Review of Import Trends and Trade Regulations of Live Testudines in Japan
Abstract
This study investigates the import trends of live Testudines into Japan following a previous study on trade in live freshwater turtles and tortoises as pets in Japan from 1980s to the early 2000s. We have observed a declining trend in imports over the past two decades. However, it is important to note that this does not necessarily indicate a shrinking market; instead, it likely reflects changes driven by stricter regulations for trade and ownership as pets.
A large amount of wildlife is traded globally every year, which is worth over a $100 billion (IPBES 2020). In recent years, the global popularity of exotic pets has increased the interest in wildlife trade for pet purposes. Reptiles are one of the most sought-after exotic pets, with the pet trade threatening many species (Auliya et al. 2016). Marshall et al. (2020) analyzed a global online webscrape of reptile retailers and found that three-quarters of traded species are not covered by international trade regulation, that is, the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). In Japan, an active reptile pet market exists (Janssen 2018; Wakao et al. 2018; Sigaud et al. 2023), and reptiles are the fourth most popular group of pet animals, after cats, dogs, and fish, according to the Ministry of the Environment (MoE) survey (MoE 2022a). Squamata has gained popularity in recent years (Wakao et al. 2018). However, Testudines remain the most traded group among registered pet businesses and reflected in import statistics (MoE 2022b).
Historically, turtles have been perceived as familiar to the Japanese because of their symbolism of longevity and depiction in folktales (Yano 2005). There are 5 native taxa of Testudines, with the exception of marine turtles, in Japan (Matsui and Mori 2021): the Japanese pond turtle (Mauremys japonica), Asian brown pond turtle (Mauremys mutica kami), yellow-margined box turtle (Cuora flavomarginata evelynae), Ryukyu black-breasted leaf turtle (Geoemyda japonica), and Chinese softshell turtle (Pelodiscus sinensis). It is believed that these native turtles and Reeve’s pond turtle (Mauremys reevesii), which is considered to have been introduced in the 18th century, were mainly used as pets and for religious release in historical days. However, the custom of releasing animals to accumulate virtues is now considered obsolete in Japan. After World War II, turtle species targeted for the pet trade have shifted to exotic ones, as represented by pond slider (Trachemys scripta) (Lovich and Yamamoto 2016).
Kameoka and Kiyono (2005) analyzed trade data from 1981 to 2001 and conducted a physical market survey of live freshwater turtles and tortoises in Japan in 2002. Their research revealed that the Japanese pet market included numerous exotic species, which might pose a threat to the conservation of target species, and they called for stricter regulations. However, no such research has focused on the trade of Testudines as pets since then. This study aims to examine the changes in Testudines import and the related legislation. If imports have decreased, it suggests that strengthened regulation of domestic trade and ownership has been effective. Conversely, if imports have increased, it indicates that the alarm raised by the previous study did not resonate. Our hypothesis is that the market will not shrink, at least for some time, and will evolve in 2 ways. The first way is that we may see a decrease in the number of wild-caught individuals in the pet market and an increase in individuals bred in captivity, especially those bred in Japan. The second way in which the market may evolve is that traders may explore new target species. We sought to verify this hypothesis by analyzing import trends and legislative changes such as the revision of the Act on the Prevention of Adverse Ecological Impacts Caused by Designated Invasive Alien Species of 2004 (IAS Act).
IMPORT TRENDS
To review the import trend of live Testudines to Japan, we used the trade statistics of the Ministry of Finance of Japan and the trade data of CITES. The Ministry of Finance’s statistical data indicate the value and quantity of goods exported from or imported into Japan by item, country, and period. One caveat is that trade data are not included if their total value is less than 200,000 JPY (approximately $1320). We extracted trade data using the trade item “live Testudines, 0106.20.010” introduced in 2002. Accordingly, we obtained more detailed information on the scale of international trade in Japan than that obtained with the previously available item “live reptiles, 0106.20.” Testudines have been primarily used as food and medicine and are kept as pets worldwide (CITES 2019). According to previous studies, the use of live Testudines in Japan is mainly as pets (Kameoka and Kiyono 2005; Eito 2006; Kitade and Naruse 2020). Unlike other Asian countries, no widespread custom of eating turtles exists in Japan, with the exception of soft-shelled turtles and domestic marine turtles captured by local fisheries. Soft-shelled turtles are farmed and consumed as a delicacy in Japan (Goto 2021), where they are captive-bred in domestic farms or imported from other Asian countries, such as China, the largest producer of captive soft-shelled turtles (FAO 2020). Given that the production of the turtles in Japan has decreased from 360 metric tons in 2009 to 200 tons in 2018 and that the number of domestic aquaculture businesses has been maintained under 100 entities since 2003 (FAO 2020; Goto 2021), it seems that demand has not risen. However, because of the lack of comprehensive information, it remains in the realm of speculation. Notably, the import data of live Testudines includes data other than those for pet purposes. Japan imported more than 717,000 individuals from 35 countries in 2002. This import volume has decreased gradually, reaching a low of 88,028 individuals, which is a mere 12% of the 2002 imports, from 28 countries in 2018 (Fig. 1). Subsequently, it showed a slight recovery after 2019, rising to approximately 100,000 individuals. The low level of imports after 2018 was likely because of economic stagnation and the impact of the COVID-19 pandemic (WTO 2020; Urata 2023). Notably, the import amount and number of export countries has evidently increased since 2020. Compared to the data from the early 2000s—2002 and 2004—new exporting countries such as Vietnam, Mexico, Nicaragua, Italy, and Austria as well as African countries like Egypt, Kenya, and Seychelles have emerged in the data from 2021 and 2022.
Citation: Chelonian Conservation and Biology: Celebrating 25 Years as the World’s Turtle and Tortoise Journal 23, 2; 10.2744/CCB-1640.1
Japan was the top importer of CITES-listed Testudines in 1996, with its import quantities representing almost half of global trade (Kameoka and Kiyono 2005). In this study, we compared data in 1996, when Japan was the largest importer, with data from 2001, the last year reviewed by Kameoka and Kiyono (2005), and 20 years later, 2021.
Table 1 shows the import quantities of live CITES-listed Testudines in 1996, 2001, and 2021, with importer-reported quantities of 27,082, 37,416, and 47,860, respectively. The import quantity in 2021 was approximately 1.7 times that in 1996. The numbers of listed species have changed over the years (Table 1). The number of Appendix-listed species was 93 in 1996 and 107 in 2001 and drastically increased to 193 in 2021. CITES requires parties to report their trade records including the source of the specimen of the Appendix-listed species annually. Looking at the percentage of wild-caught individuals would help to determine the direct impact on wild populations. The decrease in the percentage of wild-caught individuals was inversely proportional to the increase in listed species. In 1996, 72% of imported Testudines were wild-caught, decreasing to 65% in 2001 and to only 5% in 2021. Given that many of the species traded as pets in Japan are of foreign origin (Kameoka and Kiyono 2005; Wakao et al. 2018), the increase in CITES-listed species and decrease in the import quantities of wild-sourced individuals indicates that international trade restrictions may have contributed to the change in species found on the pet market. The influence of other domestic regulations in this situation remains to be investigated.
REGULATORY CHANGES SINCE 2001
Legislation such as the Foreign Exchange Law of 1949, which is the collateral law of CITES, the Act on Conservation of Endangered Species of Wild Fauna and Flora (ACE) of 1992, the IAS Act, and the Act on Welfare and Management of Animals of 1973 regulate the trade and ownership of Testudines in Japan (Table 2).
The ACE limits the domestic trade of designated endangered native species referred to as “nationally rare species of wild fauna and flora (nationally rare species)” and “internationally rare species of wild fauna and flora (internationally rare species),” which are species listed in CITES Appendix I and in bilateral conventions and agreements for the protection of migratory birds. In 2001, there were no protected native Testudines. In 2020, the Ryukyu black-breasted leaf turtle became the only native turtle protected as a nationally rare species, which prohibited its capture, international and domestic trade, and display without special permission. The domestic trade of CITES Appendix I–listed species is prohibited in general, but commercial trade of this species is possible if the individual was imported before the CITES Appendices came into force or if it the offspring of a pre-Convention specimen and the owner has registered it in accordance with the act. The internationally rare species of Testudines were represented by 21 and 32 taxa in 2001 and 2021, respectively.
The IAS Act aims to prevent adverse effects on ecosystems caused by invasive alien species by regulating the ownership, possession, import, trade, sale, release, and transport of live specimens. It is prohibited to trade and own species specified as “designated invasive alien species (designated IAS)” with very limited exceptions. The common snapping turtle (Chelydra serpentina), Chinese stripe-necked turtle (Mauremys sinensis), and hybrids of M. sinensis × M. Japonica, M. sinensis × M. mutica, and M. sinensis × M. reevesii fall under this designation. The common snapping turtle was designated in 2005, and the other turtle species were specified as designated IAS in 2016. A certificate of identification is required to import species that are not subject to designated IAS but belong to the same higher taxa, i.e., Chelydridae, Mauremys, and hybrids of M. sinensis and Geoemydidae. This highly restrictive act was introduced in June 2005.
The Act on the Welfare and Management of Animals had 2 major purposes: preventing animal cruelty and preventing animals from causing an infringement on humans and their lives. To achieve the latter, the act designated animals that may cause physical or economic harm to humans as “specified animals” and required owners to obtain permission for their possession and ownership since 2006. The specified animal system in the act has been tightened, and their possession and ownership as pets have been prohibited since June 2020. Approximately 650 species are on the list of specified animals. Chelydridae, except for the common snapping turtle, is the only family under Testudines on the list. The common snapping turtle is exempt because it is covered by the IAS Act. Furthermore, it covers businesses related to animals in Mammalia, Aves, and Reptilia, such as breeders, traders, retailers, and exhibitors, including zoos, pet hotels, and salons. These businesses are required to register with the local authorities in advance and renew their registration every 5 yr. This regulation first applied to businesses handling mammals and birds; subsequently, its scope was extended to businesses handling reptiles upon its revision in 1999.
DISCUSSION
Change in the Market. —
Several significant changes have been made to domestic legislation related to the trade and keeping of exotic pets in the past 20 yr. Regulations related to the trade and ownership of Testudines have been tightened in line with the growth of global recognition of the negative impacts of pet use on species conservation (CITES 2019). The 17th meeting of the Conference of the Parties of CITES in 2016, which established several changes to the trade regulation for Testudines, may have caused the decrease in their import volume in Japan around 2018. Kameoka and Kiyono (2005) reported the top 20 most frequently observed species in 2002. Thirteen of them were CITES Appendix II–listed species, and they displayed no restrictions for domestic trade, i.e., all 20 species could be legally traded at the time. After several legal revisions, the alligator snapping turtle (Macrochelys temminckii) became a specified animal under the Animal Welfare Act, and its ownership was prohibited. The Indian star tortoise (Geochelone elegans), which was sold in 93.8% of surveyed pet stores in Japan in 2002, and 4 other species were listed CITES Appendix I and then designated internationally rare species, whose commercial import is prohibited (Kameoka and Kiyono 2005). Domestic trade is also banned except for registered individuals. This means that 6 species from the former 20 popular species cannot or can hardly be traded as pets since 2020. It is easy to suggest that strengthened regulation of domestic trade and ownership leads to decreased import volume. Did it lead to the pet market shrinkage? We want to see if our hypothesis of the first way to the market evolution.
Many CITES-listed species have been historically conceived as commodities, which means that many people know how to breed them. Of course, the commercial motivation should contribute to improving breeding techniques. This has probably encouraged the trend that the increasing recognition of the risk of zoonosis promotes the avoidance of wild-caught individuals, which may carry unknown pathogens (WWF 2020). It is also well known by exotic pet breeders/distributors and veterinarians that wild-caught individuals can be infected with parasites or mites that can cause disease in them and/or in humans (Rataj 2011). This trend can explain the increase in the percentage of imports of source “C” individuals bred in captivity. The second way is that businesses explore new target species. It is well known that demand shifts to nonregulated alternatives if a certain taxon is listed by CITES (Williams et al. 2017; Kubo et al. 2022). The statistical analysis reveals that the number of countries exporting to Japan is increasing, despite the total number of imported individuals remaining at a low level (Fig. 1). Looking at exporting countries, we found several new suppliers of live Testudines, including Egypt, Vietnam, Mexico, and Nicaragua, which may have exported animals native to these countries. Moreover, a shift in target species and supplier countries is possible. A similar event was observed in the amphibian pet market (Kitade and Wakao 2022).
From Pets to Invasive Species. —
The pond slider, known as “midori game” (green turtle) in Japanese, is the most common pet turtle in Japan, with approximately 8 million individuals estimated to exist in this country. In the 1950s, this turtle became a popular pet species, with Japan importing a million individuals of the species per year in the mid-1990s (MOE 2016). Back then, children easily obtained this North America native slider by “turtle scooping” at festival stalls or in town pet stores for a few hundred JPY (a few USD). These small bright green turtles change to a dark color as they grow, thus losing their charm and often being abandoned in the wild, where they become an invasive species. Research has indicated the negative impact of pond sliders on the native ecosystem and economic activities to which the government was compelled to respond (MOE 2015; Yamaji and Yano 2020). Governmental countermeasures include laws to protect domestic wildlife and human safety by a ban on the trade and ownership of specified species as designated IAS. However, designating the pond slider as a designated IAS can worsen the situation. One survey estimated that 1.6 million pond sliders are kept in households as pets in Japan, and many of them would probably be abandoned by keepers who would not like to deal with potential legal trouble if the species falls into designated IAS status (MoE 2023a). Therefore, a new type of restriction was established in 2022 that does not restrict ownership but prohibits abandonment and commercial trade. Two species, the pond slider and red swamp crayfish (Procambarus clarkia), were designated as this new category of “designated IAS with condition” in June 2023 by the IAS Act. This recent legal measure may be the last approach to deter the abandonment of pet animals into the wild. As this example shows, trade in live animals without adequate precautions against abandonment and escape has serious and long-term consequences to ecosystems in introduced countries.
Twenty years ago, our major concern was the conservation of target species. However, we must now consider the influence of imported species on native ecosystems. A total of 140 animal taxa, including pond sliders, common snapping turtles, black soft-shelled turtles (Nilssonia nigricans), and 3 types of hybrids, are legally specified as designated IAS (MoE 2023b). Other foreign-origin species can also potentially become IAS. For example, the Mississippi map turtle (Graptemys pseudogeographica kohnii), Ouachita map turtle (Graptemys ouachitensis), false map turtle (Graptemys pseudogeographica), Apalone spp., and Pseudemys spp. are featured on the alert lists of potential invasive species provided by the National Institute for Environment Studies, Japan (NIES 2024). The IAS Act specifies preventive measures such as the restriction of import of “unevaluated alien species,” which are defined as specified species likely to cause adverse ecological impacts because of their different nature from that of native species. However, the current regulation for species introduced intentionally is not sufficiently precautionary and fails to prevent the emergence of new IAS. Once the authorities declare a species (such as Mississippi map turtle) as a designated IAS and ban its trade, new species are likely to show up in pet stores. It is impossible to say that a new species has no possibility of becoming an IAS. This longstanding regulatory rat race ought to be addressed. Thus, several countries have introduced a whitelist system, which lists the species that citizens can keep as pets (Clark 2023). This measure should prevent an increase in IAS and the outbreak of unknown zoonoses while promoting the conservation of target species. Introducing such proactive legislation into Japan as a truly precautionary principle could be reasonable.
CONCLUSION
We identified a downward trend in the import quantities of live Testudines to Japan, and preliminary analyses and observations suggested a possible correlation between this decrease and the tightening of international and domestic trade and ownership regulations. An increase in the number of CITES-listed Testudines may promote domestic breeding and the import of nonregulated species from new origin countries. The restriction of trade and ownership appears to have changed the composition of taxa sold in pet stores in Japan. To confirm the impact of legislative changes, further evaluation of each regulation and the monitoring of species in the market are necessary. Sharing and discussing the results with the government and private sector stakeholders and considering more precautionary methods of regulation such as a whitelist is crucial. As the country that once traded the most live Testudines in the world, Japan should be responsible and provide exemplary measures for sustainable pet use.
Import volume of live Testudines into Japan, 2002–2022. Source: Trade Statistics of Japan (MoF 2024).
Contributor Notes
Handling Editor: Chris R. Shepherd
