Enforcement seizures reveal large-scale illegal trade in India's tortoises and freshwater turtles by Freeland

Biological Conservation 207 (2017) 100–105

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Short communication

Enforcement seizures reveal large-scale illegal trade in India's tortoises and freshwater turtles Uttara Mendiratta a,⁎, Vallari Sheel a, Shailendra Singh b a b

Freeland India, B 9, Sarita Vihar, New Delhi 110076, India Turtle Survival Alliance-India, D1/317, Sector F, Jankipuram, Lucknow 226021, India

a r t i c l e

i n f o

Article history: Received 2 September 2016 Received in revised form 12 January 2017 Accepted 28 January 2017 Available online 9 February 2017 Keywords: Tortoise Freshwater turtle Internet search Illegal trade Seizures India

a b s t r a c t Illegal trade in tortoises and freshwater turtles (TFTs) for pet, meat and traditional medicine markets in East and Southeast Asia poses signiﬁcant threats to wild TFTs globally. South Asian countries such as India are believed to be disproportionately large sources of wild TFTs in illegal international markets, but the nature and dynamics of this trade in India are poorly understood. Using data from 223 enforcement seizure reports obtained through systematic online searches, we show that at least 15 of India's 28 TFT species, including 10 IUCN Threatened species, are illegally harvested, with over 58,000 live individuals seized during 2011–15. Geochelone elegans, Geoclemys hamiltonii and Lissemys punctata were recorded in the largest number of seizures and comprised the largest numbers of TFTs seized overall. Nearly 90% of all seizures were from illegal commercial trade, and there were numerous reports of Indian TFTs being transported by road, rail and air within India, as well as to known pet and meat trading hubs in Bangladesh, Thailand, and four other East/Southeast Asian countries. Commercial trade of live TFTs now targets twice as many Indian species as reported in the 1990s. Alongside illegal harvests for local consumption and TFT body parts for traditional East Asian medicines, this illegal trade poses a growing threat to Indian TFTs. Our ﬁndings indicate that building awareness and capacity for handling TFT seizures among enforcement agencies, and strengthening international cooperation for law enforcement, are important steps needed for conserving India's endangered tortoises and freshwater turtles. © 2017 Elsevier Ltd. All rights reserved.

1. Introduction Illegal wildlife harvest and trade is one of the largest illegitimate businesses globally, with an estimated annual market value of around US$ 20 billion, and is a growing global biodiversity threat (Haken, 2011; Maxwell et al., 2016; Rosen and Smith, 2010; UNODC, 2016). In East and Southeast Asia, there exists a large and growing market for tortoises and freshwater turtles (TFTs) for pets, meat and use in traditional medicines (Chen et al., 2009; Cheung and Dudgeon, 2006; Gong et al., 2009; Haitao et al., 2008; Harrison et al., 2016; Nijman, 2010; Nijman and Shepherd, 2014; van Dijk, 2000). This international trade is an important driver of the ongoing Asian turtle crisis, with over half of all Asian TFT species currently threatened with extinction (van Dijk et al., 2012). While East and Southeast Asia are the largest markets for illegally traded TFTs globally (Cheung and Dudgeon, 2006; Gong et al., 2009; Nijman and Shepherd, 2014), around 25% of the seizures of illegally traded TFTs originate from South Asia (UNODC, 2016). Globally, India ranks sixth, in terms of TFT richness, and is recognized as a TFT ‘mega ⁎ Corresponding author at: 12/1, 5th Main Road, Malleswaram, Bangalore 560003, India E-mail address: uttara.mendiratta@gmail.com (U. Mendiratta).

diverse country’, with the Gangetic plain in particular considered a TFT diversity hotspot (Buhlmann et al., 2009; Mittermeier et al., 2015). Over 78% (22 species) of Indian TFT species are considered threatened with extinction i.e. either Vulnerable, Endangered or Critically Endangered in the International Union for Conservation of Nature and Natural Resources (IUCN) Red List of Threatened Species (Supplementary Table 1). Although Indian laws prohibit harvest and trade of native TFT species, illegal commercial trade in Indian TFTs has long been recognized (Choudhury and Bhupathy, 1993; Moll, 1990). However, an in-depth understanding of this illegal trade is limited to the Star Tortoise (Geochelone elegans) and, to a lesser extent, the Spotted Pond Turtle (Geoclemys hamiltonii), both of which are traded in international markets (Chng, 2014; D'Cruze et al., 2015). Apart from these two species, there is a paucity of information on what species are traded, in what volumes, and on TFT trading hotspots and mechanisms. Given that international TFT markets are known to be highly dynamic, with demands regularly shifting to new species (Nijman and Shepherd, 2014), understanding the current illegal trade in India is essential for conserving India's endangered tortoises and freshwater turtles. As in the case of most illegal wildlife trade, documenting and understanding illegal TFT trade can pose a considerable challenge, owing to its highly clandestine nature. Recent studies have taken advantage of the

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increasing availability of and ease of access to media reports on enforcement seizures to obtain new insights into the workings of illegal wildlife trade networks (Patel et al., 2015). Although such datasets are prone to biases arising from variation in enforcement effort and effectiveness, they are currently perhaps the best source of information for documenting and understanding illegal wildlife trade (Hansen et al., 2012). Here, we use media reports of seizures of Indian TFT species, obtained through systematic online searches, to study the characteristics of the illegal trade in India during 2011–15. Specifically, we (1) assess what TFT species are present in seizures, how frequently they are encountered and in what volumes, (2) examine shifts in TFT species targeted for trade from 1990s to present, based on comparisons with previous reports, and (3) identify TFT trading hotspots, in terms of preferred trading hubs and routes, both within India and internationally. 2. Materials and methods 2.1. TFT seizure data We collated information on TFT seizures by systematically searching global online media reports on seizures made between 1st January 2011 to 31st December 2015. We employed a combination of active searches and automated alerts to locate reports of TFT seizures in online newsletters, newspapers, news channels, blogs and YouTube channels. For our searches, we used phrases commonly linked to TFT seizures, such as “turtle seizure”, “tortoise seizure” and “wildlife trade”. Reports in English, and six Indian languages which were translated to English, were retained for further analysis. We reviewed reports to (1) retain those on seizures of live tortoises and freshwater turtles in India and international seizures of Indian species originating from India and (2) follow up on leads from the reports to locate information on other relevant seizures of live Indian TFTs. For each report, we extracted information on the seizure location, numbers and species identities of the seized animals, whenever possible. Internet search results containing information on TFT species from other South Asian countries and information on seized TFT parts were also noted separately (Supplementary Table 2), and not included in any of the analyses. As our searches were not geared to detect reports in other languages, seizures of Indian TFTs outside India that were not reported in English are likely to have been missed, thus underrepresenting international trade in Indian TFTs. Because media reports do not always provide reliable information on seizure composition, species identities were only recorded from reports that attributed identification to subject experts, trained enforcement agencies (e.g. forest department, wildlife wings of customs and police) and wildlife NGOs having relevant expertise in the respective regions (25% of seizures). In cases where reports were accompanied by seizure photographs or videos, or such visuals were independently obtained from participating experts/officials, these were reviewed by the authors in consultation with other TFT experts to identify as many of the species involved as possible (35% of seizures). For the remaining 40% of seizures, there neither was adequate information within the reports, nor were we able to independently obtain visuals or expert inputs to ascertain species identities. News media photographs that were used for species identification were first run through reverse image search applications such as Google Images and TinEye to ensure that they were actually from the reported seizure, and were not file images. In cases where species identities could not be confirmed, seized animals were either classified to genus (e.g. Pangshura spp.) or family level (e.g. unidentified soft-shell/Trionychidae), or left unidentified. Seizure sizes were obtained from media reports, and where multiple articles on the same seizure reported different numbers, the more conservative estimates were recorded. We recorded the geographic coordinates of each seizure as well as more specific information on seizure locations, such as whether the animals were seized at the point of harvest, in transit (e.g. rail/road/air), or in pet shops or warehouses. Animals seized in transit or in pet shops and warehouses were classified

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as being in commercial trade, while seizures that appeared to be for subsistence use, or for which end use was not clear (e.g. seizures made at source or in private residences), were marked as non-commercial and unknown, respectively. Given that some fraction of harvests that appear to be for subsistence use may also be commercially sold, as has been observed elsewhere in the tropics (Nasi et al., 2008), our assessment of commercial trade is likely to be a conservative one. For seizures in transit, consignment origins, destinations and transit routes were also recorded, whenever such information was clearly traceable (e.g. flight records in airport/air transit seizures). 2.2. Analysis We assessed species' prevalence in seizures from 2011–15 by calculating the proportion of total seizures in which each species was reported (frequency) and total numbers of individuals of each species seized (volume). To evaluate shifts over time in species recorded in commercial trade, we compared the species list from our 2011–15 dataset with the list of species reported in commercial trade in India during the early 1990s (Choudhury and Bhupathy, 1993). Based on these comparisons, we identified species that were previously unreported in commercial trade in India, and those that were previously traded, but not reported currently. Finally, we used information on geographic locations and transit status of seizures to generate maps of trading hotspots and routes. Data were analyzed and plotted using R-3.0.2 (R Core Team, 2013). Maps were made using R-3.0.2 (R Core Team, 2013) and ArcGIS-9.3 (ESRI, 2006). 3. Results We obtained media reports of 223 seizures containing live Indian TFTs during the period from 1st January 2011 to 31st December 2015. Over 91% of these seizures were made in India, while the remaining 9% were of TFTs that originated from India and were seized in Bangladesh, Thailand and China. At least 58,442 TFTs belonging to at least 15 species (54% of India's TFT species) were reported in seizures during the study period (Table 1). Quality and completeness of information varied across seizures: overall seizure sizes were known for 98% of the seizures and all seized TFTs were identified to at least the family level in 56% of the seizures. On the other hand, nearly 50% of the seizures contained some unidentified species and/or incomplete species-wise counts. The number of confirmed species per seizure ranged from 1 to 5 (47% contained a single identified species) and numbers of individuals per seizure ranged from 1 to 4980 (median = 81 individuals). Hard-shell turtles (nine species) and tortoises (three species), which were present in at least 50% of the seizures, contributed at least 13,135 individuals. Soft-shell turtles (three species) were present in at least 22% seizures and contributed at least 5831 individuals seized. G. elegans (8533 individuals), G. hamiltonii (4011 individuals) and Lissemys punctata (5186 individuals) were the most commonly encountered species, occurring in at least 23%, 20%, 12% of the seizures respectively (Fig. 1). Ten Threatened species (seven Vulnerable and three Endangered) were recorded in the seizures, including the Endangered Chitra indica (six seizures, at least 68 individuals) and Indotestudo elongata (one seizure, two individuals) (Table 1). The seizures also recorded two Indian endemic species, namely Vijayachelys silvatica (one seizure, seven individuals) and Indotestudo travancorica (one seizure, one individual). Nearly 90% of seizures, and 99% of all seized TFTs, were classified as being in commercial trade (i.e. in transit and in pet shops, or stored in warehouses), while the remaining seizures were classified as non-commercial or unknown. Out of the 15 species detected across seizures in this study, 14 were also recorded in commercial trade seizures (Table 1). In comparison, surveys in the 1990s only recorded seven

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Table 1 Information on species names, IUCN threat status, CITES appendix and, historic (1990s) and current trade status of Indian TFTs recoded in this study. Species recorded in transit along air and road on international routes in this study are marked using * and #, respectively. Records for commercial trade: Sources: 1 – Current study; 2 – (Choudhury and Bhupathy, 1993); 3 – (Chng, 2014).

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15

Scientiﬁc name

Common name

Current IUCN status

CITES appendix

Post-1990 records of commercial trade

Chitra indica* Geochelone elegans*# Geoclemys hamiltonii*# Hardella thurjii Indotestudo elongata Indotestudo travancorica* Lissemys punctata# Melanochelys tricarinata* Melanochelys trijuga Morenia petersi* Nilssonia gangetica Pangshura smithii Pangshura tecta Pangshura tentoria Vijayachelys silvatica

Indian Narrow-headed Softshell Turtle Indian Star Tortoise Spotted Pond Turtle Crowned River Turtle Elongated Tortoise Travancore turtle Indian Flapshell Turtle Tricarinate Hill Turtle Indian Black Turtle Indian Eyed Turtle Gangetic Softshell Turtle Brown Roofed Turtle Indian Roofed Turtle Indian Tent Turtle Cochin Forest Cane Turtle

Endangered Vulnerable Vulnerable Vulnerable Endangered Vulnerable Least concern Vulnerable Near threatened Vulnerable Vulnerable Lower risk/near threatened Lower risk/least concern Lower risk/least concern Endangered

II II I Not listed II II II I Not listed Not listed I II II II II

1 1, 2 1, 3 1, 2 1 1 1, 2 1 1, 2 1 1, 2 1 1 1 None

TFT species in commercial trade (Choudhury and Bhupathy, 1993). While five species were recorded in commercial trade in both historic and present day seizures, nine species were recorded in commercial trade in our study but not in the 1990s (Table 1). In contrast, two species that were reported as commercially traded by Choudhury and Bhupathy (1993), namely Nilssonia leithii and N. hurum, were not recorded in trade from India in the current study. Over 70% of all commercial seizures were of TFT consignments in transit (28% air, 32% rail and 41% road), including 15 road-transit seizures containing at least five species moving from India to Bangladesh and 38 seizures containing at least seven species at international airports (six species listed in Table 1, plus unidentified Pangshura spp.). The airport seizures comprised 31 outbound consignments from Indian airports (Chennai: 15, Mumbai: 6, Bangalore: 3, Cochin: 3, Tiruchirappalli: 3, and Madurai: 1) as well as six consignments in Thailand and one in China, from flights that had originated in India (Supplementary Table 2). Consignments seized along international air routes were destined for Malaysia (15), Thailand (13), China (1), Indonesia (1), and Japan (1). The Gangetic Plain, which is well-recognized as a global hotspot for TFT diversity and conservation (Buhlmann et al., 2009; Mittermeier et al., 2015), and adjoining areas, accounted for 46% of all reported seizures, with 15 seizures reported from in and around the cities of Lucknow and Kanpur in the Upper Gangetic Plains (Fig. 2). Twenty-two seizures were also reported from the Lower Gangetic Plains along the India-Bangladesh border, including the largest seizures of 4980 individuals.

4. Discussion Our study shows that half of India's 28 TFT species, including several Threatened and endemic species are harvested and traded illegally. The Gangetic Plain, which is a region of global conservation importance for TFTs, constitutes the major center for this large-scale trade. A number of traded species are currently rare (e.g. Melanochelys tricarinata (Das, 2009)), have restricted ranges (e.g. I. travancorica (Kanagavel and Raghavan, 2012)) and have shown recent population declines (e.g. G. hamiltonii and Hardella thurjii (Bhupathy et al., 2000; Das and Bhupathy, 2009)), further underscoring the conservation threats posed by this large-scale and widespread illegal trade. Our results highlight the threats posed to Indian TFTs by illegal international smuggling and trade to commercial markets in China and Southeast Asia. We recorded at least seven Indian TFT species (including ﬁve species listed under Appendixes I and II of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES)) in seizures on eastbound international air routes from India during 2011–15 (Fig. 3). Seizures along these routes typically comprised tortoise and hard-shell turtle species such as G. elegans and G. hamiltonii, which are popular as pets in China and Southeast Asia (Chng, 2014; D'Cruze et al., 2015; Gong et al., 2009; Nijman and Shepherd, 2014), but also included soft-shell turtles like the Endangered C. indica. In the case of other soft-shells such as L. punctata, which are already well known for local consumption-driven harvest in India (Bhupathy et al.,

Fig. 1. Frequency (percentage of total seizures) of different Indian TFT species recorded in seizures during 2011–15.

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Fig. 2. Geographic distribution, numbers and sizes of reported TFT seizures from India during 2011–15, aggregated to the district level. Areas colored blue represent the Gangetic Plain. Seizures originating from India made at locations outside India are not marked here.

2014), the large proportion (59%) and sizes (up to 4000 individuals) of ‘in-transit’ seizures, especially along the India-Bangladesh border, shed light on the organized international trade in these species that also exists. These results also suggest that, in spite of growing supply from TFT farms to Chinese and Southeast Asian markets (Gong et al., 2009; Haitao et al., 2008, 2007), illegal harvests of wild TFTs in India – where wildlife farming is not legally permitted – remain substantial. We recorded nearly twice as many species in recent seizures of commercially traded TFTs compared to reports from the early 1990s (Choudhury and Bhupathy, 1993). However, the turnover in present day seizures includes both the addition of new species and absence of previously reported species. The appearance of new species in present day seizures could be because they were missed by previous assessments, considering the limited number of comprehensive surveys from earlier periods. However, it is also very likely that trade in these species from India has actually risen, given the increasing diversity of TFT species being reported from SE Asian markets, including the appearance of G. hamiltonii from India in recent times (Cheung and Dudgeon, 2006; Chng, 2014; Nijman and Shepherd, 2014). New species appearing in trade could also be as replacements for previously traded species, whose populations have declined to a point where harvests are no longer commercially viable. In the case of N. leithii, which is one of the species that was formerly traded but absent from present day seizures, this species is known to have been extirpated from many parts of its range, and its IUCN threat status has accordingly been elevated from Least Concern (1996) to Critically Endangered (van Dijk et al., 2012). India has witnessed similar trade-driven TFT species declines and extirpations in previous times, notably of the genus Batagur during the 1960s–1980s, when most TFTs were not legally protected from harvest and commercial trade (Choudhury and Bhupathy, 1993; Moll, 1990).

While our results reveal the large scale and international nature of TFT trade in India, our ﬁndings, especially in terms of the numbers of species and individuals affected, must be viewed as highly conservative. Reasons for this include low rates of illegal trade detection by enforcement agencies (Wasser et al., 2007), incomplete reporting in news and media outlets and imperfect detection by our searches, particularly for non-English articles. Enforcement presence and effectiveness are also likely to vary considerably across the study area, which could create the artifact of species from regions with good enforcement being overrepresented in our data. Moreover, in addition to trade in live TFTs, which formed the focus of this study, TFTs are also harvested for trade in body parts – such as plastrons and carapace – to supply the massive and growing traditional medicine market in China and Southeast Asia (Chen et al., 2009; Compton, 2000). Though we recorded seven seizures of TFT parts (four from India, two from Bangladesh and one from Pakistan; Supplementary Table 2) during our study, it is clear that this trade is considerably more difﬁcult to detect than the trade in live animals, and enforcement agencies perhaps lack the required expertise to do so effectively. Future investigations that focus on this highly cryptic trade in TFT parts will be important for understanding, monitoring and combating illegal TFT trade more effectively in India. 5. Conclusion Our study shows that the majority of Indian tortoises and freshwater turtles, including several Threatened species, are targeted for illegal domestic trade and international trade to East and Southeast Asian markets. Together with harvest for local consumption (Bhupathy et al., 2014; Kanagavel and Raghavan, 2013; Krishnakumar et al., 2009), and trade in body parts such as plastrons and carapace (Das and Singh, 2009; Sundar, 2004), this commercial trade in live animals represents

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Fig. 3. International air routes originating from India on which seizures of illegally traded TFTs were recorded during 2011–15. International air seizure reports from Pakistan, Bangladesh and Sri Lanka, which were detected during our searches, are also displayed on the map. The number of seizures per route ranged from one to seven.

a significant and possibly growing threat to TFT species in India. While enforcement agencies must be commended for executing over 220 TFT seizures during 2011–15, focused capacity building will be important for strengthening their ability to combat this illegal trade. The large proportion of seizures with unidentified species illustrates the need for better training in species identification, which in turn will help expedite law enforcement and prosecution. Also, existing infrastructure for housing seized TFT is inadequate (Shailendra Singh, pers. obs.), and needs to be improved in order to achieve better success at rehabilitating seized animals. Given the large scale and international nature of this trade, there is also clear need for improving coordination among different enforcement agencies, as well as coordination across international borders. Alongside strengthening law enforcement, a better understanding of Indian TFT species' ecology, distributions and population status is urgently needed for sustaining their conservation in this region of high TFT diversity and endemism. Acknowledgments We acknowledge Freeland India (UM, VS) and Turtle Survival Alliance-India (SS) for financial and institutional support. This project was partly funded by World Animal Protection. We thank Shashwat Sirsi, Tarun Nair, S.M.A. Rashid and the staff of Wildlife SOS and Wildlife Crime Control Bureau for helping with species identifications. We also

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