Introductions of invasive alien species have a major global impact on ecosystem integrity, with negative consequences for community structure and diversity that can persist for decades. Developing countries undergoing rapid economic growth can be especially vulnerable to such introductions, driven by new commercial opportunities. In China the profitability of selling exotic species has led to substantial numbers being bred in captivity to supply demand for pets, Chinese traditional medicine, and food. Online trade, or e-commerce, has become a major distribution channel, exacerbating the spread of invasive species and challenging biosecurity.
Although the Slider Turtle, Trachemys scripta elegans, and Snapping Turtles of the genera Chelydra and Macrochelys, all native to the Americas, are amongst the most invasive exotic species, the market for these taxa and the extent of their colonisation has not been assessed in China. Turtles are bred in freshwater aquaculture facilities in China, 65% of which are in the Yangtze river basin. This region is highly susceptible to the establishment of alien invasive Turtles (e.g. Trachemys scripta elegans, Chelydra serpentina, Macrochelys temminckii) because of the area’s suitable climate and habitats.
In a paper published in the journal Orynx on 17 January 2017, Sha Liu of the Key Laboratory of Southwest China Wildlife Resources Conservation at China West Normal University, Chris Newman, Christina Buesching, and David Macdonald of the Wildlife Conservation Research Unit at the University of Oxford, and Yu Zhang, Kai-Jie Zhang, Feng Li and Zhao-Min Zhou, also of the Key Laboratory of Southwest China Wildlife Resources Conservation at China West Normal University, evaluate how online trade (e-commerce) adds a new dimension to this problem, facilitating purchase of Turtles, driving production in breeding facilities, and risking escape and release of Turtles along all stages of the supply chain.
Liu et al. document national online sales of live Slider and Snapping Turtles via mainland China’s largest domestic consumer-to-consumer internet trading platform, Taobao.com (a subsidiary of the Alibaba Group). Liu et al. examined the spatial distribution of Turtle sales to generate a sales map, and explore how this is associated with media reports of feral Turtle populations in the Yangtze river basin, and provide recommendations for how to mitigate Turtle trade and the establishment of invasive species.
Liu et al. conducted three surveys (23 February–27 March 2017, 14 April–10 May 2017, 3-18 October 2017), searching for the terms ‘Slider Turtle, live’ and ‘Snapping Turtle, live’ (in Chinese) on Taobao.com. They included ‘live’ to distinguish Animals traded, as opposed to toys, pet supplies, and similar items. To avoid recording a vendor’s goods sold more than once, Liu et al. re-inspected vendors after an interval of at least 30 days to see if they had made subsequent sales of additional goods. When new vendors comprised less than 3% of total vendors on Liu et al.'s list in each survey, they ceased searching for additional vendors, assuming they had accounted for the majority.
Taobao.com provides retrospective transaction information, including ‘species’ (which Liu et al. 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 Liu et al. presumed to be accurate), and ‘successful transactions’, which provided the number of individual Animals sold during the 30 days preceding Liu et al.'s 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 Liu et al.'s 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 hotspots, Liu et al. used Moran’s I (a measure of spatial autocorrelation developed by Patrick Moran in 1950) to assess spatial autocorrelation at 10 distance classes (42-3482 km for the Slider Turtle and 42-2937 km for the Snapping Turtle) using Spatial Analysis in Macroecology 4.0.
To examine for any link (whether causal or coincidental) between areas where sales originated and sites where invasive Freshwater Turtles were recorded, Liu et al. 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. Liu et al. tested whether the proportion of prefectures reporting invasive non-native Turtles were significantly higher in trading hotspots, using cross tabulation with a chi-squared test (a statistical test applied to sets of categorical data to evaluate how likely it is that any observed difference between the sets arose by chance). Liu et al. 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 commerce), Liu et al. recorded 840 193 transactions involving Slider Turtles (by 469 vendors) and 108 047 involving Snapping Turtles (by 472 vendors), which extrapolates to naive estimates of annual trade volumes of about 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). From the spatial correlation coefficient at the first distance class Liu et al. found clustering for log-transformed regional sales of Slider Turtles (at distances of 42-304 km, involving 482 pairs of prefectures). 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. 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 (3806).
Liu et al. found 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. Similarly, 74 news reports mentioning Snapping Turtles involved 42 prefectures in the Yangtze region, whereas only 26 reports were from elsewhere in China. This indicates significantly more reports of invasive Turtles in the Yangtze region. 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 3 792 000 Turtles traded per year on Taobao.com, as extrapolated from Liu et al.'s 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 roughly 500 000 Turtles sold from aquaculture centers in 2002. In addition to Taobao.com, other smaller e-commerce platforms (e.g. JD.com, 1688.com) also offer Turtles for sale, and thus Liu et al.'s findings provide an indication of only a portion of the e-commerce trade of Freshwater Turtles in China.
A 2008 study led by Philip Hulme identified six introduction pathways (release, escape, contaminant, stowaway, corridor and unaided) that can facilitate the establishment of alien Vertebrate pest species such as invasive Freshwater Turtles. In addition to turtles that escape from aquaculture facilities, Buddhists release various exotic species (including Turtles) deliberately, hoping to generate good karma. Eighty-eight of 123 Buddhist temple release event organisers 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 Fish species).
Currently, there are no specific regulations or legislation 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 regulating Turtle trade is challenging, with options such as eradication, containment and control difficult and expensive to implement. A multi-pronged approach is most feasible, managing risks from trade and tightening regulations, implementing punitive fines, and policing breeding facilities. Given the massive volume of online trade in invasive species, including Animals other than Turtles, and Plants, and the consequent invasion risk, Liu et al. recommend that including an ecological hazard warning should be compulsory for all advertisements for taxa known to be invasive. This should be enforced through amendments to advertising laws and/ or through self-regulation codes of conduct implemented across the internet industry. Liu et al. acknowledge, however, that attempts to regulate turtle breeding and trading could face resistance on both social and economic grounds.
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