MS-140 - pistoni, toledo.indd

South American Journal of Herpetology, 5(1), 2010, 51-56
© 2010 Brazilian Society of Herpetology
Amphibian illegal trade in Brazil: what do we know?
Juliana Pistoni1 and Luís Felipe Toledo2,3
Universidade Estadual Paulista “Júlio de Mesquita Filho” (UNESP), Instituto de Biociências, Rio
Claro, São Paulo, Brasil, Caixa Postal 199, 13506‑900. E‑mail: [email protected]
2 Museu de Zoologia “Prof. Adão José Cardoso”, Instituto de Biologia, Universidade Estadual de Campinas
(UNICAMP), Caixa Postal 6109, 13083‑970, Campinas, SP, Brasil. E‑mail: [email protected]
3 Corresponding author: LFT: [email protected]
1
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, 1st 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.
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
e-mail, 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
2009. 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.
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)
CAUDATA
Salamandridae
Cynops orientalis (1)*
ANURA
Bombinatoridae
Bombina bombina (4)*
Bombina orientalis (3)*
Bombina variegata (5)*
Bufonidae
“Bufo” sp. (1)
Rhinella marina (8)
Pseudepidalea viridis (2)*
Ceratophryidae
Ceratophrys cornuta (1)
Ceratophrys cranwelli (2)
Ceratophrys cranwelli (4)
Ceratophrys ornata (1)
Ceratophrys joazeirensis (130)
Dendrobatidae
Adelphobates cf. galactonotus (279)
Dendrobates tinctorius (281)
Hylidae
Hypsiboas albomarginatus (1)
Phyllomedusa sauvagii (1)
Litoria sp. (1)*
Litoria caerulea (2)*
Trachycephalus imitatrix (1)
Leptodactylidae
Leptodactylus sp. (1)
Pipidae
Xenopus laevis (15)*
Xenopus laevis (2)*
Informed origin
Apprehension site in Brazil
Viracopos Int. Airport, Campinas, SP
Incident date
Planned
destination
Price
(USD)
04/23/2004 Florida, USA
05/08/1998
07/16/1998
05/08/1998
12/05/2007
10/2007
Belém, PA
05/08/1998
Belém, PA
Belém, PA
Argentina
Viracopos Int. Airport, Campinas, SP
Sorocaba, SP
Joazeiro, BA
Guerém, Valença, BA
Alto Trombetas, PA Guarulhos International Airport
Alto Trombetas, PA Guarulhos International Airport
São Paulo, SP
São Paulo, SP
São Paulo, SP
Viracopos Int. Airport, Campinas, SP
São Paulo, SP
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
9.00
07/16/1998
04/23/2004 Florida, USA
08/11/2009 State of São
Paulo, Brazil
12/07/2005
2002
1999
1999
Germany
Germany
2005
07/16/1998
1998
04/23/2004 Florida, USA
2005
12/05/2007
05/08/1998
12/19/2000
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 Dendro‑
bates 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
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 2007. Prices varied in the
same seller due to the color and size of the animal.
Species
Bufonidae
Rhinella marina
Rhinella marina
Ceratophryidae
Ceratophrys cornuta
Ceratophrys cornuta
Ceratophrys cornuta
Ceratophrys cranwelli
Ceratophrys cranwelli
Ceratophrys cranwelli
Ceratophrys cranwelli (albino)
Ceratophrys cranwelli
Ceratophrys cranwelli
Ceratophrys ornatus
Ceratophrys ornatus
Ceratophrys ornatus
Ceratophrys ornatus
Dendrobatidae
Adelphobates galactonotus
Ameerega trivittata
Ameerega trivittata (red)
Ameerega trivittata (green)
Dendrobates leucomelas
Dendrobates leucomelas
Dendrobates leucomelas
Dendrobates leucomelas (green)
Dendrobates leucomelas
Dendrobates tinctorius (yellow)
Dendrobates tinctorius (blue – as D. azureus)
Dendrobates tinctorius (blue)
Hylidae
Phyllomedusa hypochondrialis
Phyllomedusa sauvagii
Phyllomedusa tomopterna
Trachycephalus resinifictrix
Trachycephalus resinifictrix
Pipidae
Pipa pipa
Pipa pipa
Pipa pipa
Pipa pipa
Price
Seller location
7.5 USD
24 Euros
Florida, USA
Barcelona, Spain
35‑40 USD
79 Euros
57.27 Pounds
10‑12.5 USD
18 USD
34 Euros
45 Euros
22.5‑35.95 Pounds
35.69 Pounds
12.99‑29.99
45 Euros
23.5 Pounds
38.15 Pounds
California, USA
Paris, France
Chesterfield, England
Florida, USA
California, USA
Paris, France
Paris, France
Loughton, England
Chesterfield, England
California, USA
Paris, France
Loughton, England
Chesterfield, England
50‑80 USD
79 USD
119 Euros
99 Euros
45‑60 USD
59.99 USD
59 Euros
99 Euros
95.95 Pounds
65 USD
55‑90 USD
120 Pounds
Maryland, USA
Florida, USA
Paris, France
Paris, France
California, USA
Florida, USA
Paris, France
Paris, France
Loughton, England
California, USA
California, USA
Loughton, England
29.99 USD
99.99 Pounds
54.99 USD
39.99 USD
38.99 USD
California, USA
Lancashire, England
California, USA
California, USA
Florida, USA
39.5 Pounds
65 USD
49.99 USD
89 Euros
Loughton, England
California, USA
Florida, USA
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 lae‑
vis) 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.,
Pistoni, J. and Toledo, L. F.
2004), 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
55
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
(2008/50325‑5) and a JP scholarship (2008/ 52847‑9).
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Submitted 25 June 2009
Accepted 05 March 2010