Priorities for the trade of less charismatic freshwater turtle and tortoise species

Despite decades of numerous calls for action by policymakers and citizen groups to regulate the biodiversity market, unsustainable trade in wildlife continues to be a leading cause of population declines world-wide (Engler & Parry-Jones 2007; Rosen & Smith 2010). While mainstream conservation attention is mostly focused on the illegal trade of ivory, horns and other products from charismatic species, demand for products from less charismatic species such as turtles has led to multiple forms of unsustainable trade (both legal and illegal). In fact, data illustrate that less charismatic taxa such as reptiles comprise a significant portion of the illegal trade (Rosen & Smith 2010) (Fig. 1). Herein, we discuss the issue of unsustainable trade of less charismatic species, specifically freshwater turtle and tortoise and outline potential solutions. Charismatic species such as large-bodied mammals and birds typically receive the most attention in terms of conservation research, funding, coverage and public consideration (Clark & May 2002; Clucas, McHugh & Caro 2008). Many less charismatic taxa, including reptiles such as freshwater turtles, are prevalent in the legal and illegal trade yet receive comparatively little conservation funding, publicity or political will for meaningful enforcement of regulations (Table 1). Freshwater turtles and tortoises are harvested for food, use in traditional Chinese medicine (TCM) and the international pet trade. In addition to factors such as habitat loss and pollution, widespread exploitation puts many of the world's turtle species at risk of extinction, with an estimated 60% of all 328 modern freshwater turtle and tortoise species listed either as Threatened or Extinct by the IUCN after adjusting for the predicted threat rate of Data Deficient species (Turtle Taxonomy Working Group 2014). The wildlife trade has self-reinforcing feedback loops, as the growing demand for species can lead to greater market prices, further incentivizing the trade. This phenomenon, known as the anthropogenic Allee effect, can ultimately drive the extinction of species (Courchamp et al. 2006). Increased demand for freshwater turtles and tortoises has led to higher pricing, making turtle collecting a source of supplemental income in many parts of the world. Some highly sought-after turtle species have been especially impacted; for example, products made from the critically endangered golden coin turtle Cuora trifasciata were marketed to have cancer curing properties which led to extreme price spikes and rampant collecting of wild individuals (van Dijk, Stuart & Rhodin 2000). Globalization, which has led to increased international exchange and interconnected markets, further drives the trade by removing geographical barriers, in some cases incentivizing former subsistence harvesters to sell into the trade. This makes turtle markets truly global, as demonstrated by the millions of turtles (including wild-caught adults, and farmed and ranched hatchlings) sent from the United States to supply Asian food markets between 2002 and 2012 (Mali et al. 2014). It is important to note that there are different drivers between the food and pet trades. Pet markets typically value turtles by species type and rarity and tend to have a larger proportion of juvenile animals which are easier to keep as pets and ship, whereas size is the most important factor in the food markets which demand large mature adults (van Dijk, Stuart & Rhodin 2000). In the light of the growing turtle trade and its detrimental impacts on many species, it is important to map out potential solutions (Fig. 2). One approach is to determine ways to meet demand that also conserve species and their habitats. Turtle farming is a potential solution that already produces large volumes for sale each year in China (Table 2); however, there are several serious issues with the practice that must be addressed. First, some consumers prefer products from wild-caught, rather than farmed, turtles. These consumers will pay a premium when possible for wild turtle products which are a fashionable luxury in many parts of Asia, particularly in China where wild turtles are believed to provide better nutrition and health benefits than captive-raised animals (Zhou & Jiang 2008). Another issue is that not all species are easily farmed given the long life cycle of many turtles. For this reason, turtle farms are often not sustainable given low survival rates and farmers’ reluctance to wait at least 5–10 years for many species to reach maturity and another 10–20 years for captive females to attain maximum clutch size and frequency. This long (and for farmers, costly) maturation period is why large, wild-caught turtles are so highly prized by food traders and farmers. It is also why farmers often collect additional individuals from the wild, making large-scale turtle farms one of the largest buyers of mature wild-caught turtles to begin and restock their programmes (van Dijk, Stuart & Rhodin 2000). Further, when turtle farming is not closely regulated it can provide a front for wildlife laundering given the difficulty in distinguishing between wild-caught and farm-raised individuals. For turtle farming to be sustainable, it would have to be managed on a smaller scale that provides higher quality care for the turtles. These smaller farms would require initial stock of turtles with relatively shorter maturation periods (e.g. Chinese softshell Pelodiscus sinensis) and a long-term commitment to rearing these species. A regulatory system that controls the wild collection and interfarm trade would need to be developed, taking into account species’ current population size and reproductive rate. Ideally, monitoring with genetic testing would be used to ensure the origin of individual turtles and prevent laundering of wild-caught specimen (Ogden, Dawnay & McEwing 2009). Close cooperation among traders, breeders and conservationists is imperative to ensure the sustainability of farming operations and to reduce pressure on wild populations. In theory, sustainable harvesting is another possible alternative to avoid extinction of wild turtle populations; however, this has never been demonstrated as a viable methodology with mature individuals as even small annual increases in adult mortality can result in population extirpations (Congdon, Dunham & van Loben Sels 1993). For sustainable harvesting to succeed, it should be compatible with turtle life-history traits while providing socio-economic benefits to local people. One such approach is turtle ranching, in which wild eggs are harvested or hatchlings are caught and reared in a controlled environment (Mali et al. 2014). This method is feasible because collection of eggs and/or hatchlings has a lower impact on wild populations than the harvesting of mature adults given the low recruitment of turtles (Caputo, Canestrelli & Boitani 2005). For example, community-based management of yellow-spotted river turtle Podocnemis unifilis eggs by the Cofan people in the Amazon appears to be sustainable given that consumption needs are less than the number of nests potentially lost to flooding (Caputo, Canestrelli & Boitani 2005). This community-based programme includes harvesting from nests threatened by flooding and also includes initiatives to transplant nests to higher ground, monitor key beaches from nesting to hatching season, and pay a reward for each successful hatchling (Caputo, Canestrelli & Boitani 2005). This model could potentially be tailored to other regions that still support healthy turtle populations; however, any form of egg collection or turtle ranching should be closely regulated, with the best available science used to determine optimal harvest volumes and collection age. Further, historical instances of nest management failure, including the collapse of river turtle populations from overharvest as discussed by Moll & Moll (2004), should provide a cautionary tale as to the delicate balance required for such approaches to be successful. Inconsistencies across local, regional and national regulations provide opportunity for turtle trafficking and therefore must be eliminated. For example, China's National Key Protected Wild Animal Species list has not been updated since it was created in 1989 which can lead to inconsistencies with current taxonomic and global conservation statuses (Zhou 2015). Of the 26 IUCN Threatened chelonian species native to China, only 12 are listed as Class I or II on China's protected species list. In the United States, regulation around management of freshwater turtles varies drastically on a state-by-state basis. For example, Florida has banned all commercial harvest of freshwater turtles, while Louisiana has limited regulations and Arkansas has essentially no restrictions on the harvest of most turtle species (Arkansas Game and Fish Commission 2015; Louisiana Department of Wildlife and Fisheries 2015; Florida Fish and Wildlife Conservation Commission 2015). As an intercountry example, strict laws in India around the ownership and trade of Indian Star Tortoises Geochelone elegans are greatly undermined by the legal trade of the species in other Asian countries. Ending such discrepancies and managing turtle species based on a larger landscape approach is necessary to safeguard species and avoid over-exploitation and extirpation. By focusing on CITES, a common world-wide conservation listing status with regulatory restrictions, we can best protect threatened species traded on a global scale. Many turtle species are in urgent need of being uplisted to CITES Appendix I, which would not only provide greater protection for these species, but also bring international attention to the plight of turtles. While we believe CITES listing upgrades would be an overall positive, it is worth noting that one potential unintended consequence is increased trade value. For example, Courchamp et al. (2006) found that CITES listed turtle species being sold as pets were significantly more expensive than non-listed species, likely as a result of their perceived rarity. Integrating turtle species data into global customs systems is another important step which would help provide the necessary data for management (Chan et al. 2015). Current systems lack the taxonomic detail that is necessary to account for species-level impacts of the turtle trade and do not provide enough information on a significant number of turtle products and their value chains. For example, Chan et al. (2015) reported that there currently are no specific codes for many major taxonomic groups, including turtles, leading to poor global wildlife trade monitoring. This compares to the relatively robust classification system for fisheries and presents a clear opportunity for improvements to the animal coding system (Chan et al. 2015). Detailed information on species type, origin, size and maturity from CITES signatories would provide a better understanding of the global trade impacts. Universal definitions are also needed around determining a turtle's origin; for example, there is no specific time in which wild-caught turtles must be raised in a controlled environment before being considered ‘ranched’ instead of wild-caught (Mali et al. 2014). Understanding trade data from a wildlife market perspective could provide information to help better regulate the trade (Harris et al. 2015). Monitoring traffic and markets over an extended duration helps local authorities to observe real-time changes in supply and demand of turtles. Consistent records of species availability and quantity are useful for determining longer-term patterns and trends. A depository for market surveys, where researchers, NGOs and governments share species and volume data from wildlife markets, seizures or other sources and make the data widely available, would also be a useful tool. This information could be shared through an aggregate wildlife trade data base where species, source countries and end market countries are listed. Developing warning systems for the trade of highly trafficked species such as turtles is another potential tactic. Others have launched a website that aggregates official and unofficial reports of the illegal wildlife trade (Hansen et al. 2012), and TRAFFIC lists developing an early warning system in China as a priority, but we are not aware of an instance where this has been fully operationalized. Ideally, a system that connects enforcement agents with real-time trade information (from a wildlife trading data base) would allow for more proactive policing. This sort of system could alert the appropriate authorities to spikes in market volumes, creating the opportunity for adaptive management around wildlife laws and harvests. Closing the information loop through coordination that sends timely feedback to appropriate source country governing bodies would allow nations to take a more offensive approach in managing trade of turtle and other species. All of these suggested solutions are of little use to turtle conservation without sufficient penalties and the political will to properly enforce regulations and prosecute offenders. Many countries have inadequate legislation to properly police the illegal wildlife trade with legislative weaknesses, lax penalties and lack of prosecutorial capacity (DLA Piper 2014). Perhaps the less charismatic nature of turtles leads to even greater disregard for laws meant to protect them and a lack of punishment for violators. For example, in China, market surveys observed the open sale of numerous CITES Appendix I and Appendix II as well as China nationally protected freshwater turtle and tortoise species which contrasts with the markets for high-profile species such as tiger which seem to have moved underground (Cheung & Dudgeon 2006; Barber-Meyer 2010). One way to help improve policing efforts is to develop capacity with the appropriate law enforcement agents by educating agents about the turtle trade as well as by providing training and materials necessary for species identification of protected species. For instance, smartphone applications with a decision tree style format that aid agents in taxonomic identification, such as the ‘Wildlife Guardian’ application developed by the Wildlife Conservation Society, appear promising as an economical way to improve enforcement of wildlife crimes (Kretser et al. 2015). It is equally important that with increased enforcement comes increased prosecution rates; studies have shown that there is often a high level of discretion regarding wildlife crime penalties that can result in light sentencing (DLA Piper 2014). Brought together, the factors of weak legislation, poor enforcement and limited prosecution can make wildlife crimes such as turtle smuggling a relatively low-risk venture versus other types of illicit trade. In many countries, corruption is a significant factor limiting successful policing and prosecution with bribery of forest guards, customs and government officials facilitating the trade (DLA Piper 2014). For this reason, tougher anticorruption legislation and convictions are also crucial to reducing the illegal wildlife trade (DLA Piper 2014). Future work should also address the key driver of the turtle trade: end market demand. Surveys and focus group studies could provide a better understanding of attitudes towards turtle consumption and responsible pet ownership. Educational programmes in highly impacted rural areas such as in Madagascar and Southeast Asia, for instance, could help teach the need for conservation to ensure that turtle populations persist into the future. Public awareness campaigns should also target urban food consumers and international pet trade players in an effort to raise awareness regarding the plight of turtles from over-collection for these end markets. Capacity building is also needed in the form of additional rescue and rehabilitation centres with turtle and tortoise expertise, which are currently very few in number (e.g. 1–2 in Myanmar, Vietnam and Madagascar; B. Horne, personal observation), possibly limiting the likelihood of confiscation. Going forward, it is imperative that a multipronged approach is used to combat the growing and evolving (e.g. wild turtles imported to China are increasingly being sourced from South America and Africa as supply from Southeast Asia decreases) global trade of turtles. Alternative ways to meet end market demand should be studied for their viability as a long-term solution. We believe a first priority should be to devise a fully regulated market for turtle species that have been successfully captive-bred in quantities large enough to meet demand (e.g. Chinese softshell) in an effort to reduce unsustainable pressure on wild populations from food markets. Another key priority should be improving the global enforcement of regulations based on CITES and uplisting additional species to Appendix I. Lastly, national level efforts should focus on improving the consistency and relevancy of internal protected species listing systems. Crucial to all of these priorities is the building of political will and capacity to improve enforcement and prosecution rates of those dealing in the illicit trade of species such as turtles. This article presents key solutions which, with successful implementation, can better regulate the trade of freshwater turtles and other less charismatic species and help stem the dramatic loss of turtle species world-wide. This work benefited from our interactions with colleagues from the Center of International Forestry Research (CIFOR) and Wildlife Conservation Society (WCS). We would also like to thank the reviewers for their detailed comments and suggestions on an earlier draft. We are grateful to USAID and DFID (UK) for providing funding. This study was carried out as part of the CGIAR Research Program on Forests, Trees and Agroforestry (FTA) that is led by CIFOR. Data have not been archived because this article does not contain data. Amanda Sigouin and Tien Ming Lee research the global wildlife trade, working to better understand the flow of species and related goods within wildlife markets and how this information can provide detail on trade routes and inform smarter monitoring and enforcement efforts. Colin Poole and Brian Horne work on global conservation issues such as how to combat the illegal wildlife trade on the ground in hot spots such as Asia, with a focus on turtle trafficking. Robert Nasi and Miguel Pinedo-Vasquez research issues such as the sustainable use of forest products and how to implement better designed forest management policies.