Serpent's source: Determining the source and geographic origin of traded python skins using isotopic and elemental markers
Introduction
The international trade in wildlife is receiving increasing attention as overexploitation drives declines in the wild populations of many species (Broad et al., 2003, Biggs et al., 2016, UNODC, 2016). To combat this, captive breeding has been promoted to relieve harvesting pressure on wild animal populations (Lyons and Natusch, 2011, Nogueira and Nogueira-Filho, 2011, Challender and MacMillan, 2014) and, in several cases, this approach has been successful. For example, captive breeding and ranching of crocodilians for international trade has offered a meaningful substitute for wild-caught specimens (Hutton and Webb, 2003, Macgregor, 2006). In other cases, however, captive breeding facilities have been implicated in the laundering and export of wild-caught specimens under the guise of being captive-bred (Brooks et al., 2010, Lyons and Natusch, 2011). Such illicit activity undermines the rule of law and makes it challenging to accurately determine the true number of wild specimens entering trade and, thus, makes it difficult to undertake effective sustainability assessments.
The international trade in wildlife is regulated by the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). The Parties to CITES have recognised the laundering of wild specimens through captive-breeding facilities and have dedicated significant time and resources to tackling this problem (e.g., see TRAFFIC, 2013, Lyons et al., 2016, Lyons and Natusch, 2015). To facilitate such efforts, there is a need for the increased involvement of forensic science to combat wildlife crime (UNODC, 2016). A novel approach to establish the provenance of specimens entering trade involves the forensic application of stable isotope and elemental markers naturally present in the tissue of wild and captive-bred specimens.
The diets and environments of animals living at different sites or being raised within different production systems (e.g., wild versus captive-bred) vary greatly. For example, specimens born into and raised in captivity are typically fed a regular and uniform diet, whereas the diets and feeding frequency of wild individuals are highly variable, and fluctuate according to environment (e.g., seasonal resource availability) and physiology (e.g., diet changes over ontogeny) (Hobson, 1999, Bowen et al., 2005, Fry, 2006, Satterfield and Finney, 2002, Lyons and Natusch, 2015). For these reasons, the ratios of stable isotopes and the concentrations of many elements (e.g., heavy metals) accumulate at different rates within tissues, which can manifest as a specific isotopic or elemental “signature” indicative of the source or geographic origin of a particular specimen (Fry, 2006). Isotopic and elemental signatures have been successfully used to differentiate between wild and captive-bred mink (Hammershøj et al., 2005), between wild and farmed crustaceans, fish, and sea turtles (Moncada et al., 1998, Dempson and Power, 2004, Carter et al., 2015), and have recently been tested as a means to determine the origin of traded elephant ivory (Ziegler et al., 2016) and the source of Vietnamese crocodile lizards (M. van Schingen pers. comm. 2016).
Worldwide, reptiles are the wildlife group most commonly represented in illegal wildlife seizures (UNODC, 2016). Reptile trade is dominated by the trade in skins (primarily snakes, crocodilians and large lizards), with tens of millions of specimens traded annually to meet demand for exotic leathers (Luxmoore and Groombridge, 1990, Jenkins and Broad, 1994). Two of the most commercially important reptile species are the Burmese python (Python bivittatus) and reticulated python (Python reticulatus). Annual trade in skins of these species is estimated at a combined total of 500,000 specimens, with the value of their export, transformation, and product sales, estimated to be worth $US 1 billion (Kasterine et al., 2012). Both species are sourced either from the wild in Indonesia and Malaysia or from captive breeding farms in China, Thailand and Viet Nam (Kasterine et al., 2012, Natusch and Lyons, 2014, Natusch et al., 2016a). There is evidence of significant illegal trade in python skins (Kasterine et al., 2012, Natusch et al., 2016a). Specifically, concerns exist that those countries breeding snakes in captivity may be supplementing breeding efforts with wild-caught specimens, or that skins are being smuggled from one country to another (Kasterine et al., 2012, Natusch and Lyons, 2014, Natusch et al., 2016a).
Reticulated pythons remain common throughout their range, but Burmese pythons are considered vulnerable due to habitat loss and overexploitation (IUCN, 2012). Although both species are in no immediate risk of extinction, an accurate knowledge of the geographic origin and source (wild or captive-bred) of skins entering trade is critical for certifying export legality and confirming ongoing sustainability. Beyond these species, development of techniques to verify the source and origin of reptile skins in trade may prove vital for conserving other taxa at far greater risk of overexploitation. To test the efficacy of using isotopic and elemental markers for regulating the trade in reptile skins, we collected tissue samples from wild and captive-bred Burmese and reticulated pythons, as well as experimentally reared Burmese pythons under different diet regimes. We addressed three central questions: can isotopic and elemental markers be used to determine (1) the source of reptile skins (i.e., differentiate between wild and captive-bred specimens); (2) the geographic origin of reptile skins; and (3) if manipulation of those markers can create specific signatures useful for future forensic examinations of reptile skins entering trade.
Section snippets
Compliance statement
We stress that no snakes were harmed for the purpose of our study; we merely utilised an existing trade. Our data were gathered from snakes bred for a commercial industry, which employs humane methods of killing reptiles for the skin trade (by brain destruction; Swiss Federal Veterinary Office, 2013). We collected all skin samples from dead snakes. All fieldwork was carried out with relevant permissions and permits from the Ministry of Research and Technology of the Republic of Indonesia
Results
We obtained a total of 117 skin samples of known origin from the two snake species in our study (68 Burmese python; 49 reticulated python; sample sizes for each treatment analysed are provided in Table 1, Table 2, Table 3, Table 4).
Discussion
Isotopic and elemental analyses on the skins of pythons reared in different locations and under different environmental conditions hold immense potential for verifying the source and origin of specimens entering trade. Differences in both isotope ratios (in particular of δ13C and δ15N) and elemental concentrations allowed 100% discrimination between wild and captive-bred pythons. Elemental concentrations also offered 100% discrimination between pythons of different origin (Indonesia versus Viet
Acknowledgments
We thank staff from the Vietnamese Forest Protection Departments of Ca Mau and Ho Chi Minh City, Viet Nam, and from the Nature Conservation Department (BKSDA), Indonesia, for assistance in collecting tissue from wild and captive-bred pythons. We thank Cao Tran Thinh and Cao Tran Tung for allowing us to use their python breeding facilities and specimens in our experimental treatments. Thanks to Tomas Waller for assistance in collecting data from captive pythons. Thanks to the CITES Management
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