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UNIVERSIDADE FEDERAL DE GOIÁS INSTITUTO DE CIÊNCIAS BIOLÓGICAS PROGRAMA DE PÓS-GRADUAÇÃO EM ECOLOGIA E EVOLUÇÃO Tráfico de Animais Silvestres: Da captura ao retorno à natureza GUILHERME FERNANDO GOMES DESTRO DEZEMBRO – 2018 GOIÂNIA – GO
Transcript of Tráfico de Animais Silvestres: Da captura ao retorno à natureza › weby › up › 102 › o ›...
UNIVERSIDADE FEDERAL DE GOIÁSINSTITUTO DE CIÊNCIAS BIOLÓGICAS
PROGRAMA DE PÓS-GRADUAÇÃO EM ECOLOGIA E EVOLUÇÃO
Tráfico de Animais Silvestres:Da captura ao retorno à natureza
GUILHERME FERNANDO GOMES DESTRO
DEZEMBRO – 2018
GOIÂNIA – GO
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UNIVERSIDADE FEDERAL DE GOIÁSINSTITUTO DE CIÊNCIAS BIOLÓGICAS
PROGRAMA DE PÓS-GRADUAÇÃO EM ECOLOGIA E EVOLUÇÃO
Guilherme Fernando Gomes Destro
Tráfico de Animais Silvestres:Da captura ao retorno à natureza
Tese apresentada ao Programa de Pós-graduação
Stricto Sensu em Ecologia e Evolução como parte
dos requisitos para obtenção do título de doutor
pela Universidade Federal de Goiás
Orientadora: Levi Carina Terribile
Co-orientador: Paulo De Marco Júnior
DEZEMBRO – 2018
GOIÂNIA – GO
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A todos aqueles que abdicam de suas próprias
vidas em função da coletividade e das causas
difusas, em especial, às ambientais, DEDICO!
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No dia em que o homem descobrir que faz parte da teia da vida e que, da natureza, depende à sua
sobrevivência, nenhum rio mais fluirá poluído com seu orgulho, nenhuma árvore mais cairá com
sua ganância e nenhum pássaro mais lamentará aprisionado ao seu egoísmo…
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AGRADECIMENTOS
A Deus, pela existência;
Aos meus pais, Dorival Destro e Mirian Gomes, e irmãos, Gustavo Destro e Gláucia Destro, por
serem alicerce em minha vida;
Aos amigos Nelyson Oliveira, Raquel Barreto, Raquel Sabaini, Maria Rachel Pereira, Rafael
Magris, Roberto Cabral, Tatiana Pimentel, Nadja Süffert, Flávia Fialho, Seli Oliveira e Marlei
Paulino, pelo incentivo e amizade sincera;
Aos amigos da Superintendência do IBAMA em Goiás, em especial Renato Bittar, Paulo Lopes,
Helen Ribeiro, Solange Miranda, Indiária Clemente e Cristianne Miguel, pelo apoio incondicional;
Aos amigos da Universidade Federal de Goiás, em especial Virgínia de Fernandes, Flávio
Rodrigues, Anderson Medina e Flávia Machado, pelos momentos compartilhados;
Aos meus orientadores, Levi Carina Terribile e Paulo De Marco Junior, pelos exemplos,
ensinamentos e confiança depositada;
Ao Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis – IBAMA, pelo
suporte técnico e financeiro;
À Universidade Federal de Goiás, pela oportunidade do estudo gratuito e de qualidade...
AGRADEÇO!
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SUMÁRIO
RESUMO ……………………………………………………………………………………………... 12
ABSTRACT ………………………………………………………………………………………….. 14
INTRODUÇÃO GERAL: Tráfico de Animais Silvestres: Da captura ao retorno à natureza …...…… 16
Tráfico de animais silvestres …………………………………………………………………... 16
Tráfico de animais silvestres no Brasil ………………………………………...…………...…. 17
Retorno dos animais apreendidos à natureza ………………………………...…………..…… 19
Medindo o sucesso das restaurações populacionais …………………………...………..…….. 22
Organização da Tese de Doutorado …………………………………………………………… 23
Referências bibliográficas ……………………………………………………………………... 24
CAPÍTULO 1: Drivers behind the illegal capture of wild birds in Brazil …………………………… 34
Abstract ……………………………………………………………………………………………….. 35
Introduction …………………………………………………………………………………………... 36
Methods ………………………………………………………………………………………………. 39
Selection of source-municipalities and main drivers for illegal capture ……………………… 39
Multivariate Modeling …………………………………………………………………………. 42
Results ………………………………………………………………………………………………... 43
Discussion …………………………………………………………………………………………….. 46
References …………………………………………………………………………………………….. 50
Supplementary material S1. Main source-municipalities for the illegal capture of wild animals inBrazil …………………………………………………………………………………………………. 58
CAPÍTULO 2. Predicting invasion risks for the most seized bird species in Brazil …………………. 76
Abstract ……………………………………………………………………………………………….. 77
Introduction …………………………………………………………………………………………... 78
Methods ………………………………………………………………………………………………. 82
Species occurrence records and environmental layers ………………………………………... 82
Ecological Niche Models (ENM) ……………………………………………………………… 83
Invasion risk analysis ………………………………………………………………………….. 85
Results ………………………………………………………………………………………………... 86
Discussion …………………………………………………………………………………………….. 91
References …………………………………………………………………………………………….. 95
Supplementary material S1. Parameters chosen to elaborate final suitability maps ………………… 107
Supplementary material S2. TSS and AUC values …………………………………………………… 108
Supplementary material S3. Moran's I index and Multivariate environmental similarity surface …... 111
CAPÍTULO 3. Threats for bird population restoration: a systematic review ………………………… 112
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Abstract ……………………………………………………………………………………………….. 113
Introduction …………………………………………………………………………………………... 114
Methods ………………………………………………………………………………………………. 116
Results ………………………………………………………………………………………………... 118
Discussion …………………………………………………………………………………………….. 120
References …………………………………………………………………………………………….. 125
Supplementary material S1. Conceptual model of drivers that can negatively impact populationrestoration programs …………………………………………………………………………………. 133
Supplementary material S2. Reintroduction or reinforcement attempts according to the systematicreview …………………………………………………………………………………………………. 134
CAPÍTULO 4: Back home? Uncertainties for returning seized animals to the source-areas under cli-mate change …………………………………………………………………………………………... 137
Abstract ……………………………………………………………………………………………….. 138
Introduction …………………………………………………………………………………………... 139
Methods ………………………………………………………………………………………………. 142
Species occurrence records and environmental layers ………………………………………... 142
Ecological Niche Models (ENM) ……………………………………………………………… 145
Main source-areas for animal trafficking and protected areas in Brazil ……………………… 147
Climate change analysis ……………………………………………………………………….. 147
Results ………………………………………………………………………………………………... 148
Discussion …………………………………………………………………………………………….. 152
References …………………………………………………………………………………………….. 156
Supplementary material S1. Parameters chosen to elaborate final suitability maps ………………… 168
Supplementary material S2. Main source-municipalities for the illegal capture of wild animals inBrazil …………………………………………………………………………………………………. 169
Supplementary material S3. TSS and AUC values …………………………………………………… 188
Supplementary material S4. Moran's I index and Multivariate environmental similarity surface …... 191
Supplementary material S5. Predicted area (Km2) by the ten most seized bird species in Brazil un-der the current climate and four evaluated future scenarios ……………………………………….... 192
Supplementary material S6. Suitability average of the most seized species in Brazil according to theevaluated variables …………………………………………………………………………………… 193
CONCLUSÕES GERAIS: Tráfico de Animais Silvestres: Da captura ao retorno à natureza ……….. 194
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RESUMO
O tráfico de animais silvestres, uma das atividades ilegais mais lucrativas e dispersas por todo o
mudo, tem gerado inúmeras consequências socioambientais como perda de divisas, introdução de espécies
exóticas, transmissão de doenças e alterações em processos ecológicos. Não obstante aos prejuízos causados
por sua ilicitude, milhares de animais são apreendidos anualmente, requerendo das autoridades
governamentais elevados custos técnico-operacionais para a sua adequada destinação. Nesta Tese de
Doutorado, nós discutimos a temática do tráfico de animais silvestres sob um olhar amplo e atualizado,
elucidando questões originadas na dissociação do conhecimento científico com a resolução de problemas
ambientais, também conhecida como lacuna ciência-prática. Desta forma, no primeiro capítulo, sintetizamos
os principais macrofatores relacionados à captura de animais silvestres para o tráfico, buscando apontar os
mais relevantes para a retirada ilegal de aves no Brasil. Assim, nós demonstramos que a cobertura por
vegetação nativa e a proximidade às áreas protegidas, em detrimento aos fatores socioeconômicos, foram os
motivadores mais relevantes sob uma análise em ampla escala. No segundo capítulo, nós avaliamos como o
comércio legal ou ilegal da biodiversidade influencia na introdução de espécies exóticas e alterações dos
padrões biogeográficos das espécies sobrexplotadas. Deste modo, nós observamos que a região amazônica
foi uma das áreas mais vulneráveis à invasão das espécies de aves mais traficadas no Brasil. No terceiro
capítulo, compilamos os principais fatores responsáveis pelo insucesso da restauração populacional de aves,
seja esta relacionada à reintrodução ou revigoramento populacional. Neste capítulo, nós destacamos que,
controlando ou eliminando fatores como predação, movimentos de dispersão pós-soltura e doenças, as ações
que visem o retorno dos animais à natureza tendem a ser mais bem-sucedidas. Por fim, no quarto capítulo,
nós avaliamos se os municípios-fonte para o tráfico são, de fato, os melhores locais para promover o retorno
da fauna apreendida à natureza tendo em vista os irremediáveis impactos das alterações do clima. Deste
modo, por meio da modelagem de nicho ecológico e utilizando as unidades de conservação de proteção
integral como grupo controle, nós demonstramos que áreas diferentes da origem dos espécimes podem
apresentar condições mais favoráveis para manter suas populações em longo prazo. Em síntese, por meios
destes quatro capítulos, nós acreditamos ter trazido importantes avanços não somente no âmbito acadêmico,
pela promoção de uma abordagem inovadora de temas ecológicos relevantes, mas também reforçamos a
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necessidade de maior junção da teoria com a prática, buscando fornecer subsídios diretos a gestores e
tomadores de decisão envolvidos na proteção e conservação da fauna traficada em todo o mundo.
Palavras-chave: Comércio de biodiversidade; invasão biológica; modelagem de nicho ecológico; mudanças
climáticas globais; restauração populacional; revisão sistemática; tráfico de animais silvestres
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ABSTRACT
Animal trafficking, one of the most lucrative illegal activities worldwide, generates serious social
and environmental consequences, including economic losses, introduction of exotic species, disease trans-
mission and changes in ecological processes. Apart from legality issues, thousands of animals are appre-
hended each year, leading to high technical and operational costs from governmental authorities for the
proper destination of these specimens. Herein, the animal trafficking thematic was discussed under a broad
and updated view, seeking to elucidate issues originated from the dissociation of scientific knowledge from
the resolution of environmental problems, also known as research–implementation gap. Thus, in the first
chapter, the main drivers related to wild animals capture for trafficking were enumerated, prioritizing the fac-
tors most relevant concerning illegal bird capture in Brazil. In this chapter, after a broad scale analysis, in -
stead of socioeconomic factors, native vegetation coverage and proximity to protected areas were pointed out
as the main factors regarding illegal capture. In the second chapter, the role of legal or illegal wildlife trade
on the introduction of exotic species and changes in biogeographic patterns of overexploited species were as -
sessed. In this chapter, the Amazon was pointed out as one of the most vulnerable regions for the invasion of
bird species used as pets in Brazil. In chapter 3, the main drivers related to failures in the bird population
restoration efforts were compiled, be they reintroduction or reinforcement efforts. According to the results,
actions aiming at returning birds to the wild will be more successful when factors like predation, post-release
dispersion movements and diseases are controlled or eliminated. Lastly, in the fourth chapter, assessments
were carried out on whether source-municipalities are the most suitable areas for seized animal population
restoration efforts considering the irremediable impacts of climate change. Thus, ecological niche modeling
and the use of protected areas as a control group allowed for the observation that areas unrelated to the cap-
ture of trafficked specimens in Brazil may be more suitable long-term population maintenance. In summary,
through these four chapters, we hope to bring advances not only to the academic field, by promoting an inno-
vative approach to relevant ecological issues, but also reinforce the importance of joining theory and practice
by providing direct subsidies to managers and decision-makers involved in the protection and conservation
of overexploited wildlife by trafficking, worldwide.
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Keywords: Animal trafficking; biological invasion; ecological niche modeling – ENM; global climate chan-
ge; restoration population; systematic review; wildlife trade
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INTRODUÇÃO GERAL
TRÁFICO DE ANIMAIS SILVESTRES: DA CAPTURA AO RETORNO À NATUREZA
Tráfico de animais silvestres
O tráfico de animais silvestres é uma das atividades ilegais mais disseminadas e lucrativas do mundo
(Lawson e Vines, 2014), e inclui a caça, a captura e o comércio da vida selvagem, viva ou morta, para uso
medicinal, esportes, como animal doméstico, para consumo humano, ornamental ou religioso (Hansen et al.,
2012; Barber-Meyer, 2010; Phelps et al., 2016). Todas as regiões do planeta desempenham um importante
papel no tráfico e comércio ilegal de animais silvestres, seja como fonte, trânsito ou destino da vida silvestre
contrabandeada (UNODC, 2016). Elefantes e rinocerontes, por exemplo, são caçados indiscriminadamente
na África para satisfazer a crescente demanda por seus produtos no Sudeste da Ásia, onde são tidos como
símbolos de status ou usados como ingredientes na medicina tradicional (Lawson e Vines, 2014). Do mesmo
modo, aves são geralmente associadas à América Central e do Sul, répteis à Europa e América do Norte, e
corais à Oceania (UNODC, 2016). Em escala crescente, o comércio ilegal internacional atingiu, entre 2004 e
2015, mais de 164.000 apreensões, envolvendo mais de 7.000 espécies em 120 países (UNODC, 2016).
Deixando de lado a questão da legalidade, a captura clandestina da vida silvestre também tem gerado
graves consequências ambientais, incluindo a introdução de espécies exóticas, a disseminação de doenças e a
interrupção dos processos ecossistêmicos e serviços ecológicos como a polinização, a dispersão das
sementes, o controle populacional de outros animais, e, em médio e longo prazos, a extinção das espécies
sobrexplotadas (e.g. Dai e Zhang, 2017; Do Nascimento et al., 2015). Dentre estas questões, os problemas
advindos das invasões biológicas têm se destacado, sendo uma das grandes preocupações ambientais e
ameaça primária para a biodiversidade global (Clavero e García-Berthou, 2005). De fato, animais de
estimação podem escapar ou ser abandonados (e.g. Kuhnen e Kanaan, 2014; Ferronato et al., 2009; Silva e
Oren, 1990) e, de volta à vida livre, podem se estabelecer em regiões fora da sua distribuição original (e.g.
Fernandes-Ferreira et al., 2012; Bertolino, 2009; Leven e Corlett, 2004; Fontoura et al, 2013), ocasionando
inúmeros problemas ecológicos como a disseminação de patógenos, perda genética por hibridização e
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introgressão, competição interespecífica e extinção de espécies, além de inúmeros impactos em processos
ecossistêmicos (Gama e Sassi 2008; Allendorf et al. 2001; Wittenberg e Cock, 2001). Assim, identificar
potenciais espécies invasores antes da sua introdução e analisar a implicação ecológica de possíveis fugas de
indivíduos cativos é uma questão atual e fundamental para prevenir os impactos de espécies exóticas
invasoras antes mesmo delas se estabelecerem (e.g. Rosa et al. 2018; Alves et al. 2010; Kolar e Lodge 2001).
De modo geral, as causas do comércio ilegal de vida selvagem são frequentemente atribuídas às
características socioeconômicas do país e de suas regiões, especialmente em nações com alta biodiversidade
e desigualdade social (Regueira e Bernard, 2012). Neste contexto, onde prevalecem as altas taxas de
desemprego e os baixos níveis de educação formal, as atividades relacionadas ao tráfico de animais silvestres
podem ser muito lucrativas (Alves et al., 2013), inclusive fornecendo renda adicional às famílias envolvidas
(Souto et al., 2017). Contudo, distante de ser um problema exclusivo de países com instabilidade política ou
baixa capacidade governamental (López-Bao et al., 2015), o tráfico de fauna tem se tornado uma indústria
global maciça, atraindo grupos de criminosos movidos especialmente pelos baixos riscos, altos lucros e
fracas punições (Ratchford et al., 2013). Ademais, devido à sua grande lucratividade, o tráfico também tem
financiado novas frentes ilegais e crimes transnacionais, gerando prejuízos econômicos e desestabilização
política nos países em que as espécies ameaçadas não podem ser facilmente protegidas e onde os atores da
atividade criminosa dificultam o desenvolvimento, o investimento e o turismo no país (Lawson e Vines,
2014). Longe de ser mais uma questão de conservação ou bem-estar animal, o tráfico e comércio ilegal de
animais silvestres deve ser visto como uma questão de segurança nacional e global (Ratchford et al., 2013).
Neste contexto, entender os fatores que, de fato, motivem a captura ilegal dos espécimes na sua origem tem
se tornado tarefa primordial para qualquer ação que vise o combate e controle efetivos desta atividade ilícita.
Tráfico de animais silvestres no Brasil
O Brasil exibe uma das mais ricas biodiversidades do mundo e sua diversidade biológica e cultural
fazem do país um excepcional local para examinar o comércio da vida selvagem e suas implicações para a
conservação (Alves et al., 2013). Dentre os diversos fatores que fomentam o tráfico, os aspectos
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socioeconômicos são preponderantes para explicar a captura ilegal e o intenso comércio da vida silvestre no
país (e.g. Alves e Rosa, 2010; Regueira e Bernard, 2012). De fato, da mesma forma que em outros países-
fonte para o tráfico como o México (González-Marín et al., 2016), Peru (Gastañaga et al., 2011), Camboja
(Gray et al., 2017), Zimbabué (Lindsey et al., 2011), Congo (Nasi et al., 2011) e Nigéria (Atuo et al., 2015) ,
o Brasil possui características que o dirigem para o comércio ilegal: é um país megadiverso com grande
desigualdade social em todas as suas regiões (Regueira e Bernard, 2012). Contudo, um olhar mais atento
sobre a relação pobreza e consumo ilegal da vida silvestre revela que o conhecimento sobre este assunto é
limitado e que conservacionistas precisam ter uma visão mais ampla sobre o que constitui, de fato, o
comércio ilegal da vida silvestre, os fatores que motivam as pessoas a caçarem ilegalmente e como é possível
resolver tais problemas em médio e longo prazos (Duffy et al., 2016). Assim, embora o comércio ilegal da
vida silvestre seja comumente caracterizado como um resultado da pobreza, a ligação entre saúde, pobreza e
engajamento no comércio da vida selvagem são fatores ainda muito distantes de serem entendidos
(TRAFFIC, 2008; Duffy et al., 2016). Não obstante, além das cores, cantos e comportamentos dos animais,
acesso aos espécimes e hábitos culturais podem ter uma influência ainda maior sobre o comércio e
manutenção em cativeiro da fauna silvestre no Brasil (Alves et al., 2010; Souto et al., 2017), devendo ser
melhor investigados.
Estudos prévios apontam que aves é o grupo animal mais cobiçado pelos traficantes de animais
silvestres no Brasil (Destro et al., 2012). Culturalmente, manter aves em cativeiro, especialmente as canoras,
tem sido uma atividade de destaque e preservada por séculos em diferentes classes sociais, sendo difundida
em diferentes regiões urbanas e rurais do país (e.g. Alves et al., 2013; Kuhnen et al., 2012; Alves et al.,
2010). Como consequência dessa sobrexploração, das quase 2.000 espécies de aves nativas no Brasil
(Piacentini et al., 2015), centenas já estão ameaçadas de extinção, e o tráfico de animais silvestres é um dos
principais responsáveis (Marini e Garcia, 2005; Alves et al., 2013). De fato, embora a maioria das espécies
de aves traficadas no país está listada como “Pouco Preocupantes” (Destro et al., 2012) e possui ampla
distribuição geográfica (ver Sick, 1997), muitas apresentam sérias diminuições populacionais e outras já
estão localmente extintas (Freitas et al., 2015; Fernandes-Ferreira et al., 2012; Gama e Sassi, 2008). No meio
rural, onde a cadeia de interações comerciais iniciam, coletores capturam os animais utilizando várias
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técnicas (ver Souto et al., 2017) e os entregam a comerciantes locais que os negociam em mercados e feiras
públicas (Regueira e Bernard, 2012; Licarião et al., 2013). Não obstante, muitos animais são enviados a
criadores ou empreendimentos autorizados e não autorizados por meios de traficantes intermediários (Destro
et al., 2012; Kuhnen et al., 2012), que inúmeras vezes os comercializam pela internet (Ratchford et al., 2013;
Souto et al., 2017). Assim, embora o comércio ilegal de animais silvestres caracteriza-se com uma atividade
ilícita difusa (Alves et al., 2013), é possível inferir que: i) o comércio interno é o principal destino da fauna
ilegalmente traficada no Brasil (Destro et al., 2012); ii) a maioria dos espécimes ilegalmente comercializados
provém das regiões Norte, Nordeste e Centro-Oeste do país (Ferreira e Glock, 2004); e, iii) o maior
quantitativo de animais ilegalmente capturados é enviado, por meio de rotas terrestres, às regiões Sul e
Sudeste do Brasil, onde estão seus principais centros consumidores (Ferreira e Glock, 2004; Destro et al.,
2012). Exceção é verificada, contudo, nos estados amazônicos, onde os rios são a principal rota para o
comércio ilegal e as aves têm pouca representatividade em relação ao quantitativo de vertebrados silvestres
traficados e apreendidos (Do Nascimento et al., 2015).
Retorno dos animais apreendidos à natureza
Quando animais silvestres vivos são apreendidos pelas autoridades governamentais, essas têm a
responsabilidade de destiná-los adequadamente, sempre zelando por seu bem-estar e a conservação das
populações silvestres existentes (IUCN, 2002). Segundo a União Internacional para a Conservação da
Natureza, há três destinos principais para os animais apreendidos: i) manutenção do(s) indivíduo(s) em
cativeiro; ii) retorno do(s) espécime(s) à natureza; e, iii) eutanásia (IUCN, 2002; CITES, 2016). No Brasil,
mesmo considerando os altos recursos humanos e financeiros inerentes ao resgate e reabilitação dos animais
(Magroski et al., 2017), o retorno da fauna apreendida ao seu habitat de origem tem sido a estratégia mais
adotada pelos órgãos governamentais (Destro et al., 2012). Solturas mal-planejadas, contudo, são passíveis
de causar diversos impactos ambientais, como a introdução de patógenos ou doenças (Cunningham, 1996;
Jiménez e Cadena, 2004; Godoy e Matushima, 2010), mudanças nas interações ecológicas inter e
intraespecíficas, como competição, predação, parasitismo e mutualismo (Jiménez e Cadena, 2004; Molony et
al., 2006), e modificação na estrutura genética das populações como perda de adaptações locais e eliminação
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da diferença genética entre populações (Moritz, 1999; Champagnon et al., 2012). Por outro lado, se bem
planejado e considerando questões como bem-estar, valor de conservação e custos, o retorno de animais
apreendidos à natureza apresenta inúmeros benefícios: i) melhora o potencial de conservação das espécies ou
populações; ii) permite que os espécimes voltem a cumprir seu papel biológico e ecológico; iii) promove
valores de conservação locais por meio de programas de educação ou consciencialização pública; e, iv) faz
uma forte declaração política/educacional sobre o destino dos espécimes apreendidos (e.g. IUCN, 2002;
Champagnon et al., 2012; Magroski et al., 2017).
Em termos conceituais, o ato de translocar organismos vivos para dentro de sua área de distribuição
original indígena por meio de metas conservadoras é denominado de restauração populacional (IUCN, 2013)
e compreende duas atividades: reintrodução e revigoramento populacional, que diferem entre si não pelas
técnicas de manejo utilizadas, mas sim, pela presença ou ausência de populações específicas antes da soltura
(IUCN, 2013; CITES, 2016; Destro et al., 2018). Neste sentido, soltar um organismo dentro de uma área na
qual sua espécie desapareceu é denominado reintrodução e a liberação de um organismo junto à uma
população existente de coespecíficos é chamada de revigoramento populacional (IUCN, 2013). No geral,
ambas as atividades são consideradas de baixo risco porque são apoiadas em dados históricos sobre o
desempenho das espécies em seu habitat natural (Thomas, 2011; Payne e Bro-Jørgensen, 2016). Além disso,
possuem melhor aplicabilidade em países-fonte para tráfico, como Brasil, que ainda possuem uma
quantidade significativa de vegetação nativa remanescente (ver MMA, 2007) e onde as espécies mais
cobiçadas tendem a ser abundantes e possuir uma ampla distribuição (Godoy e Matushima, 2010).
Os biólogos da conservação, a fim de verdadeiramente salvaguardar as linhagens genéticas das aves
(Magroski et al., 2017), têm sugerido que o retorno dos animais apreendidos à natureza ocorra
prioritariamente nos mesmos locais onde estes foram retirados (Martins et al., 2018). Contudo, determinar a
origem exata dos espécimes a partir dos pontos de apreensão é uma tarefa difícil, uma vez que estas ocorrem
geralmente ao longo de rotas comerciais, distantes do local onde os indivíduos foram capturados, e muito
pouca informação é obtida com os traficantes (Hernandez e Carvalho, 2006; Presti et al., 2015; Martins et al.,
2018). Ademais, as técnicas necessárias para implementação deste trabalho investigativo são consideradas
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caras, indisponíveis ou, muitas vezes, de difícil aplicação (Fernandes e Caparroz, 2013; Magroski et al.,
2017; Martins et al., 2018), e as pressões que motivam as capturas ilegais geralmente são contínuas e de
árduo combate (Silva e Bernard, 2016). Não obstante, diante dos irremediáveis efeitos a serem ocasionados
pelas mudanças climáticas globais, será que o retorno dos espécimes traficados às áreas-fonte seria a solução
mais acertada na perspectiva de persistência das populações em longo prazo?
Diversos estudos têm debatido os impactos da mudança no clima sobre a sobrevivência e
manutenção da fauna silvestre (e.g. Thomas et al., 2004; Marini et al., 2009; Travis et al., 2013) e, neste
contexto, a América do Sul ganha destaque pois é uma das regiões do planeta mais vulneráveis (Boulanger et
al., 2010; Urban, 2015; Anjos e Toledo, 2018). Dentre os animais mais bem estudados, as aves se destacam
pois são consideradas importantes indicadores dos reais impactos das mudanças climáticas, especialmente
em ecossistemas tropicais (Marini et al., 2009; Sekercioglu et al., 2012). De fato, estudos prévios já
demonstraram que, além de impulsionar mudanças nos fenótipos de acordo com as novas condições
ambientais através da plasticidade fenotípica e/ou mudanças evolutivas dos organismos (Møller et al., 2010;
Maggini et al., 2011), as mudanças climáticas podem levar à alterações na distribuição das espécies, ou seja:
i) amplia, se a mudança for benéfica à sua necessidade ecológica; ii) contrai, quando a mudança é
prejudicial; ou, iii) simplesmente altera a área de distribuição, quando em busca de novas condições
climáticas favoráveis (e.g. Maggini et al., 2011; Crossman et al., 2012; Braidwood et al., 2018).
A migração de organismos reintroduzidos em direção a habitats climaticamente mais adequados
pode ser uma condição natural de adaptação (Carroll et al., 2009), especialmente para as aves, que tendem a
responder mais facilmente às mudanças climáticas por meio da alteração na sua distribuição original (Triviño
et al., 2018). Contudo, em alguns casos, os deslocamentos dos espécimes em vida livre podem ser frustrados
porque as populações reintegradas à natureza podem não se adaptar às novas condições ou não conseguir se
adaptar com a rapidez suficiente (Kokko e Lopez-Sepulcre, 2006; Devictor et al., 2008; Visser, 2008). Neste
contexto, as áreas de origem podem, em longo prazo, fornecer soluções inadequadas para a persistência das
espécies (Araújo et al., 2004; Watson e Watson, 2015), levando-as à extinção mesmo com um substancial e
contínuo investimento humano (Chauvenet et al., 2013). Assim, considerar as mudanças climáticas no
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planejamento de translocação e no exercício de priorização de áreas para projetos de
reintrodução/revigoramento é tarefa fundamental e pode oferecer uma essencial informação para a
conservação: a adequação atual e de longo prazo das áreas candidatas (Martínez-Meyer et al. 2006;
Chauvenet et al., 2013). Neste contexto, a despeito de sua importância, poucos estudos têm avaliado as
possíveis mudanças temporais das áreas adequadas para os projetos de restauração populacional (Martínez-
Meyer et al., 2006), incluindo, aqui, as ações de o retorno à natureza dos espécimes advindos do tráfico.
Medindo o sucesso das restaurações populacionais
Avaliar como bem-sucedidos os esforços de restauração populacional de fauna ainda é uma questão
muito controversa no meio acadêmico, mesmo com as inúmeras propostas metodológicas disponíveis
(Soorae, 2013). Como uma métrica básica de sucesso, alguns autores consideram que as taxas de
sobrevivência no primeiro ano após a soltura, dentro da distribuição original relatada para os filhotes de aves,
são indicativos de uma liberação bem-sucedida (White Jr. et al., 2005). Em outros estudos, pesquisadores
consideram a sobrevivência e a reprodução como dois parâmetros fundamentais em termos de
estabelecimento e persistência da população, definindo 'sucesso' como aquelas translocações em que a
sobrevivência no primeiro ano foi > 0,50 (sobrevivência > mortalidade) e na qual as aves liberadas se
reproduzem naturalmente com coespecíficos criados em cativeiro ou selvagens (White Jr. et al., 2012).
Outros autores acreditam, contudo, que três objetivos devem ser alcançados em um esforço de restauração
populacional: i) estabelecimento: a sobrevivência da geração após a soltura; ii) crescimento: reprodução da
geração solta e seus descendentes; e, iii) regulação: persistência da população reintroduzida (Seddon, 1999;
Sarrazin, 2007; Miller et al., 2014). Contudo, para esses mesmos autores, embora as fases de estabelecimento
e crescimento sejam fundamentais para o sucesso, elas não fornecem estimativas precisas sobre a viabilidade
em longo prazo de uma população reintroduzida (Seddon, 1999; Sarrazin, 2007; Miller et al., 2014). Assim,
os critérios de sucesso final devem se concentrar na fase de regulação, durante a qual a dinâmica
populacional depende criticamente das interações entre espécies e características do habitat, a fim de que se
possa tirar conclusões mais confiáveis sobre a dinâmica populacional em longo prazo (Armstrong e
Reynolds, 2012).
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Para contribuir com o desenvolvimento da ciência da biologia da reintrodução, Robert e
colaboradores (2015) propuseram um método que avalia se a viabilidade de populações reintroduzidas
poderia ser feita utilizando os mesmos critérios utilizados para populações remanescentes, como os adotados
pela União Internacional para a Conservação da Natureza para elaboração da Lista Vermelha de Espécies
Ameaçadas de Extinção. Para isso, dois postulados foram propostos: i) que programas bem-sucedidos de
reintrodução devam produzir populações viáveis e, ii) que avaliações confiáveis de sucesso final exijam que
as populações atinjam sua fase de regulamentação (Robert et al., 2015). Contudo, Haskins (2015) aponta
fragilidades nesta metodologia, uma vez que o tempo e os recursos necessários a este tipo de avaliação não
conseguem acompanhar a crescente demanda por ações de conservação, especialmente sob as rápidas
mudanças no clima. Ademais, segundo este mesmo autor, a definição padronizada do sucesso da
reintrodução poderia ser uma tarefa quase impossível se considerar o alto grau de variabilidade das
necessidades das espécies quando se trata de critérios de sucesso da reintrodução (Haskins, 2015). De fato,
considerando que muitas questões da biologia da reintrodução ainda permanecem inconclusivas (White Jr. et
al., 2012; Robert et al., 2015), estudar os fatores de insucesso parece despontar como uma alternativa mais
prática e viável de avaliar o quão bem-sucedidas são as ações de restauração populacional dos mais variados
grupos animais (Robert et al., 2015).
Organização da Tese de Doutorado
Diante das inúmeras questões inerentes ao tráfico de animais silvestres e a restauração populacional
de fauna, buscamos sintetizar nesta Tese de Doutorado alguns do temas ecológicos mais atuais e urgentes,
debatidos aqui sob um enfoque inovador a partir da junção da teoria com a prática. Neste sentido, a Tese foi
dividida em quatro capítulos, cada qual estruturado como um artigo científico. Assim, embora cada capítulo
tenha seguido a formatação proposta pela revista a qual foi submetido, o conjunto textual e de organização
foi padronizado de modo a facilitar a leitura e compreensão do leitor.
23/195
A importância de cada capítulo na problemática do tráfico de animais silvestres foi esquematizada
por meio de um modelo conceitual (Figura 1). No Capítulo 1 nós sintetizamos e priorizamos os macrofatores
que mais motivam a captura ilegal de fauna no Brasil. No Capítulo 2 nós avaliamos como o comércio legal
ou ilegal da biodiversidade influencia na introdução de espécies exóticas e alterações dos padrões
biogeográficos das espécies sobrexplotadas. Já no Capítulo 3 nós sistematizamos os principais fatores
responsáveis pelo insucesso da restauração populacional de aves, seja esta relacionada à reintrodução ou
revigoramento populacional. Por fim, no Capítulo 4, nós avaliamos se os municípios-fonte para o tráfico são,
de fato, os melhores locais para as ações que visem o retorno da fauna apreendida à natureza, tendo em vista
os irremediáveis efeitos das alterações climáticas no planeta.
Figura 1. Modelo conceitual destacando os quatro capítulos que compõem a Tese de Doutorado
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Capítulo 1
Drivers behind the illegal capture
of wild birds in Brazil
Guilherme Fernando Gomes Destro, Paulo De Marco e
Levi Carina Terribile
Artigo submetido à revista “Environmental Conservation” em outubro de 2018
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Drivers behind the illegal capture of wild birds in Brazil
Guilherme Fernando Gomes Destroa,b,*, Paulo De Marcoc, Levi Carina Terribiled
a. Programa de Pós-Graduação em Ecologia e Evolução, Universidade Federal de Goiás, Campus
Samambaia, CP 131, 74001-970, Goiânia, GO, Brazil.b. Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis, Superintendência no
Estado de Goiás, Rua 229, nº 95 – Setor Universitário, 74605-090 – Goiânia, GO, Brazil.c. Departamento de Ecologia, Instituto de Ciências Biológicas, Universidade Federal de Goiás, Campus
Samambaia, CP 131, 74001-970, Goiânia, GO, Brazil.d. Instituto de Ciências Biológicas, Universidade Federal de Goiás, Regional Jataí, 75801-615, Jataí,
GO, Brazil.
*Corresponding author at: Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis,
Superintendência no Estado de Goiás, Rua 229, nº 95 – Setor Universitário, 74605-090 – Goiânia, GO,
Brazil.
E-mail addresses: [email protected] (GFG Destro), [email protected] (P De Marco),
[email protected] (LC Terribile)
Abstract: In order to conserve species exploited by trafficking, governmental actions should be
directed to source-areas, in order to reduce or eliminate illegal and indiscriminate trapping. However,
there are few academic studies aimed at diagnosing and prioritizing the most relevant drivers for
illegal capture of wild animals. In this study, we aimed to evaluate the main drivers for the illegal
capture of wild birds in Brazil and its regions. A broad literature review was carried out and, a
multivariate modeling approach indicated the economic, social or environmental factors that display
the greatest importance in boosting this illicit activity worldwide. Our search revealed seven drivers
for illegal wildlife capture addressed by researchers in studies carried out in source-countries. In
Brazil, native vegetation coverage and proximity to protected areas were the main factors. This is the
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first broad scale study to point out environmental factors as the main drivers for illegal wild bird
capture destined for trafficking in Brazil.
Keywords: animal trafficking; avian conservation; crimes against wildlife; general discriminant
analysis – GDA; multivariate analysis; passerine.
Introduction
Wildlife trafficking is one of the most widely spread and lucrative illegal activities worldwide
(Lawson & Vines, 2014; UNODC, 2016), comprising the capture, poaching, and trade of living and
dead wildlife for medicinal, pet, sport, human consumption and ornamental or religious purposes
(Barber-Meyer, 2010; Hansen et al., 2012). Not taking into account legality issues (see Ratchford et
al., 2013; Lawson & Vines, 2014), unregulated wildlife trade generates serious environmental
consequences, including introduction of exotic species, spread of wildlife diseases, disruption of
ecosystem processes and ecological services, such as pollination, seed dispersal, population control of
other animals, and, in the medium and long-term, extinction of exploited species (e.g. Fernandes-
Ferreira et al., 2012; Do Nascimento et al., 2015; Dai & Zhang, 2017). Consequently, although it is
difficult to measure the amount of illegally traded specimens (Barber-Meyer, 2010; Duffy, 2016),
characterizing the origin of the trafficking chain could aid in efforts to reduce or eliminate
indiscriminate captures (Primmer et al., 2000; Lawson & Vines, 2014).
Brazil has one of the richest avifauna in the world, with many species currently threatened by
illegal trade (Marini & Garcia, 2005; Freitas et al., 2015) which is related to the depletion of 295
Brazilian bird species (Alves et al., 2013a), with Thraupidae, which received the most genera from the
former Emberizidae (Barker et al., 2013), being the most representative family (e.g. Destro et al.,
2012; Fernandes-Ferreira et al., 2012; Licarião et al., 2013). In rural upland and farmland areas, where
the commercial interaction chain begins, collectors capture animals using various techniques (see
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Souto et al., 2017). Once captured, most illegal birds are delivered to traders who negotiate the
specimens in public markets and fairs (Regueira & Bernard, 2012; Licarião et al., 2013), or sent to
both authorized and unauthorized breeders and enterprises by intermediary traffickers (Destro et al.,
2012; Kuhnen et al., 2012), who subsequently negotiate them mainly through the internet (Ratchford
et al., 2013; Souto et al., 2017). Figure 1 groups the stages involved in wild animal trafficking in
Brazil, from capture in the wild to final consumers.
Fig. 1. Wildlife trafficking chain in Brazil, from capture in the wild to final consumers.
Illegal wild bird captures and their trade are widespread throughout Brazil (Alves et al.,
2013a) and identifying source-areas is not an easy task, as the apprehension site of the animals
generally differs from their capture area (Hernandez & Carvalho, 2006). However, it is possible to
infer that most illegally traded animals come from the north, northeast and midwest Brazilian regions
(Ferreira & Glock, 2004) and are then smuggled to both south and southeast regions by federal
highways (Fig. 2). Rivers are also important routes for the sale of trafficked animals in the Amazon
states (north) However, birds are less represented among the total number of wild vertebrates
trafficked and seized (Do Nascimento et al., 2015). In the same way as in other wildlife supply
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countries (Gastañaga et al., 2011), the main purpose for illegally captured wild animals in Brazil is
internal trade (Destro et al., 2012).
Fig. 2. Main source-areas for illegal wild animal capture in Brazil and main river and land routes used
for their transportation. (Source: updated from Destro et al. 2012).
Despite its great territorial extension and extreme socio-environmental complexity, Brazilian
socioeconomic aspects are the main factors in the literature used to explain and characterize regional
wildlife trade in the country (e.g. Alves & Rosa, 2010; Regueira & Bernard, 2012), although with little
scientific basis. In order to better understand the national dynamics of wildlife trafficking and propose
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effective measures for the national protection of exploited species, it is necessary to integrate socio-
environmental peculiarities which are always treated locally (e.g. Gama & Sassi, 2008; Licarião et al.,
2013; Alves et al., 2016). Thus, the present study aimed to systematize the most influential drivers in
illegal animal captures in source countries worldwide and evaluate, at a broad scale, which of these
most contribute for illegal bird capture in Brazil. The specific objectives were to map the main
supplier regions for trafficked wild animals in Brazil and assess the factors that most promote this
illicit activity in each region of the country.
Methods
Selection of source-municipalities and main drivers for illegal capture
An extensive literature search was carried out at the National Electronic Brazilian Library
“CAPES Portal de Periódicos” (CAPES, 2016) to identify papers related to trafficked wild animals in
Brazil. The terms “illegal” AND “trade” AND “Brazil” were used, without restricting journal,
language, year of publication or information platform. A total of 139 papers were identified. In
addition, the Google Search Engine (www.google.com) was also used, in both Portuguese and English,
to search for gray literatures, such as newsletter articles, magazines, and newspapers, published
abstracts, books, book chapters, and technical reports, adding 60 other publications. Thus, analyzing
this literary framework, all drivers cited by researchers that could explain the practice of illegal wild
animals capture in source-countries were obtained, totaling seven in all (Table 1). Furthermore, this
same literature review was used to list the source-municipalities for animal trafficking in Brazil, i.e.
municipalities described in the literature as wild animal suppliers, referred to herein as source-areas
(Fig. 2; Appendix A).
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Table 1. Drivers addressed by researchers that could explain the practice of illegal wildlife capture in
source countries. Legend: APAs: Environmental Protection Areas.
Driver Theoretical background Reference authorReference
yearData source
Remnants of natural vegetation from Brazilian biomes
A greater numbers of specimens and, consequently, higher capture rates are expected in regions with more available habitats
Santos and Araujo(2015)
2008
Amazon:INPE (2008);Other biomes:MMA (2008)
Municipal Human Development Index
Higher capture rates are expected in regions with lower education and income rates
Godoy and Matushima(2010); Santos and
Araujo (2015); Regueiraand Bernard (2012)
2010 UNDP (2010)
Municipal Gross Domestic Product
Higher capture rates are expected in poorer regions
Godoy and Matushima(2010); Santos and
Araujo (2015); Regueiraand Bernard (2012)
2010 IBGE (2010a)
Most Trafficked Species Richness
Higher capture rates are expected in regions presenting greater species richeness
Atuo et al. (2015) CurrentBirdLife(2016)
Federal, state andmunicipal protected areas (excluding APAs)
Higher capture rates are expected in less protected regions
Wright et al. (2001) 2010 MMA (2017)
Road networkHigher capture rates are expected in more accessible regions
Alves et al. (2013a);Clements et al. (2014)
2008 MT (2008)
Municipal population density
Higher capture rates are expected in more densely populated regions
Santos and Araujo(2015)
2010 IBGE (2010b)
To obtain data for the analyses of these seven drivers, the year of last decennial census in
Brazil (year 2010) was used as reference - except for native vegetation coverage and road systems, not
available for 2010, but available for 2008. All geographic databases were obtained from Brazilian
governmental websites, such as the Ministry of the Environment (MMA, 2008; MMA, 2017), Ministry
of Transport (MT, 2008), the Instituto Nacional de Pesquisas Espaciais (INPE, 2008), and the Instituto
Brasileiro de Geografia e Estatística (IBGE, 2010a; IBGE, 2010b), or international organizations such
as the United Nations Development Programme (UNDP, 2010) (Table 1). We excluded Environmental
Protection Areas (APAs, as abbreviated in Portuguese) were excluded from the analysis regarding
quantitative protected areas, as this type of category displays a low degree of land use restriction
(Rylands & Brandon, 2005). The union of the distribution maps of the 10 most seized bird species in
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Brazil (Table 2), according to a survey conducted by Destro et al. (2012), was used as a surrogate to
obtain the richness map of most trafficked species. The 10 most seized bird species belonging to
Thraupidae (7), Passerellidae (1), Icteridae (1) and Cardinalidae (1) families, are nationally coveted by
trafficking, due to their beautiful plumage, shape and song (e.g. Fernandes-Ferreira et al., 2012;
Licarião et al., 2013; Teixeira et al., 2014). Moreover, species like the Saffron Finch and Red-cowled
Cardinal are also used in fights, the same way as roosters in cock fighting (Gama & Sassi, 2008; Alves
et al., 2010; Souto et al., 2017). According to Destro et al. (unpublished results), these 10 species
matched over 60% of the amount of wild birds seized in the country from 2005 to 2009. In this sense,
although all are categorized as "Least Concern" by IUCN (2016) and present a wide geographic
distribution (Sick, 1997), many have suffered severe population reductions, and some have already
become locally extinct (Fernandes-Ferreira et al., 2012). In fact, understanding the scale and breadth
of the illegal trade for species that are not global conservation flagships has been pointed out by
researchers as required, since they represent a significant proportion of live wildlife seizures in
tropical countries and often have no guarantee of financial resources for protection (Gray et al., 2017).
We obtained the distribution polygons of the most seized species from the BirdLife website (BirdLife,
2016) and all geoprocessing steps were performed using the ArcGis 10.2.2 software (ESRI, 2014).
Table 2. Most seized wild bird species in Brazil from 2005 and 2009 (Source: Destro et al. 2012).
Family Specie Author Common nameConservation
status
Thraupidae Sicalis flaveola (Linnaeus, 1766) Saffron Finch Least Concern
Thraupidae Saltator similisd'Orbigny and Lafresnaye, 1837
Green-winged Saltator Least Concern
Thraupidae Sporophila caerulescens (Vieillot, 1823) Double-collared Seedeater Least Concern
Cardinalidae Cyanoloxia brissonii (Lichtenstein, 1823) Ultramarine Grosbeak Least Concern
Thraupidae Sporophila angolensis (Linnaeus, 1766) Chestnut-bellied Seed-Finch Least Concern
Icteridae Gnorimopsar chopi (Vieillot, 1819) Chopi Blackbird Least Concern
Thraupidae Paroaria dominicana (Linnaeus, 1758) Red-cowled Cardinal Least Concern
Thraupidae Sporophila lineola (Linnaeus, 1758) Lined Seedeater Least Concern
Passerellidae Zonotrichia capensis (Statius Muller, 1776) Rufous-collared Sparrow Least Concern
Thraupidae Sporophila nigricollis (Vieillot, 1823) Yellow-bellied Seedeater Least Concern
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Multivariate Modeling
The values corresponding to the seven selected drivers were extracted for each of the 5,563
Brazilian municipalities: i) Percentage of native vegetation coverage – NVC; ii) Municipal Human
Development Index - MHDI; iii) Municipal Gross Domestic Product – GDP; iv) Most Trafficked
Species Richness – RIC; v) Percentage of protected areas – PA; vi) Road density (m2/m2 X 1000) –
ROA; and, vii) Municipal population density (per/Km2) – MPD.
Multivariate modeling approaches were applied to answer the following questions: 1) Which
amongst the seven drivers identified in the literature most explain the illegal bird capture in Brazil? 2)
Are the preponderant drivers the same in the five Brazilian regions? This was carried out using a
General Discriminant Analysis (GDA), a multivariate statistical technique that uses information
available from a group of independent variables with normal distribution to predict the value of a
categorical dependent variable (Ragsdale, 2001). The GDA was performed using the Statistica 7.0
software, using Brazil followed by the north, northeast, midwest, and south/southeast regions as
individualized units. We grouped the south and southeast regions due to a low number of
municipalities with illegal capture incidence and because they are considered the main national
consumers for Brazilian trafficked wildlife (Ferreira & Glock, 2004). As the dependent variable, all
Brazilian municipalities were categorized into two groups: a) "source-areas": municipalities where
wildlife illegal capture has been pointed out in the literature; or, b) “control group”: remaining
municipalities. In this sense, the GDA was used to determine which independent variables (drivers)
most contributed to the differences among groups (source-areas and controls) (Malhotra, 2001). To
obtain simple correlations between the variables and the discriminant function, i.e., to identify which
independent variables cause the discrimination between the dependent variables, we used “Factor
Structure Coefficients”, also called “Structure correlations” or “Discriminant loadings”. This metric is
useful to assign substantive "meaningful" labels to the discriminant functions, akin to the
interpretation of factors in a factor analysis (Hair et al., 2009). Variables that reached “Factor Structure
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Coefficients” > 0.4 were considered relevant (Hair et al., 2009). We standardized all data for the
statistical analyses and used a stepwise method, which considers the step-by-step inclusion of
significant variables only (Hair et al., 2005). In addition, we considered the Wilks’ lambda statistic test
(λ) to evaluate the differences between means for each variable among groups, where λ = 1 indicates) to evaluate the differences between means for each variable among groups, where λ) to evaluate the differences between means for each variable among groups, where λ = 1 indicates = 1 indicates
no significant difference (Subramanian et al., 2007).
Results
In total, 195 municipalities displaying incidences of illegal capture of wild animals were
identified: 40 in the north, 71 in the northeast, 45 in the midwest and 39 in the south/southeast regions
(Fig. 2). The R2 obtained from Chi-square tests with successive roots removed (Table 3) explained
between 3.48% (northeast) and 10.85% (midwest) of the variation observed among dependent
variables. The Wilks’ lambda statistic test (λ) to evaluate the differences between means for each variable among groups, where λ = 1 indicates) indicated that, although significant, there is little
difference between the “source-areas” and control group.
Table 3. Chi-square tests with successive roots removed.
RegionEigen-value
CanonicalR
CanonicalR ^2
Wilk'sLambda
Chi-Sqr. df p-level
Brazil 0.039 0.193 0.0372 0.963 210.521 4 < 0.05
North 0.118 0.324 0.1052 0.895 49.409 5 < 0.05
Midwest 0.122 0.329 0.1085 0.891 53.198 2 < 0.05
Northeast 0.036 0.187 0.0348 0.965 63.340 3 < 0.05
South/Southeast
0.101 0.302 0.0914 0.909 273.372 3 < 0.05
Natural factors, such as native vegetation coverage and protected areas, were the most
important drivers for illegal wild bird captures in Brazil, followed by road density and most trafficked
species richness (Table 4). Socioeconomic factors, such as municipal population density, municipal
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gross domestic product and municipal human development index, had secondary or null roles. An
exception was observed for the northeast, where the high municipal human development index was
noteworthy as an important discriminant driver for illegal wild bird captures. Table 5, that presents the
significance tests for each variable in Brazil and for each of its regions, separately, shows which
independent variables were significant in each Brazilian region.
Table 4. Factor structure coefficients. MPD: Municipal population density; GDP: Municipal Gross
Domestic Product; MHDI: Municipal Human Development Index; NVC: Native Vegetation Coverage;
ROA: Road Density; PA: Protected Areas; RIC: Most Trafficked Species Richness. The most
important variables were showed with gray (coefficients higher than 0.4).
Variables Brazil north midwest northeast south/southeast SUM
MPD -0.114 0.110 -0.068 0.137 -0.028 0
GDP -0.132 0.267 -0.017 0.146 -0.035 0
MHDI -0.314 -0.321 -0.260 0.679 -0.163 1
NVC 0.877 0.144 0.562 0.200 0.813 3
ROA -0.447 -0.432 -0.126 -0.297 -0.201 2
PA 0.609 0.050 0.126 0.514 0.809 3
RIC -0.213 0.493 0.539 -0.049 -0.073 2
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Table 5. Multivariate tests of significance for the independent variables. MPD: Municipal population
density; GDP: Municipal Gross Domestic Product; MHDI: Municipal Human Development Index;
NVC: Native Vegetation Coverage; ROA: Road Density; PA: Protected Areas; RIC: Most Traffiked
Species Richness.
Variables
Brazil midwest
Test Value FEffect
dfError
dfp Test Value F
Effectdf
Errordf
p
Intercept Wilks 0.034 158907.095 1 5588 < 0.05 Wilks 0.087 4859.036 1 463 < 0.05
MPD Wilks 1.000 0 Wilks 1.000 0
GDP Wilks 1.000 0 Wilks 1.000 0
MHDI Wilks 1.000 0 Wilks 1.000 0
NVC Wilks 0.982 100.134 1 5588 < 0.05 Wilks 0.923 36.618 1 463 < 0.05
ROA Wilks 0.997 15.347 1 5588 < 0.05 Wilks 1.000 0
PA Wilks 0.994 31.384 1 5588 < 0.05 Wilks 1.000 0
RIC Wilks 0.999 6.451 1 5588 < 0.05 Wilks 0.926 37.124 1 463 < 0.05
north northeast
Intercept Wilks 0.080 5062.229 1 443 < 0.05 Wilks 0.03844902.52
51 1788 < 0.05
MPD Wilks 0.990 4.347 1 443 < 0.05 Wilks 1.000 0
GDP Wilks 0.982 8.317 1 443 < 0.05 Wilks 1.000 0
MHDI Wilks 0.970 13.672 1 443 < 0.05 Wilks 0.977 42.789 1 1788 < 0.05
NVC Wilks 1.000 0 Wilks 1.000 0
ROA Wilks 0.978 10.028 1 443 < 0.05 Wilks 0.992 14.881 1 1788 < 0.05
PA Wilks 1.000 0 Wilks 0.991 16.441 1 1788 < 0.05
RIC Wilks 0.943 26.931 1 443 < 0.05 Wilks 1.000 0
south/southeast
Intercept Wilks 0.012 226721.573 1 2852 < 0.05
MPD Wilks 1.000 0
GDP Wilks 1.000 0
MHDI Wilks 1.000 0
NVC Wilks 0.973 78.088 1 2852 < 0.05
ROA Wilks 0.998 6.523 1 2852 < 0.05
PA Wilks 0.970 87.753 1 2852 < 0.05
RIC Wilks 1.000 0
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Discussion
Our study demonstrated, on a broad scale, that drivers not directly related to socioeconomic
variables may be more relevant, reinforcing the need for multi-scale approaches in similar
socioecological studies (Cumming et al., 2015; McGarigal et al., 2016). Historically, however, the
causes of illegal wildlife trade in countries presenting high biodiversity and social inequality have
been frequently attributed to the socioeconomic characteristics of the country and its regions (Regueira
& Bernard, 2012). In this context, where high unemployment rates and low levels of formal education
conditions prevail, activities related to illegal bird trade can be very lucrative (Alves et al., 2013a) and
provide additional income sources to families (Souto et al., 2017). Brazil fits this description,
presenting high social inequality, including in its main large cities (Regueira & Bernard, 2012), with
1,919 bird species cataloged so far, (Piacentini et al., 2015), many of them threatened (IUCN, 2016).
Thus, several studies have empirically pointed out to the prevalence of socioeconomic factors as the
best predictors for poacher participation in the avian trade in Brazil (e.g. Gama and Sassi, 2008;
Santos & Araujo 2015; Souto et al., 2017), as well as in other developing countries, such as Mexico
(González-Marín et al., 2016), Zimbabwe (Lindsey et al., 2011), Congo (Nasi et al., 2011), and
Nigeria (Atuo et al., 2015).
Native vegetation coverage was the most important driver for illegal wild bird captures in
Brazil considered in its entirety, as well as in the midwest and south/southeast regions. This had been
previously described in the Brazilian Cerrado, where the highest vegetation coverage index was
associated with greater biodiversity availability for harvesting by the resident population (Santos &
Araujo, 2015). In addition, the higher concentrations of protected areas also boost illegal capture in the
country in its entirety, as well as in the northeast and south/southeast regions, probably due to a higher
supply of specimens compared to unprotected sites, revealing a possible fragility of Brazilian
protected areas regarding poachers or trappers (Tebaldi et al., 2012; Carvalho Jr & Morato, 2013).
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These results do not corroborate the study developed by Wright et al. (2001), that detected that
Neotropical parrot poaching was higher in unprotected sites when compared to protected sites.
Low road density also positively influences illegal bird capture in Brazil, especially in the
north (Brazilian Amazon), which presents the lowest road density in the country and where rivers are
important means of transport for trafficked animals (Do Nascimento et al., 2015). In fact, the large
number of roadways and pathways favor bird captures, since it is more convenient to transfer the
animals to vehicles and trade them in public shops and street markets (Shepherd et al., 2007; Alves et
al., 2013a). However, in the long term, regions that display lower highway concentrations tend to
present higher fauna stocks, because roads make it easier to open forests for hunting, and may also
cause negative environmental effects, such as chemical and nutrient pollution, edge and barrier effects,
animal car accidents, invasion of exotic species and other impacts on local soil, hydrology and aquatic
ecosystems, especially if not previously planned (Laurance et al., 2009; Clements et al., 2014). Finally,
the most trafficked species richness was also noteworthy as an important driver for fauna capture in
the Brazilian north and midwest, as previously observed in Nigeria, where poachers have directed
efforts to areas that contain a higher number of species (Atuo et al., 2015). In fact, in the northern
Brazil region, most of the 10 species display a marginal distribution to the eastern Amazon, coinciding
with the location of source-municipalities, while in the midwest region they present a great overlap
with the Pantanal Biome, where most of the selected municipalities are located.
Contrary to our expectations, socioeconomic drivers were relevant only in northeastern Brazil,
the main animal supplier for illegal wildlife trade (Godoy & Matushima 2010), comprising 36.41% of
all summarized source-municipalities. A positive relationship between source-municipalities and
municipal human development index is noted, i.e., illegal fauna capture occurred mainly in the
municipalities presenting higher MHDI. This lack of relationship between low socioeconomic index
and captive birds has been pointed out in other studies (see Alves et al., 2013b), and indicates that the
demand for songbirds in Brazil presents a high cultural bias (Licarião et al., 2013; Souto et al., 2017)
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and is widespread among the local population, independent of socioeconomic factors (Alves et al.,
2016). This makes surveillance and enforcement difficult and time-consuming (Silva & Bernard,
2015). For Duffy et al., (2016), the relationship between poverty and illegal wildlife consumption
reveals that knowledge on this subject is limited and that conservationists should broaden their view of
what constitutes illegal wildlife trade, what motivates people to hunt illegally, and how to tackle the
problem. Thus, although illegal wildlife trade is frequently characterized as the result of economic
poverty or greed, links among wealth, poverty, and engagement in the wildlife trade are usually far
more complex (TRAFFIC, 2008; Duffy et al., 2016). In fact, besides bird colors, songs and behavior,
access to birds and cultural habits seem to have a direct influence on common bird captures in Brazil
(Alves et al., 2010; Souto et al., 2017), making the Brazilian internal trade the main target for animals
illegally collected from the wild (Destro et al., 2012). This interpretation was evident in our results,
since the seven drivers explained between 3.48% (northeast) and 10.85% (midwest) of the variations
observed among the “source-areas” and control group, revealing the participation of other variables,
immeasurable or described by literature. In fact, the low risk of detection, relatively small penalties,
and minimal consequences for perpetrating wildlife crime, allied with the lack of enforcement and
basic governance structures of local authorities are attractive incentives to participate in this illegal
activity (Ratchford et al., 2013), although difficult to measure and evaluate.
In sum, our results highlight that conservation measures for trafficked bird species should
incorporate interactions between natural, cultural and socioeconomic drivers, promoting actions
capable of reversing the current exploitation situation (e.g. Alves et al., 2013b; Tella & Hiraldo, 2014;
Atuo et al., 2015). Thus, in order to reverse illegal captures, it is essential to implement effective
public policies which involve education, policing/enforcement, the creation of alternative sources of
income, and pro-active ecosystem management and conservation (e.g. Fernandes-Ferreira et al., 2012;
Souza & Alves, 2014; Santos & Araujo, 2015), always under a multiple spatial scale approach
(Cumming et al., 2015; McGarigal et al., 2016). In fact, expert opinions suggest that only improving
the income or livelihood status of harvester communities often does not reduce their participation in
48/195
the wildlife trade (TRAFFIC, 2008) and well-intentioned policies that do not take into account
variations in different spatial dimensions may collapse at a local scale and, ultimately, fail to reduce
the risks associated with environmental insecurity and biodiversity exploitation (Gore et al., 2016).
In many countries, especially those located in tropical regions with great fauna diversity, the
illegal commerce of wild animals removes many species from their natural environments, certainly
one of the gravest threats to many native populations (Alves & Souto, 2015). In the present study, a
diagnostic-method capable of discriminating drivers related to illegal bird capture in supply countries
was presented. However, other factors should be diagnosed and evaluated in future studies, especially
those related to local and national governance power. In fact, illegal wildlife trade requires broader
debates on associated science and policy, since it has historically been focused on only a few high-
profile species (i.e. rhinoceros, tigers, elephants) and often overlooks or combines complex actors,
networks, and contexts (Phelps et al., 2016). Thus, understanding the dynamics related to wildlife
trafficking drivers is part of this transnational effort aiming at better geographically allocation of
conservation actions and resources worldwide, leading to more precise and effective public policies
for wildlife crime prevention and control.
Supplementary material S1
This paper contains supplementary data entitled "Main source municipalities for illegal capture of wild
animals in Brazil".
Acknowledgements
The authors would like to thank the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais
Renováveis (IBAMA) for supporting our research. LCT and PDMJ also thank the support provided by
CNPq Productivity grants.
49/195
Funding sources
This research did not receive any specific grant from funding agencies in the public, commercial, or
not-for-profit sectors.
Declarations of interest
None.
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Supplementary material S1
Main source-municipalities for the illegal capture of wild animals in Brazil
Region State Municipality Data Source
Midwest GoiásAlto Paraíso de
Goiás
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Midwest Goiás Bonópolis
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Midwest Goiás Campos Belos
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Midwest Goiás Cavalcante
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Midwest Goiás Colinas do Sul
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Midwest GoiásMonte Alegre
de Goiás
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Midwest Goiás Nova Roma
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Midwest GoiásSão Joãod'Aliança
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Midwest GoiásSão Miguel do
Araguaia
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
58/195
Midwest GoiásTeresina de
Goiás
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
GrossoBarão deMelgaço
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
GrossoCáceres
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
GrossoChapada dosGuimarães
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
GrossoCuiabá
RENCTAS (2001) Rede Nacional de Combate ao Tráfico de Animais Silvestres. 1º Relatório Nacional sobre o Tráfico de Fauna Silvestre. RENCTAS, Brasília, BRA. Http://www.renctas.org.br/wp-content/uploads/2014/02/REL_RENCTAS_pt_final.pdf [acessed 15 August 2016].
MidwestMato
GrossoCurvelândia
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
GrossoItiquira
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
GrossoNossa Senhorado Livramento
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
GrossoPoconé
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
GrossoSanto Antôniodo Leverger
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Midwest MatoGrosso do
Sul
Anastácio BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report.
59/195
Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Anaurilândia O ECO (2012) Começou a temporada do tráfico de papagaios. Http://www.oeco.org.br/noticias/26542-comecou-a-temporada-do-trafico-de-papagaios/ [acessed 15 March 2017].
MidwestMato
Grosso doSul
Aquidauana
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Bataguassu O ECO (2012) Começou a temporada do tráfico de papagaios. Http://www.oeco.org.br/noticias/26542-comecou-a-temporada-do-trafico-de-papagaios/ [acessed 15 March 2017].
MidwestMato
Grosso doSul
Batayporã O ECO (2012) Começou a temporada do tráfico de papagaios. Http://www.oeco.org.br/noticias/26542-comecou-a-temporada-do-trafico-de-papagaios/ [acessed 15 March 2017].
MidwestMato
Grosso doSul
Bela Vista
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Bodoquena
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Bonito
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Brasilândia O ECO (2012) Começou a temporada do tráfico de papagaios. Http://www.oeco.org.br/noticias/26542-comecou-a-temporada-do-trafico-de-papagaios/ [acessed 15 March 2017].
MidwestMato
Grosso doSul
Caracol
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Corguinho
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Corumbá
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Midwest MatoGrosso do
Sul
Coxim BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report.
60/195
Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Ivinhema O ECO (2012) Começou a temporada do tráfico de papagaios. Http://www.oeco.org.br/noticias/26542-comecou-a-temporada-do-trafico-de-papagaios/ [acessed 15 March 2017].
MidwestMato
Grosso doSul
Ladário
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Miranda
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Mundo Novo O ECO (2012) Começou a temporada do tráfico de papagaios. Http://www.oeco.org.br/noticias/26542-comecou-a-temporada-do-trafico-de-papagaios/ [acessed 15 March 2017].
MidwestMato
Grosso doSul
Naviraí O ECO (2012) Começou a temporada do tráfico de papagaios. Http://www.oeco.org.br/noticias/26542-comecou-a-temporada-do-trafico-de-papagaios/ [acessed 15 March 2017].
MidwestMato
Grosso doSul
NovaAndradina
O ECO (2012) Começou a temporada do tráfico de papagaios. Http://www.oeco.org.br/noticias/26542-comecou-a-temporada-do-trafico-de-papagaios/ [acessed 15 March 2017].
MidwestMato
Grosso doSul
NovoHorizonte do
Sul
O ECO (2012) Começou a temporada do tráfico de papagaios. Http://www.oeco.org.br/noticias/26542-comecou-a-temporada-do-trafico-de-papagaios/ [acessed 15 March 2017].
MidwestMato
Grosso doSul
Porto Murtinho
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Rio Negro
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Rio Verde deMato Grosso
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Santa Rita doPardo
O ECO (2012) Começou a temporada do tráfico de papagaios. Http://www.oeco.org.br/noticias/26542-comecou-a-temporada-do-trafico-de-papagaios/ [acessed 15 March 2017].
MidwestMato
Grosso doSul
Sonora
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Midwest Mato Três Lagoas O ECO (2012) Começou a temporada do tráfico de papagaios.
61/195
Grosso doSul
Http://www.oeco.org.br/noticias/26542-comecou-a-temporada-do-trafico-de-papagaios/ [acessed 15 March 2017].
North Pará Afuá
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Anajás
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Bagre
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Belém
RENCTAS (2001) Rede Nacional de Combate ao Tráfico de Animais Silvestres. 1º Relatório Nacional sobre o Tráfico de Fauna Silvestre. RENCTAS, Brasília, BRA. Http://www.renctas.org.br/wp-content/uploads/2014/02/REL_RENCTAS_pt_final.pdf [acessed 15 August 2016].
North Pará Bragança
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Breves
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North ParáCachoeira do
Arari
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North ParáCanaã dos
Carajás
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Chaves
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North ParáConceição do
Araguaia
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
62/195
North Pará Curralinho
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Gurupá
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Marabá
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Melgaço
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Muaná
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North ParáNovo
Repartimento
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North ParáOurilândia do
Norte
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Parauapebas
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North ParáPonta dePedras
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Portel
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Redenção BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report.
63/195
Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Salvaterra
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North ParáSanta Cruz do
Arari
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Santarém
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North ParáSão Félix do
Xingu
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North ParáSão Sebastiãoda Boa Vista
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Soure
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Xinguara
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Tocantins Araguaçu
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Tocantins Araguanã
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Tocantins Centenário
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
64/195
North TocantinsFormoso do
Araguaia
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North TocantinsLagoa daConfusão
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Tocantins Lizarda
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Tocantins Mateiros
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Tocantins Pium
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North TocantinsPonte Alta do
Tocantins
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Tocantins Recursolândia
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North TocantinsSanta Rosa do
Tocantins
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Tocantins Silvanópolis
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Alagoas Palestina
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Alagoas Pão de Açúcar BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report.
65/195
Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Alagoas Pariconha
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Bahia Amargosa
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Bahia BarreirasSouza, G.M. de & Soares Filho, A. de O. (2005) O comércio ilegal de aves silvestres na região do Paraguaçu e Sudoeste da Bahia. Enciclopédia Biosfera, 1, 1-10.
Northeast BahiaCampo
Formoso
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Bahia Canudos
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Bahia Cipó
RENCTAS (2001) Rede Nacional de Combate ao Tráfico de Animais Silvestres. 1º Relatório Nacional sobre o Tráfico de Fauna Silvestre. RENCTAS, Brasília, BRA. Http://www.renctas.org.br/wp-content/uploads/2014/02/REL_RENCTAS_pt_final.pdf [acessed 15 August 2016].
Northeast Bahia Cocos
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Bahia Curaçá
RENCTAS (2001) Rede Nacional de Combate ao Tráfico de Animais Silvestres. 1º Relatório Nacional sobre o Tráfico de Fauna Silvestre. RENCTAS, Brasília, BRA. Http://www.renctas.org.br/wp-content/uploads/2014/02/REL_RENCTAS_pt_final.pdf [acessed 15 August 2016].
Northeast BahiaEuclides da
Cunha
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast BahiaFeira deSantana
RENCTAS (2001) Rede Nacional de Combate ao Tráfico de Animais Silvestres. 1º Relatório Nacional sobre o Tráfico de Fauna Silvestre. RENCTAS, Brasília, BRA. Http://www.renctas.org.br/wp-content/uploads/2014/02/REL_RENCTAS_pt_final.pdf [acessed 15 August 2016].
Northeast Bahia Ibotirama Souza, G.M. de & Soares Filho, A. de O. (2005) O comércio ilegal de aves silvestres na região do Paraguaçu e Sudoeste da Bahia.
66/195
Enciclopédia Biosfera, 1, 1-10.
Northeast Bahia Itaberaba
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Bahia Jeremoabo
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Bahia JuazeiroSouza, G.M. de & Soares Filho, A. de O. (2005) O comércio ilegal de aves silvestres na região do Paraguaçu e Sudoeste da Bahia. Enciclopédia Biosfera, 1, 1-10.
Northeast BahiaLivramento deNossa Senhora
Souza, G.M. de & Soares Filho, A. de O. (2005) O comércio ilegal de aves silvestres na região do Paraguaçu e Sudoeste da Bahia. Enciclopédia Biosfera, 1, 1-10.
Northeast Bahia Mascote
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Bahia Milagres
RENCTAS (2001) Rede Nacional de Combate ao Tráfico de Animais Silvestres. 1º Relatório Nacional sobre o Tráfico de Fauna Silvestre. RENCTAS, Brasília, BRA. Http://www.renctas.org.br/wp-content/uploads/2014/02/REL_RENCTAS_pt_final.pdf [acessed 15 August 2016].
Northeast BahiaMorro doChapéu
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast BahiaRibeira do
Pombal
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Bahia Rio de ContasSouza, G.M. de & Soares Filho, A. de O. (2005) O comércio ilegal de aves silvestres na região do Paraguaçu e Sudoeste da Bahia. Enciclopédia Biosfera, 1, 1-10.
Northeast BahiaSanta Maria da
Vitória
Souza, G.M. de & Soares Filho, A. de O. (2005) O comércio ilegal de aves silvestres na região do Paraguaçu e Sudoeste da Bahia. Enciclopédia Biosfera, 1, 1-10.
Northeast Bahia Tucano
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Bahia Uauá BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/
67/195
[accessed 01 September 2017].
Northeast BahiaVitória daConquista
RENCTAS (2001) Rede Nacional de Combate ao Tráfico de Animais Silvestres. 1º Relatório Nacional sobre o Tráfico de Fauna Silvestre. RENCTAS, Brasília, BRA. Http://www.renctas.org.br/wp-content/uploads/2014/02/REL_RENCTAS_pt_final.pdf [acessed 15 August 2016].
Northeast Ceará Araripe
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Ceará Crateús
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Ceará Jati
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Ceará São Benedito
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Ceará Ubajara
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Maranhão Alto Parnaíba
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Maranhão Balsas
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast MaranhãoBarão deGrajaú
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Maranhão Buriticupu
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Maranhão Tasso Fragoso BRASIL (2003) Comissão Parlamentar de Inquérito destinada a
68/195
investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Maranhão Zé Doca
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Paraíba Alagoa GrandeGama, T.F. & Sassi, R. (2008) Aspectos do comércio ilegal de pássaros silvestres na cidade de João Pessoa, Paraíba, Brasil. Gaia Scientia, 2, 2, 01-20.
Northeast Paraíba Cabaceiras
Rocha, M. da S.P., Cavalcanti, P.C. de M., Souza, R. de L., Alves & R.R.N. (2006) Aspectos de comercialização ilegal de aves nas feiras livres de Campina Grande, Paraíba, Brasil. Revista de Biologia e Ciências da Terra, 6, 2, 204-221.
Northeast Paraíba Cajazeiras
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast ParaíbaCampinaGrande
Rocha, M. da S.P., Cavalcanti, P.C. de M., Souza, R. de L., Alves & R.R.N. (2006) Aspectos de comercialização ilegal de aves nas feiras livres de Campina Grande, Paraíba, Brasil. Revista de Biologia e Ciências da Terra, 6, 2, 204-221.
Northeast Paraíba Lagoa Seca
Rocha, M. da S.P., Cavalcanti, P.C. de M., Souza, R. de L., Alves & R.R.N. (2006) Aspectos de comercialização ilegal de aves nas feiras livres de Campina Grande, Paraíba, Brasil. Revista de Biologia e Ciências da Terra, 6, 2, 204-221.
Northeast Paraíba MamanguapeGama, T.F. & Sassi, R. (2008) Aspectos do comércio ilegal de pássaros silvestres na cidade de João Pessoa, Paraíba, Brasil. Gaia Scientia, 2, 2, 01-20.
Northeast Paraíba Patos
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Paraíba PilarGama, T.F. & Sassi, R. (2008) Aspectos do comércio ilegal de pássaros silvestres na cidade de João Pessoa, Paraíba, Brasil. Gaia Scientia, 2, 2, 01-20.
Northeast Paraíba Pombal
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Paraíba Queimadas
Rocha, M. da S.P., Cavalcanti, P.C. de M., Souza, R. de L., Alves & R.R.N. (2006) Aspectos de comercialização ilegal de aves nas feiras livres de Campina Grande, Paraíba, Brasil. Revista de Biologia e Ciências da Terra, 6, 2, 204-221.
Northeast Paraíba Remígio Rocha, M. da S.P., Cavalcanti, P.C. de M., Souza, R. de L., Alves & R.R.N. (2006) Aspectos de comercialização ilegal de aves nas feiras livres de Campina Grande, Paraíba, Brasil. Revista de Biologia e
69/195
Ciências da Terra, 6, 2, 204-221.
Northeast Paraíba Seridó
Rocha, M. da S.P., Cavalcanti, P.C. de M., Souza, R. de L., Alves & R.R.N. (2006) Aspectos de comercialização ilegal de aves nas feiras livres de Campina Grande, Paraíba, Brasil. Revista de Biologia e Ciências da Terra, 6, 2, 204-221.
Northeast Paraíba Serra Branca
Rocha, M. da S.P., Cavalcanti, P.C. de M., Souza, R. de L., Alves & R.R.N. (2006) Aspectos de comercialização ilegal de aves nas feiras livres de Campina Grande, Paraíba, Brasil. Revista de Biologia e Ciências da Terra, 6, 2, 204-221.
Northeast Paraíba Sousa
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Pernambuco Petrolândia
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Pernambuco Recife
RENCTAS (2001) Rede Nacional de Combate ao Tráfico de Animais Silvestres. 1º Relatório Nacional sobre o Tráfico de Fauna Silvestre. RENCTAS, Brasília, BRA. Http://www.renctas.org.br/wp-content/uploads/2014/02/REL_RENCTAS_pt_final.pdf [acessed 15 August 2016].
Northeast Pernambuco Salgueiro
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Pernambuco Serra Talhada
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast PiauíBarreiras do
Piauí
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Piauí Canto do Buriti
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Piauí Corrente
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Piauí Floriano BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report.
70/195
Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Piauí Gilbués
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Piauí Guadalupe
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast PiauíMonte Alegre
do Piauí
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Piauí Piripiri
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast PiauíSanta
Filomena
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast PiauíSão Gonçalodo Gurguéia
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
NortheastRio Grande
do NorteCaicó
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
NortheastRio Grande
do NorteCurrais Novos
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
NortheastRio Grande
do NorteJardim do
Seridó
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Sergipe Cristinápolis
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
71/195
Northeast SergipeNossa Senhora
da Glória
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Sergipe Tobias Barreto
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
South Paraná Céu AzulHernandez, E.F.T. & Carvalho, M.S. de (2006) O tráfico de animais silvestres no Estado do Paraná. Acta Scientiarum. Human and SocialSciences, 28, 2, 257-266.
South Paraná Foz do IguaçuHernandez, E.F.T. & Carvalho, M.S. de (2006) O tráfico de animais silvestres no Estado do Paraná. Acta Scientiarum. Human and SocialSciences, 28, 2, 257-266.
South Paraná GuaraqueçabaHernandez, E.F.T. & Carvalho, M.S. de (2006) O tráfico de animais silvestres no Estado do Paraná. Acta Scientiarum. Human and SocialSciences, 28, 2, 257-266.
South Paraná MatelândiaHernandez, E.F.T. & Carvalho, M.S. de (2006) O tráfico de animais silvestres no Estado do Paraná. Acta Scientiarum. Human and SocialSciences, 28, 2, 257-266.
South Paraná MedianeiraHernandez, E.F.T. & Carvalho, M.S. de (2006) O tráfico de animais silvestres no Estado do Paraná. Acta Scientiarum. Human and SocialSciences, 28, 2, 257-266.
South ParanáSão Miguel do
Iguaçu
Hernandez, E.F.T. & Carvalho, M.S. de (2006) O tráfico de animais silvestres no Estado do Paraná. Acta Scientiarum. Human and SocialSciences, 28, 2, 257-266.
SouthRio Grande
do SulRio Grande
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
SouthRio Grande
do SulSant' Ana doLivramento
Hernandez, E.F.T. & Carvalho, M.S. de (2006) O tráfico de animais silvestres no Estado do Paraná. Acta Scientiarum. Human and SocialSciences, 28, 2, 257-266.
SouthRio Grande
do SulSanta Vitória
do Palmar
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
SoutheastMinasGerais
Almenara
RENCTAS (2001) Rede Nacional de Combate ao Tráfico de Animais Silvestres. 1º Relatório Nacional sobre o Tráfico de Fauna Silvestre. RENCTAS, Brasília, BRA. Http://www.renctas.org.br/wp-content/uploads/2014/02/REL_RENCTAS_pt_final.pdf [acessed 15 August 2016].
SoutheastMinasGerais
Arinos
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
72/195
SoutheastMinasGerais
Buritis
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
SoutheastMinasGerais
ChapadaGaúcha
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
SoutheastMinasGerais
Formoso
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
SoutheastMinasGerais
Urucuia
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Apiaí
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São PauloBarra doChapéu
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Barra do Turvo
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Cajati
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Cananéia
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Eldorado
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Iguape BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report.
73/195
Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Ilha Comprida
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Iporanga
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Itaóca
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São PauloItapirapuãPaulista
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Itariri
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Jacupiranga
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Juquiá
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Juquitiba
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Miracatu
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Pariquera-Açu
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
74/195
Southeast São PauloPedro deToledo
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Registro
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Ribeira
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São PauloRibeirãoBranco
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São PauloSão Lourenço
da Serra
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Sete Barras
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Tapiraí
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
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Capítulo 2
Predicting invasion risks for the
most seized bird species in Brazil
Guilherme Fernando Gomes Destro, André Felipe Alves de Andrade,
Levi Carina Terribile e Paulo De Marco
Artigo submetido à revista “IBIS - The International Journal of Avian Science”
em julho de 2018
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Predicting invasion risks for the most seized bird species in Brazil
Short running page heading: Invasion risks for seized bird species in Brazil
1,2Guilherme Fernando Gomes Destro*, 1André Felipe Alves de Andrade, 3Levi Carina Terribile, 4Paulo
De Marco
1. Programa de Pós-Graduação em Ecologia e Evolução, Universidade Federal de Goiás, Campus
Samambaia, CP 131, 74001-970, Goiânia, GO, Brazil.
2. Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis, Superintendência no
Estado de Goiás, Rua 229, nº 95 – Setor Leste Universitário, 74605-090 – Goiânia, GO, Brazil.
3. Instituto de Ciências Biológicas, Universidade Federal de Goiás, Regional Jataí, 75801-615, Jataí,
GO, Brazil.
4. Departamento de Ecologia, Instituto de Ciências Biológicas, Universidade Federal de Goiás,
Campus Samambaia, CP 131, 74001-970, Goiânia, GO, Brazil.
*email address: [email protected]
Abstract: Wildlife trade is considered one of the most significant pathways for the spread of exotic
species, as it is present worldwide and crosses abiotic and biotic barriers. In this sense, identifying
potential invaders before they are introduced and analyzing the ecological implications of possible
escapes of captive species to the wild is an important issue for preventing invasive species impacts. In
Brazil, several studies have demonstrated the consequences of wildlife trade on the biogeographic
patterns of some species. However, the link between wildlife trade and biological invasion processes is
still poorly understood. In this context, the invasion risks of the ten most seized bird species in Brazil
were evaluated, seeking to identify the most susceptible areas for invasion in Brazilian regions, as well
as in other South American countries. To this end, we used an ecological niche modeling to evaluate
region invasibility by the ten assessed species. In addition, natural distribution polygons and actual
records were used to evaluate changes in the distribution ranges of the evaluated species. Overall,
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‘Red-cowled Cardinal’, ‘Saffron Finch’, ‘Yellow-bellied Seedeater’ and ‘Rufous-collared Sparrow’
reached the highest rate of potential invasion inn susceptible areas. Proportionally, French Guiana,
Guyana and Suriname showed the highest amount of potential areas for invasion in South America.
Ecuador and Bolivia reached the highest percentage of suitable areas for four or more species.
Regarding Brazil, all regions were suitable for potential invasion by at least three of the ten analyzed
species, whereas the north and midwest were the most vulnerable regions. We discuss the need to
consider the animal trade as one of the main means to promote organism translocation and cause
alterations in the biogeographical patterns of several species.
Keywords: Animal trade; Animal trafficking; Ecological Niche Modeling – ENM; Ensemble; Invasive
species; Passerine
Introduction
The wildlife trade, one of the most spread out and profitable activities worldwide (e.g. Smith
et al. 2017; Duffy 2016; Ratchford et al. 2013; Barber-Meyer 2010), shifts hundreds of millions of
plants and animals annually (UNODC 2016; Nijman 2010; Broad et al. 2003). In both the legal or
illegal trade, birds are most strongly associated to Central and South America, mammals to Africa and
Asia, reptiles to Europe and north America, and corals with Oceania (UNODC 2016). Wild species are
used as the source of a wide variety of goods, including as food, medicine, pets, display, fashion and
cultural items, industrial resins and extracts, and household items (Dai and Zhang 2017; TRAFFIC
2008). The legal sustainable trade can provide an important income for rural communities and
developing nations, while conserving wild populations (Nijman 2010; Cooney and Jepson 2006).
Notwithstanding the issue of legality (see López-Bao et al. 2015; Lawson and Vines 2014; Ratchford
et al. 2013), unregulated or illegal wildlife trade can generates serious environmental consequences,
including introduction of exotic species, spread of wildlife diseases, disruption of ecosystem processes
and ecological services, such as pollination, seed dispersal, population control of other animals and, in
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the medium and long-term ranges, the extinction of exploited species (e.g. Dai and Zhang 2017; Do
Nascimento et al. 2015; Fernandes-Ferreira et al. 2012). In fact, the wildlife trade has been considered
one of the most important causes of global biodiversity loss (Broad et al. 2003) and, given its
magnitude and impacts on conservation, more studies in this regard must be carried out, thereby
generating knowledge for decision-making and tools to manage and supervise this activity (Kuhnen et
al. 2012; Regueira and Bernard 2012).
Brazil has one of the richest avifauna in the world (Marini and Garcia 2005), and its biological
and cultural diversity make it an exceptional location for examining live wildlife trade and its
implications for wildlife conservation (Alves et al. 2013a). In this sense, bird-keeping activity,
especially songbirds, has been preserved through the centuries across social classes and is widespread
in both urban and rural regions (e.g. Alves et al. 2013a; Kuhnen et al. 2012; Alves et al. 2010).
Passeriformes are one of the most coveted order by breeders (e.g. Do Nascimento et al. 2015; Licarião
et al. 2013; Regueira and Bernard 2012), due to the their plumage beauty, shape, and song melody
(e.g. Teixeira et al. 2014; Licarião et al. 2013; Fernandes-Ferreira et al. 2012). According to the
Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis - IBAMA, more than three
million passerine bird specimens belonging to 144 species have been bred in Brazil (IBAMA 2018).
Saltator similis (Green-winged Saltator), Sporophila angolensis (Chestnut-bellied Seed-Finch),
Sporophila caerulescens (Double-collared Seedeater), and Sicalis flaveola (Saffron Finch) are the
most coveted species by authorized breeders (IBAMA 2013), corresponding to almost 70% of captive
specimens (IBAMA 2018). Geographically, 88% of legally captive birds in Brazil are concentrated in
the south and southeastern regions (IBAMA 2018), the most rich Brazilian areas, with the highest
consumer market for pet birds in the country.
Several studies point out that the majority of birds marketed in Brazilian cities come from
unauthorized capture in nature, mainly in the north, northeast and midwest regions (e.g. Alves et al.
2010; Godoy and Matushima 2010; Ferreira and Glock 2004). Once captured, illegal birds are either
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delivered to traders, who negotiate the specimens in public markets and fairs (Licarião et al. 2013;
Regueira and Bernard 2012), or smuggled by middlemen to the south and southeast regions by federal
highways before reaching final consumers (Destro et al. 2012). In other cases, wild animals are sent by
intermediary traffickers to authorized and unauthorized breeders and enterprises (Kuhnen et al. 2012;
Destro et al. 2012), who subsequently negotiate the specimens through the internet to every corner of
the country (Souto et al. 2017; Alves et al. 2013a), evidencing a significant relationship between
authorized bird breeding and wild animal trafficking (IBAMA 2013). In the same way as in the legal
trade, Thraupidae, which received the most genera from the former Emberizidae (Barker et al. 2013),
is the most coveted trafficked bird family (e.g. Licarião et al. 2013; Fernandes-Ferreira et al. 2012;
Regueira and Bernard 2012) and represent the most frequent bird species seized by police forces
(Destro et al. 2012).
In this sense, although the most trafficked species in Brazil are categorized as "Least Concern"
by IUCN (2017) and display a wide geographic distribution (Sick 1997), many present severe
population decreases, and some became locally extinct (Freitas et al. 2015; Fernandes-Ferreira et al.
2012; Gama and Sassi 2008). Thus, regardless of how birds are acquired or their geographic
distribution range, it is possible to find several bird species in both authorized and unauthorized
Brazilian breeders, many from different regions of the country (e.g. Alves et al. 2016; Do Nascimento
et al. 2015; Rocha et al. 2006; Ferreira and Glock 2004) and even from other countries (Fernandes-
Ferreira et al. 2012; Kuhnen et al. 2012). This situation is worrying, as pets can escape or be
abandoned (e.g. Kuhnen and Kanaan 2014; Ferronato et al. 2009; Silva and Oren 1990) and, back in
wild, may establish themselves in areas other than their original habitats (e.g. Fernandes-Ferreira et al.
2012; Bertolino 2009; Leven and Corlett 2004; Fontoura et al 2013). In fact, inter-regional and
international animal trades, allied to a lack of appropriate care by their managements, increase the
possibility of nonindigenous species introduction (Fernandes-Ferreira et al. 2012; Van Wilgen et al.
2010; Cassey et al. 2004).
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To become harmful and be considered invasive, a nonindigenous species must spread from its
point of introduction and become abundant, i.e., overcoming four different stages throughout the
introduction pathway: (i) transport; (ii) release; (iii) establishment; and, (iv) spread (Kolar and Lodge
2001). Besides generating enormous costs to agriculture, forestry, fisheries and other human
enterprises (Wittenberg and Cock 2001), invasive species may also cause numerous ecological
problems, such as pathogen dissemination, genetic loss by hybridization and introgression,
interspecific competition and species extinction, as well as impacts in ecosystem processes through
hydrology, fire regime and nutrient cycling modifications (Gama and Sassi 2008; Allendorf et al.
2001; Wittenberg and Cock 2001). The most seized birds in Brazil display certain characteristics that
make them more apt for establishment as alien or invasive birds compared to other species, such as a
wide range of habitat use in their native distribution range, feeding in flocks or small groups,
displaying wide climatic tolerance, nesting and roosting in alien vegetation, and being passerine (Dean
2000). Thus, as invasive birds, these species can cause serious impacts on native ecosystems and
humans, and their presence could compound the survival pressures on avifauna through predation,
disturbance or competition for resources (Yap and Sodhi 2004; Stiels et al. 2011; Miller et al. 2016). In
fact, the correct diagnosis of invasion status is necessary to understand natural biodiversity patterns
and changes, as well as for proposing measures to ensure the conservation of native species (Fontoura
et al. 2013).
Although the link between wildlife trade and biological invasion processes is still poorly
understood (García-Díaz et al. 2015), widespread and abundant species are more likely to be
encountered by trappers, marketed and become free, either accidentally or deliberately (Cassey et al.
2004; Duncan et al. 2001). Moreover, the risk of a species becoming invasive is increased by higher
propagule pressure, habitat matching and number of release events (e.g. Van Wilgen et al. 2010;
Bertolino 2009; Kolar and Lodge 2001; Duncan et al. 2001). In this sense, identifying potential
invaders before they are introduced and analyzing the ecological implications of possible captivity
escapes to the wild is applied to prevent invasive species impacts (e.g. Rosa et al. 2018; Alves et al.
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2010; Kolar and Lodge 2001). In the present study, invasion risks of the ten most seized bird species in
Brazil were evaluated, seeking to identify the most susceptible areas concerning potential invasion in
both Brazilian regions and other South American countries. Thus, using the most seized bird species in
Brazil as surrogates, we offer a general insight in order improve management strategies and laws
aimed at controlling the wildlife trade in source-countries.
Methods
Species occurrence records and environmental layers
The ten most seized bird species in Brazil were selected (Destro et al. 2012; Table 1),
corresponding to over 60% of the wild specimens seized in the country from 2005 to 2009 (Destro et
al., unpublished data). A total of 187,955 occurrence records from the following online databases were
gathered: (i) CRIA Species Link (http://splink.cria.org.br/); (ii) Global Biodiversity Information
Facility (http://www.gbif.org/); and, (iii) VertNet (http://vertnet.org/). Records with geographic
location errors (e.g. located outside the study area or in the ocean) were excluded through the use of
ArcGis 10.2.2 for Desktop software (ESRI 2014). Bird nomenclature follows the Brazilian
Ornithological Records Committee (Piacentini et al. 2015), although, synonyms such as Cyanocompsa
brissonii (Lichtenstein, 1823), Passerina brissonii Stotz et al. (1996) and Oryzoborus angolensis
(Linnaeus, 1766) were also used. In addition, to reduce spatial autocorrelation, the SDMToolBox 2.1.0
extension for ArcGis (http://sdmtoolbox.org/) was applied, to exclude dubious records and establish a
minimum distance of 20 km among records of the same species, avoiding the analysis of contiguous
cells (cell size grid = 10 km). In the end, a total of 12,047 occurrence points without subspecies
distinction were used, with ‘Rufous-collared Sparrow’ (Zonotrichia capensis) presenting the highest
number of records (4,069) and ‘Red-cowled Cardinal’ (Paroaria dominicana), the lowest (184).
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Table 1. Most seized wild bird species in Brazil between 2005 and 2009. Conservation status was obtained from
IUCN (2017).
Family Specie Author Common nameConservation
statusAmount of
records
Thraupidae Sicalis flaveola (Linnaeus, 1766) Saffron Finch Least Concern 2,530
Thraupidae Saltator similisd'Orbigny and
Lafresnaye, 1837Green-winged
SaltatorLeast Concern 581
ThraupidaeSporophila
caerulescens(Vieillot, 1823)
Double-collaredSeedeater
Least Concern 1,132
Cardinalidae Cyanoloxia brissonii (Lichtenstein, 1823)UltramarineGrosbeak
Least Concern 558
ThraupidaeSporophilaangolensis
(Linnaeus, 1766)Chestnut-bellied
Seed-FinchLeast Concern 755
Icteridae Gnorimopsar chopi (Vieillot, 1819) Chopi Blackbird Least Concern 824
Thraupidae Paroaria dominicana (Linnaeus, 1758)Red-cowled
CardinalLeast Concern 184
Thraupidae Sporophila lineola (Linnaeus, 1758) Lined Seedeater Least Concern 492
Passerellidae Zonotrichia capensis(Statius Muller,
1776)Rufous-collared
SparrowLeast Concern 4,069
ThraupidaeSporophilanigricollis
(Vieillot, 1823)Yellow-bellied
SeedeaterLeast Concern 922
All the 19 WorldClim dataset environmental layers (http://worldclim.com/), as well as altitude,
FLOW and SLOPE relief variables elaborated using the ArcGis 10.2.2 software (ESRI 2014), were
used to derive principal components (PCs) through a Principal Components Analysis (PCA). In this
sense, in order to decrease the collinearity among environmental variables, but also to avoid model
overfitting that may result in biologically unreliable areas (Jiménez-Valverde et al. 2011), eight PCs
were select as new environmental layers during the modeling procedures (Silva et al. 2014a; Silva et
al. 2014b), reaching more than 96% of the original set variation.
Ecological Niche Models (ENM)
Ecological niche modeling (ENM) is widely applied to estimate the coarse-resolution
environmental requirements of species, which can be projected to real-world landscapes in order to
identify regions where these requirements are manifested (Barve et al. 2011). Thus, based on the
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observed occurrences of the target species and on the environmental variables correlated with these
records, computational algorithms create a multidimensional environmental space that infers niche
parameters and predict species distributions (e.g. Elith and Leathwick 2009; Araújo and Guisan 2006;
Soberón and Peterson 2005). Herein, the ecological niche of the ten most seized bird species in Brazil
were initially assessed considering eight different modeling algorithms: i) Bioclimatic Envelope
Method – BioClim (Beaumont et al. 2005); ii) Generalized Additive Model – GAM (Hastie and
Tibshirani 1986); iii) Gaussian Model (Golding and Purse 2016); iv) Generalized Linear Model –
GLM (Guisan et al. 2002); v) Maxent, with default features - MaxNet (Phillips et al. 2006; Philips et
al. 2017); vi) Simple Maxent Model (Williams 2010); vii) Random Forest – RDF (Breiman 2001);
and, viii) Support Vector Machine – SVM (Tax and Duin 2004). All models were trained with the
“ENM_TheMetaLand” script (https://github.com/andrefaa/ENM_TheMetaLand), developed by the
Metacommunities and Landscapes Ecology Laboratory at the Universidade Federal de Goiás, Brazil,
and implemented in the “R” software (R Core Team 2017). Simulations were performed for each
species through the combinations of different parameters: (i) Pseudo-absence selection method; (ii)
Data partitioning method; (iii) Threshold; and (iv) Ensemble, with the selection of those who reached
better solutions according to the evaluated species (see Supplementary material S1). All modeling
procedures were performed considering the entire Neotropical region, aiming to cover the maximum
range of the evaluated species. The grid for all variables was set at a 5 arc-min resolution (0.083o ≈ 10
km).
The Area Under the Receiver–operator Curve (AUC) and True Skilled Statistics (TSS;
Allouche et al. 2006) were used to assess model performance (Liu et al., 2011). Both AUC and TSS
account for the sensitivity (quantifying omission errors) and specificity (quantifying commission
errors) of the models (Allouche et al. 2006). The AUC is a threshold-independent statistic analysis
ranging from 0 to 1, where values around 0.5 represent distribution models no better than random and
values around 1, representing a perfect fitting between the observed and the predicted species
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distribution. Acceptable distribution models exhibit values higher than 0.7. On the other hand, TSS is a
threshold-dependent statistical analysis that varies from −1 to +1 (Allouche et al. 2006). TSS values
near 0 or negative represent distributions no better than random, while values equal to +1 represent a
perfect agreement between the observed and the predicted distribution. Acceptable models considering
these statistics reach at least 0.5, while excellent models reach a minimum of 0.7, similar to what is
employed in AUC statistics (Fielding and Bell 1997).
Only presence data were used to elaborate the final models. Moreover, despite the usual
recommendation of using the lowest presence threshold – LPT (Pearson et al. 2007) to generate the
presence/absence distribution matrices (binary maps) of the modeled exotic species (Jiménez-Valverde
et al. 2011; Pearson et al. 2007), we chose to cut the modeled suitability matrices at the highest
sensitivity and specificity sum threshold (Vale et al. 2014; Ferraz et al. 2012), reducing the risk of
choosing unsuitable sites (Pearce and Ferrier 2000). This conservative strategy was adopted because
the species investigated herein are well sampled and abundant throughout the entire study area (see
Sick 1997). Finally, given the overall biases and uncertain nature of species distribution models (Zhu
and Peterson 2017; Diniz-Filho et al. 2009), the mean consensus of the models with above-average
TSS was used to elaborate the final maps. In fact, although consensus models do not outperform
individual models, they can reflect the central tendency of individual models, reducing uncertainties
by consolidating consistency across individual models (Zhu and Peterson 2017; Araújo and New
2007).
Invasion risk analysis
Three datasets were used to evaluate invasion risks: i) Suitability maps – SM; ii) Natural
distribution polygons (BirdLife 2016) – ND, and; iii) Actual records of the most seized bird species
(WikiAves 2008) – AR. Thus, we calculated the potential invasion risk in South America and Brazilian
regions through the difference between SM and ND for each species and sum of all resulting maps,
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i.e., we obtained the suitable areas still not colonized by the analysed species. In this sense, invasion
risk was classified into four classes, according to the amount of nonindigenous species: (i) one species;
(ii) two; (iii) three; and, (iv) four or more. Furthermore, the average suitability was also calculated for
each Brazilian region or country. All spatial analyses were performed using the ArcGis 10.2.2 software
(ESRI 2014). Later, through a comparison between ND and AR, current changes in species'
distribution were identified, and scenarios for geographical expansion were discussed. Actual records
were also used for external model validation. In this sense, the importance of collaborative sites such
as WikiAves (WikiAves 2008), that provides free and updated information on species occurrence, as
well as the bird-watching community, an important tool to gather information and support
conservation efforts, are highlighted (García-Moreno et al. 2007).
Results
The final models we produced reached TSS values that ranged from 0.52 to 0.98, while the
AUC values ranged from 0.71 to 1 (see Supplementary material S2), demonstrating the good
predictive capability of the ENMs (Fielding and Bell 1997; Metz 1986). Training-test subsets values
for spatial autocorrelation (Moran's I index) and MESS (Multivariate Environmental Similarity
Surface) are also presented as Supplementary material S3. Almost all ND were contained in suitable
areas (SM) (Fig. 1), indicating that, besides their predictive accuracy, all models were biologically
relevant. Some species such as ‘Red-cowled Cardinal’, ‘Saffron Finch’, ‘Yellow-bellied Seedeater’
and ‘Rufous-collared Sparrow’ reached much greater suitable areas than ND, i.e., these species present
a higher amount of potential invasion areas. Indeed, comparing ND and AR, the results indicate that
the current polygons proposed by BirdLife have already been overcome by some species, such as
‘Saffron Finch’ and ‘Yellow-bellied Seedeater’ in the Amazon region, and ‘Red-cowled Cardinal’ in
southeastern Brazil (Fig. 1).
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All South American countries showed a certain amount of invasion risk by the most seized
bird species in Brazil, i.e., presenting suitable areas not yet invaded by at least one of the species
analyzed herein (Fig. 2). In this sense, French Guiana, Guyana and Suriname showed the greatest
amount of available areas for invasion while Chile reached the lowest (Fig. 3). Ecuador and Bolivia
presented the highest percentage of suitable areas for four or more species. Regarding Brazil, all
regions showed suitable areas for invasion by at least three of the ten analyzed species (Fig. 4). The
north and midwest regions displayed the highest amount of suitable areas, whereas the north region
reached the greatest available area for potential invasion by a greater number of species (four or
more). In contrast, the northeastern region showed one of the lowest percentage of suitable areas not
yet colonized by the most seized species. As expected, in the south and southeast regions, where are
the main natural distribution areas of the species evaluated, the potential invasion was the lowest.
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a b c d
e f g h
i j
Fig. 1 Suitability map by the ten most seized bird species in Brazil. Warm colors represent highsuitability (SM) and hatching represents the natural species distribution (ND). The actual records ofthe bird species (AR) were reached in the smaller squares. Species: (a) Cyanoloxia brissonii; (b)Gnorimopsar chopi; (c) Paroaria dominicana; (d) Sporophila angolensis; (e) Sporophila caerulescens;(f) Sicalis flaveola; (g) Sporophila lineola; (h) Sporophila nigricollis; (i) Saltator similis; and, (j)Zonotrichia capensis
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Fig. 2 Invasion risks in South America by the ten most seized bird species in Brazil
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Fig. 3 Average suitability and potential area (%) in South American countries for invasion by the ten
most seized species in Brazil. Legend: columns = amount of nonindigenous species; line = average
suitability
Fig. 4 Average suitability and potential area (%) in Brazilian regions for invasion by the ten most
seized species in Brazil. Legend: columns = amount of nonindigenous species; line = average
suitability
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Discussion
Overall, the most coveted bird species in Brazil reached suitable areas in all Brazilian regions
and South American countries, although varying in variable intensity and response. In this sense, Chile
showed the lowest amount of suitable areas, whereas the Amazon region, where bird pet breeding is
still not much coveted due to cultural issues (Do Nascimento et al. 2015), was the most vulnerable
area, with a significant suitability area still not been colonized by certain species, such as the ‘Red-
cowled Cardinal’, ‘Saffron Finch’, and ‘Rufous-collared Sparrow’. In fact, although the wildlife trade
has been considered one of the most significant pathways for the spread of exotic species (Dai and
Zhang 2017; Kolar and Lodge 2001), as it occurs worldwide (UNODC 2016) and crosses abiotic and
biotic barriers (Richardson et al. 2000), understanding its impacts and relationships to biological
invasions is still a complex task (García-Díaz et al. 2015).
Previous studies in Brazil have demonstrated the influence of the wildlife trade on changes in
the biogeographic patterns of certain native bird species (Alves et al. 2013a). For example, the ‘Red-
cowled Cardinal’, a species originally endemic and very abundant in northeastern Brazil (Alves et al.
2016), is easily found in the wild in southern and southeastern Brazil regions (Sick 1997; Ferreira and
Glock 2004; Fontoura et al 2013), in some areas in the north region (Silva and Oren 1990; Fontoura et
al 2013) and even in Africa (Dean 2000). In Brazil, the genus Paroaria is divided into two species
complexes or superspecies: (i) P. dominicana (northeastern Brazil) and P. coronata (meridional
representative of the group); (ii) P. gularis (Amazon), P. baeri (Central Brazil) e P. capitata
(meridional representative of the group) (Sick 1997). Thus, in case its geographical barriers are
eliminated, group members may reproduce with each other and generate fertile hybrids (Sick 1997).
On the other hand, the ‘Chopi Blackbird’, ‘Ultramarine Grosbeak’, and ‘Rufous-collared Sparrow’,
although widely coveted by the legal and illegal trade for centuries (Alves et al. 2016), have not yet
expanded their distribution beyond their original range (Fig. 1).
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Translocations derived from the animal trade reveal a serious concern, namely inter and
intraspecific hybridization. According to Rhymer and Simberloff (1996), hybridization is the
interbreeding of individuals from what are believed to be genetically distinct populations, regardless of
taxonomic status. In some cases, interpopulation hybrids can suffer a reduction in fitness relative to the
parental types, a process termed Outbreeding Depression – OD, affecting intrinsic interactions
between genes or interactions between genes and environment (Edmands 2007; Waller 2015;
Allendorf et al. 2001). The ‘Saffron Finch’, one of the most coveted species by the Brazilian bird trade
(e.g. Freitas et al. 2015; Alves et al. 2013b; Regueira and Bernard 2012) and already considered
potentially invasive in south Africa, as it outcompetes indigenous bird species (ISSA 2018),
historically comprises four isolated subspecies in South America (Clements et al. 2017; Silveira and
Méndez 1999) that may be intermingling due to intense and unrestricted trade: (i) S. flaveola
brasiliensis (Brazil); (ii) S. flaveola pelzelni (Brazil, Bolivia, Paraguay, Argentina and Uruguay); (iii)
S. flaveola valida (Ecuador and Peru); and iv) S. flaveola flaveola (Colombia, Venezuela, Suriname,
Guyana, French Guiana and Trinidad and Tobago).
Regarding interspecific hybridization, several cases have been cited in the literature, including
for species belonging to the Sporophila and Cyanoloxia genera (Sick 1997). In other situations,
increased anthropogenic hybridization has caused the extinction of many taxa (species, subspecies and
locally adapted populations) by both replacement and genetic mixing (Allendorf et al. 2001).
However, several authors assert that the introduction of novel genetic variants into small or genetically
depauperate wild populations have, over multiple generations, been shown to augment genetic
diversity, reverse indications of inbreeding depression, and increase population size in a range of other
animal taxa (Frankham 2015; Frankham et al. 2011; Madsen et al. 1999). Moreover, empirical data has
indicated that the predicted OD probability in crosses between two populations comprising the same
species is low for populations with the same karyotype, isolated for <500 years, and that occupy
similar environments (Frankham et al. 2011). In fact, the distinction between natural and
anthropogenic hybridization is of primary importance (Allendorf et al. 2001) and that, in the face of
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uncertainty, conservation biologists have preferred to respect genetic identity, shying away from
routinely cross-breeding populations (Waller 2015).
In this study, we also evaluated the invasion risk of four species belonging to the Sporophila
genus, namely S. angolensis (Chestnut-bellied Seed-Finch), S. nigricollis (Yellow-bellied Seedeater),
S. caerulescens (Double-collared Seedeater), and S. lineola (Lined Seedeater). This genus attracts
breeders not only due to a beautiful song, but also because these birds are commercially cheap and
easy to manage (Souto e al. 2017; Rocha et al. 2006; Gama and Sassi 2008). Encouraging the trade of
common species increases their invasion risk through higher propagule pressure, since they are more
likely to be abundant and, thus, cheaper, increasing the likelihood of being released when owners tire
of the pet (Van Wilgen et al., 2010). In fact, the availability of individuals for transport and release
seems to be most important factor for undergoing these stages, although establishment success seems
to be higher for sedentary species and for those exhibiting broad diets (Cassey et al. 2004). All species
of genus Sporophila reached a low invasion risk in South America except for ‘Yellow-bellied
Seedeater’, as these species have already occupied almost the entire suitable and available area. In this
sense, ‘Yellow-bellied Seedeater’ expansion to suitable areas in the Amazon region is already taking
place (Fig. 1), even though this is the region exhibiting the lowest bird pet pressure in Brazil (Do
Nascimento et al. 2015). Thus, considering this taxa particularity, detailed studies on introduction
pathways for each species are required, in order to identify specific characteristics of potential
invaders that can subsequently reduce current rates of biotic homogenization (Cassey et al. 2004).
Moreover, there is a need to further understand the scale and breadth of the legal and illegal trade
related to species that, although are not considered global conservation flagships, are the most coveted
for commercial transactions (Gray et al. 2017).
Considering the extent of the damage, tighter measures to restrict wildlife trade may be
necessary to control the introduction of potentially invasive nonindigenous species (Alves et al.
2013a), especially in the entry pathways and concerning the risks related to species establishment
93/195
(Bertolino 2009). In fact, considering the key role that the propagule number has in the establishment
success of exotic species (e.g. Van Wilgen et al. 2010; Bertolino 2009; Forsyth et al. 2004; Duncan et
al. 2001), actions to prevent introductions should focus not only on the attributes of the species and
jurisdiction, but, critically, also on reducing the number of commercialized specimens and kept as pets
(García-Díaz et al. 2015; Kolar and Lodge 2001). Internationally, the Convention on International
Trade in Endangered Species of Wild Fauna and Flora (CITES) is considered the main instrument for
controlling world wildlife trade (Duffy 2016; Nijman 2010). It strongly influences national legislations
on wildlife crime, provides a cooperation framework to protect and regulate the international trade for
over 35,000 protected species and requires its parties to penalize trades carried out in violation of the
agreement (UNODC 2016). However, the actual problem originates when wildlife, not listed under
CITES, is taken illegally from one country and transported to another (UNODC 2016). In this sense,
Guyana, French Guiana and Suriname are the highest priority, as they display a greater extent of
climatically suitable habitats and, consequently, are more susceptible to the introduction of exotic
species from Brazil (Duncan et al. 2001; Forsyth et al. 2004). In fact, the likelihood of establishment
of a species outside its historical distribution increases when the latitudinal distance between donor
and recipient areas is low or when rough differences in climate and habitats do not exist (Bertolino
2009).
Scientists have already reported several damages caused by biological invasion, considered
one of the main global concerns and primary threats to global biodiversity (e.g. Clavero and García-
Berthou 2005). Similarly, many studies have focused on the impacts of animal trade, especially in
developing countries like Nigeria (Atuo et al. 2015), Cambodia (Gray et al. 2017), Peru (Gastañaga et
al. 2011), China (Dai and Zhang 2017; Leven and Corlett 2004) and Indonesia (Jepson and Ladle
2005). However, the knowledge of spatiotemporal distribution of biodiversity is still very incomplete
in the tropics, and is one of the major problems for preventing the assessment and effectiveness of
conservation actions (Carvalho et al. 2017). In this sense, ecological niche modeling, considered the
most effective way to evaluate the potential geographical species distribution (Vaz et al. 2015), has
94/195
been widely applied to predict the impacts of invasive species worldwide (e.g. Mainali et al. 2015;
Kulhanek et al. 2011; Peterson et al. 2006; Thuiller et al. 2005) and may be an important tool to solve
this conservation gap. We point out herein that the Amazon is the most vulnerable biome for invasion
by some of the most trafficked species in Brazil, such as ‘Saffron Finch’ and ‘Yellow-bellied
Seedeater’. In fact, within the Neotropics, the Amazon basin presents a high variety of environments
and is one of the most interesting ecotonal areas within South America (Carvalho et al. 2017). Finally,
we highlight the need to consider animal trade as one of the main means to promote organism
translocations and boost changes in species biogeographical patterns, not only in Brazil, but also in
other megadiverse and developing countries where biodiversity is equally important. Indeed, studies
aiming a evaluating the de facto and immediate impacts of wildlife trade in these countries should be
prioritized, thus providing updated tools for effective decision-making in an increasingly globalized
world subject to rapid and intense transformations.
Acknowledgements
The authors would like to thank the Instituto Brasileiro do Meio Ambiente e dos Recursos
Naturais Renováveis (IBAMA) for supporting our research, and WikiAves
(http://www.wikiaves.com.br) for free access to the collaborative database on Brazilian birds. LCT and
PDM also thank the support provided by CNPq Productivity grants.
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Supporting Information
Additional Supporting information may be found in the online version of this article:
Supplementary material S1 Parameters chosen to elaborate final suitability maps.
Supplementary material S2 TSS and AUC values.
Supplementary material S3 Moran's I index and Multivariate environmental similarity surface.
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Supplementary material S1
Parameters chosen to elaborate final suitability maps
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ThresholdThreshold at which the sum
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EnsembleMean consensus of themodels with TSS above
average
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Supplementary material S2
TSS and AUC values
Species Algorithm AUC TSS
Cyanoloxia brissonii
Bioclimatic Envelope Method - BioClim 0.98124 0.958985
Generalized Additive Model – GAM 0.96986 0.93703
Gaussian Model 0.98566 0.94765
Generalized Linear Model – GLM 0.8973 0.79249
Maxent with default features – MaxNet 0.8651 0.731835
Simple Maxent Model 0.82001 0.675465
Random Forest – RDF 0.99285 0.96293
Support Vector Machine – SVM 0.99119 0.96216
Gnorimopsar chopi
Bioclimatic Envelope Method - BioClim 0.97833 0.938995
Generalized Additive Model – GAM 0.98555 0.95027
Gaussian Model 0.98966 0.96046
Generalized Linear Model – GLM 0.93195 0.83274
Maxent with default features – MaxNet 0.87954 0.74702
Simple Maxent Model 0.86612 0.735055
Random Forest – RDF 0.99094 0.97033
Support Vector Machine – SVM 0.99132 0.967425
Paroaria dominicana
Bioclimatic Envelope Method - BioClim 0.92322 0.884835
Generalized Additive Model – GAM 0.9583 0.89953
Gaussian Model 0.98455 0.945365
Generalized Linear Model – GLM 0.96427 0.91177
Maxent with default features – MaxNet 0.91588 0.822185
Simple Maxent Model 0.90753 0.81019
Random Forest – RDF 0.98219 0.94739
Support Vector Machine – SVM 0.99013 0.95952
Sporophila angolensis
Bioclimatic Envelope Method - BioClim 0.97283 0.945625
Generalized Additive Model – GAM 0.98203 0.954245
Gaussian Model 0.98738 0.95759
Generalized Linear Model – GLM 0.94051 0.88262
Maxent with default features – MaxNet 0.80455 0.630815
Simple Maxent Model 0.77708 0.605025
Random Forest – RDF 0.9888 0.960975
Support Vector Machine – SVM 0.9894 0.96394
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Sporophila caerulescens
Bioclimatic Envelope Method - BioClim 0.9794 0.95236
Generalized Additive Model – GAM 0.98872 0.956945
Gaussian Model 0.99392 0.96457
Generalized Linear Model – GLM 0.93047 0.828805
Maxent with default features – MaxNet 0.88129 0.75809
Simple Maxent Model 0.86719 0.73923
Random Forest – RDF 0.9949 0.971285
Support Vector Machine – SVM 0.99233 0.969615
Sicalis flaveola
Bioclimatic Envelope Method - BioClim 0.97811 0.945255
Generalized Additive Model – GAM 0.97411 0.920505
Gaussian Model 0.98913 0.946705
Generalized Linear Model – GLM 0.87276 0.752525
Maxent with default features – MaxNet 0.78656 0.628625
Simple Maxent Model 0.7406 0.568175
Random Forest – RDF 0.99386 0.966945
Support Vector Machine – SVM 0.98593 0.9475
Sporophila lineola
Bioclimatic Envelope Method - BioClim 0.91129 0.85468
Generalized Additive Model – GAM 0.96815 0.90658
Gaussian Model 0.9745 0.918505
Generalized Linear Model – GLM 0.90377 0.82522
Maxent with default features – MaxNet 0.73786 0.543335
Simple Maxent Model 0.70623 0.51917
Random Forest – RDF 0.96468 0.908255
Support Vector Machine – SVM 0.97328 0.9123
Sporophila nigricollis
Bioclimatic Envelope Method - BioClim 0.97712 0.948985
Generalized Additive Model – GAM 0.98011 0.93634
Gaussian Model 0.99204 0.949135
Generalized Linear Model – GLM 0.95288 0.897245
Maxent with default features – MaxNet 0.85991 0.709535
Simple Maxent Model 0.83127 0.65311
Random Forest – RDF 0.99293 0.96141
Support Vector Machine – SVM 0.98902 0.94714
Saltator similis Bioclimatic Envelope Method - BioClim 0.97711 0.94061
Generalized Additive Model – GAM 0.98875 0.957775
Gaussian Model 0.99337 0.96622
Generalized Linear Model – GLM 0.92548 0.817055
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Maxent with default features – MaxNet 0.93506 0.84452
Simple Maxent Model 0.92518 0.824385
Random Forest – RDF 0.99625 0.978105
Support Vector Machine – SVM 0.99471 0.97557
Zonotrichia capensis
Bioclimatic Envelope Method - BioClim 0.98347 0.95811
Generalized Additive Model – GAM 0.96973 0.90973
Gaussian Model 0.98949 0.947495
Generalized Linear Model – GLM 0.83473 0.742315
Maxent with default features – MaxNet 0.84084 0.69768
Simple Maxent Model 0.81315 0.66042
Random Forest – RDF 0.99526 0.971215
Support Vector Machine – SVM 0.98638 0.95089
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Supplementary material S3
Moran's I index and Multivariate environmental similarity surface
SpeciesGrid
NumberCell Size
Moran's Iindex Grid
Mess valueGrid
SD Grid
Cyanoloxia brissonii 8 4 0.348 15.705 0.013
Gnorimopsar chopi 8 4 0.185 14.974 0.042
Paroaria dominicana 5 2.5 0.136 8.876 0.085
Sporophila angolensis 2 1 0.240 14.898 0.004
Sporophila caerulescens 2 1 0.337 13.363 0.018
Sicalis flaveola 6 3 0.372 15.795 0.037
Sporophila lineola 12 6 0.356 11.110 0.081
Sporophila nigricollis 2 1 0.191 18.658 0.056
Saltator similis 1 0.5 0.241 13.823 0.007
Zonotrichia capensis 3 1.5 0.354 15.854 0.022
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Capítulo 3
Threats for bird population
restoration: a systematic review
Guilherme Fernando Gomes Destro, Paulo De Marco e
Levi Carina Terribile
Artigo publicado na revista “Perspectives in Ecology and Conservation” em abril de 2018
DOI: 10.1016/j.pecon.2018.03.003
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Threats for bird population restoration: a systematic review
Guilherme Fernando Gomes Destro a, b, Paulo De Marco c, Levi Carina Terribile d
a Programa de Pós-Graduação em Ecologia e Evolução, Universidade Federal de Goiás, Campus
Samambaia, CP 131, 74001-970, Goiânia, GO, Brazil. [email protected] Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis, Superintendência no
Estado de Goiás, Rua 229, nº 95 – Setor Universitário, 74605-090, Goiânia, GO, Brazil.c Departamento de Ecologia, Instituto de Ciências Biológicas, Universidade Federal de Goiás, Campus
Samambaia, CP 131, 74001-970, Goiânia, GO, Brazil. [email protected] Instituto de Ciências Biológicas, Universidade Federal de Goiás, Regional Jataí, 75801-615, Jataí,
GO, Brazil. [email protected]
* Corresponding author: Guilherme Fernando Gomes Destro
Abstract: Although widespread, actions aiming at the restoration of native species populations within
their indigenous range still lack a clear definition of success, given the high degree of variability in
species needs. In this sense, to understand and manage the mechanisms that lead to reintroduction or
reinforcement failures may be a more feasible alternative to ensure conservation objectives. In this
study, we aimed to systematize the main drivers that can negatively impact bird population restoration
according to researchers and practitioners. Thus, a systematic review was performed in peer-reviewed
journals, identifying 75 attempts, conducted from 1990 to 2016, in 30 countries involving 64 bird
species and subspecies. Thirteen drivers that negatively impact reintroduction or reinforcement
attempts were identified, where predation, unexpected dispersal movement and diseases were the main
factors. We believe that if these drivers were prioritized during pre-release planning and post-release
monitoring, restoration population programs would be more successful.
Keywords: avian; predation; reinforcement; reintroduction; systematic review; threatened species
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Introduction
The IUCN Red List process has been globally applied to reveal the threat degree of species
and ecosystems (Mace et al., 2008; IUCN, 2015; Rodríguez et al., 2015). To reverse or even mitigate
the threat degree, different conservation strategies have been executed (Tulloch et al., 2015), and
population restoration stands out as one of the most widespread (Soorae, 2013). According to the
IUCN (2013), population restoration is any intentional movement (translocation) and release of a
living organism to within its indigenous range. It comprises two activities: reinforcement and
reintroduction, that differ in the presence or absence of conspecific populations before release, and not
specifically in management techniques (IUCN, 2013; Seddon et al., 2014). Reinforcement, also known
as augmentation, supplementation, re-stocking, or enhancement (plants only), is the release of an
organism into an existing population of conspecifics (IUCN, 2013; Hardouin et al., 2014), aiming to
enhance population viability by increasing population size, genetic diversity, or representation of
specific demographic groups or stages (Bretagnolle and Inchausti, 2005; Champagnon et al., 2012;
IUCN, 2013). Reintroduction, on the other hand, is the release of an organism inside the indigenous
range from which it has disappeared (Armstrong and Seddon, 2007; IUCN, 2013). Its main objective
is to re-establish a viable population of the focal species within its indigenous range, fulfilling a role as
a keystone component of an ecosystem, and/or create the public and political support necessary to
undertake habitat restoration or to put species protection measures in place (Seddon, 1999; Lipsey and
Child, 2007). However, while conceptually well established, there is no consensus on how to measure
the success of reintroduction or reinforcement efforts (Seddon, 1999; Haskins, 2015; Robert et al.,
2015).
Several methodological proposals to evaluate population restoration are available worldwide
(Soorae, 2013). As a basic metric of success, some authors consider first-year survival rates within the
normal range reported for avian fledglings to be indicative of a successful release (White Jr. et al.,
2005). In other studies, researchers regard survival and reproduction as the two most fundamental
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parameters in terms of population establishment and persistence, defining ‘success’ as those
translocations in which first-year survival was >0.50 (i.e. survival > mortality) and in which released
birds later bred with conspecifics, either captive-reared or wild (White Jr. et al., 2012). Moreover,
other authors also believe that three objectives should be achieved in an effort to restore a population:
(i) establishment: the survival of the release generation; (ii) growth: breeding by the release generation
and their offspring; and, (iii) regulation: persistence of the re-established population (Seddon, 1999;
Sarrazin, 2007; Miller et al., 2014). For these authors, although the establishment and growth phases
are necessary for success, they do not provide accurate estimates of the long-term viability of a
reintroduced population. Thus, the ultimate success criteria should focus on the regulation phase,
during which population dynamics critically depend on the interactions among species and habitat
characteristics, in order to draw reliable conclusions about long-term population dynamics (Armstrong
and Reynolds, 2012).
To contribute to the development of the science of reintroduction biology, Robert et al. (2015)
proposed a method that assesses if the viability of reintroduced populations could be evaluated using
the same criteria as for remnant populations, such as the International Union for Conservation of
Nature (IUCN) Red List criteria. For this, two postulates were proposed: (i) that successful
reintroduction programs should produce viable populations and (ii) that reliable assessments of
ultimate success require that populations reach their regulation phase (Robert et al., 2015). However,
Haskins (2015) point out fragilities in this methodology, since the time and resources required cannot
keep pace with the ever-growing demand for conservation action, particularly under a rapidly
changing climate, and the standardized definition of reintroduction success is nearly impossible to
obtain, due to the high degree of variability in species needs when it comes to reintroduction success
criteria.
Despite recent efforts to develop the science of reintroduction biology, many issues are still
the subject of inconclusive debate (White Jr. et al., 2012; Robert et al., 2015), and thus, pointing out
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reintroduction failures seems to be an easier and more viable alternative to evaluate reintroduction
success (Robert et al., 2015). The environmental drivers that can negatively impact population
restoration programs are listed through a conceptual model presented herein (see Supplementary
material S1). Intrinsic factors evidence interactions among reintroduced and resident populations, and
extrinsic factors are related to other species or environment. Either isolated or taken together, these
drivers may harm a reintroduced population by hampering its establishment, growth or regulation, or
destabilize resident populations and ecological processes. Thus, in order to better understand these
failure dynamics and be able to better plan prevention and control actions, we aimed herein to
systematize the main drivers that can negatively impact the bird population restoration programs
according to researchers and practitioners. In addition, the conservation status of the bird species and
countries with the most attempts in population restoration were listed and evaluated.
Methods
Our search was performed on the online database ISI Web of Knowledge
(www.isiknowledge.com) to identify papers published from 1990 to 2016 that report bird
reintroduction or reinforcement attempts. Birds were chosen because, alongside mammals, this group
presents the most available data (Champagnon et al., 2012; Seddon et al., 2014), probably due to their
social image (Bajomi et al., 2010) or because they are relatively easily studied and rapid results can be
obtained (Armstrong and Seddon, 2011). For the literature search, the terms “reintroduction” OR
“reinforcement” AND “bird” OR “avian” were used. However, to fulfill the purposes of the study and
better detail the presentation of the methods, experimental design and results, paper selection was
restricted. Thus, the analysis conducted herein did not consider: (i) accidental translocations or other
conservation translocation initiatives, such as as Conservation Introduction (Assisted Colonisation or
Ecological Replacement) (see IUCN, 2013); (ii) newsletter articles, published abstracts, books, book
chapters, technical reports or other gray literature; (iii) strictly theoretical studies, such as population
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modeling; and, (iv) studies without direct results on reintroduction/reinforcement attempts or related to
other fields of science in which these terms have another meaning (e.g. molecular biology).
In the final database, population restoration attempts were individualized according to species,
country and year of release. Each species was featured according to its taxonomic family and
conservation status (IUCN, 2017). Studies involving more than one species in a single article were
individualized and considered as a unique restoration attempt (e.g. Miskelly et al., 2009), and identical
restoration efforts presented in more than one article were grouped (e.g. Bernardo et al. 2011a;
Bernardo et al. 2011b). Altogether, 75 restoration efforts were identified which, although not resulting
in an exhaustive bibliographical review, since researchers are more likely to report a "success'' (Fischer
and Lindenmayer, 2000), represent a reliable synthesis of peer-reviewed literature, less prone to bias
and with quality assured information (Bajomi et al., 2010).
Each study was also categorized according to drivers that can negatively impact population
restoration. These drivers were extracted from issues that researchers addressed in their research,
reflecting their theoretical perspectives and problems they thought were relevant to the study. In sum,
we identified: (i) environmental causes; (ii) anthropogenic causes; and (iii) unknown causes.
Anthropogenic causes are those specifically related to failures during the pre and post-release
management. Environmental causes are those who suffer the action of biotic components (e.g.
predation, intra or interspecific competition or diseases), abiotic components (e.g. low environmental
quality and extreme weather), or are the result of individual responses to release events or applied
management (e.g. non-establishment of an animal in the release site, low population size, genetic
vulnerability, reproductive limitation, nest abandonment or infanticide-chick cannibalism) (see
Supplementary material S1). The results were presented using tables and histograms that illustrate
some of the broadest prevalent trends apparent in the data (Fischer and Lindenmayer, 2000). Thus, the
most common species in this regard and their threat degree, the countries with the most restoration
attempts, and the main failures drivers were identified.
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Results
According to the review conducted herein, from 1990 to 2016, 64 bird species and subspecies
across 33 different families were used in reintroduction/reinforcement attempts in 30 countries (see
Supplementary material S2). The most common species were Grus americana (5 instances) and
Notiomystis cincta (3), and the most frequent families were Procellariidae (8) and Gruidae (5).
Regarding conservation status, 45% of the species were classified as being of Least Concern, 16% as
Vulnerable, 14% as Critically Endangered and 13% as Endangered (Fig. 1). The highest number of
studies was carried out in New Zealand (22 instances), USA (16), Spain (4) and Japan (4) (Fig. 2).
Fig. 1. IUCN Red List status for all the bird species worldwide (BirdLife International, 2017) and for
all bird species compiled in this study. *Other categories: Extinct, Extinct in the wild and Data
Deficient
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Fig. 2. Bird population restoration attempts from 1990 to 2016
Thirteen drivers that may negatively impact reintroduction or reinforcement attempts were
pointed out by researchers and practitioners in their studies (Table 1). Most studies reached two or
more negative drivers, although some reports did not point out any obstacle. Considering only
environmental causes, predation was the greatest impact (27 instances), followed by unexpected
dispersal movement (24) and diseases (12). The most important anthropogenic causes were negative
human interference (13 instances) (e.g. hunting, trampling or poisoning), pre-release management (12)
(e.g. unexpected death during transport or inappropriate animal handling) and failures in post-release
management (8) (e.g. lack of shelter or supplementary feeding). Unknown causes of mortality were
identified in 18 studies.
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Table 1. Drivers reported as relevant by researchers and practitioners in bird population restoration
programs. These were grouped as: a) Environmental; b) Anthropogenic; and c) Unknown
Causes Specific drivers ReferencesSum of
instances%
Environmental
PredationCarrlson et al., 2014; VanderWerf et al.,2014; White Jr. et al., 2005; Pérez et al.,
2004; Lovegrove, 199627 36
Unexpected dispersalmovement
Kesler et al., 2012; Dickens et al., 2009;Groombridge et al., 2004; Armstrong,
199524 32
Diseases Candelora et al., 2010; Work et al., 2000 12 16
Population sizeJamieson, 2011; Pereira and Wajntal,
1999; Clarke and Schedvin, 19978 11
Unexpected behavioralresponses
Bennett et al., 2012; Miskelly et al., 2009 7 9
Genetic vulnerability Brekke et al., 2010; Pereira and Wajntal,
19997 9
Low environmental quality Pérez et al., 2011; Castro et al., 2004 6 8
Reproductive limitation Deguchi et al., 2013; Moore et al., 2012 5 7
Intra or interspecificcompetition
Hardouin et al., 2014; Bosé and Sarrazin,2007; Clarke and Schedvin, 1997
5 7
Extreme weather Hardouin et al., 2014; Deguchi et al., 2012 5 7
Anthropogenic
Negative humaninterference
Rideout et al., 2012; Margalida et al.,2008; Meek et al., 2003
13 17
Pre-release management Deguchi et al., 2013; Deguchi et al., 2012;
Dickens et al., 200912 16
Post-release management Yu et al., 2015; Miskelly et al., 2009 8 11
UnknownMeek et al., 2003; Armstrong et al., 2013;
Imlay et al., 201018 24
Discussion
In our study, predation was reported as the most common cause of failure for bird restoration
(e.g. Pérez et al., 2004; Carrlson et al., 2014), in the same way that it seems to be the major problem in
the population restoration of other animal groups (Short et al., 1991; Moseby et al., 2011). For birds,
high predation threats significantly decrease overall success rates by reducing both post-release
survival and the probability of subsequent breeding by released birds (White Jr. et al., 2012). Thus, in
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order to minimize predation impacts, some biologists suggest anti-predator behavioral training during
the pre-release phase (White Jr. et al., 2005; Sanz and Grajal, 1998), or even predator removal by
culling or translocation (Smith et al., 2010). Predator impact is even more worrying on islands, such as
Hawaii (VanderWerf et al., 2014), or island countries, such as New Zealand (Miskelly et al., 2009),
where the return of native species to the original range is only possible after the total eradication these
predators/competitors (Leech et al., 2007; Richardson et al., 2013). For example, eight Procellariidae
species, the family best represented in this study, could only be reintroduced to islands in New Zealand
after the complete eradication of introduced mammals, such as cats (Felis catus) and rats (Rattus
exulans) (Miskelly et al. 2009).
Unexpected dispersal movement of released individuals was another important failure driver
highlighted herein. This driver decreases the possibility of the population establishment post-release
(Dickens et al., 2009), mainly owing to either chance fates of those individuals (demographic
stochasticity) and to low reproduction or survival rates of the remaining population, due to low
densities - Allee effects (Caughley 1994; Armstrong and Wittmer, 2011). In our study, we observed
one critical reintroduction attempt involving Tuamotu kingfishers (Todiramphus gambieri gertrudae),
where all animals returned to the donor area (Kesler et al., 2012). However, in contrast, another study
with Mauritius kestrel (Falco punctatus) revealed that restricted dispersal affected territory occupancy
patterns (Burgess et al., 2008). For Armstrong et al. (2013), post-release dispersal is a key factor
affecting the success of ecological restoration projects, and therefore, the failure risk should be
potentially reduced by managing dispersal, by translocating more animals to compensate for dispersal,
or by avoiding release in areas prone to dispersal.
Pathologies, also highlighted herein, have always been a great concern for professionals
involved in population restoration efforts, either due the transmitted diseases among released and
resident populations or to interspecific forms (Candelora et al., 2010). Aspergillosis (Castro et al.,
2004), poxviruses (Krone et al., 2004), and toxoplasmosis (Work et al., 2000) were some of the most
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commonly mentioned diseases. However, the majority of population restoration attempts around the
world have applied intense veterinary protocols during the pre-release phase (e.g. Brightsmith et al.,
2005; Bernardo et al., 2011a; Keller and Hartup, 2013), thus inhibiting disease transmission risks.
The Whooping Crane (Grus americana), an endangered north American migratory bird since
1967, was the most common species used in the restoration actions summarized herein. However,
despite several reintroduction activities and conservation projects, the survival of this species is still
worrying, mainly due to its low reproductive success, predation, and trauma caused by firearms or
collisions (Cole et al., 2009; Converse et al., 2013). Overall, although the threat rate of the species
analyzed herein was higher than the baseline rate of all known species from all threat categories (Fig.
1), most studies focused on bird species categorized as “Least Concern” (e.g. Leech et al., 2007;
Dickens et al., 2009; Bennett et al., 2012). These data corroborate the study by Seddon et al. (2005),
who observed that reintroduction project bias for both mammals and birds was not related to
differences between orders regarding vulnerability to threat. In general, most bird species were
released in areas where the original population still exists (reinforcement), usually aiming to evaluate
different release methods through the surrogate species of the actual target species (Hardouin et al.,
2014), or in sites where the target species had become locally extinct (e.g. Jamieson, 2011; Slater and
Altman, 2011; Estrada, 2014). Moreover, in many tropical countries, such as Brazil, it is also common
that trafficked animals return to capture areas after being seized by the authorities (Destro et al., 2012).
Thus, the selection of candidates for reintroduction programmes does not only consider the threat
degree of the species, but also national priorities, funding availability, and local community support
over global conservation status (Seddon et al., 2005).
Regardless of environmental drivers that have been the main cause for reintroduction/
reinforcement failures, some studies point out that direct or indirect human impact may be primarily
responsible for the high mortality of released birds (Margalida et al., 2008; Rideout et al., 2012).
Among the negative human impacts observed herein, the following are noteworthy: poisoning
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(Margalida et al., 2008; Rideout et al., 2012), hunting (Perez et al., 2004), trauma and death caused by
collision with vehicles or power infrastructures (Margalida et al., 2008; Mitchell et al., 2011; Keller
and Hartup, 2013) and litter ingestion (Rideout et al., 2012). On the other hand, some species such
Lesser Kestrels (Falco naumanni), one of the most endangered birds in Europe, may be favored by
urbanization and human influence because they nest in crevices or cavities of farm buildings, old
churches or castles (Perez et al., 2011).
Although widely implemented worldwide, reintroduction or reinforcement actions carried out
in island countries, such as New Zealand (Miskelly et al., 2009; Jamieson, 2011; Richardson et al.,
2013) and other territories bordered by the sea, like Hawaii (Groombridge et al. 2004; VanderWerf et
al.; 2004), are again noteworthy, since they were the major focus of the studies analyzed herein. In
these areas where natural resources are limited, certain environmental management measures are
frequently performed before reintroduction efforts, such as habitat restoration and enrichment
(Reynolds et al., 2008; Endo and Nagata, 2013), and control of exotic species (Groombridge et al.,
2004). However, as they are considered dynamic processes modeled by intrinsic and extrinsic factors,
release plans must be even more carefully planned out (Groombridge et al., 2004), requiring
researchers and practitioners to recognize poor performance caused by internal weaknesses or other
causes, so they can take remedial steps (Clark and Westrum, 1989). Furthermore, considering that only
three of the ten countries with the largest numbers of reintroduction/reinforcement efforts (Fig. 2) were
listed among the 17 most megadiverse countries in the world (Mittermeier et al., 1997), with eight of
these belonging to the list of the 15 largest economies (IMF, 2016), we can infer that population
restoration efforts are concentrated in rich countries, instead of more megadiverse nations.
Population restoration is a long-standing practice (Jørgensen, 2013) and appears to be more
successful when the source population is wild, when many specimens is released, and when the cause
of original decline was previously removed (Fischer and Lindenmayer, 2000). However, its success
rate is often overestimated, since successful projects are more likely to be published than failed
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projects or those with uncertain outcomes (Miller et al., 2014). In fact, causes for restoration failures
are difficult to evaluate due to lack of monitoring (Fischer and Lindenmayer, 2000), although an
understanding of the frequency and causes of restoration failures is valuable for reintroduction biology
and may be a singular way to understand the dynamics involved in population restoration actions
(Miller et al., 2014). Herein, even though some species and restoration efforts have not been evaluated
due to search criteria used, we have made an important contribution to the reintroduction biology,
because we summarized the main failure drivers involved in bird population restoration attempts.
Because of its generality, our review may also be applied in a wide variety of other studies, since,
independent of the chosen bird species, many programmatic similarities among these animals and their
conservation programs are noted (Clark and Westrum, 1989). Thus, we stimulate researchers and
practitioners to predict these failure drivers during pre-release planning and, subsequently, evaluate
them in the post-release monitoring stages, to better understand the actual problems inherent to
population restoration programs.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or
not-for-profit sectors.
Acknowledgements
We thank the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA)
for supporting our research, as well as anonymous reviewers for valuable suggestions on previous
versions of this manuscript. LCT and PDMJ also thank the support provided by CNPq Productivity.
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Supplementary material S1
Conceptual model of drivers that can negatively impact population restoration programs
Intrinsic factors are directly related to the target species, and extrinsic factors include interactions
with other species or environment. Interaction among resident and reintroduced populations is
provided only in reinforcement attempts
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Supplementary material S2
Reintroduction or reinforcement attempts according to the systematic review
Country Specie FamilyConservation
StatusTotal ofStudies
AustraliaClimacteris picumnus Climacteridae Least concern 1
Manorina melanocephala Meliphagidae Least concern 1
Brazil
Crax blumenbachii Cracidae Endangered 1
Penelope obscura bronzina Cracidae Least concern 1
Penelope superciliaris jacumpeba Cracidae Least concern 1
CanadaAthene cunicularia hypugaea Strigidae Least concern 1
Lanius ludovicianus migrans Laniidae Least concern 1
China Nipponia nippon Threskiornithidae Endangered 1
FranceAegypius monachus Accipitridae Near threatened 1
Gyps fulvus Accipitridae Least concern 1
FrenchPolynesia
Todiramphus gambieri gertrudae AlcedinidaeCritically
endangered1
Germany Falco peregrinus Falconidae Least concern 1
Indonesia Leucopsar rothschildi SturnidaeCritically
endangered1
Japan
Nipponia nippon Threskiornithidae Endangered 1
Phoebastria albatrus Diomedeidae Vulnerable 1
Phoebastria immutabilis Diomedeidae Near threatened 1
Phoebastria nigripes Diomedeidae Near threatened 1
MauritiusFalco punctatus Falconidae Endangered 1
Foudia rubra Ploceidae Endangered 1
Mexico Ara macao cyanoptera Psittacidae Least concern 1
Morocco Chlamydotis undulata undulata Otididae Vulnerable 1
New Zealand Notiomystis cincta Notiomystidae Vulnerable 3
Petroica longipes Petroicidae Least concern 2
Philesturnus carunculatus carunculatus
Callaeidae Near threatened 2
Philesturnus carunculatus rufusater
Callaeidae Near threatened 2
Acanthisitta chloris Acanthisittidae Least concern 1
Himantopus novaezelandiae RecurvirostridaeCritically
endangered1
Pachyptila turtur Procellariidae Least concern 1
Pelecanoides urinatrix Procellariidae Least concern 1
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Petroica australis longipes Petroicidae Least concern 1
Petroica australis rakiura Petroicidae Least concern 1
Porphyrio hochstetteri Rallidae Endangered 1
Pterodroma axillaris Procellariidae Vulnerable 1
Pterodroma macroptera gouldi Procellariidae Least concern 1
Pterodroma magentae ProcellariidaeCritically
endangered1
Pterodroma pycrofti Procellariidae Vulnerable 1
Puffinus gavia Procellariidae Least concern 1
Puffinus huttoni Procellariidae Endangered 1
Panama Harpia harpyja Accipitridae Near threatened 1
Peru andCosta Rica
Ara macao Psittacidae Least concern 1
Poland Tetrao urogallus Phasianidae Least concern 1
Puerto Rico Amazona vittata PsittacidaeCritically
endangered1
Saudi Arabia Chlamydotis macqueenii Otidae Vulnerable 1
Seychelles Dryolimnas cuvieri aldabranus Rallidae Least concern 1
Singapore Anthracoceros albirostris Bucerotidae Least concern 1
south Africa Spheniscus demersus Spheniscidae Endangered 1
Spain
Alectoris rufa Phasianidae Least concern 1
Falco naumanni Falconidae Least concern 1
Marmaronetta angustirostris Anatidae Vulnerable 1
Porphyrio porphyrio Rallidae Least concern 1
UnitedKingdom
Otis tarda Otididae Vulnerable 1
Tyto alba Tytonidae Least concern 1
USA Grus americana Gruidae Endangered 5
Gymnogyps californianus CathartidaeCritically
endangered2
Alectoris chukar Phasianidae Least concern 1
Falco femoralis septentrionalis Falconidae Least concern 1
Sialia mexicana Turdidae Least concern 1
Sitta pusilla Sittidae Least concern 1
Tympanuchus cupido Phasianidae Vulnerable 1
Anas laysanensis AnatidaeCritically
endangered1
Corvus hawaiiensis Corvidae Extinct in the wild 1
Melamprosops phaeosoma Fringillidae Critically 1
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endangered
Myadestes palmeri TurdidaeCritically
endangered1
Venezuela Amazona barbadensis Psittacidae Vulnerable 1
“Alps”(Switzerland,Austria, Italyand France)
Gypaetus barbatus Accipitridae Near threatened 1
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Capítulo 4
Back home? Uncertainties for
returning seized animals to the source-areas
under climate change
Guilherme Fernando Gomes Destro, Virgínia de Fernandes,
Paulo De Marco e Levi Carina Terribile
Artigo submetido à revista “Global Change Biology” em outubro de 2018
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Back home? Uncertainties for returning seized animals to the source-areas under climate change
Running Head: Population restoration under climate change
1,2Guilherme Fernando Gomes Destro*, 1Virgínia de Fernandes, 3Paulo De Marco, 4Levi Carina
Terribile
1. Programa de Pós-Graduação em Ecologia e Evolução, Universidade Federal de Goiás, Campus
Samambaia, CP 131, 74001-970, Goiânia, GO, Brazil.
2. Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis, Superintendência no
Estado de Goiás, Rua 229, nº 95 – Setor Leste Universitário, 74605-090 – Goiânia, GO, Brazil.
3. Departamento de Ecologia, Instituto de Ciências Biológicas, Universidade Federal de Goiás,
Campus Samambaia, CP 131, 74001-970, Goiânia, GO, Brazil.
4. Instituto de Ciências Biológicas, Universidade Federal de Goiás, Regional Jataí, 75801-615, Jataí,
GO, Brazil.
* Corresponding author: [email protected]; (+55) 62982441253
Keywords: Animal trafficking; Ecological Niche Modeling – ENM; Global Warming; Passerine;
Population restoration; Reinforcement; Reintroduction
Paper type: Primary Research
Abstract: Regardless of the economic, social and environmental impacts caused by wild animal
trafficking worldwide, the suitable destination of seized specimens is one of the main challenges faced
by environmental managers and authorities. In Brazil, returning seized animals to the wild has been
the most frequent path in population restoration programs, and has been carried out, as a priority, in
areas where the animals were captured. However, in addition to the difficulty in identifying the exact
locations of illegal captures, little scientific knowledge is available on the future viability of these
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areas due to global climate change. Thus, the current work aims to evaluate the impacts of climate
change on the main source-municipalities for animal trafficking in Brazil, referred to herein as source-
areas. For this, using ecological niche modeling, the environmental suitability of the source-areas for
illegal animal captures were evaluated in two scenarios at two differ time horizons: optimistic (RCP
26) and a pessimistic (RCP 85) emission scenarios in both 2050 and 2070 projections. Moreover, the
source-areas were compared with the Brazilian Federal protected areas, used here as the control group.
According to the results, Brazilian source-municipalities are not always the best option for maintaining
the most seized species in the future simulations, and, therefore, seem not be the best option for
projects that aim for the return of these animals to the wild. In this sense, despite the genetic and
ecological issues inherent in translocation projects, our results suggest that population restoration
programs for seized species need to be rethought, and furthermore other suitable areas could be
considered for truly ensuring the survival and maintenance of overexploited populations in the long-
term.
Introduction
When live wild animals are seized by government authorities, these authorities have the
responsibility to relocate them appropriately, prioritizing their welfare and the conservation of existing
wild populations (IUCN, 2002). According to the International Union for Conservation of Nature,
there are three main paths for seized animals: i) maintenance of the individual(s) in captivity; ii)
returning the individual(s) to the wild; and, iii) euthanasia (IUCN, 2002; CITES, 2016). In many
source-countries for trafficking, even considering the great human and monetary resources inherent in
the rescue and rehabilitation of these specimens (Magroski et al., 2017), the return of seized animals to
the wild has been the most widely adopted strategy by government agencies (Destro et al., 2012).
However, if poorly planned, these releases into can cause several negative effects on the environment
such as pathogens or diseases introduction (Cunningham, 1996; Jiménez and Cadena, 2004; Godoy
and Matushima, 2010), changes in the inter- and intraspecific ecological interactions such as
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competition, predation, parasitism and mutualism (Jiménez and Cadena, 2004; Molony et al., 2006),
and modification in the genetic structure of populations such as loss of local adaptations and
elimination of genetic difference among populations (Moritz, 1999; Champagnon et al., 2012). On the
other hand, well-managed reintroduction that considers welfare issues, conservation value, and costs
could improve the long-term conservation potential of species or populations. This can occur if seized
animals fulfill their biological and ecological role again, or if wildlife management promotes local
conservation values through education or public awareness programs and makes a strong
political/educational statement concerning the destination of seized specimens (e.g. IUCN, 2002;
Champagnon et al., 2012; Magroski et al., 2017).
In order to truly safeguard the genetic lineages of birds (Magroski et al., 2017), the return of
seized animals to the wild ideally should be carried out within the original locality of the specimens,
i.e., at the same local that they were captured (Martins et al., 2018). However, determining the exact
origin of individuals from seizure places is a difficult task because they typically occur along trade
routes far from the region where the individuals were captured, and little information is retrieved from
arrested traffickers (Hernandez and Carvalho, 2006; Presti et al., 2015; Martins et al., 2018).
Moreover, techniques required for this investigative work, such as genetic testing, are often expensive,
unavailable or difficult to implement (Fernandes and Caparroz, 2013; Magroski et al., 2017; Martins et
al., 2018), and trafficking pressures that motivated the illegal captures usually are continuous and
difficult to combat in the source-area regions (Silva and Bernard, 2016). Regardless of these issues,
the question emerges: are source-areas the most suitable for long-term persistence of species
overexploited by trafficking, even in face of the unfavorable global climate change effects?
Several studies have recently debated the impacts of climate change on the survival and
maintenance of wildlife (e.g. Thomas et al., 2004; Marini et al., 2009; Travis et al., 2013), and South
America stands out as one of the most vulnerable regions (Boulanger et al., 2010; Urban, 2015; Anjos
and Toledo, 2018). Among the animal groups, birds have been of particular interest because they serve
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as an important indicator of the effects of climate change, particularly on tropical ecosystems (Marini
et al., 2009; Sekercioglu et al., 2012). In this sense, besides propagating shifts in phenotypes according
to the new environmental conditions through phenotypic plasticity and/or evolutionary changes of
organisms (Møller et al., 2010; Maggini et al., 2011), climate change can directly lead to species
distribution changes: i) expanding range size, if the change is beneficial to the ecological need; ii)
contracting it where change is detrimental; or, iii) shifting their ranges to track new favorable climatic
conditions (e.g. Maggini et al., 2011; Crossman et al., 2012; Braidwood et al., 2018). In fact, the
migration of released organisms to climatically-suitable habitats could be a condition of natural
adaptation (Carroll et al., 2009), specially the birds which respond more easily to climatic changes by
shifting their distributions (Triviño et al., 2018). However, in some cases, such displacements may be
frustrated because released populations cannot adapt to new conditions or cannot adapt fast enough
(Kokko and Lopez-Sepulcre, 2006; Devictor et al., 2008; Visser, 2008). In other words, source-areas
may have conditions that are inadequate to ensure species’ long-term persistence (Araújo et al., 2004;
Watson and Watson, 2015), leading the species to extinction even with a substantial and continuous
investment in management (Chauvenet et al., 2013). In fact, considering the effects of climate change
on translocation planning and area-prioritization exercises for reintroduction projects is a key aspect
and could provide fundamental information for the conservation of both current and longer term
suitability of candidate areas (Martínez-Meyer et al., 2006; Chauvenet et al., 2013). However, despite
its importance, few studies have considered the shifts (or changes) in the long-term suitability of areas
for species' reintroductions (Martínez-Meyer et al., 2006), including projects seeking the return of wild
birds exploited by trafficking.
Brazil exhibits one of the richest avifauna in the world (Marini and Garcia, 2005), and its
biological and cultural diversity make it an exceptional location for examining live wildlife trade and
its implications for wildlife conservation (Alves et al., 2013). In this sense, bird-keeping activity,
especially of songbirds, has been preserved throughout the centuries across social classes and is
widespread in both urban and rural regions (e.g. Alves et al., 2013; Kuhnen et al., 2012; Alves et al.,
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2010). However, Brazil, like other source-countries such as Mexico (González-Marín et al., 2016),
Peru (Gastañaga et al., 2011), Cambodia (Gray et al., 2017), Zimbabwe (Lindsey et al., 2011), the
Congo (Nasi et al., 2011) and Nigeria (Atuo et al., 2015), has characteristics that give rise to illegal
wildlife trade: it is a megadiverse country with high social inequality in all of its regions (Regueira and
Bernard, 2012). Hence, although the majority of the trafficked bird species in the country are
categorized as "Least Concern" (Destro et al., 2012) and have a wide geographic distribution (see
Sick, 1997), many of them have reached severe population decreases, and some have already become
locally extinct due to overexploitation (Freitas et al., 2015; Fernandes-Ferreira et al., 2012; Gama and
Sassi, 2008). In this sense, considering the negative social, economic, and ecological impacts from the
illegal wildlife trade globally (e.g. Broad et al., 2003; Shepherd and Nijman, 2008; Lawson and Vines,
2014), as well as the great quantity of specimens seized annually (Destro et al., 2012; Cruze and
Macdonald, 2016; UNODC, 2016), it is necessary to conduct research aimed at fine-tuning the care,
rehabilitation, and optimal destination for seized fauna, ensuring the long-term conservation of
overexploited species or populations, even under anthropogenic change effects. Thus, based on this
context and using the most seized bird species in Brazil as surrogates for conservation, the effects of
global climate on the main source-municipalities for animal trafficking in Brazil were evaluated
herein, offering general insight for improvements in area-selection methods for the release of seized
animals in their source-countries.
Methods
Species occurrence records and environmental layers
Passeriformes is one of the most coveted orders of bird, by legal and illegal breeders alike, in
Brazil (e.g. Souto et al., 2017; Do Nascimento et al., 2015; Regueira and Bernard, 2012), especially
due to the beauty of their plumage, shape and song melody (e.g. Teixeira et al., 2014; Licarião et al.,
2013; Fernandes-Ferreira et al., 2012). Thraupidae, which received the most genera from the former
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Emberizidae (Barker et al., 2013), is the most relevant bird family (e.g. Licarião et al., 2013;
Fernandes-Ferreira et al., 2012; Regueira and Bernard, 2012), also representing the most frequent bird
species seized by government authorities in the country (Destro et al., 2012). Herein, the ten most
seized bird species in Brazil were selected (Destro et al., 2012; Table 1), corresponding to over 60% of
the wild bird specimens seized in the country from 2005 to 2009 (Destro et al., unpublished date). A
total of 187,955 occurrence records from the following online databases were gathered: (i) CRIA
Species Link (http://splink.cria.org.br/); (ii) Global Biodiversity Information Facility
(http://www.gbif.org/); and, (iii) VertNet (http://vertnet.org/). Records with geographic location errors,
e.g. located outside the study area, were excluded through the use of ArcGis 10.2.2 for Desktop (ESRI,
2014). Bird nomenclature follows the Brazilian Ornithological Records Committee (Piacentini et al.,
2015), however, synonyms such as Cyanocompsa brissonii (Lichtenstein, 1823), Passerina brissonii
Stotz et al. (1996) and Oryzoborus angolensis (Linnaeus, 1766) were also used. In addition, to reduce
spatial autocorrelation, the software SDMToolBox 2.1.0 extension for ArcGis (http://sdmtoolbox.org/)
was used to exclude dubious records and establish a minimum distance of 20 km among records of the
same species, avoiding analysis of contiguous cells (cell size grid = 10 km). In the end, a total of
12,047 occurrence points without subspecies distinction were used, with Zonotrichia capensis
presenting the highest number of records (4,069) and Paroaria dominicana, the lowest (184).
For current climate, all 19 WorldClim’s climatic variables dataset (www.worldclim.org) were
used to derive principal components (PCs) through a Principal Components Analysis (PCA). Thus, in
order to decrease the collinearity among environmental variables and avoid model overfitting that may
result in biologically unreliable areas (Jiménez-Valverde et al., 2011; Silva et al., 2014a), six PCs were
selected as new environmental layers during the modeling procedures (Silva et al., 2014a; Silva et al.,
2014b; Silva et al., 2015), comprising more than 96% of the original set variation. The same 19
variables were obtained considering both an optimistic (RCP 26) and a pessimistic (RCP 85) CO2
emission scenarios for the years 2050 and 2070 for three different coupled atmosphere-ocean general
circulation models (AOGCMs): CCSM4, MRI-CGCM3, and GISS-E2-R. These AOGCMs were also
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obtained from the WorldClim database and chosen for belonging to groups of models with different
predictions and covering the widest range of climatic predictions (Varela et al., 2015). The linear
combinations of all 19 PCs obtained in the current climate were projected into each different future
AOGCMs scenarios, using the first six PCs, for each AOGCM and emission scenario, to predict the
future distribution of the evaluated species. Thus, two scenarios at two differ time horizons were
obtained: i) 2050 with optimistic scenario; ii) 2050 with pessimistic scenario; iii) 2070 with optimistic
scenario; and, iv) 2070 with pessimistic scenario.
Table 1. The ten most seized wild bird species in Brazil between 2005 and 2009. Conservation status
was obtained from IUCN (2017).
Family Specie Author Common nameConservation
statusNumber of
records
Thraupidae Sicalis flaveola (Linnaeus, 1766) Saffron Finch Least Concern 2,530
Thraupidae Saltator similisd'Orbigny and
Lafresnaye, 1837Green-winged
SaltatorLeast Concern 581
ThraupidaeSporophila
caerulescens(Vieillot, 1823)
Double-collaredSeedeater
Least Concern 1,132
CardinalidaeCyanoloxia
brissonii(Lichtenstein,
1823)UltramarineGrosbeak
Least Concern 558
ThraupidaeSporophilaangolensis
(Linnaeus, 1766)Chestnut-bellied
Seed-FinchLeast Concern 755
IcteridaeGnorimopsar
chopi(Vieillot, 1819) Chopi Blackbird Least Concern 824
ThraupidaeParoaria
dominicana(Linnaeus, 1758) Red-cowled Cardinal Least Concern 184
ThraupidaeSporophila
lineola(Linnaeus, 1758) Lined Seedeater Least Concern 492
Passerellidae Zonotrichia
capensis(Statius Muller,
1776)Rufous-collared
SparrowLeast Concern 4,069
ThraupidaeSporophilanigricollis
(Vieillot, 1823)Yellow-bellied
SeedeaterLeast Concern 922
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Ecological Niche Models (ENM)
Ecological niche modeling (ENM) is widely used to estimate the realized coarse-resolution
environmental requirements of species, which can be projected onto real-world landscapes to identify
regions in which these requirements are manifested (Barve et al., 2011). In fact, this method is
currently the most effective way to evaluate the potential geographical distribution of species, and to
predict the distribution under different environmental conditions (i.e., future or past simulations)
(Chauvenet et al., 2013; Vaz et al., 2015), therefore re-prioritizing areas for conservation (Blair et al.,
2012). Thus, based on the observed occurrences of the target species and on the environmental
variables correlated with these records, computational algorithms create a multidimensional
environmental space that infers niche parameters and predicts species distributions (e.g. Elith and
Leathwick, 2009; Araújo and Guisan, 2006; Soberón and Peterson, 2005). Herein, the ecological niche
of the ten most seized bird species in Brazil were initially assessed considering eight different
modeling algorithms: i) Bioclimatic Envelope Method – BioClim (Beaumont et al., 2005); ii)
Generalized Additive Model – GAM (Hastie and Tibshirani, 1986); iii) Gaussian Model (Golding and
Purse, 2016); iv) Generalized Linear Model – GLM (Guisan et al., 2002); v) Maxent, with default
features - MaxNet (Phillips et al., 2006; Philips et al., 2017); vi) Simple Maxent Model (Williams,
2010); vii) Random Forest – RDF (Breiman, 2001); and, viii) Support Vector Machine – SVM (Tax
and Duin, 2004). Current climate and future simulation models were performed using the
“ENM_TheMetaLand” script (https://github.com/andrefaa/ENM_TheMetaLand), developed by
“Laboratório de Metacomunidades e Ecologia de Paisagens” of “Universidade Federal de Goiás” -
Brazil, and implemented in the “R” software (R Core Team, 2017). Simulations were performed for
each species through the combination of different parameters: i) Pseudo-absence selection method; ii)
Data partitioning method; iii) Threshold; and iv) Ensemble, with the selection of those who reached
better solutions according to the evaluated species (Supplementary material S1). All modeling
procedures were performed considering the entire Neotropical region with the aim of covering the
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maximum range of the evaluated species. The grid for all variables was set to 5 arc-min resolution
(0.083o ≈ 10 km).
Geographic partition structured as a checkerboard was used as the data partition method and
the Area Under the Receiver–operator Curve (AUC) and True Skilled Statistics (TSS; Allouche et al.,
2006) were used to assess model performance (Liu et al., 2011). The AUC and TSS account for the
sensitivity (quantifying omission errors) and specificity (quantifying commission errors) of the models
(Allouche et al., 2006). The AUC is a threshold-independent statistical analysis ranging from 0 to 1,
where values around 0.5 represent distribution models no better than random and values around 1
represent a perfect fit between the observed and the predicted species distribution. Acceptable
distribution models exhibit values higher than 0.7. On the other hand, TSS is a threshold-dependent
statistical analysis that varies from −1 to +1 (Allouche et al., 2006). The TSS values near 0 or negative
values represent distributions no better than random, while values equal to +1 represent perfect
agreement between the observed and the predicted distribution. Acceptable models considering these
statistics achieve at least 0.5, and excellent models are a minimum of 0.7, similar to what is employed
in the AUC statistics (Fielding and Bell, 1997).
Only presence data were used to elaborate the models. The modeled suitability matrices were
cut using the threshold at which the sum of the sensitivity and specificity was highest (Vale et al.,
2014; Ferraz et al., 2012), reducing the risk of choosing unsuitable sites (Pearce and Ferrier, 2000).
Finally, given the overall biases and uncertain nature of species distribution models (Zhu and Peterson,
2017; Diniz-Filho et al., 2009), the mean consensus of the models with above average TSS was used
to elaborate the final maps. In fact, although consensus models do not outperform individual models,
they can reflect the central tendency of individual models, thus reducing uncertainties by consolidating
consistency across individual models (Zhu and Peterson, 2017; Araújo and New, 2007).
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Main source-areas for animal trafficking and protected areas in Brazil
We conducted an extensive literature search at the Brazilian National Electronic Library
“CAPES Portal de Periódicos” (www.periodicos.capes.gov.br/) to identify papers related to trafficked
wild animals in Brazil. We used the terms “illegal” AND “trade” AND “Brazil”, without restricting
journal, language, year of publication or information platform. A total of 139 papers were identified. In
addition, we also used the Google Search Engine (www.google.com) to search for gray literature:
newsletter articles, magazines and newspapers, published abstracts, books, book chapters and
technical reports. Thus, through this literary framework, were extracted the main source-municipalities
for animal trafficking in Brazil, i.e., the municipalities described in the literature as source-areas for
trafficked wild animals. A total of 209 municipalities were listed (Supplementary material S2). We
used 105 Brazilian Federal Protected Areas as the control group because of their importance for long-
term biodiversity conservation, excluding from the analysis the marine protected areas and other
protected areas that reached a total area less than 100 Km2 (= grid area). The protected area database
were extracted from Instituto Chico Mendes de Conservação da Biodiversidade website
(www.icmbio.gov.br).
Climate change analysis
We compared two scenarios at two differ time horizons (2050-optimistic, 2050-pessimistic,
2070-optimistic, and 2070-pessimistic) with the current climate niche maps for evaluating changes in
the predicted distributional areas. For this, the predicted area for each AOGCM (CCSM4, MRI-
CGCM3 and GISS-E2-R) was calculated and, based on the average, the final area was obtained for
each species and future projection. We also compared the future simulations with the current climate
for evaluating suitability change in the source-areas for trafficking. Thus, for each species, we
elaborated four final future maps with the average of the three AOGCMs maps. The average suitability
values from all source-areas were extracted from current and final future maps. The same procedure
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was applied to protected areas, used herein as the control for the statistical tests. We also calculated the
average suitable area for each sample unit (source-areas - SA and protected areas - PA) for estimating
the difference between SA and PA overall. Regression through the origin (see Eisenhauer, 2003) was
used to estimate the correlation among predicted areas in the current and future. For assessing the
significance of the difference between SA and PA (herein named “group variable”), and among current
climate and future (time variable) for each species, we used a Permutation Test for Two-Way Repeated
Measure Analysis of Variance, since variances were usually unequal for the majority of the species.
Two-Way Repeated Measure Analysis of Variance was also used for evaluating the difference between
SA and PA overall. All statistic tests were performed in the “R” software (R Core Team, 2017) and the
spatial analyses were carried out using the software ArcGis 10.2.2 for Desktop (ESRI, 2014),
considering South America as the spatial limit.
Results
The TSS values obtained from final models obtained through of ensemble ranged between
0.879 and 0.972, while AUC values ranged between 0.984 and 0.999 (Supplementary material S3),
demonstrating a good predictive capability of the ENMs (Fielding and Bell, 1997; Metz, 1986).
Training-test subsets values for spatial autocorrelation (Moran's I index) and MESS (Multivariate
Environmental Similarity Surface) are presented in the Supplementary material S4. Zonotrichia
capensis, S. flaveola and S. lineola attained the largest predicted areas, while S. similis, P. dominicana
and S. caerulescens had the smallest (see Supplementary material S5). In this sense, species that
reached the most restricted predicted areas in the current climate should become even more restricted
in future simulations (Fig. 1 and Table 2). However, a correlation between lost suitable area in the
future and suitable area in the current climate was not observed here (Table 3). Even so, S. similis,
which had the smallest current predicted area, presented disproportionately the greatest lost predicted
area, attaining more than 40% of the pessimistic scenario from 2070 (Fig. 2). Zonotrichia capensis and
S. caerulescens also reached large losses in this scenario, attaining more than 30% of original
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predicted area. S. flaveola, which had the second largest predicted area, was the species that obtained
the lowest ratio of lost area in all future time/scenarios.
Figure 1. Regression through the origin among current and future predicted areas (million Km2)
Table 2. Regression through the origin among current and future predicted areas (Km2)
Time/ScenariosAngular
Coefficient (b)Confidence Interval Results
2050 Optimistic 0.9890 0.9110 - 1.0670 R2 = 0.9907; F1,8 = 854.1; P < 0.001
2070 Optimistic 0.9821 0.8944 – 1.0699 R2 = 0.9881; F1,8 = 666.9; P < 0.001
2050 Pessimistic 0.9234 0.7653 – 1.0816 R2 = 0.9578; F1,8 = 181.4; P < 0.001
2070 Pessimistic 0.8148 0.6118 – 1.0178 R2 = 0.9146; F1,8 = 85.65; P < 0.001
Table 3. Regression through the origin among current predicted area and lost predicted areas. In red,
nonsignificant correlations
Time/Scenarios Results2050 Optimistic R2 = 0.01302; F1,8 = 0.1055; P = 0.75362070 Optimistic R2 = 0.0268; F1,8 = 0.2203; P = 0.65132050 Pessimistic R2 = 0.1348; F1,8 = 1.247; P = 0.29662070 Pessimistic R2 = 0.3562; F1,8 = 4.426; P = 0.06852
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Figure 2. Lost predicted area (%) by the ten most seized bird species in Brazil under the future
simulations. Species: Ssimilis = Saltator similis; Scaerulescens = Sporophila caerulescens;
Pdominicana = Paroaria dominicana; Sangolensis = Sporophila angolensis; Zcapensis = Zonotrichia
capensis; Gchopi = Gnorimopsar chopi; Snigricollis = Sporophila nigricollis; Slineola = Sporophila
lineola; Cbrissonii = Cyanoloxia brissonii; Sflaveola = Sicalis flaveola
Excluding S. caerulescens, all species showed interaction between group variable (SA and PA)
and time variable (current climate and future), i.e., there is distinction in the differences of magnitude
among analyzed variables (Table 4). C. brissonii, G. chopi and P. dominicana had better suitability for
SA in all time/scenarios, while S. angolensis, S. nigricollis and Z. capensis reached a more suitable PA
(Supplementary material S6). As opposed to other species, S. lineola had only significant differences
in the pessimistic scenarios, where protected areas revealed better suitability than source-areas. S.
caerulescens, S. flaveola and S. similis did not present differences between SA and PA. Overall,
through proportion of suitable areas between all SA and PA evaluated, no differences were observed
for the majority of simulations (Fig. 3), except for the pessimistic scenario in 2070, where PA reached
more suitable areas than SA.
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Table 4. Permutation Test for Two-Way Repeated Measure Analysis of Variance using average
suitability of all source-areas (SA) and protected areas (PA) evaluated. In red, the species for which the
differences between SA and PA or through the climatic simulations was not significant . (df: Group =
312; Time = 1248; Group:Time = 1248)
Species Variables F p
Cyanoloxia brissoniiGroup 14.86 < 0.05Time 294.16 < 0.05
Group:Time 14.47 < 0.05
Gnorimopsar chopiGroup 5.23 < 0.05Time 325.60 < 0.05
Group:Time 10.96 < 0.05
Paroaria dominicanaGroup 7.78 < 0.05Time 152.89 < 0.05
Group:Time 4.55 < 0.05
Sporophila angolensisGroup 25.78 < 0.05Time 270.45 < 0.05
Group:Time 3.87 < 0.05
Sporophila caerulescensGroup 0.67 0.41Time 228.57 < 0.05
Group:Time 1.66 0.17
Sicalis flaveolaGroup 0.23 0.62Time 374.99 < 0.05
Group:Time 8.74 < 0.05
Sporophila lineolaGroup 3.92 < 0.05Time 219.19 < 0.05
Group:Time 8.43 < 0.05
Sporophila nigricollisGroup 26.55 < 0.05Time 376.46 < 0.05
Group:Time 11.94 < 0.05
Saltator similisGroup 0.012 0.91Time 189.33 < 0.05
Group:Time 12.63 < 0.05
Zonotrichia capensisGroup 10.90 < 0.05Time 577.07 < 0.05
Group:Time 6.39 < 0.05
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Figure 3. Two-Way Repeated Measure Analysis of Variance among future time/scenarios and suitable
areas (%) of all source-areas (SA) and protected areas (PA) evaluated
Discussion
In our study, S. similis, P. dominicana, and S. caerulescens were the species that had the
greatest decrease of predicted areas due to climate change, probably because they reached a smaller
area of climatically suitable habitat available in the current climate (see Fig. 2 and Supplementary
material S5). Although not confirmed here, this negative correlation between current range extension
and predicted range loss have already been demonstrated in previous studies (Marini et al., 2009), and
reveal that range contraction is harmful, since it can force geographically restricted birds into refugia,
which could make them even rarer where they occur, or lead to species extirpation (Braidwood et al.,
2018). In this sense, climate change project significant temperature and precipitation changes for most
of South America (e.g. Marini et al., 2009; Loiselle et al., 2010; Junk, 2013) and its current and
predicted impacts on tropical birds can be used to suggest management strategies to prevent the future
decline and extinction of species (Gardali et al., 2012; Sekercioglu et al., 2012).
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However, generalist species that can survive in a wide range of habitats and/or feed on
different kinds of food could be more likely to adapt to or even benefit from climate change
(Sekercioglu et al., 2012). Herein, S. flaveola, S. lineola and C. brissonii should be the species least
affected by climate change, since S. flaveola e S. lineola reached one of the greatest areas of
climatically suitable habitat available in the current climate. In fact, considering that some populations
and species will be less affected than others by climate change due to the differences in species
attributes, such as generation time and microhabitat preference (Crossman et al., 2012; Bowler et al.,
2015), different conservation measures should be undertaken (Marini et al., 2009; Gardali et al., 2012).
Furthermore, previous studies have highlighted that most tropical bird species vulnerable to climate
change are not currently considered threatened with extinction, often due to a lack of knowledge,
making the systematic and regular gathering of information on the ecology and the current and future
distributions of these species an urgent priority (Sekercioglu et al., 2012). Thus, efforts aimed at
assessing the impact of climate change should be comprehensive, covering not only currently
threatened taxa but also common and widespread species, since even they could also experience
substantial changes in abundance, distribution, and species interactions, affecting ecosystems and their
services to humans (Lawler et al., 2009).
Overall, source-areas (SA), ideally considered priority sites in the restoration efforts of
trafficked species, reached less suitable areas than protected areas (PA) in the pessimistic scenario of
2070. Specifically, PA showed better suitability for S. angolensis, S. nigricollis and Z. capensis in all
evaluated time/scenarios, as well as for S. lineola in the pessimistic scenarios (see Suplementar
Material S6). Moreover, although PA reached worse suitability than SA in the future simulations for C.
brissonii, G. chopi and P. dominicana, this difference was inversely proportional to the pessimism of
emission scenarios. S. caerulescens, S. flaveola and S. similis did not present differences between SA
and PA in the future. In summary, SA for trafficking are not necessarily the best options for
maintaining the most seized species in Brazil in face of the climate change, and, likewise, seem not be
the best options for projects that aim for the return of these animals to the wild. Thus, areas with lower
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trafficking pressure and most suitable environmental conditions for the maintenance of stable and self-
sustaining populations could be a priority for wildlife restoration projects, regardless of where the
animals were captured. In this sense, new suitable areas might emerge in what were previously
unsuitable or marginal habitats, and previously suitable areas might be converted into unsuitable or
marginal ones (Araújo et al., 2004).
New sites projected to maintain suitable climatic conditions in the medium to long term could
become refugia, providing also habitat space for several species ahead of the climate’s leading edge
(see Braidwood et al., 2018), among them, many tropical forest understory species, birds on low
tropical mountains, low-lying island specialists, and sedentary birds whose current and future ranges
are not connected (Sekercioglu et al., 2012). Moreover, in the case of common and widespread
species, the translocation of animals to suitable sites where the populations are fragile or have been
extinct could in-fill distributional ranges, increase population size and improve both demographic and
genetic connectivity, therefore keeping common species common even under climate change (Watson
and Watson, 2015). In fact, this strategy of translocating specimens to locations where the climate is
most suitable is not a new solution, and has been increasingly debated and considered as one of the
main options for maintaining several species under anthropogenic climate change (e.g. Thomas, 2011;
Rout et al., 2013; Payne and Bro-Jørgensen, 2016).
However, despite the benefits that conservation translocations may bring, the release of seized
individuals into the wild should be conducted with caution, because local populations may suffer
adverse genetic effects (Fernandes and Caparroz, 2013; Presti et al., 2015; Magroski et al., 2017), such
as inter- and intraspecific hybridization. Among the species studied herein, Sicalis flaveola comprises
four historically-isolated subspecies in South America (Clements et al., 2017; Silveira and Mendez,
1999) that if intermingled, could induce intraspecific hybridization. Regarding interspecific
hybridization, several cases have been cited in the literature, including species belonging to the
Sporophila and Cyanoloxia genera (Sick, 1997). Moreover, when the seized animals are released into
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non-indigenous ranges, another problem that arises is related to the invasive species issue, considered
one of the main global concerns and main threats to global biodiversity worldwide (IUCN, 2002;
Clavero and Garcia-Berthou, 2005). Thus, in order to avoid possible impacts from poorly planned
programs and uncertainties from translocations into non-indigenous ranges (Webber et al., 2011), the
return of seized animals to the wild should be primarily carried out into indigenous areas, regardless of
whether they are source-areas or not. Furthermore, considering that selected sites for restoration
population are expected to match the biotic and abiotic needs of the candidate species now and in the
future (Chauvenet et al., 2013), considering changes in the suitability of these areas due to climate
change is an essential task. In fact, new researches could be directed at assessing destruction and
degradation of habitats through land-use and land-cover changes, a rather neglected theme at
biodiversity scenarios (Titeux et al., 2016; Sirami et al., 2017).
Indeed, climate change has placed many traditional conservation targets out of reach. This
demands a comprehensive rethink of conservation aims and strategies (e.g. Chauvenet et al., 2013;
Travis et al., 2013; Corlett, 2016). In this scenario, a philosophy of conserving the composition of
biological communities as they are, or restoring them to some specified (or imagined) historical state,
sits uneasily with the reality of environmental and biological change (Thomas, 2011). Returning seized
animals to the wild is part of this reality, where interventions seem to be inevitable in order to avoid
further species extinctions (Chauvenet et al., 2013; Travis et al., 2013). Herein, it was demonstrated
that more refined climate projections and species distribution models may provide a better
understanding of the possible scenarios, thus enabling to consider future projections as an integral part
of the design of wildlife restoration sites (see Braidwood et al., 2018). In fact, considering the high
investments related to these programs, prioritizing ecologically suitable and safe areas within the
framework of long-term conservation planning seems to be a practical and viable solution for
returning seized specimens to the wild, even when these sites are not the same as the sites where the
animals were captured.
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Acknowledgements
We thank the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis
(IBAMA) for supporting our research. LCT and PDM also thank the support provided by CNPq
Productivity grants.
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Supplementary material S1
Parameters chosen to elaborate final suitability maps
Parameter Evaluated method Reference
Pseudo-absenceselection method
Constrained by a BioclimModel
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models and their predictions? An information-theoretic approach based on simulated data.
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Data partitioningmethod
Geographic partitioningstructured as a checkerboard
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(2014) ENMeval: An R package for conductingspatially independent evaluations and estimating
optimal model complexity for MAXENTecological niche models. Methods Ecol Evol 5:
1198–1205.
ThresholdThreshold at which the sum
of the sensitivity andspecificity is highest
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38: 921–931.
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28: 385-393.
EnsembleMean consensus of themodels with TSS above
average
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Supplementary material S2
Main source-municipalities for the illegal capture of wild animals in Brazil
Region State Municipality Data Source
Midwest GoiásAlto Paraíso de
Goiás
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Midwest Goiás Bonópolis
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Midwest Goiás Campos Belos
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Midwest Goiás Cavalcante
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Midwest Goiás Colinas do Sul
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Midwest GoiásMonte Alegre
de Goiás
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Midwest Goiás Nova Roma
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Midwest GoiásSão Joãod'Aliança
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Midwest GoiásSão Miguel do
Araguaia
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
169/195
Midwest GoiásTeresina de
Goiás
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
GrossoBarão deMelgaço
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
GrossoCáceres
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
GrossoChapada dosGuimarães
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
GrossoCuiabá
RENCTAS (2001) Rede Nacional de Combate ao Tráfico de Animais Silvestres. 1º Relatório Nacional sobre o Tráfico de Fauna Silvestre. RENCTAS, Brasília, BRA. Http://www.renctas.org.br/wp-content/uploads/2014/02/REL_RENCTAS_pt_final.pdf [acessed 15 August 2016].
MidwestMato
GrossoCurvelândia
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
GrossoItiquira
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
GrossoNossa Senhorado Livramento
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
GrossoPoconé
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
GrossoSanto Antôniodo Leverger
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Midwest MatoGrosso do
Sul
Anastácio BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report.
170/195
Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Anaurilândia O ECO (2012) Começou a temporada do tráfico de papagaios. Http://www.oeco.org.br/noticias/26542-comecou-a-temporada-do-trafico-de-papagaios/ [acessed 15 March 2017].
MidwestMato
Grosso doSul
Aquidauana
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Bataguassu O ECO (2012) Começou a temporada do tráfico de papagaios. Http://www.oeco.org.br/noticias/26542-comecou-a-temporada-do-trafico-de-papagaios/ [acessed 15 March 2017].
MidwestMato
Grosso doSul
Batayporã O ECO (2012) Começou a temporada do tráfico de papagaios. Http://www.oeco.org.br/noticias/26542-comecou-a-temporada-do-trafico-de-papagaios/ [acessed 15 March 2017].
MidwestMato
Grosso doSul
Bela Vista
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Bodoquena
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Bonito
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Brasilândia O ECO (2012) Começou a temporada do tráfico de papagaios. Http://www.oeco.org.br/noticias/26542-comecou-a-temporada-do-trafico-de-papagaios/ [acessed 15 March 2017].
MidwestMato
Grosso doSul
Caracol
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Corguinho
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Corumbá
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Midwest MatoGrosso do
Sul
Coxim BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report.
171/195
Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Ivinhema O ECO (2012) Começou a temporada do tráfico de papagaios. Http://www.oeco.org.br/noticias/26542-comecou-a-temporada-do-trafico-de-papagaios/ [acessed 15 March 2017].
MidwestMato
Grosso doSul
Ladário
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Miranda
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Mundo Novo O ECO (2012) Começou a temporada do tráfico de papagaios. Http://www.oeco.org.br/noticias/26542-comecou-a-temporada-do-trafico-de-papagaios/ [acessed 15 March 2017].
MidwestMato
Grosso doSul
Naviraí O ECO (2012) Começou a temporada do tráfico de papagaios. Http://www.oeco.org.br/noticias/26542-comecou-a-temporada-do-trafico-de-papagaios/ [acessed 15 March 2017].
MidwestMato
Grosso doSul
NovaAndradina
O ECO (2012) Começou a temporada do tráfico de papagaios. Http://www.oeco.org.br/noticias/26542-comecou-a-temporada-do-trafico-de-papagaios/ [acessed 15 March 2017].
MidwestMato
Grosso doSul
NovoHorizonte do
Sul
O ECO (2012) Começou a temporada do tráfico de papagaios. Http://www.oeco.org.br/noticias/26542-comecou-a-temporada-do-trafico-de-papagaios/ [acessed 15 March 2017].
MidwestMato
Grosso doSul
Porto Murtinho
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Rio Negro
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Rio Verde deMato Grosso
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
MidwestMato
Grosso doSul
Santa Rita doPardo
O ECO (2012) Começou a temporada do tráfico de papagaios. Http://www.oeco.org.br/noticias/26542-comecou-a-temporada-do-trafico-de-papagaios/ [acessed 15 March 2017].
MidwestMato
Grosso doSul
Sonora
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Midwest Mato Três Lagoas O ECO (2012) Começou a temporada do tráfico de papagaios.
172/195
Grosso doSul
Http://www.oeco.org.br/noticias/26542-comecou-a-temporada-do-trafico-de-papagaios/ [acessed 15 March 2017].
North Pará Afuá
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Anajás
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Bagre
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Belém
RENCTAS (2001) Rede Nacional de Combate ao Tráfico de Animais Silvestres. 1º Relatório Nacional sobre o Tráfico de Fauna Silvestre. RENCTAS, Brasília, BRA. Http://www.renctas.org.br/wp-content/uploads/2014/02/REL_RENCTAS_pt_final.pdf [acessed 15 August 2016].
North Pará Bragança
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Breves
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North ParáCachoeira do
Arari
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North ParáCanaã dos
Carajás
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Chaves
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North ParáConceição do
Araguaia
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
173/195
North Pará Curralinho
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Gurupá
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Marabá
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Melgaço
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Muaná
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North ParáNovo
Repartimento
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North ParáOurilândia do
Norte
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Parauapebas
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North ParáPonta dePedras
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Portel
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Redenção BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report.
174/195
Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Salvaterra
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North ParáSanta Cruz do
Arari
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Santarém
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North ParáSão Félix do
Xingu
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North ParáSão Sebastiãoda Boa Vista
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Soure
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Pará Xinguara
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Tocantins Araguaçu
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Tocantins Araguanã
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Tocantins Centenário
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
175/195
North TocantinsFormoso do
Araguaia
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North TocantinsLagoa daConfusão
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Tocantins Lizarda
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Tocantins Mateiros
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Tocantins Pium
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North TocantinsPonte Alta do
Tocantins
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Tocantins Recursolândia
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North TocantinsSanta Rosa do
Tocantins
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
North Tocantins Silvanópolis
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Alagoas Palestina
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Alagoas Pão de Açúcar BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report.
176/195
Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Alagoas Pariconha
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Bahia Amargosa
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Bahia BarreirasSouza, G.M. de & Soares Filho, A. de O. (2005) O comércio ilegal de aves silvestres na região do Paraguaçu e Sudoeste da Bahia. Enciclopédia Biosfera, 1, 1-10.
Northeast BahiaCampo
Formoso
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Bahia Canudos
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Bahia Cipó
RENCTAS (2001) Rede Nacional de Combate ao Tráfico de Animais Silvestres. 1º Relatório Nacional sobre o Tráfico de Fauna Silvestre. RENCTAS, Brasília, BRA. Http://www.renctas.org.br/wp-content/uploads/2014/02/REL_RENCTAS_pt_final.pdf [acessed 15 August 2016].
Northeast Bahia Cocos
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Bahia Curaçá
RENCTAS (2001) Rede Nacional de Combate ao Tráfico de Animais Silvestres. 1º Relatório Nacional sobre o Tráfico de Fauna Silvestre. RENCTAS, Brasília, BRA. Http://www.renctas.org.br/wp-content/uploads/2014/02/REL_RENCTAS_pt_final.pdf [acessed 15 August 2016].
Northeast BahiaEuclides da
Cunha
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast BahiaFeira deSantana
RENCTAS (2001) Rede Nacional de Combate ao Tráfico de Animais Silvestres. 1º Relatório Nacional sobre o Tráfico de Fauna Silvestre. RENCTAS, Brasília, BRA. Http://www.renctas.org.br/wp-content/uploads/2014/02/REL_RENCTAS_pt_final.pdf [acessed 15 August 2016].
Northeast Bahia Ibotirama Souza, G.M. de & Soares Filho, A. de O. (2005) O comércio ilegal de aves silvestres na região do Paraguaçu e Sudoeste da Bahia.
177/195
Enciclopédia Biosfera, 1, 1-10.
Northeast Bahia Itaberaba
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Bahia Jeremoabo
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Bahia JuazeiroSouza, G.M. de & Soares Filho, A. de O. (2005) O comércio ilegal de aves silvestres na região do Paraguaçu e Sudoeste da Bahia. Enciclopédia Biosfera, 1, 1-10.
Northeast BahiaLivramento deNossa Senhora
Souza, G.M. de & Soares Filho, A. de O. (2005) O comércio ilegal de aves silvestres na região do Paraguaçu e Sudoeste da Bahia. Enciclopédia Biosfera, 1, 1-10.
Northeast Bahia Mascote
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Bahia Milagres
RENCTAS (2001) Rede Nacional de Combate ao Tráfico de Animais Silvestres. 1º Relatório Nacional sobre o Tráfico de Fauna Silvestre. RENCTAS, Brasília, BRA. Http://www.renctas.org.br/wp-content/uploads/2014/02/REL_RENCTAS_pt_final.pdf [acessed 15 August 2016].
Northeast BahiaMorro doChapéu
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast BahiaRibeira do
Pombal
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Bahia Rio de ContasSouza, G.M. de & Soares Filho, A. de O. (2005) O comércio ilegal de aves silvestres na região do Paraguaçu e Sudoeste da Bahia. Enciclopédia Biosfera, 1, 1-10.
Northeast BahiaSanta Maria da
Vitória
Souza, G.M. de & Soares Filho, A. de O. (2005) O comércio ilegal de aves silvestres na região do Paraguaçu e Sudoeste da Bahia. Enciclopédia Biosfera, 1, 1-10.
Northeast Bahia Tucano
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Bahia Uauá BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/
178/195
[accessed 01 September 2017].
Northeast BahiaVitória daConquista
RENCTAS (2001) Rede Nacional de Combate ao Tráfico de Animais Silvestres. 1º Relatório Nacional sobre o Tráfico de Fauna Silvestre. RENCTAS, Brasília, BRA. Http://www.renctas.org.br/wp-content/uploads/2014/02/REL_RENCTAS_pt_final.pdf [acessed 15 August 2016].
Northeast Ceará Araripe
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Ceará Crateús
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Ceará Jati
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Ceará São Benedito
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Ceará Ubajara
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Maranhão Alto Parnaíba
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Maranhão Balsas
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast MaranhãoBarão deGrajaú
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Maranhão Buriticupu
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Maranhão Tasso Fragoso BRASIL (2003) Comissão Parlamentar de Inquérito destinada a
179/195
investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Maranhão Zé Doca
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Paraíba Alagoa GrandeGama, T.F. & Sassi, R. (2008) Aspectos do comércio ilegal de pássaros silvestres na cidade de João Pessoa, Paraíba, Brasil. Gaia Scientia, 2, 2, 01-20.
Northeast Paraíba Cabaceiras
Rocha, M. da S.P., Cavalcanti, P.C. de M., Souza, R. de L., Alves & R.R.N. (2006) Aspectos de comercialização ilegal de aves nas feiras livres de Campina Grande, Paraíba, Brasil. Revista de Biologia e Ciências da Terra, 6, 2, 204-221.
Northeast Paraíba Cajazeiras
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast ParaíbaCampinaGrande
Rocha, M. da S.P., Cavalcanti, P.C. de M., Souza, R. de L., Alves & R.R.N. (2006) Aspectos de comercialização ilegal de aves nas feiras livres de Campina Grande, Paraíba, Brasil. Revista de Biologia e Ciências da Terra, 6, 2, 204-221.
Northeast Paraíba Lagoa Seca
Rocha, M. da S.P., Cavalcanti, P.C. de M., Souza, R. de L., Alves & R.R.N. (2006) Aspectos de comercialização ilegal de aves nas feiras livres de Campina Grande, Paraíba, Brasil. Revista de Biologia e Ciências da Terra, 6, 2, 204-221.
Northeast Paraíba MamanguapeGama, T.F. & Sassi, R. (2008) Aspectos do comércio ilegal de pássaros silvestres na cidade de João Pessoa, Paraíba, Brasil. Gaia Scientia, 2, 2, 01-20.
Northeast Paraíba Patos
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Paraíba PilarGama, T.F. & Sassi, R. (2008) Aspectos do comércio ilegal de pássaros silvestres na cidade de João Pessoa, Paraíba, Brasil. Gaia Scientia, 2, 2, 01-20.
Northeast Paraíba Pombal
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Paraíba Queimadas
Rocha, M. da S.P., Cavalcanti, P.C. de M., Souza, R. de L., Alves & R.R.N. (2006) Aspectos de comercialização ilegal de aves nas feiras livres de Campina Grande, Paraíba, Brasil. Revista de Biologia e Ciências da Terra, 6, 2, 204-221.
Northeast Paraíba Remígio Rocha, M. da S.P., Cavalcanti, P.C. de M., Souza, R. de L., Alves & R.R.N. (2006) Aspectos de comercialização ilegal de aves nas feiras livres de Campina Grande, Paraíba, Brasil. Revista de Biologia e
180/195
Ciências da Terra, 6, 2, 204-221.
Northeast Paraíba Seridó
Rocha, M. da S.P., Cavalcanti, P.C. de M., Souza, R. de L., Alves & R.R.N. (2006) Aspectos de comercialização ilegal de aves nas feiras livres de Campina Grande, Paraíba, Brasil. Revista de Biologia e Ciências da Terra, 6, 2, 204-221.
Northeast Paraíba Serra Branca
Rocha, M. da S.P., Cavalcanti, P.C. de M., Souza, R. de L., Alves & R.R.N. (2006) Aspectos de comercialização ilegal de aves nas feiras livres de Campina Grande, Paraíba, Brasil. Revista de Biologia e Ciências da Terra, 6, 2, 204-221.
Northeast Paraíba Sousa
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Pernambuco Petrolândia
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Pernambuco Recife
RENCTAS (2001) Rede Nacional de Combate ao Tráfico de Animais Silvestres. 1º Relatório Nacional sobre o Tráfico de Fauna Silvestre. RENCTAS, Brasília, BRA. Http://www.renctas.org.br/wp-content/uploads/2014/02/REL_RENCTAS_pt_final.pdf [acessed 15 August 2016].
Northeast Pernambuco Salgueiro
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Pernambuco Serra Talhada
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast PiauíAlvorada do
Gurguéia
Souto, W.M.S.; Torres, M.A.R.; Sousa, B.F.C.F.; Lima, K.G.G.C.; Vieira, L.T.S.; Pereira, G.A.; Guzzi, A.; Silva, M.V. & Pralon, B.G.N. (2017) Singing for cages: The use and trade of passeriformesas wild pets in an economic center of the Amazon - NE Brazil route.Tropical Conservation Science, 10, 1–19.
Northeast PiauíBarreiras do
Piauí
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Piauí Bom Jesus
Souto, W.M.S.; Torres, M.A.R.; Sousa, B.F.C.F.; Lima, K.G.G.C.; Vieira, L.T.S.; Pereira, G.A.; Guzzi, A.; Silva, M.V. & Pralon, B.G.N. (2017) Singing for cages: The use and trade of passeriformesas wild pets in an economic center of the Amazon - NE Brazil route.Tropical Conservation Science, 10, 1–19.
Northeast Piauí Brejo do Piauí Souto, W.M.S.; Torres, M.A.R.; Sousa, B.F.C.F.; Lima, K.G.G.C.; Vieira, L.T.S.; Pereira, G.A.; Guzzi, A.; Silva, M.V. & Pralon, B.G.N. (2017) Singing for cages: The use and trade of passeriformes
181/195
as wild pets in an economic center of the Amazon - NE Brazil route.Tropical Conservation Science, 10, 1–19.
Northeast Piauí Canto do Buriti
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Piauí Caracol
Souto, W.M.S.; Torres, M.A.R.; Sousa, B.F.C.F.; Lima, K.G.G.C.; Vieira, L.T.S.; Pereira, G.A.; Guzzi, A.; Silva, M.V. & Pralon, B.G.N. (2017) Singing for cages: The use and trade of passeriformesas wild pets in an economic center of the Amazon - NE Brazil route.Tropical Conservation Science, 10, 1–19.
Northeast PiauíCoronel José
Dias
Souto, W.M.S.; Torres, M.A.R.; Sousa, B.F.C.F.; Lima, K.G.G.C.; Vieira, L.T.S.; Pereira, G.A.; Guzzi, A.; Silva, M.V. & Pralon, B.G.N. (2017) Singing for cages: The use and trade of passeriformesas wild pets in an economic center of the Amazon - NE Brazil route.Tropical Conservation Science, 10, 1–19.
Northeast Piauí Corrente
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Piauí Cristino Castro
Souto, W.M.S.; Torres, M.A.R.; Sousa, B.F.C.F.; Lima, K.G.G.C.; Vieira, L.T.S.; Pereira, G.A.; Guzzi, A.; Silva, M.V. & Pralon, B.G.N. (2017) Singing for cages: The use and trade of passeriformesas wild pets in an economic center of the Amazon - NE Brazil route.Tropical Conservation Science, 10, 1–19.
Northeast Piauí Curimatá
Souto, W.M.S.; Torres, M.A.R.; Sousa, B.F.C.F.; Lima, K.G.G.C.; Vieira, L.T.S.; Pereira, G.A.; Guzzi, A.; Silva, M.V. & Pralon, B.G.N. (2017) Singing for cages: The use and trade of passeriformesas wild pets in an economic center of the Amazon - NE Brazil route.Tropical Conservation Science, 10, 1–19.
Northeast Piauí Floriano
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Piauí Gilbués
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Piauí Guadalupe
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Piauí Guaribas
Souto, W.M.S.; Torres, M.A.R.; Sousa, B.F.C.F.; Lima, K.G.G.C.; Vieira, L.T.S.; Pereira, G.A.; Guzzi, A.; Silva, M.V. & Pralon, B.G.N. (2017) Singing for cages: The use and trade of passeriformesas wild pets in an economic center of the Amazon - NE Brazil route.Tropical Conservation Science, 10, 1–19.
182/195
Northeast Piauí Jurema
Souto, W.M.S.; Torres, M.A.R.; Sousa, B.F.C.F.; Lima, K.G.G.C.; Vieira, L.T.S.; Pereira, G.A.; Guzzi, A.; Silva, M.V. & Pralon, B.G.N. (2017) Singing for cages: The use and trade of passeriformesas wild pets in an economic center of the Amazon - NE Brazil route.Tropical Conservation Science, 10, 1–19.
Northeast PiauíMonte Alegre
do Piauí
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Piauí Piripiri
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast PiauíRedenção do
Gurguéia
Souto, W.M.S.; Torres, M.A.R.; Sousa, B.F.C.F.; Lima, K.G.G.C.; Vieira, L.T.S.; Pereira, G.A.; Guzzi, A.; Silva, M.V. & Pralon, B.G.N. (2017) Singing for cages: The use and trade of passeriformesas wild pets in an economic center of the Amazon - NE Brazil route.Tropical Conservation Science, 10, 1–19.
Northeast PiauíSanta
Filomena
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Piauí Santa Luz
Souto, W.M.S.; Torres, M.A.R.; Sousa, B.F.C.F.; Lima, K.G.G.C.; Vieira, L.T.S.; Pereira, G.A.; Guzzi, A.; Silva, M.V. & Pralon, B.G.N. (2017) Singing for cages: The use and trade of passeriformesas wild pets in an economic center of the Amazon - NE Brazil route.Tropical Conservation Science, 10, 1–19.
Northeast PiauíSão Gonçalodo Gurguéia
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast PiauíSão João do
Piauí
Souto, W.M.S.; Torres, M.A.R.; Sousa, B.F.C.F.; Lima, K.G.G.C.; Vieira, L.T.S.; Pereira, G.A.; Guzzi, A.; Silva, M.V. & Pralon, B.G.N. (2017) Singing for cages: The use and trade of passeriformesas wild pets in an economic center of the Amazon - NE Brazil route.Tropical Conservation Science, 10, 1–19.
Northeast PiauíSão Raimundo
Nonato
Souto, W.M.S.; Torres, M.A.R.; Sousa, B.F.C.F.; Lima, K.G.G.C.; Vieira, L.T.S.; Pereira, G.A.; Guzzi, A.; Silva, M.V. & Pralon, B.G.N. (2017) Singing for cages: The use and trade of passeriformesas wild pets in an economic center of the Amazon - NE Brazil route.Tropical Conservation Science, 10, 1–19.
Northeast PiauíTamboril do
Piauí
Souto, W.M.S.; Torres, M.A.R.; Sousa, B.F.C.F.; Lima, K.G.G.C.; Vieira, L.T.S.; Pereira, G.A.; Guzzi, A.; Silva, M.V. & Pralon, B.G.N. (2017) Singing for cages: The use and trade of passeriformesas wild pets in an economic center of the Amazon - NE Brazil route.Tropical Conservation Science, 10, 1–19.
Northeast Rio Grandedo Norte
Caicó BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report.
183/195
Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
NortheastRio Grande
do NorteCurrais Novos
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
NortheastRio Grande
do NorteJardim do
Seridó
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Sergipe Cristinápolis
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast SergipeNossa Senhora
da Glória
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Northeast Sergipe Tobias Barreto
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
South Paraná Céu AzulHernandez, E.F.T. & Carvalho, M.S. de (2006) O tráfico de animais silvestres no Estado do Paraná. Acta Scientiarum. Human and SocialSciences, 28, 2, 257-266.
South Paraná Foz do IguaçuHernandez, E.F.T. & Carvalho, M.S. de (2006) O tráfico de animais silvestres no Estado do Paraná. Acta Scientiarum. Human and SocialSciences, 28, 2, 257-266.
South Paraná GuaraqueçabaHernandez, E.F.T. & Carvalho, M.S. de (2006) O tráfico de animais silvestres no Estado do Paraná. Acta Scientiarum. Human and SocialSciences, 28, 2, 257-266.
South Paraná MatelândiaHernandez, E.F.T. & Carvalho, M.S. de (2006) O tráfico de animais silvestres no Estado do Paraná. Acta Scientiarum. Human and SocialSciences, 28, 2, 257-266.
South Paraná MedianeiraHernandez, E.F.T. & Carvalho, M.S. de (2006) O tráfico de animais silvestres no Estado do Paraná. Acta Scientiarum. Human and SocialSciences, 28, 2, 257-266.
South ParanáSão Miguel do
Iguaçu
Hernandez, E.F.T. & Carvalho, M.S. de (2006) O tráfico de animais silvestres no Estado do Paraná. Acta Scientiarum. Human and SocialSciences, 28, 2, 257-266.
SouthRio Grande
do SulRio Grande
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
South Rio Grande Sant' Ana do Hernandez, E.F.T. & Carvalho, M.S. de (2006) O tráfico de animais
184/195
do Sul Livramentosilvestres no Estado do Paraná. Acta Scientiarum. Human and SocialSciences, 28, 2, 257-266.
SouthRio Grande
do SulSanta Vitória
do Palmar
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
SoutheastMinasGerais
Almenara
RENCTAS (2001) Rede Nacional de Combate ao Tráfico de Animais Silvestres. 1º Relatório Nacional sobre o Tráfico de Fauna Silvestre. RENCTAS, Brasília, BRA. Http://www.renctas.org.br/wp-content/uploads/2014/02/REL_RENCTAS_pt_final.pdf [acessed 15 August 2016].
SoutheastMinasGerais
Arinos
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
SoutheastMinasGerais
Buritis
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
SoutheastMinasGerais
ChapadaGaúcha
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
SoutheastMinasGerais
Formoso
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
SoutheastMinasGerais
Urucuia
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Apiaí
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São PauloBarra doChapéu
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Barra do Turvo
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
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Southeast São Paulo Cajati
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Cananéia
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Eldorado
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Iguape
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Ilha Comprida
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Iporanga
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Itaóca
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São PauloItapirapuãPaulista
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Itariri
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Jacupiranga
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Juquiá BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report.
186/195
Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Juquitiba
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Miracatu
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Pariquera-Açu
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São PauloPedro deToledo
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Registro
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Ribeira
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São PauloRibeirãoBranco
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São PauloSão Lourenço
da Serra
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Sete Barras
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
Southeast São Paulo Tapiraí
BRASIL (2003) Comissão Parlamentar de Inquérito destinada a investigar o tráfico ilegal de animais e plantas silvestres da fauna e da flora brasileiras (Cpitrafi). Final Report. Http://www2.camara.gov.br/atividade-legislativa/comissoes/ [accessed 01 September 2017].
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Supplementary material S3
TSS and AUC values
Species Algorithm AUC TSS
Cyanoloxia brissonii
Bioclimatic Envelope Method - BioClim 0.9504 0.880
Generalized Additive Model – GAM 0.9791 0.8601
Gaussian Model 0.9778 0.9092
Generalized Linear Model – GLM 0.9008 0.6938
Maxent with default features – MaxNet 0.8416 0.5722
Simple Maxent Model 0.8222 0.5515
Random Forest – RDF 0.9879 0.9092
Support Vector Machine – SVM 0.9878 0.9273
Final Model 0.9926 0.9219
Gnorimopsar chopi
Bioclimatic Envelope Method - BioClim 0.9771 0.9164
Generalized Additive Model – GAM 0.9832 0.9024
Gaussian Model 0.9878 0.9214
Generalized Linear Model – GLM 0.9183 0.7445
Maxent with default features – MaxNet 0.871 0.6174
Simple Maxent Model 0.8656 0.6047
Random Forest – RDF 0.9884 0.9124
Support Vector Machine – SVM 0.9891 0.9389
Final Model 0.9952 0.9349
Paroaria dominicana
Bioclimatic Envelope Method - BioClim 0.9299 0.8598
Generalized Additive Model – GAM 0.9575 0.8601
Gaussian Model 0.9806 0.8918
Generalized Linear Model – GLM 0.9529 0.8439
Maxent with default features – MaxNet 0.9155 0.7215
Simple Maxent Model 0.9023 0.6773
Random Forest – RDF 0.9824 0.915
Support Vector Machine – SVM 0.9873 0.9336
Final Model 0.9957 0.9271
Sporophila angolensisBioclimatic Envelope Method - BioClim 0.975 0.9151
Generalized Additive Model – GAM 0.9773 0.9067
Gaussian Model 0.9866 0.9298
Generalized Linear Model – GLM 0.9496 0.836
Maxent with default features – MaxNet 0.7836 0.4561
Simple Maxent Model 0.7552 0.4049
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Random Forest – RDF 0.9899 0.9283
Support Vector Machine – SVM 0.9882 0.9257
Final Model 0.9881 0.9336
Sporophila caerulescens
Bioclimatic Envelope Method - BioClim 0.982 0.937
Generalized Additive Model – GAM 0.9812 0.8938
Gaussian Model 0.9888 0.9118
Generalized Linear Model – GLM 0.9015 0.6764
Maxent with default features – MaxNet 0.8837 0.6371
Simple Maxent Model 0.8713 0.6059
Random Forest – RDF 0.9917 0.9441
Support Vector Machine – SVM 0.990 0.9298
Final Model 0.9917 0.9351
Sicalis flaveola
Bioclimatic Envelope Method - BioClim 0.9772 0.8927
Generalized Additive Model – GAM 0.9743 0.8723
Gaussian Model 0.9851 0.8985
Generalized Linear Model – GLM 0.8661 0.6221
Maxent with default features – MaxNet 0.7675 0.4283
Simple Maxent Model 0.7452 0.3958
Random Forest – RDF 0.9847 0.9086
Support Vector Machine – SVM 0.9831 0.8963
Final Model 0.990 0.9173
Sporophila lineola
Bioclimatic Envelope Method - BioClim 0.9592 0.8786
Generalized Additive Model – GAM 0.9692 0.8517
Gaussian Model 0.9787 0.8662
Generalized Linear Model – GLM 0.9305 0.7799
Maxent with default features – MaxNet 0.7766 0.432
Simple Maxent Model 0.732 0.3481
Random Forest – RDF 0.9768 0.8761
Support Vector Machine – SVM 0.9832 0.8726
Final Model 0.9838 0.8785
Sporophila nigricollis Bioclimatic Envelope Method - BioClim 0.9809 0.9269
Generalized Additive Model – GAM 0.9865 0.9114
Gaussian Model 0.9941 0.9281
Generalized Linear Model – GLM 0.9525 0.8395
Maxent with default features – MaxNet 0.8657 0.5726
Simple Maxent Model 0.8307 0.484
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Random Forest – RDF 0.996 0.9502
Support Vector Machine – SVM 0.9928 0.9359
Final Model 0.9966 0.9502
Saltator similis
Bioclimatic Envelope Method - BioClim 0.9767 0.9307
Generalized Additive Model – GAM 0.9952 0.9392
Gaussian Model 0.996 0.9468
Generalized Linear Model – GLM 0.9229 0.7123
Maxent with default features – MaxNet 0.9375 0.7673
Simple Maxent Model 0.9331 0.7553
Random Forest – RDF 0.997 0.9722
Support Vector Machine – SVM 0.9969 0.9429
Final Model 0.9992 0.972
Zonotrichia capensis
Bioclimatic Envelope Method - BioClim 0.9859 0.9479
Generalized Additive Model – GAM 0.9779 0.8658
Gaussian Model 0.9894 0.9029
Generalized Linear Model – GLM 0.8303 0.6507
Maxent with default features – MaxNet 0.8409 0.5581
Simple Maxent Model 0.8196 0.5316
Random Forest – RDF 0.995 0.9563
Support Vector Machine – SVM 0.9875 0.9017
Final Model 0.993 0.9467
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Supplementary material S4
Moran's I index and Multivariate environmental similarity surface
SpeciesGrid
NumberCell Size
Moran's Iindex Grid
Mess valueGrid
SD Grid
Cyanoloxia brissonii 14 7 0.035 17.098 0.010
Gnorimopsar chopi 16 8 0.209 16.450 0.035
Paroaria dominicana 10 5 0.146 11.694 0.034
Sporophila angolensis 8 4 0.278 12.628 0.064
Sporophila caerulescens 4 2 0.354 14.504 0.048
Sicalis flaveola 16 8 0.371 15.084 0.034
Sporophila lineola 9 4.5 0.348 12.487 0.012
Sporophila nigricollis 2 1 0.240 14.647 0.019
Saltator similis 6 3 0.244 19.999 0.086
Zonotrichia capensis 4 2 0.374 14.563 0.02
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Supplementary material S5
Predicted area (Km2) by the ten most seized bird species* in Brazil
under the current climate and four evaluated future scenarios
* Species: Zcapensis: Zonotrichia capensis; Sflaveola: Sicalis flaveola; Slineola: Sporophila lineola;
Snigricollis: Sporophila nigricollis; Sangolensis: Sporophila angolensis; Gchopi: Gnorimopsar chopi;
Cbrissonii: Cyanoloxia brissonii; Scaerulescens: Sporophila caerulescens; Pdominicana: Paroaria dominicana;
Ssimilis: Saltator similis
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Supplementary material S6
Suitability average of the most seized species in Brazil according to the evaluated variables
A B C
D E F
G H I
J
A. Cyanoloxia brissonii; B. Gnorimopsar chopi; C. Paroaria dominicana; D. Sporophila angolensis; E.
Sporophila caerulescens; F. Sicalis flaveola; G. Sporophila lineola; H. Sporophila nigricollis; I. Saltator similis;
J. Zonotrichia capensis
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CONCLUSÕES GERAIS
TRÁFICO DE ANIMAIS SILVESTRES: DA CAPTURA AO RETORNO À NATUREZA
Sob o aspecto científico, o tema tráfico de animais silvestres ainda é um assunto jovem e com
muitas questões a serem respondidas. No entanto, devido aos inúmeros impactos negativos que a ativi-
dade traz não somente à biodiversidade e ao meio natural, mas também à saúde pública nas regiões
afetadas e à socioeconomia global, esta área do conhecimento tem um grande potencial de crescimen-
to. Nesta Tese de Doutorado, nós refutamos a hipótese clássica de que a captura ilegal de animais sil-
vestres para o tráfico provém, exclusivamente, das baixas condições socioeconômicas das populações
humanas envolvidas. Assim, ao apontar como preponderantes as características naturais da região de
origem dos espécimes, como remanescentes de vegetação nativa e proximidade às áreas protegidas,
nós reforçamos a necessidade de uma abordagem mais ampla do problema, e inevitável enfoque multi -
disciplinar. Além disso, nós alertamos que o comércio descontrolado da fauna silvestre pode ser um
importante propulsor para difusão e estabelecimento da fauna exótica, mesmo em se tratando de es -
pécies abundantes e de ampla distribuição. Neste sentido, ressaltamos a necessidade de um maior apri-
moramento das medidas de controle do comércio nacional e internacional da biodiversidade, bem
como um maior número de estudos voltados para prevenção dos possíveis impactos negativos que es-
pécies advindas desta via de translocação podem ocasionar. Não obstante, também destacamos a ne-
cessidade de um maior controle dos fatores responsáveis pelo insucesso das restaurações populacio-
nais, especialmente os relacionados à predação, movimentos de dispersão pós-soltura e doenças, de
modo que as ações que visem o retorno dos animais à natureza sejam mais bem-sucedidas. Ademais,
alertamos sobre os potenciais impactos que as mudanças climáticas podem ocasionar, em longo prazo,
nos municípios-fonte para o tráfico no Brasil, estes comumente considerados prioritários nos esforços
de reintrodução ou revigoramento populacional das espécies traficadas. Assim, por meio desta Tese,
nós acreditamos ter trazido respostas à questões bastante atuais e relevantes no contexto da gestão am-
biental mundial, contudo, muitas inúmeras lacunas de conhecimento permanecem. Isto posto, sugeri-
mos que novas iniciativas congêneres sejam incentivadas e fomentadas no meio acadêmico, primando-
194/195
se, sempre, por uma maior interação do conhecimento científico com os problemas ambientais reais
enfrentados cotidianamente pela sociedade, em síntese, uma maior aproximação da academia com a
prática.
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