularly acute in Asia because of a demand for their meat for consumption and shells for traditional Chinese medicine (van Dijk et al. 2000; Turtle Conservation Fund 2002). In addition, the global pet trade adds another aspect of threat because it focuses on different species, and trade flows involve different countries, particularly the main importing countries of the European Union, the United States, and Japan (Hoover 1998; Auliya 2003).

Tortoises of the Testudo graeca complex inhabit a range that covers part of 3 continents (Africa, Europe, and Asia) (Fig. 1). Tortoises face serious threats to their survival throughout their range, including habitat destruction and overharvesting for food, traditional medicine, and the pet trade. Lambert (1969) reported that more than 300,000 tortoises were exported every year from Morocco to Britain for pets. He also mentioned the increase of trade after the World War II. Collecting tortoises directly from the wild for the pet trade is one of the factors threatening species of Testudo (Tümrkozan and Kiremit 2007). Noncommercial collection, captive breeding, and uncontrolled release of tortoises into the wild is another problem reported from Spain (Pérez et al. 2004).

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The genus Testudo was included in Appendix II of Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) as early as 1975. More recently, Theile (2002) reviewed the CITES database for the family Testudinidae between the years 1977 and 1999. She emphasized in her study that “the genus Testudo is by far the most important Testudinidae genus, with 1,888,198 live specimens in trade accounting for almost 80% of all recorded trade.” In this review, we, therefore, focused on the trade of genus Testudo and examined it in detail.

Methods. — The data on Testudo exports and imports from 1975 to 2005 from the CITES database were supplied in the form of a compiled comparative tabulation table by United Nations Environment Program/World Conservation Monitoring Center. The database contains information on the numbers of specimens exported or imported, the countries involved in the trade, species import term, import purpose, and source of specimens. The data set on declared exports were used for discussion to show major discrepancies in reporting. Reporting was not complete in the early years of CITES, and, importantly, the database does not include illegal or unreported trade. Therefore, the data we present here reflect a minimum value of actual international trade.

Results. — During a 31-year period, from 1975 to 2005, 58 importing counties and 112 exporting countries were recorded as being involved in the Testudo trade. Of the importing countries, 43% have traded for 2 years or less; whereas, 14% have traded for 20 years or more. Switzerland has traded for the longest period (30 years), followed by the United Kingdom and the United States (29 years each), Germany (25 years), and Japan (22 years). Of the exporting countries, 43% have traded or 2 years or less; whereas, 6% have traded for 20 years or more. Germany has traded for the longest period (31 years), followed by Turkey, the United Kingdom, and Switzerland (28 years each), and the United States (24 years).

Turkey, the former Soviet Union, former Yugoslavia, Morocco, Uzbekistan, Russia, and Ukraine accounted for 81% of the recorded exports; whereas, the United Kingdom, Germany, and the United States dominated the import market with 67% of the individuals (Tables 1 and 2). A total of 2,062,289 individual Testudo were recorded in the trade between 1975 and 2005. Five Testudo species were involved in this trade (Tables 1 and 2). Testudo horsfieldi accounted for 48% of the exports, followed by Testudo graeca (37%) and Testudo hermanni (13%). The trend of each species showed a drastic decline over the years; although, Testudo horsfieldi showed a distinct second trade pulse during the 1990s (Fig. 2). All turtles were in the trade since trade record collection began in 1976, except Testudo kleinmanni, which was first reported in trade in 1986. The declared volume of the trade of T. kleinmanni was very small in comparison with other species, with the highest volume recorded being 2848 individuals in 1994. The trade in Testudo marginata was similar, with the highest volume recorded being 788 individuals in 1997. Testudo horsfieldi, T. graeca, and T. hermanni are subject to the highest recorded trade volumes. Although the trade volume of the latter 2 species showed declines in the last decade, an increasing volume of T. horsfieldi trade after 1992 is remarkable. This is most probably related to the restriction of European Union on pet trade, especially on T. graeca and T. hermanni (these 2 species were included in List A of Annex IV of EU Council Directive 92/43/EEC [Habitats Directive], which require strict protection and in effect prohibiting all commercial trade as of 1994). The trade pulse of T. horsfieldi also follows the collapse of the Soviet Union and the attempts of newly independent East European and Central Asian states to develop their economies in a more open, global trade context.

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Table 1. Numbers of Testudo exported between 1975 and 2005, cross-tabulated by dominant exporting countries (≥7.5% of total trade) and Testudo species accounting for substantial amounts of the total recorded exports in each category.

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Table 2. Numbers of Testudo imported between 1975 and 2005, cross tabulated by dominant import countries (≥2% of total trade) and Testudo species accounting for substantial amounts of the total recorded imports in each category.

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The source of animals in trade (Fig. 3) that was unknown is 70%. However, the proportion of animals in trade recorded as source unknown has declined over time. Of the known sources (614,763 animals), 67% were from the wild, and 16% were declared as captive-bred animals. The main purpose of the import was commercial trade (61%); whereas, 38% was unknown. Database information on the import purpose was available since 1975 with some gaps; however, information on import source was limited and only available after 1980 with huge gaps. The first captive-bred trade report was from 1981 with 4006 individuals; whereas, the first wild source was recorded in 1990. The comparative trend evaluation on import source was only possible between 1990 and 2005 (Fig. 4). Interestingly, both the trend of captive-bred and wild sources followed almost the same pattern, a gradual increase until 1995, a sharp decline in 1996, again a gradual increase until 2000 and a gradual decrease after 2000. This was surprising because we were expecting a negative correlation (especially in the last decade) of wild source animals compared with an increase on captive-breeding sources. Such a negative correlation pattern was only observed in 2002. Unfortunately, trade from the wild persists.

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Of the known sources reported as wild or captive bred, Lebanon (44%) and Jordan (33%) were the main origins of declared captive-bred T. graeca; whereas, Lebanon (39%) and Turkey (35%) were the origins of wild T. graeca. Slovenia (83%) was the main supplier of captive-bred T. hermanni; whereas, Ukraine (87%) was the main supplier of wild T. hermanni. For T. horsfieldi, Ukraine (60%) and Uzbekistan (49%) were the main origin of captive-bred and wild animals, respectively. The United Kingdom (71%) was the main origin of captive-bred T. kleinmanni; whereas, Egypt (96%) was the main supplier of wild stock. For T. marginata, Switzerland (74%) was the main source of captive-bred trade and Romania (52%) for the wild trade. Vietnam (46%) and Germany (42%) were the main exporters of captive-bred Testudo spp. and Malaysia (63%) for the wild (although no wild Testudo occur in Malaysia). The quantitative differences in species between captive bred and wild collected is presented in Table 3. Most of the Testudo tortoises in declared trade were live animals (99%); whereas, the remainder were derivatives, specimens, bodies, carvings, etc.

Table 3. Quantitative differences in species between captive-bred (C) and wild collected (W).

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The total trade volume trend of Testudo tortoises over the 31-year period shows a drastic initial decline with a slight increase after 1995 (Fig. 5). However, while trade volume was decreasing, the frequency of the trade increased. The trade volume was quite high (over 100,000 per year) between 1977 and 1983. This high volume accounted for 60% of the overall Testudo trade. After 1983, the trade volume decreased (less than 50,000 annually) until 2000. At this time, Kazakhstan and Uzbekistan announced annual quotas of T. horsfieldi of 30,000–50,000. A total of 2042 import transactions were recorded during 31 years. The import frequency of the trade ranged from 2 (1975) to 149 (2002), with a mean of 66 trade transactions per year. The highest frequency was observed in the United States (485 transactions) followed by the United Kingdom (335) and Japan (279).

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Discussion. — The countries predominantly involved in the export of Testudo were, not surprisingly, from within the geographical range of this genus. The main importing countries were the United Kingdom, Germany, and Switzerland in Europe (Table 2, values of former Eastern Germany and Germany were combined and evaluated as “Germany”) and to a lesser extend the United States and Japan. Similar high imports into European countries, the United States, and Japan were also reported for chameleon species (Carpenter et al. 2004). An increasing demand from traditional importing countries, such as the United Kingdom, Germany, the United States, and Japan could have major impacts on the future dynamics of the Testudo trade. Theile (2002) emphasized that the “4-inch rule” (=10 cm) imposed by the United States and Canada as a measure to limit trade in potentially Salmonella-bearing farmed hatchlings often deflects trade to wild-collected adult animals. Captive breeding and ranching, even on a commercial basis to supply the pet market, have been suggested for turtles (van Dijk 2000; Theile 2002) and chameleons (Carpenter et al. 2004) to reduce the demand for wild stocks. van Dijk (2000) also noted that commercial breeding might create conditions in which wild turtles are even more valued. In China, turtle farms are reported to be a problem because they purchase wild-caught animals (Shi et al. 2007) to increase their stock of adult breeding animals.

There was a huge discrepancy between declared imports and declared exports (Fig. 5). Although import records declared the trade of 2,062,289 Testudo individuals, the export records declared 1,443,469 Testudo individuals (a 30% difference). However, the quantity of declared export records were higher than imports between 1996 and 2003 (Fig. 5). The leading countries for exports were the former Soviet Union (37%), Uzbekistan (17%), Russia (15%), and former East Germany (9%).

In terms of imports, the United States (19%), unknown (18%), Germany (16%), Japan (14%), and the former East Germany (8%) were the leading countries (see Table 2). The difference between the declared import and export quantities of T. horsfieldi, T. kleinmanni, and T. marginata are not comparable (Fig. 6). Although import sources pointed to a trade of 7127 T. kleinmanni, the re-export records showed a trade of 49,138 animals. When taking into consideration the species distribution and population levels, the uplisting of T. kleinmanni by CITES to Appendix I was an important action for the conservation of this species.

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This study demonstrated that national and international policies were partially successful in regulating the exports of individual species and of individual countries. Turkey was the main supplier of the Testudo trade (Table 1) in the 1970s. However, after the European Union imposed restrictions, the export volume from Turkey decreased sharply after 1984 (Türkozan and Kiremit 2007). Since 2000, in Turkey, the animals for export are captive bred. According to Theile (2002) the decrease in the volume of the world trade in 1980s coincided with the restrictions in the European Union market for a number of popular tortoise pet species, in particular, T. hermanni and T. graeca, which were imported by European Union member states in volumes of more than 100,000 live specimens a year in the 1970s. CITES coming into force in the late 1970s was the start of this strong downward trade tend in at least western Europe. Although the illegal trade of tortoises persists in an unknown volume, which is considered to be smaller than in the past, it is clear that national and international applications have been helpful for the control of mass trade in Testudo tortoises.