Illegal trade on non-native amphibians and reptiles in southeast Brazil: the status of e-commerc

André Lincoln Barroso de Magalhães

Vinícius Avelar São-Pedro

Magalhães, André Lincoln Barroso de

São-Pedro, Vinícius Avelar

Cadernos Espinosanos (E-Journal)

Illegal trade on non-native amphibians and reptiles in southeast Brazil: the status of e-commerce

Directory of Open Access Journals

155Phyllomedusa - 11(2), December 2012Phyllomedusa 11(2):155–160, 2012© 2012 Departamento de Ciências Biológicas - ESALQ - USP ISSN 1519-1397Received 19 October 2012.Accepted 11 December 2012.Distributed December 2012.Short CommuniCationIllegal trade on non-native amphibians and reptiles in southeast Brazil: the status of e-commerceAndré Lincoln Barroso de Magalhães1 and Vinícius Avelar São-Pedro21  Instituto de Ciência Biológicas e da Saúde, Centro Universitário UNA, 30180-100, Belo Horizonte, MG, Brazil. E-mail: andrebiomagalhaes@gmail.com. 2 Centro de Biociências - DBEZ Campus Universitário - Lagoa Nova, Universidade Federal do Rio Grande do Norte, 59078-970, Natal, RN, Brazil. E-mail: vasaopedro@yahoo.com.br.Keywords: CITES, herpetofauna, non-native species, wildlife trade.Palavras-chave: CITES, comércio de animais selvagens, espécies exóticas, herpetofauna.Legal statutes and associated regulations on the importation of non-native species vary among countries. In Queensland, Australia, toads of the genus Bombina, salamanders of the genus Cynops and snakes of the genus Pantherophis, for example, are considered potential threats to the local fauna and, as a consequence, their importation is forbidden by the Land Protection Act of 2002 (Queensland Government 2012). In Brazil, the pet trade as a vector for amphibian and reptile introduction has received little attention. The Ordinance Nº 93 of 1998 was enacted to regulate the management of non-native amphibian and reptiles. This act empha-sizes trade regulation of these non-native taxa through vectors such as importation via the pet trade (Brasil 1998).The introduction of non-native amphibians and reptiles such as the American bullfrog (Lithobates catesbeianus) and the red-eared slider (Trachemys scripta elegans) through the release of pets has occurred in southeastern and southern regions of Brazil, resulting in the establishment of feral populations (Quintela et al. 2006, Afonso et al. 2010). Both species are on the list of the 100 world’s worst invasive   non-indigenous species (Lowe et al. 2000). American bullfrogs, in particular, may have caused detrimental effects to native Brazilian frogs (Silva et al. 2009), particularly through the introduction of disease (Mazzoni et al. 2009, Schloegel et al. 2010). In Brazil, all non-native amphibian and reptile species but L. catesbeianus were placed on the Ordinance Nº 93 of 1998 in order to reduce the likelihood of similar introduction and establishment. The Brazilian Institute of Environment and Renewable Natural Resources (IBAMA) has the responsibility to carry out the enforcement of this ordinance (Brasil 1998).156Phyllomedusa - 11(2), December 2012Although the Brazilian government has declared the importation of non-native herpeto-fauna illegal (Brasil 1998), the efficacy of this regulatory policy has not been determined, and data on trade are incomplete and likely inaccurate, especially regarding trade carried out through the Internet (Pistoni and Toledo 2010). The illegal trade in wildlife appears to be increasing on the Internet, as evidenced by the burgeoning number of websites and social media outlets where wildlife goods are offered, often with clearly suspect origins. Although wildlife law enforcement has made gains in policing physical markets, the Internet presents new challenges via virtual markets that have yet to be properly regulated (Wu 2007). In order to understand the extent of potentially illegal trade, we conducted a study of the offerings of non-native amphibians and reptiles that are currently available through Internet and social media outlets in southeastern Brazil.Species were surveyed in the social network Orkut (http://www.orkut.com/About.aspx) from mid-2006 to mid-2012. Seventeen community forums were accessed to determine the availa-bility of species for sale. We calculated the absolute and relative frequencies of non-anony-mous dealers selling amphibian and reptile species in three cities of southeastern Brazil (Belo Horizonte, Minas Gerais state, Rio de Janeiro, Rio de Janeiro state, and São Paulo, São Paulo state), as well as anonymous dealers. These cities were chosen because they are the main centers of the Brazilian pet trade (Eterovic and Duarte 2002).A total of 49 non-native species (three frogs, two salamanders, 16 lizards, 26 snakes, two turtles) were detected during the seven year survey period. Corn snakes (Pantherophis guttatus), milk snakes (Lampropeltis triangulum), central bearded dragons (Pogona vitticeps), ball pythons (Python regius), and African clawed frogs (Xenopus laevis) comprised the largest percentage of e-commerce trade (43.37, 9.40, 8.67, 6.99 and 4.82%, respectively). Seventeen species  identified  in  our  survey  are  considered endangered by the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). São Paulo was the city with the greatest demand, and anonymous dealers were the ones that most negotiated animals (Table 1).The Internet has become an invaluable tool for facilitating commerce worldwide. With its popularity, however, the opportunities to trade in live animals have increased and, unfortunately, many of these species are endangered and/or non-native species (Eterovic and Duarte 2002, Henderson and Bomford 2011).  Our results suggest that a complete ban on pet-traded species via e-commerce would be ineffective. Because many dealers omit their names, cities, and the origin of specimens offered in community forums, much of this trade is likely illegal, a fact which dealers are no doubt well aware of. Evading the law is a common component of the worldwide amphibian and reptile trade, both through physical and electronic means (Pistoni and Toledo 2010, Natusch and Lyons 2011).The reasons for a lack of compliance with existing Brazilian law are probably related to (1) a lack of enforcement by IBAMA on wildlife e-commerce and (2) ignorance of the law by most people involved in the pet trade, especially pet owners. IBAMA simply lacks the staff needed to monitor and regulate the pet trade (both physical pet stores and e-commerce); a lack of resources and manpower is a recurring problem in this Federal agency, as in many around the world (Lacava et al. 1995). The great commercial potential of the Internet is that it allows  individuals  to  readily  find  information about products and sales. The Internet can also be a powerful tool for educating dealers and pet owners about regulations and the ethics of releasing non-native species into native habitats, but IBAMA and others in the herpetological com  munity need to develop more effective methods to harness the power of the Internet to inform those involved in on-line transactions about their responsibilities (Kikillus and Hatley 2012). Before a non-native species has been intro-duced to a new country, the possibility of a Magalhães and São-Pedro157Phyllomedusa - 11(2), December 2012Table 1.  Number of internet dealers selling prohibited amphibians and reptiles in southeast Brazil (2006–2012). BH: Belo Horizonte, RJ: Rio de Janeiro, SP: São Paulo.Non-native species CITES BH RJ SPAnonymous dealersTotal % dealersFROGS/TOADSBombinatoridaeBombina orientalis – – – 2 1 3 0.72CeratophryidaeCeratophrys cranwelli – – – 1 – 1 0.24PipidaeXenopus laevis – 4 4 11 1 20 4.82SALAMANDERSAmbystomatidaeAmbystoma mexicanum Appendix II – 1 14 1 16 3.85SalamandridaePleurodeles waltl – – – 1 – 1 0.24LIZARDSAgamidaeHydrosaurus amboinensis – – – 1 – 1 0.24Pogona vitticeps – 1 – 5 30 36 8.67Uromastyx sp. Appendix II – – 1 – 1 0.24AnguidaeAbronia graminea – – – – 1 1 0.24Abronia taeniata – – – – 1 1 0.24ChamaeleonidaeChamaeleo calyptratus Appendix II – 1 1 3 5 1.20Trioceros jacksonii Appendix II – – – 1 1 0.24DiplodactylidaeRhacodactylus auriculatus – – – – 1 1 0.24Rhacodactylus ciliatus – – – – 1 1 0.24EublepharidaeEublepharis macularius – – 2 7 5 14 3.37Hemitheconyx caudicinctus – – – 1 – 1 0.24ScincidaeTiliqua scincoides chimaerea – – – – 2 2 0.48VaranidaeVaranus exanthemathicus Appendix II – – 1 – 1 0.24Varanus niloticus Appendix II – – 1 – 1 0.24Varanus salvator Appendix II – – 1 – 1 0.24Varanus timorensis Appendix II – – 1 – 1 0.24Illegal trade on non-native amphibians and reptiles in southeast Brazil: the status of e-commerce158Phyllomedusa - 11(2), December 2012SNAKESBoidaeAcrantophis dumerili Appendix I – – 1 – 1 0.24ColubridaeHeterodon nasicus – – – 1 – 1 0.24Lampropeltis californiae – – 2 1 1– 13 3.13L. californiae × L. triangulum hybrid– – – – 1 1 0.24Lampropeltis mexicana – – – 1 – 1 0.24Lampropeltis nigra – – – 1 2 3 0.72Lampropeltis triangulum – – 4 20 15 39 9.40Pantherophis guttatus – 3 12 67 98 180 43.37Philodryas baroni – – – 1 – 1 0.24Pituophis catenifer sayi – – – 1 – 1 0.24Thamnophis marcianus – – – 1 – 1 0.24PythonidaeBroghammerus reticulatus Appendix II – – 1 1 2 0.48Morelia spilota cheynei Appendix II – – – 1 1 0.24Morelia spilota mcdowelli Appendix II – – – 1 1 0.24Morelia viridis Appendix II – – 1 – 1 0.24Python brongersmai Appendix II – – – 1 1 0.24Python molurus Appendixes I and II – – 1 11 12 2.89Python regius Appendix II 1 1 16 11 29 6.99ViperidaeAgkistrodon contortrix laticinctus– – – – 1 1 0.24Atropoides olmec – – – – 1 1 0.24Bothriechis schlegelii Appendix II – – – 1 1 0.24Crotalus triseriatus – – – – 1 1 0.24Deinagkistrodon acutus – – – – 1 1 0.24Trimeresurus trigonocephalus – – – – 1 1 0.24Trimeresurus vogeli – – – – 1 1 0.24Trimeresurus venustus – – – – 1 1 0.24TURTLESChelydridaeChelydra serpentina – – – 2 – 2 0.48EmydidaeTrachemys scripta elegans – 1 – 4 1 6 1.4417 10 27 169 209 415Non-native species CITES BH RJ SPAnonymous dealersTotal % dealersMagalhães and São-PedroTable 1.  Continued.159Phyllomedusa - 11(2), December 2012successful invasion must be considered. Esta-blishment risk resulting via an individual pet owner who may keep a few animals of any species likely will be minimal. However, when this risk is multiplied by hundreds of pet owners, releases are inevitable (Henderson and Bomford 2011). If this occurs, extremely detrimental consequences can result, such as biological competition for space and food (e.g., Cha-maeleonidae species impacting Brazilian bush anoles, Polychrus acutirostris; T. scripta elegans competing with D’Orbigny’s sliders, T. dor-bigni), hybridization (e.g., Mexican dusky rattlesnakes, Crotalus triseriatus, hybridizing with South American rattlesnakes, Crotalus durissus), predation on native species by pythons (e.g.,  Acrantophis,  Morelia,  Python), and the spread of emerging infectious diseases (e.g., as has occurred involving Xenopus laevis and other species; Fischer and Garner 2007). The introduction of non-native species may have unforeseen consequences beyond direct ecological effects. Recent attention has been given to the problem of secondary invaders, such as fungi and viruses, which hitchhike along with individuals in the live animal trade. Amphibian chytrid fungus (Batrachochytrium dendrobatidis) and  Ranavirus (Iridoviridae) are pathogens responsible for mass amphibian mortality and population declines and exemplify the dangers of un-checked trade in non-native species (Robert et al. 2007). Another particular feature of the live animal trade is the potential release of venomous snakes, such as adders and cobras, which could lead to public health concerns (Eterovic and Duarte 2002). A number of species found in our survey of trade are highly venomous (e.g., Agkistrodon, Atropoides, Bothriechis, Crotalus, Deinagkistro-don, Philodryas, Trimeresurus), and no antisera for non-native species is available in Brazil.Brazil has been signatory of CITES since 1975 (Brasil 1975). Each nation that is party to CITES must make efforts to monitor wildlife trade (Hemley 1994). An effective inspection protocol monitoring the sales of amphibians and reptiles via e-commerce is necessary in order to combat illegal trade and to avoid the potential establishment of non-native species mediated through the pet trade. We strongly suggest two measures: (1) IBAMA should work with Brazilian web administrators, such as Google and Yahoo, to provide warnings to dealers and enthusiasts about Brazilian law regarding non-native wildlife trade, as well as the dangers of releasing amphibians and reptiles into native habitats; (2) Orkut and other social media must intensify their educational campaigns concerning the illegal pet trade and popularize the goals of CITES to ensure that the international trade of animals and plants does not threaten native species survival in the wild.Finally, our study examined only a small portion of the extent of the Brazilian Internet pet trade. For example, there are other non-native taxa included in Appendix II of CITES, such as plants (e.g., blue orchid Vanda coerulea), invertebrates (e.g., emperor scorpion Pandinus imperator, Mexican red-kneed tarantula Bra-chypelma smithi), and vertebrates (e.g., grey parrot Psittacus erithacus) that are also sold by anonymous dealers in Orkut. Indeed, the problem seems to be much larger than we can imagine, a situation similar to that in other countries when trying to monitor the impacts of international wildlife trade (Schlapfer et al. 2005).AcknowledgmentsThe authors are grateful to the Centro Univer-sitário  UNA  for  financial  support,  and  VAS thanks CAPES for his current PhD scholarship. Two anonymous referees have greatly contri-buted to the final version of this manuscript. ReferencesAfonso, L. G., R. Carvalho, F. M. Santos, A. N. B. Coelho, and A. L. B. Magalhães. 2010. Reprodução da exótica rã-touro  Lithobates catesbeianus (Shaw, 1802) (Amphibia, Anura, Ranidae) em riachos de Mata Atlântica no estado de Minas Gerais, Brasil. Biotemas 23: 85–91.Illegal trade on non-native amphibians and reptiles in southeast Brazil: the status of e-commerce160Phyllomedusa - 11(2), December 2012Brasil. 1975. Presidência da República. Decreto n° 76623, de 17 de novembro de 1975. Promulga a convenção sobre comércio  internacional  das  espécies  da  flora  e  fauna selvagem em perigo de extinção. DOU 1: 372–382.Brasil. 1998. Ministério do Meio Ambiente. Portaria n° 93, de 7 de julho de 1998. Fica proibida a importação de espécimes vivos para fins de criação com fins comerciais, manutenção em cativeiro como animal de estimação ou ornamentação e para a exibição em espetáculos itine-rantes e fixos, salvo em jardins zoológicos, os seguintes taxa: I. invertebrados, II. anfíbios (exceto Rana catesbeiana - rã-touro), III. répteis, IV. ave da espécie Sicalis  flaveola  e suas subespécies, V. mamíferos das Ordens: Artiodactyla (exceto os considerados domésticos para fins de operacionalização do IBAMA), Carnivora, Cetacea, Insectivora, Lagomorpha, Marsupialia, Penni-pedia, Perissodactyla, Proboscidea, Rodentia e Sirenia. DOU 128: 1–7.Eterovic, A. and M. R. Duarte. 2002. Exotic snakes in São Paulo City. Why xenophobia? Biodiversity and Con-servation 11: 327–339.Fischer, M. C. and T. W. J. Garner. 2007. The relationship between the emergence of Batrachochytrium dendro-batidis, the international trade in amphibians and introduced amphibian species. Fungal Biology Reviews 21: 2–9.Hemley, G. (ed.). 1994. International Wildlife Trade: a CITES Sourcebook. Washington. World Wildlife Fund and Island Press. 166 pp.Henderson, W. and M. Bomford (eds.). 2011. Detecting and Preventing New Incursions of Exotic Animals in Australia. Canberra. Invasive Animals Cooperative Research Centre. 60 pp.Kikillus, K. H., K. M. Hare, and S. Hartley. 2012. Online trading tools as a method of estimating propagule pressure via the pet-release pathway. Biological Invasions 14: 2657–2664. Lacava, U., F. M. Rocha, and V. Saracura (eds.). 1995. Tráfico de Animais Silvestres no Brasil: um Diagnóstico Preliminar. Brasília. WWF Brasil. 54 pp.Lowe, S., M. Browne, S. Boudjelas, and M. De Poorter (eds.). 2000. 100 of the World’s Worst Invasive Alien Species. A selection from the Global Invasive Species Database. Auckland. Hollands Printing Ltd. 12 pp.Mazzoni, R., A. A. J. de Mesquita, L. F. F. Fleury, W. M. E. Diederichsen Brito, I. A. Nunes, J. Robert, H. Morales, A. S. G. Coelho, D. L. Barthasson, L. Galli, and M. H. B. Catroxo. 2009. Mass mortality associated with a frog virus 3-like Ranavirus infection in farmed tadpoles Rana catesbeiana from Brazil. Diseases of Aquatic Organisms 86: 181–191.Natusch, D. J. D. and J. A. Lyons. 2011. Exploited for pets: the harvest and trade of amphibians and reptiles from Indonesian New Guinea. Biodiversity and Conservation 21: 2899–2911. Pistoni, J. and L. F. Toledo. 2010. Amphibian illegal trade in Brazil: what do we know? South American Journal of Herpetology 5: 51–56.Queensland Government. 2012. Prohibited pets. Electronic Database accessible at http://www.daff.qld.gov.au/4790_ 8263.htm. Queensland Government, Department of Agriculture, Fisheries and Forestry, Queensland, Australia. Captured on 20 August 2012.Quintela, F. M., D. Loebmann, and N. M. Gianuca. 2006. Répteis continentais do município de Rio Grande, Rio Grande do Sul, Brasil. Biociências 14: 180–188.Robert, J., L. Abramowitz, J. Gantress, and H. D. Morales. 2007.  Xenopus laevis: a possible vector of Ranavirus infection? Journal of Wildlife Diseases 43: 645–652.Schlaepfer, M. A., C. Hoover, and C. K. Dodd Jr. 2005. Challenges in evaluating the impact of the trade in amphibians and reptiles on wild populations. BioScience 55: 256–263.Schloegel, L. M., C. M. Ferreira, T. Y. James, M. Hipolito, J. E. Longcore, A. D. Hyatt, M. Yabsley, A. M. C. R. P. F. Martins, R. Mazzoni, A. J. Davies, and P. Daszak. 2010. The North American bullfrog as a reservoir for the spread of Batrachochytrium dendrobatidis in Brazil. Animal Conservation 13: 53–61.Silva, E. T., E. P. Reis, R. N. Feio, and O. P. R. Filho. 2009. Diet of the invasive frog Lithobates catesbeianus in Viçosa, Minas Gerais State, Brazil. South American Journal of Herpetology 4: 286–294.Wu, J. 2007. World without borders: wildlife trade on the Chinese-language Internet. TRAFFIC Bulletin  21: 75–84.Magalhães and São-Pedro

Illegal trade on non-native amphibians and reptiles in southeast Brazil: the status of e-commerce

Abstract

Similar works

Full text

Available Versions

Cadernos Espinosanos (E-Journal)

Directory of Open Access Journals