Editorial Type: ARTICLES
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Online Publication Date: 06 Jan 2025

Global Testudo Trade: Update and Recent Trends

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Article Category: Research Article
Page Range: 161 – 168
DOI: 10.2744/CCB-1643.1
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Abstract

This study examines the global trade dynamics of Testudo tortoises from 2006 to 2021, using data from the CITES database, and compares it to a prior study between 1975 to 2005. The analysis covers trade volumes, patterns, and sources, highlighting discrepancies in reported figures and the impact of illegal trade. Over this period, 125 countries imported and 97 countries exported Testudo species, with the majority of transactions involving Testudo hermanni, Testudo horsfieldii, and Testudo graeca. The United States emerged as the largest importer, and Germany was the leading exporter. A significant portion of the trade involved live tortoises for the pet industry, with captive-bred sources surpassing wild-caught specimens in later years. However, discrepancies between declared imports and exports suggest ongoing challenges in trade regulation. Statistical analysis indicated varying trends among species, with a noticeable decline in the T. horsfieldii trade after 2017. The study emphasizes the need for enhanced regulatory enforcement and consumer awareness to mitigate illegal trade and promote sustainable practices. It also calls for continued international cooperation to address the socioeconomic drivers of wildlife trafficking. The findings aim to inform policy interventions and conservation strategies to ensure the long-term sustainability and welfare of Testudo populations.

Wildlife trade is the buying and selling of wild animals and plants for various purposes, including food, medicine, pets, and ornamental purposes. The global wildlife trade is a major driver of species decline (Hughes 2021). The scale of the wildlife trade is vast, with millions of wild animals and plants traded each year, both legally and illegally (Hughes 2021; Morton et al. 2021).

The IUCN and several volunteer specialists involved in the Species Survival Commission are essential collaborators for Convention on International Trade in Endangered Species (CITES) parties and the Secretariat. This ongoing partnership aims to ensure that the actions of the parties are informed by the most reliable scientific evidence. Species are categorized into 3 distinct appendices, each imposing varying regulations on international trade based on the specific appendix. Appendix I comprises species that are endangered, and Appendix II encompasses species that are not necessarily endangered but require regulated commerce to prevent threats to their survival. Appendix III comprises around 200 species for which a single nation is soliciting assistance from other parties for their conservation. Commercial international trading in wild-caught specimens of species listed in Appendix I is often forbidden. Trade in species listed in Appendix II and Appendix III is authorized, contingent upon laws that guarantee legality, traceability, and nondetrimental impact on the existence of those species. IUCN expertise is critical in providing information and guidance to parties regarding species trade, conservation, and biological status, as well as aiding in the development of their assessments and proposals. However, CITES and the IUCN Red List possess distinct scopes and methodologies. The CITES appendices may or may not include an IUCN-endangered species, depending on how much trade poses a major threat to the species. Conversely, a species listed in CITES Appendix I or II may not necessarily be classified as critically endangered by the IUCN, yet it may still encounter trade-related threats.

Legal trade is subject to regulations and permits designed to ensure that it is sustainable and does not harm wild populations or ecosystems. However, illegal trade, which involves the smuggling and trafficking of wild animals and plants, is a major concern (D’Cruze et al. 2015). It is estimated that the illegal wildlife trade is worth billions of dollars annually, making it one of the largest illegal industries in the world (Pires and Moreto 2016). The illegal part of this trade is a global conservation issue that threatens thousands of species, including fish, fungi, medicinal plants, and charismatic mammals (Phelps et al. 2016).

The impact of wildlife trade on biodiversity and conservation is significant, as it can lead to declines in population numbers and even the extinction of species (Hughes et al. 2023a). The trade can also affect ecosystems by disrupting food webs and other ecological processes. Additionally, wildlife trade, as it can threaten livestock, international trade, rural livelihoods, native wildlife populations, and the health of ecosystems, can also pose a risk to human health through facilitating the spread of zoonotic diseases (Bezerra-Santos et al. 2021), such as COVID-19, which is believed to have originated in a wildlife market in China. Outbreaks resulting from the wildlife trade have caused hundreds of billions of dollars of economic damage globally (Karesh et al. 2005).

Reptiles are among the most sought after in wildlife animal trade for their unique characteristics and aesthetic value, which has led to their capture and trade on a global scale (Robinson et al. 2015). However, this trade has had significant implications for the conservation and welfare of reptiles, as many species are harvested from the wild and subjected to poor conditions during transport and captivity (Hughes 2021). The trade of reptiles is a multi-billion-dollar industry that involves the capture, breeding, and sale of reptiles for a variety of purposes, including the pet trade, scientific research, and the production of leather and other products. The pet trade is the largest sector of the reptile trade, with millions of reptiles traded each year for use as pets (Robinson et al. 2015). Tortoises are one of those pets and one of the oldest living creatures on earth, with some species believed to have been around for more than 200 million years (Graciá et al. 2020).

The trade in tortoises can be broadly divided into 2 categories: legal and illegal. Legal trade in tortoises refers to the sale and trade of individuals that are captive-bred or have been legally sourced from the wild, with appropriate permits and licenses (Hughes 2021). This trade is subject to strict regulations, particularly for species that are endangered or threatened. Illegal trade, on the other hand, refers to the sale and trade of tortoises that have been illegally sourced from the wild, often through poaching and smuggling. Illegal trade in tortoises is a significant problem, with thousands of animals taken from the wild each year to meet demand in the pet trade and for their meat and shells. This has led to the decline of many tortoise populations and, in some cases, their extinction (Luiselli et al. 2016; Mandimbihasina et al. 2020). In addition, the trade often involves cruel and inhumane practices, with animals transported in cramped and unsanitary conditions (Hughes 2021).

The genus Testudo is a species of tortoise found throughout northern Africa, western Asia, and Europe (Türkozan et al. 2008, 2023). Three taxa (Testudo graeca, Testudo horsfieldii, and Testudo hermanni) were classified as vulnerable (VU) in the IUCN Red List assessments, whereas Testudo marginata was categorized as least concern (LC). All taxa were incorporated into Appendix II of CITES, with the exception of Testudo kleinmanni, which was designated as critically endangered (CR) and included in Appendix I of CITES. Because of its popularity as a pet and its cultural significance in some areas, T. graeca specifically has become a target of illegal trade (Nijman and Bergin 2017). Illegal trade in Testudo tortoises poses a serious threat to the species, because it often involves the poaching of wild individuals from their natural habitat (Auliya et al. 2016). This has resulted in declines in population numbers and the fragmentation of populations, which can negatively impact genetic diversity and increase the risk of extinction (Türkozan et al. 2008). Additionally, the conditions in which illegally traded tortoises are kept are often poor, leading to suffering and disease (Jacobson 1994).

Efforts to combat the illegal trade in T. graeca include stricter enforcement of laws and regulations, raising awareness among consumers and the public, and promoting sustainable alternatives such as captive breeding. The European Union has implemented regulations to control the trade of T. graeca, including requiring permits for their trade and banning the importation of wild-caught individuals through the EU Wildlife Trade Regulations, which mainly originate from CITES. However, the illegal trade in Testudo species remains a significant problem, with the demand for the species continuing to drive illegal activity (Auliya et al. 2016). As such, further action is needed to tackle the root causes of the trade, including reducing consumer demand and addressing the social and economic factors that drive poaching and smuggling.

This paper highlights an updated and comprehensive overview of the global trade in Testudo species, focusing on recent trends, developments, and comparison to previous trends. By synthesizing the latest available data from CITES and scholarly research, the objective of this research is to clarify the status of Testudo trade, including patterns of demand, supply, and declared trade. Additionally, this paper seeks to analyze the underlying drivers and factors influencing the trade dynamics, such as regulatory frameworks, socioeconomic factors, and conservation efforts. By doing a comprehensive analysis of these elements, the paper aims to contribute to a better understanding of the challenges and opportunities associated with the global Testudo trade, and to inform future policy interventions and conservation strategies aimed at ensuring the sustainability and welfare of Testudo populations worldwide.

METHODS

The data on Testudo species exports and imports from 2006 to 2021 from the CITES database were supplied in the form of a compiled comparative tabulation table by United Nations Environment Program/World Conservation Monitoringnter (CITES Wildlife Tradeview 2023). The database contains information on the quantity of specimens exported or imported, the countries involved in the trade, species import terms, import purposes, and sources of specimens. The data set on declared exports and imports reported still shows major discrepancies in figures since 2005. To illuminate significant inconsistencies in reporting, the data set on declared exports was employed. The database does not include information from illegal or unreported trade. Therefore, the data we present here still reflect a minimum value of actual international trade between 2006 and 2021.

The data have been analyzed with Excel, using filtering and sorting tools to distinguish between categories (species, years, source, importing countries, and exporting countries) to later make tables from which figures were then created. The data were further analyzed with GNU PSPP Statistical Analysis Software Release 2.0.0-g5b54d1 (PSPP v2.0.0; 2015) to perform statistical analysis tests such as paired samples t-tests, bivariate correlations tests, and regression and ANOVA analysis to test for significance between data.

RESULTS

Over the 16-yr period from 2006 to 2021, 125 importing countries and 97 exporting countries were reported as involved in the Testudo trade (Supplemental Tables 1 and 2; all supplemental material is available at http://dx.doi.org/10.2744/CCB-1643.1.s1). A total of 3871 transactions were reported, with the United States having 12.4% of the importing transections, followed by Japan (11.6%), the Republic of Korea (7.9%), Germany (7.4%), and the United Kingdom (6.5%). The main exporters were Germany (14.7%), Uzbekistan (11.3%), Ukraine (7.3%), Switzerland (7%), Hong Kong (5.3%), and the United States (5.1%). Of these transactions, 33.6% were T. hermanni, 28.6% T. horsfieldii, 25.6% T. graeca, and 10.5% T. marginata. A total of 96.2% of the transactions were live tortoises. The main purpose was trade (66.6%), personal (27%), and educational (1%). The main source was tortoises bred in captivity (58.3%), taken from the wild (10.6%), born in captivity (10.5%), ranched tortoises (6.7%), and confiscated or seized (4%). From the importing countries, 38% have been trading for up to 2 yr, and only 22% have been trading for 10 yr and above within these 16 yr.

Of the main importing countries, Switzerland has been trading the longest consistently for 46 yr importing and 44 yr exporting. The United Kingdom and the United States have been trading consistently for 45 yr importing. The United Kingdom has been exporting for 44 yr, the United States for 40 yr, and Türkiye for 39 yr. Japan has been importing for 27 yr, yet Germany has been importing consistently only for 26 yr and exporting for 31 yr.

Uzbekistan, Ukraine, Jordan, North Macedonia, the Syrian Arab Republic, Slovenia, and Türkiye dominate the export percentage with a coverage of 93.7% (Table 1), whereas importing is dominated by the United States, France, the United Kingdom, Japan, Italy, Hong Kong, and Germany with a coverage of 73.7% (Table 2).

Table 1. Number of Testudo spp. tortoises exported between 2006 and 2021, cross-tabulated by dominating countries and data reported by exporters across each taxa category. The country codes are as follows: UZ = Uzbekistan, UA = Ukraine, JO = Jordan, NMK = North Macedonia, SY = Syrian Arab Republic, SI = Slovenia, TR = Türkiye.
Table 1.
Table 2. Number of Testudo spp. tortoises imported between 2006 and 2021, cross-tabulated by dominating countries and data reported by exporters across each taxa category. The country codes are as follows: US = United States of America, FR = France, GB = United Kingdom of Great Britain and Northern Ireland, JP = Japan, IT= Italy, HK = Hong Kong, DE = Germany.
Table 2.

A total of 2,110,486 individual Testudo tortoises was recorded in the trade by exporters between 2006 and 2021. Similar to the period 1975 to 2005, 5 Testudo species were still involved in this period of trade (Tables 1 and 2). Across exporting and importing, T. horsfieldii remained the highest in demand, accounting for 67% and 66.9%, followed by T. hermanni (17.5%, 17.8%) and then T. graeca (13.8% for both). Testudo horsfieldii exceeded its highest export since 1976 in 2017 with 164,840 individuals traded in total that year, before steadily declining to 5688 individuals in 2021. The decline in demand for T. graeca can be seen until 2011, when a brief increase in export can be found, before it begins to fluctuate and experience a steady decline (Fig. 1). The trade in T. kleinmanni has remained small since its first reported trade in 1986, with the highest trade amount, between 2006 to 2021, being 1002 individuals in 2015, which is not unexpected with the species being on IUCN Red List and assessed in 2003 and 2022 as “Critically Endangered”. The trade in T. marginata has similarly been small, with a maximum of 4841 individuals traded in 2017. A very small increase has been building sporadically between 2006 and 2017. In 2021, a clear, large decline was seen in individuals traded across almost all species, which could be an effect of the 2020 COVID-19 global pandemic with different legislation across each country.

Figure 1.Figure 1.Figure 1.
Figure 1. Trading volume across a 47-yr period of the 3 most in-demand species of Testudo spp. with a broken line distinction between past trend and current trend (1975–2005 and 2006–2021).

Citation: Chelonian Conservation and Biology:lebrating 25 Years as the World’s Turtle and Tortoise Journal 23, 2; 10.2744/CCB-1643.1

When testing the trend data across the 3 species, through a paired samples t-test and bivariate correlation test, a larger correlation was found between T. horsfieldii and T. hermanni frequencies (p < 0.05) than between T. graeca and T. hermanni and T. horsfieldii and T. graeca (p > 0.05). However, when testing the data with regression analysis, T. hermanni and T. graeca showed a correlation between each taxa’s frequency and the years (p < 0.05 and p < 0.001), whereas T. horsfieldii indicated no correlation (p > 0.05).

The largest source of animals for trade between 2006 and 2021 were wild (34%) Testudo tortoises caught for trading, closely followed by captive-bred (33%), others (21%), born in captivity (10%), and unknown (2%) (Fig. 2). Wild-sourced Testudo individuals have been the most popular source from 2006 to 2013 and then again in 2017; captive-bred has also shown to be a popular source, and born in captivity has been the least popular (Fig. 3). The number of individuals sourced from born in captivity was very consistent until 2011, when it slowly began to decline before steadily rising between 2016 and 2020. It then peaked in 2020 at its highest number of individuals sourced (40,335). Captive-bred also had a small second peak in 2020, just after wild-sourced had one of its largest declines in 2019. However, wild-sourced and captive-bred both had their largest number of individuals sourced in 2017, with 88,517 for wild-sourced and 83,030 for captive-bred.

Figure 2.Figure 2.Figure 2.
Figure 2. The source of animals involved in trade between 2006 and 2021. (C = Captive bred, W = Wild, F = Born in captivity, U = Unknown (including unreported), Others = Ranched, Pre-convention, Confiscation/seizures, Captive bred/artificially propagated.

Citation: Chelonian Conservation and Biology:lebrating 25 Years as the World’s Turtle and Tortoise Journal 23, 2; 10.2744/CCB-1643.1

Figure 3.Figure 3.Figure 3.
Figure 3. Frequency of 3 most popular sources for Testudo spp. individuals across a 47-yr period (C = captive bred; W = wild, F = born in captivity) with a broken line distinction between past trend and current trend (1975–2005 and 2006–2021).

Citation: Chelonian Conservation and Biology:lebrating 25 Years as the World’s Turtle and Tortoise Journal 23, 2; 10.2744/CCB-1643.1

Of the most in demand species, 71% of T. horsfieldii is sourced from wild-collected, whereas every other species is mostly sourced from captive-bred. This large number for wild collection may result from increases in poaching for trafficking and pets for local people. The only exception is Testudo spp. with 50% sourced from each of the 2 most popular forms of sourcing Testudo tortoises (Table 3). Between 1975 and 2005 wild collecting was the most popular source for T. gracea, T. kleinmanni, and Testudo spp. as well as for T. horsfieldii. Another category was added because of the increase in quality of the information being reported. Most of the individuals in declared export were live animals (99%), but the other 1% was made up of specimens, derivatives, carapaces, bodies, bone pieces, carvings, and other items.

Table 3. Differences in Testudo spp. numbers between captive-bred (C), wild-collected (W), and born in captivity (F).
Table 3.

A visible difference exists between the quantity of declared imports and exports each year (Fig. 4). Most years (81.25%) have a higher quantity of declared exports; 2014–2018 and 2020 have a substantially higher quantity of declared exports. The years 2008, 2010, and 2021 are the only ones with a higher quantity of reported imports. Figure 4 shows that exporting had its highest quantity reported in 2017 with 226,432 individuals exported. Following that, 2018 was the year with the highest quantity of imports with several 145,039 individuals reported.

Figure 4.Figure 4.Figure 4.
Figure 4. The trends showing quantity of declared imports and declared exports of Testudo spp. individuals reported yearly from 2006 to 2021.

Citation: Chelonian Conservation and Biology:lebrating 25 Years as the World’s Turtle and Tortoise Journal 23, 2; 10.2744/CCB-1643.1

Across the 16-yr period, a total of 1,411,150 T. horsfieldii individuals were declared as exported, and only 1,135,871 were declared as imported, leaving the largest difference of 275,279 (Fig. 5). Testudo graeca had the next largest difference between declared import and export (54,017), followed by T. hermanni (53,720), T. marginata (9267), Testudo spp. (2730), and T. kleinmanni (959). Testudo hermanni had the second highest quantity of individuals traded, with 83,904 more individuals declared as exported than T. graeca. Testudo spp. had the lowest number of individuals declared as exported with just 7 but a declared imported number of individuals of 2737.

Figure 5.Figure 5.Figure 5.
Figure 5. Quantity of declared imports and exports of Testudo spp. individuals reported yearly from 1975 to 2021.

Citation: Chelonian Conservation and Biology:lebrating 25 Years as the World’s Turtle and Tortoise Journal 23, 2; 10.2744/CCB-1643.1

DISCUSSION

Between 1975–2005 and 2006–2021 an increase was seen in the number of importing countries (125) by 67 but a decrease in the number of exporting countries (97) by 15. An increase was also seen in the number of transactions (3871) by 974 and by the number of individuals traded (2,110,079) by 47,790. This is likely because the reptile trade and pet trade is a multibillion-dollar industry that just keeps growing, as our data currently indicate (Robinson et al. 2015).

Globally a shift was seen in the main 7 exporting and importing countries between 1975–2005 and 2006–2021. Türkiye (TR) went from being the main exporting country of the 7 to being the lowest exporting country of the group, decreasing its trade by 20%, whereas Uzbekistan (UZ) went from being the third lowest of the 7 to the highest exporter, increasing by 46.2% in the trading table (Table 1). The trading period between 2006 and 2021 saw a loss of the Soviet Union (SU), the former Yugoslavia (YU), Morocco (MA) (“MA” standing for “Maroc”), the Russian Federation (RU), and Unknown (XX) but a gain of Ukraine (UA), North Macedonia (NMK), Slovenia (SI), Jordan (JO), and the Syrian Arab Republic (SY) in their table (Türkozan et al. 2008). The top 7 exporting countries percentage also saw an increase of 12% from 1975–2005 (81%) to 2006–2021. With the splitting up of territory that used to be formally known as the Soviet Union and Yugoslavia, this left room for Ukraine, formerly part of the Soviet Union, and Slovenia and North Macedonia (formerly Macedonia), 2 of the former Yugoslavian countries, to take their place in the top 7 exporting countries (Ljubisavljevic et al. 2011). The loss of trade of unknown countries (XX) within the top 7 indicates that the Testudo trade is being reported at a much more accurate level and that new stricter regulations must be working in tracking the trade of these animals.

The change in the 7 main importing countries displayed a loss in the former East Germany (DD) and Switzerland (CH), but a gain in Hong Kong (HK) and France (FR) (Table 2) (Türkozan et al. 2008). Great Britian and Northern Ireland (GB) went from being the top importers to the third highest importers, losing 18.5% of their trading volume. Italy (IT) has gone from being the lowest of the 7 main importers to being the second highest importer, gaining a total of 9.6% of importing trade. Germany (DE) went from being the second highest importer to being the fourth highest, dropping 15% of importing trade. The United States (US) has gained 9.4% of trade since 1975–2005, and Japan has lost only 0.9%, leaving it the fifth highest importing country. Like the top 7 exporting countries, the top 7 importing countries percentage also saw an increase of 6.7% from 1975–2005 (67%) to 2006–2021. This change in importing by European Union countries from 2006 onwards could be a result of the European Union becoming a full party to CITES in 2005, helping to escalate the previous adoptions of CITES regulations that had started in 1984 (Stefes 2021). The increase in reptile trade for Hong Kong gaining it a place in the top 7 importing countries could have to do with the fact that many species of freshwater turtles and Testudo species are traded not only as pets but also with the intention of consumption in this region and within China (Luiselli et al. 2016). The United States becoming the highest trading country is not surprising because of its already established, yet constantly growing, pet trade and primentral geographic location for trading (Robinson et al. 2015).

Between 2006–2021 Switzerland, the United Kingdom, and the United States continued to consistently trade through both importing and exporting. Japan also continued importing consistently; Germany on the other hand was only consistently importing trading Testudo species for another year (2006) before 2 hiatuses, 1 until 2010 and again until 2019, when their last importing transaction was reported up until the end of the 2021 period. Germany was also consistently exporting for 31 yr up until 2010, when their last exporting transaction was reported. Germany has suffered from a large amount of illegal trading of reptiles (Auliya et al. 2016; Stefes 2021), which could have caused an impact on their legal trading. Türkiye had also been consistently exporting Testudo tortoises for 39 yr up to its last exporting transaction reported in 2017. With the decline in reptile populations worldwide, it makes sense that trading of them would decline to try and repopulate before risk of potential loss of species. For Türkiye many threats such as fire outbreaks (2016) and urbanization problems have led to a lower population density in 2016 and 2017, which alongside many other effects such as overgrazing and agricultural intensification could be a small part in the decline of Testudo exports from Türkiye (Arslan et al. 2021).

The total of transactions increased from 1975–2005 by almost 1000; however, the number of traded individuals increased by only over 45,000. Across the total number of transactions made between 1975 and 2005 each transaction averaged 712 individuals, yet between 2006 and 2021 this was an average of 545 individuals in each transaction. This increase in trade despite new regulations may have influenced the number of individuals one can trade in one transaction, but it seems not to have influenced the number of transactions that can be made because this has seen a large increase across a much smaller time frame. This could be a result of under-regulation within the reptile wildlife trade with more than 35% of reptile species being traded online (Marshall et al. 2020).

As seen in Fig. 1, T. graeca proved most popular in 1978, 1980–1981, and 1987–1989, but did not have the highest popularity at any point afterwards all the way through to 2021. Testudo horsfieldii saw the most popularity starting from 1979, as well in 1982–1984 and 1990 and then from 1992 through to 2020. However, in 2021 T. hermanni was the most popular with just under 20,000 individuals traded. The large decline in trading that all species faced in 2021 could be because of the COVID-19 viral outbreak that had an enormous impact on trading and the costs of trading, causing up to a 50% increase in trading costs at times (Vo and Tran 2021). The decline in legal trading of T. graeca could be affected by the increase in illegal trading of the species due to its popularity as pets and significance within some cultures (Nijman and Bergin 2017).

The highest number of T. horsfieldii individuals between 1975–2005 can be seen in 1977, whereas this was higher by more than 38,000 individuals in 2017, supporting the data that the popularity of T. horsfieldii continued to grow despite harsher trading legislations and regulations. Yet for T. graeca and T. hermanni the highest number of individuals traded was in 1978 and never increased from then through to 2021. Testudo hermanni had the lowest popularity out of the 3 most in-demand species, trading almost 85,000 individuals in its peak year, and it was sourced through wild collection for the European pet trade in very large numbers, up until the European tortoise trade was banned in the early 1980s, and it was then the most seized species in Europe in 2019, showing the returned increase in popularity, alongside the conservation programs in Spain, France, and Italy for this species (Rueness et al. 2024).

Between 2006 and 2021, we can see that wild-caught and captive-bred sources have increased considerably when looked at in comparison with the data on source information from 1975 to 2005. Wild-collected has increased by 14%, captive-bred has increased by 28%, and “other” sources have increased by 16% (Fig. 2). Previously between 1975 and 2005, trading individuals were most sourced from unknown sources 70%, wild-sourced 20%, captive-bred 5%, and others 5%. This is greatly improved with unknown sources now making up only 2% of source information. Better reporting of Testudo trading sources gives us a more definitive image for future trading and how it has and may change. The previous gaps in reporting and knowledge have closed considerably since 1975 and should only continue to improve with time, suggesting that CITES regulations are proving to be effective.

When looking deeper into the 5 most in-demand species and the 3 most popular sources, captive-bred (C), wild-collected (W), and born in captivity (F), between 1975–2005 (Fig. 3), we find that for T. horsfieldii (91%), T. graeca (52%), and T. kleinmanni (92%) wild-collected was the most popular sourcing, but for T. hermanni (89.1%) and T. marginata (68.3%) captive-bred was the most popular. The reason for this change is due to a change in national regulations and restrictions on wild collecting of species (Rueness et al. 2024). This popularity shifts from mostly wild-caught to captive-bred between 2006 and 2021 (Table 3), with T. graeca (91.7%), T. hermanni (99.5%), T. marginata (97.3%), and T. kleinmanni (99.3%) all having more than 90% of their traded individuals sourced this way. However, T. horsfieldii, although no longer in the 90% bracket of sourcing from wild-collected, has dropped by only 19.3%, causing an increase in both captive-bred (11%) and born in captivity (21.6%) but still maintaining its most popular sourcing from wild-collected. This is likely because of the lack of national and international protection laws for this species, but information for some countries and their regulations is still lacking (Rueness et al. 2024). Wild collecting is still a main source for illegal trade despite its being the second largest threat to them (Luiselli et al. 2016) with many countries such as Ukraine, the Russian Federation, Slovenia, Pakistan, and Türkiye experiencing extensive activity (Rueness et al. 2024). For many species such as T. hermanni and T. graeca strict regulations are still developing to inhibit the trade of wild-collected species (Rueness et al. 2024), which is likely why a large decline was seen in reported legally wild-sourced species after the large increase in 2016.

Between 1975 and 2005, Testudo trading saw a much higher declared import in individuals than in export individuals, but this changes across 2006 to 2021, when a larger quantity in exports was recorded. This might be affected by the increase in national protection legislations on exporting across many countries involved in wildlife trading.

The visible large discrepancies between annual reported import and export trade seen across both periods (Fig. 4) suggest that there is still much room for improvement when accurate reports are being taken and input. However, this gap in numbers of individuals imported and exported does narrow considerably from 1992 to 2013, signaling that data collection improvements may have been made during that time frame, which could be a result of CITES regulations having a positive effect. Since CITES regulations provided a legal acquisition finding tortify that the specimens have been taken in accordance with national law and forced a biological sustainability finding (nondetrimental finding), such enormous numbers of Testudo tortoises being traded generally did not impact the conservation status of each species where CITES rules applied. Furthermore, the trend is increasing in the source of animals in the direction of captive breeding rather than collection from the wild for the trade in recent decades (Table 3). Moreover, CITES also reviews the appendices regularly to ensure that species are listed in the correct appendix, through a process called the periodic review of the appendices. The IUCN Red List assessments are very important in this regard.

On the other hand, illegal wildlife trade (IWF) persists for Testudo species. Of the transections of exports in the recent study, 4% include confiscated or seized specimens of the genus Testudo. Such illegal collection may cause unnatural selection of desirable traits, create male bias, or decrease the body size of populations (Hughes et al. 2023b). Türkozan et al. (2019) reported male bias and possible population decline on T. hermanni boettgeri population in Türkiye, where the population was overharvested for the pet trade between 1974 and 2005 (Türkozan and Kiremit 2007). Salinas et al. (2011) discussed the possible effect of multiple introductions of North African Testudo populations to Spain for the pet trade and its possible effect on the reduction of genetic diversity. The loss of genetic diversity can lead to inbreeding depression and population collapse in the long term. This effect is more pronounced for the small populations inhabiting smaller areas. Lower genetic diversity and bottlenecks due to a possible founder effect and pet trade were reported for the T. hermanni boettgeri population of Türkiye recently (Yılmaz et al. 2023). Moreover, IWF increases mortality rates during transportation and captivity. In addition, a risk also exists of introducing invasive species and diseases (Mozer and Prost 2023 and references therein).

Acknowledgments

The authors extend thanks to the CITES database team for providing access to the comprehensive data that made this study possible. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

LITERATURE CITED

  • Arslan, D., Olivier, A., Ernoul, L., Béchet, A., and Çiçek,K. 2021. Demography, distribution, and threat assessment of the Spur-thighed Tortoise (Testudo graeca) in the Gediz Delta, Turkey (Reptilia: Testudines). Zoology in the Middle East67(
    3
    ):216227.
  • Auliya, M., Altherr, S., Ariano-Sanchez, D., Baard, E.H., Brown, C., Brown, R. M., Cantu, J. C., Gentile, G., Gildenhuys, P., Henningheim, E., Hintzmann, J., Kanari, K., Krvavac, M., Lettink, M., Lippert, J., Luiselli, L., Nilson, G., Nguyen, T. Q., Nijman, V., Parham, J. F., Pasachnik, S. A., Pedrono, M., Rauhaus, A., Córdova, D. R., Sanchez, M. E., Schepp, U., van Schingen, M., Schneeweiss, N., Segniagbeto, G. H., Somaweera, R., Y.Sy, E., Türkozan, O., Vinke, S., Vinke, T., Vyas, R., Williamson, S. and Ziegler,T. 2016. Trade in live reptiles, its impact on wild populations, and the role of the European market. Biological Conservation204:103119.
  • Bezerra-Santos, M.A., Mendoza-Roldan, J.A., Thompson, R.A., Dantas-Torres, F., and Otranto,D. 2021. Legal versus illegal wildlife trade: zoonotic disease risks. Trends in Parasitology37(
    5
    ):360361.
  • CITES Wildlife TradeView. 2023. UNEP-WCMC and the CITES Secretariat. TradeView.cites.org. Accessed February 2, 2023.
  • D’Cruze, N., Singh, B., Morrison, T., Schmidt-Burbach, J., Macdonald, D.W., and Mookerjee,A. 2015. A star attraction: the illegal trade in Indian Star Tortoises. Nature Conservation13:119.
  • Full CITES Trade Database Download . 2024. Compiled by UNEP-WCMC, Cambridge, UK for the CITES Secretariat,
    Geneva, Switzerland
    . trade.cites.org. Accessed March 3, 2024.
  • GNU Project . 2015. GNU PSPP (Version 2.0.0). Free Software Foundation. Boston, MA. Available from: https://www.gnu.org/software/pspp/.
  • Graciá, E., Rodríguez-Caro, R.C, Ferrández, M., Martínez-Silvestre, A., Pérez-Ibarra, I., Amahjour, R., Aranda, C., Benelkadi, H.A., Bertolero, A., Biaggini, M., Botella, F., Budó, J., Cadenas, V., Chergui, B., Corti, C., Esperón, F., Esteve-Selma, M.A., Fahd, S., García de La Fuente, M.I., Golubovic, A., Heredia, A., Jiménez-Franco, M.V., Arakelyan, M., Marini, D., Martínez-Fernández, J., Martínez-Pastos, M.C., Mascort, R., Mira-Jover, A., Pascual-Rico, R., Perera-Leg, A., Pfau, B., Pinya, S., Santos, X., Segura, A., Semaha, M.J., Soler-Massana, J., Vidal, J.M., and Giménez,A. (2020). From troubles to solutions: conservation of Mediterranean tortoises under global change. Basic and Applied Herpetology34:516.
  • Hughes, A., Auliya, M., Altherr, S., Scheffers, B., Janssen, J., Nijman, V., Shepherd, C.R., D’Cruze, N., Sy, E., and Edwards,D.P. 2023a. Determining the sustainability of legal wildlife trade. Journal of Environmental Management341:117987.
  • Hughes, A.C. 2021. Wildlife trade. Current Biology31(
    19
    ):R1218R1224.
  • Hughes, J.L., Morton, O., Scheffers, B.R., and Edwards,D.P. 2023b. The ecological drivers and consequences of wildlife trade. Biological Reviews. 98:775791.
  • IUCN 2024. The IUCN Red List of Threatened Species. Version 2024-1. Available from: https://www.iucnredlist.org.
  • Jacobson, E.R. 1994. Causes of mortality and diseases in tortoises: a review. Journal of Zoo and Wildlife Medicine25(
    1
    ):217.
  • Karesh, W.B., Cook, R.A., Bennett, E.L., and Newcomb,J. 2005. Wildlife trade and global disease emergence. Emerging Infectious Diseases11(
    7
    ):10001002.
  • Ljubisavljević, K., Džukić, G., and Kalezić,M.L. 2011. The commercial export of the land tortoises (Testudo spp.) from the territory of the former Yugoslavia: a historical review and the impact of overharvesting on wild populations. North-Western Journal of Zoology7(
    2
    ):250260.
  • Luiselli, L., Starita, A., Carpaneto, G.M., Segniagbeto, G.H., and Amori,G. 2016. A short review of the international trade of wild tortoises and freshwater turtles across the world and throughout two decades. Chelonian Conservation and Biology15(
    2
    ):167172.
  • Mandimbihasina, A.R., Frasier, C.L., Hagenson, R.A., Robertson, B.A., Engberg, S.E., Lewis, R.E., Woolaver, L.G., Razafimahatratra, E., Rabetafika, L.L., and LouisE.E.Jr, (2020). Conservation genetics of Madagascar’s critically endangered ploughshare tortoise (Astrochelys yniphora). Conservation Genetics21(
    1
    ):109121.
  • Marshall, B.M., Strine, C., and Hughes,A.C. 2020. Thousands of reptile species threatened by under-regulated global trade. Nature Communications11(
    1
    ):112.
  • Morton, O., Scheffers, B.R., Haugaasen, T., and Edwards,D.P. 2021. Impacts of wildlife trade on terrestrial biodiversity. Nature Ecology & Evolution5(
    4
    ):540548.
  • Mozer, A. and Prost,S. 2023. An introduction to illegal wildlife trade and its effects on biodiversity and society. Forensic Science International: Animals and Environment3:100064.
  • Nijman, V. and Bergin,D. 2017. Trade in spur-thighed tortoises Testudo graeca in Morocco: volumes, value and variation between markets. Amphibia-Reptilia38(
    3
    ):275287.
  • Phelps, J., Biggs, D., and Webb,E.L. 2016. Tools and terms for understanding illegal wildlife trade. Frontiers in Ecology and the Environment14(
    9
    ):479489.
  • Pires, S.F. and Moreto,W.D. 2016.
    The Illegal Wildlife Trade
    , Oxford Handbook Topics in Criminology and Criminal Justice (2012; online edition, Oxford Academic, 2 June 2014).
  • Robinson, J.E., Griffiths, R.A., John, F.A.S., and Roberts,D.L. 2015. Dynamics of the global trade in live reptiles: shifting trends in production and consequences for sustainability. Biological Conservation184:4250.
  • Salinas, M., Altet, L., Clavel, C., Almela, R.M., Bayón, A., Burguete, I. and Sánchez,A. 2011. Genetic assessment, illegal trafficking and management of the Mediterranean spur-thighed tortoise in Southern Spain and Northern Africa. Conservation Genetics12:113.
  • Stefes, C. 2021. Wildlife protection in Germany: sound legislation and deficient implementation. Revista Catalana de Dret Ambiental12(
    1
    ):124.
  • Türkozan, O., Javanbakht, H., Mazanaeva, L., Meiri, S., Kornilev, Y.V., Tzoras, E., Popgeorgiev, G., Shanas, U., and Escoriza,D. 2023. Testudo graeca Linnaeus 1758 (Eastern Subspecies Clades: Testudo g. armeniaca, Testudo g. buxtoni, Testudo g. ibera, Testudo g. terrestris, Testudo g. zarudnyi) – Armenian Tortoise, Zagros Tortoise, Anatolian Tortoise, Levantine Tortoise, Kerman Tortoise. In: Rhodin,A.G.J.,Iverson,J.B.,van Dijk,P.P.,Stanford,C.B.,Goode,E.V.,Buhlmann,K.A., and Mittermeier,R.A. (Eds.).
    Conservation Biology of Freshwater Turtles and Tortoises: A Compilation Project of the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group
    . Chelonian Research Monographs5(17):133.
  • Türkozan, O. and kiremit,F. 2007. Testudo trade in Turkey. Applied Herpetology4:3137.
  • Türkozan, O., Özdemir, A., and Kiremit,F. 2008. International Testudo trade. Chelonian Conservation and Biology7(
    2
    ):269274.
  • Türkozan, O., Yılmaz, C., Karakaya, Ş., Karaman,S., and Ulger,C. 2019. Distribution, size and demographics of eastern Hermann’s Tortoise, Testudo hermanni boettgeri, in Turkey. Chelonian Conservation and Biology18(
    2
    ):210216.
  • VKM Rueness, E.K., Flø, D., Gehrke, B., Grainger, M., Hermansen J.S., Eldegard, K., Järnegren, J., Kausrud, K., Kopatz, A., and de BoerH. 2024. Scientific assessment of risk to the populations of tortoises listed by CITES as a result of trade. Scientific Opinion of the Panel on CITES of the Norwegian Scientific Committee for Food and Environment. VKM Report 2024:1.
    Oslo
    :
    Norwegian Scientific Committee for Food
    .
  • Vo, T.D. and Tran,M.D. 2021. The impact of COVID-19 pandemic on the global trade. International Journal of Social Science and Economics Invention7(
    1
    ):17.
  • Yılmaz, C., Türkozan, O., Karaman, S., and Ülger,C. 2023. Population genetic structure of Testudo hermanni boettgeri (Hermann’s Tortoise) in Türkiye. Turkish Journal of Zoology47:505516.
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Figure 1.
Figure 1.

Trading volume across a 47-yr period of the 3 most in-demand species of Testudo spp. with a broken line distinction between past trend and current trend (1975–2005 and 2006–2021).


Figure 2.
Figure 2.

The source of animals involved in trade between 2006 and 2021. (C = Captive bred, W = Wild, F = Born in captivity, U = Unknown (including unreported), Others = Ranched, Pre-convention, Confiscation/seizures, Captive bred/artificially propagated.


Figure 3.
Figure 3.

Frequency of 3 most popular sources for Testudo spp. individuals across a 47-yr period (C = captive bred; W = wild, F = born in captivity) with a broken line distinction between past trend and current trend (1975–2005 and 2006–2021).


Figure 4.
Figure 4.

The trends showing quantity of declared imports and declared exports of Testudo spp. individuals reported yearly from 2006 to 2021.


Figure 5.
Figure 5.

Quantity of declared imports and exports of Testudo spp. individuals reported yearly from 1975 to 2021.


Contributor Notes

Corresponding author

Handling Editor: Jeffrey A. Seminoff

Received: 12 Aug 2024
Accepted: 28 Sept 2024
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