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Trade in invasive turtles 353 Taobao.com provides retrospective transaction infor-


mation, including ‘species’ (which we verified from the description and photographs provided by sellers), ‘item location’ (i.e. site of origin of the sale, used to calculate freight charges, and which we presumed to be accurate), and ‘successful transactions’, which provided the number of individual animals sold during the 30 days preceding our inspection of Taobao trading records (one transaction equates to one animal traded). The destination of sales was not, however, included and thus did not form part of our analyses. Data were collected and analysed using prefecture as the administrative unit (mainland China comprises 334 prefectures, in 34 provinces, and four province-level municipalities). To determine whether the number of sales (log-transformed) were similar between neighbouring prefectures, which would suggest trading hot- spots,we usedMoran’s I (Moran, 1950) to assess spatial auto- correlation at 10 distance classes (42–3,482 km for the slider turtle and 42–2,937 km for the snapping turtle) using Spatial Analysis in Macroecology 4.0 (Rangel et al., 2010). To examine for any link (whether causal or coincidental)


between areas where sales originated and sites where in- vasive freshwater turtles were recorded, we searched Baidu News (on 8 August 2018) for reports containing the search term ‘exotic, turtle’ (in Chinese) in the full text of articles for 2008–2018. We tested whether the proportion of prefec- tures reporting invasive non-native turtles were significantly (P,0.05) higher in trading hotspots, using cross tabulation with a χ2 test. We applied Yates’s correction for continuity because of the small number of news reports available. From the three surveys, each covering 1 month (30


days) of trade (i.e. monitoring 25% of total annual com- merce), we recorded 840,193 transactions involving slider turtles (by 469 vendors) and 108,047 involving snapp- ing turtles (by 472 vendors), which extrapolates to naive estimates of annual trade volumes of c. 3,360,000 and 432,000, respectively. Geographical patterns of sales were similar between taxa, although sales originated in only 106 of 338 prefectures and province-level municipalities (slider turtles in 89, snapping turtles in 70; Fig. 1). From the spatial correlation coefficient at the first distance class (P,0.05) we found clustering for log-transformed regional sales of slider turtles (at distances of 42–339 km, involving 782 pairs of prefectures, Moran’s I = 0.12) and snapping turtles (at distances of 42–304 km, involving 482 pairs of prefec- tures, Moran’s I = 0.14). This revealed a sales hotspot, with 82.4% of slider turtles and 68.3% of snapping turtles sold from 26 and 17 prefectures, respectively. These prefectures lie in the middle and lower reaches of the Yangtze river basin, the predominant aquaculture region in China, from where turtles are bred and disseminated through wholesalers, retailers and consumer-to-consumer traders (Fig. 1). The majority of the sales of slider turtles originated from Shanghai (198,289 individuals), Suzhou (174,698) and


Changsha (165,952), and of snapping turtles from Suzhou (53,572), Shanghai (12,620) and Changsha (3,806). Wefound 30 news reports that mentioned invasive slider


turtle populations, across 23 prefectures, 16 of which were amongst the 66 prefectures comprising the middle and lower Yangtze river basin; 14 news reports were amongst mainland China’s other 272 prefectures (Fig. 1). Similarly, 74 news reports mentioning snapping turtles involved 42 prefectures in the Yangtze region, whereas only 26 reports were from elsewhere in China (Fig. 1). This indicates signifi- cantly more reports of invasive turtles in the Yangtze region (χ2 with Yates’s correction, P,0.05,df = 1, for both taxa). Reports mentioned ‘ceremonial animal release’ events (12 for slider and four for snapping turtles) and reported predation on native species such as fish, tadpoles, small turtles and eggs of waterfowl (nine for slider and three for snapping turtles). The estimated c. 3,792,000 turtles traded per year on Taobao.com, as extrapolated from our surveys, suggests that e-commerce is contributing to the purchase and release of potentially invasive turtle species in China. This number is greater than the c. 500,000 turtles sold from aquaculture centers in 2002 (Shi et al., 2008). In addition to Taobao.com, other smaller e-commerce platforms (e.g. JD.com, 1688.com) also offer turtles for sale, and thus our findings provide an indication of only a portion of the e-commerce trade of freshwater turtles in China. Hulme et al. (2008) identified six introduction pathways


(release, escape, contaminant, stowaway, corridor and un- aided) that can facilitate the establishment of alien vertebrate pest species (Kraus, 2015) such as invasive freshwater turtles. In addition to turtles that escape from aquaculture facilities (Casimiro et al., 2018), Buddhists release various exotic species (including turtles) deliberately, hoping to generate good karma (Liu et al., 2012). Eighty-eight of 123 Bud- dhist temple release event organizers surveyed in China released large numbers of turtles and other invasive species (e.g. American bullfrog Lithobates catesbeianus, Asian swamp eels Monopterus albus, Oriental weatherfish Misgurnus anguillicaudatus, several Cyprinid species; Liu et al., 2013). Currently, there are no specific regulations or legisla-


tion pertaining to importation, domestic trade and captive breeding of non-native turtles in China. Snapping turtles are promoted as food, as a source of medicines and as pets, under China’s Ministry of Agriculture announcement No. 485, 2005. Preventing further introductions and regulat- ing turtle trade is challenging, with options such as eradi- cation, containment and control difficult and expensive to implement (Hulme, 2009). A multi-pronged approach is most feasible, managing risks from trade and tightening reg- ulations, implementing punitive fines, and policing breed- ing facilities (Shi et al., 2008) and importation (Perrings et al., 2005). Given the massive volume of online trade in


Oryx, 2021, 55(3), 352–355 © The Author(s), 2020. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605319001030


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