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International trade in amphibians: a customs perspective Helen Gerson M.Sc. Food, Plant and Animal Program, Commercial Border Programs, Canada Border Services Agency, 150 Isabella Street, 5th Floor, Ottawa, Ontario Canada K1A 0L8;

Little is known about amphibian species in international trade. Canadian customs documentation for importation of live amphibians, frogs’ legs and medicinal amphibian products was reviewed to determine the species imported into Canada. Descriptions of amphibian species in trade, origins and quantities are provided. Recommendations are made to improve the species-specific trade data collected by regulatory authorities with a view to addressing conservation concerns for amphibians.

Introduction International trade of amphibians for use as pets, bait, medicinal products, biological supplies and food contributes to overexploitation of species, introductions of invasive alien species and the spread of diseases (Carpenter et al., 2007; Kriger & Hero, 2009; Schloegel et al., 2009). Recent publications describe the significant quantities of amphibians in international trade. For example, Warkentin et al. (2009) and Gratwicke et al. (2010) used the United Nations (UN) Commodity Trade Statistics Database to highlight the annual global imports of between 8,000,000 and 12,000,000 kg of frogs’ legs between 1996 and 2006. The information missing from most reviews of international trade in amphibians is the actual species in trade. Furthermore, international Harmonized Commodity Description and Coding System (HS) codes for trade specific to live amphibians do not exist and the HS code for meat of amphibians ¢ frogs’ legs ¢ was removed from the HS in 2007. If countries are to accurately identify risks to amphibian species of overexploitation for commercial international trade, of introductions of invasive amphibian species and of spread of amphibian diseases, it is essential that the species in trade be identified and that monitoring of global amphibian trade be enabled by separate international commodity codes for amphibians. Customs documentation for importations of amphibians into Canada was reviewed to contribute to the discussion of what species of amphibians are traded globally, how these

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species are identified on customs and other regulatory documentation, and how amphibians are currently classified in the HS.

Material and methods From 1996 to the present, selected import documents were reviewed to determine species, quantities and origins of live amphibians, frogs’ legs and medicinal amphibian products imported into Canada. Reports, based on HS codes for live reptiles, live fish, live ‘‘other’’ animals, frogs’ legs, and medicinal and herbal products as criteria, were generated from Canada Border Services Agency (CBSA) systems to provide lists of imports of these commodities. Overall, approximately 900 commercial invoices and associated import documents from CBSA archives and electronic systems for shipments most likely to contain amphibians (based on the author’s experience) were selected for review from the reports generated. Species information is based on documentation reviews only. Much of the information on the importation of live amphibians and medicinal products was obtained opportunistically while reviewing import documentation for other commodities; information on quantities of live amphibians in individual shipments was not usually recorded. Nevertheless, a comprehensive review of documentation concerning shipments of live fishes imported into Canada from October 1, 2004 to September 30, 2005 provided the opportunity to include detailed observations on species, quantities and origins of live amphibians imported into Canada under the HS code for live ornamental fishes. Information on species of live amphibians exported from the USA to Canada in 2002 was obtained from an unpublished report produced by TRAFFIC North America. The source of the data was the U.S. Fish and Wildlife Service’s Law Enforcement Management Information System (E. Cooper, unpublished data). There is no requirement for traders to indicate on Canadian import documentation whether amphibians are sourced from the wild or bred in captivity. These data are available, however, for some shipments on associated import documents, such as Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) permits and the U.S. Fish and Wildlife Service Declaration for Importation or Exportation of Fish or Wildlife. Thus, information on source of amphibians could not be consistently collected, particularly for amphibians from countries other than the United States and for non-CITES species.

Results Origin, quantities and species of frogs’ legs, live frogs and amphibian products imported into Canada for food and medicine Large quantities of frozen frogs’ legs are imported into Canada, mainly from Indonesia and Viet Nam (fig. 1). The quantities imported from Indonesia have been declining since 1998

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Fig. 1. ¢ Frogs’ legs imports into Canada from 1996 to 2009. ‘‘Other Countries’’ include China, Korea, France, Taiwan, Turkey and the United States.

and currently make up a relatively small proportion of the total imports, whereas the quantities from Viet Nam have been increasing and seem to have levelled off since 2006. Overall, there are large fluctuations, but there is no apparent trend in imports of frogs’ legs into Canada. The only species that was observed recorded on customs documentation for Indonesian frogs’ legs is Limnonectes macrodon. This species was often indicated on commercial invoices from vendors in Indonesia and Belgium (country of re-export) from 1996 to the present. It is highly unlikely that this is the only species from Indonesia that is imported into Canada; Kusrini & Alford (2006) report that exports of frogs’ legs from Indonesia consist of several species. Import documentation for frogs’ legs from Viet Nam did not indicate the species name on all of the entries reviewed from 1996 to 2002. Most commercial invoices from Viet Nam indicated the product simply as frogs’ legs or frozen frogs’ legs. Beginning in 2003, the species name Rana tigerina, or Hoplobatrachus tigerinus, began to be indicated on some of the commercial invoices and Viet Nam was issuing CITES export permits for this species. Once the Scientific Authority of Viet Nam was advised by the Nomenclature Committee of CITES that the species concerned is H. rugulosus, and that H. tigerinus (included in CITES Appendix II) does not occur in Viet Nam (Anonymous, 2002), Viet Nam began to use the scientific name Hoplobatrachus rugulosus and continues to issue export permits (non-CITES) for this species.

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All of the permits issued by Viet Nam indicate that the H. rugulosus exported from the country is captive reared. Other species recorded on import documentation for frozen and fresh frogs’ legs are Rana catesbeiana (importers still use this synonym; valid name is Lithobates catesbeianus) from China, the United States, Canada and Taiwan, and Rana esculenta from Turkey and France. Importers also bring three thousand to five thousand live bullfrogs, annually, from the United States into Canada for human consumption. The HS code used by traders for the importation of frogs’ legs before 2007 was HS0208.20; however, this HS code was discontinued in the 2007 version of the HS. The reason cited for this deletion by the World Customs Organization (WCO) was ‘‘the low volume of trade’’ in this commodity (Anonymous, 2007). As of 2007, there is no longer a separate HS code that can be used to monitor international trade of frogs’ legs. Frogs’ legs now fall under HS0208.90, which is a catch-all category for animal species not elsewhere specified in the HS nomenclature for meat. Thus a major part of the UN data that Warkentin et al. (2009) and Gratwicke et al. (2010) relied on to analyze the frogs’ legs trade is no longer collected, thereby eliminating the possibility of similar future analyses. Amphibian products that are part of herbal or medicinal products from China are reported as Oviductus Ranae, Forest Frog’s Oviduct and Dried Toad Ovary. Other than the description, Ranae, indicating that the amphibians may be ranid species, the scientific name of species is not reported on the customs documentation for these products. Such products are usually imported in quantities of 5 to 20 kg within large shipments of herbal medicines and foodstuffs. They are reported under a variety of HS codes (in some cases incorrectly), such as HS0410.00, which refers to edible products of animal origin not specifically described elsewhere in the HS nomenclature; HS0210.99, which refers to meat and edible meat offal, salted, in brine, dried or smoked; and HS1211.90, which includes ‘‘herbs’’. Origin, quantities and species of live amphibians imported into Canada for the pet, aquarium and water garden trades The amphibian species reported on commercial import documentation over the past eight years are indicated in tab. 1. Of note is the high degree of use of non-valid scientific names (synonyms) that are reported to customs. The Taxonomic Serial Numbers (TSN) of the Integrated Taxonomic Information System (ITIS) are included both for the synonyms reported and the valid names for each species in tab. 1. Unlike the frogs’ legs trade, which generally consists of large shipments on the order of 10,000 to 20,000 kg each, shipments of live amphibians are typically much smaller, ranging from one to several hundred individuals in a single shipment. Rarely, shipments include as many as 2,000 individuals. Most shipments consist of adults, but Xenopus sp. and L. castesbeianus tadpoles are imported. The only detailed quantity data available for live amphibians are the records for those amphibians classified under the HS code for live ornamental fishes as described in the Material and methods section. Records indicate that during the one-year period reviewed, almost 180,000 individual live amphibians were imported for the aquarium and water garden trades under HS0301.10 (B. Cudmore, N. Mandrak

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& H. Gerson, unpublished data). The species most commonly reported in these shipments were Bombina orientalis, Cynops orientalis, Hymenochirus sp., L. catesbeianus, and Xenopus laevis. Although a significant proportion of the trade consists of captive bred amphibians, particularly for aquaria and water gardens, many of the other species imported live in smaller quantities were indicated on associated import documents as being sourced from the wild. Of the 172 species identified in tab. 1, 26 are assessed as threatened in the IUCN Red List of Threatened Species (Anonymous, 2010a). An additional eight species are identified as Data Deficient. Live amphibians imported into Canada originate from a wide variety of countries (fig. 2). The United States is by far the major source of live amphibians exported to Canada. More than one half of the species imported into Canada were exported or re-exported from the United States. Although some of these species are native to the United States and sourced from the wild (e.g., Hyla cinerea), most are either captive bred in the United States (e.g., L. catesbeianus) or sourced from the wild (e.g., Litoria infrafenata) or captive rearing facilities (e.g., Agalychnis callidryas) in other countries and imported into the United States from where they are exported, or re-exported, to Canada. Weldon et al. (2004) placed the origin of the amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd) in Africa, and international trade of X. laevis, beginning in the mid-1930s, as the means of dissemination of the fungus. Alternatively, Goka et al. (2009) detected Bd in captive bred and wild, native, exotic and imported species and proposed that some strains of Bd are endemic to amphibians native to Japan and that Bd may have originated in Asia. The species in tab. 1 whose names are in bold are those that have tested positive for Bd (Aanensen et al., 2010). Of the 172 different species in tab. 1 that have been imported into Canada, a minimum of 43 or 25 % can potentially carry Bd. It is a difficult and time-consuming process to document species in trade because most countries, including Canada, do not currently have the mechanisms to electronically capture, store and retrieve wildlife trade data, in particular species data. It is even more challenging to retrieve amphibian data from data systems because of the lack of separate HS codes for amphibians. Document reviews indicate that live amphibians are reported by importers and customs brokers under the HS codes for live fishes (HS0301.10 and HS0301.99), live reptiles (HS0106.20) and other live animals (HS0106.90). The latter HS code is where live amphibians are currently correctly classified; nevertheless, in a review in 2002 of 710 data records for imports of commodities classified as HS0106.90, only ten records were actually amphibians. All other amphibians imported that year were classified incorrectly under the other HS codes.

Discussion Collection and harvesting of amphibians may pose serious threats to some species, particularly those with more restricted distributions and population sizes, and may exacerbate the effects of diseases, invasive species, pollution and habitat alteration already affecting species. Knowledge of species in international trade assists assessors in determining threats to

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Fig. 2. ¢ Number of live amphibian species imported from each country.

species and recommending conservation actions (e.g., Sharifi et al., 2008; Veloso et al., 2008). The large proportion of species indicated in tab. 1 that have tested positive for Bd demonstrates the potential for the introduction and spread of this disease through the international amphibian trade. Of particular concern in Canada is the increasing trend in importation of L. catesbeianus (adults and tadpoles) for water gardens and ponds, which increases the likelihood of the spread of Bd and ranavirus directly to the environment. Schloegel et al. (2009) demonstrated that a high proportion of L. catesbeianus imported into the United States is infected with Bd and to a lesser extent with ranavirus and thus provide support for the World Organization for Animal Health listing of B. dendrobatidis and ranaviral diseases of amphibians (Anonymous, 2010b). Despite the concerns for global environmental and social issues, which are incorporated in the HS 2012 amendments, particularly those identified by the UN Food and Agriculture Organization for aquatic organisms, specific HS codes for frogs’ legs and live amphibians continue to be absent from the HS (Anonymous, 2010c). Apparently this issue has not been brought to the WCO for consideration. It would be important for both environmental and social reasons to include amphibians in the next version of the HS after 2012. Since the HS is amended every five to six years, the next version is scheduled for 2017 at the earliest. In the meantime, even if amphibians are eventually incorporated into the HS, it is necessary to establish an international mechanism to capture specific species data. Much of the customs documentation provided to Canadian border authorities currently does not indicate the scientific names of species. Nevertheless, with the development of single window

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reporting and adoption of the WCO data model, many countries and organizations, such as CITES, are moving towards the adoption of electronic, harmonized trade data standards (Anonymous, 2010c), which will facilitate the standardized reporting of scientific names of species. Gerson et al. (2008a¢b) proposed the use of the TSN as a coded data element for reporting scientific names of taxa and as a complement to the HS to monitor species in international trade. Canada proposed this idea at the Fifteenth Meeting of the Conference of the Parties of CITES (Anonymous, 2009). Based on Canada’s description of the potential usefulness of TSNs to assist customs and other regulatory authorities with species data collection and management, monitoring and enforcement, Canada’s proposed draft decisions were accepted, including encouragement of the Parties to consider the usefulness of incorporating TSNs in their domestic data systems (Anonymous, 2010d). Considering that amphibians in international trade are well covered in ITIS (there are only three scientific names identified in tab. 1 that do not have a TSN assigned to them); that some species of amphibians are subject to CITES controls; that importers and customs brokers frequently report older scientific names, or synonyms, for amphibians and that these synonyms usually have TSNs assigned to them that can subsequently be linked to valid scientific names in ITIS; and that importers and customs brokers frequently misspell scientific names; the taxon Amphibia, might be a good place to start collecting species trade information in the form of TSNs from the trade community. Canada’s customs legislation (Customs Act, Section 7.1) requires that any information provided to an officer in the administration or enforcement of the Act, as well as the Customs Tariff or under any other Act of Parliament that prohibits, controls or regulates the importation or exportation of goods, shall be true, accurate and complete. For plants and animals, and their parts and derivatives, the most accurate and complete information is the scientific name of the species. To date, this requirement has not translated into a legal requirement for traders to specify the scientific names of

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species in trade in Canada, and this has resulted in a lack of knowledge and confusion about what species are being traded globally. Fragoso & Ferriss (2008) agreed that mechanisms to monitor trade in species are needed, but they proposed an alternative approach that involves a reporting system to identify relevant regulatory instruments, which could be linked to forms requiring taxonomic and other information. Future decisions by countries to regulate international trade in amphibians because of the clear threats posed by trade in species that are carriers of Bd and ranavirus and to prevent overharvesting and spread of invasive amphibian species must be based on a sound knowledge of amphibian trade data. Whatever approaches are adopted by decision-makers, accurate, standardized and internationally harmonized reporting of scientific names of amphibian species in trade to customs and other regulatory authorities is a necessary first step in enabling conservation decisions and consequent policy, legislative and regulatory development.

Literature cited Anonymous [IUCN], 2001. ¢ IUCN Red List Categories and Criteria Version 3.1. IUCN Species Survival Commission IUCN, Gland: Switzerland and Cambridge, UK ii + 30 pp. Anonymous [CITES], 2002. ¢ Nomenclature Committee Report. CoP12 Doc. 10.3 (Rev. 1). Twelfth meeting of the Conference of the Parties Santiago (Chile), 3¢15 November 2002. Anonymous [WCO/OMD ¢ World Customs Organization / Organisation Mondiale des Douanes], 2007. ¢ Correlating the 2007 version to the 2002 version of the harmonized system. Brussels, Belgium, World Customs Organization. http://www.wcoomd.org/home_hsoverviewboxes_tools_and_instruments_hscorrelationtables200 22007.htm> [accessed September 2010]. Anonymous [Environment Canada], 2009. ¢ Using the Taxonomic Serial Number (TSN) in international wildlife trade data: a role for CITES. CoP15 Doc. 39. Submitted to the Fifteenth meeting of the Conference of the Parties, Doha (Qatar), 13¢25 March 2010. [accessed November 2010]. ----- [OIE ¢ Office International des Epizooties], 2010b. ¢ OIE listed diseases. World Organisation for Animal Health, Paris, France. [accessed May 2010]. Aanensen, D. M., Spratt, B. G., Fisher, M. C., Olson, D. & Ronnenberg, K., 2010. ¢ Bd-Maps. < http://www.spatialepidemiology.net/bd-maps/> [accessed July 2010]. Carpenter, A. I., Dublin, H., Lau, M., Syed, G., Mckay, J. E. & Moore, R. D., 2007. ¢ Chapter 5: Over-harvesting. In: C. Gascon, J. P. Collins, R. D. Moore, D. R. Church, J. Mckay &

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J. R. Mendelson III (ed.), Amphibian Conservation Action Plan, Gland, International Union for Conservation of Nature and Natural Resources: 26¢31. Fragoso, G. & Ferriss, S., 2008. ¢ Monitoring international wildlife trade with coded species data: response to Gerson et al. Conserv. Biol., 22 (6): 1648¢1650. Gerson, H., Cudmore, B., Mandrak, N. E., Coote, L., Farr, K. & Baillargeon, G., 2008a. ¢ Monitoring international wildlife trade with coded species data. Conserv. Biol., 22 (1): 4¢7. ----- 2008b. ¢ Use of the Taxonomic Serial Number (TSN) as a required data element in international wildlife trade: response to Fragoso and Ferriss. Conserv. Biol., 22 (6): 1651¢1654. Goka, K., Yokoyama, J., Une, Y., Kuroki, T., Suzuki, K., Nakahara, M., Kobayashi, M., Inaba, S., Mizutani, S. & Hyatt, A. D., 2009. ¢ Amphibian chytridiomycosis in Japan: distribution, haplotypes and possible route of entry into Japan. Molec. Ecol., 18: 4757¢4774. Gratwicke, B., Evans, M. J., Jenkins, P. T., Kusrini, M. D., Moore, R. D., Sevin, J. & Wildt, D. E., 2010. ¢ Is the international frog legs trade a potential vector for deadly amphibian pathogens? Front. Ecol. Environ., 8 (8): 438¢442. Kriger, K. M. & Hero, J. M., 2009. ¢ Chytridiomycosis, amphibian extinctions, and lessons for the prevention of future panzootics. EcoHealth, 6 (1): 148¢151. Kusrini, M. D. & Alford, R. A., 2006. ¢ Indonesia’s exports of frogs’ legs. TRAFFIC Bull., 21 (1): 14¢24. Schloegel, L. M., Picco, A. M., Kilpatrick, A. M., Davies, A. J., Hyatt, A. D. & Daszak, P., 2009. ¢ Magnitude of the US trade in amphibians and presence of Batrachochytrium dendrobatidis and ranavirus infection in imported North American bullfrogs (Rana catesbeiana). Biol. Cons., 142: 1420¢1426. Sharifi, M., Papenfuss, T., Rastegar-Pouyani, N., Anderson, S. & Kuzmin, S., 2008. ¢ Neurergus kaiseri. In: IUCN 2010, IUCN Red List of Threatened Species, Version 2010.4. [accessed November 2010]. Veloso, A., Formas, R. & Gerson, H., 2008. ¢ Calyptocephalella gayi. In: IUCN 2010, IUCN Red List of Threatened Species, Version 2010.4. [accessed November 2010]. Warkentin, I., Bickford, D., Sodhi, N. & Bradshaw, C., 2009. ¢ Eating frogs into extinction. Conserv. Biol., 23 (4): 1056¢1059. Weldon, C ., Du Preez, L. H., Hyatt, A. D., Muller, R. & Spears, R., 2004. ¢ Origin of the amphibian chytrid fungus. Emerg. infect. Dis., 10 (12): 2100¢2105. Corresponding editor: Ariadne Angulo.

Disclaimer The views of the author expressed in this publication do not necessarily reflect those of the Canada Border Services Agency.

© ISSCA 2012