REVIEW OF NON-CITES AMPHIBIA SPECIES THAT ARE KNOWN OR LIKELY TO BE IN INTERNATIONAL TRADE

REVIEW OF NON-CITES AMPHIBIA SPECIES THAT ARE KNOWN OR LIKELY TO BE IN INTERNATIONAL TRADE (Version edited for public release) Prepared for the European Commission Directorate General E - Environment ENV.E.2. Development and Environment by the United Nations Environment Programme World Conservation Monitoring Centre November, 2007

Prepared and produced by: UNEP World Conservation Monitoring Centre, Cambridge, UK ABOUT UNEP WORLD CONSERVATION MONITORING CENTRE www.unep-wcmc.org The UNEP World Conservation Monitoring Centre is the biodiversity assessment and policy implementation arm of the United Nations Environment Programme (UNEP), the world s foremost intergovernmental environmental organisation. UNEP-WCMC aims to help decision-makers recognize the value of biodiversity to people everywhere, and to apply this knowledge to all that they do. The Centre s challenge is to transform complex data into policy-relevant information, to build tools and systems for analysis and integration, and to support the needs of nations and the international community as they engage in joint programmes of action. UNEP-WCMC provides objective, scientifically rigorous products and services that include ecosystem assessments, support for implementation of environmental agreements, regional and global biodiversity information, research on threats and impacts, and development of future scenarios for the living world. Prepared for: The European Commission, Brussels, Belgium Prepared by: UNEP World Conservation Monitoring Centre 219 Huntingdon Road, Cambridge CB3 0DL, UK The contents of this report do not necessarily reflect the views or policies of UNEP or contributory organisations. The designations employed and the presentations do not imply the expressions of any opinion whatsoever on the part of UNEP, the European Commission or contributory organisations concerning the legal status of any country, territory, city or area or its authority, or concerning the delimitation of its frontiers or boundaries.

TABLE OF CONTENTS 1. INTRODUCTION... 4 1.1. TRADE IN AMPHIBIANS... 4 1.2. AMPHIBIANS AND THE IUCN RED LIST... 5 1.3. THE IMPACT OF TRADE ON AMPHIBIANS... 6 1.4. SELECTION OF SPECIES FOR REVIEW... 7 1.4.1. Current review (SRG 42)... 7 1.4.2. Potential future review... 7 1.5. REFERENCES... 19 2. SPECIES REVIEWS... 20 2.1. METHODOLOGY... 20 SPECIES: Agalychnis annae... 22 SPECIES: Limnonectes macrodon... 25 SPECIES: Neurergus kaiseri... 29 SPECIES: Neurergus microspilotus... 32 SPECIES: Rana shqiperica... 34 SPECIES: Bolitoglossa dofleini... 38 SPECIES: Chacophrys pierottii... 41 SPECIES: Heterixalus rutenbergi... 44 SPECIES: Leptodactylus laticeps... 46 SPECIES: Melanophryniscus fulvoguttatus... 50 SPECIES: Pachytriton labiatus... 53 SPECIES: Paramesotriton hongkongensis... 55 SPECIES: Phyllomedusa sauvagii... 59 ANNEX 1. Overview of amphibian species for which regional/international trade (threats 3.1.3, 3.2.3, 3.3.3., 3.4.3, and 3.5.3) may pose a major threat.... 63 ANNEX 2. Country codes.... 67 INDEX OF TABLES Table 1. Summary table of CITES and/or EC-listed amphibians.... 4 Table 2. Overview of global exporter-reported trade in CITES Appendix II and/or EC Annex B amphibians between 1994-2006.... 5 Table 3. Number of amphibian species within each of the IUCN Red List categories.... 6 Table 4. Non-CITES globally threatened amphibian species, with regional/international trade as major threat type.... 9 Table 5. Non-CITES-listed amphibian species that are not considered globally threatened in the IUCN Red List but which are possibly threatened by international trade... 13 3

1. INTRODUCTION This report provides an analysis of amphibian species which are not listed in CITES but for which regional or international trade was considered to be a major threat in the 2007 IUCN Red List. In-depth reviews were undertaken for 13 species to see whether they meet the criteria for listing in any of Annexes A, B or D 1 of Council Regulation 338/97. 1.1. TRADE IN AMPHIBIANS Amphibians have been traded for food, the pet trade, medicinal products, etc. (Schlaepfer et al., 2005; AmphibiaWeb, 2006; Carpenter et al., 2007; Tyler et al. 2007). However, trade data are not generally available for most species, since only a small number of them are listed in CITES. It was noted by one author (Schlaepfer et al., 2005) that the majority of the most heavily traded amphibians were not regulated by CITES (for instance, none of the 25 amphibian species most commonly traded by the US was listed). Unlike most countries, the United States records the imports and exports of all amphibians (Schlaepfer et al., 2005). Although data are often not collected at the species level, they can, however, provide an overview of the trade in one market. Over two million amphibians were known to be imported into the US during 1970-1971; leopard frogs (Rana pipiens), fire newts (Cynops pyrrogaster) and marine toads (Bufo marinus) were imported in the highest numbers (Busack, 1974). An estimated 200 million pairs of frogs legs were imported annually from Asia to the United States before 1987 (Pough et al., 1998). During 1998-2002, the United States imported 14.7 million wild-caught amphibian specimens, and 5.2 million kg of wild-caught amphibian meat. The most frequently traded species were the American bullfrog (Rana catesbeiana) for the food trade and the African dwarf frog (Hymenochirus curtipes) and the oriental fire-bellied newt and toad (Cynops orientalis and Bombina orientalis) for the pet trade (Schlaepfer et al., 2005). A broader view of the international trade is only possible for those species listed in the CITES appendices. At present, 106 amphibian species are listed in CITES. A total of 16 species are listed in Appendix I and the remainder are listed in Appendix II, see Table 1. Recent trade (1994-2006) in CITES-listed amphibians is summarized in Table 3. Table 1. Summary table of CITES and/or EC-listed amphibians. Sources: Frost, 2004; EC Regulation No. 1332/2005. Order Family Species CITES Appendix EC Annex ANURA Bufonidae Altiphrynoides spp. I A Atelopus zeteki I A Bufo periglenes I A Bufo superciliaris I A Nectophrynoides spp. I A Nimbaphrynoides spp. I A Spinophrynoides spp. I A Dendrobatidae Allobates femoralis II B Allobates zaparo II B Dendrobates spp. II B Epipedobates spp. II B Minyobates spp. II B Phyllobates spp. II B Mantellidae Mantella spp. II B Microhylidae Dyscophus antongilii I A Scaphiophryne gottlebei II B Ranidae Conraua goliath - B Euphlyctis hexadactylus II B Hoplobatrachus tigerinus II B Rana catesbeiana - B 1 Annex C was not considered relevant as it includes only species listed in CITES Appendices II or III. 4

Order Family Species CITES Appendix EC Annex Rheobatrachidae Rheobatrachus silus II A Rheobatrachus vitellinus II B URODELA Ambystomidae Ambystoma dumerilii II B Ambystoma mexicanum II B Cryptobranchidae Andrias spp. I A Table 2. Overview of global exporter-reported trade in CITES Appendix II and/or EC Annex B amphibians between 1994-2006. Proportion of wildsourced Taxon Volume of trade in main terms 1994-2006 trade Allobates femoralis 89 live, 46 bodies 9% (live), 100% (bodies) Allobates zaparo 75 live (trade in 2000-2001 only) 0% Dendrobates spp. (25 spp.) 121,273 live (2006 excluded) 23% Epipedobates spp. (4 spp.) 16,448 live 52% Phyllobates spp. (5 spp.) 5,239 live 0.5% Mantella spp. (14 spp.) 237,676 live 99% Scaphiophryne gottlebei 1158 live (trade in 2003-2005 only) 100% Conraua goliath 19 live (trade in 2001 only) 100% Rana catesbeiana 65,000 live (single transaction in 2003) 0% Hoplobatrachus tigerinus 5,750,658 kg meat 2% Ambystoma mexicanum 59,759 live 0.13% In very general terms, most amphibians exploited for food and medicine are found in Asia, and many of the species in the pet trade occur in South America and Madagascar (Baillie et al., 2005; Carpenter et al., 2007). In China, for example, 32 species were recognized to be of medicinal value in traditional Chinese medicine (Ye et al., 1993, cited in Carpenter et al., 2005). In Asia, exploitation for food is mainly directed towards the larger-bodied species of the family Ranidae, as well as, for example, the Critically Endangered Chinese Giant Salamander, Andrias davidianus (Baillie et al., 2005). The species in the pet trade are usually salamanders and the colourful small frogs, in particular of the genera Dendrobates and Epipedobates from Central and South America, and Mantella from Madagascar (Baillie et al., 2004; Andreone et al., 2006). The latter three genera are listed in the CITES appendices. 1.2. AMPHIBIANS AND THE IUCN RED LIST The IUCN Red List of Threatened Species provides taxonomic, conservation status and distribution information on taxa that have been globally evaluated using the IUCN Red List Categories 2 and Criteria. A detailed explanation of the criteria used can be found at www.redlist.org. Critically Endangered, Endangered and Vulnerable species are generally considered to be threatened. The status of all of the world s 5,915 known amphibian species has been evaluated by the Global Amphibian Assessment (GAA) team (IUCN et al., 2007). The GAA estimated that 1,808 amphibian species (31% of the total) were globally threatened (Table 3), although this number could be considerably higher, since a further 1,426 species were Data Deficient (IUCN, 2007). 2 The IUCN Red List categories are as follows: Extinct (EX); Extinct in the Wild (EW); Critically Endangered (CR); Endangered (EN); Vulnerable (VU); Near Threatened (NT); Least Concern (LC); Data Deficient (DD); Not Evaluated (NE) 5

Table 3. Number of amphibian species within each of the IUCN Red List categories. Source: IUCN (2007). IUCN Red List Category Number of Amphibian species CR 441 EN 737 VU 630 NT 369 LC 2277 DD 1426 EW 1 EX 34 Total 5915 The IUCN Red List also provides a classification of causes of species decline. Assessors are asked to indicate the threats that triggered the listing of the taxon concerned at the finest level possible. These threats could be in the past and/or present and/or future, using a timeframe of three generations or ten years, whichever is the longer (not exceeding 100 years in the future). Threats are subdivided in a hierarchical system. For the purposes of this report, threat number 3 (Harvesting) is the most relevant one. It is subdivided in the following way: 3. Harvesting [hunting/gathering] 3.1. Food 3.1.1. Subsistence use/local trade 3.1.2. Sub-national/national trade 3.1.3. Regional/international trade 3.2. Medicine 3.2.1. Subsistence use/local trade 3.2.2. Sub-national/national trade 3.2.3. Regional/international trade 3.3. Fuel 3.3.1. Subsistence use/local trade 3.3.2. Sub-national/national trade 3.3.3. Regional/international trade 3.4. Materials 3.4.1. Subsistence use/local trade 3.4.2. Sub-national/national trade 3.4.3. Regional/international trade 3.5. Cultural/scientific/leisure activities 3.5.1. Subsistence use/local trade 3.5.2. Sub-national/national trade 3.5.3. Regional/international trade 3.6. Other 3.7. Unknown 1.3. THE IMPACT OF TRADE ON AMPHIBIANS Although habitat loss and degradation, pollution and the fungal disease chytridiomycosis are considered to be the greatest threats to amphibians at present, over-harvesting and trade have also been identified as major causes of decline for a number of species (Gibbons et al., 2000, Young et al., 2004; Gascon et al., 2007; IUCN et al., 2007). 6

The effect of trade on wild amphibian populations, however, is often unclear (e.g. Young et al., 2001; Beebee & Griffiths, 2005), both because trade levels of species are generally not known (Schlaepfer et al., 2005; Silvano & Segalla, 2005) and/or because there are usually insufficient data on wild populations and their trends (Gascon et al., 2005). In addition, several threats can interact in different ways, for instance there is strong evidence that the global trade in amphibians is driving the emergence of chytridiomycosis (Fisher & Garner, 2007) and in some cases also resulting in the introduction into the wild of invasive species that may in turn impact on native ones (Gascon et al., 2005). The most comprehensive available data on the status of amphibian species and on the threats affecting them were gathered by the Global Amphibian Assessment team and used for the IUCN Red List. According to these data, threat 3 of the IUCN Red List (Harvesting - hunting/gathering-) was considered to be a major threat type for 283 amphibian species (IUCN, 2007). More specifically, regional/international trade (threats 3.1.3, 3.2.3, 3.3.3., 3.4.3, and 3.5.3) was a major threat type for 134 of those species. These species are traded for food (17 species), medicine (10 species), or cultural/scientific/leisure activities mostly the pet trade- (114 species). Out of the 134 species for which regional/international trade was considered to be a major threat, 54 are globally threatened, and 46 are listed in CITES (Annex 1). 29 species, however, are globally threatened but not listed in CITES (see Section 1.4). 1.4. SELECTION OF SPECIES FOR REVIEW 1.4.1. Current review (SRG 42) This report aimed to identify species of amphibian that might be threatened by trade and review those species which might be most affected by the trade. Table 4 presents the globally threatened (CR/EN/VU) amphibian species that are not listed in CITES or the Annexes to the EU wildlife trade Regulations and for which regional and/or international trade has been identified as a major threat by the Global Amphibian Assessment team. Table 5 summarises those species that were not considered to be globally threatened, but for which trade was nonetheless considered to be a major threat. Species were selected from both these groups (Tables 4 and 5) for in-depth review. The selection was based on preliminary information on the trade in the species (giving priority to species for which international trade is a known ongoing threat) and on the threat status of species (giving higher priority to the most threatened species). Five globally threatened species were initially selected for review to see whether they may warrant listing in the annexes of the EU wildlife trade regulations. Eight additional species from Table 5 were also selected for review. Further details on the review methodology are provided in section 3.1. 1.4.2. Potential future review A further 15 threatened and 25 non-threatened species were identified as species that may warrant future review on the basis of their threat status and nature of the trade. These have been highlighted in Tables 4 and 6 with a? in the right hand column. It is suggested that a number of these species could be selected by the SRG for future review to assess whether they meet the criteria for listing in the annexes to Council Regulation 338/97. The species selected for this review and those flagged for potential future review are species considered to be threatened by international trade by IUCN et al. (2007). It has been noted during the preparation of this report, however, that a number of species which are not considered to be threatened by international trade, and which are therefore not considered 7

here, are actually seen in trade frequently, although the impact of the trade is not clear. It is suggested that an Internet market survey of non-cites amphibian species could be undertaken in the future in order to identify which other species are most highly traded and whether trade may present a threat. 8

ANURA Table 4. Non-CITES globally threatened amphibian species, with regional/international trade as major threat type. All species are sourced from the wild (Caudiverbera caudiverbera is also captive-bred), according to GAA. Shaded species are those selected for review. A key to country codes can be found in Annex 2. Taxon BUFONIDAE Atelopus cruciger Common name Range states IUCN Red List Category Reason for trade (IUCN Red List) Rancho Grande Harlequin Frog VE CR C/S/L activities Type of trade Purpose Global Amphibian Assessment information on utilisation Time of reg./int. trade as a threat Trend in the level of harvest in relation to total wild population numbers over the last 5 years National and international Pets Ongoing Decreasing Atelopus senex CR CR C/S/L activities International Pets Past Decreasing Atelopus varius Harlequin Frog CR, PA CR C/S/L activities International Pets Past Unknown HYLIDAE Comments Overcollecting for scientific or pet trade purposes could be a potential threat. Threats might include collecting for the pet trade. It was collected by the thousands in the 1970s and shipped to Germany as part of the international pet trade. Agalychnis annae Blue-sided Treefrog CR EN C/S/L activities International Pets Ongoing Unknown Found in the international pet trade SRG 42 Specimen Phyllodytes auratus TT CR C/S/L activities International collecting Ongoing Unknown Threatened by the over collecting of specimens No Plectrohyla dasypus HN CR C/S/L activities International Pets Past Decreasing No Plectrohyla exquisita HN CR C/S/L activities International Pets Past Decreasing No LEPTODACTYLIDAE Caudiverbera caudiverbera CL VU Food MICROHYLIDAE National and International Food Present and future Increasing Extraction as exotic food item is a threat.? Platypelis milloti MG EN C/S/L activities - - Future - There is no known utilization of this species No RANIDAE Limnonectes macrodon Fanged River Frog, Javan Giant Frog, Malaya Wart Frog, Stone Creek Frog ID VU Food Subsistence, National and International Food Ongoing Increasing Review? No No No Exploitation is a major threat. It is highly exploited as food, and is eaten locally and nationally, and animals from eastern Java are exported. SRG 42 9

Taxon Rana shqiperica CAUDATA HYNOBIIDAE Common name Range states IUCN Red List Category Reason for trade (IUCN Red List) Albanian Water Frog AL, ME EN Food Hynobius tokyoensis Tokyo Salamander JP VU C/S/L activities Central Asian Salamander, Semirechensk Ranodon sibiricus Salamander CN, KZ EN PLETHODONTIDAE Type of trade Purpose Global Amphibian Assessment information on utilisation Time of reg./int. trade as a threat Trend in the level of harvest in relation to total wild population numbers over the last 5 years National and International Food Ongoing Unknown Medicine, C/S/L activities Subsistence Medicine Ongoing Unknown Comments Review? In northern parts of its range (e.g. Lake Skadar) it is significantly threatened by over collection for commercial purposes. SRG 42 National and International Pets Ongoing Unknown It is collected for pet trade? Its small population and restricted range make this species particularly susceptible to overexploitation (medical, commercial and scientific purposes).? Bolitoglossa pesrubra CR EN C/S/L activities International Pets Past Unknown No Plethodon petraeus Pigeon Mountain Salamander US VU C/S/L activities Subsistence, National and International Pets and specimen collection Present and future Unknown Over-collecting for scientific study and possibly the illegal pet trade may threaten populations.? SALAMANDRIDAE Cynops ensicauda Sword-tailed Newt JP EN C/S/L activities Anderson's Echinotriton andersoni Crocodile Newt JP, TW EN C/S/L activities Lyciasalamandra antalyana TR EN C/S/L activities Lyciasalamandra atifi TR EN C/S/L activities Subsistence and National for medicine; National and International for Pets. National and Medicine and Pets Ongoing Unknown The species is in the pet trade in Japan and is used for medicinal purposes in Taiwan International Pets Ongoing Unknown It is illegally collected for the pet trade? Potentially threatened by overcollection for National and Specimen scientific purposes. International collecting Future Unknown? National and Specimen Potentially threatened by overcollection for International collecting Future Unknown scientific purposes.? No 10

Taxon Common name Range states IUCN Red List Category Reason for trade (IUCN Red List) Lyciasalamandra billae TR CR C/S/L activities Lyciasalamandra fazilae TR EN C/S/L activities Lyciasalamandra flavimembris TR EN C/S/L activities Luschan's Salamander, Lycian Lyciasalamandra luschani Salamander GR, TR EN C/S/L activities Neurergus kaiseri IR CR C/S/L activities Neurergus microspilotus IR EN C/S/L activities Type of trade National and International National and International National and International National and International National and International Purpose Global Amphibian Assessment information on utilisation Time of reg./int. trade as a threat Trend in the level of harvest in relation to total wild population numbers over the last 5 years Specimen collecting Future Unknown Specimen collecting Present and future Unknown Specimen collecting Future Unknown Specimen collecting Future Unknown Pets Ongoing Increasing National and International Pets Ongoing Increasing Comments Potentially threatened by overcollection for scientific purposes.? Potentially threatened by overcollection for scientific purposes.? Potentially threatened by overcollection for scientific purposes.? Review? Potentially threatened by overcollection for scientific purposes.? A few animals have been observed for sale in the Tehran market, presumably for local use in aquaria (T. Papenfuss, pers. comm.). However, of greater concern is the current growing trade in the species for the international pet trade. At present it appears that individuals caught in the wild are being illegally exported out of Iran, and are finding their way into the pet trade. Some of the individuals in the trade are reportedly captive-bred but this requires confirmation. SRG 42 It is sometimes seen in the illegal pet trade which is an increasing threat to the species. Actions need to be taken immediately to prevent the illegal export of this species for a pet as is currently taking place. This is a new and increasing threat that must be stopped before it is too late. SRG 42 11

Taxon Paramesotriton deloustali Paramesotriton fuzhongensis Salamandra algira Tylototriton kweichowensis Common name Range states IUCN Red List Category Reason for trade (IUCN Red List) Tam Dao Salamander, Vietnamese Salamander VN VU C/S/L activities Wanggao Warty Newt CN VU C/S/L activities North African Fire Salamander Type of trade Subsistence (Food); Subsistence and National (Medicine); National and International (Pets) DZ, ES, MA VU C/S/L activities International Subsistence (medicine) and International (pets) Red-tailed Knobby Newt CN VU C/S/L activities Purpose Global Amphibian Assessment information on utilisation Time of reg./int. trade as a threat Trend in the level of harvest in relation to total wild population numbers over the last 5 years Food, Medicine and Pets Past Increasing Subsistence, National and International Pets Present and future Decreasing Pets and specimen collection Ongoing Unknown Medicine and Pets Ongoing Increasing Comments Harvesting for food, medicine and the pet trade are threats.? Its restricted range makes this species particularly susceptible to over-exploitation for the pet trade.? There is some collection of this species in small numbers for the international pet trade; further investigations are needed to determine the impact of trade on populations.? Collected by the locals as a kind of traditional Chinese medicine. A small number of individuals are also traded in the international pet markets.? Review? 12

Table 5. Non-CITES-listed amphibian species that are not considered globally threatened in the IUCN Red List but which are possibly threatened by international trade. ANURA BOMBINATORIDAE Taxon Common name Range States IUCN Red List Category Reason for regional/international trade Bombina maxima Large-webbed Bell Toad CN LC C/S/L activities BUFONIDAE Atelopus siranus PE DD C/S/L activities Bufo blombergi (Syn. Rhaeto blombergi) Colombian Giant Toad CO, EC NT Medicine Bufo gargarizans Asiatic Toad, Miyako Toad, Zhoushan Toad CN, JP, KP, KR, RU LC Medicine GAA information on utilisation (comments on trade as a threat) There is a small amount of international pet trade involving this species Both the pet trade and infection with chytridiomycosis are potential threats to this species, and could lead to a rapid population decline. However, its distribution is so isolated that it might be safe from these threats. In Ecuador, there is commercial export of animals for pharmacological research and the pet trade. The species is captured for laboratory research, and has been gathered for traditional medicine by Chinese and Korean citizens in the Primorye Region of Russia over the last 10 years. Melanophryniscus atroluteus Uruguay Redbelly Toad AR, BR, UY LC C/S/L activities It is possibly threatened in the future by the pet trade.? Melanophryniscus cambaraensis Brazilian Redbelly Toad BR DD C/S/L activities It is potentially threatened by the international pet trade.. (Future threat) No Melanophryniscus fulvoguttatus AR, BR, PY LC C/S/L activities It is threatened by the pet trade (Ongoing threat) SRG 42 Melanophryniscus stelzneri Redbelly Toad AR LC C/S/L activities This species is harvested for the international pet trade in Argentina.. (But has no major threats) No Melanophryniscus tumifrons Swelling Redbelly Toad AR, BR LC C/S/L activities It is potentially threatened by the international pet trade. (Future threat)? Pedostibes hosii Common Tree Toad BN, ID, MY, TH LC C/S/L activities No HYLIDAE Hyla chinensis Common Chinese Treefrog CN, TW, VN LC C/S/L activities No Hylomantis medinai Rancho Grande Leaf Frog VE DD C/S/L activities It was overcollected in the Henri Pittier National Park up until the time it was last seen. It is not known if there are any threats to this species at present. No Phyllomedusa iheringii Southern Walking Leaf BR, UY LC C/S/L activities Possibly threatened by pet trade.? Review? No No No No 13

Taxon Common name Range States Frog IUCN Red List Category Reason for regional/international trade Phyllomedusa sauvagii Painted-belly Leaf Frog AR, BO, BR, PY LC C/S/L activities HYPEROLIIDAE Heterixalus rutenbergi Rutenberg s Reed Frog MG NT C/S/L activities LEPTODACTYLIDAE Ceratophrys aurita Brazilian Horned Frog BR LC C/S/L activities Ceratophrys calcarata Venezuelan Horned Frog CO, VE LC C/S/L activities BO, BR, CO, EC, GF, GY, Ceratophrys cornuta Amazonian Horned Frog PE, SR, VE LC C/S/L activities Ceratophrys cranwelli Chacoan Horned Frog AR, BO, BR, PY LC C/S/L activities GAA information on utilisation (comments on trade as a threat) (ongoing threat) Review? It is threatened by the international pet trade. (ongoing threat) SRG 42 It is found in international trade, with hundreds being exported annually, although it is not clear that this constitutes a threat to the species. (ongoing threat) SRG 42 The major threats are probably related to habitat loss due to agriculture, clear-cutting and human settlement, as well as harvesting for the national and international pet trade, which might be locally unsustainable. (Ongoing threat)? The national and international pet trade might have a local impact No The species could be of interest to the pet trade, which might affect some populations. No It is collected for the international pet trade. Eggs are sold internationally for scientific research.? Ceratophrys joazeirensis Caatinga Horned Frog BR DD C/S/L activities It is possibly in the national and international pet trade. No Ceratophrys ornata Ornate Horned Frog AR, BR, PY, UY NT C/S/L activities It is collected for the international pet trade and its eggs are sold internationally for scientific research.? Chacophrys pierottii Chaco Horned Frog AR, BO, PY LC C/S/L activities It is collected for the international pet trade, and subject to heavy collecting during the breeding season. (Ongoing threat) SRG 42 Leptodactylus laticeps Santa Fe Frog AR, BO, PY NT C/S/L activities Over-harvesting for the international pet trade is a major threat. It is collected in Paraguay and Argentina, and each adult is worth $300-$600. It was a rare species by 2003 in Argentina due to overharvesting for the international pet trade. (Ongoing threat). SRG 42 MEGOPHRYIDAE Megophrys nasuta Bornean Horned Frog, Horned Toad, Large Horned Frog, Malayan BN, ID, MY, SG LC C/S/L activities The species is harvested for the national and international pet trade, which might affect local populations. (Ongoing threat)? 14

Taxon Common name Range States Horned Frog IUCN Red List Category Reason for regional/international trade GAA information on utilisation (comments on trade as a threat) Review? PIPIDAE Pipa snethlageae Utinga Surinam Toad BR, CO, PE LC C/S/L activities RANIDAE Discodeles guppyi Fejervarya cancrivora Limnonectes blythii Shortland Island Webbed Frog PG, SB LC C/S/L activities Asian Brackish Frog, Crab- Eating Frog, Mangrove CN, IN, ID, MY, PH, SG, Frog, Rice Field Frog LK, TH, VN LC Food Blyth's River Frog, Giant Asian River Frog, Giant Frog ID, LA, MY, MM, SG, TH, VN NT Food Limnonectes grunniens Amboina Wart Frog ID, PG LC Food Limnonectes magnus Limnonectes malesianus Giant Philippine Frog, Large Swamp Frog, Mindanao Fanged Frog PH NT Food Malesian Frog, Peat Swamp Frog ID, MY, SG, TH NT Food Limnonectes shompenorum Shompen Frog ID, IN LC Food Paa bourreti (Syn. Nanorana bourreti) Bourret s Frog VN DD Food CN, KZ, KP, KR, KG, MN, Rana amurensis Siberian Wood Frog RU LC Medicine Forest destruction and international trade are both threats to this species. (Present and future threat).? Collection for food and for export to the pet markets in Europe and elsewhere may be impacting some populations. (Ongoing threat)? Over harvesting is a potential threat to this species. (Ongoing threat; used for food)? The major threat to this species is intensive collection for consumption at subsistence levels, and for local, national and international trade. (Ongoing threat)? The main threat is exploitation for human food, since the animals on Sulawesi, which represent an undescribed species, are very large. It is also eaten in New Guinea. (Only subsistence level at present, International trade future threat). No On Sulawesi, the major threat to the populations of this species complex is human exploitation for both local consumption and international trade. In the Philippines, threats include harvesting for human subsistence and for international export. (Present and future threat; used for food).? It is collected for subsistence consumption and trade but most collection pressure is deflected from it by the sympatric occurrence of the larger and more common Limnonectes blythii. No Animals are harvested for food and traded within Indonesia and are probably exported to Singapore. No Most of the species in the genus Paa are consumed locally to a varying degree within their range. No There is significant over harvesting of this species for food, especially in Russia where illegal collection has increased No 15

Rana chensinensis Taxon Common name Range States IUCN Red List Category Reason for regional/international trade Asiatic Grass Frog, Chinese Brown Frog CN, MN LC Food, Medicine Rana dybowskii Dybowski s Frog CN, JP, KP, KR, MN, RU LC Food, Medicine AT, BA, BE, BG, BY, CZ, DE, DK, EE, ES, FR, GB, HR, HU, IT, LV, LI, LT, LU, Rana esculenta MD, NL, PL, RO, RS, RU, (Syn. Pelophylax ridibundus) Edible Frog SK, SI, SE, CH, UA, GB LC Food Rana huanrenensis Huanren Frog CN, KP LC Food, Medicine Rana kurtmuelleri Balkan Water Frog AL, GR, MK, RS LC Food RHACOPHORIDAE Theloderma corticale Tonkin Bug-eyed Frog VN DD C/S/L activities CAUDATA HYNOBIIDAE GAA information on utilisation (comments on trade as a threat) Review? since the 1990s. (Subsistence and National levels) In northeastern China, the main threat is over-exploitation for food and traditional Chinese medicine. (Ongoing threat)? In the 1990s, mass collecting of R. dybowskii, mainly in the Primorye Region of Russia, for the trade in traditional Asian medicine led to population declines at a number of sites. (Past threat) No The frog-leg trade and high levels of pollution are leading to significant declines in populations of the former Yugoslavia. No This species is used for food and in traditional Chinese medicine. Ongoing threat. No In northern parts of its native range (e.g., Lake Skadar) it is significantly threatened by over collection for commercial purposes. (Ongoing threat)? This is one of the few regional frog species for which there is a specific demand in the global pet trade. (Future threat)? Hynobius nebulosus Clouded Salamander JP LC C/S/L activities It is collected for the pet trade.? PLETHODONTIDAE Bolitoglossa dofleini SALAMANDRIDAE Doflein s Mushroomtongue Salamander BZ, GT, HN NT C/S/L activities This species is potentially threatened by the international pet trade, in which it features significantly, and since this species takes 10-12 years to mature such trade could easily be locally unsustainable. SRG 42 Cynops cyanurus Chuxiong Fire-Bellied CN LC C/S/L activities Small numbers have been seen in the international pet No 16

Taxon Common name Range States Newt IUCN Red List Category Reason for regional/international trade Cynops orientalis Oriental Fire-Bellied Newt CN LC C/S/L activities Notophthalmus perstriatus Striped Newt US NT C/S/L activities Pachytriton brevipes Black-spotted Stout Newt CN LC C/S/L activities Pachytriton labiatus Spotless Stout Newt CN LC C/S/L activities Paramesotriton hongkongensis Hong Kong Warty Newt CN NT C/S/L activities Paramesotriton laoensis LA DD C/S/L activities AL, AD, AT, BE, BA, BG, HR, CZ, FR, DE, GR, HU, IT, LI, LU, ME, MK, NL, PL, Common Fire Salamander, PT, RO, RS, SK, SI, SM, ES, Salamandra salamandra Fire Salamander CH, TR(?), UA LC C/S/L activities Triturus alpestris (Syn. Mesotriton alpestris) Triturus cristatus Triturus karelinii Alpine Newt Great Crested Newt, Northern Crested Newt, Warty Newt Southern Crested Newt AL, AT, BY, BE, BA, BG, HR, CZ, DE, DK, FR, GB, GR, HU, IT, LI, LU, ME, MK, NL, PL, RO, RS, SK, SI, ES, CH, UA LC C/S/L activities AT, BY, BE, CH, CZ, DE, DK, EE, FI, FR, GB, LV, LI, LT, LU, MD, NL, NO, PL, RO, RS, RU, SK, SE, UA LC C/S/L activities AL, AZ, BG, GE, GR, IR, MK, RS, RU, UA, TR LC C/S/L activities Triturus marmoratus Marbled Newt ES, FR, PT LC C/S/L activities GAA information on utilisation (comments on trade as a threat) trade in recent years. Review? It is being traded in the domestic and international pet markets. (Ongoing threat)? Many potential threats, including collection for the pet trade. (Ongoing threat)? It is exported for the international pet trade. (Ongoing threat)? Over-exploitation for use as traditional Chinese medicine (subsistence level) and for the international pet trade is a major threat to this species. (Ongoing threat) SRG 42 A particular threat to this species is the collection of significant numbers for the pet trade. SRG 42 It is harvested for medicine and food locally. It will potentially be harvested as a pet in the future. No The principal threats include collection for commercial purposes (i.e., the pet trade).; (Ongoing threat)? In some areas there is over collection of the species for use in education and science (this has led to the extinction of the species from some Ukrainian localities). It is also collected in small numbers for the commercial pet trade (especially T. a. inexpectatus of Calabria).? In some parts of the range (of the former Soviet Union) there is substantial commercial collecting of this species for the pet trade. (Ongoing threat)? In the former Soviet Union there is significant commercial collecting of this species for the pet trade. (Ongoing threat)? There is some illegal collection of the species for the pet trade. No Triturus vittatus Banded Newt GE, IQ, IL, LB, RU, SY, TR, LC C/S/L activities In the Caucasus and Israel it is threatened by collection for? 17

Taxon Common name Range States AM, JO IUCN Red List Category Reason for regional/international trade Tylototriton shanjing CN NT C/S/L activities Tylototriton taliangensis Taliang Knobby Newt CN NT C/S/L activities Tylototriton verrucosus Himalayan Salamander, Red Knobby Newt BT, CN, IN, MM, NP, TH, VN LC Medicine, C/S/L activities GAA information on utilisation (comments on trade as a threat) Review? the pet trade. (Ongoing threat) The major threat to this species is over-collecting for Traditional Chinese Medicine. Small numbers are also exported for the international pet trade No A major threat to this species is over-collection for Traditional Chinese Medicine as a substitute for the Sichuan salamander (Batrachuperus pinchonii). Small numbers are also exported to supply the international pet trade. No It is in demand in the domestic and international pet trade. It is also harvested for use as a traditional medicine in India. (Ongoing threat)? 18

1.5. REFERENCES AmphibiaWeb. 2006. Information on amphibian biology and conservation. Berkeley, California. URL: www.amphibiaweb.org Accessed September 2007. Andreone, F., Mercurio, V. & Mattioli, F. 2006. Between environmental degradation and international pet trade: conservation strategies for the threatened amphibians of Madagascar. Natura Soc. it. Sci. nat. Museo civ. Stor. nat. Milano 95 (2): 81-96. Baillie, J.E.M., Hilton-Taylor, C. & Stuart, S.N. 2004. 2004 IUCN Red List of Threatened Species: A Global Species Assessment. IUCN, Gland, Switzerland and Cambridge, UK. Beebee, T.J.C. & Griffiths, R.A. 2005. The amphibian decline crisis: A watershed for conservation biology? Biological Conservation 125: 271-285. Busack, S.D. 1974. Amphibians and reptiles imported into the United States. US Fish and Wildlife Service. Carpenter, A.I., Dublin, H., Lau, M., Syed, G., McKay, J.E., & Moore, R.D. 2007. Overharvesting. In: Gascon, C., Collins, J.P., Moore, R.D., Church, D.R., McKay, J.E. and Mendelson III, J.R. (Eds) 2007. Amphibian Conservation Action Plan. IUCN/SSC Amphibian Specialist Group. Gland, Switzerland and Cambridge, UK. 64 pp. Fisher, M.C. & Garner, T.W.J. 2007. The relationship between the emergence of Batrachochytrium dendrobatidis, the international trade in amphibians and introduced amphibian species. Fungal Biology Reviews 21: 2-9. Frost, D.R. 2004. Taxonomic Checklist of CITES listed amphibians. The American Museum of Natural History. Gascon, C., Collins, J.P., Moore, R.D., Church, D.R., McKay, J.E. & Mendelson III, J.R. 2007. Amphibian Conservation Action Plan. IUCN/SSC Amphibian Specialist Group. Gland, Switzerland and Cambridge, UK. 64 pp. Gibbons, J. W., Scott, D. E., Ryan, T. J., Buhlmann, K. A., Tuberville, T. D., Metts, B. S., Greene, J. L., Mills, T., Leiden, Y., Poppy, S. & C. T. Winne. 2000. The Global Decline of Reptiles, Déjà Vu Amphibians. BioScience 50 (8): 653-666. Gorzula, S. 1996. The trade in dendrobatid frogs from 1987 to 1993. Herpetological Review 27 (3). IUCN. 2007. 2007 IUCN Red List of Threatened Species. URL: www.iucnredlist.org Accessed September 2007. IUCN, Conservation International, and NatureServe. 2007. Global Amphibian Assessment. URL: www.globalamphibians.org Accessed September 2007. Pough, F.H., Andrews, R.M., Cadle, J.E., Crump, M.L., Savitzky, A.H. & Wells, K.D. 1998. Herpetology. Prentice-Hall, Englewood Cliffs, NJ. Schlaepfer, M.A., Hoover, C. & Dodd Jr. K.D. 2005. Challenges in evaluating the impact of the trade in amphibians and reptiles on wild populations. Bioscience 55 (3): 256-264. Silvano, D.L. & Segalla, M.V. 2005. Conservation of Brazilian Amphibians. Conservation Biology 19 (3): 653-658. Tyler, M.J., Wassersug, R. & Smith, B. 2007. How frogs and humans interact: Influences beyond habitat destruction, epidemics and global warming. Applied Herpetology 4: 1-18. Ye, C. Fei, L. & Hu, S. 1993. Rare and economic amphibians of China. Sichuan Publishing House of Science and Technology, Chengdu. (in Chinese). Young, B.E., Lips, K.R., Reaser, J.K., Ibáñez, A.W., Salas, J. Rogelio Cedeño, J., Coloma, L.A., Ron, S., La Marca, E., Meyer, J.R., Muñoz, A., Bolaños, F., Chaves, G. & Romos, D. 2001. Population declines and priorities for amphibian conservation in Latin America. Conservation Biology 15 (5): 1213-1223. Young, B.E., Stuart, S.N., Chanson, J.S., Cox, N.A. & Boucher, T.M. 2004. Disappearing jewels: the status of New World amphibians. NatureServe, Arlington, Virginia. 19

2. SPECIES REVIEWS 2.1. METHODOLOGY For this report, preliminary information on known trade from the Global Amphibian Assessment (IUCN et al, 2007) formed the basis of the species selection as described in section 1.4.1. An extensive literature review was subsequently undertaken for the selected species to identify information on status and trade and a web survey was also conducted. Since records of trade in non-cites species are often non-existent or very limited and patchy at best, assessing whether these species are traded internationally or not, and especially assessing the levels of trade, sources and countries involved, is not a straightforward process. In the absence of other data, surveys of trade conducted over the Internet can provide an important source of trade information. However, such surveys can usually only provide an indication of availability or demand rather than information on whether trade actually took place and if so in what volumes. For the purpose of this report, web surveys consisted of Google searches, using the species s scientific name. Use of common names was avoided, as they were ambiguous, i.e. several species called the same name, and different common names used for the same species, and as hobbyists and specialized shops often use scientific names. In addition to general web searches, and in order to focus more specifically on the pet trade in Europe, Google searches were performed limiting the search to pages from a selection of EU countries, namely France, Germany, Italy, Spain and the UK. If no or limited evidence of trade was found for those countries, additional searches were performed for the Czech Republic, the Netherlands, Poland, Portugal and Sweden. Also, several hobbyist websites were specifically searched. These included: - www.kingsnake.com (USA) - www.sandfiredragonranch.com (USA) - www.eurofauna.com (Europe) - www.caudata.org (International) - www.amphibian.co.uk (UK) - www.exotic-pets.co.uk (UK) - www.lafermetropicale.com (France) - www.terrariumonline.com (Spain) - http://e-commerce.ysi.net/eshop/reptilmaniacom/ (Spain) - www.salamanderland.at (Austria) - www.caudata.nl (Netherlands) - http://members.chello.nl/a.kente/ (Netherlands) - www.animalfarm.cz (Czech Republic) The trade in frog legs was evaluated primarily through literature review and general web searches, but no targeted web surveys were conducted because, unlike for the pet trade, scientific names are seldom used when referring to frog legs; they appear to be rarely referred to using more accurate terms than simply frog s legs. The criteria for listing in the annexes of Council Regulation 338/97are specified in Article 3 of the regulation as follows: 1. Annex A shall contain: (a) the species listed in Appendix I to the Convention for which the Member States have not entered a reservation; (b) any species: (i) which is, or may be, in demand for utilization in the Community or for international trade and which is either threatened with extinction or so rare that any level of trade would imperil the survival of the species; or 20

(ii) which is in a genus of which most of the species or which is a species of which most of the subspecies are listed in Annex A in accordance with the criteria in subparagraphs (a) or (b)(i) and whose listing in the Annex is essential for the effective protection of those taxa. 2. Annex B shall contain: (a) the species listed in Appendix II to the Convention, other than those listed in Annex A, for which the Member States have not entered a reservation; (b) the species listed in Appendix I to the Convention for which a reservation has been entered; (c) any other species not listed in Appendices I or II to the Convention: (i) which is subject to levels of international trade that might not be compatible: with its survival or with the survival of populations in certain countries, or with the maintenance of the total population at a level consistent with the role of the species in the ecosystems in which it occurs: or (ii) whose listing in the Annex for reasons of similarity in appearance to other species listed in Annex A or Annex B, is essential in order to ensure the effectiveness of controls on trade in specimens of such species; (d) species in relation to which it has been established that the introduction of live specimens into the natural habitat of the Community would constitute an ecological threat to wild species of fauna and flora indigenous to the Community. 3. Annex C shall contain: (a) the species listed in Appendix III to the Convention, other than those listed in Annexes A or B, for which the Member States have not entered a reservation; (b) the species listed in Appendix II to the Convention for which a reservation has been entered. 4. Annex D shall contain: (a) species not listed in Annexes A to C which are imported into the Community in such numbers as to warrant monitoring; (b) the species listed in Appendix III to the Convention for which a reservation has been entered. 5. Where the conservation status of species covered by this Regulation warrants their inclusion in one of the Appendices to the Convention, the Member States shall contribute to the necessary amendments. Furthermore, the following guidelines for Annex D were agreed at SRG 36 on 9 March 2006 as follows: A species may be included in Annex D where: a) there is evidence of demand for it in the EU market and b) it might be threatened by trade due its unfavourable or unknown conservation status, distributional, ecological or reproductive potential and c) reliable trade data is not available from any other source. 21

REVIEW OF NON-CITES AMPHIBIA SPECIES THAT ARE KNOWN OR LIKELY TO BE IN INTERNATIONAL TRADE AMPHIBIA: HYLIDAE SPECIES: Agalychnis annae SYNONYMS: COMMON NAMES: RANGE STATES: IUCN RED LIST: PREVIOUS EC OPINIONS: Blue-sided Leaf Frog (English) Costa Rica Endangered n/a TRADE PATTERNS: The species is found in the international pet trade (IUCN et al., 2007). Elizondo (2000) reported that individuals of this species are very sought-after for use as pets, and they are collected from the wild in order to be illegally sold, mainly in Europe and the US. No national trade statistics were identified for this species. The following information was derived from the web survey (as outlined in the section on methodology): The species was advertised for 125 on a French website (http://www.lafermetropicale.com/boutique/rechercheboutik.php) as sub-adult specimens born in captivity in 2005, although they were not in stock at the time when the website was visited. The following websites revealed that this species is sought by some hobbyists, although hobbyists comments indicated that it was not very widely available: http://talkto.thefrog.org/index.php?action=vthread&forum=13&topic=5228; http://www.canadart.org/phpbb2/viewtopic.php?t=1126; http://www.amphibianforum.com/viewtopic.php?p=295&sid=f7bebf4d93773acad13b69c 9e066f15f). A hobbyist on one forum commented they are fairly rare especially in Canada. I see them sell for $80 US/frog, but they are offered very rarely (http://www.canadart.org/phpbb2/viewtopic.php?p=7419&sid=d263ced9d2a3badd2512 6c6a04a20125). Another noted: I plan on getting some golden-eye tree frogs (Agalychnis annae) by this summer. As far as I know, no one in Canada has these frogs and I would really like to start breeding them to make them available in Canada. I'm looking for CB adults, if possible from several bloodlines, and I would like to get at least 8-10 individuals, possibly more depending on availability and pricing. If you will have some of these frogs available for sale by this summer and don't mind exporting to Canada, please contact me either by MP or by mail. (http://www.amphibianforum.com/viewtopic.php?p=295&sid=f7bebf4d93773acad13b6 9c9e066f15f) The German website http://exotic-world.de/froesche/agalychnis_annae.htm offered some captive care information for the species. 22

CONSERVATION STATUS in range states COSTA RICA: The species occurs in Costa Rica (Leenders, 2001), specifically the Caribbean slopes and Meseta Central of the country (Frost, 2007). The following information has been extracted from the Global Amphibian Assessment website (IUCN et al., 2007): Agalychnis annae occurs in the northern Cordillera de Talamanca, Cordillera de Tilarán and Cordillera Central, Costa Rica, at 780-1,650m. However, it has disappeared from most parts of its range, surviving mainly around San José only. Since the late 1980s, it has disappeared from pristine areas, including in protected areas such as Parque Nacional Tapantí and the Monteverde Cloud Forest Preserve, where it was once common. It remains common only in highly altered habitats in metropolitan San José. It remains the most abundant species in San José and suburbs near heavily polluted streams, especially in shade-grown coffee plantations and gardens. Despite the apparent adaptability of this species, it is nonetheless subject to unconfirmed factors that have caused amphibian faunas to decline in certain locations in Central America, in particular the fungal disease, chytridiomycosis. It is possible that this species survives only in polluted areas because the chytrid fungus is more susceptible to pollution than the frog. The few, known remaining populations of this species are threatened by an introduced fish (Xiphophorus hellerii) that preys on the tadpoles; it is also found in the international pet trade. Research is needed to determine whether or not this species can survive only in polluted areas, because of the ineffectiveness of the chytrid fungus in such environments. If this proves to be the case, then well-meaning conservation measures to abate water pollution could unintentionally lead to the extinction of this species. Given the nature of the threats, it may be worth considering the establishment of a captive-breeding programme for this species. Pounds et al. (2004) noted that the drastic population decline was estimated to be more than 50% since 1990, inferred from the apparent disappearance of much of the population. Regional/international trade is considered an ongoing major threat to this species (IUCN, 2007). A. annae was not found during amphibian surveys conducted during 1990-1994 and that covered three zones where the species was known to occur (Pounds et al., 1997). It was listed as a species with reduced populations in Costa Rica (MINAE, 2006). The species is protected in Costa Rica by the Ley de Conservación de la Vida Silvestre No. 7317, and by the Ley Orgánica del Ambiente No. 7554 and decree No. 26435-MINAE (Elizondo, 2000). REFERENCES Elizondo, L.H. 2000. Especies de Costa Rica: Agalychnis annae. INBio (Instituto Nacional de Biodiversidad). URL: http://darnis.inbio.ac.cr/ubis/fmpro?-db=ubipub.fp3&- lay=weball&-error=norec.html&-format=detail.html&-op=eq&id=4180&-find Accessed September 2007. Frost, D. 2007. Amphibian Species of the World 5.0. An online reference. American Museum of Natural History. URL: http://research.amnh.org/herpetology/amphibia/index.php Accessed October 2007. 23