Amphibian illegal trade in Brazil: what do we know?

Transcrição

1 South American Journal of Herpetology, 5(1), 2010, Brazilian Society of Herpetology Amphibian illegal trade in Brazil: what do we know? Juliana Pistoni 1 and Luís Felipe Toledo 2,3 1 Universidade Estadual Paulista Júlio de Mesquita Filho (UNESP), Instituto de Biociências, Rio Claro, São Paulo, Brasil, Caixa Postal 199, E mail: jpistoni@yahoo.com.br 2 Museu de Zoologia Prof. Adão José Cardoso, Instituto de Biologia, Universidade Estadual de Campinas (UNICAMP), Caixa Postal 6109, , Campinas, SP, Brasil. E mail: toledolf2@yahoo.com 3 Corresponding author: LFT: toledolf2@yahoo.com Abstract. Brazil is estimated to account for 10 to 15% of illegal animal trade in the world. Efforts to avoid illegal trade are being made by federal agencies, but at this time there is a lack of information about the status of illegal trade of Brazilian amphibians (like in many countries). Brazil is the richest country in the world in number of amphibian species, housing more than 860 species. Many of them are endemic, some endangered, and there are even several species yet to be described. Therefore, the impact of illegal trade in Brazil must be investigated carefully in order to support future conservation action plans. In the present study, we compiled the available information on this subject, based on interviews with a representative number of Brazilian herpetologists and on research in airports, zoos, police departments, and governmental and nongovernmental organizations. Between 1998 and August 2009, we gathered reports on the trade of 746 amphibian individuals of 19 anuran and one salamander species in Brazil. Among them, 12 were native and eight were alien species. We also found other Brazilian species (but not endemic to Brazil) that were being sold in websites in Europe and the United States. We were not able to associate the internet selling with illegal trade, but this suggests that it may be possible that uncontrolled trade of Brazilian fauna is taking place. The amphibian illegal and international trade is much less representative than the present estimates for other tetrapods (reptiles, birds, and/or mammals); however, amphibians need urgent conservation action plans. Ideally, a Brazilian governmental agency should centralize all these incidents, as this would help us to understand the real impact of amphibian illegal trade and develop effective action plans to reduce this type of trade. Keywords. illegal trade, traffic, frogs, amphibians, conservation. Introduction The first official record of illegal animal trade in the world comes from the Inca civilization, which traded caimans and anacondas in the Brazilian and Peruvian Amazon (Renctas, 2001). Nowadays, illegal animal trade is the third most prevalent illicit activity in the world, behind only the weapon and drug trade, moving 10 to 20 billion dollars each year (Renctas, 2001). Brazil accounts for about 10 to 15% of illegal animal trade in the world, representing 1 to 1.5 billion dollars moved per year (Renctas, 2001). The most frequently traded species are birds, followed by some primates (PEA, 2008). On the other hand, amphibians are rarely cited in reports of illegal trade. Article 225, 1 st paragraph, of the Brazilian Federal Constitution states that it is a role of the Government to preserve and restore the essential ecological processes and provide for the ecological management of species and ecosystems, and to preserve the diversity and integrity of Brazil s genetic legacy (Brasil, 1988). The supervision of illegal wildlife trade in Brazil is done by governmental agencies, like Federal Police Departments, Customs, ICMBio (Instituto Chico Mendes de Conservação da Biodiversidade, the agency responsible for the conservation of biodiversity), and IBAMA (Instituto Brasileiro do Meio Ambiente e dos Recursos Renováveis, the federal environmental agency). There are also non-governmental organizations which help to supervise illegal wildlife trade, such as Renctas (Rede Nacional de Combate ao Tráfico de Animais Silvestres). However, despite the several actions and organizations involved, about 38 million animals depart illegally from Brazil every year (Renctas, 2001). At present, more than 6400 amphibian species have been described in the world (Frost, 2009), and the highest species diversity occurs in the Tropical region (GAA, 2007). Brazil is the richest country in number of amphibian species, housing more than 860 described species (SBH, 2009). According to the Brazilian list of endangered species (Machado et al., 2005), one amphibian species is considered extinct (Phrynomedusa fimbriata), 16 species are threatened and another 90 are classified as data-deficient (DD; Machado et al., 2005). Thus, there is no basic information available to assess the conservation status of about 10% of Brazilian amphibian diversity. Furthermore, there is a general lack of information even for most of those species which are neither threatened nor DD. Only a few species have been studied after their taxonomic description. These facts, combined with the recent global amphibian crisis (Stuart et al., 2004; Schlaepfer et al. 2005; Blaustein and Bancroft 2007; McCallum, 2007), makes it urgent to develop conservation action plans in Brazil.

2 52 Amphibian illegal trade in Brazil In the present study we compiled the available information and evaluated the current scenario of illegal amphibian trade in Brazil. Material and Methods We conducted interviews, mostly by phone and , with a representative number of Brazilian herpetologists and with authorities in airports, zoos, police departments, and governmental and non-governmental agencies, between July 2007 and August We also conducted an internet search for Brazilian species that are being sold outside the country. Results We asked information on amphibian illegal trade from a total of 15 airports from nine Brazilian states, six environmental agencies (IBAMA and ICMBio: Coordenação Geral de Fiscalização, Centro de Conservação e Manejo de Répteis e Anfíbios; IBAMA, Superintendência do Amazonas, Superintendência de São Paulo, and Superintendência do Rio de Janeiro), five Police Departments (Polícia Federal Rodoviária, Brasília, DF; Polícia Federal, Setor de crimes ambientais, Brasília, DF; Polícia Federal, Departamento de Recursos Materiais e Patrimônio, Brasília, DF; Polícia Federal, Belém, PA; Polícia Federal, São Paulo, SP), 11 zoos and similar institutions from five states, and 14 researchers from 13 institutions located in six states. From these sources, we gathered information on 746 individual amphibians belonging to 19 species of anurans and one species of salamander, which were illegally traded in Brazil (Table 1). Of these species, eight are not native to Brazil. The remaining 12 species are native and were probably captured inside the country. The seizures were recorded between 1998 and 2009, and no temporal pattern in trade (increasing, decreasing, or stable) was evident (Figure 1). On the internet, we found 13 species that occur in Brazil being sold in 11 sites from Europe and the United States (Table 2). Of the species listed in table 2, five are also listed in table 1: Rhinella marina, Ceratophrys cornuta, C. cranwelli, C. ornata, and Dendrobates tinctorius. Regarding transport methods, we were able to obtain information from only one of the apprehensions. The 560 dendrobatid frogs (279 Adelphobates cf. galactonotus and 281 Dendrobates tinctorius) apprehended at the Guarulhos International Airport in 1999 were each inside a 35 mm film canister, and canisters were inside two suitcases (M. Martins, pers. comm.). The illegally acquired amphibians were redirected to three destinations after their apprehension: they were either sent to zoos, delivered to researchers in public institutions, or sent to Zoology museums. The dendrobatids cited in the last paragraph were sent to the Zoológico de São Paulo (São Paulo, SP), the Zoo Sorocaba (Sorocaba, SP), and the Zooparque Itatiba (Itatiba, SP), and to researchers working at Universidade de Brasília (Brasília, DF), Universidade Estadual Paulista (Rio Claro, SP), Universidade de São Figure 1. Number of individuals (white bars; right axis) and species (black bars; left axis) that have been seized during illegal trade in Brazil over 12 years. An asterisk indicates that the value is higher than the right axis; the actual value of this column is 560 (individuals), and the column was cut to make the visualization of the other columns possible.

3 Pistoni, J. and Toledo, L. F. 53 Table 1. Amphibians that have been apprehended during illegal trade in Brazil. An asterisk indicates species that are not native to Brazil. The empty cells indicate that no information was available. Species (number of individuals) Informed origin Apprehension site in Brazil Incident date Planned destination CAUDATA Salamandridae Cynops orientalis (1)* Viracopos Int. Airport, Campinas, SP 04/23/2004 Florida, USA ANURA Bombinatoridae Bombina bombina (4)* 05/08/1998 Bombina orientalis (3)* 07/16/1998 Bombina variegata (5)* 05/08/1998 Bufonidae Bufo sp. (1) 12/05/2007 Rhinella marina (8) Belém, PA Belém, PA 10/2007 Belém, PA 9.00 Pseudepidalea viridis (2)* 05/08/1998 Ceratophryidae Ceratophrys cornuta (1) 07/16/1998 Ceratophrys cranwelli (2) Viracopos Int. Airport, Campinas, SP 04/23/2004 Florida, USA Ceratophrys cranwelli (4) Argentina Sorocaba, SP 08/11/2009 State of São Paulo, Brazil Ceratophrys ornata (1) 12/07/2005 Ceratophrys joazeirensis (130) Joazeiro, BA Guerém, Valença, BA 2002 Dendrobatidae Adelphobates cf. galactonotus (279) Alto Trombetas, PA Guarulhos International Airport 1999 Germany Dendrobates tinctorius (281) Alto Trombetas, PA Guarulhos International Airport 1999 Germany Hylidae Hypsiboas albomarginatus (1) São Paulo, SP São Paulo, SP 2005 Phyllomedusa sauvagii (1) 07/16/1998 Litoria sp. (1)* 1998 Litoria caerulea (2)* Viracopos Int. Airport, Campinas, SP 04/23/2004 Florida, USA Trachycephalus imitatrix (1) São Paulo, SP São Paulo, SP 2005 Leptodactylidae Leptodactylus sp. (1) 12/05/2007 Pipidae Xenopus laevis (15)* 05/08/1998 Xenopus laevis (2)* 12/19/2000 Price (USD) Paulo (São Paulo, SP), the Museu de História Natural Capão da Imbuia (Curitiba, PR), and the Museu de Zoologia da Universidade de São Paulo (São Paulo, SP; M. Martins, pers. comm.). Some of these institutions (e.g., Zoológico de São Paulo and Zooparque Itatiba) still have descendants of the apprehended frogs. Discussion Although we found that 13 species that occur in Brazil were being sold on the internet, all these species also occur in Brazil s neighboring countries (Frost, 2009), especially Suriname, which was considered the most important source of wild-caught dendrobatids (see Gorzula, 1996). Therefore, we cannot assign these records to amphibian illegal trade; however, this indicates that the species that occur in Brazil do interest herp breeders (at least) in the Northern Hemisphere, what may stimulate illegal trade in Brazil. Among the species indicated herein as targets of illegal trade, only Dendrobatidae species are featured in Appendix II of CITES (cited therein as Dendrobates spp.). These frogs seem to be the most prevalent illegally traded amphibians (see Gorzula 1996). Interestingly, what should repel their natural predators is precisely what attracts human captive breeders: their aposematic coloration (see another example in La Marca et al., 2005). These frogs can also be linked to the pharmacological industry, which benefits from

4 54 Amphibian illegal trade in Brazil Table 2. Amphibian species that occur in Brazil and that were being sold in other countries via the internet in Prices varied in the same seller due to the color and size of the animal. Species Price Seller location Bufonidae Rhinella marina 7.5 USD Florida, USA Rhinella marina 24 Euros Barcelona, Spain Ceratophryidae Ceratophrys cornuta USD California, USA Ceratophrys cornuta 79 Euros Paris, France Ceratophrys cornuta Pounds Chesterfield, England Ceratophrys cranwelli USD Florida, USA Ceratophrys cranwelli 18 USD California, USA Ceratophrys cranwelli 34 Euros Paris, France Ceratophrys cranwelli (albino) 45 Euros Paris, France Ceratophrys cranwelli Pounds Loughton, England Ceratophrys cranwelli Pounds Chesterfield, England Ceratophrys ornatus California, USA Ceratophrys ornatus 45 Euros Paris, France Ceratophrys ornatus 23.5 Pounds Loughton, England Ceratophrys ornatus Pounds Chesterfield, England Dendrobatidae Adelphobates galactonotus USD Maryland, USA Ameerega trivittata 79 USD Florida, USA Ameerega trivittata (red) 119 Euros Paris, France Ameerega trivittata (green) 99 Euros Paris, France Dendrobates leucomelas USD California, USA Dendrobates leucomelas USD Florida, USA Dendrobates leucomelas 59 Euros Paris, France Dendrobates leucomelas (green) 99 Euros Paris, France Dendrobates leucomelas Pounds Loughton, England Dendrobates tinctorius (yellow) 65 USD California, USA Dendrobates tinctorius (blue as D. azureus) USD California, USA Dendrobates tinctorius (blue) 120 Pounds Loughton, England Hylidae Phyllomedusa hypochondrialis USD California, USA Phyllomedusa sauvagii Pounds Lancashire, England Phyllomedusa tomopterna USD California, USA Trachycephalus resinifictrix USD California, USA Trachycephalus resinifictrix USD Florida, USA Pipidae Pipa pipa 39.5 Pounds Loughton, England Pipa pipa 65 USD California, USA Pipa pipa USD Florida, USA Pipa pipa 89 Euros Paris, France the presence of alkaloids in their skin secretions (e.g., review in Daly, 1998). The records of alien species do not indicate that Brazil is a destination in the international trade routes. The alien amphibians Xenopus laevis, Bombina spp., and Cynops orientalis are commonly bred in Brazil for scientific purposes (in the case of Xenopus laevis) or as pets (in all cases). So they could have been born in captivity in Brazil and not in their original countries. However, the frogs Litoria caerulea, and Pseudepidalea viridis probably came from their original regions (Australia and Europe, respectively). The income of exotic animals (via legal or illegal trade) in any country is a matter of concern because they can host emergent infectious diseases such as chytridiomycosis (Daszak et al., 2006; Rowley et al., 2007), for which Xenopus laevis is one of the most probable primary carriers among continents (Weldon et al.,

5 Pistoni, J. and Toledo, L. F ), and ranaviral agent FV3 (Daszak et al., 2006), which can cause malformations in wild populations (Burton et al., 2008). Indeed, chytridiomycosis has already been detected in Brazil (Toledo et al., 2006), although its origin has not yet been completely clarified (see Schloegel et al., 2009). The number of apprehended amphibians is many times smaller than that of other vertebrates. For example, in IBAMA s (2005) apprehension report, from almost 50,000 animals that were apprehended in Brazil, only two (< 0.01%) were amphibians. This number is probably underestimated. This is the first published article addressing amphibian illegal trade in Brazil, and our greatest difficulty during the survey was to collect the data. We know that a great amount of information is lacking and many other apprehensions may have been made in Brazil, but this information is not organized. Ideally, one of the Brazilian governmental agencies should centralize all these incidents and, as indicated before (Schlaepfer et al., 2005), include as much biological data in the reports as possible (e.g., place of origin/capture of the animals, field collecting data, correct identification of the species, etc.). This would help us to understand the real impact of amphibian illegal trade and develop effective action plans to reduce this type of trade. Resumo O Brasil é responsável por cerca de 10 a 15% do tráfico ilegal de animais do mundo. Ademais, por ser o país mais rico em espécies de anfíbios do mundo, abrigando mais de 860 espécies descritas e muitas sem informação nenhuma quanto ao grau de ameaça, surge uma preocupação com relação ao impacto do tráfico sobre nossa biodiversidade. Sendo assim, este trabalho compilou os dados disponíveis sobre o assunto para avaliar o cenário atual do tráfico no Brasil. Para tanto, foram realizadas entrevistas em aeroportos, zoológicos, departamentos de polícia, organizações governamentais e não governamentais e com pesquisadores que trabalham com anfíbios no Brasil. Entre 1998 e agosto de 2009 foram registrados 746 indivíduos apreendidos de 20 espécies de anfíbios, alvo de tráfico ilegal no Brasil, sendo que 12 são espécies nativas e oito exóticas. Por outro lado, através de pesquisa na internet, registramos diversas outras espécies que ocorrem no Brasil sendo comercializadas em países da Europa, e nos Estados Unidos. Não relacionamos estas vendas ao tráfico diretamente, mas é uma indicação de que algumas espécies podem estar passando por nossas fronteiras sem a devida fiscalização. Baseado em nossos dados, a parcela que os anfíbios representam dentro do tráfico de animais, principalmente quando considerados os demais grupos de tetrápodes (répteis, aves e mamíferos), é muito pequena. Este resultado pode estar mascarado pela ausência de informação disponível. Sendo assim, indicamos a necessidade de centralização desses dados por parte de órgãos governamentais competentes, o que nos auxiliará no entendimento do real impacto do tráfico ilegal sobre os anfíbios e é fundamental para que se criem e efetuem os planos de ação eficazes de combate ao tráfico. Acknowledgments We are grateful to Marcio Martins for reviewing the manuscript. Álvaro Victor S. Nascimento (PF), Ana Prudente (Museu Paraense Emilio Goeldi), Anderson Luis Valle (CGFis), Arif Cais (UNESP), Ariovaldo Giaretta (UFU), Camila Vianello Bastazini (IBAMA), Carla Pavan Manzato (Zoológico de Sorocaba), Carlos A. G. S. Jared (Instituto Butantan), Carlos Frederico da Rocha (UERJ), Célio F. B. Haddad (UNESP), Dener Riovanini (Renctas), Denise Rossa-Feres (UNESP), Elbano Paschoal Moraes (GAMBA), Flora Juncá (UEFS), Isaias José Reis (ICMBio), Ivan Sazima (UNICAMP), Jaime Bertoluci (ESALQ), José Bilac Saldanha (Aeroporto Viracopos), José P. Pombal Jr. (Museu Nacional), Luiz Antônio Gonçalves de Lima (IBAMA SP), Luiz Melo Lula (Zôo SP), Marcelo Napoli (UFBA), Marcio Martins (USP), Moisés Barbosa (UFA), Paula Eterovick (PUCMG), Paulo Bernarde (UFAC), Paulo Ricardo Campani (Aeroporto do Rio de Janeiro), Roberto Cabral Borges (CGFis), Sávio Stefanini Sant Anna (Insitituto Butantan), Sayuri Fitorra (IBAMA), Ulisses Caramaschi (Museu Nacional), Vinicius Ferreira (Zôo RJ), and Wellington Coelho (UEM) for granting interviews and providing unpublished information. LFT thanks FAPESP for grants (2008/ ) and a JP scholarship (2008/ ). Literature Cited Blaustein, A. R. and B. A. Bancroft Amphibian Population Declines: Evolutionary Considerations. 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